Concurrent nucleotide substitution mutations in the human genome are characterized by a significantly decreased transition/transversion ratio

Human Mutation

Volumn 36, Issue 3, 2015, Pages 333-341

  Zhu, Wenjuan ^a   Cooper, David N ^b   Zhao, Qiang ^c   Wang, Ye ^c   Liu, Ruihong ^c   Li, Qibin ^a   Férec, Claude ^d,e,f,g   Wang, Yiming ^c   Chen, Jian Min ^d,e,f  

^a BGI SHENZHEN   (China)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c SUN YAT SEN UNIVERSITY   (China)

^d INSERM   (France)

^e ETABLISSEMENT FRANÇAIS DU SANG   (France)

^f FACULTÉ DE MÉDECINE ET DES SCIENCES DE LA SANTÉ   (France)

^g CHU MORVAN   (France)

Author keywords

Multiple nucleotide substitutions; Spontaneous germline mutations; Translesion synthesis DNA polymerases

Indexed keywords

DNA POLYMERASE; NUCLEOTIDE;

ARTICLE; CHINESE; DNA SYNTHESIS; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; HUMAN GENOME; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; GENETICS; METABOLISM; POINT MUTATION;

EUKARYOTA;

GENETIC DISEASES, INBORN; GENOME, HUMAN; HUMANS; NUCLEOTIDES; POINT MUTATION;

EID: 84924577185     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22749     Document Type: Article

References (50)

1. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE, Kang HM, Marth GT, McVean GA. 2012. An integrated map of genetic variation from 1092 human genomes. Nature 491:56-65.
2. Amos W. 2013. Variation in heterozygosity predicts variation in human substitution rates between populations, individuals and genomic regions. PLoS One 8:e63048.
3. Averof M, Rokas A, Wolfe KH, Sharp PM. 2000. Evidence for a high frequency of simultaneous double-nucleotide substitutions. Science 287:1283-1286.
4. Buettner VL, Hill KA, Scaringe WA, Sommer SS. 2000. Evidence that proximal multiple mutations in Big Blue transgenic mice are dependent events. Mutat Res 452:219-229.
5. Burcham PC. 1999. Internal hazards: baseline DNA damage by endogenous products of normal metabolism. Mutat Res 443:11-36.
6. Callahan B, Neher RA, Bachtrog D, Andolfatto P, Shraiman BI. 2011. Correlated evolution of nearby residues in Drosophilid proteins. PLoS Genet 7:e1001315.
7. Campbell CD, Chong JX, Malig M, Ko A, Dumont BL, Han L, Vives L, O'Roak BJ, Sudmant PH, Shendure J, Abney M, Ober C, et al. 2012. Estimating the human mutation rate using autozygosity in a founder population. Nat Genet 44:1277-1281.
8. Campbell CD, Eichler EE. 2013. Properties and rates of germline mutations in humans. Trends Genet 29:575-584.
9. Chen JM, Cooper DN, Chuzhanova N, Férec C, Patrinos GP. 2007. Gene conversion: mechanisms, evolution and human disease. Nat Rev Genet 8:762-775.
10. Chen JM, Férec C, Cooper DN. 2009. Closely spaced multiple mutations as potential signatures of transient hypermutability in human genes. Hum Mutat 30:1435-1448.
11. Chen JM, Férec C, Cooper DN. 2013. Patterns and mutational signatures of tandem base substitutions causing human inherited disease. Hum Mutat 34:1119-1130.
12. Chen JM, Cooper DN, Férec C. 2014. A new and more accurate estimate of the rate of concurrent tandem-base substitution mutations in the human germline: ∼0.4% of the single nucleotide substitution mutation rate. Hum Mutat 35:392-394.
13. Chuzhanova N, Chen JM, Bacolla A, Patrinos GP, Férec C, Wells RD, Cooper DN. 2009. Gene conversion causing human inherited disease: evidence for involvement of non-B-DNA-forming sequences and recombination-promoting motifs in DNA breakage and repair. Hum Mutat 30:1189-1198.
14. Cooke MS, Evans MD, Dizdaroglu M, Lunec J. 2003. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17:1195-1214.
15. Cooper DN, Bacolla A, Férec C, Vasquez KM, Kehrer-Sawatzki H, Chen JM. 2011. On the sequence-directed nature of human gene mutation: the role of genomic architecture and the local DNA sequence environment in mediating gene mutations underlying human inherited disease. Hum Mutat 32:1075-1099.
16. Croteau DL, Bohr VA. 1997. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J Biol Chem 272:25409-25412.
17. Crow JF. 2000. The origins, patterns and implications of human spontaneous mutation. Nat Rev Genet 1:40-47.
18. Drake JW, Bebenek A, Kissling GE, Peddada S. 2005. Clusters of mutations from transient hypermutability. Proc Natl Acad Sci USA 102:12849-12854.
19. Drake JW. 2007. Too many mutants with multiple mutations. Crit Rev Biochem Mol Biol 42:247-258.
20. Fitch WM. 1980. Estimating the total number of nucleotide substitutions since the common ancestor of a pair of homologous genes: comparison of several methods and three beta hemoglobin messenger RNA's. J Mol Evol 16:153-209.
21. Giannoulatou E, McVean G, Taylor IB, McGowan SJ, Maher GJ, Iqbal Z, Pfeifer SP, Turner I, Burkitt Wright EM, Shorto J, Itani A, Turner K, et al. 2013. Contributions of intrinsic mutation rate and selfish selection to levels of de novo HRAS mutations in the paternal germline. Proc Natl Acad Sci USA 110:20152-20157.
22. Harris K, Nielsen R. 2014. Error-prone polymerase activity causes multinucleotide mutations in humans. Genome Res 24:1445-1454.
23. Hodgkinson A, Ladoukakis E, Eyre-Walker A. 2009. Cryptic variation in the human mutation rate. PLoS Biol 7:e1000027.
24. Hodgkinson A, Eyre-Walker A. 2010a. Human triallelic sites: evidence for a new mutational mechanism? Genetics 184:233-241.
25. Hodgkinson A, Eyre-Walker A. 2010b. The genomic distribution and local context of coincident SNPs in human and chimpanzee. Genome Biol Evol 2:547-557.
26. Hodgkinson A, Eyre-Walker A. 2011. Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12:756-766.
27. Jovelin R, Cutter AD. 2013. Fine-scale signatures of molecular evolution reconcile models of indel-associated mutation. Genome Biol Evol 5:978-986.
28. Kondrashov AS. 2003. Direct estimates of human per nucleotide mutation rates at 20 loci causing M endelian diseases. Hum Mutat 21:12-27.
29. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P, Magnusson G, Gudjonsson SA, Sigurdsson A, Jonasdottir A, Wong WS, Sigurdsson G, Walters GB, et al. 2012. Rate of de novo mutations and the importance of father's age to disease risk. Nature 488:471-475.
30. Kreutzer DA, Essigmann JM. 1998. Oxidized, deaminated cytosines are a source of C->T transitions in vivo. Proc Natl Acad Sci USA 95:3578-3582.
31. Lindahl T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709-715.
32. Loeb LA, Preston BD. 1986. Mutagenesis by apurinic/apyrimidinic sites. Annu Rev Genet 20:201-230.
33. Lynch M. 2010. Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci USA 107:961-968.
34. Markkanen E, van Loon B, Ferrari E, Parsons JL, Dianov GL, Hubscher U. 2012. Regulation of oxidative DNA damage repair by DNA polymerase lambda and MutYHby cross-talk of phosphorylation and ubiquitination. Proc Natl Acad Sci USA 109:437-442.
35. McCulloch SD, Kunkel TA. 2008. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 18:148-161.
36. McDonald MJ, Wang WC, Huang HD, Leu JY. 2011. Clusters of nucleotide substitutions and insertion/deletion mutations are associated with repeat sequences. PLoS Biol 9:e1000622.
37. Ninio J. 1991. Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics 129:957-962.
38. Obeid S, Welte W, Diederichs K, Marx A. 2012. Amino acid templating mechanisms in selection of nucleotides opposite abasic sites by a family a DNA polymerase. J Biol Chem 287:14099-14108.
39. Schrider DR, Hourmozdi JN, Hahn MW. 2011. Pervasive multinucleotide mutational events in eukaryotes. Curr Biol 21:1051-1054.
40. Seplyarskiy VB, Kharchenko P, Kondrashov AS, Bazykin GA. 2012. Heterogeneity of the transition/transversion ratio in Drosophila and Hominidae genomes. Mol Biol Evol 29:1943-1955.
41. Sharma S, Helchowski CM, Canman CE. 2013. The roles of DNA polymerase zeta and the Y family DNA polymerases in promoting or preventing genome instability. Mutat Res 743-744:97-110.
42. Smith NG, Webster MT, Ellegren H. 2003. A low rate of simultaneous double-nucleotide mutations in primates. Mol Biol Evol 20:47-53.
43. Stenson PD, Mort M, Ball EV, Shaw K, Phillips AD, Cooper DN. 2014. The Human Gene Mutation Database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine. Hum Genet 133:1-9.
44. Stone JE, Lujan SA, Kunkel TA. 2012. DNA polymerase zeta generates clustered mutations during bypass of endogenous DNA lesions in S accharomyces cerevisiae. Environ Mol Mutagen 53:777-786.
45. Sutton MD. 2010. Coordinating DNA polymerase traffic during high and low fidelity synthesis. Biochim Biophys Acta 1804:1167-1179.
46. Terekhanova NV, Bazykin GA, Neverov A, Kondrashov AS, Seplyarskiy VB. 2013. Prevalence of multinucleotide replacements in evolution of primates and Drosophila. Mol Biol Evol 30:1315-1325.
47. Tian D, Wang Q, Zhang P, Araki H, Yang S, Kreitman M, Nagylaki T, Hudson R, Bergelson J, Chen JQ. 2008. Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes. Nature 455:105-108.
48. Wang J, Gonzalez KD, Scaringe WA, Tsai K, Liu N, Gu D, Li W, Hill KA, Sommer SS. 2007. Evidence for mutation showers. Proc Natl Acad Sci USA 104:8403-8408.
49. Wang J, Wang W, Li R, Li Y, Tian G, Goodman L, Fan W, Zhang J, Li J, Guo Y, Feng B, Li H, et al. 2008. The diploid genome sequence of an Asian individual. Nature 456:60-65.
50. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. 2009. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 73:134-154.