Whole-exome sequencing of over 4100 men of African ancestry and prostate cancer risk

Human Molecular Genetics

Volumn 25, Issue 2, 2016, Pages 371-381

  Rand, Kristin A ^a,b   Rohland, Nadin ^c,d   Tandon, Arti ^c,d   Stram, Alex ^a   Sheng, Xin ^a   Do, Ron ^c,d   Pasaniuc, Bogdan ^e   Allen, Alex ^c,d   Quinque, Dominique ^c,d   Mallick, Swapan ^c,d   Le Marchand, Loic ^f,h   Kaggwa, Sam ^g   Lubwama, Alex ^g   Stram, Daniel O ^a,b   Watya, Stephen ^g,h   Henderson, Brian E ^a,b   Conti, David V ^a,b   Reich, David ^c,d   Haiman, Christopher A ^a,b   Strom, Sara S ^h   Kittles, Rick A ^h   Rybicki, Benjamin A ^h   Stanford, Janet L ^h   Goodman, Phyllis J ^h   Berndt, Sonja I ^h   Carpten, John ^h   Casey, Graham ^h   Chu, Lisa ^h   Diver, Ryan W ^h   Hennis, Anselm J M ^h   Klein, Eric A ^h   Kolb, Suzanne ^h   Cristina Leske, M ^h   Murphy, Adam B ^h   Neslund Dudas, Christine ^h   Park, Jong Y ^h   John, Esther M ^h   Kibel, Adam S ^h   Pettaway, Curtis ^h   Gapstur, Susan M ^h   Lilly Zheng, S ^h   Wu, Suh Yuh ^h   Witte, John S ^h   Xu, Jianfeng ^h   Isaacs, William ^h   Ingles, Sue A ^h   Hsing, Ann ^h   Nemesure, Barbara ^h   Blot, William J ^h   Eeles, Rosalind A ^h   Easton, Douglas ^h   Kote Jarai, Zsofia ^h   Muir, Kenneth ^h   Al Olama, Ali Amin ^h   Wiklund, Fredrik ^h   Grönberg, Henrik ^h   Kraft, Peter ^h   Gapstur, Susan ^h   Riboli, Elio ^h   Hunter, David ^h   Stevens, Victoria ^h   Chanock, Stephen J ^h   more..

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^g MAKERERE UNIVERSITY   (Uganda)

^h Urocare Clinic   (Uganda)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; PROTEIN MLH1;

ADULT; AFRICAN; AGED; ARTICLE; C1ORF100 GENE; CANCER PATIENT; CANCER RISK; CONTROLLED STUDY; EXOME; GENE; GENE FREQUENCY; GENETIC PROCEDURES; GENETIC VARIABILITY; GORAB GENE; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PTPRR GENE; SPARCL1 GENE; STOP CODON; WHOLE EXOME SEQUENCING; BLACK PERSON; CLINICAL TRIAL; DNA SEQUENCE; GENETIC ASSOCIATION STUDY; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; MULTICENTER STUDY; PROSTATIC NEOPLASMS; RISK; SINGLE NUCLEOTIDE POLYMORPHISM;

ADULT; AFRICAN CONTINENTAL ANCESTRY GROUP; AGED; EXOME; GENETIC ASSOCIATION STUDIES; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; PROSTATIC NEOPLASMS; RISK; SEQUENCE ANALYSIS, DNA;

EID: 84960803873     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv462     Document Type: Article

References (60)

1. Kolonel, L.N., Altshuler, D. and Henderson, B.E. (2004) The multiethnic cohort study: exploring genes, lifestyle and cancer risk. Nat. Rev. Cancer, 4, 519-527.
2. Hemminki, K. (2012) Familial risk and familial survival in prostate cancer. World J. Urol., 30, 143-148.
3. Hjelmborg, J.B., Scheike, T., Holst, K., Skytthe, A., Penney, K.L., Graff, R.E., Pukkala, E., Christensen, K., Adami, H.O., Holm, N. V. et al. (2014) The heritability of prostate cancer in the nordic twin study of cancer. Cancer Epidemiol. Biomarkers Prev., 23, 2303-2310.
4. Haiman, C.A., Patterson, N., Freedman, M.L., Myers, S.R., Pike, M.C.,Waliszewska, A., Neubauer, J., Tandon, A., Schirmer, C., McDonald, G.J. et al. (2007) Multiple regions within 8q24 independently affect risk for prostate cancer. Nat. Genet., 39, 638-644.
5. Gudmundsson, J., Sulem, P., Rafnar, T., Bergthorsson, J.T., Manolescu, A., Gudbjartsson, D., Agnarsson, B.A., Sigurdsson, A., Benediktsdottir, K.R., Blondal, T. et al. (2008) Common sequence variants on 2p15 and Xp11.22 confer susceptibility to prostate cancer. Nat. Genet., 40, 281-283.
6. Al Olama, A.A., Kote-Jarai, Z., Giles, G.G., Guy, M., Morrison, J., Severi, G., Leongamornlert, D.A., Tymrakiewicz, M., Jhavar, S., Saunders, E. et al. (2009) Multiple loci on 8q24 associated with prostate cancer susceptibility. Nat. Genet., 41, 1058-1060.
7. Eeles, R.A., Kote-Jarai, Z., Al Olama, A.A., Giles, G.G., Guy, M., Severi, G., Muir, K., Hopper, J.L., Henderson, B.E., Haiman, C.A. et al. (2009) Identification of seven new prostate cancer susceptibility loci through a genome-wide association study. Nat. Genet., 41, 1116-1121.
8. Gudmundsson, J., Sulem, P., Gudbjartsson, D.F., Blondal, T., Gylfason, A., Agnarsson, B.A., Benediktsdottir, K.R., Magnusdottir, D.N., Orlygsdottir, G., Jakobsdottir, M. et al. (2009) Genome-wide association and replication studies identify four variants associated with prostate cancer susceptibility. Nat. Genet., 41, 1122-1126.
9. Jia, L., Landan, G., Pomerantz, M., Jaschek, R., Herman, P., Reich, D., Yan, C., Khalid, O., Kantoff, P., Oh, W. et al. (2009) Functional enhancers at the gene-poor 8q24 cancer-linked locus. PLoS Genet., 5, e1000597.
10. Sun, J., Zheng, S.L.,Wiklund, F., Isaacs, S.D., Li, G.,Wiley, K.E., Kim, S.T., Zhu, Y., Zhang, Z., Hsu, F.C. et al. (2009) Sequence variants at 22q13 are associated with prostate cancer risk. Cancer Res., 69, 10-15.
11. Xu, J., Mo, Z., Ye, D.,Wang, M., Liu, F., Jin, G., Xu, C.,Wang, X., Shao, Q., Chen, Z. et al. (2012) Genome-wide association study in Chinese men identifies two newprostate cancer risk loci at 9q31.2 and 19q13.4. Nat. Genet., 44, 1231-1235.
12. Kote-Jarai, Z., Olama, A.A., Giles, G.G., Severi, G., Schleutker, J., Weischer, M., Campa, D., Riboli, E., Key, T., Gronberg, H. et al. (2011) Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study. Nat. Genet., 43, 785-791.
13. Lindstrom, S., Schumacher, F., Siddiq, A., Travis, R.C., Campa, D., Berndt, S.I., Diver, W.R., Severi, G., Allen, N., Andriole, G. et al. (2011) Characterizing associations and SNP-environment interactions for GWAS-identified prostate cancer risk markers-results from BPC3. PLoS One, 6, e17142.
14. Schumacher, F.R., Berndt, S.I., Siddiq, A., Jacobs, K.B., Wang, Z., Lindstrom, S., Stevens, V.L., Chen, C., Mondul, A.M., Travis, R.C. et al. (2011) Genome-wide association study identifies new prostate cancer susceptibility loci. Hum. Mol. Genet., 20, 3867-3875.
15. Akamatsu, S., Takata, R., Haiman, C.A., Takahashi, A., Inoue, T., Kubo, M., Furihata, M., Kamatani, N., Inazawa, J., Chen, G. K. et al. (2012) Common variants at 11q12, 10q26 and 3p11.2 are associated with prostate cancer susceptibility in Japanese. Nat. Genet., 44, 426-429, S421.
16. Amin Al Olama, A., Kote-Jarai, Z., Schumacher, F.R.,Wiklund, F., Berndt, S.I., Benlloch, S., Giles, G.G., Severi, G., Neal, D.E., Hamdy, F.C. et al. (2013) A meta-analysis of genome-wide association studies to identify prostate cancer susceptibility loci associated with aggressive and non-aggressive disease. Hum. Mol. Genet., 22, 408-415.
17. Lindstrom, S., Schumacher, F.R., Campa, D., Albanes, D., Andriole, G., Berndt, S.I., Bueno-de-Mesquita, H.B., Chanock, S.J., Diver,W.R., Ganziano, J.M. et al. (2012) Replication of five prostate cancer loci identified in an Asian population-results from the NCI Breast and Prostate Cancer Cohort Consortium (BPC3). Cancer Epidemiol. Biomarkers Prev., 21, 212-216.
18. Xu, J., Zheng, S.L., Isaacs, S.D.,Wiley, K.E.,Wiklund, F., Sun, J., Kader, A.K., Li, G., Purcell, L.D., Kim, S.T. et al. (2010) Inherited genetic variant predisposes to aggressive but not indolent prostate cancer. Proc. Natl Acad. Sci. USA, 107, 2136-2140.
19. Eeles, R.A., Olama, A.A., Benlloch, S., Saunders, E.J., Leongamornlert, D.A., Tymrakiewicz, M., Ghoussaini, M., Luccarini, C., Dennis, J., Jugurnauth-Little, S. et al. (2013) Identification of 23 new prostate cancer susceptibility loci using the iCOGS custom genotyping array. Nat. Genet., 45, 385-391, 391e381-382.
20. Al Olama, A.A., Kote-Jarai, Z., Berndt, S.I., Conti, D.V., Schumacher, F., Han, Y., Benlloch, S., Hazelett, D.J., Wang, Z., Saunders, E. et al. (2014) A meta-analysis of 87,040 individuals identifies 23 new susceptibility loci for prostate cancer. Nat. Genet., 46, 1103-1109.
21. Han, Y., Signorello, L.B., Strom, S.S., Kittles, R.A., Rybicki, B.A., Stanford, J.L., Goodman, P.J., Berndt, S.I., Carpten, J., Casey, G. et al. (2015) Generalizability of established prostate cancer risk variants in men of African ancestry. Int. J. Cancer, 136, 1210-1217.
22. Manolio, T.A., Collins, F.S., Cox, N.J., Goldstein, D.B., Hindorff, L.A., Hunter, D.J., McCarthy, M.I., Ramos, E.M., Cardon, L.R., Chakravarti, A. et al. (2009) Finding the missing heritability of complex diseases. Nature, 461, 747-753.
23. Eeles, R.,Goh, C., Castro, E., Bancroft, E.,Guy, M.,AlOlama,A.A., Easton, D. and Kote-Jarai, Z. (2014) The genetic epidemiology of prostate cancer and its clinical implications. Nat. Rev. Urol., 11, 18-31.
24. Gayther, S.A., de Foy, K.A., Harrington, P., Pharoah, P., Dunsmuir, W.D., Edwards, S.M., Gillett, C., Ardern-Jones, A., Dearnaley, D.P., Easton, D.F. et al. (2000) The frequency of germ-line mutations in the breast cancer predisposition genes BRCA1 and BRCA2 in familial prostate cancer. The Cancer Research Campaign/British Prostate Group United Kingdom Familial Prostate Cancer Study Collaborators. Cancer Res., 60, 4513-4518.
25. Huang, H. and Cai, B. (2014) G84E mutation in HOXB13 is firmly associated with prostate cancer risk: a meta-analysis. Tumour Biol., 35, 1177-1182.
26. Laitinen, V.H., Wahlfors, T., Saaristo, L., Rantapero, T., Pelttari, L.M., Kilpivaara, O., Laasanen, S.L., Kallioniemi, A., Nevanlinna, H., Aaltonen, L. et al. (2013) HOXB13 G84E mutation in Finland: population-based analysis of prostate, breast, and colorectal cancer risk. Cancer Epidemiol. Biomarkers Prev., 22, 452-460.
27. Ewing, C.M., Ray, A.M., Lange, E.M., Zuhlke, K.A., Robbins, C.M., Tembe,W.D.,Wiley, K.E., Isaacs, S.D., Johng, D.,Wang, Y. et al. (2012) Germline mutations in HOXB13 and prostate-cancer risk. N. Engl. J. Med., 366, 141-149.
28. Xu, J., Lange, E.M., Lu, L., Zheng, S.L.,Wang, Z., Thibodeau, S.N., Cannon-Albright, L.A.,Teerlink, C.C., Camp,N.J., Johnson,A.M. et al. (2013) HOXB13 is a susceptibility gene for prostate cancer: results fromthe International Consortium for Prostate Cancer Genetics (ICPCG). Hum. Genet., 132, 5-14.
29. Browning, B.L. and Browning, S.R. (2009) A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet., 84, 210-223.
30. Wu, M.C., Lee, S., Cai, T., Li, Y., Boehnke, M. and Lin, X. (2011) Rare-variant association testing for sequencing data with the sequence kernel association test. Am. J. Hum. Genet., 89, 82-93.
31. Leongamornlert, D., Saunders, E., Dadaev, T., Tymrakiewicz, M., Goh, C., Jugurnauth-Little, S., Kozarewa, I., Fenwick, K., Assiotis, I., Barrowdale, D. et al. (2014) Frequent germline deleterious mutations in DNA repair genes in familial prostate cancer cases are associated with advanced disease. Br. J. Cancer, 110, 1663-1672.
32. Haiman, C.A., Han, Y., Feng, Y., Xia, L., Hsu, C., Sheng, X., Pooler, L.C., Patel, Y., Kolonel, L.N., Carter, E. et al. (2013) Genome-wide testing of putative functional exonic variants in relationship with breast and prostate cancer risk in a multiethnic population. PLoS Genet., 9, e1003419.
33. Li, Y., Sidore, C., Kang, H.M., Boehnke, M. and Abecasis, G.R. (2011) Low-coverage sequencing: implications for design of complex trait association studies. Genome Res., 21, 940-951.
34. Flannick, J., Korn, J.M., Fontanillas, P., Grant, G.B., Banks, E., Depristo, M.A. and Altshuler, D. (2012) Efficiency and power as a function of sequence coverage, SNP array density, and imputation. PLoS Comput. Biol., 8, e1002604.
35. Gravel, S.,Henn, B.M.,Gutenkunst, R.N., Indap,A.R.,Marth,G.T., Clark, A.G., Yu, F., Gibbs, R.A. and Bustamante, C.D. (2011) Demographic history and rare allele sharing among human populations. Proc. Natl Acad. Sci. USA, 108, 11983-11988.
36. Fu, W., O'Connor, T.D., Jun, G., Kang, H.M., Abecasis, G., Leal, S.M., Gabriel, S., Rieder, M.J., Altshuler, D., Shendure, J. et al. (2013) Analysis of 6,515 exomes reveals the recent origin of most human protein-coding variants. Nature, 493, 216-220.
37. Mathieson, I. and McVean, G. (2012) Differential confounding of rare and common variants in spatially structured populations. Nat. Genet., 44, 243-246.
38. Zhang, Y., Guan,W. and Pan,W. (2013) Adjustment for population stratification via principal components in association analysis of rare variants. Genet. Epidemiol., 37, 99-109.
39. Zawistowski, M., Reppell, M.,Wegmann, D., St Jean, P.L., Ehm, M.G., Nelson, M.R., Novembre, J. and Zollner, S. (2014) Analysis of rare variant population structure in Europeans explains differential stratification of gene-based tests. Eur. J. Hum. Genet., 22, 1137-1144.
40. Devlin, B. and Roeder, K. (1999) Genomic control for association studies. Biometrics, 55, 997-1004.
41. Devlin, B., Bacanu, S.A. and Roeder, K. (2004) Genomic control to the extreme. Nat. Genet., 36, 1129-1130; author reply 1131.
42. Zuk, O., Schaffner, S.F., Samocha, K., Do, R., Hechter, E., Kathiresan, S., Daly, M.J., Neale, B.M., Sunyaev, S.R. and Lander, E.S. (2014) Searching for missing heritability: designing rare variant association studies. Proc. Natl Acad. Sci. USA, 111, E455-E464.
43. Edwards, S.M., Kote-Jarai, Z., Meitz, J., Hamoudi, R., Hope, Q., Osin, P., Jackson, R., Southgate, C., Singh, R., Falconer, A. et al. (2003) Two percent of men with early-onset prostate cancer harbor germline mutations in the BRCA2 gene. Am. J. Hum. Genet., 72, 1-12.
44. Castro, E., Goh, C., Olmos, D., Saunders, E., Leongamornlert, D., Tymrakiewicz, M., Mahmud, N., Dadaev, T., Govindasami, K., Guy, M. et al. (2013) Germline BRCA mutations are associated with higher risk of nodal involvement, distant metastasis, and poor survival outcomes in prostate cancer. J. Clin. Oncol., 31, 1748-1757.
45. Shao, H., Bellos, E., Yin, H., Liu, X., Zou, J., Li, Y., Wang, J. and Coin, L.J. (2013) A population model for genotyping indels from next-generation sequence data. Nucl. Acids Res., 41, e46.
46. Lescai, F., Bonfiglio, S., Bacchelli, C., Chanudet, E., Waters, A., Sisodiya, S.M., Kasperaviciute, D., Williams, J., Harold, D., Hardy, J. et al. (2012) Characterisation and validation of insertions and deletions in 173 patient exomes. PLoS One, 7, e51292.
47. MacArthur, D.G. and Tyler-Smith, C. (2010) Loss-of-function variants in the genomes of healthy humans. Hum. Mol. Genet., 19, R125-R130.
48. O'Rawe, J., Jiang, T., Sun, G.,Wu, Y.,Wang,W., Hu, J., Bodily, P., Tian, L., Hakonarson, H., Johnson, W.E. et al. (2013) Low concordance ofmultiple variant-calling pipelines: practical implications for exome and genomesequencing. GenomeMed., 5, 28.
49. Gudmundsson, J., Sulem, P., Gudbjartsson, D.F., Masson, G., Agnarsson, B.A., Benediktsdottir, K.R., Sigurdsson, A., Magnusson, O.T., Gudjonsson, S.A., Magnusdottir, D.N. et al. (2012) A study based on whole-genome sequencing yields a rare variant at 8q24 associated with prostate cancer. Nat. Genet., 44, 1326-1329.
50. Hazelett, D.J., Coetzee, S.G. and Coetzee, G.A. (2013) A rare variant, which destroys a FoxA1 site at 8q24, is associated with prostate cancer risk. Cell Cycle, 12, 379-380.
51. Kolonel, L.N., Henderson, B.E., Hankin, J.H., Nomura, A.M., Wilkens, L.R., Pike, M.C., Stram, D.O., Monroe, K.R., Earle, M.E. and Nagamine, F.S. (2000) A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am. J. Epidemiol., 151, 346-357.
52. Haiman, C.A., Chen, G.K., Blot, W.J., Strom, S.S., Berndt, S.I., Kittles, R.A., Rybicki, B.A., Isaacs, W.B., Ingles, S.A., Stanford, J.L. et al. (2011) Genome-wide association study of prostate cancer in men of African ancestry identifies a susceptibility locus at 17q21. Nat. Genet., 43, 570-573.
53. Haiman, C.A., Chen, G.K., Blot, W.J., Strom, S.S., Berndt, S.I., Kittles, R.A., Rybicki, B.A., Isaacs, W.B., Ingles, S.A., Stanford, J.L. et al. (2011) Characterizing genetic risk at known prostate cancer susceptibility loci in African Americans. PLoS Genetics, 7, e1001387.
54. Rohland, N. and Reich, D. (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res., 22, 939-946.
55. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
56. DePristo, M.A., Banks, E., Poplin, R., Garimella, K.V., Maguire, J.R., Hartl, C., Philippakis, A.A., del Angel, G., Rivas, M.A., Hanna, M. et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet., 43, 491-498.
57. Wang, K., Li, M. and Hakonarson, H. (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucl. Acids Res., 38, e164.
58. Mancuso, N., Rohland, N., Rand, K.A., Tandon, A., Allen, A., Quinque, D., Mallick, S., Li, H., Stram, A., Sheng, X. et al. (2015) The contribution of rare variation to prostate cancer heritability. Nat. Genet., in press.
59. Price, A.L., Patterson, N.J., Plenge, R.M., Weinblatt, M.E., Shadick, N.A. and Reich, D. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet., 38, 904-909.
60. Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M.A., Bender, D., Maller, J., Sklar, P., de Bakker, P.I., Daly, M.J. et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet., 81, 559-575.