Rapid evolution of BRCA1 and BRCA2in humans and other primates
Open accessAbstract
BACKGROUND: The maintenance of chromosomal integrity is an essential task of every living organism and cellular repair mechanisms exist to guard against insults to DNA. Given the importance of this process, it is expected that DNA repair proteins would be evolutionarily conserved, exhibiting very minimal sequence change over time. However, BRCA1, an essential gene involved in DNA repair, has been reported to be evolving rapidly despite the fact that many protein-altering mutations within this gene convey a significantly elevated risk for breast and ovarian cancers. RESULTS: To obtain a deeper understanding of the evolutionary trajectory of BRCA1, we analyzed complete BRCA1 gene sequences from 23 primate species. We show that specific amino acid sites have experienced repeated selection for amino acid replacement over primate evolution. This selection has been focused specifically on humans and our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). After examining BRCA1 polymorphisms in 7 bonobo, 44 chimpanzee, and 44 rhesus macaque (Macaca mulatta) individuals, we find considerable variation within each of these species and evidence for recent selection in chimpanzee populations. Finally, we also sequenced and analyzed BRCA2 from 24 primate species and find that this gene has also evolved under positive selection. CONCLUSIONS: While mutations leading to truncated forms of BRCA1 are clearly linked to cancer phenotypes in humans, there is also an underlying selective pressure in favor of amino acid-altering substitutions in this gene. A hypothesis where viruses are the drivers of this natural selection is discussed.
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Genes involved in cancer and apoptosis, including BRCA1 and BRCA2, are common targets of positive selection.
“Previous works reported that genes involved in cancer and apoptosis, including BRCA1 and BRCA2, are common targets of positive selection66, 67.”
From Distinct selective forces and Neanderthal introgression shaped genetic diversity at genes involved in neurodevelopmental disorders (2017) · cites this paper as [66]
The Conclusions (page unavailable) report recurrent positive selection in BRCA1 and BRCA2 during simian primate evolution. But the Discussion (page unavailable) describes their selection as surprising and says nearly all known recurrently selected primate genes fall into other categories. It does not support the claim that cancer- and apoptosis-related genes are common targets of positive selection. (LLM, conf=0.85)
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Clustal W and Clustal X version 2.0
Larkin, M., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., López, R., et al. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm404 · Cited by 28,221 · see citing works
PAML 4: Phylogenetic Analysis by Maximum Likelihood
Yang, Z. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm088 · Cited by 13,879 · see citing works
PAML: a program package for phylogenetic analysis by maximum likelihood
Yang, Z. (1997) · Computer applications in the biosciences · doi:10.1093/bioinformatics/13.5.555 · Cited by 5,344 · see citing works
Bayes Empirical Bayes Inference of Amino Acid Sites Under Positive Selection
Yang, Z. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi097 · Cited by 2,325 · see citing works
Codon-substitution models for heterogeneous selection pressure at amino acid sites
Yang, Z., Nielsen, R., Goldman, N., & Pedersen, A.-M. K. (2000) · Genetics · doi:10.1093/genetics/155.1.431 · Cited by 2,286 · see citing works
A codon-based model of nucleotide substitution for protein-coding DNA sequences.
(1994) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040153 · Cited by 1,960 · see citing works
Nielsen, R., & Yang, Z. (1998) · Genetics · doi:10.1093/genetics/148.3.929 · Cited by 1,622 · see citing works
Yang, Z. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025957 · Cited by 1,458 · see citing works
Yang, Z., & Nielsen, R. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004148 · Cited by 1,374 · see citing works
Hardy-Weinberg Equilibrium Testing of Biological Ascertainment for Mendelian Randomization Studies
Rodrı́guez, S., Gaunt, T. R., & Day, I. N. M. (2009) · American Journal of Epidemiology · doi:10.1093/aje/kwn359 · Cited by 1,050 · see citing works
Insights into DNA recombination from the structure of a RAD51–BRCA2 complex
Pellegrini, L., Yu, D. S., Lo, T., Anand, S., Lee, M., Blundell, T. L., & Venkitaraman, A. R. (2002) · Nature · doi:10.1038/nature01230 · Cited by 704 · see citing works
Sawyer, S. L., Wu, L. I., Emerman, M., & Malik, H. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409853102 · Cited by 688 · see citing works
Self-citationInferring Nonneutral Evolution from Human-Chimp-Mouse Orthologous Gene Trios
Clark, A. G., Glanowski, S., Nielsen, R., Thomas, P. D., Kejariwal, A., Todd, M. A., Tanenbaum, D. M., Civello, D., Lu, F., Murphy, B., et al. (2003) · Science · doi:10.1126/science.1088821 · Cited by 669 · see citing works
Wong, W. S. W., Yang, Z., Goldman, N., & Nielsen, R. (2004) · Genetics · doi:10.1534/genetics.104.031153 · Cited by 599 · see citing works
Wong, A. K. C., Pero, R. S., Ormonde, P. A., Tavtigian, S. V., & Bartel, P. L. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.51.31941 · Cited by 539 · see citing works
Ludwig, T. E., Chapman, D. L., Papaioannou, V. E., & Efstratiadis, A. (1997) · Genes & Development · doi:10.1101/gad.11.10.1226 · Cited by 539 · see citing works
Adenovirus oncoproteins inactivate the Mre11–Rad50–NBS1 DNA repair complex
Stracker, T. H., Carson, C. T., & Weitzman, M. D. (2002) · Nature · doi:10.1038/nature00863 · Cited by 522 · see citing works
Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G
Sawyer, S. L., Emerman, M., & Malik, H. S. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020275 · Cited by 485 · see citing works
Self-citationO'Donovan, P. J., & Livingston, D. M. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq069 · Cited by 296 · see citing works
Protein kinase R reveals an evolutionary model for defeating viral mimicry
Elde, N. C., Child, S. J., Geballe, A. P., & Malik, H. S. (2009) · Nature · doi:10.1038/nature07529 · Cited by 260 · see citing works
Lim, E. S., Fregoso, O. I., McCoy, C. O., Matsen, F. A., IV, Malik, H. S., & Emerman, M. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.01.004 · Cited by 260 · see citing works
A Role for DNA-PK in Retroviral DNA Integration
Daniel, R., Katz, R. A., & Skalka, A. M. (1999) · Science · doi:10.1126/science.284.5414.644 · Cited by 260 · see citing works
DNA repair proteins affect the lifecycle of herpes simplex virus 1
Lilley, C. E., Carson, C. T., Muotri, A. R., Gage, F. H., & Weitzman, M. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501916102 · Cited by 249 · see citing works
Positive selection on the human genome
Vallender, E. J. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh253 · Cited by 246 · see citing works
RAB22 and RAB163/mouse BRCA2: Proteins that specifically interact with the RAD51 protein
Mizuta, R., LaSalle, J. M., Cheng, H.-L., Shinohara, A., Ogawa, H., Copeland, N. G., Jenkins, N. A., Lalande, M., & Alt, F. W. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6927 · Cited by 235 · see citing works
Unraveling the mechanism of BRCA2 in homologous recombination
Holloman, W. K. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2096 · Cited by 220 · see citing works
Using or abusing: viruses and the cellular DNA damage response
Lilley, C. E., Schwartz, R. A., & Weitzman, M. D. (2007) · Trends in Microbiology · doi:10.1016/j.tim.2007.01.003 · Cited by 207 · see citing works
Antagonistic pleiotropy as a widespread mechanism for the maintenance of polymorphic disease alleles
Carter, A. J. R., & Nguyen, A. Q. (2011) · BMC Medical Genetics · doi:10.1186/1471-2350-12-160 · Cited by 176 · see citing works
Lees‐Miller, S. P., Long, M. C., Kilvert, M. A., Lam, V., Rice, S. A., & Spencer, C. A. (1996) · Journal of Virology · doi:10.1128/jvi.70.11.7471-7477.1996 · Cited by 176 · see citing works
Laguette, N., Rahm, N., Sobhian, B., Chable-Bessia, C., Münch, J., Snoeck, J., Sauter, D., Switzer, W. M., Heneine, W., Kirchhoff, F., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.01.007 · Cited by 172 · see citing works
Adaptive evolution of the tumour suppressor BRCA1 in humans and chimpanzees
Huttley, G. A., Easteal, S., Southey, M. C., Tesoriero, A. A., Giles, G. G., McCredie, M. R. E., Hopper, J. L., & Venter, D. J. (2000) · Nature Genetics · doi:10.1038/78092 · Cited by 169 · see citing works
BRCA1 Facilitates Microhomology-mediated End Joining of DNA Double Strand Breaks
Zhong, Q., Chen, C., Chen, P., & Lee, W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200748200 · Cited by 150 · see citing works
Common BRCA1 Variants and Susceptibility to Breast and Ovarian Cancer in the General Population
Dunning, A. M., Chiano, M. N., Smith, N. R., Dearden, J., Gore, M. E., Oakes, S., Wilson, C., Stratton, M., Peto, J., Easton, D. F., et al. (1997) · Human Molecular Genetics · doi:10.1093/hmg/6.2.285 · Cited by 138 · see citing works
Lim, E. S., Malik, H. S., & Emerman, M. (2010) · Journal of Virology · doi:10.1128/jvi.00468-10 · Cited by 134 · see citing works
Two-stepping through time: mammals and viruses
Meyerson, N. R., & Sawyer, S. L. (2011) · Trends in Microbiology · doi:10.1016/j.tim.2011.03.006 · Cited by 133 · see citing works
Self-citationUnderstanding missense mutations in the BRCA1 gene: An evolutionary approach
Fleming, M., Potter, J. D., Ramirez, C. J., Ostrander, G. K., & Ostrander, E. A. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0237285100 · Cited by 130 · see citing works
Lilley, C. E., Chaurushiya, M. S., Boutell, C., Everett, R. D., & Weitzman, M. D. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002084 · Cited by 124 · see citing works
Durocher, F. (1996) · Human Molecular Genetics · doi:10.1093/hmg/5.6.835 · Cited by 124 · see citing works
Viral manipulation of DNA repair and cell cycle checkpoints
Chaurushiya, M. S., & Weitzman, M. D. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.04.016 · Cited by 120 · see citing works
Zimmerman, E. S., Chen, J., Andersen, J. L., Ardon, O., DeHart, J. L., Blackett, J. L., Choudhary, S. K., Camerini, D., Nghiem, P., & Planelles, V. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.21.9286-9294.2004 · Cited by 119 · see citing works
Daniel, R., Greger, J., Katz, R. A., Taganov, K. D., Wu, X., Kappes, J. C., & Skalka, A. M. (2004) · Journal of Virology · doi:10.1128/jvi.78.16.8573-8581.2004 · Cited by 107 · see citing works
Evolution of the tumor suppressor BRCA1 locus in primates: implications for cancer predisposition
Pavlı́ček, A., Noskov, V. N., Kouprina, N., Barrett, J. C., Jurka, J., & Larionov, V. (2004) · Human Molecular Genetics · doi:10.1093/hmg/ddh301 · Cited by 99 · see citing works
Positive selection in the evolution of cancer
Crespi, B. J., & Summers, K. (2006) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793106007056 · Cited by 96 · see citing works
Rajendra, E., & Venkitaraman, A. R. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp873 · Cited by 90 · see citing works
Evidence for purifying selection acting on silent sites in BRCA1
Hurst, L. D., & Pál, C. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(00)02173-9 · Cited by 89 · see citing works
Suppression of retroviral infection by the RAD52 DNA repair protein
Lau, A., Kanaar, R., Jackson, S. P., & O’Connor, M. J. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600348 · Cited by 76 · see citing works
Sawyer, S. L., & Malik, H. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605468103 · Cited by 59 · see citing works
Self-citationHIV-1 Vpr induces ATM-dependent cellular signal with enhanced homologous recombination
Nakai-Murakami, C., Shimura, M., Kinomoto, M., Takizawa, Y., Tokunaga, K., Taguchi, T., Hoshino, S., Miyagawa, K., Sata, T., Kurumizaka, H., et al. (2006) · Oncogene · doi:10.1038/sj.onc.1209831 · Cited by 59 · see citing works
DNA Mismatch Repair Proteins Are Required for Efficient Herpes Simplex Virus 1 Replication
Mohni, K. N., Mastrocola, A. S., Bai, P., Weller, S. K., & Heinen, C. D. (2011) · Journal of Virology · doi:10.1128/jvi.05487-11 · Cited by 52 · see citing works
Effect of DNA Repair Protein Rad18 on Viral Infection
Lloyd, A. G., Tateishi, S., Bieniasz, P., Muesing, M., Yamaizumi, M., & Mulder, L. C. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020040 · Cited by 46 · see citing works
Cosnefroy, O., Tocco, A., Lesbats, P., Thierry, S., Calmels, C., Wiktorowicz, T., Reigadas, S., Kwon, Y., de Cian, A., Desfarges, S., et al. (2011) · Journal of Virology · doi:10.1128/jvi.05425-11 · Cited by 39 · see citing works
Ancient and Recent Adaptive Evolution of Primate Non-Homologous End Joining Genes
Demogines, A., East, A. M., Lee, J., Grossman, S. R., Sabeti, P. C., Paull, T. T., & Sawyer, S. L. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001169 · Cited by 36 · see citing works
Self-citationSmith, J. A., Wang, F., Zhang, H., Wu, K., Williams, K. J., & Daniel, R. (2008) · Virology Journal · doi:10.1186/1743-422x-5-11 · Cited by 32 · see citing works
Breast Cancer Predisposition Syndromes
Hemel, D., & Domchek, S. M. (2010) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2010.06.004 · Cited by 30 · see citing works
Burk, A., Scally, M., Amrine‐Madsen, H., Stanhope, M. J., & Springer, M. S. (2006) · Mammalian Genome · doi:10.1007/s00335-005-0067-2 · Cited by 25 · see citing works
O’Connell, M. J. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9399-y · Cited by 25 · see citing works
BRCA1 5382insC mutation in sporadic and familial breast and ovarian carcinoma in Scotland
Mullen, P., Miller, W., Mackay, J., FitzPatrick, D. R., Langdon, S., & Warner, J. P. (1997) · British Journal of Cancer · doi:10.1038/bjc.1997.233 · Cited by 13 · see citing works
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Smith, M. D., Wertheim, J. O., Weaver, S., Murrell, B., Scheffler, K., & Pond, S. L. K. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv022 · Cited by 815 · see citing works
Bhaskaran, S. P., Chandratre, K. R., Gupta, H., Zhang, L., Wang, X., Cui, J., Kim, Y. C., Sinha, S., Jiang, L., Lu, B., et al. (2019) · International Journal of Cancer · doi:10.1002/ijc.32176 · Cited by 102 · see citing works
Kim, Y. C., Zhao, L., Zhang, H., Huang, Y., Cui, J., Xiao, F., Downs, B. M., & Wang, S. M. (2016) · Oncotarget · doi:10.18632/oncotarget.7144 · Cited by 58 · see citing works
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Tromer, E. C., Snel, ., & Kops, G. J. P. L. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv140 · Cited by 50 · see citing works
MCPH1: a window into brain development and evolution
Pulvers, J. N. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00092 · Cited by 49 · see citing works
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Pfeffer, C. M., HO, B. N., & Singh, A. T. K. (2017) · Cancer Genomics & Proteomics · doi:10.21873/cgp.20040 · Cited by 46 · see citing works
Selective Pressures on Human Cancer Genes along the Evolution of Mammals
Vicens, A., & Posada, D. (2018) · Genes · doi:10.3390/genes9120582 · Cited by 43 · see citing works
Dumas, G., Malesys, S., & Bourgeron, T. (2021) · Genome Research · doi:10.1101/gr.262113.120 · Cited by 36 · see citing works
Deycmar, S., Gomes, B., Charo, J., Ceppi, M., & Cline, J. M. (2023) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-005514 · Cited by 37 · see citing works
Localizing and Classifying Adaptive Targets with Trend Filtered Regression
Mughal, M. R., & DeGiorgio, M. (2018) · Molecular Biology and Evolution · doi:10.1093/molbev/msy205 · Cited by 33 · see citing works
Viral Modulation of the DNA Damage Response and Innate Immunity: Two Sides of the Same Coin
Lopez, A., Doyle, R. N., Sandoval, C., Nisson, K., Yang, V. B., & Fregoso, O. I. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.167327 · Cited by 29 · see citing works
BRCA Mutations—The Achilles Heel of Breast, Ovarian and Other Epithelial Cancers
Loboda, A. P., Adonin, L., Zvereva, S. D., Pestov, N. B., Guschin, D. Y., Korneenko, T. V., Telegina, A. V., Kondratieva, O. K., Frolova, S. E., & Barlev, N. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24054982 · Cited by 30 · see citing works
Post-transcriptional Regulation of BRCA2 through Interactions with miR-19a and miR-19b
Mogilyansky, E., Clark, P., Quann, K., Zhou, H., Londin, E. R., Yi, J., & Rigoutsos, I. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00143 · Cited by 23 · see citing works
On the Mechanism of Hyperthermia-Induced BRCA2 Protein Degradation
van den Tempel, N., Zelensky, A. N., Odijk, H., Laffeber, C., Schmidt, C. K., Brandsma, I., Demmers, J., Krawczyk, P. M., & Kanaar, R. (2019) · Cancers · doi:10.3390/cancers11010097 · Cited by 24 · see citing works
Can postfertile life stages evolve as an anticancer mechanism?
Frédéric Thomas, A., Giraudeau, M., François Renaud, A., Újvári, B., Roche, B., Pujol, P., Michel Raymond, A., Lemaître, J., & Alvergne, A. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000565 · Cited by 21 · see citing works
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Li, J., Zhao, B., Huang, T., Qin, Z., & Wang, S. M. (2022) · Life Science Alliance · doi:10.26508/lsa.202101263 · Cited by 23 · see citing works
Wang, S. M. (2022) · Journal of the National Cancer Center · doi:10.1016/j.jncc.2022.12.001 · Cited by 23 · see citing works
Mozzi, A., Forni, D., Cagliani, R., Pozzoli, U., Clerici, M., & Sironi, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-06440-4 · Cited by 19 · see citing works
Functions of DNA damage machinery in the innate immune response to DNA virus infection
Trigg, B., & Ferguson, B. J. (2015) · Current Opinion in Virology · doi:10.1016/j.coviro.2015.08.001 · Cited by 21 · see citing works
The evolution of perennially enlarged breasts in women: a critical review and a novel hypothesis
Pawłowski, B., & Żelaźniewicz, A. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12778 · Cited by 21 · see citing works
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Judd, E. N., Gilchrist, A. R., Meyerson, N. R., & Sawyer, S. L. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-021-01783-z · Cited by 19 · see citing works
Self-citationHannan, F. A., Keogh, M. B., Taha, S., & Buainain, L. A. (2019) · Molecular Genetics & Genomic Medicine · doi:10.1002/mgg3.771 · Cited by 21 · see citing works
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Arnab, S. P., Amin, M. R., & DeGiorgio, M. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad157 · Cited by 18 · see citing works
Lee, S. H. (2021) · Viruses · doi:10.3390/v13122386 · Cited by 18 · see citing works
Inference of Evolutionary Forces Acting on Human Biological Pathways
Daub, J. T., Dupanloup, I., Robinson‐Rechavi, M., & Excoffier, L. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv083 · Cited by 16 · see citing works
Evolutionary adaptation revealed by comparative genome analysis of woolly mammoths and elephants
Smith, S. D., Kawash, J., Karaiskos, S., Biluck, I., & Grigoriev, A. (2017) · DNA Research · doi:10.1093/dnares/dsx007 · Cited by 17 · see citing works
A glycan shield on chimpanzee CD4 protects against infection by primate lentiviruses (HIV/SIV)
Warren, C. J., Meyerson, N. R., Stabell, A. C., Fattor, W. T., Wilkerson, G. K., & Sawyer, S. L. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1813909116 · Cited by 17 · see citing works
Self-citationBRCA1 and BRCA2 Variation in Taiwanese General Population and the Cancer Cohort
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Wang, H., Shu, L., Niu, N., Zhao, C., Lu, S., Li, Y., Wang, H., Liu, Y., Zou, T., Zou, J., et al. (2022) · PeerJ · doi:10.7717/peerj.13641 · Cited by 13 · see citing works
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Kou, S. H., Li, J., Tam, B., Lei, H., Zhao, B., Xiao, F., & Wang, S. M. (2023) · NAR Cancer · doi:10.1093/narcan/zcad025 · Cited by 11 · see citing works
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Huang, J., Zhong, Y., Makohon-Moore, A. P., White, T., Jasin, M., Norell, M. A., Wheeler, W. C., & Iacobuzio–Donahue, C. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110771 · Cited by 10 · see citing works
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Gu, L., Xia, C., Yang, S., & Yang, G. (2023) · BMC Genomics · doi:10.1186/s12864-023-09301-9 · Cited by 6 · see citing works
Onco-Breastomics: An Eco-Evo-Devo Holistic Approach
Neagu, A.-N., Whitham, D., Bruno, P. S., Arshad, A., Seymour, L., Morrissiey, H., Hukovic, A. I., & Darie, C. C. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25031628 · Cited by 6 · see citing works
Recurrent Duplication and Diversification of a Vital DNA Repair Gene Family Across Drosophila
Brand, C. L., Oliver, G. T., Farkas, I. Z., Buszczak, M., & Levine, M. T. (2024) · Molecular Biology and Evolution · doi:10.1093/molbev/msae113 · Cited by 5 · see citing works
An Analysis of Methylome Evolution in Primates
Sahm, A., Koch, P., Horvath, S., & Hoffmann, S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab189 · Cited by 5 · see citing works
Unique divergence of the breast cancer 2 (BRCA2) gene in Neanderthals
Michalak, P., & Kang, L. (2018) · Hereditas · doi:10.1186/s41065-018-0073-5 · Cited by 4 · see citing works
Oncogenic BRCA1,2 Mutations in the Human Lineage—A By-Product of Sexual Selection?
Korneenko, T. V., & Pestov, N. B. (2023) · Biomedicines · doi:10.3390/biomedicines12010022 · Cited by 4 · see citing works
Emam, M., Machado, J. P., & Antunes, A. (2020) · Genomics · doi:10.1016/j.ygeno.2020.08.020 · Cited by 4 · see citing works
Ruiz‐García, M., Castellanos, A., Kaston, F., Pinedo–Castro, M., & Shostell, J. M. (2024) · Genes · doi:10.3390/genes15121537 · Cited by 3 · see citing works
Nuku, a family of primate retrocopies derived from KU70
Rowley, P. A., Ellahi, A., Han, K., Patel, J. S., Leuven, J. T. V., & Sawyer, S. L. (2021) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkab163 · Cited by 3 · see citing works
Self-citationDumas, G., Malesys, S., & Bourgeron, T. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/658658 · Cited by 3 · see citing works
The patterns and spectrum of BRCA1 and BRCA2 mutations in Iranian breast and ovarian cancer patients
Forghani, S., Mirzaei, H. R., Rezvani, H., Forghani, A., Sabet, F. M., Hojjat, A., Malekzadeh, M., Akbari, A., & Tabarestani, S. (2025) · Familial Cancer · doi:10.1007/s10689-025-00459-7 · Cited by 2 · see citing works
He, J., Kou, S. H., Li, J., Ding, X., & Wang, S. M. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1408952 · Cited by 2 · see citing works
Detection of positive selection on depression-associated genes
Yang, S., Zheng, C., Xia, C., Kang, J., & Gu, L. (2025) · Heredity · doi:10.1038/s41437-025-00753-1 · Cited by 1 · see citing works
Huang, Y., Luo, M., Huang, J., Huang, S., Wei, L., Zhang, Y., & ZHANG, Z. (2020) · Iranian Journal of Public Health · doi:10.18502/ijph.v48i9.3025 · Cited by 1 · see citing works
DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · BMC Genomics · doi:10.1186/s12864-021-07983-7 · Cited by 1 · see citing works
Hemmer, L. W. (2018) · KU ScholarWorks (The University of Kansas) · Cited by 1 · see citing works
Statistical Methods in Population Genetics for Next-Generation Sequencing Data
Rothwell, R. (2016) · Deep Blue (University of Michigan)
Huang, J., Zhong, Y., Makohon-Moore, A. P., White, T., Jasin, M., Norell, M. A., Wheeler, W. C., & Iacobuzio–Donahue, C. A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.16.384677
Studies on Redox-proteins and Cytokines in inflammation and Cancer
Hossain, A. (2007) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Recent selection is a major force driving cancer evolutionPreprint
Gu, L., & Yang, G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.27.474305
Missing ethnic information in current BRCA variant databasesPreprint
Qin, Z., & Wang, S. M. (2020) · doi:10.22541/au.159493151.12172690
Swellam, M. M., Khalifa, M. K., Nageeb, A. M., Mahmoud, M. S., Hashim, M., Alshazly, A.-A. I. A., Mahfouz, M. E., Sobeih, M. E., & Arab, L. E. E. (2022) · Research Square · doi:10.21203/rs.3.rs-1443238/v1
Liu, K., Hu, L., Wang, S., Chen, X., Liu, Y., Zhao, S., Wang, H., Li, L., & Li, H. Z. (2023) · Molecular Biology Reports · doi:10.1007/s11033-023-08853-z
Additional file 1 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639884
Additional file 6 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639899
Additional file 2 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639887
Additional file 4 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639893
Additional file 5 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639896
Additional file 3 of DNA damage repair system in C57BL/6 J mice is evolutionarily stable
Wang, X., & Wang, S. M. (2021) · Figshare · doi:10.6084/m9.figshare.16639890
Fadel, Y. M., Khaled, M., Emam, M., Marzouk, N. H., Sobih, S. E., Abd-Elaty, H., Elrashedy, W. M., Mostafa, G., Eldeen, S. A., Bador, M., et al. (2024) · Journal of Molecular Evolution · doi:10.1007/s00239-024-10222-8
Decuadro, A., Sosa, M., García, F., Balemian, N., Montenegro, M. D. C., & Silvia Llambí, D. (2025) · Revista Científica de la Facultad de Ciencias Veterinarias · doi:10.52973/rcfcv-e35545
Li, J., Zhao, B., Qin, Z., Kou, S. H., Chian, J. S., Xiao, F., Lei, H., Andaluz, S., He, J., Sinha, S., et al. (2025) · Genes & Diseases · doi:10.1016/j.gendis.2025.101916
Additional file 5 of The adaptive evolution of cancer driver genes
Gu, L., Xia, C., Yang, S., & Yang, G. (2023) · Figshare · doi:10.6084/m9.figshare.22697094
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701975
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701969
Additional file 1 of The adaptive evolution of cancer driver genes
Gu, L., Xia, C., Yang, S., & Yang, G. (2023) · Figshare · doi:10.6084/m9.figshare.22697082
Additional file 2 of The adaptive evolution of cancer driver genes
Gu, L., Xia, C., Yang, S., & Yang, G. (2023) · Figshare · doi:10.6084/m9.figshare.22697085
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25547091
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25546945
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701978
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701966
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701972
Additional file 3 of The adaptive evolution of cancer driver genes
Gu, L., Xia, C., Yang, S., & Yang, G. (2023) · Figshare · doi:10.6084/m9.figshare.22697088
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701984
Zhao, B., Li, J., Sinha, S., Qin, Z., Kou, S. H., Xiao, F., Lei, H., Chen, T., Cao, W., Ding, X., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26701987
Detecting Positive Selection by Modeling Structure Within Images of Genetic Variation
Amin, M. R., Arnab, S. P., Khan, M., & DeGiorgio, M. (2026) · Genome Biology and Evolution · doi:10.1093/gbe/evag085
Jh, C., Kang, M.-L., Lin, C., Lo, Y.-H., Chen, Y.-J., Lee, H., Tanapima, V., Lin, C.-K., Lee, I., Satta, Y., et al. (2026) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2026.07.002
Ridgway, A. M., Lamelza, P., Lampson, M. A., & Levine, M. T. (2026) · Chromosome Research · doi:10.1007/s10577-026-09816-3
- Authors
- Lou, D. I., McBee, R. M., Le, U. Q., Stone, A. C., Wilkerson, G. K., Demogines, A. M., & Sawyer, S. L.
- Affiliations
- The University of Texas at Austin (US)
- Arizona State University (US)
- The University of Texas MD Anderson Cancer Center (US)
- Corresponding author
- Sawyer, Sara L
- Venue
- BMC Evolutionary Biology
- Published
- 2014-07-11
- Volume
- 14
- Issue
- 1
- Pages
- 155-155
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC4106182
- OpenAlex
- W2060886652
- Cited by
- 74
- References
- 57
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 9 · 2023: 13 · 2022: 7 · 2021: 10 · 2020: 6 · 2019: 6 · 2018: 4 · 2017: 3 · 2016: 3 · 2015: 5
- FWCI
- 2.40
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Evolutionary Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arizona State University Library Digital Repository (Arizona State University) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Burroughs Wellcome Fund
- National Institutes of Health (U42OD011197)
- National Cancer Institute (F30CA171715)
- National Institute of General Medical Sciences (R01GM093086)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › BRCA gene mutations in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- BRCA1, BRCA2, positive selection, primate evolution, DNA repair, amino acid substitutions, chimpanzees, bonobos, rhesus monkeys, cancer susceptibility, sequence variation
- MeSH terms
- Amino Acid Sequence, Animals, Breast Neoplasms, DNA Repair, Exons, Female, Humans, Models, Molecular, Molecular Sequence Data, Mutation, Ovarian Neoplasms, Polymorphism, Genetic, Primates, Selection, Genetic, Sequence Alignment, Evolution, Molecular, BRCA1 Protein, Genes, BRCA1, Genes, BRCA2, BRCA2 Protein
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