Genomic analyses of gynaecologic carcinosarcomas reveal frequent mutations in chromatin remodelling genes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Jones, Siân ^a   Stransky, Nicolas ^b   McCord, Christine L ^a   Cerami, Ethan ^b   Lagowski, James ^c   Kelly, Devon ^c   Angiuoli, Samuel V ^a   Sausen, Mark ^a   Kann, Lisa ^a   Shukla, Manish ^a   Makar, Rosemary ^c   Wood, Laura D ^d   Diaz, Luis A ^e,f   Lengauer, Christoph ^b   Velculescu, Victor E ^e  

^a Personal Genome Diagnostics ^*  (United States)

^b Blueprint Medicines   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

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

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; K RAS PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; ARID1A PROTEIN, HUMAN; ARID1B PROTEIN, HUMAN; BAZ1A PROTEIN, HUMAN; CHROMATIN; DNA BINDING PROTEIN; MLL3 PROTEIN, HUMAN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SPOP PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

DNA; GENE EXPRESSION; GENOME; MUTATION; PHENOTYPE; PROTEIN; TUMOR;

ARTICLE; CANCER LOCALIZATION; CARCINOGENESIS; CARCINOSARCOMA; CHROMATIN; CLINICAL ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPAIR; EXOME; FEMALE; FRAMESHIFT MUTATION; GENE MUTATION; GENE SEQUENCE; GENOME ANALYSIS; GENOMICS; GYNECOLOGIC CANCER; HUMAN; HUMAN TISSUE; MICROSATELLITE INSTABILITY; MISMATCH REPAIR; MISSENSE MUTATION; MUTATION RATE; NEXT GENERATION SEQUENCING; NONSENSE MUTATION; NUCLEIC ACID BASE SUBSTITUTION; ONCOGENE K RAS; PERSONALIZED MEDICINE; PHENOTYPE; RECOMBINATION REPAIR; SOMATIC MUTATION; TUMOR SUPPRESSOR GENE; AGED; FEMALE GENITAL TRACT TUMOR; GENE LIBRARY; GENETICS; METABOLISM; MIDDLE AGED; MUTATION; NUCLEOTIDE SEQUENCE; ONCOGENE RAS; VERY ELDERLY;

AGED; AGED, 80 AND OVER; CARCINOSARCOMA; CHROMATIN; DNA MUTATIONAL ANALYSIS; DNA REPAIR; DNA-BINDING PROTEINS; EXOME; FEMALE; GENE LIBRARY; GENES, P53; GENES, RAS; GENITAL NEOPLASMS, FEMALE; GENOMICS; HUMANS; MIDDLE AGED; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHATIDYLINOSITOL 3-KINASES; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

EID: 84923110898     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6006     Document Type: Article

References (70)

1. Jin, Z. et al. Carcinosarcomas (malignant mullerian mixed tumors) of the uterus and ovary: a genetic study with special reference to histogenesis. Int. J. Gynecol. Pathol. 22, 368-373 (2003).
2. El-Nashar, S. A. & Mariani, A. Uterine carcinosarcoma. Clin. Obstet. Gynecol. 54, 292-304 (2011).
3. Ahuja, A., Safaya, R., Prakash, G., Kumar, L. & Shukla, N. K. Primary mixed mullerian tumor of the vagina-a case report with review of the literature. Pathol. Res. Pract. 207, 253-255 (2011).
4. Sharma, N. K., Sorosky, J. I., Bender, D., Fletcher, M. S. & Sood, A. K. Malignant mixed mullerian tumor (MMMT) of the cervix. Gynecol. Oncol. 97, 442-445 (2005).
5. Duman, B. B., Kara, I. O., Gunaldi, M. & Ercolak, V. Malignant mixed Mullerian tumor of the ovary with two cases and review of the literature. Arch. Gynecol. Obstet. 283, 1363-1368 (2011).
6. Shen, Y. M. et al. Malignant mixed mullerian tumor of the fallopian tube: report of two cases and review of literature. Arch. Gynecol. Obstet. 281, 1023-1028 (2010).
7. Rajanbabu, A., Zahoor, A. S., Vijajkumar, D. K., Pavithran, K. & Kuriakose, S. The significance of the site of origin in primary peritoneal carcinosarcoma: case report and literature review. Ecancermedicalscience 7, 295 (2013).
8. George, E. M. et al. Carcinosarcoma of the ovary: natural history, patterns of treatment, and outcome. Gynecol. Oncol. 131, 42-45 (2013).
9. Kanthan, R. & Senger, J. L. Uterine carcinosarcomas (malignant mixed mullerian tumours): a review with special emphasis on the controversies in management. Obstet. Gynecol. Int. 2011, 470795 (2011).
10. Kernochan, L. E. & Garcia, R. L. Carcinosarcomas (malignant mixed Mullerian tumor) of the uterus: advances in elucidation of biologic and clinical characteristics. J. Natl Compr. Canc. Netw. 7, 550-556 quiz 557 (2009).
11. Meredith, R. F. et al. An excess of uterine sarcomas after pelvic irradiation. Cancer 58, 2003-2007 (1986).
12. Curtis, R. E., Freedman, D. M., Sherman, M. E. & Fraumeni, Jr J. F. Risk of malignant mixed mullerian tumors after tamoxifen therapy for breast cancer. J. Natl Cancer Inst. 96, 70-74 (2004).
13. Callister, M., Ramondetta, L. M., Jhingran, A., Burke, T. W. & Eifel, P. J. Malignant mixed Mullerian tumors of the uterus: analysis of patterns of failure, prognostic factors, and treatment outcome. Int. J. Radiat. Oncol. Biol. Phys. 58, 786-796 (2004).
14. Armstrong, A. B. et al. TP53 mutational analysis supports monoclonal origin of biphasic sarcomatoid urothelial carcinoma (carcinosarcoma) of the urinary bladder. Mod. Pathol. 22, 113-118 (2009).
15. Growdon, W. B. et al. Tissue-specific signatures of activating PIK3CA and RAS mutations in carcinosarcomas of gynecologic origin. Gynecol. Oncol. 121, 212-217 (2011).
16. de Jong, R. A. et al. Molecular markers and clinical behavior of uterine carcinosarcomas: focus on the epithelial tumor component. Mod. Pathol. 24, 1368-1379 (2011).
17. South, S. A., Hutton, M., Farrell, C., Mhawech-Fauceglia, P. & Rodabaugh, K. J. Uterine carcinosarcoma associated with hereditary nonpolyposis colorectal cancer. Obstet. Gynecol. 110, 543-545 (2007).
18. Jones, S. et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 330, 228-231 (2010).
19. Cancer Genome Atlas Research, N. Integrated genomic analyses of ovarian carcinoma. Nature 474, 609-615 (2011).
20. 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).
21. Jones, S. et al. Low-grade serous carcinomas of the ovary contain very few point mutations. J. Pathol. 226, 413-420 (2012).
22. Parsons, D. W. et al. The genetic landscape of the childhood cancer medulloblastoma. Science 331, 435-439 (2011).
23. Sausen, M. et al. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat. Genet. 45, 12-17 (2013).
24. Cancer Genome Atlas Research Network et al. Integrated genomic characterization of endometrial carcinoma. Nature 497, 67-73 (2013).
25. Pfeifer, G. P. Mutagenesis at methylated CpG sequences. Curr. Top. Microbiol. Immunol. 301, 259-281 (2006).
26. Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
27. Pena-Diaz, J. et al. Noncanonical mismatch repair as a source of genomic instability in human cells. Mol. Cell 47, 669-680 (2012).
28. Ni, T. T., Marsischky, G. T. & Kolodner, R. D. MSH2 and MSH6 are required for removal of adenine misincorporated opposite 8-oxo-guanine in S. cerevisiae. Mol. Cell 4, 439-444 (1999).
29. Wiegand, K. C. et al. ARID1A mutations in endometriosis-associated ovarian carcinomas. N. Engl. J. Med. 363, 1532-1543 (2010).
30. Jones, S. et al. Somatic mutations in the chromatin remodeling gene ARID1A occur in several tumor types. Hum. Mutat. 33, 100-103 (2012).
31. 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).
32. Stephens, P. J. et al. The landscape of cancer genes and mutational processes in breast cancer. Nature 486, 400-404 (2012).
33. Jones, D. T. et al. Dissecting the genomic complexity underlying medulloblastoma. Nature 488, 100-105 (2012).
34. Pugh, T. J. et al. Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106-110 (2012).
35. Kim, Y. et al. Integrative and comparative genomic analysis of lung squamous cell carcinomas in east asian patients. J. Clin. Oncol. 32, 121-128 (2013).
36. Bea, S. et al. Landscape of somatic mutations and clonal evolution in mantle cell lymphoma. Proc. Natl Acad. Sci. USA 110, 18250-18255 (2013).
37. Le Gallo, M. et al. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat. Genet. 44, 1310-1315 (2012).
38. Berger, M. F. et al. The genomic complexity of primary human prostate cancer. Nature 470, 214-220 (2011).
39. Kan, Z. et al. Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466, 869-873 (2010).
40. Kim, M. S., Je, E. M., Oh, J. E., Yoo, N. J. & Lee, S. H. Mutational and expressional analyses of SPOP, a candidate tumor suppressor gene, in prostate, gastric and colorectal cancers. APMIS 121, 626-633 (2013).
41. Hollenbach, A. D., McPherson, C. J., Mientjes, E. J., Iyengar, R. & Grosveld, G. Daxx and histone deacetylase II associate with chromatin through an interaction with core histones and the chromatin-associated protein Dek. J. Cell. Sci. 115, 3319-3330 (2002).
42. Racki, L. R. et al. The chromatin remodeller ACF acts as a dimeric motor to space nucleosomes. Nature 462, 1016-1021 (2009).
43. Krill-Burger, J. M. et al. Renal cell neoplasms contain shared tumor typespecific copy number variations. Am. J. Pathol. 180, 2427-2439 (2012).
44. 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).
45. Rahman, M. et al. PPP2R1A mutation is a rare event in ovarian carcinoma across histological subtypes. Anticancer Res. 33, 113-118 (2013).
46. Moroney, J. et al. Phase I study of the antiangiogenic antibody bevacizumab and the mTOR/hypoxia-inducible factor inhibitor temsirolimus combined with liposomal doxorubicin: tolerance and biological activity. Clin. Cancer Res. 18, 5796-5805 (2012).
47. Fu, S. et al. Perifosine plus docetaxel in patients with platinum and taxane resistant or refractory high-grade epithelial ovarian cancer. Gynecol. Oncol. 126, 47-53 (2012).
48. Seront, E. et al. Phase II study of everolimus in patients with locally advanced or metastatic transitional cell carcinoma of the urothelial tract: clinical activity, molecular response, and biomarkers. Ann. Oncol. 23, 2663-2670 (2012).
49. Slomovitz, B. M. et al. A phase 2 study of the oral mammalian target of rapamycin inhibitor, everolimus, in patients with recurrent endometrial carcinoma. Cancer 116, 5415-5419 (2010).
50. Jaiswal, B. S. et al. Oncogenic ERBB3 mutations in human cancers. Cancer Cell 23, 603-617 (2013).
51. Garnett, M. J. et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 483, 570-575 (2012).
52. Pennington, K. P. et al. Germline and somatic mutations in homologous recombination genes predict platinum response and survival in ovarian, fallopian tube, and peritoneal carcinomas. Clin. Cancer Res. 20, 764-775 (2013).
53. Villarroel, M. C. et al. Personalizing cancer treatment in the age of global genomic analyses: PALB2 gene mutations and the response to DNA damaging agents in pancreatic cancer. Mol. Cancer Ther. 10, 3-8 (2011).
54. Williamson, C. T. et al. Enhanced cytotoxicity of PARP inhibition in mantle cell lymphoma harbouring mutations in both ATM and p53. EMBO Mol. Med. 4, 515-527 (2012).
55. Wang, X. et al. Two related ARID family proteins are alternative subunits of human SWI/SNF complexes. Biochem. J. 383, 319-325 (2004).
56. Wilson, B. G. & Roberts, C. W. SWI/SNF nucleosome remodellers and cancer. Nat. Rev. Cancer 11, 481-492 (2011).
57. Weissman, B. & Knudsen, K. E. Hijacking the chromatin remodeling machinery: impact of SWI/SNF perturbations in cancer. Cancer Res. 69, 8223-8230 (2009).
58. Caramel, J., Quignon, F. & Delattre, O. RhoA-dependent regulation of cell migration by the tumor suppressor hSNF5/INI1. Cancer Res. 68, 6154-6161 (2008).
59. Lee, J. et al. A tumor suppressive coactivator complex of p53 containing ASC-2 and histone H3-lysine-4 methyltransferase MLL3 or its paralogue MLL4. Proc. Natl Acad. Sci. USA 106, 8513-8518 (2009).
60. Ansari, K. I. & Mandal, S. S. Mixed lineage leukemia: roles in gene expression, hormone signaling and mRNA processing. FEBS J. 277, 1790-1804 (2010).
61. Sierra, J., Yoshida, T., Joazeiro, C. A. & Jones, K. A. The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 20, 586-600 (2006).
62. Kwon, J. E. et al. BTB domain-containing speckle-type POZ protein (SPOP) serves as an adaptor of Daxx for ubiquitination by Cul3-based ubiquitin ligase. J. Biol. Chem. 281, 12664-12672 (2006).
63. Jiao, Y. et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 331, 1199-1203 (2011).
64. Jiao, Y. et al. Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas. Oncotarget 3, 709-722 (2012).
65. Amant, F. et al. PTEN mutations in uterine sarcomas. Gynecol. Oncol. 85, 165-169 (2002).
66. Lancaster, J. M., Risinger, J. I., Carney, M. E., Barrett, J. C. & Berchuck, A. Mutational analysis of the PTEN gene in human uterine sarcomas. Am. J. Obstet. Gynecol. 184, 1051-1053 (2001).
67. Risinger, J. I., Hayes, A. K., Berchuck, A. & Barrett, J. C. PTEN/MMAC1 mutations in endometrial cancers. Cancer Res. 57, 4736-4738 (1997).
68. Barretina, J. et al. Subtype-specific genomic alterations define new targets for soft-tissue sarcoma therapy. Nat. Genet. 42, 715-721 (2010).
69. Bettegowda, C. et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci. Transl. Med. 6, 224ra24 (2014).
70. Haber, D. A. et al. Blood-Based Analyses of Cancer: Circulating Tumor Cells and Circulating Tumor DNA. Cancer Discov 4, 650-661 (2014).