TP53 mutations, tetraploidy and homologous recombination repair defects in early stage high-grade serous ovarian cancer

Nucleic Acids Research

Volumn 43, Issue 14, 2015, Pages 6945-6958

  Chien, Jeremy ^a   Sicotte, Hugues ^b   Fan, Jian Bing ^c   Humphray, Sean ^c   Cunningham, Julie M ^b   Kalli, Kimberly R ^b   Oberg, Ann L ^b   Hart, Steven N ^b   Li, Ying ^b   Davila, Jaime I ^b   Baheti, Saurabh ^b   Wang, Chen ^b   Dietmann, Sabine ^d   Atkinson, Elizabeth J ^b   Asmann, Yan W ^e   Bell, Debra A ^b   Ota, Takayo ^f   Tarabishy, Yaman ^g   Kuang, Rui ^h   Bibikova, Marina ^c   Cheetham, R Keira ^c   Grocock, Russell J ^c   Swisher, Elizabeth M ⁱ   Peden, John ^c   Bentley, David ^c   Kocher, Jean Pierre A ^b   Kaufmann, Scott H ^b   Hartmann, Lynn C ^b   Shridhar, Viji ^b   Goode, Ellen L ^b   more..

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

^b MAYO CLINIC   (United States)

^c ILLUMINA INC   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e MAYO CLINIC   (United States)

^f Department of Cardiology   (Japan)

^g WASHINGTON UNIVERSITY   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

ⁱ UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; CYTOSINE; PROTEIN P53; THYMINE; DNA PRIMASE; DNA PRIMASE P58 SUBUNIT, HUMAN;

ARTICLE; CONTROLLED STUDY; CPG ISLAND; DISORDERS OF DNA SYNTHESIS AND REPAIR; FEMALE; FRAMESHIFT MUTATION; GENE DELETION; GENE DOSAGE; GENE FREQUENCY; GENE INACTIVATION; GENE MUTATION; GENE SEQUENCE; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOSITY LOSS; HIGH GRADE SEROUS OVARIAN CANCER; HOMOLOGOUS RECOMBINATION REPAIR DEFECT; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; NUCLEIC ACID BASE SUBSTITUTION; OVARY CANCER; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; TETRAPLOIDY; TUMOR SUPPRESSOR GENE; CARCINOMA; GENETICS; MUTATION; MUTATION RATE; OVARY TUMOR; RECOMBINATION REPAIR;

CARCINOMA; DNA PRIMASE; FEMALE; GENES, P53; HUMANS; LOSS OF HETEROZYGOSITY; MUTATION; MUTATION RATE; OVARIAN NEOPLASMS; RECOMBINATIONAL DNA REPAIR; TETRAPLOIDY;

EID: 84940202151     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv111     Document Type: Article

References (54)

1. Jemal,A., Bray,F., Center,M.M., Ferlay,J., Ward,E. and Forman,D. (2011) Global cancer statistics. CA Cancer J. Clin., 61, 69-90.
2. Bell,D.A. (2005) Origins and molecular pathology of ovarian cancer. Mod. Pathol., 18, S19-S32.
3. Shih Ie,M. and Kurman,R.J. (2004) Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am. J. Pathol., 164, 1511-1518.
4. Chan,J.K., Cheung,M.K., Husain,A., Teng,N.N., West,D., Whittemore,A.S., Berek,J.S. and Osann,K. (2006) Patterns and progress in ovarian cancer over 14 years. Obstet. Gynecol., 108, 521-528.
5. Seidman,J.D. and Chauhan,S. (2002) Evaluation of the relationship between adenosarcoma and carcinosarcoma and a hypothesis of the histogenesis of uterine sarcomas. Int. J. Gynecol. Pathol., 22, 75-82.
6. Cancer Genome Atlas Research Network. (2011) Integrated genomic analyses of ovarian carcinoma. Nature, 474, 609-615.
7. Li,H. and Durbin,R. (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics, 25, 1754-1760.
8. 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.
9. Larson,D.E., Harris,C.C., Chen,K., Koboldt,D.C., Abbott,T.E., Dooling,D.J., Ley,T.J., Mardis,E.R., Wilson,R.K. and Ding,L. (2012) SomaticSniper: identification of somatic point mutations in whole genome sequencing data. Bioinformatics, 28, 311-317.
10. Asmann,Y.W., Middha,S., Hossain,A., Baheti,S., Li,Y., Chai,H.S., Sun,Z., Duffy,P.H., Hadad,A.A., Nair,A. et al. (2012) TREAT: a bioinformatics tool for variant annotations and visualizations in targeted and exome sequencing data. Bioinformatics, 28, 277-278.
11. Dees,N.D., Zhang,Q., Kandoth,C., Wendl,M.C., Schierding,W., Koboldt,D.C., Mooney,T.B., Callaway,M.B., Dooling,D., Mardis,E.R. et al. (2012) MuSiC: identifying mutational significance in cancer genomes. Genome Res., 22, 1589-1598.
12. Trapnell,C., Pachter,L. and Salzberg,S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
13. Anders,S., Pyl,P.T. and Huber,W. (2014) HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics, 2012, 1-4.
14. Horaitis,O., Talbot,C.C. Jr, Phommarinh,M., Phillips,K.M. and Cotton,R.G. (2007) A database of locus-specific databases. Nat. Genet., 39, 425.
15. Ota,T., Clayton,A.C., Minot,D.M., Shridhar,V., Hartmann,L.C., Gilks,C.B. and Chien,J.R. (2011) Minichromosome maintenance protein 7 as a potential prognostic factor for progression-free survival in high-grade serous carcinomas of the ovary. Mod. Pathol., 24, 277-287.
16. Wang,C., Evans,J.M., Bhagwate,A.V., Prodduturi,N., Sarangi,V., Middha,M., Sicotte,H., Vedell,P.T., Hart,S.N., Oliver,G.R. et al. (2014) PatternCNV: a versatile tool for detecting copy number changes from exome sequencing data. Bioinformatics, 30, 2678-2680.
17. Sun,W., Wright,F.A., Tang,Z., Nordgard,S.H., Loo,P.V., Yu,T., Kristensen,V.N. and Perou,C.M. (2009) Integrated study of copy number states and genotype calls using high-density SNP arrays. Nucleic Acids Res., 37, 5365-5377.
18. Holt,C., Losic,B., Pai,D., Zhao,Z., Trinh,Q., Syam,S., Arshadi,N., Jang,G.H., Ali,J., Beck,T. et al. (2014) WaveCNV: allele-specific copy number alterations in primary tumors and xenograft models from next-generation sequencing. Bioinformatics, 30, 768-774.
19. Wang,Z.C., Birkbak,N.J., Culhane,A.C., Drapkin,R., Fatima,A., Tian,R., Schwede,M., Alsop,K., Daniels,K.E., Piao,H. et al. (2012) Profiles of genomic instability in high-grade serous ovarian cancer predict treatment outcome. Clin. Cancer Res., 18, 5806-5815.
20. Skirnisdottir,I., Mayrhofer,M., Rydaker,M., Akerud,H. and Isaksson,A. (2012) Loss-of-heterozygosity on chromosome 19q in early-stage serous ovarian cancer is associated with recurrent disease. BMC Cancer, 12, 407.
21. Peng,G., Chun-Jen Lin,C., Mo,W., Dai,H., Park,Y.Y., Kim,S.M., Peng,Y., Mo,Q., Siwko,S., Hu,R. et al. (2014) Genome-wide transcriptome profiling of homologous recombination DNA repair. Nat. Commun., 5, 3361.
22. Wang,J., Mullighan,C.G., Easton,J., Roberts,S., Heatley,S.L., Ma,J., Rusch,M.C., Chen,K., Harris,C.C., Ding,L. et al. (2011) CREST maps somatic structural variation in cancer genomes with base-pair resolution. Nat. Methods, 8, 652-654.
23. Kandoth,C., Schultz,N., Cherniack,A.D., Akbani,R., Liu,Y., Shen,H., Robertson,A.G., Pashtan,I., Shen,R., Benz,C.C. et al. (2013) Integrated genomic characterization of endometrial carcinoma. Nature, 497, 67-73.
24. Church,D.N., Briggs,S.E., Palles,C., Domingo,E., Kearsey,S.J., Grimes,J.M., Gorman,M., Martin,L., Howarth,K.M., Hodgson,S.V. et al. (2013) DNA polymerase epsilon and delta exonuclease domain mutations in endometrial cancer. Hum. Mol. Genet., 22, 2820-2828.
25. Cancer Genome Atlas Network. (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature, 487, 330-337.
26. Jones,S., Wang,T.-L., Shih,I.-M., Mao,T.-L., Nakayama,K., Roden,R., Glas,R., Slamon,D., Diaz,L.A., Vogelstein,B. et al. (2010) Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science, 330, 228-231.
27. Lawrence,M.S., Stojanov,P., Polak,P., Kryukov,G.V., Cibulskis,K., Sivachenko,A., Carter,S.L., Stewart,C., Mermel,C.H., Roberts,S.A. et al. (2013) Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature, 499, 214-218.
28. Laird,P.W. and Jaenisch,R. (1994) DNA methylation and cancer. Hum. Mol. Genet., 3, 1487-1495.
29. Alexandrov,L.B., Nik-Zainal,S., Wedge,D.C., Aparicio,S.A., Behjati,S., Biankin,A.V., Bignell,G.R., Bolli,N., Borg,A., Borresen-Dale,A.L. et al. (2013) Signatures of mutational processes in human cancer. Nature, 500, 415-421.
30. Thorvaldsdottir,H., Robinson,J.T. and Mesirov,J.P. (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform., 14, 178-192.
31. Robinson,J.T., Thorvaldsdottir,H., Winckler,W., Guttman,M., Lander,E.S., Getz,G. and Mesirov,J.P. (2011) Integrative genomics viewer. Nat. Biotechnol., 29, 24-26.
32. Vogelstein,B. and Kinzler,K.W. (2004) Cancer genes and the pathways they control. Nat. Med., 10, 789-799.
33. Ahmed,A.A., Etemadmoghadam,D., Temple,J., Lynch,A.G., Riad,M., Sharma,R., Stewart,C., Fereday,S., Caldas,C., Defazio,A. et al. (2010) Driver mutations in TP53 are ubiquitous in high grade serous carcinoma of the ovary. J. Pathol., 221, 49-56.
34. Kindelberger,D.W., Lee,Y., Miron,A., Hirsch,M.S., Feltmate,C., Medeiros,F., Callahan,M.J., Garner,E.O., Gordon,R.W., Birch,C. et al. (2007) Intraepithelial carcinoma of the fimbria and pelvic serous carcinoma: evidence for a causal relationship. Am. J. Surg. Pathol., 31, 161-169.
35. Abkevich,V., Timms,K.M., Hennessy,B.T., Potter,J., Carey,M.S., Meyer,L.A., Smith-McCune,K., Broaddus,R., Lu,K.H., Chen,J. et al. (2012) Patterns of genomic loss of heterozygosity predict homologous recombination repair defects in epithelial ovarian cancer. Br. J. Cancer, 107, 1776-1782.
36. Somyajit,K., Subramanya,S. and Nagaraju,G. (2012) Distinct roles of FANCO/RAD51C protein in DNA damage signaling and repair: implications for Fanconi anemia and breast cancer susceptibility. J. Biol. Chem., 287, 3366-3380.
37. Huang,D.W., Sherman,B.T., Tan,Q., Collins,J.R., Alvord,W.G., Roayaei,J., Stephens,R., Baseler,M.W., Lane,H.C. and Lempicki,R.A. (2007) The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol., 8, R183.
38. Crum,C.P., Drapkin,R., Kindelberger,D., Medeiros,F., Miron,A. and Lee,Y. (2007) Lessons from BRCA: the tubal fimbria emerges as an origin for pelvic serous cancer. Clin.Med.Res., 5, 35-44.
39. Muller,P.A. and Vousden,K.H. (2014) Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell, 25, 304-317.
40. Lang,G.A., Iwakuma,T., Suh,Y.A., Liu,G., Rao,V.A., Parant,J.M., Valentin-Vega,Y.A., Terzian,T., Caldwell,L.C., Strong,L.C. et al. (2004) Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell, 119, 861-872.
41. Olive,K.P., Tuveson,D.A., Ruhe,Z.C., Yin,B., Willis,N.A., Bronson,R.T., Crowley,D. and Jacks,T. (2004) Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome. Cell, 119, 847-860.
42. Kang,H.J., Chun,S.M., Kim,K.R., Sohn,I. and Sung,C.O. (2013) Clinical relevance of gain-of-function mutations of p53 in high-grade serous ovarian carcinoma. PloS One, 8, e72609.
43. Bryant,H.E., Schultz,N., Thomas,H.D., Parker,K.M., Flower,D., Lopez,E., Kyle,S., Meuth,M., Curtin,N.J. and Helleday,T. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
44. Farmer,H., McCabe,N., Lord,C.J., Tutt,A.N., Johnson,D.A., Richardson,T.B., Santarosa,M., Dillon,K.J., Hickson,I., Knights,C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
45. Li,H. and Durbin,R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
46. Leonard,B., Hart,S.N., Burns,M.B., Carpenter,M.A., Temiz,N.A., Rathore,A., Vogel,R.I., Nikas,J.B., Law,E.K., Brown,W.L. et al. (2013) APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res., 73, 7222-7231.
47. Davis,E., Teng,H., Bilican,B., Parker,M.I., Liu,B., Carriera,S., Goding,C.R. and Prince,S. (2008) Ectopic Tbx2 expression results in polyploidy and cisplatin resistance. Oncogene, 27, 976-984.
48. Lassus,H., Staff,S., Leminen,A., Isola,J. and Butzow,R. (2011) Aurora-A overexpression and aneuploidy predict poor outcome in serous ovarian carcinoma. Gynecol. Oncol., 120, 11-17.
49. Storchova,Z., Breneman,A., Cande,J., Dunn,J., Burbank,K., O'Toole,E. and Pellman,D. (2006) Genome-wide genetic analysis of polyploidy in yeast. Nature, 443, 541-547.
50. Pradhan,M., Risberg,B.A., Trope,C.G., van de Rijn,M., Gilks,C.B. and Lee,C.H. (2010) Gross genomic alterations and gene expression profiles of high- grade serous carcinoma of the ovary with and without BRCA1 inactivation. BMC Cancer, 10, 493.
51. Lv,L., Zhang,T., Yi,Q., Huang,Y., Wang,Z., Hou,H., Zhang,H., Zheng,W., Hao,Q., Guo,Z. et al. (2012) Tetraploid cells from cytokinesis failure induce aneuploidy and spontaneous transformation of mouse ovarian surface epithelial cells. Cell Cycle, 11, 2864-2875.
52. Cancer Genome Atlas Research Network, Kandoth,C., Schultz,N., Cherniack,A.D., Akbani,R., Liu,Y., Shen,H., Robertson,A.G., Pashtan,I., Shen,R., Benz,C.C. et al. (2013) Integrated genomic characterization of endometrial carcinoma. Nature, 497, 67-73.
53. Ciriello,G., Miller,M.L., Aksoy,B.A., Senbabaoglu,Y., Schultz,N. and Sander,C. (2013) Emerging landscape of oncogenic signatures across human cancers. Nat. Genet., 45, 1127-1133.
54. Kobel,M., Kalloger,S.E., Boyd,N., McKinney,S., Mehl,E., Palmer,C., Leung,S., Bowen,N.J., Ionescu,D.N., Rajput,A. et al. (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med., 5, e232.