Deep sequencing to reveal new variants in pooled DNA samples

Human Mutation

Volumn 30, Issue 12, 2009, Pages 1703-1712

  Out, Astrid A ^a   Van Minderhout, Ivonne J H M ^a   Goeman, Jelle J ^a   Ariyurek, Yavuz ^a   Ossowski, Stephan ^b   Schneeberger, Korbinian ^b   Weigel, Detlef ^b   Van Galen, Michiel ^a   Taschner, Peter E M ^a   Tops, Carli M J ^a   Breuning, Martijn H ^a   Van Ommen, Gert Jan B ^a   Den Dunnen, Johan T ^a   Devilee, Peter ^a   Hes, Frederik J ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

Association study; Illumina sequencing; MUTYH; PCR; Pooling

Indexed keywords

GENOMIC DNA;

ARTICLE; BIOINFORMATICS; BREAST CANCER; CANCER PATIENT; CONTROLLED STUDY; DNA SEQUENCE; EXON; FEMALE; FLUOROMETRY; GENE; GENE AMPLIFICATION; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC VARIABILITY; GENOMICS; HUMAN; MAJOR CLINICAL STUDY; MUTYH GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RELIABILITY;

ALLELES; DNA; GENE FREQUENCY; GENETIC VARIATION; GENOME, HUMAN; HUMANS; NUCLEIC ACID DENATURATION; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA;

EID: 71749099456     PISSN: 10597794     EISSN: None     Source Type: Journal    
DOI: 10.1002/humu.21122     Document Type: Article

References (45)

1. Albert TJ, Molla MN, Muzny DM, Nazareth L, Wheeler D, Song X, Richmond TA, Middle CM, Rodesch MJ, Packard CJ, Weinstock GM, Gibbs RA. 2007. Direct selection of human genomic loci by microarray hybridization. Nat Methods 4:903-905. (Pubitemid 350042375)
2. Aretz S, Uhlhaas S, Goergens H, Siberg K, Vogel M, Pagenstecher C, Mangold E, Caspari R, Propping P, Friedl W. 2006. MUTYH-associated polyposis: 70 of 71 patients with biallelic mutations present with an attenuated or atypical phenotype. Int J Cancer 119:807-814. (Pubitemid 44051443)
3. Bau S, Schracke N, Kränzle M, Wu H, Stähler PF, Hoheisel JD, Beier M, Summerer D. 2009. Targeted next-generation sequencing by specific capture of multiple genomic loci using low-volume microfluidic DNA arrays. Anal Bioanal Chem 393:171-175. (Pubitemid 50316505)
4. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Cheetham RK, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu X, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, Rasolonjatovo IM, Reed MT, Rigatti R, Rodighiero C, Ross MT, Sabot A, Sankar SV, Scally A, Schroth GP, Smith ME, Smith VP, Spiridou A, Torrance PE, Tzonev SS, Vermaas EH, Walter K, Wu X, Zhang L, Alam MD, Anastasi C, Aniebo IC, Bailey DM, Bancarz IR, Banerjee S, Barbour SG, Baybayan PA, Benoit VA, Benson KF, Bevis C, Black PJ, Boodhun A, Brennan JS, Bridgham JA, Brown RC, Brown AA, Buermann DH, Bundu AA, Burrows JC, Carter NP, Castillo N, Catenazzi MCE, Chang S, Cooley RN, Crake NR, Dada OO, Diakoumakos KD, Dominguez-Fernandez B, Earnshaw DJ, Egbujor UC, Elmore DW, Etchin SS, Ewan MR, Fedurco M, Fraser LJ, Fuentes Fajardo KV, Furey WS, George D, Gietzen KJ, Goddard CP, Golda GS, Granieri PA, Green DE, Gustafson DL, Hansen NF, Harnish K, Haudenschild CD, Heyer NI, Hims MM, Ho JT, Horgan AM, Hoschler K, Hurwitz S, Ivanov DV, Johnson MQ, James T, Jones TAH, Kang GD, Kerelska TH, Kersey AD, Khrebtukova I, Kindwall AP, Kingsbury Z, Kokko-Gonzales PI, Kumar A, Laurent MA, Lawley CT, Lee SE, Lee X, Liao AK, Loch JA, Lok M, Luo S, Mammen RM, Martin JW, McCauley PG, McNitt P, Mehta P, Moon KW, Mullens JW, Newington T, Ning Z, Ling NB, Novo SM, O'Neill MJ, Osborne MA, Osnowski A, Ostadan O, Paraschos LL, Pickering L, Pike AC, Pike AC, Chris PD, Pliskin DP, Podhasky J, Quijano VJ, Raczy C, Rae VH, Rawlings SR, Chiva Rodriguez A, Roe PM, Rogers J, Rogert Bacigalupo MC, Romanov N, Romieu A, Roth RK, Rourke NJ, Ruediger ST, Rusman E, Sanches-Kuiper RM, Schenker MR, Seoane JM, Shaw RJ, Shiver MK, Short SW, Sizto NL, Sluis JP, Smith MA, Sohna JE, Spence EJ, Stevens K, Sutton N, Szajkowski L, Tregidgo CL, Turcatti G, Vandevondele S, Verhovsky Y, Virk SM, Wakelin S, Walcott GC, Wang J, Worsley GJ, Yan J, Yau L, Zuerlein M, Rogers J, Mullikin JC, Hurles ME, McCooke NJ, West JS, Oaks FL, Lundberg PL, Klenerman D, Durbin R, Smith AJ. 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456:53-59.
5. Bodmer W, Bonilla C. 2008. Common and rare variants in multifactorial susceptibility to common diseases. Nat Genet 40:695-701. (Pubitemid 351748875)
6. Campbell PJ, Pleasance ED, Stephens PJ, Dicks E, Rance R, Goodhead I, Follows GA, Green AR, Futreal PA, Stratton MR. 2008. Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc Natl Acad Sci USA 105:13081-13086.
7. Cheadle JP, Sampson JR. 2007. MUTYH-associated polyposis-from defect in base excision repair to clinical genetic testing. DNA Repair (Amst) 6:274-279.
8. Cleary SP, Cotterchio M, Jenkins MA, Kim H, Bristow R, Green R, Haile R, Hopper JL, LeMarchand L, Lindor N, Parfrey P, Potter J, Younghusband B, Gallinger S. 2009. Germline MutY human homologue mutations and colorectal cancer: a multisite case-control study. Gastroenterology 136:1251-1260.
9. Database of Single Nucleotide Polymorphisms (dbSNP). Bethesda, MD: National Center for Biotechnology Information, National Library of Medicine (dbSNP Build ID: 129). Available at: www.ncbi.nlm.nih.gov/projects/SNP. Accessed 27 August 2009.
10. den Dunnen JT, Antonarakis SE. 2000. Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion. Hum Mutat 15:7-12.
11. den Dunnen JT, Paalman MH. 2003. Standardizing mutation nomenclature: why bother? Hum Mutat 22:181-182.
12. Dohm JC, Lottaz C, Borodina T, Himmelbauer H. 2008. Substantial biases in ultrashort read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36:e105.
13. Druley TE, Vallania FL, Wegner DJ, Varley KE, Knowles OL, Bonds JA, Robison SW, Doniger SW, Hamvas A, Cole FS, Fay JC, Mitra RD. 2009. Quantification of rare allelic variants from pooled genomic DNA. Nat Methods 6:263-265.
14. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, Dewinter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323:133-138.
15. Goossens D, Moens LN, Nelis E, Lenaerts AS, Glassee W, Kalbe A, Frey B, Kopal G, De Jonghe P, De RP, Del-Favero J. 2009. Simultaneous mutation and copy number variation (CNV) detection by multiplex PCR-based GS-FLX sequencing. Hum Mutat 30:472-476.
16. Grantham R. 1974. Amino acid difference formula to help explain protein evolution. Science 185:862-864.
17. Harismendy O, Frazer K. 2009. Method for improving sequence coverage uniformity of targeted genomic intervals amplified by LR-PCR using Illumina GA sequencing-by-synthesis technology. Biotechniques 46:229-231.
18. Hoggart CJ, Clark TG, De Iorio M, Whittaker JC, Balding DJ. 2008. Genome-wide significance for dense SNP and resequencing data. Genet Epidemiol 32:179-185. (Pubitemid 351288034)
19. Houlston RS, Peto J. 2004. The search for low-penetrance cancer susceptibility alleles. Oncogene 23:6471-6476. (Pubitemid 39265510)
20. Huijts PE, Vreeswijk MP, Kroeze-Jansema KH, Jacobi CE, Seynaeve C, Krol-Warmerdam EM, Wijers-Koster PM, Blom JC, Pooley KA, Klijn JG, Tollenaar RA, Devilee P, van Asperen CJ. 2007. Clinical correlates of low-risk variants in FGFR2, TNRC9, MAP3K1, LSP1 and 8q24 in a Dutch cohort of incident breast cancer cases. Breast Cancer Res 9:R78.
21. Ingman M, Gyllensten U. 2009. SNP frequency estimation using massively parallel sequencing of pooled DNA. Eur J Hum Genet 17:383-386.
22. Kaiser J. 2008. DNA sequencing. A plan to capture human diversity in 1000 genomes. Science 319:395.
23. Küry S, Buecher B, Robiou-du-Pont S, Scoul C, Colman H, Lelièvre B, Olschwang S, Le Houérou C, Le Neel N, Faroux R, Ollivry J, Lafraise B, Chupin LD, Bèzieau S. 2007. The thorough screening of the MUTYH gene in a large French cohort of sporadic colorectal cancers. Genet Test 11:373-379.
24. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25.
25. Mathe E, Olivier M, Kato S, Ishioka C, Hainaut P, Tavtigian SV. 2006. Computational approaches for predicting the biological effect of p53 missense mutations: a comparison of three sequence analysis based methods. Nucleic Acids Res 34:1317-1325.
26. Meyer M, Stenzel U, Hofreiter M. 2008. Parallel tagged sequencing on the 454 platform. Nat Protoc 3:267-278. (Pubitemid 351266511)
27. Miller SA, Dykes DD, Polesky HF. 1988. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215.
28. Nielsen M, Franken PF, Reinards TH, Weiss MM, Wagner A, van der Klift H, Kloosterman S, Houwing-Duistermaat JJ, Aalfs CM, Ausems MG, Brocker-Vriends AH, Gomez Garcia EB, Hoogerbrugge N, Menko FH, Sijmons RH, Verhoef S, Kuipers EJ, Morreau H, Breuning MH, Tops CM, Wijnen JT, Vasen HF, Fodde R, Hes FJ. 2005. Multiplicity in polyp count and extracolonic manifestations in 40 Dutch patients with MYH associated polyposis coli (MAP). J Med Genet 42:e54.
29. Notredame C, Higgins DG, Heringa J. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-217. (Pubitemid 30694431)
30. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D. 2008. Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 18:2024-2033.
31. Parameswaran P, Jalili R, Tao L, Shokralla S, Gharizadeh B, Ronaghi M, Fire AZ. 2007. A pyrosequencing-tailored nucleotide barcode design unveils opportunities for large-scale sample multiplexing. Nucleic Acids Res 35:e130. (Pubitemid 350111638)
32. Pettersson E, Lundeberg J, Ahmadian A. 2009. Generations of sequencing technologies. Genomics 93:105-111.
33. R Development Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: www.r-project.org. Accessed 27 August 2009. [ISBN 3-900051-07-0.]
34. Rohlin A, Wernersson J, Engwall Y, Wiklund L, Björk J, Nordling M. 2009. Parallel sequencing used in detection of mosaic mutations: comparison with four diagnostic DNA screening techniques. Hum Mutat 30:1012-1020.
35. Ropers HH. 2007. New perspectives for the elucidation of genetic disorders. Am J Hum Genet 81:199-207. (Pubitemid 47236069)
36. Simen BB, Simons JF, Huppler Hullsiek K, Novak RM, Macarthur RD, Baxter JD, Huang C, Lubeski C, Turenchalk GS, Braverman MS, Desany B, Rothberg JM, Egholm M, Kozal MJ. 2009. Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J Infect Dis 199:693-701.
37. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978-989. (Pubitemid 32289743)
38. Stephens M, Donnelly P. 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162-1169. (Pubitemid 37414228)
39. Tavtigian SV, Byrnes GB, Goldgar DE, Thomas A. 2008. Classification of rare missense substitutions, using risk surfaces, with genetic- and molecular-epidemiology applications. Hum Mutat 29:1342-1354.
40. Thomas RK, Nickerson E, Simons JF, Jänne PA, Tengs T, Yuza Y, Garraway LA, LaFramboise T, Lee JC, Shah K, O'Neill K, Sasaki H, Lindeman N, Wong KK, Borras AM, Gutmann EJ, Dragnev KH, DeBiasi R, Chen TH, Glatt KA, Greulich H, Desany B, Lubeski CK, Brockman W, Alvarez P, Hutchison SK, Leamon JH, Ronan MT, Turenchalk GS, Egholm M, Sellers WR, Rothberg JM, Meyerson M. 2006. Sensitive mutation detection in heterogeneous cancer specimens by massively parallel picoliter reactor sequencing. Nat Med 12:852-855. (Pubitemid 44050078)
41. Varley KE, Mitra RD. 2008. Nested Patch PCR enables highly multiplexed mutation discovery in candidate genes. Genome Res 18:1844-1850.
42. Wang C, Mitsuya Y, Gharizadeh B, Ronaghi M, Shafer RW. 2007. Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res 17:1195-1201. (Pubitemid 47204863)
43. Wendl MC, Barbazuk WB. 2005. Extension of Lander-Waterman theory for sequencing filtered DNA libraries. BMC Bioinformatics 6:245.
44. Wendl MC, Wilson RK. 2008. Aspects of coverage in medical DNA sequencing. BMC Bioinformatics 9:239.
45. Yeager M, Xiao N, Hayes RB, Bouffard P, Desany B, Burdett L, Orr N, Matthews C, Qi L, Crenshaw A, Markovic Z, Fredrikson KM, Jacobs KB, Amundadottir L, Jarvie TP, Hunter DJ, Hoover R, Thomas G, Harkins TT, Chanock SJ. 2008. Comprehensive resequence analysis of a 136 kb region of human chromosome 8q24 associated with prostate and colon cancers. Hum Genet 124:161-170.