Genomic consequences of aberrant DNA repair mechanisms stratify ovarian cancer histotypes

Nature Genetics

Volumn 49, Issue 6, 2017, Pages 856-864

  Wang, Yi Kan ^a   Bashashati, Ali ^a   Anglesio, Michael S ^b   Cochrane, Dawn R ^a   Grewal, Diljot S ^a,b   Ha, Gavin ^a,i   McPherson, Andrew ^a,b   Horlings, Hugo M ^a   Senz, Janine ^a   Prentice, Leah M ^a   Karnezis, Anthony N ^b   Lai, Daniel ^a   Aniba, Mohamed R ^a   Zhang, Allen W ^a,b,c   Shumansky, Karey ^a   Siu, Celia ^a   Wan, Adrian ^a   McConechy, Melissa K ^b   Li Chang, Hector ^b   Tone, Alicia ^b,h   Provencher, Diane ^d,e,f   De Ladurantaye, Manon ^d,e   Fleury, Hubert ^d,e   Okamoto, Aikou ^g   Yanagida, Satoshi ^g   Yanaihara, Nozomu ^g   Saito, Misato ^g   Mungall, Andrew J ^a   Moore, Richard ^a   Marra, Marco A ^a,b   Gilks, C Blake ^b   Mes Masson, Anne Marie ^d,e,f   McAlpine, Jessica N ^b   Aparicio, Samuel ^a,b   Huntsman, David G ^a,b   Shah, Sohrab P ^a,b   more..

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^e Institut du Cancer de Montreal   (Canada)

^f UNIVERSITÉ DE MONTRÉAL   (Canada)

^g JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^h PRINCESS MARGARET HOSPITAL   (Canada)

ⁱ BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE; BETA CATENIN; BRCA1 PROTEIN; BRCA2 PROTEIN; DNA; FIBROBLAST GROWTH FACTOR RECEPTOR 2; K RAS PROTEIN; MISMATCH REPAIR PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; BRCA1 PROTEIN, HUMAN; BRCA2 PROTEIN, HUMAN;

ARTICLE; CANCER SURVIVAL; CLEAR CELL CARCINOMA; DEAMINATION; DNA REPAIR; ENDOMETRIOID CARCINOMA; FEMALE; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; GERMLINE MUTATION; GRANULOSA CELL TUMOR; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MICROSATELLITE INSTABILITY; OVARY CANCER; OVERALL SURVIVAL; POINT MUTATION; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN LOCALIZATION; SOMATIC MUTATION; CLINICAL TRIAL; COMPLICATION; ENDOMETRIOSIS; GENE EXPRESSION REGULATION; GENETICS; HUMAN GENOME; MORTALITY; MULTICENTER STUDY; MUTATION; OVARIAN NEOPLASMS; PATHOLOGY; PROGNOSIS;

BRCA1 PROTEIN; BRCA2 PROTEIN; DNA REPAIR; ENDOMETRIOSIS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; MUTATION; OVARIAN NEOPLASMS; PROGNOSIS;

EID: 85018321342     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3849     Document Type: Article

References (51)

1. Kobel, M. et al. Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med. 5, e232 (2008).
2. Vaughan, S. et al. Rethinking ovarian cancer: recommendations for improving outcomes. Nat. Rev. Cancer 11, 719-725 (2011).
3. Risch, H.A. et al. Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada. J. Natl. Cancer Inst. 98, 1694-1706 (2006).
4. Alsop, K. et al. BRCA mutation frequency and patterns of treatment response in BRCA mutation-positive women with ovarian cancer: a report from the Australian Ovarian Cancer Study Group. J. Clin. Oncol. 30, 2654-2663 (2012).
5. Berns, E.M. & Bowtell, D.D. The changing view of high-grade serous ovarian cancer. Cancer Res. 72, 2701-2704 (2012).
6. Anglesio, M.S., Carey, M.S., Kobel, M., Mackay, H. & Huntsman, D.G. Clear cell carcinoma of the ovary: a report from the first Ovarian Clear Cell Symposium, June 24th, 2010. Gynecol. Oncol. 121, 407-415 (2011).
7. Munksgaard, P.S. & Blaakaer, J. The association between endometriosis and ovarian cancer: a review of histological, genetic and molecular alterations. Gynecol. Oncol. 124, 164-169 (2012).
8. Ahmed, A.A. et al. Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J. Pathol. 221, 49-56 (2010).
9. Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615 (2011).
10. Wiegand, K.C. et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532-1543 (2010).
11. Jones, S. et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330, 228-231 (2010).
12. Obata, K. et al. Frequent PTEN/MMAC mutations in endometrioid but not serous or mucinous epithelial ovarian tumors. Cancer Res. 58, 2095-2097 (1998).
13. Wu, R., Zhai, Y., Fearon, E.R. & Cho, K.R. Diverse mechanisms of β-catenin deregulation in ovarian endometrioid adenocarcinomas. Cancer Res. 61, 8247-8255 (2001).
14. Campbell, I.G. et al. Mutation of the PIK3CA gene in ovarian and breast cancer. Cancer Res. 64, 7678-7681 (2004).
15. Kuo, K.-T. et al. Frequent activating mutations of PIK3CA in ovarian clear cell carcinoma. Am. J. Pathol. 174, 1597-1601 (2009).
16. Kurman, R.J. & Shih, IeM. Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum. Pathol. 42, 918-931 (2011).
17. McConechy, M.K. et al. Subtype-specific mutation of PPP2R1A in endometrial and ovarian carcinomas. J. Pathol. 223, 567-573 (2011).
18. Nissenblatt, M. Endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 364, 482-483, author reply 484-485 (2011).
19. Wu, R.-C. et al. Frequent somatic mutations of the telomerase reverse transcriptase promoter in ovarian clear cell carcinoma but not in other major types of gynaecological malignancy. J. Pathol. 232, 473-481 (2014).
20. Niskakoski, A. et al. Distinct molecular profiles in Lynch syndrome-associated and sporadic ovarian carcinomas. Int. J. Cancer 133, 2596-2608 (2013).
21. Shah, S.P. et al. Mutation of FOXL2 in granulosa-cell tumors of the ovary. N. Engl. J. Med. 360, 2719-2729 (2009).
22. Piccart, M.J. et al. Randomized intergroup trial of cisplatin-paclitaxel versus cisplatin-cyclophosphamide in women with advanced epithelial ovarian cancer: three-year results. J. Natl. Cancer Inst. 92, 699-708 (2000).
23. Rauh-Hain, J.A. & Penson, R.T. Potential benefit of sunitinib in recurrent and refractory ovarian clear cell adenocarcinoma. Int. J. Gynecol. Cancer 18, 934-936 (2008).
24. McAlpine, J.N. et al. HER2 overexpression and amplification is present in a subset of ovarian mucinous carcinomas and can be targeted with trastuzumab therapy. BMC Cancer 9, 433 (2009).
25. Anglesio, M.S. et al. IL6-STAT3-HIF signaling and therapeutic response to the angiogenesis inhibitor sunitinib in ovarian clear cell cancer. Clin. Cancer Res. 17, 2538-2548 (2011).
26. Farley, J.H., Gibson, S.J. & Monk, B.J. American Society of Clinical Oncology 2012 annual meeting update: summary of selected gynecologic cancer abstracts. Gynecol. Oncol. 126, 319-324 (2012).
27. Anglesio, M.S. et al. Molecular characterization of mucinous ovarian tumours supports a stratified treatment approach with HER2 targeting in 19% of carcinomas. J. Pathol. 229, 111-120 (2013).
28. Ledermann, J. et al. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N. Engl. J. Med. 366, 1382-1392 (2012).
29. Ledermann, J. et al. Olaparib maintenance therapy in patients with platinum-sensitive relapsed serous ovarian cancer: a preplanned retrospective analysis of outcomes by BRCA status in a randomised phase 2 trial. Lancet Oncol. 15, 852-861 (2014).
30. Mirza, M.R. et al. Niraparib maintenance therapy in platinum-sensitive, recurrent ovarian cancer. N. Engl. J. Med. 375, 2154-2164 (2016).
31. Swisher, E.M. et al. Rucaparib in relapsed, platinum-sensitive high-grade ovarian carcinoma (ARIEL2 Part 1): an international, multicentre, open-label, phase 2 trial. Lancet Oncol. 18, 75-87 (2017).
32. Alexandrov, L.B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
33. Nik-Zainal, S. et al. Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979-993 (2012).
34. Campbell, P.J. et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467, 1109-1113 (2010).
35. Sudmant, P.H. et al. An integrated map of structural variation in 2,504 human genomes. Nature 526, 75-81 (2015).
36. Ng, C.K.Y. et al. The role of tandem duplicator phenotype in tumour evolution in high-grade serous ovarian cancer. J. Pathol. 226, 703-712 (2012).
37. Sasaki, S. et al. Molecular processes of chromosome 9p21 deletions in human cancers. Oncogene 22, 3792-3798 (2003).
38. Yang, L. et al. Diverse mechanisms of somatic structural variations in human cancer genomes. Cell 153, 919-929 (2013).
39. Hermetz, K.E. et al. Large inverted duplications in the human genome form via a fold-back mechanism. PLoS Genet. 10, e1004139 (2014).
40. Patch, A.-M. et al. Whole-genome characterization of chemoresistant ovarian cancer. Nature 521, 489-494 (2015).
41. Tothill, R.W. et al. Novel molecular subtypes of serous and endometrioid ovarian cancer linked to clinical outcome. Clin. Cancer Res. 14, 5198-5208 (2008).
42. Ottaviani, D., LeCain, M. & Sheer, D. The role of microhomology in genomic structural variation. Trends Genet. 30, 85-94 (2014).
43. Sfeir, A. & Symington, L.S. Microhomology-mediated end joining: a back-up survival mechanism or dedicated pathway? Trends Biochem. Sci. 40, 701-714 (2015).
44. Le'tourneau, I.J. et al. Derivation and characterization of matched cell lines from primary and recurrent serous ovarian cancer. BMC Cancer. 12 1 (2012).
45. Bashashati, A. et al. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J. Pathol. 231, 21-34 (2013).
46. Schwarz, R.F. et al. Spatial and temporal heterogeneity in high-grade serous ovarian cancer: a phylogenetic analysis. PLoS Med. 12, e1001789 (2015).
47. Mateos-Gomez, P.A. et al. Mammalian polymerase Θ promotes alternative NHEJ and suppresses recombination. Nature 518, 254-257 (2015).
48. Ceccaldi, R. et al. Homologous-recombination-deficient tumours are dependent on PolΘ-mediated repair. Nature 518, 258-262 (2015).
49. Le, D.T. et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372, 2509-2520 (2015).
50. Swanton, C., McGranahan, N., Starrett, G.J. & Harris, R.S. APOBEC enzymes: mutagenic fuel for cancer evolution and heterogeneity. Cancer Discov. 5, 704-712 (2015).
51. Taghiyar, M.J. et al. Kronos: a workflow assembler for genome analytics and informatics. Preprint at bioRxiv http://dx.doi.org/10.1101/040352 (2016).