Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes

Nature Genetics

Volumn 44, Issue 12, 2012, Pages 1310-1315

  Le Gallo, Matthieu ^a   O'Hara, Andrea J ^a   Rudd, Meghan L ^a   Urick, Mary Ellen ^a   Hansen, Nancy F ^a   O'Neil, Nigel J ^b   Price, Jessica C ^a   Zhang, Suiyuan ^a   England, Bryant M ^a   Godwin, Andrew K ^c   Sgroi, Dennis C ^d   Hieter, Philip ^b   Mullikin, James C ^a,e   Merino, Maria J ^f   Bell, Daphne W ^a  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e NATIONAL INSTITUTES OF HEALTH   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

E1A ASSOCIATED P300 PROTEIN; UBIQUITIN PROTEIN LIGASE;

ABCC9 GENE; ARID1A GENE; ARTICLE; CHD4 GENE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENDOMETRIUM CANCER; EXOME; FBXW7 GENE; FEMALE; GENE; GENE DISRUPTION; GENE SEQUENCE; GENETIC CODE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR PATHOLOGY; NUCLEOTIDE SEQUENCE; PRIMARY TUMOR; PRIORITY JOURNAL; SEROUS ENDOMETRIAL CANCER; SOMATIC MUTATION; SPOP GENE;

ADENOCARCINOMA, CLEAR CELL; ADULT; ATP-BINDING CASSETTE TRANSPORTERS; AUTOANTIGENS; BASE SEQUENCE; CARCINOMA, ENDOMETRIOID; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; E1A-ASSOCIATED P300 PROTEIN; ENDOMETRIAL NEOPLASMS; EXOME; F-BOX PROTEINS; FEMALE; GENE FREQUENCY; HUMANS; MAP KINASE KINASE KINASE 4; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; RECEPTORS, DRUG; REPRESSOR PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITIN-PROTEIN LIGASES;

EID: 84870532434     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.2455     Document Type: Article

References (64)

1. Ferlay, J. et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int. J. Cancer 127, 2893-2917 (2010).
2. Sherman, M.E. Theories of endometrial carcinogenesis: a multidisciplinary approach. Mod. Pathol. 13, 295-308 (2000). (Pubitemid 30207514)
3. Hamilton, C.A. et al. Uterine papillary serous and clear cell carcinomas predict for poorer survival compared to grade 3 endometrioid corpus cancers. Br. J. Cancer 94, 642-646 (2006). (Pubitemid 43361894)
4. Hendrickson, M., Ross, J., Eifel, P., Martinez, A. & Kempson, R. Uterine papillary serous carcinoma: a highly malignant form of endometrial adenocarcinoma. Am. J. Surg. Pathol. 6, 93-108 (1982). (Pubitemid 12108965)
5. McConechy, M.K. et al. Subtype-specific mutation of PPP2R1A in endometrial and ovarian carcinomas. J. Pathol. 223, 567-573 (2011).
6. Rudd, M.L. et al. A unique spectrum of somatic PIK3CA (p110α) mutations within primary endometrial carcinomas. Clin. Cancer Res. 17, 1331-1340 (2011).
7. Shih, I.M. et al. Somatic mutations of PPP2R1A in ovarian and uterine carcinomas. Am. J. Pathol. 178, 1442-1447 (2011).
8. Hayes, M.P., Douglas, W. & Ellenson, L.H. Molecular alterations of EGFR and PIK3CA in uterine serous carcinoma. Gynecol. Oncol. 113, 370-373 (2009).
9. National Cancer Institute, SEER Program. SEER Survival Monograph: Cancer Survival Among Adults: U.S. SEER Program, 1988-2001. Patient and Tumor Characteristics (eds. Ries, L.A.G., Young, J.L., Keel, G.E., Eisner, M.P., Lin, Y.D. & Horner, M.-J.) (National Cancer Institute, SEER Program, Bethesda, MD, 2007).
10. Zhang, Y., LeRoy, G., Seelig, H.P., Lane, W.S. & Reinberg, D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95, 279-289 (1998). (Pubitemid 28473788)
11. Li, J., Lin, Q., Wang, W., Wade, P. & Wong, J. Specific targeting and constitutive association of histone deacetylase complexes during transcriptional repression. Genes Dev. 16, 687-692 (2002). (Pubitemid 34274038)
12. Tong, J.K., Hassig, C.A., Schnitzler, G.R., Kingston, R.E. & Schreiber, S.L. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 395, 917-921 (1998). (Pubitemid 28503435)
13. Xue, Y. et al. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 2, 851-861 (1998). (Pubitemid 128378992)
14. Hall, J.A. & Georgel, P.T. CHD proteins: a diverse family with strong ties. Biochem. Cell Biol. 85, 463-476 (2007). (Pubitemid 47518041)
15. Lai, A.Y. & Wade, P.A. Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11, 588-596 (2011).
16. Polo, S.E., Kaidi, A., Baskcomb, L., Galanty, Y. & Jackson, S.P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 29, 3130-3139 (2010).
17. Smeenk, G. et al. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 190, 741-749 (2010).
18. Chou, D.M. et al. A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. USA 107, 18475-18480 (2010).
19. Larsen, D.H. et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J. Cell Biol. 190, 731-740 (2010).
20. Boerkoel, C.F. et al. Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat. Genet. 30, 215-220 (2002).
21. Tsurusaki, Y. et al. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat. Genet. 44, 376-378 (2012).
22. Van Houdt, J.K. et al. Heterozygous missense mutations in SMARCA2 cause Nicolaides-Baraitser syndrome. Nat. Genet. 44, 445-449 (2012).
23. Welcker, M. & Clurman, B.E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer 8, 83-93 (2008). (Pubitemid 351161321)
24. Cassia, R. et al. Cyclin E gene (CCNE) amplification and hCDC4 mutations in endometrial carcinoma. J. Pathol. 201, 589-595 (2003). (Pubitemid 38256408)
25. Dutt, A. et al. Drug-sensitive FGFR2 mutations in endometrial carcinoma. Proc. Natl. Acad. Sci. USA 105, 8713-8717 (2008). (Pubitemid 351987745)
26. Spruck, C.H. et al. hCDC4 gene mutations in endometrial cancer. Cancer Res. 62, 4535-4539 (2002).
27. Suehiro, Y. et al. Aneuploidy predicts outcome in patients with endometrial carcinoma and is related to lack of CDH13 hypermethylation. Clin. Cancer Res. 14, 3354-3361 (2008).
28. Forbes, S.A. et al. The Catalogue of Somatic Mutations in Cancer (COSMIC). Curr. Protoc. Hum. Genet. Ch. 10, Unit 10.11 (2008).
29. Reva, B., Antipin, Y. & Sander, C. Predicting the functional impact of protein mutations: application to cancer genomics. Nucleic Acids Res. 39, e118 (2011).
30. Wertz, I.E. et al. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471, 110-114 (2011).
31. Garnett, M.J. et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 483, 570-575 (2012).
32. Barbieri, C.E. et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat. Genet. 44, 685-689 (2012).
33. Li, C. et al. Tumor-suppressor role for the SPOP ubiquitin ligase in signal-dependent proteolysis of the oncogenic co-activator SRC-3/AIB1. Oncogene 30, 4350-4364 (2011).
34. Glaeser, M., Floetotto, T., Hanstein, B., Beckmann, M.W. & Niederacher, D. Gene amplification and expression of the steroid receptor coactivator SRC3 (AIB1) in sporadic breast and endometrial carcinomas. Horm. Metab. Res. 33, 121-126 (2001). (Pubitemid 32429982)
35. Huang, D.W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
36. Huang, D.W., Sherman, B.T. & Lempicki, R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13 (2009).
37. Dalgliesh, G.L. et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463, 360-363 (2010).
38. Fujimoto, A. et al. Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat. Genet. 44, 760-764 (2012).
39. Grasso, C.S. et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 487, 239-243 (2012).
40. Gui, Y. et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat. Genet. 43, 875-878 (2011).
41. Guichard, C. et al. Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat. Genet. 44, 694-698 (2012).
42. Jiao, Y. et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203 (2011).
43. Jones, S. et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330, 228-231 (2010).
44. Ong, C.K. et al. Exome sequencing of liver fluke-associated cholangiocarcinoma. Nat. Genet. 44, 690-693 (2012).
45. Parsons, D.W. et al. The genetic landscape of the childhood cancer medulloblastoma. Science 331, 435-439 (2011).
46. Schwartzentruber, J. et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231 (2012).
47. Shain, A.H. et al. Convergent structural alterations define SWItch/Sucrose NonFermentable (SWI/SNF) chromatin remodeler as a central tumor suppressive complex in pancreatic cancer. Proc. Natl. Acad. Sci. USA 109, E252-E259 (2012).
48. Varela, I. et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469, 539-542 (2011).
49. Wiegand, K.C. et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532-1543 (2010).
50. Wang, K. et al. Exome sequencing identifies frequent mutation of ARID1A in molecular subtypes of gastric cancer. Nat. Genet. 43, 1219-1223 (2011).
51. Ogryzko, V.V., Schiltz, R.L., Russanova, V., Howard, B.H. & Nakatani, Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87, 953-959 (1996). (Pubitemid 26404293)
52. Huang, J., Zhao, Y.L., Li, Y., Fletcher, J.A. & Xiao, S. Genomic and functional evidence for an ARID1A tumor suppressor role. Genes Chromosom. Cancer 46, 745-750 (2007). (Pubitemid 46912345)
53. Guan, B., Wang, T.L. & Shih, I.M. ARID1A, a factor that promotes formation of SWI/SNF-mediated chromatin remodeling, is a tumor suppressor in gynecologic cancers. Cancer Res. 71, 6718-6727 (2011).
54. Hargreaves, D.C. & Crabtree, G.R. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396-420 (2011).
55. Guan, B. et al. Mutation and loss of expression of ARID1A in uterine low-grade endometrioid carcinoma. Am. J. Surg. Pathol. 35, 625-632 (2011).
56. McConechy, M.K. et al. Use of mutation profiles to refine the classification of endometrial carcinomas. J. Pathol. 228, 20-30 (2012).
57. Wiegand, K.C. et al. Loss of BAF250a (ARID1A) is frequent in high-grade endometrial carcinomas. J. Pathol. 224, 328-333 (2011).
58. Urick, M.E. et al. PIK3R1 (p85α) is somatically mutated at high frequency in primary endometrial cancer. Cancer Res. 71, 4061-4067 (2011).
59. Kuhn, E. et al. Identification of molecular pathway aberrations in uterine serous carcinoma by genome-wide analyses. J. Natl. Cancer Inst. 104, 1503-1513 (2012).
60. Teer, J.K. et al. Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res. 20, 1420-1431 (2010).
61. Teer, J.K., Green, E.D., Mullikin, J.C. & Biesecker, L.G. VarSifter: visualizing and analyzing exome-scale sequence variation data on a desktop computer. Bioinformatics 28, 599-600 (2012).
62. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J.R. Stat. Soc. 57, 289-300 (1995).
63. Sjöblom, T. et al. The consensus coding sequences of human breast and colorectal cancers. Science 314, 268-274 (2006). (Pubitemid 44571966)
64. Rubin, A.F. & Green, P. Comment on "The consensus coding sequences of human breast and colorectal cancers". Science 317, 1500 (2007).