Exome sequencing of African-American prostate cancer reveals loss-of-function ERF mutations

Cancer Discovery

Volumn 7, Issue 9, 2017, Pages 973-983

  Huang, Franklin W ^a,b,c   Mosquera, Juan Miguel ^d   Garofalo, Andrea ^c   Oh, Coyin ^c   Baco, Maria ^c   Amin Mansour, Ali ^c   Rabasha, Bokang ^a,c   Bahl, Samira ^c   Mullane, Stephanie A ^c   Robinson, Brian D ^d   Aldubayan, Saud ^a,c   Khani, Francesca ^d   Karir, Beerinder ^d   Kim, Eejung ^a,c   Chimene Weiss, Jeremy ^c   Hofree, Matan ^c   Romanel, Alessandro ^e   Osborne, Joseph R ^d,f   Kim, Jong Wook ^a,c   Azabdaftari, Gissou ^g   Woloszynska Read, Anna ^g   Sfanos, Karen ^h   De Marzo, Angelo M ^h,i   Demichelis, Francesca ^d,e   Gabriel, Stacey ^c   Van Allen, Eliezer M ^a,b,c   Mesirov, Jill ^c,j,k   Tamayo, Pablo ^c,j,k   Rubin, Mark A ^d   Powell, Isaac J ^l,m   Garraway, Levi A ^a,b,c   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF TRENTO   (Italy)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g ROSWELL PARK CANCER INSTITUTE   (United States)

^h JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

ⁱ JOHNS HOPKINS UNIVERSITY   (United States)

^j UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^k UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^l KARMANOS CANCER INSTITUTE   (United States)

^m WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 2; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; LENTIVIRUS VECTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SPOP PROTEIN; TRANSCRIPTION FACTOR ETS; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ERF PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PIK3CA PROTEIN, HUMAN; PTEN PROTEIN, HUMAN; REPRESSOR PROTEIN;

AFRICAN AMERICAN; ARTICLE; CANCER GENETICS; CANCER INHIBITION; COHORT ANALYSIS; CONTROLLED STUDY; COPY NUMBER VARIATION; CRISPR-CAS9 SYSTEM; DOWN REGULATION; FLUORESCENCE IN SITU HYBRIDIZATION; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE FREQUENCY; GENETIC TRANSDUCTION; GERMLINE MUTATION; GLEASON SCORE; HUMAN; HUMAN TISSUE; LOSS OF FUNCTION MUTATION; MAJOR CLINICAL STUDY; MALE; PROSTATE CANCER; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SOMATIC MUTATION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; WHOLE EXOME SEQUENCING; ANIMAL; EXOME; GENETICS; MOUSE; MUTATION; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

AFRICAN AMERICANS; ANIMALS; CELL LINE, TUMOR; CLASS I PHOSPHATIDYLINOSITOL 3-KINASES; EXOME; HUMANS; MALE; MICE; MUTATION; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; REPRESSOR PROTEINS; WHOLE EXOME SEQUENCING;

EID: 85026420328     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-16-0960     Document Type: Article

References (50)

1. Taksler GB, Keating NL, Cutler DM. Explaining racial differences in prostate cancer mortality. Cancer 2012;118:4280-9.
2. Khani F, Mosquera JM, Park K, Blattner M, O’Reilly C, MacDonald TY, et al. Evidence for molecular differences in prostate cancer between African American and Caucasian men. Clin Cancer Res 2014;20:4925-34.
3. Petrovics G, Li H, Stumpel T, Tan SH, Young D, Katta S, et al. A novel genomic alteration of LSAMP associates with aggressive prostate cancer in African American men. EBioMedicine 2015;2:1957-64.
4. Lindquist KJ, Paris PL, Hoffmann TJ, Cardin NJ, Kazma R, Mefford JA, et al. Mutational landscape of aggressive prostate tumors in African American men. Cancer Res 2016;76:1860-8.
5. Cher ML, Lewis PE, Banerjee M, Hurley PM, Sakr W, Grignon DJ, et al. A Similar pattern of chromosomal alterations in prostate cancers from African-Americans and Caucasian Americans. Clin Cancer Res 1998;4:1273-8.
6. Rose AE, Satagopan JM, Oddoux C, Zhou Q, Xu R, Olshen AB, et al. Copy number and gene expression differences between African American and Caucasian American prostate cancer. J Transl Med 2010;8:70.
7. Shi Y, Li J, Zhang S, Wang M, Yang S, Li N, et al. Molecular epidemiology of EGFR mutations in Asian patients with advanced non-small-cell lung cancer of adenocarcinoma histology - Mainland China Subset Analysis of the PIONEER study. PLoS One 2015;10:e0143515.
8. Spratt DE, Chan T, Waldron L, Speers C, Feng FY, Ogunwobi OO, et al. Racial/ethnic disparities in genomic sequencing. JAMA Oncol 2016; 2:1070-4.
9. Baca SC, Prandi D, Lawrence MS, Mosquera JM, Romanel A, Drier Y, et al. Punctuated evolution of prostate cancer genomes. Cell 2013; 153:666-77.
10. Barbieri CE, Baca SC, Lawrence MS, Demichelis F, Blattner M, Theurillat JP, et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat Genet 2012;44:685-9.
11. Cancer Genome Atlas Research Network. The molecular taxonomy of primary prostate cancer. Cell 2015;163:1011-25.
12. DeSantis CE, Siegel RL, Sauer AG, Miller KD, Fedewa SA, Alcaraz KI, et al. Cancer statistics for African Americans, 2016: progress and opportunities in reducing racial disparities. CA Cancer J Clin 2016;66:290-308.
13. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.
14. Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R, Getz G. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol 2011;12:R41.
15. Migita T, Ruiz S, Fornari A, Fiorentino M, Priolo C, Zadra G, et al. Fatty acid synthase: a metabolic enzyme and candidate oncogene in prostate cancer. J Natl Cancer Inst 2009;101:519-32.
16. Mateo J, Carreira S, Sandhu S, Miranda S, Mossop H, Perez-Lopez R, et al. DNA-repair defects and olaparib in metastatic prostate cancer. 2015;373:1697-708.
17. Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 2013;499:214-8.
18. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun X, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310:644-8.
19. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods 2010;7:248-9.
20. Beltran H, Prandi D, Mosquera JM, Benelli M, Puca L, Cyrta J, et al. Divergent clonal evolution of castration-resistant neuroendocrine prostate cancer. Nat Med 2016;22:298-305.
21. Beltran H, Eng K, Mosquera JM, Sigaras A, Romanel A, Rennert H, et al. Whole-exome sequencing of metastatic cancer and biomarkers of treatment response. JAMA Oncol 2015;1:466-74.
22. Robinson D, Van Allen EM, Wu YM, Schultz N, Lonigro RJ, Mosquera JM, et al. Integrative clinical genomics of advanced prostate cancer. Cell 2015;161:1215-28.
23. Kumar A, Coleman I, Morrissey C, Zhang X, True LD, Gulati R, et al. Substantial interindividual and limited intraindividual genomic diversity among tumors from men with metastatic prostate cancer. Nat Med 2016;22:369-78.
24. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012;483:603-7.
25. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY, Beare D, et al. COSMIC: Mining complete cancer genomes in the catalogue of somatic mutations in cancer. Nucleic Acids Res 2011;39(Database issue):D945-50.
26. Sgouras DN, Athanasiou MA, Beal GJ, Fisher RJ, Blair DG, Mavrothalassitis GJ. ERF: an ETS domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. EMBO J 1995;14:4781-93.
27. Le Gallic L, Sgouras D, Beal G Jr, Mavrothalassitis G. Transcriptional repressor ERF is a Ras/mitogen-activated protein kinase target that regulates cellular proliferation. Mol Cell Biol 1999;19:4121-33.
28. Giannakis M, Mu XJ, Shukla SA, Qian ZR, Cohen O, Nishihara R, et al. Genomic correlates of immune-cell infiltrates in colorectal carcinoma. Cell Rep 2016;17:1206.
29. Crompton BD, Stewart C, Taylor-Weiner A, Alexe G, Kurek KC, Calicchio ML, et al. The genomic landscape of pediatric Ewing sarcoma. Cancer Discov 2014;4:1326-41.
30. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012;2:401-4.
31. Chen Y, Chi P, Rockowitz S, Iaquinta PJ, Shamu T, Shukla S, et al. ETS factors reprogram the androgen receptor cistrome and prime prostate tumorigenesis in response to PTEN loss. Nat Med 2013;19:1023-9.
32. Baena E, Shao Z, Linn DE, Glass K, Hamblen MJ, Fujiwara Y, et al. ETV1 directs androgen metabolism and confers aggressive prostate cancer in targeted mice and patients. Genes Dev 2013;27:683-98.
33. Berger R, Febbo PG, Majumder PK, Zhao JJ, Mukherjee S, Signoretti S, et al. Androgen-induced differentiation and tumorigenicity of human prostate epithelial cells. Cancer Res 2004;64:8867-75.
34. Nelson PS, Clegg N, Arnold H, Ferguson C, Bonham M, White J, et al. The program of androgen-responsive genes in neoplastic prostate epithelium. Proc Natl Acad Sci U S A 2002;99:11890-5.
35. Sharma NL, Massie CE, Ramos-Montoya A, Zecchini V, Scott HE, Lamb AD, et al. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell 2013;23:35-47.
36. Shalem O, Sanjana NE, Hartenian E, Shi X, Scott DA, Mikkelsen TS, et al. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014;343:84-7.
37. Sheridan CM, Grogan TR, Nguyen HG, Galet C, Rettig MB, Hsieh AC, et al. YB-1 and MTA1 protein levels and not DNA or mRNA alterations predict for prostate cancer recurrence. Oncotarget 2015;6:7470-80.
38. Tosoian JJ, Almutairi F, Morais CL, Glavaris S, Hicks J, Sundi D, et al. Prevalence and prognostic significance of PTEN loss in African-American and European-American men undergoing radical prostatectomy. Eur Urol 2017;71:697-700.
39. Romanel A, Zhang T, Elemento O, Demichelis F. EthSEQ: ethnicity annotation from whole exome sequencing data. Bioinformatics. 2017 Mar 27. [Epub ahead of print].
40. Dissanayake K, Toth R, Blakey J, Olsson O, Campbell DG, Prescott AR, et al. ERK/p90(RSK)/14-3-3 signalling has an impact on expression of PEA3 Ets transcription factors via the transcriptional repressor capicua. Biochem J 2011;433:515-25.
41. Magi-Galluzzi C, Tsusuki T, Elson P, Simmerman K, LaFargue C, Esgueva R, et al. TMPRSS2-ERG gene fusion prevalence and class are significantly different in prostate cancer of Caucasian, African-American and Japanese patients. Prostate 2011;71:489-97.
42. Blattner M, Lee DJ, O’Reilly C, Park K, MacDonald TY, Khani F, et al. SPOP mutations in prostate cancer across demographically diverse patient cohorts. Neoplasia 2014;16:14-20.
43. Faisal FA, Sundi D, Tosoian JJ, Choeurng V, Alshalalfa M, Ross AE, et al. Racial variations in prostate cancer molecular subtypes and androgen receptor signaling reflect anatomic tumor location. Eur Urol 2016;70:14-7.
44. Yamoah K, Johnson MH, Choeurng V, Faisal FA, Yousefi K, Haddad Z, et al. Novel biomarker signature that may predict aggressive disease in African American men with prostate cancer. J Clin Oncol 2015;33:2789-96.
45. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012;487:239-43.
46. Duggan D, Zheng SL, Knowlton M, Benitez D, Dimitrov L, Wiklund F, et al. Two genome-wide association studies of aggressive prostate cancer implicate putative prostate tumor suppressor gene DAB21P. J Natl Cancer Inst 2007;99:1836-44.
47. Rand KA, Rohland N, Tandon A, Stram A, Sheng X, Do R, et al. Whole-exome sequencing of over 4100 men of African ancestry and prostate cancer risk. Hum Mol Genet 2016;25:371-81.
48. Manrai AK, Funke BH, Rehm HL, Olesen MS, Maron BA, Szolovits P, et al. Genetic misdiagnoses and the potential for health disparities. N Engl J Med 2016;375:655-65.
49. Chakravarty D, Sboner A, Nair SS, Giannopoulou E, Li R, Hennig S, et al. The oestrogen receptor alpha-regulated lncRNA NEAT1 is a critical modulator of prostate cancer. Nat Commun 2014;5:5383.
50. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdottir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics 2011;27:1739-40.