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MINI REVIEW article

Front. Oncol., 13 January 2022
Sec. Cancer Epidemiology and Prevention
https://doi.org/10.3389/fonc.2021.810060

New Insights Into c.815_824dup Pathogenic Variant of BRCA1 in Inherited Breast Cancer: A Founder Mutation of West African Origin

Jean Pascal Demba Diop1, Andréa Régina Gnilane Sène1, Yacouba Dia1, Seydi Abdoul Ba1, Serigne Saliou Mbacke1, Cheikh Ameth Tidiane Ly1, Pierre Diaga Sarr1, Doudou Diouf2, Sidy Ka2, Babacar Mbengue3, Serigne Modou Kane Gueye4, Pape Saloum Diop5, Maguette Sylla Niang3, Papa Madieye Gueye6, Philomene Lopez Sall6, Ahmadou Dem2, Aynina Cisse6, Alioune Dieye3 and Rokhaya Ndiaye1*
  • 1Division of Human Genetics, Faculty of Medicine, Pharmacy and Odontology, University Cheikh Anta Diop (UCAD), Dakar, Senegal
  • 2Joliot Curie Institute, Aristide Le Dantec Hospital, Dakar, Senegal
  • 3Immunology Unit, Faculty of Medicine, Pharmacy and Odontology, University Cheikh Anta Diop (UCAD), Dakar, Senegal
  • 4Gynecology Unit, Aristide Le Dantec Hospital, Dakar, Senegal
  • 5Unit of General Surgery, General Hospital Idrissa Pouye, Dakar, Senegal
  • 6Laboratory of Pharmaceutical Biochemistry, Faculty of Medicine, Pharmacy and Odontology, University Cheikh Anta Diop (UCAD), Dakar, Senegal

Founder mutations have been reported in BRCA1 and BCRA2 in different ethnic groups with inherited breast cancer. Testing of targeted mutations in specific populations is important for cancer prevention in mutation carriers. In Sub-Saharan Africa, only a few studies have reported specific founder mutations in inherited breast cancer. The pathogenic variant c.815_824dup of BRCA1 has been reported as the most frequent among African American populations with inherited breast cancer and was supposed to have a West African origin. Recent report from Senegal identified this variant in women with inherited breast cancer at the highest frequency ever reported. The variant was linked to a common haplotype confirming its founder effect in West Africa. In this article, we review the mutation history of c.815_824dup and discuss how it spread out of Africa through the transatlantic slave trade.

Introduction

About 5%–10% of breast cancer cases are associated with inherited susceptibility. A subset of these are linked to germline pathogenic variants in BRCA1 and BRCA2 tumor suppressor genes (1). Women who have inherited the BRCA1 or the BRCA2 mutation are at greater risk of developing breast and/or ovarian cancer (2, 3). Studies in different populations have identified pathogenic variants stored in BRCA mutation consortia databases: CIMBA (Consortium of Investigators of Modifiers of BRCA1/2), ENIGMA (Evidence-Based Network for the Interpretation of Germline Mutant Alleles), BRCA Share (formerly the UMD-BRCA1 mutations database), and BRCA Exchange (https://brcaexchange.org). Some of these variants are at very high frequencies in specific ethnic groups, suggesting their founding effect. In Sub-Saharan Africa, a few studies have reported specific founder mutations (4, 5). Recently, we have reported a founder mutation, c.815_824dup, of the BRCA1 gene in Senegalese women with inherited breast cancer (6). This mutation is a duplication of 10 nucleotides (c.815_824dupAGCCATGTGG, p.Thr276AfsX14) located in exon 11 of BRCA1 according to the Human Genome Variation Society (HGVS) nomenclature and leads to a frameshift and a truncated protein. A previous study on African American women has reported the variant as a founder mutation of West African Origin (7).

History of the c.815_824dup BRCA1 Pathogenic Variant

Review from the literature has shown that c.815_824dup was first described in 1997 in a breast cancer patient from the Ivory Coast living in the US who had a familial history of breast, ovarian, and prostate cancers (8). In 1999, Mefford et al. identified the variant in four other families of African origin: one from the Bahamas and three in the US (South Carolina, Florida, and Washington, DC) (7). It was suggested that the variant may be an ancient West African founder mutation (7). Thereafter, the variant was reported in other African admixture populations with inherited breast cancer throughout the world (Bahamas, Peru, Mexico, France, Spain, and North America) (917). Literature search showed that the variant has been reported in 23 studies (Table 1). A review by Friebel et al. (31) revealed that the c.815_824dup pathogenic variant was detected in 76 individuals from the CIMBA database, 34 individuals from the Breast Cancer Information Core (BIC) database, and 16 individuals from ClinVar. Overall, the variant was identified in 155 patients. Of these, 100 were self-reported African ancestry (SRAA): 46 African American, 2 African (from Senegal), 6 Caribbean, and 46 of other African descent (31). The allelic frequency of the variant was estimated among African American women with inherited breast cancer at 16% in 2018 (15) and at 12% in 2020 (18).

TABLE 1
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Table 1 Studies reporting the c.815_824dup pathogenic variant throughout the world.

BRCA1 c.815_824dup Pathogenic Variant in Africa

In Africa, until October 2021, only one study from our team has reported the variant in patients diagnosed with inherited breast cancer (6). The variant was identified in 15 index cases with a family history of breast and/or ovarian cancer, out of 27 recruited. Allelic frequency was estimated at 27.7% compared to sporadic breast cancer cases (5%) and healthy controls (0.55%) (6). We have then implemented in our laboratory a PCR genotyping method of the variant for oncogenetic counseling. Screening of the variant in 19 other index cases with a family history of breast cancer identified the variant in heterozygous state in 11 cases. The variant was also found in 8 out of 36 patients diagnosed without a known family history of breast cancer at under 50 years of age (allelic frequency estimated at 11.11%). These data strongly support the implication of the variant in inherited breast cancer.

Overall, the c.815_824dup variant was identified in 26 families out of 46 (allelic frequency estimated at 28.26%). Screening of the variant in healthy relatives also identified the variant in 13 out of 29, confirming its implication in disease etiology. This is the highest frequency of this variant ever reported in a population. The allelic frequency of c.815_824dup is rarely documented throughout the different BRCA variant databases. Available information is from gnomAD and TopMed, where frequencies were estimated at 2.09726 × 10−5 and 7.15273 × 10−5, respectively, worldwide and in the African population. Other databases revealed the presence of this variant in individuals with African origin [Allele Frequency Aggregator (ALFA), CIMBA, ClinVar, and BIC databases], while any allelic frequency was documented. Larger studies in African countries are needed to estimate the exact allelic frequency of the variant among the African population.

West African Origin of BRCA1 c.815_824dup

Haplotype analysis of seven microsatellite markers flanking the BRCA1 gene and distributed in 2.15 Mb has identified a common haplotype of ~400 kb in Senegalese patients. This haplotype was not observed in any of the 48 healthy controls studied and is shorter than the one reported among African Americans spanning 700 kb (6). Age estimation of the Senegalese haplotype was 1,400 years, while it was 200 years in the US (7). Subsequently, we hypothesized that the variant appeared first in West Africa and spread throughout the world by population migration.

Discussion

Founder mutations linked to inherited breast cancer have been reported in BRCA1 and BRCA2 genes in different populations. The most known is the Ashkenazi Jewish pathogenic variant c.66_67AG (p.Glu23fs) reported in the US, Europe, Asia, and among Afrikaners from South Africa, while it was not reported in Sub-Saharan Africa, where other mutations have been identified (15, 26). In Northern Africa, a few founder mutations have been linked to inherited breast cancer: c.5309G>T (p.Gly1770Val) reported in five unrelated Moroccan families (32) and c.5335delC (p.Gln1779Asnfs) reported in Egypt (33). In Sub-Saharan Africa, the most frequent founder mutations linked to inherited breast cancer are c.303T>G (p.Tyr101Ter), reported in 4 out of 434 patients in Nigeria (5); c.2641G>T (p.Glu881Ter), identified in 5 patients out of 90 in South Africa (4); and c.815_824dup, identified in 26 out of 46 Senegalese families (6). The high allelic frequency of the c.815_824dup variant (28.26%) combined with the common haplotype observed in patients bearing the mutation suggested a founder effect in West Africa. Studies from Nigeria and Burkina Faso have not reported the variant in inherited breast cancer cases (5, 34). Then, it is actually of interest to screen the variant in other West African countries, particularly those located along the coast such as Ghana, Guinea-Bissau, Benin, Ivory Coast, Guinea, Togo, Sierra Leone, Liberia, and The Gambia. It would also be of interest to screen other neighboring countries to Senegal, such as Mali and Burkina Faso, where slaves have been deported toward West African coasts. From these countries, three played a key role in the transatlantic slave trade during the 18th century. The Senegal, Ghana, and Benin borders served as departure ports of slaves from Africa to the US, the Caribbean, and Europe. Since the distribution of the BRCA1 c.815_824dup variant around the world overlapped black population migration, we have hypothesized that the variant first appeared in West Africa and spread out to the other continents (Figure 1). The high frequency of the variant among African Americans (18) and Hispanic people living in the Caribbean and Europe (13, 31), the African descent status of people harboring the variant through genomic databases, and the shorter single haplotype observed in Senegalese patients (6) all together support the African founding effect of c.815_824dup. The variant has spread out from Africa to other continents essentially through the transatlantic slave trade. Screening in other African countries may also highlight the implication of the transcontinental slave trade in the distribution of the variant across Africa.

FIGURE 1
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Figure 1 Distribution of the BRCA1 c.815_824dup variant through the transatlantic slave trade from West Africa to other continents.

BRCA1 mutations have also been involved in the occurrence of other cancers, including prostate and pancreatic cancer. The c.815_824dup variant has been associated with a risk up to 16% in prostate cancer and 1% in pancreatic cancer at age 70 years, according to clinical genetic testing reports from the Myriad Genetics Laboratories. Results from our study also showed, in two index case carriers, male relatives diagnosed with pancreatic/prostate cancer. Hence, it will be of interest to screen the mutation in Senegalese patients with these cancers in order to evaluate the burden of this mutation in the Senegalese population.

Founder mutations are useful for disease prevention since genetic testing can be targeted. In low-income settings, this will allow more rapid and less expensive testing and enable risk assessment and medical follow-up of people at risk. Studies focusing on a cohort of individuals with the same mutation will also be of interest to identify factors affecting penetrance, phenotype variability, or environmental risk modifiers for a better follow-up of affected individuals.

Author Contributions

JD, RN, AS, YD, SB, SM, CL, and PDS drafted the manuscript. DD, SK, BM, SG, PD, MN, PG, PLS, ADe, AC, and ADi gave advise on drafting the manuscript. All authors contributed to the article and approved the submitted version.

Funding

This research project was funded by the Ministry of Higher Education and Research of the Republic of Senegal through the 2015 FIRST program.

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.

Acknowledgments

We thank all families who agreed to participate in this study. We also thank the staff of the Joliot Curie Institute in Dakar, the Laboratory of Molecular Oncogenetics of the Paoli-Calmette Institute at Marseille, and the Senegalese Ministry of Higher Education and Research who funded the research project.

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Keywords: inherited breast cancer, BRCA1 gene, pathogenic variant, founder mutation, Africa

Citation: Diop JPD, Sène ARG, Dia Y, Ba SA, Mbacke SS, Ly CAT, Sarr PD, Diouf D, Ka S, Mbengue B, Gueye SMK, Diop PS, Sylla Niang M, Gueye PM, Lopez Sall P, Dem A, Cisse A, Dieye A and Ndiaye R (2022) New Insights Into c.815_824dup Pathogenic Variant of BRCA1 in Inherited Breast Cancer: A Founder Mutation of West African Origin. Front. Oncol. 11:810060. doi: 10.3389/fonc.2021.810060

Received: 05 November 2021; Accepted: 07 December 2021;
Published: 13 January 2022.

Edited by:

Hajo Zeeb, Leibniz Institute for Prevention Research and Epidemiology (LG), Germany

Reviewed by:

Fiona Baine-Savanhu, University of the Witwatersrand, South Africa

Copyright © 2022 Diop, Sène, Dia, Ba, Mbacke, Ly, Sarr, Diouf, Ka, Mbengue, Gueye, Diop, Sylla Niang, Gueye, Lopez Sall, Dem, Cisse, Dieye and Ndiaye. 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: Rokhaya Ndiaye, rokhaya9.ndiaye@ucad.edu.sn

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