REVIEW article

Front. Pharmacol., 22 October 2024

Sec. Pharmacology of Anti-Cancer Drugs

Volume 15 - 2024 | https://doi.org/10.3389/fphar.2024.1483160

DNA damage caused by chemotherapy has duality, and traditional Chinese medicine may be a better choice to reduce its toxicity

  • 1. Institute of Interdisciplinary Integrative Medicine Research, Shanghai University of Traditional Chinese Medicine, Shanghai, China

  • 2. Department of Intensive Care Medicine, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, China

  • 3. Breast Surgery Department, Baoshan Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, China

  • 4. Shanghai Institute of Stem Cell Research and Clinical Translation, Dongfang Hospital Affiliated to Shanghai Tongji University, Shanghai, China

Abstract

Background:

DNA damage induced by chemotherapy has duality. It affects the efficacy of chemotherapy and constrains its application. An increasing number of studies have shown that traditional Chinese medicine (TCM) is highly effective in reducing side-effects induced by chemotherapy due to its natural, non-toxic and many sourced from food. Recent advancements have demonstrated survival rates are improved attributable to effective chemotherapy. DNA damage is the principal mechanism underlying chemotherapy. However, not all instances of DNA damage are beneficial. Chemotherapy induces DNA damage in normal cells, leading to side effects. It affects the efficacy of chemotherapy and constrains its application.

Objectives:

This review aims to summarize the dual nature of DNA damage induced by chemotherapy and explore how TCM can mitigate chemotherapy-induced side effects.

Results:

The review summarized the latest research progress in DNA damage caused by chemotherapy and the effect of alleviating side effects by TCM. It focused on advantages and disadvantages of chemotherapy, the mechanism of drugs and providing insights for rational and effective clinical treatment and serving as a basis for experiment. In this review, we described the mechanisms of DNA damage, associated chemotherapeutics, and their toxicity. Furthermore, we explored Chinese herb that can alleviate chemotherapy-induced side-effects.

Conclusion:

We highlight key mechanisms of DNA damage caused by chemotherapeutics and discuss specific TCM herbs that have shown potential in reducing these side effects. It can provide reference for clinical and basic research.

1 Introduction

Cancer is the second-leading global cause of death, with nearly one-sixth fatalities in 2020 caused by cancer (). In 2020, the most common cancer types included breast, lung, colon, rectal, and prostate cancers, while the primary contributors to cancer-related mortality encompassed lung, colon, rectal, liver, stomach, and breast cancers (; ). Furthermore, in low-income and lower-middle-income countries, about 30% of cancer cases are attributed to cancer-causing infections such as human papillomavirus and hepatitis (; ). Breast, cervical, lung, thyroid, and colorectal cancers are the most common types of cancer in women, while prostate, lung, colorectal, liver, and stomach cancers are the most frequent among men (; ).

While numerous cancer treatments are available, including radiotherapy, surgery, immunotherapy, endocrine therapy, and gene therapy. Chemotherapy remains the most prevalent treatment approach (). The term “chemotherapy” refers to the utilization of chemicals for disease treatment (). It involves the use of cytotoxic drugs to treat various types of cancer by hindering their replication, thereby impeding their growth and further dissemination. In the 1960s, surgery and radiation therapy predominated cancer treatment (). However, their curative rate after local treatment was only approximately 33% owing to micro-metastasis. Subsequently, a study combining drugs with surgery or radiation in the treatment of breast cancer demonstrated effective inhibition of tumor micro-metastasis, paving the way for adjuvant chemotherapy. Chemotherapy can serve as a curative, palliative, or adjuvant to improve the efficacy of other therapies, such as radiotherapy (). The synergy of chemotherapy, surgery and radiation maximizes the antitumor effect while minimizing toxicity toward normal tissues, making it an established clinical tool in the treatment of cancer (). There are many types of chemotherapy drugs, usually divided into several main categories, such as anthracycline antibiotics, antimetabolites, alkylating agents, and plant alkaloids ().

However, cancer patients receiving chemotherapy may experience a series of side effects. The most prevalent side effects are fatigue, nausea, vomiting (), mucositis, hair loss (), dry skin, rashes, intestinal alterations, decreased blood cell counts, and an increased risk of infections. Moreover, chemotherapeutic drugs also cause cardiac, pulmonary, hepatic, renal, and neuronal inflammation, as well as disruptions in the coagulation cascade (). This leads to a general decrease in the quality of survival of patients, which may necessitate treatment discontinuation due to intolerance. Hence, it is imperative to minimize the side effects associated with chemotherapy (). Chinese medicine has also played an indispensable role in cancer treatment (). For example, quercetin, the main component of Astragalus membranaceus, which interacted with PI3K to inhibit the phosphorylation of PI3K/AKT, inhibited DNA damage repair (DDR) and triggered mitotic catastrophe and apoptosis in non-small cell lung cancer (). There is already a large amount of clinical data proving that TCM enhances the efficacy of chemotherapy and reduces chemotherapy-induced side effects and complications in the whole cancer treatment process (). TCM not only serves as an adjuvant to chemotherapy, but also plays an adjuvant therapeutic role (), and provides useful information for the development of more effective anticancer drugs (). Nevertheless, chemotherapy-induced DNA damage responses have introduced numerous challenges, such as alterations in DNA damage repair capabilities, which is one of the important factors contributing to the emergence of chemotherapeutic resistance (). Chemotherapy causes DNA damage, and DDR is a very complex network. Chromatin regulation induced by the DNA damage response triggers the DNA repair process, or alters signaling pathways such as EGFR, PI3K/AKT, PTEN and mTOR, which enhanced resistance to chemotherapeutic agents (). DNA damage caused by chemotherapy can lead to effective cancer cell death, which is beneficial for treatment. However, the same mechanism can also damage normal cells, leading to side effects and reduced quality of life. This duality poses a challenge in optimizing chemotherapy efficacy while minimizing harm. In this review, we focus on chemotherapy-induced DNA damage responses. We briefly describe the benefits of chemotherapeutic agents that induce DNA damage, as well as the fact that it exhibits certain drawbacks in its use, such as chemotherapy resistance, normal tissue damage, and secondary tumors caused by genetic mutations, thus leading to strategies for reducing adverse effects using TCM ingredients, aiming to explore both the advantages and disadvantages it poses in the treatment of malignant tumors and identify novel treatment strategies for malignant tumors.

2 DNA damage repair pathways

Damage to one or multiple bases within cellular DNA can result from both internal and external mechanical or chemical factors, and these damages are primarily repaired through several DNA damage repair pathways, including base excision repair (BER), single strand break repair (SSBR), nucleotide excision repair (NER), mismatch repair (MMR), homologous recombination repair (HRR), non-homologous end joining (NHEJ), translesion synthesis (TLS), fanconi anemia (FA), and methylguanine methyltransferase (MGMT) () (Figure 1).

FIGURE 1

2.1 BER

BER is highly conserved that addresses oxidative damage resulting from respiration, natural hydrolysis, and alkylation reactions (). This pathway constitutes a coordinated and sequential process wherein single-strand breaks are generated as intermediates during the repair process. BER predominantly addresses non-bulky small nucleobase lesions, involving the excision and replacement of incorrect (e.g., uracil) or damaged bases (e.g., 3-methyladenine, 8-oxoG) arising from deamination, alkylation, or oxidation (; ).

2.2 NER

The function of NER is to remove distortions within the helix structure of DNA. NER can eliminate the widest range of structurally unrelated DNA lesions. NER exhibits two distinct mechanisms for detecting DNA damage, which may manifest through either global genome NER or transcription-coupled NER (). NER is characterized by endonuclease excision of nucleotides of the damaged site after specific recognition of the damaged site, followed by resynthesis of the correct new strand (; ).

2.3 MMR

The MMR system is responsible for the removal of base mismatches arising from spontaneous and induced base deamination, oxidation, methylation, and replication errors (). During MMR repair, base mismatches can arise during DNA replication. These DNA damages are recognized by MutSα or MutSβ. Subsequently, the MutLα complex interacts with MutS to excise the damaged DNA. The resulting gaps are then ligated through DNA polymerase δ and ligase (). However, the MMR status affects meiotic and mitotic recombination, DNA damage signaling, apoptosis, and cell-type-specific processes (). The loss of MMR leads to the emergence of a mutator phenotype, which predisposes individuals to a heightened risk of cancer ().

2.4 DNA double-strand break (DSB) repair

DSBs play crucial roles in suppressing genomic instability. However, when these repair mechanisms are activated, they can facilitate chromosome rearrangements that underlie various human diseases, ranging from developmental disorders to cancer (). In mammalian cells, two primary mechanisms for DSB repair predominate: homologous recombination and NHEJ ().

2.4.1 HRR

HRR is a relatively error-free repair pathway that primarily operates (). In this process, single-stranded DNA bound by Rad51 invades the sister chromatids to search for homologous sequences and accomplishes repair through sequence synthesis and exchange ().

2.4.2 NHEJ

NHEJ is an error-prone repair pathway that can occur throughout all cell cycle phases. The NHEJ repair process initiates with the recognition and binding of Ku70/Ku80 to damaged double-stranded DNA, followed by the subsequent recruitment of the catalytic subunit DNA-dependent protein kinase catalytic subunit (DNA-PKcs). Upon activation, DNA-PKcs mediates the repair of broken DNA through X-ray repair cross-complementing protein 4 (XRCC4) and DNA ligase IV ().

2.5 Others

DNA undergoes crosslinking due to environmental induction or exposure to chemotherapeutic agents, such as platinum-based chemotherapeutic agents. This disrupts the DNA replication fork process, which can be repaired through TLS (). The DNA interstrand and intrastrand crosslinks can be uncrosslinked through the FA repair pathway and subsequently repaired by the synergistic action of the TLS, NER, and HRR pathways (). The common base damage, 6-methylguanine, can be directly repaired via the MGMT pathway (). Various chemotherapeutic drugs induce diverse forms of DNA damage, activate distinct signaling pathways, and are repaired through different repair mechanisms ().

3 Types of DNA damage-inducing chemotherapeutic agents

3.1 DNA methylating and alkylating agents

DNA methylating and alkylating agents are traditional chemotherapeutic agents that induce DNA damage. They induce cancer cell death mainly through the BER, MMR or NER pathways. Alkylating agents, such as Apigenin and melphalan, contain alkylating groups capable of releasing electron-deficient carbon positive ions or reactive radicals in the body. These agents form covalently crosslinked alkylating groups on DNA, ultimately leading to the eradication of cancer cells (). Methylating drugs, such as procarbazine and Temozolomide, instigate methylation modifications on DNA bases, including N7- and N3-methyl guanine (N7MeG, N3MeG), N3-methyl adenine (N3MeA), and O6-methyl guanine (O6MeG) (). Although these modifications do not directly induce cytotoxicity, they provoke mismatches during DNA replication. These mismatches are recognized by the BER, MMR, or NER pathways and converted into DSBs. The accumulation of a substantial number of DSBs resulted in unrepaired cells and halted replication (), ultimately inducing cell death.

3.2 DNA replication inhibitors

Frequent DNA replication is a characteristic of tumor cells. Therefore, chemotherapeutic drugs for tumor therapy seek to regulate DNA replication in tumor cells by inhibiting DNA deconvolution and nucleotide synthesis that occur during DNA replication.

Topoisomerase inhibitors: Under normal conditions, DNA adopts a tightly intertwined double helix structure. During the S, G2, and M phases of the cell cycle, two types of topoisomerases, Topo I and Topo II act on single and double strands of DNA, respectively, to create a transient, readily dissociable complex intermediate (enzyme-DNA break complex) by non-covalently binding to the terminal DNA fragment after cleaving both single- and double-stranded DNA. Once the enzymatic processes are completed, these cleaved DNA segments are rejoined (). Topo I and Topo II inhibitors operate through similar mechanisms and they mainly cause apoptosis through SSB and DSB pathways. Some inhibitors directly target the enzymes, inhibiting their physiological activity, whereas most inhibitors can bind to DNA, forming a stable and rigid enzyme-DNA break complex that is covalently attached to the aforementioned enzyme-DNA break complex (). The resulting enzyme-drug-DNA triplet complex hinders the rejoining of single- and double-stranded DNA cuts mediated by Topo. This leads to the irreversible formation of permanent SSBs and DSBs in the complex fragments. Once these permanent breaks occur in genes, they become targets for gene recombination and repair processes, stimulating the exchange of sister chromosomes in the offspring and the insertion and deletion of large gene segments, eventually causing chromatin translocation and aberration, ultimately leading to apoptosis (). Camptothecin (CPT), an alkaloid derived from the dove tree, is the most widely utilized class of Topo I inhibitors (). Three CPT analogs have been commercially marketed: irinotecan (CPT-11), topotecan (TPT), and hydroxycamptothecin (HCPT). These analogs have found application in the treatment of colon, ovarian, and lung cancers (). Research has demonstrated that CPT analogs are not only effective for the treatment of colon and lung cancer but also for the treatment of other types of cancer. There are several antitumor drugs targeting Topo II, and many of them have been used in clinic settings, including etoposide (VP-16) and teniposide (VM-26) of the podophyllotoxin family (), as well as amrubicin, doxorubicin (DOX), and pirarubicin (THP) in the adriamycin family (). Among these, etoposide and doxorubicin are the most frequently used anticancer drugs in clinical practice, serving as the first choice of drugs for the management of malignant tumors such as small-cell lung cancer and lymphoma.

Nucleotide synthesis inhibitors: They inhibit DNA replication by reducing deoxyribonucleotide production and induce apoptosis mainly through the DSB pathway. Several chemotherapeutic drugs target pivotal enzymes involved in nucleotide synthesis during metabolism, thereby inhibiting nucleotide production and affecting DNA replication. 5-fluorouracil (5-FU) inhibits thymidylate synthase (). Gemcitabine targets ribonucleic acid reductase (). Methotrexate (MTX), inhibits dihydrofolate reductase (), which inhibits DNA replication by depleting deoxyribonucleotide production.

3.3 DNA crosslinking agents

DNA crosslinking agents are a class of compounds that can interact with two distinct sites in DNA, leading to the formation of various types of lesions (). There are three forms of DNA crosslinking: intrastrand DNA crosslinking, where covalent crosslinking occurs between two different sites on the same strand of DNA inter-strand crosslinking (ICL), where covalent crosslinking occurs between two strands of DNA. And inter-helix crosslinking, where covalent crosslinking occurs between two independent double strands of the DNA double helix (). Whereas DNA intrastrand cross-links are repaired by NER alone, ICL repair involves parts of NER, HR, and translesion synthesis. The cytotoxicity of DNA platinum-based chemotherapeutic agents arises from both intrastrand crosslinking and ICL. Platinum-based drugs, such as cisplatin and carboplatin, covalently crosslink DNA through platinum atoms, while cyclophosphamide generates DNA crosslinks through alkylated metabolites, thereby disrupting S-phase replication and inhibiting transcriptional activity, leading to DNA replication stress, cytotoxic effects, and eventual cell death (). Intrastrand crosslinking damage can be tolerated by some DNA polymerases, rendering it less toxic than inter-strand crosslinks during replication (). Although intrastrand DNA crosslinks represent approximately 95% of all DNA lesions, ICLs are more cytotoxic. ICLs simultaneously bind to both strands of the DNA double helix, inhibiting DNA replication and RNA transcription, and induce cell cycle arrest and regulatory death ().

3.4 Neoadjuvant chemotherapy: molecular targeted therapy

3.4.1 PARP inhibitors (PARPi)

PARPi exert their anticancer effects through the inhibition of BER, the accumulation of naturally occurring SSBs, resulting in conversion of these SSBs into DSBs at stalled replication forks during the S phase. They destabilize replication forks by entrapping DNA with PARP, ultimately inducing cell death through replication stress-induced mitotic catastrophe (). The PARP enzyme family comprises 17 members, among which PARP1, PARP2, and PAPR-5a/5b (tankyrases) are poly-ADP-ribosylated protein-modifying enzymes, while the remaining PARP proteins are mono-ADP-ribosylated protein-modifying enzymes (). PARP1 and PARP2 are key DNA damage repair enzymes that are activated upon recognizing damaged DNA fragments and serve as DNA damage sensors (). Due to a DNA repair defect, BRCA1/2-deficient tumor cells exhibit heightened sensitivity to PARPi, a phenomenon known as synthetic lethality (). Currently, there are four PARPi: olaparib, rucatinib, talazoparib, and niraparib. In 2014, the U.S. Food and Drug Administration (FDA) approved olaparib for treating advanced ovarian cancer in individuals with germline BRCA mutations (). More recently, niraparib demonstrated a significant extension of progression-free survival in patients with ovarian cancer, leading to FDA approval for the treatment of recurrent platinum-sensitive ovarian cancer ().

3.4.2 Ataxia-telangiectasia mutated (ATM) inhibitors and ataxia-telangiectasia and Rad3-related (ATR) inhibitors

The ATM and ATR genes are key genes associated with DNA DSB damage repair and can be recruited as DNA damage sensing sites, either by the MRN complex (MRE11/RAD50/NBS1 complex) or the 9-1-1 complex, respectively, to initiate the damage repair pathway. ATM and ATR are both members of the PI3K-like kinase (PIKK) protein family (). ATM inhibitors enhance the sensitivity of radiotherapy (), and the ATM inhibitors AZD0156 and AZD1390 have progressed to preclinical studies (). In contrast, ATR inhibitors are currently in the early stages of development. VX-970, an ATR inhibitor, has been investigated in combination with various chemotherapy regimens for advanced solid tumors (), and these inhibitors are now undergoing phase I clinical trials.

3.4.3 DNA-PKcs inhibitor

DNA-PKcs, an enzyme encoded by the DNA-activated protein kinase catalytic subunit peptide (PRKDC) gene, is a core protein kinase associated with the regulation of the NHEJ repair pathway (). It is a member of the PIKK protein family. Two DNA-PKcs are undergoing clinical trials: M3814, is primarily employed for the treatment of advanced solid tumors and leukemia in phase I clinical trials (; ). C-115 is a novel compound that can be used in synergy with radiation therapy and temozolomide chemotherapy to improve the prognosis of patients with malignancies () (Table 1).

TABLE 1

Chemotherapeutic drugsLesionMolecular targetRepresentative drugsRepair pathways
DNA methylating agents; DNA alkylating agentsN7MeG, N3MeG, O6MeG, Base Mismatch, DSBMGMT, PARP1, APE1, DNA-PK, ATM, CHK1Procarbazine, Temozolomide; Bendamustine, MelphalanMGMT, BER, MMR, NER, NHEJ, HR
DNA replication inhibitorDSB, SSBPARP1, APE1, DNA-PK, ATM, CHK1CPT-11, TPT, HCPT
VP-16, VM-26
Amrubicin, ADM, THP
5-FU, Gemcitabine Methotrexate
NHEJ, HR, BER
DNA cross-linking agentIntrastrand cross-link, ICLXPA, XPB, XPG, ATM, CHK1Cisplatin, CarboplatinNER, HR
PARP inhibitorN7MeG, N3MeG, SSBPARPOlaparib, Rucatinib, Talazoparib, NiraparibBER
ATM and ATR inhibitorsDSBATM, ATRAZD0156, AZD1390, VX-970HR
DNA-PKcs inhibitorDSBDNA-PKcsM3814, C-115NHEJ

Types of DNA damage-inducing chemotherapeutic agents.

4 Chemotherapy-induced DNA damage “evil” and the regulatory effect of natural products

The effects of chemotherapy drugs that induce DNA damage are not always beneficial. It exhibits certain disadvantages in use. DNA damage from chemotherapy can contribute to drug resistance in cancer cells (), cause collateral damage to healthy tissues (), and increase the risk of secondary malignancies due to mutagenic effects (). Chemotherapy induced tissue damage is one of its most serious side effects. We focus on describing the damage to different normal tissues and the strategies to reduce adverse reactions using TCM ingredients.

4.1 Kidney injury

Conventional chemotherapeutic drugs, primarily including alkylating agents, antimetabolites, and anticancer antibiotics, inflict harm on various components of the kidney, such as the tubulointerstitial region, renal vasculature, and glomeruli, which can lead to acute kidney injury (AKI) (). The most common etiology of AKI is acute tubulointerstitial injury. Platinum (carboplatin), as a representative drug, can induce AKI through direct toxicity to renal tubular epithelial cells, activation of apoptosis, oxidative stress, and mitochondrial damage (). Cisplatin is a classic chemotherapeutic drug, 90% of which is metabolized by the kidneys. This is especially evident with multiple high-dose and repeated short-term administrations (). It has been demonstrated that apurinic/apyrimidinic endonuclease 2 (APE2), a critical molecule, is upregulated in proximal tubule cells following cisplatin-induced nuclear DNA and mitochondrial DNA damage (). Antifolate-metabolizing drugs (MTX) have a propensity to crystallize within the renal tubules, leading to tubular obstruction and interstitial damage. MTX is primarily eliminated by the kidneys, and its blood levels exhibit a marked rise following AKI (). Moreover, there is an overlap between the pathways implicated in tumor growth inhibition and those associated with kidney function. This overlap may explain the propensity of such drugs to induce kidney injury. Antiangiogenic targeted agents, such as bevacizumab, sorafenib, and sunitinib, which therapeutically target vascular endothelial growth factor (), predispose individuals to renal thrombotic microangiopathy. Additionally, isolated cases have reported the development of focal segmental glomerulosclerosis and acute interstitial nephritis with severe hypertension () (Figure 2).

FIGURE 2

However, an increasing number of studies indicated that natural products can alleviate chemotherapy induced kidney injury (Table 2).

TABLE 2

Mitigation of injuryName of monomerDosagesMechanism of action
Kidney injuryCurcumin20 μMInfluenced the NF-κB signaling pathway and reduced the expression of IL-1β, IL-6, IL-8, and TNF-α
Panduratin A10 µMReduced cisplatin-induced mitochondria dysfunction, ROS generation, activation of ERK1/2, and cleaved-caspase 3 and 7
Asiatic acid50 mg/kgSuppressed the enhanced mRNA expression of proinflammatory cytokines IL-1β, TNF-α, MCP-1 and caspase-1, inhibited NF-κB activation and the inflammatory response, blood urea nitrogen, and histologic changes
Umbelliferone40 mg/kgAffected on the NRF2 signaling pathway
Quercetin50 mg/kgDownregulated Mincle2/Syk/NF-jB, reduced macrophage infiltration
Celastrol1 mg/kgInhibited NF-κB and improves mitochondrial function
Madecassoside50 mg/kg, 20 μMReduced the activation of the MAPK signaling pathway
Dendropanoxide5 μg/mLAffected AMPK/mTOR signaling pathway
Ginsenoside Rb310 mg/kg, 1 μmol/LRegulated AMPK-/mTOR-mediated autophagy and inhibited apoptosis
Ginsenoside Rg510 mg/kgIncreased expression of Bcl-2 and decreased expression of Bax
Liquiritigenin15 mg/kgImpacted on NRF2/SIRT3-mediated mitochondrial function
Apigenin100 μMInhibited ROS/ASK1-mediated activation of the MAPK signaling pathway
Kaempferol10 mg/kg, 100 μMInhibited ROS overproduction and activated the MAPK signaling pathway
α-Bisabolol25 mg/kgActivated NF-κB/MAPK signaling pathway and endogenous apoptosis pathway, inhibited oxidative stress and inflammatory response
Liver injuryApigenin3 mg/kgRestored antioxidant defences and reduced inflammation
Betulin8 mg/kgTargeted apoptosis and the Nek7-dependent NLRP3 inflammasome pathway
Genistein15–45 mg/kgModulated various signaling pathways
Methanolic15 mg/kgRestored biochemical and oxidative stress parameters, reduced DNA damage and IFN-γ levels
Naringin20 mg/kgActivated Bax and downregulated Bcl-2 protein expression
Paeonol100 mg/kgInhibited oxidative stress, inflammation, fibrosis and apoptosis pathways
Luteolin100 mg/kgReduced oxidative and inflammatory stress and inhibited apoptosis
Quercetin50 mg/kgRegulated the SIRT1 pathway and attenuatedNLRP3 inflammasome activation
Cardiac injuryHyperoside100 μM, 30 mg/kgInhibited ASK1/p38 signaling pathway and NOXs/ROS/NLRP3 inflammasome signaling pathway
Matrine200 mg/kgMaintained AMPKα/UCP2 pathway
Apocynum venetum L.70 μg/mLAffected the AKT/Bcl-2 signaling pathway
Glycyrrhetinic acid40 μM, 40 mg/kgActivated Nrf2/HO-1 signaling pathway
Amentoflavone20 µMInhibited STING/NLRP3 signaling pathway
Paeonol50 μmol/LActivated the PKCε-Stat3 pathway, promoted Mfn2-mediated mitochondrial fusion
Astragaloside IV40 mg/kgInhibited NOX2 and NOX4
Ginsenoside Rg215 mg/kgDownregulated the expression of pro-apoptotic proteins caspase-3, caspase-9 and BAX
Nerve injuryCurcumin1 mg/mLDid not inhibit p53 mRNA transcription and did not interfere with the therapeutic effect of cisplatin
Quercetin25 mg/kgInvolved oxidative stress pathways in the inhibition of chronic painful peripheral neuropathy
Cannabidiol2.5 mg/kgInhibited neuropathic pain via 5-HT1A receptors
Rutin30 mg/kg, 50 mg/kgAssociated with antioxidant and anti-apoptotic pathways
Ear injuryCurcumin0.5 μM, 200 mg/kgRegulated STAT3 and Nrf2
Paeoniflorin30 mg/kgAttenuated SGN damage through the PINK1/BAD pathway
Allicin18.2 mg/kgPrevented hearing loss through the mitochondrial apoptosis pathway
Ginkgo100 mg/kgProtected the inner ear from cisplatin-induced ototoxicity
Hesperetin20 mg/kgPrevented ototoxicity by increasing antioxidant enzymes and decreased oxidative parameters

Effect of natural products on chemotherapy-induced DNA damage.

Curcumin, a flavonoid obtained from ginger family, prevented renal inflammatory injury by influencing the nuclear factor-κB (NF-κB) signaling pathway and reducing the expression of interleukin-1β (IL-1β), IL-6, IL-8, and tumor necrosis factor (TNF-α) (). Panduratin A is a bioactive compound derived from Boehmeria nilotica that exerts a protective effect against nephrotoxicity by reducing cisplatin-induced mitochondria dysfunction, intracellular reactive oxygen species (ROS) generation, activation of ERK1/2, and cleaved-caspase 3 and 7 (). Asiatic acid (AA) has been reported to possess anti-inflammatory and anti-apoptotic effects. AA suppressed the enhanced mRNA expression of proinflammatory cytokines IL-1β, TNF-α, MCP-1 and caspase-1 in kidneys. AA pretreatment inhibited NF-κB activation and the inflammatory response, blood urea nitrogen, and histologic changes, and protected against cisplatin-induced AKI (). Umbelliferone (UMB), a benzopyrone belonging to the coumarin family, is the main active ingredient of the Chinese herb Cortex Fraxini. UMB protected against cisplatin-induced nephrotoxicity by the NRF2 signaling pathway (). Quercetin prevented the nephrotoxic effects of cisplatin by down-regulating Mincle2/Syk/NF-jB and reducing macrophage infiltration without affecting its anti-tumour activity (; ). Celastrol is an active ingredient of Chinese medicine Tripterygium wilfordii. It protected against cisplatin-induced AKI possibly through suppressing NF-κB and improving mitochondrial function (). Madecassoside (MA), an active constituent of Centella asiatica, had antioxidant and anti-inflammatory effects and ameliorated cisplatin-induced renal tubular damage possibly by decreasing activation of the MAPK signaling pathway (). Dendropanoxide (DPx), a triterpenoid isolated from Dendropanax morbifera. DPx resisted cisplatin-induced acute kidney injury via the AMPK/mTOR signaling pathway (). Ginsenoside Rb3 (G-Rb3) provided protective effects against cisplatin-induced nephrotoxicity via regulation of AMPK-/mTOR-mediated autophagy and inhibition of apoptosis. Ginsenoside Rg5 (G-Rb5) inhibited the activation of apoptotic pathway by increasing the expression of Bcl-2 and decreasing the level of Bax, and significantly reduced cisplatin-induced nephrotoxicity, oxidative stress and inflammation (; ). Liquiritigenin (4′,7-dihydroxyflavone) is a major bioactive ingredient extracted from the root of licorice (Glycyrrhiza uralensis), could be used as a potential nephroprotective agent to protect against cisplatin-Induced nephrotoxicity via NRF2/SIRT3-mediated improvement of mitochondrial function (). Apigenin (APG), a naturally occurring flavonoid found in various plants, and Kaempferol, a naturally occurring flavonoid, ameliorated DOX-induced kidney injury by inhibiting ROS/ASK1-mediated activation of the MAPK signaling pathway (). Kaempferol, can protect against DOX-induced nephrotoxicity by inhibiting ROS overproduction and activating the MAPK signalling pathway, as well as maintaining DOX cytotoxicity in breast cancer cells (). α-Bisabolol is a naturally occurring monocyclic sesquiterpene alcohol, was found in the essential oils of various aromatic plants. It also has the potential to attenuate DOX-induced nephrotoxicity by inhibiting oxidative stress and inflammation through the activation of the NF-κB/MAPK signaling pathway as well as the intrinsic apoptosis pathway ().

4.2 Liver injury

Liver is the primary site of drug metabolism and a prominent organ susceptible to chemotherapy-induced injury, which can develop into acute liver failure. Chemotherapy can induce hepatotoxicity directly or aggravate pre-existing liver diseases, leading to deterioration of liver function and alterations in hepatic drug metabolism (). Among platinum-based drugs, cisplatin induced hepatotoxicity characterized by elevating aminotransferases, steatosis, and cholestasis (), whereas oxaliplatin induced vascular alterations and sinusoidal tubular occlusion or dilatation (). Gefitinib induced hepatotoxicity, with only slight increase in transaminase levels. In contrast, imatinib, another tyrosine kinase inhibitor, induced more severe hepatotoxicity, including hepatic failure and hepatic necrosis () (Figure 3).

FIGURE 3

The individual components of natural products in TCM can be categorized into four distinct groups for the treatment of liver injury: phenols, flavonoids, terpenoids, and glycosides () (Table 2).

APG is a potent flavonoid with antioxidant and anti-inflammatory properties. APG reduced malondialdehyde expression while enhancing the expression of superoxide dismutase1, catalase, and glutathione, thereby downregulating the expression of Caspase-3, C-reactive protein, and inducible nitric oxide synthase. These actions restored the antioxidant defense system and significantly attenuated MTX-induced hepatotoxicity (). Furthermore, when combined with MTX, APG lowers the expression levels of TNF-α and IL-1β, signifying its potential to ameliorate MTX-induced hepatotoxicity by reducing inflammation (). Betulin, a lupane pentacyclic triterpene composed of six isoprene units, is widely found in plants such as jujube, pomegranate bark, and birch bark. It has been shown that serum levels of albumin were significantly reduced and aspartate aminotransferase (AST), alanine aminotransferase (ALT), and total bilirubin levels were significantly increased in cisplatin-treated individuals. Betulin effectively reversed cisplatin-induced liver injuries by targeting apoptosis and Nek7-independent NLRP3 inflammasome pathways (). Genistein is a sedative, hypnotic, and anticonvulsant drug derived from asparagus that protected liver function by modulating various signaling pathways (). Methanolic extract (ME) and ephedrine (EP), major compound of Ephedra alata, could attenuate cisplatin-induced hepatotoxicity by restoring biochemical and oxidative stress parameters, reducing DNA damage and IFN-γ levels (). Naringin (Nar) is a flavonoid derived from Citrus paradise. Nar decreased MTX-induced functional and ultrastructural liver damage. Nar as promising antiproliferative agents, induced apoptosis in cancer cells through activation of Bax and downregulation of Bcl-2 (). Paeonol, a nature active compound derived from the root bark of the medicinal plant Paeonia suffruticosa, offered a potent protective effect against MTX-induced hepatotoxicity through suppressing oxidative stress, inflammation, fibrosis, and apoptosis pathways (). Luteolin is a polyphenolic phytochemical with a variety of anticancer activities () that attenuated doxorubicin-induced derangements of liver and kidney by reducing oxidative and inflammatory stress to suppress apoptosis. Luteolin reduced lipid peroxidation, caspases-3 and -9 activities (). Quercetin attenuated NLRP3 inflammasome activation and apoptosis to protect isoniazid (INH)-induced liver injury via regulating SIRT1 pathway ().

4.3 Cardiac injury

Cardiotoxicity is the most significant adverse effect associated with chemotherapeutic drugs and contributes to heightened mortality. This directly impacts the efficacy of chemotherapeutic drugs. Chemotherapeutic agents are known to induce cardiotoxicity including anthracyclines and fluorouracil. In addition, some targeted agents, such as human epidermal growth factor 2 inhibitors and vascular growth inhibitors also present a relative cardiotoxicity (). The most prevalent manifestations of cardiotoxicity are left ventricular dysfunction and heart failure (). The precise mechanism underlying the cardiotoxicity remains elusive, potentially involving oxidative stress, apoptosis, aberrant expression of related genes, calcium overload, and the production of toxic metabolites (). Fluorouracil fluoride, a pyrimidine antimetabolite widely employed in the chemotherapy of epithelial-origin malignant tumors, ranks as the second killer of cardiotoxicity, following anthracyclines. Its molecular mechanisms encompass vasoconstriction, hypercoagulability attributable to endothelial damage, and direct myocardial toxicity (). Subsequent mechanisms involve endothelial dysfunction, thrombosis, and oxidative stress in cardiomyocytes, all ascribed to 5-FU. 5-FU can directly induce endothelial damage, subsequently leading to platelet and fibrin accumulation and thrombosis. 5-FU induced a significant production of mitochondrial ROS in H9C2 cells, concomitant with elevated ROS levels in cardiomyocytes, a decrease in the antioxidant dismutase and glutathione levels in cardiomyocytes, and an increase in the levels of malondialdehyde, a marker of mitochondrial membrane damage. With prolonged drug exposure, these processes ultimately led to cell apoptosis (). The cardiotoxicity associated with alkylating agents (cyclophosphamide, isocyclophosphamide, and platinum) often manifests as asymptomatic pericardial effusion, myocarditis, cardiac insufficiency, and cardiac arrhythmias. The potential mechanism of myocardial toxicity induced by alkylating agents mainly involved the damage of toxic metabolites and DNA base alkylation to endothelial cells. It can disrupt the replication and transcription of DNA (; ) (Figure 4).

FIGURE 4

Some natural products have a protective role against chemotherapy induced cardiac dysfunction. Hyperoside, a flavonoid glycoside extracted from various herbs, exhibited anti-apoptotic and anticancer properties. It protected HL-1 cells from DOX-induced cardiotoxicity by suppressing the ASK1/p38 signaling pathway (). It could also bind to both nicotinamide adenine dinucleotide phosphate (NADPH) oxidases (NOXs, the main source of ROS in cardiomyocytes) and cyclooxygenases to prevent DOX-induced cardiotoxicity by inhibiting the NOXs/ROS/NLRP3 inflammasome signaling pathway (). Matrine ameliorated DOX-induced uncoupling protein 2 (UCP2) downregulation and inhibition in DOX-induced cardiotoxicity via maintaining the AMPKα/UCP2 pathway (). Apocynum venetum L. (AVLE) is a member of the Apocynaceae family. AVLE alleviated DOX-induced cardiotoxicity through the AKT/Bcl-2 signaling pathway. In addition, the administration of AKT inhibitors counteracted the inhibitory effects of AVLE on DOX-induced apoptosis (). Glycyrrhetinic acid (GA), the major biologically active compound of licorice, protected against DOX-induced cardiotoxicity by activating the Nrf2/HO-1 signaling pathway (). Amentoflavone (AMF), a naturally occurring biflavone, mitigated DOX-induced cardiotoxicity by suppressing cardiomyocyte pyroptosis and inflammation through inhibition of the STING/NLRP3 signaling pathway (). Paeonol (Pae) is the main component isolated from the root bark of Paeonia suffruticosa (). Proanthocyanidins were found in seeds, nuts, fruits and vegetables. Both of them combined with Dox protected against DOX-induced cardiotoxicity, with Pae promoting Mfn2-mediated mitochondrial fusion through activating the PKCε-Stat3 pathway (). Ginsenoside Rg2 and Astragaloside IV (AS-IV) attenuated DOX-induced cardiomyopathy through the suppression of NOX2 and NOX4 (). They have a potential to be applied in patients with breast cancer () (Table 2).

4.4 Nerve injury

Chemotherapy drugs can induce a spectrum of neurological dysfunctions in peripheral or autonomic nerves, referred to as chemotherapy-induced peripheral neurotoxicity (CIPN). Common chemotherapeutic agents responsible for CIPN include microtubule inhibitors, platinum, thalidomide and bortezomib (). Paclitaxel alters microtubule dynamics, prompting mitochondrial dysfunction and inducing oxidative stress in peripheral nerves. Collectively, these effects triggered peripheral and central inflammation while also causing modifications in ion channel activity (). Among the platinum, oxaliplatin ranks highest in terms of neurotoxicity incidence. The prevailing consensus now attributes the mechanism of acute neurotoxicity to the impact of platinum on ion channel opening, resulting in substantial internal loss of calcium ions () (Figure 5).

FIGURE 5

Chemotherapeutic agents accumulated in the dorsal root ganglion (DRG) and ultimately led to DRG apoptosis by affecting DNA. However, Curcumin has protective effects against cisplatin-induced neurotoxicity that did not suppress transcription of p53 mRNA and disturb cisplatin’s therapeutic effect (; ). Quercetin inhibited oxaliplatin-induced chronic painful peripheral neuropathy by involving oxidative stress pathways (). Cannabidiol (a phytocannabinoid isolated from Cannabis sativa) inhibited paclitaxel-induced neuropathic pain through 5-HT1A receptors without diminishing chemotherapy efficacy (). Rutin (a natural flavonoid compound) (; ) exhibited potential neuroprotective effects against cisplatin or paclitaxel-induced neurotoxicity (Table 2).

4.5 Ear injury

The mechanism of cisplatin-induced ear injury remains incompletely understood. It comprises three primary molecular mechanisms: DNA damage, oxidative stress, and an inflammatory response. Cisplatin () induced the formation of DNA crosslinking which inhibited DNA replication and transcription, leading to cell cycle arrest and apoptosis (). Cisplatin predominantly activated the cochlear-specific NADPH oxidase NOX-3, leading to elevated levels of ROS in the cochlea. This surge in ROS depleted the endogenous antioxidant system, disrupted cytoplasmic organelle function, and ultimately led to apoptosis (). Furthermore, ROS activated apoptosis associated signaling molecules, such as caspases and JNK (). The toxic effects of cisplatin also included triggering an inflammatory response in the cochlea and increased the production of pro-inflammatory cytokines TNF-α, IL-1β, IL-6, and NF-κB (). This inflammation within the cochlea contributed to the damage and death of auditory neurons (). Additionally, cisplatin induced the expression of STAT1 in the cochlea while concurrently downregulating the expression of STAT3. STAT1 is pro-inflammatory in nature, ultimately leading to apoptosis of cochlear cells () (Figure 6).

FIGURE 6

Curcumin has been employed as a remedy for mitigating ototoxicity caused by cisplatin (). It functions effectively as an adjuvant to cisplatin. In the treatment of head and neck cancer, curcumin diminished cisplatin-related ototoxic effects modulating STAT3 and Nrf2 (; ). Paeoniflorin pre-treatment obviously mitigated cisplatin-induced spiral ganglion neuron (SGN) damage via the PINK1/BAD pathway (). Allicin, the main biologically active compound derived from garlic, prevented hearing loss induced by cisplatin effectively through the mitochondrial apoptosis pathway (). Ginkgo biloba extract protected the inner ear against cisplatin-induced ototoxicity (). Hesperetin, a flavonoid from citrus fruits, prevented ototoxicity by increasing antioxidant enzymes and decreasing oxidative parameters () (Table 2).

5 TCM interventions and conventional treatments

5.1 Available clinical studies

TCM has been used to treat cancer patients. There have been a large number of studies showing that TCM has been used clinically, but these studies have mainly focused on, relieving symptoms (e.g., fatigue, chronic pain, and insomnia) in cancer patients, and reducing the adverse effects and complications caused by chemotherapy. Ginsenosides derived from American ginseng (Xi-Yang-Shen in Chinese) purported actions against aging, cancer, stress, fatigue, and anxiety (). American ginseng demonstrated benefits in alleviating cancer-related fatigue (CRF) in a multi-site, double-blind, randomised trial with no significant toxic effects during treatment (). A pilot, randomized, double-blind, placebo controlled trial found that Shiquan-da-bu-tang had a potential benefit in terms of anorexia management for patients with cancer (). Liu-jun-zi-tang has also been shown in a randomised controlled trial to alleviate cancer-related anorexia nervosa and has been shown to be both efficacious and safe (). Zhi-gan-cao-tang is reported to be the Chinese herbal formula most frequently prescribed by TCM practitioners to treat heart failure. In the case of an 18-year-old adolescent male with refractory acute lymphoblastic leukemia (ALL), anthracycline-induced cardiotoxicity gradually resolved after administration of a modified Zhigengtang ().

5.2 Shortcomings of TCM in clinical studies

Although TCM is currently receiving increasing attention worldwide as an alternative and complementary therapy for cancer treatment, there are some limitations in the published studies, such as the lack of scientific validity of the studies with large samples, multi-centre participation, randomised control and efficacy comparisons. Most of the current studies focus on the efficacy rather than the systemic and in-depth pharmacological effects of the drugs, which is also related to the complexity of TCM theories and prescriptions. This is a gap between TCM and traditional antitumour drug research, and more mechanistic studies or long-term safety data are needed in the future.

Therefore, the study of TCM theory and prescription should be taken seriously. Full and complete discovery of TCM should be conducted. Experiments with high level of reproducibility and clear results should be carried out. In conclusion, more mechanistic studies and long-term safety data are needed, and more rigorous cancer treatment trials must be designed, including comprehensive quality control and standardised models at the cellular, organismal, animal and clinical levels, in order to study the multiple forms and levels of TCM to mitigate the damage to normal tissues caused by chemotherapy.

6 Discussion

With the application and development of chemotherapy, the emergence of tumors chemoresistance and side-effects poses a significant challenge in the treatment of malignant tumors. This review described the advantages and disadvantages of chemotherapy-induced DNA damage responses in the context of malignant tumors. It also provided an overview of several major DNA damage repair pathways, elucidated the mechanisms through which different chemotherapeutic agents inflict damage on malignant tumors by inducing DNA damage, and discussed strategies aimed at minimizing acute or long-term toxicities in different organs in the human body associated with chemotherapeutic agents-induced DNA damage. It also focuses on the damage to different normal tissues caused by chemotherapeutic drugs and strategies to reduce adverse reactions using TCM ingredients. Genomic instability constitutes a pivotal feature of tumors, and tumorigenesis is closely associated with defective cellular DNA damage repair, the accumulation of mutations, and an abnormal proto-oncogene or oncogene cascade response in proliferating tissues. Genomic instability and mutability facilitate the acquisition of genetic alterations in cancer cells, which propel tumor progression (). Efforts have been invested in seeking innovative breakthroughs for chemotherapy with increased efficacy and reduced side-effects. Therefore, in-depth research on signaling pathways and mechanisms associated with DNA damage repair is of profound significance for identifying potential targets and chemotherapeutics. This review aims to reveal the advantages and disadvantages of chemotherapy drugs, providing a basis for improving the efficacy of tumor treatment.

The chemotherapeutic drugs commonly employed in clinical practice nowadays possess the ability to not only inhibit or kill cancer cells but also induce a certain level of toxicity and side effects on normal bodily tissues, especially in terms of impeding normal cell proliferation. This phenomenon constitutes a significant impediment to the enhancement of the therapeutic efficacy of chemotherapeutic drugs. Chemotherapy remains essential, but it cannot ignore its side effects as DNA damaged. Therefore, it is particularly necessary to find methods that can improve the efficacy of chemotherapy while reducing its side effects. Furthermore, the development of alternative drugs within the same treatment category, characterized by reducing side effects, can harness the vast resources of TCM. This approach can utilize synergistic effects and reduce overall toxicity. TCM effectively inhibits the occurrence of tumors by regulating precancerous lesions. The efficacy enhancement and detoxification treatment of TCM further hinder the development of malignant tumor. Combining TCM with modern medical approaches such as surgery, radiotherapy, and chemotherapy can reduce the toxicity and side-effects of radiotherapy and chemotherapy, improve the body’s sensitivity to the drugs, and prevent or attenuate the recurrence of tumors or metastases after surgery. The utilization of TCM in tumor treatment can evidently prolong the survival period of cancer patients and significantly improve their quality of life. A large number of studies have demonstrated that TCM compounds can be used in anti-tumor therapy by regulating DNA damage repair pathways, activating signaling pathways, reducing oxidative stress or enhancing immune responses.

The summary of natural medicines in this review which mitigate the toxicity of chemotherapy helps researchers gain a quick understanding of the field. However, TCM faces significant challenges in clinical research, such as issues of standardization of TCM products, quality control and the need for careful monitoring of herb interactions. There is also a lack of a unified standard for clinical research, such as guidelines, recommended dosages or formulations, and efficacy monitoring criteria for the combination of TCM with conventional cancer treatments. Therefore, future development of TCM requires the identification of biomarkers to explore synergistic effects between herbs and specific chemotherapeutic agents, prediction of patient response to TCM, and large-scale clinical trials to validate the efficacy of herbs. There exists a need for the above recommendations to be validated through additional preclinical and clinical trials. These efforts are key areas of focus for researchers studying the efficacy of TCM in malignant tumors.

Statements

Author contributions

BB: Methodology, Writing–original draft. YM: Supervision, Writing–original draft. DL: Conceptualization, Investigation, Writing–review and editing. YZ: Conceptualization, Writing–review and editing. WZ: Investigation, Writing–review and editing. RS: Project administration, Resources, Writing–review and editing. QZ: Project administration, Writing–review and editing.

Funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Research Projects of Shanghai Municipal Commission of Science and Technology (21Y11920600), National Natural Science Foundation of China (82174121), Peak Disciplines (Type IV) of Institutions of Higher Learning in Shanghai, Science and Technology Development Project of Shanghai University of Traditional Chinese Medicine (23KFL020) and the Shanghai Municipal Key Clinical Specialty (shslczdzk04402).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Glossary

  • TCM

    traditional Chinese medicine

  • DDR

    DNA damage repair

  • BER

    base excision repair

  • SSBR

    single strand break repair

  • NER

    nucleotide excision repair

  • MMR

    mismatch repair

  • HRR

    homologous recombination repair

  • NHEJ

    non-homologous end joining

  • TLS

    translesion synthesis

  • FA

    fanconi anemia

  • MGMT

    methylguanine methyltransferase

  • DSB

    DNA double-strand break

  • DNA-PKcs

    DNA-dependent protein kinase catalytic subunit

  • XRCC4

    X-ray repair cross-complementing protein 4

  • N7MeG, N3MeG

    N7- and N3-methyl guanine

  • N3MeA

    N3-methyl adenine

  • O6MeG

    O6-methyl guanine

  • CPT

    camptothecin

  • CPT-11

    irinotecan

  • TPT

    topotecan

  • HCPT

    hydroxycamptothecin

  • VP-16

    etoposide

  • VM-26

    teniposide

  • DOX

    doxorubicin

  • THP

    pirarubicin

  • 5-FU

    5-fluorouracil

  • MTX

    methotrexate

  • ICL

    inter-strand crosslinking

  • PARPi

    PARP inhibitors

  • FDA

    Food and Drug Administration

  • ATM

    ataxia-telangiectasia mutated

  • ATR

    ataxia-telangiectasia and Rad3-related

  • MRN

    complex MRE11/RAD50/NBS1 complex

  • PIKK

    PI3K-like kinase

  • PRKDC

    DNA-activated protein kinase catalytic subunit peptide

  • AKI

    acute kidney injury

  • APE2

    apurinic/apyrimidinic endonuclease 2

  • MTX

    antifolate-metabolizing drugs

  • NF-κB

    nuclear factor-κB

  • IL-1β

    interleukin-1β

  • IL-6

    interleukin-6

  • IL-8

    interleukin-8

  • TNF-α

    tumor necrosis factor

  • ROS

    reactive oxygen species

  • AA

    Asiatic acid

  • UMB

    Umbelliferone

  • MA

    Madecassoside

  • DPx

    Dendropanoxide

  • G-Rb3

    Ginsenoside Rb3

  • G-Rb5

    Ginsenoside Rg5

  • APG

    Apigenin

  • AST

    aspartate aminotransferase

  • ALT

    alanine aminotransferase

  • ME

    methanolic extract

  • EP

    ephedrine

  • Nar

    Naringin

  • INH

    isoniazid

  • NADPH

    nicotinamide adenine dinucleotide phosphate

  • NOXs

    NADPH oxidases

  • UCP2

    uncoupling protein 2

  • AVLE

    Apocynum venetum L.

  • GA

    Glycyrrhetinic acid

  • AMF

    Amentoflavone

  • Pae

    Paeonol

  • AS-IV

    Astragaloside IV

  • CIPN

    chemotherapy-induced peripheral neurotoxicity

  • DRG

    dorsal root ganglion

  • SGN

    spiral ganglion neuron

  • CRF

    cancer-related fatigue

  • ALL

    acute lymphoblastic leukemia

References

  • 1

    AlmutairiM. M.AlanaziW. A.AlshammariM. A.AlotaibiM. R.AlhoshaniA. R.Al-RejaieS. S.et al (2017). Neuro-protective effect of rutin against Cisplatin-induced neurotoxic rat model. Bmc Complementary Altern. Med.17, 472. 10.1186/s12906-017-1976-9

  • 2

    AmarilloD.De BoniD.CuelloM. (2022). Translated article chemotherapy, alopecia, and scalp cooling systems. Actas Sifiliogr.113, T278T283. 10.1016/j.ad.2022.02.014

  • 3

    ArunachalamS.MeeranM. F. N.AzimullahS.JhaN. K.SaraswathiammaD.SubramanyaS.et al (2022). α-Bisabolol attenuates doxorubicin induced renal toxicity by modulating NF-κB/MAPK signaling and caspase-dependent apoptosis in rats. Int. J. Mol. Sci.23, 10528. 10.3390/ijms231810528

  • 4

    AzevedoM. I.PereiraA. F.NogueiraR. B.RolimF. E.BritoG. A. C.WongD. V. T.et al (2013). The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatin-induced chronic painful peripheral neuropathy. Mol. Pain9, 53. 10.1186/1744-8069-9-53

  • 5

    BahirwaniR.ReddyK. R. (2014). Drug-induced liver injury due to cancer chemotherapeutic agents. Seminars Liver Dis.34, 162171. 10.1055/s-0034-1375957

  • 6

    BahramiH.TafrihiM. (2023). Global trends of cancer: the role of diet, lifestyle, and environmental factors. Cancer innov.2, 290301. 10.1002/cai2.76

  • 7

    BarettiM.LeD. T. (2018). DNA mismatch repair in cancer. Pharmacol. and Ther.189, 4562. 10.1016/j.pharmthera.2018.04.004

  • 8

    BartonD. L.LiuH.DakhilS. R.LinquistB.SloanJ. A.NicholsC. R.et al (2013). Wisconsin ginseng (Panax quinquefolius) to improve cancer-related fatigue: a randomized, double-blind trial, N07C2. Jnci-Journal Natl. Cancer Inst.105, 12301238. 10.1093/jnci/djt181

  • 9

    BaskarR.LeeK. A.YeoR.YeohK.-W. (2012). Cancer and radiation therapy: current advances and future directions. Int. J. Med. Sci.9, 193199. 10.7150/ijms.3635

  • 10

    BiauJ.ChautardE.VerrelleP.DutreixM. (2019). Altering DNA repair to improve radiation therapy: specific and multiple pathway targeting. Front. Oncol.9, 1009. 10.3389/fonc.2019.01009

  • 11

    BrulikovaL.HlavacJ.HradilP. (2012). DNA interstrand cross-linking agents and their chemotherapeutic potential. Curr. Med. Chem.19, 364385. 10.2174/092986712803414295

  • 12

    BukowskiK.KciukM.KontekR. (2020). Mechanisms of multidrug resistance in cancer chemotherapy. Int. J. Mol. Sci.21, 3233. 10.3390/ijms21093233

  • 13

    CaiY.HuangC.ZhouM.XuS.XieY.GaoS.et al (2022). Role of curcumin in the treatment of acute kidney injury: research challenges and opportunities. Phytomedicine104, 154306. 10.1016/j.phymed.2022.154306

  • 14

    CakilB.BasarF. S.AtmacaS.CengelS. K.TekatA.TanyeriY. (2012). The protective effect of Ginkgo biloba extract against experimental cisplatin ototoxicity: animal research using distortion product otoacoustic emissions. J. Laryngology Otology126, 10971101. 10.1017/s0022215112002046

  • 15

    CarneiroB. A.El-DeiryW. S. (2020). Targeting apoptosis in cancer therapy. Nat. Rev. Clin. Oncol.17, 395417. 10.1038/s41571-020-0341-y

  • 16

    CeccaldiR.RondinelliB.D’AndreaA. D. (2016). Repair pathway choices and consequences at the double-strand break. Trends Cell Biol.26, 5264. 10.1016/j.tcb.2015.07.009

  • 17

    ChatterjeeN.WalkerG. C. (2017). Mechanisms of DNA damage, repair, and mutagenesis. Environ. Mol. Mutagen.58, 235263. 10.1002/em.22087

  • 18

    ChenL.QinZ.RuanZ. (2023). Hyperoside alleviates doxorubicin-induced myocardial cells apoptosis by inhibiting the apoptosis signal-regulating kinase 1/p38 pathway. Peerj11, e15315. 10.7717/peerj.15315

  • 19

    ChengY.WuX.NieX.WuY.ZhangC.LeeS. M.-Y.et al (2022). Natural compound glycyrrhetinic acid protects against doxorubicin-induced cardiotoxicity by activating the Nrf2/HO-1 signaling pathway. Phytomedicine106, 154407. 10.1016/j.phymed.2022.154407

  • 20

    CheonC.YooJ.-E.YooH.-S.ChoC.-K.KangS.KimM.et al (2017). Efficacy and safety of sipjeondaebo-tang for anorexia in patients with cancer: a pilot, randomized, double-blind, placebo-controlled trial. Evidence-Based Complementary Altern. Med.2017, 8780325. 10.1155/2017/8780325

  • 21

    ChongJ. H.GhoshA. K. (2019). Coronary artery vasospasm induced by 5-fluorouracil: proposed mechanisms, existing management options and future directions. Interv. Cardiol. Lond. Engl.14, 8994. 10.15420/icr.2019.12

  • 22

    CuriglianoG.CardinaleD.DentS.CriscitielloC.AseyevO.LenihanD.et al (2016). Cardiotoxicity of anticancer treatments: epidemiology, detection, and management. Ca-a Cancer J. Clin.66, 309325. 10.3322/caac.21341

  • 23

    da CostaR.PassosG. F.QuintaoN. L. M.FernandesE. S.MaiaJ. R. L. C. B.CamposM. M.et al (2020). Taxane-induced neurotoxicity: pathophysiology and therapeutic perspectives. Br. J. Pharmacol.177, 31273146. 10.1111/bph.15086

  • 24

    DeansA. J.WestS. C. (2011). DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer11, 467480. 10.1038/nrc3088

  • 25

    DeoS. V. S.SharmaJ.KumarS. (2022). GLOBOCAN 2020 report on global cancer burden: challenges and opportunities for surgical oncologists. Ann. Surg. Oncol.29, 64976500. 10.1245/s10434-022-12151-6

  • 26

    DingM.ShiR.FuF.LiM.DeD.DuY.et al (2023). Paeonol protects against doxorubicin-induced cardiotoxicity by promoting Mfn2-mediated mitochondrial fusion through activating the PKCε-Stat3 pathway. J. Adv. Res.47, 151162. 10.1016/j.jare.2022.07.002

  • 27

    DongC.WangY.TuZ.YanJ.JiangY.LuT.et al (2022). Recent advances in ATM inhibitors as potential therapeutic agents. Future Med. Chem.14, 18111830. 10.4155/fmc-2022-0252

  • 28

    DylgjeriE.KnudsenK. E. (2022). DNA-PKcs: a targetable protumorigenic protein kinase. Cancer Res.82, 523533. 10.1158/0008-5472.Can-21-1756

  • 29

    EisaN. H.El-SherbinyM.El-MagdN. F. A. (2021). Betulin alleviates cisplatin-induced hepatic injury in rats: targeting apoptosis and Nek7-independent NLRP3 inflammasome pathways. Int. Immunopharmacol.99, 107925. 10.1016/j.intimp.2021.107925

  • 30

    ElsawyH.AlgefareA. I.AlfwuairesM.KhalilM.ElmenshawyO. M.SedkyA.et al (2020). Naringin alleviates methotrexate-induced liver injury in male albino rats and enhances its antitumor efficacy in HepG2 cells. Biosci. Rep.40. 10.1042/bsr20193686

  • 31

    EpiskopouH.KyrtopoulosS. A.SfikakisP. P.FousteriM.DimopoulosM. A.MullendersL. H. F.et al (2009). Association between transcriptional activity, local chromatin structure, and the efficiencies of both subpathways of nucleotide excision repair of melphalan adducts. Cancer Res.69, 44244433. 10.1158/0008-5472.Can-08-3489

  • 32

    EskandariM. R.MoghaddamF.ShahrakiJ.PourahmadJ. (2015). A comparison of cardiomyocyte cytotoxic mechanisms for 5-fluorouracil and its pro-drug capecitabine. Xenobiotica45, 7987. 10.3109/00498254.2014.942809

  • 33

    EstradaC. C.MaldonadoA.MallipattuS. K. (2019). Therapeutic inhibition of VEGF signaling and associated nephrotoxicities. J. Am. Soc. Nephrol.30, 187200. 10.1681/asn.2018080853

  • 34

    FangG.LiX.YangF.HuangT.QiuC.PengK.et al (2023). Amentoflavone mitigates doxorubicin-induced cardiotoxicity by suppressing cardiomyocyte pyroptosis and inflammation through inhibition of the STING/NLRP3 signalling pathway. Phytomedicine117, 154922. 10.1016/j.phymed.2023.154922

  • 35

    FetoniA. R.PacielloF.MezzogoriD.RolesiR.EramoS. L. M.PaludettiG.et al (2015). Molecular targets for anticancer redox chemotherapy and cisplatin-induced ototoxicity: the role of curcumin on pSTAT3 and Nrf-2 signalling. Br. J. Cancer113, 14341444. 10.1038/bjc.2015.359

  • 36

    FishelR. (2015). Mismatch repair. J. Biol. Chem.290, 2639526403. 10.1074/jbc.R115.660142

  • 37

    FrikhaI.FakhfakhY.SahnounR.ChtourouL.MedhaffarM.ElloumiM. (2023). Imatinib mesylate-induced acute hepatotoxicity. J. Oncol. Pharm. Pract.29, 20272030. 10.1177/10781552231188307

  • 38

    GanaiS. A.SheikhF. A.BabaZ. A.MirM. A.MantooM. A.YatooM. A. (2021). Anticancer activity of the plant flavonoid luteolin against preclinical models of various cancers and insights on different signalling mechanisms modulated. Phytotherapy Res.35, 35093532. 10.1002/ptr.7044

  • 39

    GhoshR.BryantD. L.FaroneA. L. (2020). Panax quinquefolius (north American ginseng) polysaccharides as immunomodulators: current research status and future directions. Molecules25, 5854. 10.3390/molecules25245854

  • 40

    GoldsteinM.KastanM. B. (2015). The DNA damage response: implications for tumor responses to radiation and chemotherapy. Annu. Rev. Med.66, 129143. 10.1146/annurev-med-081313-121208

  • 41

    GoldsteinM.RoosW. P.KainaB. (2008). Apoptotic death induced by the cyclophosphamide analogue mafosfamide in human lymphoblastoid cells: contribution of DNA replication, transcription inhibition and Chk/p53 signaling. Toxicol. Appl. Pharmacol.229, 2032. 10.1016/j.taap.2008.01.001

  • 42

    GoodmanM. F.WoodgateR. (2013). Translesion DNA polymerases. Cold Spring Harb. Perspect. Biol.5, a010363. 10.1101/cshperspect.a010363

  • 43

    GordonP.LeGrandS. B.WalshD. (2014). Nausea and vomiting in advanced cancer. Eur. J. Pharmacol.722, 187191. 10.1016/j.ejphar.2013.10.010

  • 44

    GoudarziM.KalantarM.SadeghiE.KaramallahM. H.KalantarH. (2021). Protective effects of apigenin on altered lipid peroxidation, inflammation, and antioxidant factors in methotrexate-induced hepatotoxicity. Naunyn-Schmiedebergs Archives Pharmacol.394, 523531. 10.1007/s00210-020-01991-2

  • 45

    GrundyG. J.ParsonsJ. L. (2020). Base excision repair and its implications to cancer therapy. Essays Biochem.64, 831843. 10.1042/EBC20200013

  • 46

    HamdyN. M.EskanderG.BasaliousE. B. (2022). Insights on the dynamic innovative tumor targeted-nanoparticles-based drug delivery systems activation techniques. Int. J. Nanomedicine17, 61316155. 10.2147/ijn.S386037

  • 47

    HanahanD.WeinbergR. A. (2011). Hallmarks of cancer: the next generation. Cell144, 646674. 10.1016/j.cell.2011.02.013

  • 48

    HazlittR. A.MinJ.ZuoJ. (2018). Progress in the development of preventative drugs for cisplatin-induced hearing loss. J. Med. Chem.61, 55125524. 10.1021/acs.jmedchem.7b01653

  • 49

    HoeijmakersJ. H. J. (2001). Genome maintenance mechanisms for preventing cancer. Nature411, 366374. 10.1038/35077232

  • 50

    HossainM. B.Haldar NeerA. H. (2023). Chemotherapy. Cancer Treat. Res.185, 4958. 10.1007/978-3-031-27156-4_3

  • 51

    HuC.ZhangX.WeiW.ZhangN.WuH.MaZ.et al (2019). Matrine attenuates oxidative stress and cardiomyocyte apoptosis in doxorubicin-induced cardiotoxicity via maintaining AMPKα/UCP2 pathway. Acta Pharm. Sin. B9, 690701. 10.1016/j.apsb.2019.03.003

  • 52

    HuY.YangC.AmorimT.MaqboolM.LinJ.LiC.et al (2021). Cisplatin-mediated upregulation of APE2 binding to MYH9 provokes mitochondrial fragmentation and acute kidney injury. Cancer Res.81, 713723. 10.1158/0008-5472.Can-20-1010

  • 53

    HuangR.ZhouP.-K. (2021). DNA damage repair: historical perspectives, mechanistic pathways and clinical translation for targeted cancer therapy. Signal Transduct. Target. Ther.6, 254. 10.1038/s41392-021-00648-7

  • 54

    HuennekensF. M. (1994). The methotrexate story - a paradigm for development of cancer chemotherapeutic-agents. Adv. Enzyme Regul.34, 397419. 10.1016/0065-2571(94)90025-6

  • 55

    JinM. H.OhaD.-Y. (2019). ATM in DNA repair in cancer. Pharmacol. and Ther.203, 107391. 10.1016/j.pharmthera.2019.07.002

  • 56

    JiricnyJ. (2006). The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol.7, 335346. 10.1038/nrm1907

  • 57

    JongenJ. L. M.BroijlA.SonneveldP. (2015). Chemotherapy-induced peripheral neuropathies in hematological malignancies. J. Neuro-Oncology121, 229237. 10.1007/s11060-014-1632-x

  • 58

    KaraM.TurkonH.KaracaT.GucluO.UysalS.TurkyilmazM.et al (2016). Evaluation of the protective effects of hesperetin against cisplatin-induced ototoxicity in a rat animal model. Int. J. Pediatr. Otorhinolaryngology85, 1218. 10.1016/j.ijporl.2016.03.019

  • 59

    KatsuyaH.TamuraK. (2015). Side effects of chemotherapy. Nihon rinsho. Jpn. J. Clin. Med.73 (Suppl. 2), 3944.

  • 60

    KawaiY.NakaoT.KunimuraN.KohdaY.GembaM. (2006). Relationship of intracellular calcium and oxygen radicals to cisplatin-related renal cell injury. J. Pharmacol. Sci.100, 6572. 10.1254/jphs.FP0050661

  • 61

    KciukM.GielecinskaA.MujwarS.KolatD.Kaluzinska-KolatZ.CelikI.et al (2023). Doxorubicin-an agent with multiple mechanisms of anticancer activity. Cells12, 659. 10.3390/cells12040659

  • 62

    KeeY.D'AndreaA. D. (2010). Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes and Dev.24, 16801694. 10.1101/gad.1955310

  • 63

    KimG.IsonG.McKeeA. E.ZhangH.TangS.GwiseT.et al (2015). FDA approval summary: olaparib monotherapy in patients with deleterious germline BRCA-mutated advanced ovarian cancer treated with three or more lines of chemotherapy. Clin. Cancer Res.21, 42574261. 10.1158/1078-0432.Ccr-15-0887

  • 64

    KimH.-J.LeeJ.-H.KimS.-J.OhG. S.MoonH.-D.KwonK.-B.et al (2010). Roles of NADPH oxidases in cisplatin-induced reactive oxygen species generation and ototoxicity. J. Neurosci.30, 39333946. 10.1523/jneurosci.6054-09.2010

  • 65

    KimY.-J.WilsonD. M. (2012). Overview of base excision repair biochemistry. Curr. Mol. Pharmacol.5, 313. 10.2174/1874467211205010003

  • 66

    KoM.-H.SongS.-Y.HaS.-J.LeeJ. Y.YoonS. W.ParkJ.-H.et al (2021). Efficacy and safety of yukgunja-tang for patients with cancer-related anorexia: a randomized, controlled trial, pilot study. Integr. cancer Ther.20, 15347354211019107. 10.1177/15347354211019107

  • 67

    KruegerK.ThomaleJ.StojanovicN.OsmakM.HenningerC.BormannS.et al (2015). Platinum-induced kidney damage: unraveling the DNA damage response (DDR) of renal tubular epithelial and glomerular endothelial cells following platinum injury. Biochimica Biophysica Acta-Molecular Cell Res.1853, 685698. 10.1016/j.bbamcr.2014.12.033

  • 68

    KuperJ.KiskerC. (2023). At the core of nucleotide excision repair. Curr. Opin. Struct. Biol.80, 102605. 10.1016/j.sbi.2023.102605

  • 69

    KutuzovM. M.BelousovaE. A.IlinaE. S.LavrikO. I. (2020). “Impact of PARP1, PARP2 and PARP3 on the base excision repair of nucleosomal DNA,” in Mechanisms of genome protection and repair (Springer), 4757.

  • 70

    LefebvreJ.GlezermanI. G. (2017). Kidney toxicities associated with novel cancer therapies. Adv. Chronic Kidney Dis.24, 233240. 10.1053/j.ackd.2017.05.006

  • 71

    LiB.ShaoH.GaoL.LiH.ShengH.ZhuL. (2022). Nano-drug co-delivery system of natural active ingredients and chemotherapy drugs for cancer treatment: a review. Drug Deliv.29, 21302161. 10.1080/10717544.2022.2094498

  • 72

    LiH.LiuZ.-Y.WuN.ChenY.-C.ChengQ.WangJ. (2020). PARP inhibitor resistance: the underlying mechanisms and clinical implications. Mol. Cancer19, 107. 10.1186/s12943-020-01227-0

  • 73

    LiW.YanM.-H.LiuY.LiuZ.WangZ.ChenC.et al (2016). Ginsenoside Rg5 ameliorates cisplatin-induced nephrotoxicity in mice through inhibition of inflammation, oxidative stress, and apoptosis. Nutrients8, 566. 10.3390/nu8090566

  • 74

    LinJ.FangL.LiH.LiZ.LyuL.WangH.et al (2019). Astragaloside IV alleviates doxorubicin induced cardiomyopathy by inhibiting NADPH oxidase derived oxidative stress. Eur. J. Pharmacol.859, 172490. 10.1016/j.ejphar.2019.172490

  • 75

    LindahlT. (1993). Instability and decay of the primary structure of DNA. Nature362 (6422), 70915. 10.1038/362709a0

  • 76

    LiuG.ZhangJ.SunF.MaJ.QiX. (2022). Ginsenoside Rg2 attenuated trastuzumab-induced cardiotoxicity in rats. Biomed Res. Int.2022, 8866660. 10.1155/2022/8866660

  • 77

    LiuY.-Q.LiW.-Q.Morris-NatschkeS. L.QianK.YangL.ZhuG.-X.et al (2015). Perspectives on biologically active camptothecin derivatives. Med. Res. Rev.35, 753789. 10.1002/med.21342

  • 78

    LiuY.-Q.WangX.-L.HeD.-H.ChengY.-X. (2021). Protection against chemotherapy- and radiotherapy-induced side effects: a review based on the mechanisms and therapeutic opportunities of phytochemicals. Phytomedicine80, 153402. 10.1016/j.phymed.2020.153402

  • 79

    LoprinziC. L.LacchettiC.BleekerJ.CavalettiG.ChauhanC.HertzD. L.et al (2020). Prevention and management of chemotherapy-induced peripheral neuropathy in survivors of adult cancers: ASCO guideline update. J. Clin. Oncol.38, 33253348. 10.1200/jco.20.01399

  • 80

    Luis ZamoranoJ.LancellottiP.Rodriguez MunozD.AboyansV.AsteggianoR.GalderisiM.et al (2017). 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines the Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur. J. Heart Fail.19, 942. 10.1002/ejhf.654

  • 81

    MadedduC.DeiddaM.PirasA.CadedduC.DemurtasL.PuzzoniM.et al (2016). Pathophysiology of cardiotoxicity induced by nonanthracycline chemotherapy. J. Cardiovasc. Med.17, S12S18. 10.2459/jcm.0000000000000376

  • 82

    MarcusL.Fashoyin-AjeL. A.DonoghueM.YuanM.RodriguezL.GallagherP. S.et al (2021). FDA approval summary: pembrolizumab for the treatment of tumor mutational burden-high solid tumors. Clin. Cancer Res.27, 46854689. 10.1158/1078-0432.Ccr-21-0327

  • 83

    MarteijnJ. A.LansH.VermeulenW.HoeijmakersJ. H. J. (2014). Understanding nucleotide excision repair and its roles in cancer and ageing. Nat. Rev. Mol. Cell Biol.15, 465481. 10.1038/nrm3822

  • 84

    McCabeK. M.OlsonS. B.MosesR. E. (2009). DNA interstrand crosslink repair in mammalian cells. J. Cell. Physiology220, 569573. 10.1002/jcp.21811

  • 85

    McGowanJ. V.ChungR.MaulikA.PiotrowskaI.WalkerJ. M.YellonD. M. (2017). Anthracycline chemotherapy and cardiotoxicity. Cardiovasc. Drugs Ther.31, 6375. 10.1007/s10557-016-6711-0

  • 86

    MendoncaL. M.MachadoC. d. S.Correia TeixeiraC. C.Pedro de FreitaL. A.Pires BianchiM. d. L.Greggi AntunesL. M. (2013). Curcumin reduces cisplatin-induced neurotoxicity in NGF-differentiated PC12 cells. Neurotoxicology34, 205211. 10.1016/j.neuro.2012.09.011

  • 87

    MittalK.KoonH.ElsonP.TriozziP.DowlatiA.ChenH.et al (2014). Dual VEGF/VEGFR inhibition in advanced solid malignancies Clinical effects and pharmacodynamic biomarkers. Cancer Biol. and Ther.15, 975981. 10.4161/cbt.29187

  • 88

    ModrichP.LahueR. (1996). Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem.65, 101133. 10.1146/annurev.bi.65.070196.000533

  • 89

    MohiuddinI. S.KangM. H. (2019). DNA-PK as an emerging therapeutic target in cancer. Front. Oncol.9, 635. 10.3389/fonc.2019.00635

  • 90

    MorsyM. A.Abdel-LatifR.HafezS. M. N. A.KandeelM.Abdel-GaberS. A. (2022). Paeonol protects against methotrexate hepatotoxicity by repressing oxidative stress, inflammation, and apoptosis-the role of drug efflux transporters. Pharmaceuticals15, 1296. 10.3390/ph15101296

  • 91

    MotykaS.JafernikK.EkiertH.Sharifi-RadJ.CalinaD.Al-OmariB.et al (2023). Podophyllotoxin and its derivatives: potential anticancer agents of natural origin in cancer chemotherapy. Biomed. and Pharmacother.158, 114145. 10.1016/j.biopha.2022.114145

  • 92

    MoynahanM. E.JasinM. (2010). Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol.11, 196207. 10.1038/nrm2851

  • 93

    MunsterP.MitaM.MahipalA.NemunaitisJ.MassardC.MikkelsenT.et al (2019). First-in-human phase I study of A dual mTOR kinase and DNA-PK inhibitor (CC-115) in advanced malignancy. Cancer Manag. Res.11, 1046310476. 10.2147/cmar.S208720

  • 94

    NajafiM.TavakolS.ZarrabiA.AshrafizadehM. (2022). Dual role of quercetin in enhancing the efficacy of cisplatin in chemotherapy and protection against its side effects: a review. Archives Physiology Biochem.128, 14381452. 10.1080/13813455.2020.1773864

  • 95

    OhG.-S.KimH.-J.ChoiJ.-H.ShenA.KimC.-H.KimS.-J.et al (2011). Activation of lipopolysaccharide-TLR4 signaling accelerates the ototoxic potential of cisplatin in mice. J. Immunol.186, 11401150. 10.4049/jimmunol.1002183

  • 96

    OwumiS. E.LewuD. O.ArunsiU. O.OyelereA. K. (2021). Luteolin attenuates doxorubicin-induced derangements of liver and kidney by reducing oxidative and inflammatory stress to suppress apoptosis. Hum. and Exp. Toxicol.40, 16561672. 10.1177/09603271211006171

  • 97

    PacielloF.FetoniA. R.MezzogoriD.RolesiR.Di PinoA.PaludettiG.et al (2020). Publisher Correction: the dual role of curcumin and ferulic acid in counteracting chemoresistance and cisplatin-induced ototoxicity. Sci. Rep.10, 16468. 10.1038/s41598-020-70073-3

  • 98

    PanditB.RoyzenM. (2022). Recent development of prodrugs of gemcitabine. Genes13, 466. 10.3390/genes13030466

  • 99

    ParkY. J.KimK. S.ParkJ. H.LeeS. H.KimH. R.LeeS. H.et al (2020). Protective effects of dendropanoxide isolated from Dendropanax morbifera against cisplatin-induced acute kidney injury via the AMPK/mTOR signaling pathway. Food Chem. Toxicol.145, 111605. 10.1016/j.fct.2020.111605

  • 100

    PengY.PeiH. (2021). DNA alkylation lesion repair: outcomes and implications in cancer chemotherapy. J. Zhejiang University-Science B22, 4762. 10.1631/jzus.B2000344

  • 101

    PepponiR.MarraG.FuggettaM. P.FalcinelliS.PaganiE.BonmassarE.et al (2003). The effect of O-6-alkylguanine-DNA alkyltransferase and mismatch repair activities on the sensitivity of human melanoma cells to temozolomide, 1,3-bis(2-chloroethyl)-1-nitrosourea, and cisplatin. J. Pharmacol. Exp. Ther.304, 661668. 10.1124/jpet.102.043950

  • 102

    PommierY. (2006). Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer6, 789802. 10.1038/nrc1977

  • 103

    PuyoS.MontaudonD.PourquierP. (2014). From old alkylating agents to new minor groove binders. Crit. Rev. Oncol. Hematol.89, 4361. 10.1016/j.critrevonc.2013.07.006

  • 104

    QiF.ZhaoL.ZhouA.ZhangB.LiA.WangZ.et al (2015). The advantages of using traditional Chinese medicine as an adjunctive therapy in the whole course of cancer treatment instead of only terminal stage of cancer. Biosci. Trends9, 1634. 10.5582/bst.2015.01019

  • 105

    QiL.LuoQ.ZhangY.JiaF.ZhaoY.WangF. (2019). Advances in toxicological research of the anticancer drug cisplatin. Chem. Res. Toxicol.32, 14691486. 10.1021/acs.chemrestox.9b00204

  • 106

    RajskiS. R.WilliamsR. M. (1998). DNA cross-linking agents as antitumor drugs. Chem. Rev.98, 27232796. 10.1021/cr9800199

  • 107

    RezaeeR.MomtaziA. A.MonemiA.SahebkarA. (2017). Curcumin: a potentially powerful tool to reverse cisplatin-induced toxicity. Pharmacol. Res.117, 218227. 10.1016/j.phrs.2016.12.037

  • 108

    RocaJ. (1995). The mechanisms of DNA topoisomerases. Trends Biochem. Sci.20, 156160. 10.1016/s0968-0004(00)88993-8

  • 109

    Sahindokuyucu-KocasariF.AkyolY.OzmenO.Erdemli-KoseS. B.GarliS. (2021). Apigenin alleviates methotrexate-induced liver and kidney injury in mice. Hum. and Exp. Toxicol.40, 17211731. 10.1177/09603271211009964

  • 110

    SamodelovS. L.GaiZ.Kullak-UblickG. A.VisentinM. (2019). Renal reabsorption of folates: pharmacological and toxicological snapshots. Nutrients11, 2353. 10.3390/nu11102353

  • 111

    Sanchez-GonzalezP. D.Lopez-HernandezF. J.Perez-BarriocanalF.MoralesA. I.Lopez-NovoaJ. M. (2011). Quercetin reduces cisplatin nephrotoxicity in rats without compromising its anti-tumour activity. Nephrol. Dial. Transplant.26, 34843495. 10.1093/ndt/gfr195

  • 112

    ScullyR.PandayA.ElangoR.WillisN. A. (2019). DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat. Rev. Mol. Cell Biol.20, 698714. 10.1038/s41580-019-0152-0

  • 113

    SedgwickB.BatesP. A.PaikJ.JacobsS. C.LindahlT. (2007). Repair of alkylated DNA: recent advances. DNA Repair6, 429442. 10.1016/j.dnarep.2006.10.005

  • 114

    SethyC.KunduC. N. (2021). 5-Fluorouracil (5-FU) resistance and the new strategy to enhance the sensitivity against cancer: implication of DNA repair inhibition. Biomed. and Pharmacother.137, 111285. 10.1016/j.biopha.2021.111285

  • 115

    ShethS.MukherjeaD.RybakL. P.RamkumarV. (2017). Mechanisms of cisplatin-induced ototoxicity and otoprotection. Front. Cell. Neurosci.11, 338. 10.3389/fncel.2017.00338

  • 116

    SiegelR. L.MillerK. D.WagleN. S.JemalA. (2023). Cancer statistics, 2023. Ca-a Cancer J. Clin.73, 1748. 10.3322/caac.21763

  • 117

    SinhaB. K. (1995). Topoisomerase inhibitors - a review of their therapeutic potential in cancer. Drugs49, 1119. 10.2165/00003495-199549010-00002

  • 118

    SioudF.Ben ToumiaI.LahmerA.KhlifiR.DhaouefiZ.MaatoukM.et al (2020). Methanolic extract of Ephedra alata ameliorates cisplatin-induced nephrotoxicity and hepatotoxicity through reducing oxidative stress and genotoxicity. Environ. Sci. Pollut. Res.27, 1279212801. 10.1007/s11356-020-07904-3

  • 119

    SladeD. (2020). PARP and PARG inhibitors in cancer treatment. Genes and Dev.34, 360394. 10.1101/gad.334516.119

  • 120

    SuX.-L.WangJ.-W.CheH.WangC.-F.JiangH.LeiX.et al (2020). Clinical application and mechanism of traditional Chinese medicine in treatment of lung cancer. Chin. Med. J.133, 29872997. 10.1097/cm9.0000000000001141

  • 121

    SunY.ZhangY.XieL.RongF.ZhuX.XieJ.et al (2022). Progress in the treatment of drug-induced liver injury with natural products. Pharmacol. Res.183, 106361. 10.1016/j.phrs.2022.106361

  • 122

    TangC.LivingstonM. J.SafirsteinR.DongZ. (2023). Cisplatin nephrotoxicity: new insights and therapeutic implications. Nat. Rev. Nephrol.19, 5372. 10.1038/s41581-022-00631-7

  • 123

    ThongnuanjanP.SoodvilaiS.FongsupaS.ThipboonchooN.ChabangN.MunyooB.et al (2021). Panduratin A derivative protects against cisplatin-induced apoptosis of renal proximal tubular cells and kidney injury in mice. Molecules26, 6642. 10.3390/molecules26216642

  • 124

    TokucG. (2014). Relationship between cisplatin administration and the development of ototoxicity. Pediatr. Blood and Cancer61, S312.

  • 125

    TorreL. A.SiegelR. L.WardE. M.JemalA. (2016). Global cancer incidence and mortality rates and trends-an update. Cancer Epidemiol. Biomarkers and Prev.25, 1627. 10.1158/1055-9965.Epi-15-0578

  • 126

    UiA.ChibaN.YasuiA. (2020). Relationship among DNA double-strand break (DSB), DSB repair, and transcription prevents genome instability and cancer. Cancer Sci.111, 14431451. 10.1111/cas.14404

  • 127

    VyasS.ChangP. (2014). New PARP targets for cancer therapy. Nat. Rev. Cancer14, 502509. 10.1038/nrc3748

  • 128

    WangJ.LadrechS.PujolR.BrabetP.Van De WaterT. R.PuelJ. L. (2004). Caspase inhibitors, but not c-Jun NH2-terminal kinase inhibitor treatment, prevent cisplatin-induced hearing loss. Cancer Res.64, 92179224. 10.1158/0008-5472.Can-04-1581

  • 129

    WardS. J.McAllisterS. D.KawamuraR.MuraseR.NeelakantanH.WalkerE. A. (2014). Cannabidiol inhibits paclitaxel-induced neuropathic pain through 5-HT1A receptors without diminishing nervous system function or chemotherapy efficacy. Br. J. Pharmacol.171, 636645. 10.1111/bph.12439

  • 130

    WeiG.WangY.YangG.WangY.JuR. (2021). Recent progress in nanomedicine for enhanced cancer chemotherapy. Theranostics11, 63706392. 10.7150/thno.57828

  • 131

    WeiS.MaW.JiangC.LiuJ.LiuJ.ZhangB.et al (2023). Hyperoside prevents doxorubicin-induced cardiotoxicity by inhibiting NOXs/ROS/NLRP3 inflammasome signaling pathway. Phytotherapy Res.37, 41964209. 10.1002/ptr.7900

  • 132

    World Health Organization (2022). World Health organization cancer detail key facts. Available at: https://www.who.int/news-room/fact-sheets/detail/cancer.

  • 133

    WrightW. D.ShahS. S.HeyerW.-D. (2018). Homologous recombination and the repair of DNA double-strand breaks. J. Biol. Chem.293, 1052410535. 10.1074/jbc.TM118.000372

  • 134

    WuB.-Y.LiuC.-T.ChenS.-Y.TsaiM.-Y. (2015). A case of chemotherapy-induced congestive heart failure successfully treated with Chinese herbal medicine. Complementary Ther. Med.23, 251256. 10.1016/j.ctim.2015.01.006

  • 135

    WuQ.ChenJ.ZhengX.SongJ.YinL.GuoH.et al (2023). Kaempferol attenuates doxorubicin-induced renal tubular injury by inhibiting ROS/ASK1-mediated activation of the MAPK signaling pathway. Biomed. and Pharmacother.157, 114087. 10.1016/j.biopha.2022.114087

  • 136

    WuQ.LiW.ZhaoJ.SunW.YangQ.ChenC.et al (2021). Apigenin ameliorates doxorubicin-induced renal injury via inhibition of oxidative stress and inflammation. Biomed. and Pharmacother.137, 111308. 10.1016/j.biopha.2021.111308

  • 137

    WuX.LiX.SongY.LiH.BaiX.LiuW.et al (2017). Allicin protects auditory hair cells and spiral ganglion neurons from cisplatin - induced apoptosis. Neuropharmacology116, 429440. 10.1016/j.neuropharm.2017.01.001

  • 138

    WyldL.AudisioR. A.PostonG. J. (2015). The evolution of cancer surgery and future perspectives. Nat. Rev. Clin. Oncol.12, 115124. 10.1038/nrclinonc.2014.191

  • 139

    XiaoG.TangR.YangN.ChenY. (2023). Review on pharmacological effects of gastrodin. Archives Pharmacal Res.46, 744770. 10.1007/s12272-023-01463-0

  • 140

    XingJ.HouJ.MaZ.WangZ.RenS.WangY.et al (2019). Ginsenoside Rb3 provides protective effects against cisplatin-induced nephrotoxicity via regulation of AMPK-/mTOR-mediated autophagy and inhibition of apoptosis in vitro and in vivo. Cell Prolif.52, e12627. 10.1111/cpr.12627

  • 141

    YangC.GuoY.HuangT.ZhaoJ.HuangX.TangH.et al (2018). Asiatic acid protects against cisplatin-induced acute kidney injury via anti-apoptosis and anti-inflammation. Biomed. and Pharmacother.107, 13541362. 10.1016/j.biopha.2018.08.126

  • 142

    YangZ.NingR.LiuQ.ZangR.LiuS.SunS. (2023). Umbelliferone attenuates cisplatin-induced acute kidney injury by inhibiting oxidative stress and inflammation via NRF2. Physiol. Rep.11, e15879. 10.14814/phy2.15879

  • 143

    YapT. A.O'CarriganB.PenneyM. S.LimJ. S.BrownJ. S.LukenM. J. d. M.et al (2020). Phase I trial of first-in-class ATR inhibitor M6620 (VX-970) as monotherapy or in combination with carboplatin in patients with advanced solid tumors. J. Clin. Oncol.38, 31953204. 10.1200/jco.19.02404

  • 144

    YasarH.ErsoyA.CimenF. K.MammadovR.KurtN.ArslanY. K. (2019). Peripheral neurotoxic effects of cisplatin on rats and treatment with rutin. Adv. Clin. Exp. Med.28, 15371543. 10.17219/acem/111819

  • 145

    YelamosJ.Moreno-LamaL.JimenoJ.AliS. O. (2020). Immunomodulatory roles of PARP-1 and PARP-2: impact on PARP-centered cancer therapies. Cancers12, 392. 10.3390/cancers12020392

  • 146

    YouF.GaoC. (2019). Topoisomerase inhibitors and targeted delivery in cancer therapy. Curr. Top. Med. Chem.19, 713729. 10.2174/1568026619666190401112948

  • 147

    YuX.ManR.LiY.YangQ.LiH.YangH.et al (2019). Paeoniflorin protects spiral ganglion neurons from cisplatin-induced ototoxicity: possible relation to PINK1/BAD pathway. J. Cell. Mol. Med.23, 50985107. 10.1111/jcmm.14379

  • 148

    YuX.MengX.XuM.ZhangX.ZhangY.DingG.et al (2018). Celastrol ameliorates cisplatin nephrotoxicity by inhibiting NF-κB and improving mitochondrial function. Ebiomedicine36, 266280. 10.1016/j.ebiom.2018.09.031

  • 149

    YuanH.ZhaoY.LiS.QinJ.YuX. (2023). Madecassoside ameliorates cisplatin-induced nephrotoxicity by inhibiting activation of the mitogen activated protein kinase pathway. Environ. Toxicol.38, 14731483. 10.1002/tox.23777

  • 150

    ZhangL.LiD.LinL. (2019). Paeonol: pharmacological effects and mechanisms of action. Int. Immunopharmacol.72, 413421. 10.1016/j.intimp.2019.04.033

  • 151

    ZhangX.QiuH.LiC.CaiP.QiF. (2021). The positive role of traditional Chinese medicine as an adjunctive therapy for cancer. Biosci. Trends15, 283298. 10.5582/bst.2021.01318

  • 152

    ZhangY.LiuS.MaJ.-L.ChenC.HuangP.JiJ.-H.et al (2022). Apocynum venetum leaf extract alleviated doxorubicin-induced cardiotoxicity through the AKT/Bcl-2 signaling pathway. Phytomedicine94, 153815. 10.1016/j.phymed.2021.153815

  • 153

    ZhangY.LouY.WangJ.YuC.ShenW. (2021). Research status and molecular mechanism of the traditional Chinese medicine and antitumor therapy combined strategy based on tumor microenvironment. Front. Immunol.11, 609705. 10.3389/fimmu.2020.609705

  • 154

    ZhangY.QuX.GaoH.ZhaiJ.TaoL.SunJ.et al (2020). Quercetin attenuates NLRP3 inflammasome activation and apoptosis to protect INH-induced liver injury via regulating SIRT1 pathway. Int. Immunopharmacol.85, 106634. 10.1016/j.intimp.2020.106634

  • 155

    ZhouB.YangY.PangX.ShiJ.JiangT.ZhengX. (2023). Quercetin inhibits DNA damage responses to induce apoptosis via SIRT5/PI3K/AKT pathway in non-small cell lung cancer. Biomed. and Pharmacother.165, 115071. 10.1016/j.biopha.2023.115071

  • 156

    ZhouM.DaiY.MaY.YanY.HuaM.GaoQ.et al (2022). Protective effects of liquiritigenin against cisplatin-induced nephrotoxicity via NRF2/SIRT3-mediated improvement of mitochondrial function. Molecules27, 3823. 10.3390/molecules27123823

  • 157

    ZhuC.RenX.LiuD.ZhangC. (2021). Oxaliplatin-induced hepatic sinusoidal obstruction syndrome. Toxicology460, 152882. 10.1016/j.tox.2021.152882

Summary

Keywords

DNA damage, chemotherapy, cancer treatment, traditional Chinese medicine, side-effects

Citation

Bai B, Ma Y, Liu D, Zhang Y, Zhang W, Shi R and Zhou Q (2024) DNA damage caused by chemotherapy has duality, and traditional Chinese medicine may be a better choice to reduce its toxicity. Front. Pharmacol. 15:1483160. doi: 10.3389/fphar.2024.1483160

Received

19 August 2024

Accepted

14 October 2024

Published

22 October 2024

Volume

15 - 2024

Edited by

Mohammed Abu El-Magd, Kafrelsheikh University, Egypt

Reviewed by

Ali AbdElKader, Kafrelsheikh University, Egypt

Nemany A. N. Hanafy, Kafrelsheikh University, Egypt

Amr Adel Elkelish, Suez Canal University, Egypt

Updates

Copyright

*Correspondence: Rong Shi, ; Qianmei Zhou,

† These authors have contributed equally to this work

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Outline

Figures

Cite article

Copy to clipboard


Export citation file


Share article

Article metrics