BRCA1/2 mutation analysis in 41 ovarian cell lines reveals only one functionally deleterious BRCA1 mutation

Molecular Oncology

Volumn 7, Issue 3, 2013, Pages 567-579

  Stordal, Britta ^a   Timms, Kirsten ^b   Farrelly, Angela ^c   Gallagher, Danielle ^c   Busschots, Steven ^a   Renaud, Mickaël ^c   Thery, Julien ^a   Williams, Deborah ^b   Potter, Jennifer ^b   Tran, Thanh ^b   Korpanty, Greg ^d   Cremona, Mattia ^c   Carey, Mark ^e   Li, Jie ^e   Li, Yang ^e   Aslan, Ozlem ^c   O'Leary, John J ^a   Mills, Gordon B ^e   Hennessy, Bryan T ^c,d,e  

^a ST JAMES S HOSPITAL   (Ireland)

^b Utah   (United States)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d BEAUMONT HOSPITAL   (Ireland)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

BRCA1 2; Methylation; Mutation; Olaparib; Ovarian; Parp inhibitor; Veliparib

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; MESSENGER RNA; OLAPARIB; VELIPARIB;

ARTICLE; CANCER CELL; CLINICAL ARTICLE; COMPARATIVE STUDY; DRUG CYTOTOXICITY; FEMALE; GENE DELETION; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; HUMAN; HUMAN CELL; OVARY CANCER; OVARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN METHYLATION; WILD TYPE;

EID: 84878108726     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.12.007     Document Type: Article

References (74)

1. Anonymous A2780 ECACC Datasheet 2012, http://www.hpacultures.org.uk.
2. Anonymous CRL-1978™ (ES-2) ATCC Datasheet 2012, http://www.lgcstandards-atcc.org.
3. Anonymous HTB-75™ (CAOV3) ATCC Datasheet 2012, http://www.lgcstandards-atcc.org.
4. Anonymous HTB-78™ (SW626) ATCC Datasheet 2012, http://www.lgcstandards-atcc.org/.
5. Anonymous Prevalence and penetrance of BRCA1 and BRCA2 mutations in a population-based series of breast cancer cases. Anglian breast cancer study group. British Journal of Cancer 2000, 83:1301-1308.
6. Aaronson S.A. Personal Communication 2012.
7. Alama A., Barbieri F., Favre A., et al. Establishment and characterization of three new cell lines derived from the ascites of human ovarian carcinomas. Gynecologic Oncology 1996, 62:82-88.
8. Audeh M.W., Carmichael J., Penson R.T., et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet 2010, 376:245-251.
9. Baldwin R.L., Nemeth E., Tran H., et al. BRCA1 promoter region hypermethylation in ovarian carcinoma: a population-based study. Cancer Research 2000, 60:5329-5333.
10. Bauer K.R., Brown M., Cress R.D., et al. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype. Cancer 2007, 109:1721-1728.
11. Benard J., Da Silva J., De Blois M.C., et al. Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice. Cancer Research 1985, 45:4970-4979.
12. Berchuck A., Heron K.A., Carney M.E., et al. Frequency of germline and somatic BRCA1 mutations in ovarian cancer. Clinical Cancer Research 1998, 4:2433-2437.
13. Bryant H.E., Schultz N., Thomas H.D., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 2005, 434:913-917.
14. Buick R.N., Pullano R., Trent J.M. Comparative properties of five human ovarian adenocarcinoma cell lines. Cancer Research 1985, 45:3668-3676.
15. Casalini P., Botta L., Menard S. Role of p53 in HER2-induced proliferation or apoptosis. Journal of Biological Chemistry 2001, 276:12449-12453.
16. Choi J.H., Choi K.C., Auersperg N., et al. Gonadotropins upregulate the epidermal growth factor receptor through activation of mitogen-activated protein kinases and phosphatidyl-inositol-3-kinase in human ovarian surface epithelial cells. Endocrine-related Cancer 2005, 12:407-421.
17. Colombo N., Peiretti M., Castiglione M., et al. Non-epithelial ovarian cancer: ESMO Clinical Recommendations for diagnosis, treatment and follow-up. Annals of Oncology 2009, 20:iv24-iv26.
18. Colombo N., Peiretti M., Parma G., et al. Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Annals of Oncology 2010, 21:v23-v30.
19. Cooke S.L., Ng C.K.Y., Melnyk N., et al. Genomic analysis of genetic heterogeneity and evolution in high-grade serous ovarian carcinoma. Oncogene 2010, 29:4905-4913.
20. Cruet-Hennequart S., Maubant S., Luis J., et al. [Alpha]v integrins regulate cell proliferation through integrin-linked kinase (ILK) in ovarian cancer cells. Oncogene 2003, 22:1688-1702.
21. DelloRusso C., Welcsh P.L., Wang W., et al. Functional characterization of a novel BRCA1-null ovarian cancer cell line in response to ionizing radiation. Molecular Cancer Research: MCR 2007, 5:35-45.
22. Elstrodt F., Hollestelle A., Nagel J.H., et al. BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants. Cancer Research 2006, 66:41-45.
23. Emoto M., Oshima K., Ishiguro M., et al. Establishment and characterization of a serous papillary adenocarcinoma cell line of the human ovary in a serum-free culture. Pathology - Research and Practice 1999, 195:238-243.
24. Fajac A., Da Silva J., Ahomadegbe J.C., et al. Cisplatin-induced apoptosis and p53 gene status in a cisplatin-resistant human ovarian carcinoma cell line. International Journal of Cancer 1996, 68:67-74.
25. Farmer H., McCabe N., Lord C.J., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
26. Filmus J., Trent J.M., Pullano R., et al. A cell line from a human ovarian carcinoma with amplification of the K-ras gene. Cancer Research 1986, 46:5179-5182.
27. Filmus J.E., Buick R.N. Stability of c-K-ras amplification during progression in a patient with adenocarcinoma of the ovary. Cancer Research 1985, 45:4468-4472.
28. Foray N., Randrianarison V., Marot D., et al. Gamma-rays-induced death of human cells carrying mutations of BRCA1 or BRCA2. Oncogene 1999, 18:7334-7342.
29. Foulkes W.D., Metcalfe K., Sun P., et al. Estrogen receptor status in BRCA1- and BRCA2-related breast cancer. Clinical Cancer Research 2004, 10:2029-2034.
30. Furlong M.T., Hough C.D., Sherman-Baust C.A., et al. Evidence for the colonic origin of ovarian cancer cell line SW626. Journal of the National Cancer Institute 1999, 91:1327-1328.
31. Hamilton T.C. Personal Communication 2012.
32. Hamilton T.C., Young R.C., McKoy W.M., et al. Characterization of a human ovarian carcinoma cell line (NIH: OVCAR-3) with androgen and estrogen receptors. Cancer Research 1983, 43:5379-5389.
33. Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Molecular Oncology 2011, 5:387-393.
34. Hennessy B.T., Timms K.M., Carey M.S., et al. Somatic mutations in BRCA1 and BRCA2 could expand the number of patients that benefit from poly (ADP ribose) polymerase inhibitors in ovarian cancer. Journal of Clinical Oncology 2010, 28:3570-3576.
35. Hills C.A., Kelland L.R., Abel G., et al. Biological properties of ten human ovarian carcinoma cell lines: calibration in vitro against four platinum complexes. British. Journal of Cancer 1989, 59:527-534.
36. Kao J., Salari K., Bocanegra M., et al. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 2009, 4:e6146.
37. Kunzmann R., Hozel F. Karyotype alterations in human ovarian carcinoma cells during long-term cultivation and nude mouse passage. Cancer Genetics and Cytogenetics 1987, 28:201-212.
38. Lakhani S.R., Manek S., Penault-Llorca F., et al. Pathology of ovarian cancers in BRCA1 and BRCA2 carriers. Clinical Cancer Research 2004, 10:2473-2481.
39. Langdon S.P., Lawrie S.S., Hay F.G., et al. Characterization and properties of nine human ovarian adenocarcinoma cell lines. Cancer Research 1988, 48:6166-6172.
40. Li X., Delzer J., Voorman R., et al. Disposition and drug-drug interaction potential of veliparib (ABT-888), a novel and potent inhibitor of poly(ADP-ribose) polymerase. Drug Metabolism and Disposition 2011, 39:1161-1169.
41. Liang Y., McDonnell S., Clynes M. Examining the relationship between cancer invasion/metastasis and drug resistance. Current Cancer Drug Targets 2002, 2:257-277. [Review] [134 refs].
42. Mackillop W.J., Trent J.M., Stewart S.S., et al. Tumor progression studied by analysis of cellular features of serial Ascitic ovarian carcinoma tumors. Cancer Research 1983, 43:874-878.
43. Martin A., Clynes M. Comparison of 5 microplate colorimetric assays for in vitro cytotoxicity testing and cell proliferation assays. Cytotechnology 1993, 11:49-58.
44. Martins F.C., De S., Almendro V., et al. Evolutionary pathways in BRCA1-associated breast tumors. Cancer Discovery 2012, 2:503-511.
45. Merkel D.E., Fuqua S.A., Tandon A.K., et al. Electrophoretic analysis of 248 clinical breast cancer specimens for P-glycoprotein overexpression or gene amplification. Journal of Clinical Oncology 1989, 7:1129-1136.
46. National Cancer Institute EER Cancer Statistics Review 1975-2007. Lifetime Risk (Percent) of Dying from Cancer by Site and Race/Ethnicity: Males, Total US, 2005-2007 (Table 1.18) and Females, Total US, 2005-2007 (Table 1.19) 2010, http://seer.cancer.gov/csr/1975_2007/results_merged/topic_lifetime_risk_death.pdf.
47. Newman B., Mu H., Butler L.M., et al. Frequency of breast cancer attributable to BRCA1 in a population-based series of American women. JAMA 1998, 279:915-921.
48. Nieuwenhuis B., Assen-Bolt A.J.V., Van Waarde-Verhagen W.H., et al. BRCA1 and BRCA2 heterozygosity and repair of X-ray-induced DNA damage. International Journal of Radiation Oncology Biology 2002, 78:285-295.
49. Pal T., Permuth-Wey J., Betts J.A., et al. BRCA1 and BRCA2 mutations account for a large proportion of ovarian carcinoma cases. Cancer 2005, 104:2807-2816.
50. Papelard H., De Bock G.H., van Eijk R., et al. Prevalence of BRCA1 in a hospital-based population of Dutch breast cancer patients. British Journal of Cancer 2000, 83:719-724.
51. Pohl G., Ho C.L., Kurman R.J., et al. Inactivation of the mitogen-activated protein kinase pathway as a potential target-based therapy in ovarian serous tumors with KRAS or BRAF mutations. Cancer Research 2005, 65:1994-2000.
52. Risch H.A., McLaughlin J.R., Cole D.E., et al. Prevalence and penetrance of germline BRCA1 and BRCA2 mutations in a population series of 649 women with ovarian cancer. American Journal of Human Genetics 2001, 68:700-710.
53. Rottenberg S., Jaspers J.E., Kersbergen A., et al. High sensitivity of BRCA1-deficient mammary tumors to the PARP inhibitor AZD2281 alone and in combination with platinum drugs. Proceedings of the National Academy of Sciences U S A 2008, 105:17079-17084.
54. Rouleau M., Patel A., Hendzel M.J., et al. PARP inhibition: PARP1 and beyond. Nature Reviews Cancer 2010, 10:293-301.
55. Rubin S.C., Blackwood M.A., Bandera C., et al. BRCA1, BRCA2, and hereditary nonpolyposis colorectal cancer gene mutations in an unselected ovarian cancer population: relationship to family history and implications for genetic testing. American Journal of Obstetrics and Gynecology 1998, 178:670-677.
56. Russell P.A., Pharoah P.D., De Foy K., et al. Frequent loss of BRCA1 mRNA and protein expression in sporadic ovarian cancers. International Journal of Cancer 2000, 87:317-321.
57. Sakai W., Swisher E.M., Karlan B.Y., et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature 2008, 451:1116-1120. [see comment].
58. Sakai W., Swisher E.M., Jacquemont C., et al. Functional Restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Research 2009, 69:6381-6386.
59. Schilder R.J., Hall L., Monks A., et al. Metallothionein gene expression and resistance to cisplatin in human ovarian cancer. International Journal of Cancer 1990, 45:416-422.
60. Sikic B.I. Personal Communication 2012.
61. Sood A.K., Fletcher M.S., Gruman L.M., et al. The paradoxical expression of maspin in ovarian carcinoma. Clinical Cancer Research 2002, 8:2924-2932.
62. Stronach E.A., Alfraidi A., Rama N., et al. HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Research 2011, 71:4412-4422.
63. Swisher E.M., Sakai W., Karlan B.Y., et al. Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance. Cancer Research 2008, 68:2581-2586.
64. Syed V., Ulinski G., Mok S.C., et al. Expression of gonadotropin receptor and growth responses to key reproductive hormones in normal and malignant human ovarian surface epithelial cells. Cancer Research 2001, 61:6768-6776.
65. Timms K.M. Personal Communication 2011.
66. Tung N., Miron A., Schnitt S., et al. Prevalence and predictors of loss of wild type BRCA1 in estrogen receptor positive and negative BRCA1-associated breast cancers. Breast Cancer Research 2010, 12:R95.
67. Tung N., Wang Y., Collins L., et al. Estrogen receptor positive breast cancers in BRCA1 mutation carriers: clinical risk factors and pathologic features. Breast Cancer Research 2010, 12:R12.
68. Tutt A., Robson M., Garber J.E., et al. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-of-concept trial. The Lancet 2010, 376:235-244.
69. Warren M., Lord C.J., Masabanda J., et al. Phenotypic effects of heterozygosity for a BRCA2 mutation. Human Molecular Genetics 2003, 12:2645-2656.
70. Wong A.S.T., Roskelley C.D., Pelech S., et al. Progressive changes in Met-dependent signaling in a human ovarian surface epithelial model of malignant transformation. Experimental Cell Research 2004, 299:248-256.
71. Wong W.S.F., Wong Y.F., Ng Y.T.A., et al. Establishment and characterization of a new human cell line derived from ovarian clear cell carcinoma. Gynecologic Oncology 1990, 38:37-45.
72. Young T.N., Pizzo S.V., Stack M.S. A plasma membrane-associated component of ovarian adenocarcinoma cells enhances the catalytic efficiency of matrix metalloproteinase-2. Journal of Biological Chemistry 1995, 270:999-1002.
73. Yuan Y., Kim W.H., Han H.S., et al. Establishment and characterization of human ovarian carcinoma cell lines. Gynecologic. Oncology 1997, 66:378-387.
74. Yu J., Roy D., Brockmeyer A.D., et al. Increased chromosomal stability in cultures of ovarian tumours of low malignant potential compared to cystadenomas. British Journal of Cancer 2007, 96:1908-1913.