Somatic point mutations occurring early in development: A monozygotic twin study

Journal of Medical Genetics

Volumn 51, Issue 1, 2014, Pages 28-34

  Li, Rui ^a,b   Montpetit, Alexandre ^a   Rousseau, Marylène ^a   Wu, Si Yu Margaret ^a   Greenwood, Celia M T ^a,b   Spector, Timothy D ^c   Pollak, Michael ^a   Polychronakos, Constantin ^a   Brent Richards, J ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DISEASE MARKER; GENE FREQUENCY; GENOME; GENOTYPE; HUMAN; LEUKOCYTE; MONOZYGOTIC TWINS; MOSAICISM; MUTATION RATE; POINT MUTATION; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION;

GENETIC DISCORDANCE; GENOME-WIDE GENOTYPING; MONOZYGOTIC TWINS; NEXT-GENERATION SEQUENCING; SOMATIC MUTATION;

GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION RATE; POINT MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; TWINS, MONOZYGOTIC;

EID: 84890857705     PISSN: 00222593     EISSN: 14686244     Source Type: Journal    
DOI: 10.1136/jmedgenet-2013-101712     Document Type: Article

References (49)

1. Nowell PC. The clonal evolution of tumor cell populations. Science 1976;194:23-8.
2. Erickson RP. Somatic gene mutation and human disease other than cancer: an update. Mutat Res 2010;705:96-106.
3. Vadlamudi L, Dibbens LM, Lawrence KM, Iona X, McMahon JM, Murrell W, Mackay-Sim A, Scheffer IE, Berkovic SF. Timing of de novo mutagenesis-a twin study of sodium-channel mutations. N Engl J Med 2010;363:1335-40.
4. Lindhurst MJ, Sapp JC, Teer JK, Johnston JJ, Finn EM, Peters K, Turner J, Cannons JL, Bick D, Blakemore L, Blumhorst C, Brockmann K, Calder P, Cherman N, DeardorffMA, Everman DB, Golas G, Greenstein RM, Kato BM, Keppler-Noreuil KM, Kuznetsov SA, Miyamoto RT, Newman K, Ng D, O'Brien K, Rothenberg S, Schwartzentruber DJ, Singhal V, Tirabosco R, Upton J, Wientroub S, Zackai EH, Hoag K, Whitewood-Neal T, Robey PG, Schwartzberg PL, Darling TN, Tosi LL, Mullikin JC, Biesecker LG. A mosaic activating mutation in AKT1 associated with the Proteus syndrome. N Engl J Med 2011;365:611-19.
5. Busque L, Patel JP, Figueroa ME, Vasanthakumar A, Provost S, Hamilou Z, Mollica L, Li J, Viale A, Heguy A, Hassimi M, Socci N, Bhatt PK, Gonen M, Mason CE, Melnick A, Godley LA, Brennan CW, Abdel-Wahab O, Levine RL. Recurrent somatic TET2 mutations in normal elderly individuals with clonal hematopoiesis. Nat Genet 2012;44:1179-81.
6. Araten DJ, Golde DW, Zhang RH, Thaler HT, Gargiulo L, Notaro R, Luzzatto L. A quantitative measurement of the human somatic mutation rate. Cancer Res 2005;65:8111-17.
7. Araten DJ, Luzzatto L. The mutation rate in PIG-A is normal in patients with paroxysmal nocturnal hemoglobinuria (PNH). Blood 2006;108:734-6.
8. Lichtenauer-Kaligis EG, Thijssen J, den Dulk H, van de Putte P, Tasseron-de Jong JG, Giphart-Gassler M. Comparison of spontaneous hprt mutation spectra at the nucleotide sequence level in the endogenous hprt gene and five other genomic positions. Mutat Res 1996;351:147-55.
9. Umar A, Risinger JI, Glaab WE, Tindall KR, Barrett JC, Kunkel TA. Functional overlap in mismatch repair by human MSH3 and MSH6. Genetics 1998;148:1637-46.
10. Glaab WE, Tindall KR. Mutation rate at the hprt locus in human cancer cell lines with specific mismatch repair-gene defects. Carcinogenesis 1997;18:1-8.
11. Iwama T. Somatic mutation rate of the APC gene. Jpn J Clin Oncol 2001;31:185-7.
12. Hornsby C, Page KM, Tomlinson I. The in vivo rate of somatic adenomatous polyposis coli mutation. Am J Pathol 2008;172:1062-8.
13. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, Yue P, Haverty PM, Bourgon R, Zheng J, Moorhead M, Chaudhuri S, Tomsho LP, Peters BA, Pujara K, Cordes S, Davis DP, Carlton VE, Yuan W, Li L, Wang W, Eigenbrot C, Kaminker JS, Eberhard DA, Waring P, Schuster SC, Modrusan Z, Zhang Z, Stokoe D, de Sauvage FJ, Faham M, Seshagiri S. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 2010;466:869-73.
14. Peifer M, Fernandez-Cuesta L, Sos ML, George J, Seidel D, Kasper LH, Plenker D, Leenders F, Sun R, Zander T, Menon R, Koker M, Dahmen I, Muller C, Di Cerbo V, Schildhaus HU, Altmuller J, Baessmann I, Becker C, de Wilde B, Vandesompele J, Bohm D, Ansen S, Gabler F, Wilkening I, Heynck S, Heuckmann JM, Lu X, Carter SL, Cibulskis K, Banerji S, Getz G, Park KS, Rauh D, Grutter C, Fischer M, Pasqualucci L, Wright G, Wainer Z, Russell P, Petersen I, Chen Y, Stoelben E, Ludwig C, Schnabel P, Hoffmann H, Muley T, Brockmann M, Engel-Riedel W, Muscarella LA, Fazio VM, Groen H, Timens W, Sietsma H, Thunnissen E, Smit E, Heideman DA, Snijders PJ, Cappuzzo F, Ligorio C, Damiani S, Field J, Solberg S, Brustugun OT, Lund-Iversen M, Sanger J, Clement JH, Soltermann A, Moch H, Weder W, Solomon B, Soria JC, Validire P, Besse B, Brambilla E, Brambilla C, Lantuejoul S, Lorimier P, Schneider PM, Hallek M, Pao W, Meyerson M, Sage J, Shendure J, Schneider R, Buttner R, Wolf J, Nurnberg P, Perner S, Heukamp LC, Brindle PK, Haas S, Thomas RK. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet 2012;44:1104-10.
15. Imielinski M, Berger AH, Hammerman PS, Hernandez B, Pugh TJ, Hodis E, Cho J, Suh J, Capelletti M, Sivachenko A, Sougnez C, Auclair D, Lawrence MS, Stojanov P, Cibulskis K, Choi K, de Waal L, Sharifnia T, Brooks A, Greulich H, Banerji S, Zander T, Seidel D, Leenders F, Ansen S, Ludwig C, Engel-Riedel W, Stoelben E, Wolf J, Goparju C, Thompson K, Winckler W, Kwiatkowski D, Johnson BE, Janne PA, Miller VA, Pao W, Travis WD, Pass HI, Gabriel SB, Lander ES, Thomas RK, Garraway LA, Getz G, Meyerson M. Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing. Cell 2012;150:1107-20.
16. Lee W, Jiang Z, Liu J, Haverty PM, Guan Y, Stinson J, Yue P, Zhang Y, Pant KP, Bhatt D, Ha C, Johnson S, Kennemer MI, Mohan S, Nazarenko I, Watanabe C, Sparks AB, Shames DS, Gentleman R, de Sauvage FJ, Stern H, Pandita A, Ballinger DG, Drmanac R, Modrusan Z, Seshagiri S, Zhang Z. The mutation spectrum revealed by paired genome sequences from a lung cancer patient. Nature 2010;465:473-7.
17. Forsberg LA, Rasi C, Razzaghian HR, Pakalapati G, Waite L, Thilbeault KS, Ronowicz A, Wineinger NE, Tiwari HK, Boomsma D, Westerman MP, Harris JR, Lyle R, Essand M, Eriksson F, Assimes TL, Iribarren C, Strachan E, O'Hanlon TP, Rider LG, Miller FW, Giedraitis V, Lannfelt L, Ingelsson M, Piotrowski A, Pedersen NL, Absher D, Dumanski JP. Age-related somatic structural changes in the nuclear genome of human blood cells. Am J Hum Genet 2012;90:217-28.
18. Laurie CC, Laurie CA, Rice K, Doheny KF, Zelnick LR, McHugh CP, Ling H, Hetrick KN, Pugh EW, Amos C, Wei Q, Wang LE, Lee JE, Barnes KC, Hansel NN, Mathias R, Daley D, Beaty TH, Scott AF, Ruczinski I, Scharpf RB, Bierut LJ, Hartz SM, Landi MT, Freedman ND, Goldin LR, Ginsburg D, Li J, Desch KC, Strom SS, Blot WJ, Signorello LB, Ingles SA, Chanock SJ, Berndt SI, Le Marchand L, Henderson BE, Monroe KR, Heit JA, de Andrade M, Armasu SM, Regnier C, Lowe WL, Hayes MG, Marazita ML, Feingold E, Murray JC, Melbye M, Feenstra B, Kang JH, Wiggs JL, Jarvik GP, McDavid AN, Seshan VE, Mirel DB, Crenshaw A, Sharopova N, Wise A, Shen J, Crosslin DR, Levine DM, Zheng X, Udren JI, Bennett S, Nelson SC, Gogarten SM, Conomos MP, Heagerty P, Manolio T, Pasquale LR, Haiman CA, Caporaso N, Weir BS. Detectable clonal mosaicism from birth to old age and its relationship to cancer. Nature genetics 2012;44:642-50.
19. Jacobs KB, Yeager M, Zhou W, Wacholder S, Wang Z, Rodriguez-Santiago B, Hutchinson A, Deng X, Liu C, Horner MJ, Cullen M, Epstein CG, Burdett L, Dean MC, Chatterjee N, Sampson J, Chung CC, Kovaks J, Gapstur SM, Stevens VL, Teras LT, Gaudet MM, Albanes D, Weinstein SJ, Virtamo J, Taylor PR, Freedman ND, Abnet CC, Goldstein AM, Hu N, Yu K, Yuan JM, Liao L, Ding T, Qiao YL, Gao YT, Koh WP, Xiang YB, Tang ZZ, Fan JH, Aldrich MC, Amos C, Blot WJ, Bock CH, Gillanders EM, Harris CC, Haiman CA, Henderson BE, Kolonel LN, Le Marchand L, McNeill LH, Rybicki BA, Schwartz AG, Signorello LB, Spitz MR, Wiencke JK, Wrensch M, Wu X, Zanetti KA, Ziegler RG, Figueroa JD, Garcia-Closas M, Malats N, Marenne G, Prokunina-Olsson L, Baris D, Schwenn M, Johnson A, Landi MT, Goldin L, Consonni D, Bertazzi PA, Rotunno M, Rajaraman P, Andersson U, Beane Freeman LE, Berg CD, Buring JE, Butler MA, Carreon T, Feychting M, Ahlbom A, Gaziano JM, Giles GG, Hallmans G, Hankinson SE, Hartge P, Henriksson R, Inskip PD, Johansen C, Landgren A, McKean-Cowdin R, Michaud DS, Melin BS, Peters U, Ruder AM, Sesso HD, Severi G, Shu XO, Visvanathan K, White E, Wolk A, Zeleniuch-Jacquotte A, Zheng W, Silverman DT, Kogevinas M, Gonzalez JR, Villa O, Li D, Duell EJ, Risch HA, Olson SH, Kooperberg C, Wolpin BM, Jiao L, Hassan M, Wheeler W, Arslan AA, Bueno-de-Mesquita HB, Fuchs CS, Gallinger S, Gross MD, Holly EA, Klein AP, LaCroix A, Mandelson MT, Petersen G, Boutron-Ruault MC, Bracci PM, Canzian F, Chang K, Cotterchio M, Giovannucci EL, Goggins M, Hoffman Bolton JA, Jenab M, Khaw KT, Krogh V, Kurtz RC, McWilliams RR, Mendelsohn JB, Rabe KG, Riboli E, Tjonneland A, Tobias GS, Trichopoulos D, Elena JW, Yu H, Amundadottir L, Stolzenberg-Solomon RZ, Kraft P, Schumacher F, Stram D, Savage SA, Mirabello L, Andrulis IL, Wunder JS, Patino Garcia A, Sierrasesumaga L, Barkauskas DA, Gorlick RG, Purdue M, Chow WH, Moore LE, Schwartz KL, Davis FG, Hsing AW, Berndt SI, Black A, Wentzensen N, Brinton LA, Lissowska J, Peplonska B, McGlynn KA, Cook MB, Graubard BI, Kratz CP, Greene MH, Erickson RL, Hunter DJ, Thomas G, Hoover RN, Real FX, Fraumeni JF Jr, Caporaso NE, Tucker M, Rothman N, Perez-Jurado LA, Chanock SJ. Detectable clonal mosaicism and its relationship to aging and cancer. Nat Genet 2012;44:651-8.
20. Frank SA. Evolution in health and medicine Sackler colloquium: Somatic evolutionary genomics: mutations during development cause highly variable genetic mosaicism with risk of cancer and neurodegeneration. Proc Natl Acad Sci USA 2010;107(Suppl 1):1725-30.
21. Cairns J. Mutation selection and the natural history of cancer. Nature 1975;255:197-200.
22. Aretz S, Stienen D, Friedrichs N, Stemmler S, Uhlhaas S, Rahner N, Propping P, Friedl W. Somatic APC mosaicism: a frequent cause of familial adenomatous polyposis (FAP). Hum Mutat 2007;28:985-92.
23. Hes FJ, Nielsen M, Bik EC, Konvalinka D, Wijnen JT, Bakker E, Vasen HF, Breuning MH, Tops CM. Somatic APC mosaicism: an underestimated cause of polyposis coli. Gut 2008;57:71-6.
24. Rohlin A, Wernersson J, Engwall Y, Wiklund L, Bjork J, Nordling M. Parallel sequencing used in detection of mosaic mutations: comparison with four diagnostic DNA screening techniques. Hum Mutat 2009;30:1012-20.
25. Finishing the euchromatic sequence of the human genome. Nature 2004;431:931-45.
26. Ndegwa N, Cote RG, Ovelleiro D, D'Eustachio P, Hermjakob H, Vizcaino JA, Croft D. Critical amino acid residues in proteins: a BioMart integration of Reactome protein annotations with PRIDE mass spectrometry data and COSMIC somatic mutations. Database: J Biolo Databases Curation 2011;2011:bar047.
27. Ding L, Getz G, Wheeler DA, Mardis ER, McLellan MD, Cibulskis K, Sougnez C, Greulich H, Muzny DM, Morgan MB, Fulton L, Fulton RS, Zhang Q, Wendl MC, Lawrence MS, Larson DE, Chen K, Dooling DJ, Sabo A, Hawes AC, Shen H, Jhangiani SN, Lewis LR, Hall O, Zhu Y, Mathew T, Ren Y, Yao J, Scherer SE, Clerc K, Metcalf GA, Ng B, Milosavljevic A, Gonzalez-Garay ML, Osborne JR, Meyer R, Shi X, Tang Y, Koboldt DC, Lin L, Abbott R, Miner TL, Pohl C, Fewell G, Haipek C, Schmidt H, Dunford-Shore BH, Kraja A, Crosby SD, Sawyer CS, Vickery T, Sander S, Robinson J, Winckler W, Baldwin J, Chirieac LR, Dutt A, Fennell T, Hanna M, Johnson BE, Onofrio RC, Thomas RK, Tonon G, Weir BA, Zhao X, Ziaugra L, Zody MC, Giordano T, Orringer MB, Roth JA, Spitz MR, Wistuba II, Ozenberger B, Good PJ, Chang AC, Beer DG, Watson MA, Ladanyi M, Broderick S, Yoshizawa A, Travis WD, Pao W, Province MA, Weinstock GM, Varmus HE, Gabriel SB, Lander ES, Gibbs RA, Meyerson M, Wilson RK. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 2008;455:1069-75.
28. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, Lilenbaum R, Johnson DH. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006;355:2542-50.
29. Stephens P, Hunter C, Bignell G, Edkins S, Davies H, Teague J, Stevens C, O'Meara S, Smith R, Parker A, Barthorpe A, Blow M, Brackenbury L, Butler A, Clarke O, Cole J, Dicks E, Dike A, Drozd A, Edwards K, Forbes S, Foster R, Gray K, Greenman C, Halliday K, Hills K, Kosmidou V, Lugg R, Menzies A, Perry J, Petty R, Raine K, Ratford L, Shepherd R, Small A, Stephens Y, Tofts C, Varian J, West S, Widaa S, Yates A, Brasseur F, Cooper CS, Flanagan AM, Knowles M, Leung SY, Louis DN, Looijenga LH, Malkowicz B, Pierotti MA, Teh B, Chenevix-Trench G, Weber BL, Yuen ST, Harris G, Goldstraw P, Nicholson AG, Futreal PA, Wooster R, Stratton MR. Lung cancer: intragenic ERBB2 kinase mutations in tumours. Nature 2004;431:525-6.
30. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, Slamon DJ, Murphy M, Novotny WF, Burchmore M, Shak S, Stewart SJ, Press M. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 2002;20:719-26.
31. Happle R. The McCune-Albright syndrome: a lethal gene surviving by mosaicism. Clin Genet 1986;29:321-4.
32. Waisfisz Q, Morgan NV, Savino M, de Winter JP, van Berkel CG, Hoatlin ME, Ianzano L, Gibson RA, Arwert F, Savoia A, Mathew CG, Pronk JC, Joenje H. Spontaneous functional correction of homozygous fanconi anaemia alleles reveals novel mechanistic basis for reverse mosaicism. Nat Genet 1999;22:379-83.
33. Kvittingen EA, Rootwelt H, Brandtzaeg P, Bergan A, Berger R. Hereditary tyrosinemia type I. Self-induced correction of the fumarylacetoacetase defect. J Clin Invest 1993;91:1816-21.
34. Ellis NA, Lennon DJ, Proytcheva M, AlhadeffB, Henderson EE, German J. Somatic intragenic recombination within the mutated locus BLM can correct the high sister-chromatid exchange phenotype of Bloom syndrome cells. Am J Hum Genet 1995;57:1019-27.
35. Stephan JL, Vlekova V, Le Deist F, Blanche S, Donadieu J, De Saint-Basile G, Durandy A, Griscelli C, Fischer A. Severe combined immunodeficiency: a retrospective single-center study of clinical presentation and outcome in 117 patients. J Pediatr 1993;123:564-72.
36. Jonkman MF, Scheffer H, Stulp R, Pas HH, Nijenhuis M, Heeres K, Owaribe K, Pulkkinen L, Uitto J. Revertant mosaicism in epidermolysis bullosa caused by mitotic gene conversion. Cell 1997;88:543-51.
37. Bruder CE, Piotrowski A, Gijsbers AA, Andersson R, Erickson S, Diaz De Stahl T, Menzel U, Sandgren J, von Tell D, Poplawski A, Crowley M, Crasto C, Partridge EC, Tiwari H, Allison DB, Komorowski J, van Ommen GJ, Boomsma DI, Pedersen NL, den Dunnen JT, Wirdefeldt K, Dumanski JP. Phenotypically concordant and discordant monozygotic twins display different DNA copy-number-variation profiles. Am J Hum Genet 2008;82:763-71.
38. Razzaghian HR, Shahi MH, Forsberg LA, de Stahl TD, Absher D, Dahl N, Westerman MP, Dumanski JP. Somatic mosaicism for chromosome X and Y aneuploidies in monozygotic twins heterozygous for sickle cell disease mutation. Am J Med Genet 2010;152A:2595-8.
39. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aguilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 2005;102:10604-9.
40. Lynch M. Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci USA 2010;107:961-8.
41. Conrad DF, Keebler JE, DePristo MA, Lindsay SJ, Zhang Y, Casals F, Idaghdour Y, Hartl CL, Torroja C, Garimella KV, Zilversmit M, Cartwright R, Rouleau GA, Daly M, Stone EA, Hurles ME, Awadalla P. Variation in genome-wide mutation rates within and between human families. Nat Genet 2011;43:712-14.
42. Wasserstrom A, Frumkin D, Adar R, Itzkovitz S, Stern T, Kaplan S, Shefer G, Shur I, Zangi L, Reizel Y, Harmelin A, Dor Y, Dekel N, Reisner Y, Benayahu D, Tzahor E, Segal E, Shapiro E. Estimating cell depth from somatic mutations. PLoS Comput Biol 2008;4:e1000058.
43. Messer PW. Measuring the rates of spontaneous mutation from deep and large-scale polymorphism data. Genetics 2009;182:1219-32.
44. Moayyeri A, Hammond CJ, Valdes AM, Spector TD. Cohort Profile: TwinsUK and Healthy Ageing Twin Study. Int J Epidemiol 2013;42:76-85.
45. Andrew T, Hart DJ, Snieder H, de Lange M, Spector TD, MacGregor AJ. Are twins and singletons comparable? A study of disease-related and lifestyle characteristics in adult women. Twin Res 2001;4:464-77.
46. Teo YY, Inouye M, Small KS, Gwilliam R, Deloukas P, Kwiatkowski DP, Clark TG. A genotype calling algorithm for the Illumina BeadArray platform. Bioinformatics 2007;23:2741-6.
47. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009;25:1754-60.
48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009;25:2078-9.
49. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010;20:1297-303.