Abstract
Foodbone norovirus (NoV) is the leading cause of acute gastroenteritis worldwide. Candidate vaccines are being developed, however, no licensed vaccines are currently available for managing NoV infections. Screening for stimulated antibodies with broad-spectrum binding activities can be performed for the development of NoV polyvalent vaccines. In this study, we aimed to develop an indirect enzyme-linked immunosorbent assay (ELISA) for testing the broad spectrum of anti-NoV antibodies. Capsid P proteins from 28 representative NoV strains (GI.1–GI.9 and GII.1–GII.22 except GII.11, GII.18, and GII.19) were selected, prepared, and used as coating antigens on one microplate. Combined with incubation and the horseradish peroxidase chromogenic reaction, the entire process for testing the spectrum of unknown antibodies required 2 h for completion. The intra-assay and inter-assay coefficients of variation were less than 10%. The new method was successfully performed with monoclonal antibodies and polyclonal antibodies induced by multiple antigens. In conclusion, the indirect ELISA assay developed in this study had a good performance of reliability, convenience, and high-throughput screening for broad-spectrum antibodies.
Introduction
Foodbone Norovirus (NoV) is one of the leading causes of epidemic acute gastroenteritis (AGE) worldwide, accounting for one-fifth of all gastroenteritis cases globally (). Annually, NoV has been estimated to cause 677 million episodes of diarrheal disease (95% uncertainty interval [UI]: 468–1,153 million) and 213,515 deaths (95% UI: 171,783–266,561) for all ages and among all modes of transmission (). NoV is extremely contagious, and transmission occurs directly from person to person via fecal-oral and vomit-oral routes, but can also be caused by food-borne, water-borne, or environmental factors (). Vomitus and feces of infected patients contain a considerable number of virions, whereas as few as 10 infectious particles are sufficient to cause AGE (). Additionally, NoV shedding after infection usually lasts for several weeks, and prolonged shedding post-infection can also contribute to spreading (). Thus, NoV remains a major threat to public health. Owing to the significant social and economic burden associated with the disease, adequate preventive measures against this virus should be formulated.
NoV strains can be classified into 10 genogroups (GI–GX) and at least 48 genotypes based on the diversity of the VP1 amino acid sequence; GI, GII, and GIV have been shown to cause infections in humans (). Human histo-blood group antigens (HBGAs) can be used as receptor or co-receptor for NoV infection (; ). The binding ability between NoVs and HBGAs is diverse, resulting in different infectivity. The global pandemic GII.4 NoV can infect almost all secretory individuals (); GI.1 VLP binds to A, AB, and O type, but not to B type saliva (); individuals with O type saliva are relatively susceptible to NoV, while with B type are not (); some strains do not bind any phenotype of HGBAs ().
Several possible barriers hinder the development of effective NoV vaccines (). First, circulating NoV exhibits genetic diversity and high variation, which may limit the durability of protection conferred by a vaccine that does not elicit broadly neutralizing antibodies. Second, the lack of sufficient cell lines for virus culture and successful animal models further hinders the development of antiviral drugs and vaccines. The following three types of NoV vaccines have been developed: virus-like particles (VLPs) that resemble the organization and morphology of native virus, P particles that resemble the P domain of native virus, and recombinant adenoviruses ().
Enzyme-linked immunosorbent assay (ELISA) is a sensitive and specific analytical biochemistry assay utilized for the detection and quantitative or qualitative analysis of an analyte without the requirement for sophisticated or expensive equipment (). Currently, ELISA is used as an ideal method for the detection of viruses and antibodies (; ; ). However, few ELISA techniques demonstrate the ability to directly detect the broad-spectrum binding activities of antibodies against all NoV strains that infect humans. Therefore, it is necessary to develop an indirect ELISA technique for the detection of a wide range of antibodies.
In this study, we aimed to develop an ELISA technique for vaccine development via rapid, efficient, and accurate screening of a substantial number of broad-spectrum antibodies.
Materials and Methods
Selection of Representative Strains
The antigen used in this experiment was capsid P protein for each representative strain of NoV stored in our laboratory. We selected nine GI strains (GI.1–GI.9) and nineteen GII strains (GII.1–GII.22) as representative NoV strains; GII.11, GII.18, and GII.19, which were detected in swine (), were excluded. In our previous study, GII.2, GII.3, GII.4, GII.6, GII.8, and GII.17 NoV were detected and preserved (; ; ), which could be directly used for cloning. Others were synthesized.
Pre-coated of Antigen
For preparation of microplates, 96-well plates were coated with 0.2 μg of 28 NoV capsid P proteins after incubation at 4°C overnight (three well per P protein). After subjecting the wells to washing steps with phosphate-buffered saline containing Tween 20 (PBST) three times, the wells were blocked using 5% skim milk for 2 h at 37°C; then, the wells were washed three times using PBST, dried, and stored at 4°C until further use. A combination of glutathione S-transferase (GST)-tagged protein and commercial anti-GST antibodies was used as a quality control. The negative serum was used as a negative control.
Enzyme Linked Immunosorbent Assay (ELISA)
The indirect ELISA method was used to detect the broad spectrum of antibodies (Figure 1). Briefly, the pre-coated microtiter plate was taken out. Serum samples were added at an appropriate dilution, which corresponded to the OD value in the range of 0.8–1.2, followed by incubation for 1 h at 37°C. Subsequently, secondary horseradish peroxidase-conjugated goat anti-mouse IgG antibodies (diluted 1: 3,000) were added and the plates were incubated for 30 min at 37°C. Tetramethylbenzidine was added as a peroxidase chromogenic substrate and reaction for 8 min at 37°C was performed. After terminating the substrate reaction with 2 M H2SO4, the optical density (OD) was measured at 450 nm. Positive signal is defined as a mean OD450 >0.2 after background subtraction (; ; ).
FIGURE 1
Performance Analysis
Intra-Assay Precision
Three replicates for each monoclonal antibody sample were analyzed using the same microplate. Precision was determined by calculating the mean, standard deviation, and coefficient of variation (CV%).
Inter-Assay Precision
For determination of inter-assay reproducibility, three replicates for each sample were analyzed in different microplates. Precision was determined by calculating the mean, standard deviation, and CV%.
Statistical Analysis
Statistical analyses were performed using Microsoft Excel 2016 and GraphPad Prism 8.0 software. Broad spectrum plot data are presented as mean ± standard deviation.
Results
Assembly of Microplates
To perform this experiment, we selected representative strains for capsid P proteins of all genotypes in GI (GI.1–GI.9) and GII (GII.1–GII.22), except for GII.18, GII.19, and GII.20 (Table 1 and Supplementary Figure 1). As shown in Figure 2, the microplate was coated with 28 capsid P proteins obtained from representative strains, and each P protein was coated in three wells.
TABLE 1
| Strain designation | GenBank accession no. |
| GI.1 | NC_001959 |
| GI.2 | L07418 |
| GI.3 | KJ196292 |
| GI.4 | AB042808 |
| GI.5 | AB039774 |
| GI.6 | LC342057 |
| GI.7 | KU311161 |
| GI.8 | KJ196298 |
| GI.9 | KF586507 |
| GII.1 | HCU07611 |
| GII.2 | MK729086 |
| GII.3 | KY348697 |
| GII.4 | KT202793 |
| GII.5 | KJ196288 |
| GII.6 | JX989075 |
| GII.7 | KJ196295 |
| GII.8 | MK213549 |
| GII.9 | AY038599 |
| GII.10 | AF504671 |
| GII.12 | AB045603 |
| GII.13 | KJ196276 |
| GII.14 | KJ196278 |
| GII.15 | KJ196290 |
| GII.16 | AY772730 |
| GII.17 | KT970369 |
| GII.20 | EU424333 |
| GII.21 | KJ196284 |
| GII.22 | MG495082 |
Selection of norovirus strains used as coating antigens.
FIGURE 2
Broad-Spectrum Antibody Assay
To determine the effectiveness of the method, two GII.4 monoclonal antibodies (GII.4-4A21C1 and GII.4-5D41A12) and one bivalent (GII.4 + GII.8) polyclonal antibody were tested for broad-spectrum detection. When the OD was in the range of 0.8–1.2, the dilution of the above three antibodies were between 1:4000–1:16000, 1:4000–1:16000, and 1:500–1:1000, respectively (unpublished data). Accordingly, the two monoclonal antibodies dilution of 1:5000 and the polyclonal antibody dilution of 1:500 were used for broad-spectrum detection.
The GII.4-4A21C1 monoclonal antibodies only showed reaction with GII.4 P particles at a high OD value of 0.96 and did not exhibit reaction with the other 27 NoV P particles (Figure 3A), demonstrating that this monoclonal antibody had strong specificity. Similarly, GII.4-5D41A12 monoclonal antibodies had a binding signal of 0.95 (Figure 3B). The polyclonal antibodies (GII.4 + GII.8) showed the highest signal reaction with GII.4 and GII.8 P particles, followed by GI.1, GII.2, GII.7, GII.9, GII.14, GII.20, and GII.22, and moderate signals were observed for the remaining antibodies (Figure 3C). GST bound with GST monoclonal antibodies at OD values of 0.98, 0.96, and 0.98, indicating that the developed ELISA technique was reliable.
FIGURE 3
Reproducibility of ELISA
Next, we evaluated intra-assay and inter-assay variabilities to test the reproducibility of the method. The monoclonal antibodies GII.4-4A21C1 and GII.4-5D41A12 and the polyclonal antibodies GII.4 + GII.8 were analyzed three times in each microplate. Intra-assay CVs were observed to be in the ranges of 0.63–9.62% (Table 2), 0–9.99% (Table 3), and 0.55–9.88% (Table 4), respectively. After repeating the experiments in three batches of plates prepared for 3 days, the inter-assay CVs were found to be in the ranges of 0.22–9.08% (Table 2), 0.3–9.76% (Table 3), and 0.21–9.99% (Table 4). These results indicated that the developed ELISA technique showed good reproducibility.
TABLE 2
| GII.4-4A21C1 | Intra-assay Precision CV/% | Inter-assay Precision CV/% | ||
| Antigen designation | 1 | 2 | 3 | – |
| GI.1 | 1.80 | 8.02 | 9.01 | 3.52 |
| GI.2 | 3.87 | 4.02 | 5.76 | 1.83 |
| GI.3 | 9.45 | 3.22 | 2.94 | 5.37 |
| GI.4 | 2.12 | 0.83 | 2.22 | 1.65 |
| GI.5 | 3.81 | 4.68 | 7.88 | 1.98 |
| GI.6 | 1.67 | 5.08 | 7.53 | 1.43 |
| GI.7 | 2.50 | 1.85 | 7.22 | 1.08 |
| GI.8 | 5.65 | 2.66 | 8.41 | 1.52 |
| GI.9 | 2.55 | 3.77 | 6.42 | 5.26 |
| GII.1 | 2.59 | 3.13 | 5.80 | 4.07 |
| GII.2 | 2.31 | 3.87 | 0.81 | 0.22 |
| GII.3 | 6.32 | 4.49 | 7.12 | 1.27 |
| GII.4 | 3.36 | 4.82 | 5.24 | 9.08 |
| GII.5 | 4.63 | 3.28 | 3.72 | 3.18 |
| GII.6 | 0.63 | 0.65 | 2.62 | 1.85 |
| GII.7 | 8.62 | 3.13 | 2.34 | 1.54 |
| GII.8 | 1.86 | 6.25 | 6.78 | 1.59 |
| GII.9 | 8.09 | 0.97 | 2.71 | 1.39 |
| GII.10 | 1.75 | 6.81 | 5.59 | 1.54 |
| GII.12 | 2.35 | 8.70 | 5.28 | 2.99 |
| GII.13 | 3.20 | 4.92 | 4.58 | 0.26 |
| GII.14 | 1.64 | 3.70 | 9.23 | 1.08 |
| GII.15 | 0.00 | 8.84 | 0.88 | 5.09 |
| GII.16 | 4.01 | 3.23 | 8.80 | 3.13 |
| GII.17 | 0.82 | 3.28 | 9.62 | 0.24 |
| GII.20 | 2.55 | 2.30 | 5.88 | 1.24 |
| GII.21 | 1.61 | 2.40 | 1.52 | 1.33 |
| GII.22 | 3.81 | 3.44 | 3.28 | 7.69 |
Intra- and inter-assay coefficients of variation (%) for the broad-spectrum detection of GII.4-4A21C1 monoclonal antibodies by ELISA.
TABLE 3
| GII.4-5D41A12 | Intra-assay Precision CV/% | Inter-assay Precision CV/% | ||
| Antigen designation | 1 | 2 | 3 | – |
| GI.1 | 5.41 | 6.14 | 2.83 | 2.59 |
| GI.2 | 1.81 | 2.41 | 1.32 | 8.92 |
| GI.3 | 1.61 | 1.63 | 5.53 | 9.76 |
| GI.4 | 2.71 | 4.27 | 2.34 | 8.71 |
| GI.5 | 9.88 | 4.41 | 0.83 | 2.87 |
| GI.6 | 4.20 | 0.00 | 6.40 | 4.07 |
| GI.7 | 4.68 | 3.68 | 3.08 | 5.57 |
| GI.8 | 0.00 | 6.83 | 3.63 | 8.63 |
| GI.9 | 2.26 | 2.71 | 3.89 | 2.98 |
| GII.1 | 0.00 | 1.82 | 2.79 | 1.23 |
| GII.2 | 2.08 | 7.23 | 2.51 | 6.57 |
| GII.3 | 8.52 | 3.76 | 1.95 | 8.95 |
| GII.4 | 6.80 | 5.54 | 5.38 | 3.81 |
| GII.5 | 3.12 | 1.68 | 1.79 | 3.26 |
| GII.6 | 3.72 | 6.59 | 1.28 | 9.47 |
| GII.7 | 4.27 | 2.36 | 1.79 | 2.28 |
| GII.8 | 8.52 | 2.94 | 9.05 | 3.38 |
| GII.9 | 0.98 | 1.76 | 1.64 | 5.77 |
| GII.10 | 0.88 | 2.37 | 6.09 | 5.61 |
| GII.12 | 1.67 | 2.11 | 5.62 | 3.61 |
| GII.13 | 5.23 | 5.91 | 9.99 | 1.77 |
| GII.14 | 8.65 | 4.13 | 5.95 | 0.30 |
| GII.15 | 0.00 | 0.91 | 1.61 | 1.54 |
| GII.16 | 2.44 | 2.30 | 5.00 | 2.85 |
| GII.17 | 4.20 | 4.26 | 2.17 | 1.64 |
| GII.20 | 2.22 | 2.31 | 3.74 | 5.82 |
| GII.21 | 3.59 | 1.49 | 2.37 | 2.36 |
| GII.22 | 4.68 | 0.83 | 5.01 | 2.52 |
Intra- and inter-assay coefficients of variation for the broad-spectrum detection of GII.4-5D41A12 monoclonal antibodies by ELISA.
TABLE 4
| GII.4 + II.8 | Intra-assay Precision CV/% | Inter-assay Precision CV/% | ||
| Antigen designation | 1 | 2 | 3 | – |
| GI.1 | 3.44 | 2.81 | 3.88 | 9.21 |
| GI.2 | 5.49 | 3.50 | 4.21 | 0.94 |
| GI.3 | 2.50 | 2.94 | 6.57 | 9.99 |
| GI.4 | 3.26 | 4.40 | 2.81 | 1.27 |
| GI.5 | 2.68 | 2.40 | 2.60 | 3.63 |
| GI.6 | 6.46 | 4.00 | 5.03 | 4.48 |
| GI.7 | 3.72 | 4.73 | 0.97 | 8.74 |
| GI.8 | 3.77 | 1.27 | 1.24 | 9.16 |
| GI.9 | 3.43 | 0.92 | 1.71 | 3.56 |
| GII.1 | 4.67 | 1.43 | 3.76 | 4.39 |
| GII.2 | 3.29 | 3.22 | 2.27 | 3.31 |
| GII.3 | 4.35 | 4.22 | 3.07 | 1.88 |
| GII.4 | 3.35 | 1.48 | 1.68 | 2.43 |
| GII.5 | 4.03 | 6.63 | 5.23 | 3.83 |
| GII.6 | 4.35 | 0.95 | 0.62 | 9.79 |
| GII.7 | 4.59 | 1.88 | 3.77 | 2.50 |
| GII.8 | 1.75 | 2.09 | 3.40 | 4.95 |
| GII.9 | 4.46 | 0.55 | 5.55 | 2.25 |
| GII.10 | 3.20 | 2.84 | 3.00 | 1.12 |
| GII.12 | 0.82 | 1.10 | 1.01 | 2.25 |
| GII.13 | 4.42 | 3.09 | 2.85 | 9.25 |
| GII.14 | 3.65 | 1.58 | 2.52 | 2.73 |
| GII.15 | 8.80 | 8.86 | 4.57 | 7.19 |
| GII.16 | 2.43 | 3.79 | 4.28 | 2.12 |
| GII.17 | 0.75 | 4.23 | 3.17 | 1.79 |
| GII.20 | 1.76 | 0.81 | 4.09 | 1.89 |
| GII.21 | 1.47 | 1.71 | 4.89 | 0.21 |
| GII.22 | 2.03 | 0.49 | 6.46 | 3.27 |
Intra- and inter-assay coefficients of variation for the broad-spectrum detection of GII.4 + GII.8 polyclonal antibodies by ELISA.
Discussion
Owing to the high frequencies of NoV outbreaks (; ; ) and severe acute gastroenteritis (; ), high risk of infection transmission (; ; ), and enormous socioeconomic burden after infection (), the development of NoV vaccines is critical for improving public health. However, the characteristics of NoV genetic diversity and high variation have markedly hindered vaccine development.
At present, NoV vaccines rely on VLP and P particles prepared by bioengineering technology as subunit vaccines. The morphology and antigenicity of recombinant NoV VLP are similar to natural virus particles (). Preclinical studies have shown that VLP is immunogenic when administered by intranasal, oral or parenteral routes, which can induce serum and mucosal immune responses, and co-administration with mucosal adjuvants induces stronger immune responses (). Three surface loops per P domain are potential sites for foreign antigen presentation, which could enhance the antigenicity and immunogenicity of antigens (). have shown that immune P particles induced antiserum in both mice (1:245,600) and rabbits (1:145,700), and also induced neutralizing antibodies to block the binding of NoV variants and receptors. The results prove the immunogenicity of P particles. Therefore, both NoV VLP and P particles are suitable choices for vaccine preparation.
Several NoV vaccines using a variety of different technologies have been developed, including three in clinical trials. The first is the bivalent intramuscular GI/GII.4 vaccine developed by Takeda Pharmaceutical Company Limited (). The second, developed by Vaxart, Inc., is based on a G I.1 NoV sequence (). The third is the NoV tetravalent vaccine developed by Institut Pasteur of Shanghai Chinese Academy of Sciences and Chongqing Zhifei Biological Products Co., Ltd. (). Therefore, analysis of cross-protection among different strains is a significant step for the development of a successful NoV vaccine.
The immune cross-protection between different genotypes is complicated. Studies have shown GI.1 can induce blockade antibodies against other GI strains (); GII.4 antiserum and GII.17 antiserum have limited cross-reactivity or no cross-protection; demonstrated there is no cross-cluster protection between GI and GII, but the research of showed GI.1 infection will cause an increase of GII.4 antiserum. In short, the development of effective vaccines must contain both GI and GII viruses.
In addition to vaccine development, detection technology is also an important part of NoV prevention and control. The immunoassay methods mainly include enzyme linked immunosorbent assay (ELISA) and immunochromatographic (ICG). In this study, capsid P proteins of 28 representative NoV strains were used as coating antigens for the development of an indirect ELISA to detect their binding ability with antibodies. The broad spectrum of NoV antisera could be quickly detected using this method. Furthermore, one genotype or a combination of genotypes with broad-spectrum detection could be screened for the design of multivalent vaccines. Owing to the genetic diversity of NoV and 5%–10% cross-reactivity observed among genotypes (lower cross-reactivity among genogroups), the development of a broad-spectrum multivalent vaccine platform is necessary to protect against as many NoV-prevalent strains as possible ().
In summary, in this study, we developed an indirect ELISA with the potential to serve as a rapid, reliable, and high-throughput method for screening broad-spectrum antibodies to expedite the development of NoV vaccines.
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Statements
Data availability statement
The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding authors.
Author contributions
YZ and LX designed the experiments and wrote the manuscript. YJ and WC contributed reagents, materials, and analysis tools. JG, YyL, and YhL performed the experiments. YLi, TC, and LW analyzed the data. MC and JW revised the manuscript. YD, JZ, and QW provided project funding. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by the National Natural Science Foundation of China (31872912 and 31701717), the Natural Science Foundations of Guangdong Province for Distinguished Young Scholars (2019B151502065), the Key Research and Development Program of Guangdong Province (2019B020209001), and GDAS’Project of Science and Technology Development (2020GDASYL-20200104008).
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. The handling editor declared a shared affiliation, with one of the author YD at the time of the review.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb.2021.670488/full#supplementary-material
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Summary
Keywords
norovirus, capsid P protein, enzyme-linked immunosorbent assay, broad-spectrum antibodies, inter-assay/intra-assay variation
Citation
Zuo Y, Xue L, Gao J, Liao Y, Jiang Y, Li Y, Liang Y, Wang L, Cai W, Cheng T, Wang J, Chen M, Zhang J, Ding Y and Wu Q (2021) Development and Application of a Novel Rapid and Throughput Method for Broad-Spectrum Anti-Foodborne Norovirus Antibody Testing. Front. Microbiol. 12:670488. doi: 10.3389/fmicb.2021.670488
Received
21 February 2021
Accepted
13 August 2021
Published
03 September 2021
Volume
12 - 2021
Edited by
Xiyang Wu, Jinan University, China
Reviewed by
Hongtao Lei, South China Agricultural University, China; Tony Mutukumira, Massey University, New Zealand
Updates
Copyright
© 2021 Zuo, Xue, Gao, Liao, Jiang, Li, Liang, Wang, Cai, Cheng, Wang, Chen, Zhang, Ding and Wu.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Qingping Wu, wuqp203@163.comYu Ding, dingyu@jnu.edu.cn
†These authors share first authorship
This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology
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