Impact of germline BRCA1 mutations and overexpression of p53 on prognosis and response to treatment following breast carcinoma: 10-Year follow-up data

Cancer

Volumn 97, Issue 3, 2003, Pages 527-536

  Goffin, John R ^a,g   Chappuis, Pierre O ^b,h   Bégin, Louis R ^a,i   Wong, Nora ^c   Brunet, Jean Sébastien ^a,d   Hamel, Nancy ^e   Paradis, Ann Josée ^c   Boyd, Jeff ^f   Foulkes, William D ^a,b,c,e,j  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d Algorithme Pharma   (Canada)

^e RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g DANA FARBER CANCER INSTITUTE   (United States)

^h GENEVA UNIVERSITY HOSPITALS   (Switzerland)

ⁱ HÔPITAL DU SACRÉ COEUR DE MONTRÉAL   (Canada)

^j MONTREAL GENERAL HOSPITAL   (Canada)

more..

Author keywords

Adjuvant chemotherapy; BRCA1; Breast neoplasms; Hereditary; Neoplastic syndromes; Prognosis; Protein p53; Tamoxifen

Indexed keywords

CISPLATIN; DOXORUBICIN; PACLITAXEL; PROTEIN P53; TAMOXIFEN;

ADULT; ARTICLE; BREAST CARCINOMA; CANCER ADJUVANT THERAPY; CANCER HORMONE THERAPY; CANCER MORTALITY; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; FOLLOW UP; GENE MUTATION; GENE OVEREXPRESSION; GERM LINE; HETEROZYGOTE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INVASIVE CARCINOMA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MULTIVARIATE ANALYSIS; ONCOGENE; PRIORITY JOURNAL; PROGNOSIS; STATISTICAL ANALYSIS;

ADULT; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; FEMALE; GENES, BRCA1; GENES, BRCA2; GERM-LINE MUTATION; HUMANS; IMMUNOHISTOCHEMISTRY; JEWS; LYMPHATIC METASTASIS; MIDDLE AGED; MULTIVARIATE ANALYSIS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; SURVIVAL ANALYSIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0037303255     PISSN: 0008543X     EISSN: None     Source Type: Journal    
DOI: 10.1002/cncr.11080     Document Type: Article

References (75)

1. National Cancer Institute of Canada. Canadian cancer statistics, 2001. Electronic citation available at URL http:// 66.59.133.166/stats/tables/table.htm. (Accessed 15 May 2002).
2. Kelsey JL, Berkowitz GS. Breast cancer epidemiology. Cancer Res. 1988;48:5615-5623.
3. Foulkes W, Rosenblatt J, Chappuis P. The contribution of inherited factors to the clinicopathological features and behaviour of breast cancer. J Mammary Gland Biol Neoplasia. 2001;6:453-462.
4. Blackwood MA, Weber BL. BRCA1 and BRCA2: from molecular genetics to clinical medicine. J Clin Oncol. 1998;16: 1969-1977.
5. Futreal PA, Liu Q, Shattuck-Eidens D, et al. BRCA1 mutations in primary breast and ovarian carcinomas. Science. 1994;266:120-122.
6. Niwa Y, Oyama T, Nakajima T. BRCA1 expression status in relation to DNA methylation of the BRCA1 promoter region in sporadic breast cancers. Jpn J Cancer Res. 2000;91:519-526.
7. Eisinger F, Stoppa-Lyonnet D, Longy M, et al. Germ line mutation at BRCA1 affects the histoprognostic grade in hereditary breast cancer. Cancer Res. 1996;56:471-474.
8. Hamann U, Sinn HP. Survival and tumor characteristics of German hereditary breast cancer patients. Breast Cancer Res Treat. 2000;59:185-192.
9. Johannsson OT, Idvall I, Anderson C, et al. Tumour biological features of BRCA1-induced breast and ovarian cancer. Eur J Cancer. 1997;33:362-371.
10. Karp SE, Tonin PN, Bégin LR, et al. Influence of BRCA1 mutations on nuclear grade and estrogen receptor status of breast carcinoma in Ashkenazi Jewish women. Cancer. 1997; 80:435-441.
11. Noguchi S, Kasugai T, Miki Y, Fukutomi T, Emi M, Nomizu T. Clinicopathologic analysis of BRCA1- or BRCA2-associated hereditary breast carcinoma in Japanese women. Cancer. 1999;85:2200-2205.
12. Robson M, Gilewski T, Haas B, et al. BRCA-associated breast cancer in young women. J Clin Oncol. 1998;16:1642-1649.
13. Lakhani SR, van de Vijver MJ, Jacquemier J, et al. The pathology of familial breast cancer: predictive value of immunohistochemical markers estrogen receptor, progesterone receptor, HER-2, and p53 in patients with mutations in BRCA1 and BRCA2. J Clin Oncol. 2002;20:2310-2318.
14. Wagner TM, Moslinger RA, Muhr D, et al. BRCA1-related breast cancer in Austrian breast and ovarian cancer families: specific BRCA1 mutations and pathological characteristics. Int J Cancer. 1998;77:354-360.
15. Chappuis PO, Rosenblatt J, Foulkes WD. The influence of familial and hereditary factors on the prognosis of breast cancer. Ann Oncol. 1999;10:1163-1170.
16. Phillips KA, Andrulis IL, Goodwin PJ. Breast carcinomas arising in carriers of mutations in BRCA1 or BRCA2: are they prognostically different? J Clin Oncol. 1999;17:3653-3663.
17. Chappuis PO, Kapusta L, Bégin LR, et al. Germline BRCA1/2 mutations and p27(Kip1) protein levels independently predict outcome after breast cancer. J Clin Oncol. 2000;18:4045- 4052.
18. Foulkes WD, Wong N, Brunet JS, et al. Germ-line BRCA1 mutation is an adverse prognostic factor in Ashkenazi Jewish women with breast cancer. Clin Cancer Res. 1997;3(12 Pt 1):2465-2469.
19. Stoppa-Lyonnet D, Ansquer Y, Dreyfus H, et al. Familial invasive breast cancers: worse outcome related to BRCA1 mutations. J Clin Oncol. 2000;18:4053-4059.
20. Fisher DE. The p53 tumor suppressor: critical regulator of life and death in cancer. Apoptosis. 2001;6:7-15.
21. Fan S, Cherney B, Reinhold W, Rucker K, O'Connor PM. Disruption of p53 function in immortalized human cells does not affect survival or apoptosis after Taxol or vincristine treatment. Clin Cancer Res. 1998;4:1047-1054.
22. Phillips HA. The role of the p53 tumour suppressor gene in human breast cancer. Clin Oncol (R Coll Radiol). 1999;11: 148-155.
23. Akashi M, Koeffler HP. Li-Fraumeni syndrome and the role of the p53 tumor suppressor gene in cancer susceptibility. Clin Obstet Gynecol. 1998;41:172-199.
24. Greenblatt MS, Chappuis PO, Bond JP, Hamel N, Foulkes WD. TP53 mutations in breast cancer associated with BRCA1 or BRCA2 germ-line mutations: distinctive spectrum and structural distribution. Cancer Res. 2001;61:4092-4097.
25. Phillips KA, Nichol K, Ozcelik H, et al. Frequency of p53 mutations in breast carcinomas from Ashkenazi Jewish carriers of BRCA1 mutations. J Natl Cancer Inst. 1999;91:469-473.
26. Sasa M, Kondo K, Komaki K, Morimoto T, Monden Y. p53 alteration correlates with negative ER, negative PgR, and high histologic grade in breast cancer. J Surg Oncol. 1994; 56:46-50.
27. Bhargava V, Thor A, Deng G, et al. The association of p53 immunopositivity with tumor proliferation and other prognostic indicators in breast cancer. Mod Pathol. 1994;7:361-368.
28. Schmutzler RK, Bierhoff E, Werkhausen T, et al. Genomic deletions in the BRCA1, BRCA2 and TP53 regions associate with low expression of the estrogen receptor in sporadic breast carcinoma. Int J Cancer. 1997;74:322-325.
29. Thorlacius S, Borresen AL, Eyfjord JE. Somatic p53 mutations in human breast carcinomas in an Icelandic population: a prognostic factor. Cancer Res. 1993;53:1637-1641.
30. Chappuis PO, Estreicher A, Dieterich B, et al. Prognostic significance of p53 mutation in breast cancer: frequent detection of non-missense mutations by yeast functional assay. Int J Cancer. 1999;84:587-593.
31. Zellars RC, Hilsenbeck SG, Clark GM, et al. Prognostic value of p53 for local failure in mastectomy-treated breast cancer patients. J Clin Oncol. 2000;18:1906-1913.
32. Elledge RM, Green S, Howes L, et al. bcl-2, p53, and response to tamoxifen in estrogen receptor-positive metastatic breast cancer: a Southwest Oncology Group study. J Clin Oncol. 1997;15:1916-1922.
33. Gentile M, Bergman JM, Olsen KE, Soderkvist P, Wingren S. p53 and survival in early onset breast cancer: analysis of gene mutations, loss of heterozygosity and protein accumulation. Eur J Cancer. 1999;35:1202-1207.
34. Isola J, Visakorpi T, Holli K, Kallioniemi OP. Association of overexpression of tumor suppressor protein p53 with rapid cell proliferation and poor prognosis in node-negative breast cancer patients. J Natl Cancer Inst. 1992;84:1109-1114.
35. Mottolese M, Benevolo M, Del Monte G, et al. Role of P53 and BCL-2 in high-risk breast cancer patients treated with adjuvant anthracycline-based chemotherapy. J Cancer Res Clin Oncol. 2000;126:722-729.
36. Thorlacius S, Thorgilsson B, Bjornsson J, et al. TP53 mutations and abnormal p53 protein staining in breast carcinomas related to prognosis. Eur J Cancer. 1995;31A:1856-1861.
37. Falette N, Paperin MP, Treilleux I, et al. Prognostic value of P53 gene mutations in a large series of node-negative breast cancer patients. Cancer Res. 1998;58:1451-1455.
38. Cunningham JM, Ingle JN, Jung SH, et al. p53 gene expression in node-positive breast cancer: relationship to DNA ploidy and prognosis. J Natl Cancer Inst. 1994;86:1871-1873.
39. Xu X, Wagner KU, Larson D, et al. Conditional mutation of Brca1 in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat Genet. 1999;22: 37-43.
40. Brodie SG, Xu X, Qiao W, Li WM, Cao L, Deng CX. Multiple genetic changes are associated with mammary tumorigenesis in Brca1 conditional knockout mice. Oncogene. 2001;20: 7514-7523.
41. Foulkes WD, Chappuis PO, Wong N, et al. Primary node negative breast cancer in BRCA1 mutation carriers has a poor outcome. Ann Oncol. 2000;11:307-313.
42. Bergh J, Norberg T, Sjogren S, Lindgren A, Holmberg L. Complete sequencing of the p53 gene provides prognostic information in breast cancer patients, particularly in relation to adjuvant systemic therapy and radiotherapy. Nat Med. 1995;1:1029-1034.
43. Berns EM, Foekens JA, Vossen R, et al. Complete sequencing of TP53 predicts poor response to systemic therapy of advanced breast cancer. Cancer Res. 2000;60:2155-2162.
44. Silvestrini R, Benini E, Veneroni S, et al. p53 and bcl-2 expression correlates with clinical outcome in a series of node-positive breast cancer patients. J Clin Oncol. 1996;14: 1604-1610.
45. Archer SG, Eliopoulos A, Spandidos D, et al. Expression of ras p21, p53 and c-erbB-2 in advanced breast cancer and response to first line hormonal therapy. Br J Cancer. 1995; 72:1259-1266.
46. Berry DA, Muss HB, Thor AD, et al. HER-2/neu and p53 expression versus tamoxifen resistance in estrogen receptor-positive, node-positive breast cancer. J Clin Oncol. 2000; 18:3471-3479.
47. Bottini A, Berruti A, Bersiga A, et al. p53 but not bcl-2 immunostaining is predictive of poor clinical complete response to primary chemotherapy in breast cancer patients. Clin Cancer Res. 2000;6:2751-2758.
48. Geisler S, Lonning PE, Aas T, et al. Influence of TP53 gene alterations and c-erbB-2 expression on the response to treatment with doxorubicin in locally advanced breast cancer. Cancer Res. 2001;61:2505-2512.
49. Tetu B, Brisson J, Plante V, Bernard P. p53 and c-erbB-2 as markers of resistance to adjuvant chemotherapy in breast cancer. Mod Pathol. 1998;11:823-830.
50. Chappuis PO, Goffin J, Wong N, et al. A significant response to neoadjuvant chemotherapy in BRCA1/2 related breast cancer. J Med Genet. 2002;39:608-610.
51. Ren Q, Carbonne C, Potoczek M, et al. Differential response of BRCA1 wild type and BRCA1 mutant breast cancer cells to ionizing radiation and paclitaxel [abstract]. Clin Cancer Res. 2001;7(Suppl):3723s.
52. Fan S, Yuan R, Ma YX, Meng Q, Goldberg ID, Rosen EM. Mutant BRCA1 genes antagonize phenotype of wild-type BRCA1. Oncogene. 2001;20:8215-8235.
53. Bhattacharyya A, Ear US, Koller BH, Weichselbaum RR, Bishop DK. The breast cancer susceptibility gene BRCA1 is required for subnuclear assembly of Rad51 and survival following treatment with the DNA cross-linking agent cisplatin. J Biol Chem. 2000;275:23899-23903.
54. Husain A, He G, Venkatraman ES, Spriggs DR. BRCA1 upregulation is associated with repair-mediated resistance to cis-diamminedichloroplatinum(II). Cancer Res. 1998;58: 1120-1123.
55. Freneaux P, Stoppa-Lyonnet D, Mouret E, et al. Low expression of bcl-2 in Brca1-associated breast cancers. Br J Cancer. 2000;83:1318-1322.
56. Thangaraju M, Kaufmann SH, Couch FJ. BRCA1 facilitates stress-induced apoptosis in breast and ovarian cancer cell lines. J Biol Chem. 2000;275:33487-33496.
57. Kauff ND, Satagopan JM, Robson ME, et al. Risk-reducing salpingo-oophorectomy in women with a BRCA1 or BRCA2 mutation. N Engl J Med. 2002;346:1609-1615.
58. Rebbeck TR, Levin AM, Eisen A, et al. Breast cancer risk after bilateral prophylactic oophorectomy in BRCA1 mutation carriers. J Natl Cancer Inst. 1999;91:1475-1479.
59. Rebbeck TR, Lynch HT, Neuhausen SL, et al. Prophylactic oophorectomy in carriers of BRCA1 or BRCA2 mutations. N Engl J Med. 2002;346:1616-1622.
60. Narod SA, Brunet JS, Ghadirian P, et al. Tamoxifen and risk of contralateral breast cancer in BRCA1 and BRCA2 mutation carriers: a case-control study. Hereditary Breast Cancer Clinical Study Group. Lancet. 2000;356:1876-1881.
61. Kauff ND, Perez-Segura P, Robson ME, et al. Incidence of non-founder BRCA1 and BRCA2 mutations in high risk Ashkenazi breast and ovarian cancer families. J Med Genet. 2002;39:611-614.
62. Tonin P, Weber B, Offit K, et al. Frequency of recurrent BRCA1 and BRCA2 mutations in Ashkenazi Jewish breast cancer families. Nat Med. 1996;2:1179-1183.
63. Kuperstein G, Foulkes WD, Ghadirian P, Hakimi J, Narod SA. A rapid fluorescent multiplexed-PCR analysis (FMPA) for founder mutations in the BRCA1 and BRCA2 genes. Clin Genet. 2000;57:213-220.
64. Yuan ZQ, Bégin LR, Wong N, et al. The effect of the I1307KAPC polymorphism on the clinicopathological features and natural history of breast cancer. Br J Cancer. 1999;81:850-854.
65. Early Breast Cancer Trialists' Collaborative Group. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet. 1998;351:1451-1467.
66. Zheng L, Annab LA, Afshari CA, Lee WH, Boyer TG. BRCA1 mediates ligand-independent transcriptional repression of the estrogen receptor. Proc Natl Acad Sci U S A. 2001;98: 9587-9592.
67. Fan S, Ma YX, Wang C, et al. p300 Modulates the BRCA1 inhibition of estrogen receptor activity. Cancer Res. 2002;62: 141-151.
68. Cameron DA, Ritchie AA, Miller WR. The relative importance of proliferation and cell death in breast cancer growth and response to tamoxifen. Eur J Cancer. 2001;37:1545-1553.
69. Mandlekar S, Kong AN. Mechanisms of tamoxifen-induced apoptosis. Apoptosis. 2001;6:469-477.
70. Zhang GJ, Kimijima I, Onda M, et al. Tamoxifen-induced apoptosis in breast cancer cells relates to down-regulation of bcl-2, but not bax and bcl-X(L), without alteration of p53 protein levels. Clin Cancer Res. 1999;5:2971-2977.
71. Xu X, Qiao W, Linke SP, et al. Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat Genet. 2001;28:266-271.
72. McAllister KA, Wiseman RW. Are Trp53 rescue of Brca1 embryonic lethality and Trp53/Brca1 breast cancer association related? Breast Cancer Res. 2002;4:54-57.
73. Visscher DW, Sarkar FH, Shimoyama RK, Crissman JD. Correlation between p53 immunostaining patterns and gene sequence mutations in breast carcinoma. Diagn Mol Pathol. 1996;5:187-193.
74. Sjogren S, Inganas M, Norberg T, et al. The p53 gene in breast cancer: prognostic value of complementary DNA sequencing versus immunohistochemistry. J Natl Cancer Inst. 1996;88:173-182.
75. Kandel R, Li SQ, Ozcelik H, Rohan T. p53 protein accumulation and mutations in normal and benign breast tissue. Int J Cancer. 2000;87:73-78.