Acta Med. 2008, 51: 107-112

https://doi.org/10.14712/18059694.2017.11

Expression of Bcl-2 in Breast Cancer: Correlation with Clinicopathological Characteristics and Survival

Filip Čečkaa, Helena Hornychováb, Bohuslav Melicharc, Aleš Ryškab, Pavel Jandíka, Jindřiška Mergancováa, Hana Klozová-Urminskád

aCharles University in Prague, Faculty of Medicine and University Hospital Hradec Králové, Department of Surgery, Hradec Králové, Czech Republic
bCharles University in Prague, Faculty of Medicine and University Hospital Hradec Králové, The Fingerland Department of Pathology, Hradec Králové, Czech Republic
cCharles University in Prague, Faculty of Medicine and University Hospital Hradec Králové, Department of Oncology and Radiotherapy, Hradec Králové, Czech Republic
dCharles University in Prague, Faculty of Medicine and University Hospital Hradec Králové, Department of Radiology, Hradec Králové, Czech Republic

Received March 1, 2008
Accepted April 1, 2008

References

1. Allred DC, Clark GM, Elledge R, et al. Accumulation of mutant p53 is associated with increased proliferation and poor clinical outcome in node negative breast cancer. J Natl Cancer Inst 1993; 85:200–6. <https://doi.org/10.1093/jnci/85.3.200>
2. Allred DC, Clark GM, Molina R, et al. Overexpression of HER-2/neu and its relationship with other prognostic factors change during the progression of in situ to invasive breast cancer. Hum Pathol 1992; 23:974–9. <https://doi.org/10.1016/0046-8177(92)90257-4>
3. Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 1998; 11: 155–68.
4. Barnes DM, Dublin EA, Fisher CJ, Levison DA, Millis RR. Immunohistochemical detection of p53 protein in mammary carcinoma: an important new independent indicator of prognosis? Hum Pathol 1993; 24:469–76. <https://doi.org/10.1016/0046-8177(93)90158-D>
5. Barnes DM, Harris WH, Smith P, Millis RR, Rubens RD. Immunohistochemical determination of oestrogen receptor: comparison of different methods of assessment of staining and correlation with clinical outcome of breast cancer patients. Br J Cancer 1996; 74:1445–51. <https://doi.org/10.1038/bjc.1996.563> <PubMed>
6. Beenken SW, Grizzle WE, Crowe DR, et al. Molecular biomarkers for breast cancer prognosis: coexpression of c-erbB-2 and p53. Ann Surg 2001; 233:630–8. <https://doi.org/10.1097/00000658-200105000-00006> <PubMed>
7. Bhatavdekar JM, Patel DD, Shah NG, et al. Prognostic significance of immunohistochemically localized biomarkers in stage II and stage III breast cancer: a multivariate analysis. Ann Surg Oncol 2000; 7:305–11. <https://doi.org/10.1007/s10434-000-0305-5>
8. Callagy GM, Pharoah PD, Pinder SE, et al. Bcl-2 is a prognostic marker in breast cancer independently of the Nottingham Prognostic Index. Clin Cancer Res 2006; 12:2468–75. <https://doi.org/10.1158/1078-0432.CCR-05-2719>
9. Carter CL, Allen C, Henson DE. Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 1989; 63:181–7. <https://doi.org/10.1002/1097-0142(19890101)63:1<181::AID-CNCR2820630129>3.0.CO;2-H>
10. Castiglione F, Sarotto I, Fontana V, et al. Bcl2, p53 and clinical outcome in a series of 138 operable breast cancer patients. Anticancer Res 1999; 19:4555–63.
11. Chang J, Powles TJ, Allred DC, et al. Biologic markers as predictors of clinical outcome from systemic therapy for primary operable breast cancer. J Clin Oncol 1999; 17:3058–63. <https://doi.org/10.1200/JCO.1999.17.10.3058>
12. Charpin C, Garcia S, Bonnier P, et al. bcl-2 automated and quantitative immunocytochemical assays in breast carcinomas: correlation with 10-year follow-up. J Clin Oncol 1998; 16:2025–31. <https://doi.org/10.1200/JCO.1998.16.6.2025>
13. Coradini D, Biganzoli E, Pellizzaro C, et al. Vascular endothelial growth factor in node-positive breast cancer patients treated with adjuvant tamoxifen. Br J Cancer 2003; 89:268–70. <https://doi.org/10.1038/sj.bjc.6601060> <PubMed>
14. Daidone MG, Luisi A, Martelli G, et al. Biomarkers and outcome after tamoxifen treatment in node-positive breast cancers from elderly women. Br J Cancer 2000; 82:270–7. <https://doi.org/10.1054/bjoc.1999.0914> <PubMed>
15. Del Bufalo D, Biroccio A, Leonetti C, Zupi G. Bcl-2 overexpression enhances the metastatic potential of a human breast cancer line. FASEB J 1997; 11:947–53. <https://doi.org/10.1096/fasebj.11.12.9337147>
16. Fisher ER, Anderson S, Redmond C, Fisher B. Pathologic findings from the National Surgical Adjuvant Breast Project Protocol B-06: 10–year pathologic and clinical prognostic discriminants. Cancer 1993; 71:2507–14. <https://doi.org/10.1002/1097-0142(19930415)71:8<2507::AID-CNCR2820710813>3.0.CO;2-0>
17. Fisher ER, Sass R, Fisher B. Pathologic findings from the National Surgical Adjuvant Breast Project for breast cancers (protocol no 4): discrimination for tenth year treatment failure. Cancer 1984; 53(suppl. 3):712–23.
18. Gasparini G, Barbareschi M, Doglioni C, et al. Expression of bcl-2 protein predicts efficacy of adjuvant treatments in operable node-positive breast cancer. Clin Cancer Res 1995; 1:189–98.
19. Gion M, Mione R, Dittadi R, et al. Relationship between cathepsin D and other pathologic and biological parameters in 1752 patients with primary breast cancer. Eur J Cancer 1995; 31:671–7. <https://doi.org/10.1016/0959-8049(94)00532-A>
20. Gross A, McDonnell JM, Korsmeyer SJ. BCL-2 family members and the mitochondria in apoptosis. Genes Dev 1999; 13:1899–911. <https://doi.org/10.1101/gad.13.15.1899>
21. Harries M, Smith I. The development and clinical use of trastuzumab (Herceptin). Endocr Relat Cancer 2002; 9:72–85. <https://doi.org/10.1677/erc.0.0090075>
22. Henson DE, Ries L, Freedman LS, Carriaga M. Relationship among outcome, stage of disease, and histologic grade for 22,616 cases of breast cancer. The basis for a prognostic index. Cancer 1991; 68:2142–9. <https://doi.org/10.1002/1097-0142(19911115)68:10<2142::AID-CNCR2820681010>3.0.CO;2-D>
23. Huang Y, Ray S, Reed JC, et al. Estrogen increases intracellular p26Bcl-2 to p21Bax ratios and inhibits taxol-induced apoptosis of human breast cancer MCF- 7 cells. Breast Cancer Res Treat 1997; 42:73–81. <https://doi.org/10.1023/A:1005777219997>
24. Isola J, Weitz S, Visakorpi T, et al. Cathepsin D expression detected by immunohistochemistry has independent prognostic value in axillary node negative breast cancer. J Clin Oncol 1993; 11:36–43. <https://doi.org/10.1200/JCO.1993.11.1.36>
25. Jansen RL, Joosten-Achjanie SR, Volovics A, et al. Relevance of the expression of bcl-2 in combination with p53 as a prognostic factor in breast cancer. Anticancer Res 1998; 18:4455–62.
26. Kennedy SM, O’Driscoll L, Purcell R, et al. Prognostic importance of survivin in breast cancer. Br J Cancer 2003; 88:1077–83. <https://doi.org/10.1038/sj.bjc.6600776> <PubMed>
27. Kenny FS, Hui R, Musgrowe EA, et al. Overexpression of cyclin D1 messenger RNA predicts for poor prognosis in estrogen receptor-positive breast cancer. Clin Cancer Res 1999; 5:2069–76.
28. Keyomarsi K, Tucker SL, Buchholz TA, et al. Cyclin E and survival in patients with breast cancer. N Engl J Med 2002; 347:1566–75. <https://doi.org/10.1056/NEJMoa021153>
29. Krajewski S, Blomvqvist C, Franssila K, et al. Reduced expression of pro-apoptotic gene Bax is associated with poor response rates to combination chemotherapy and shorter survival in women with metastatic breast adenocarcinoma. Cancer Res 1995; 55:4471–8.
30. Krajewski S, Krajewska M, Turner BC, et al. Prognostic significance of apoptosis regulators in breast cancer. Endocr Relat Cancer 1999; 6:29–40. <https://doi.org/10.1677/erc.0.0060029>
31. Krajewski S, Thor AD, Edgerton SM, Moore DH, Krajewska M, Reed JC. Analysis of Bax and Bcl-2 expression in p53–immunopositive breast cancers. Clin Cancer Res 1997; 3:199–208.
32. Kuhling H, Alm P, Olsson H, et al. Expression of cyclins E, A, and B, and prognosis in lymph node-negative breast cancer. J Pathol 2003; 199:424–31. <https://doi.org/10.1002/path.1322>
33. Kymionis GD, Dimitrakakis CE, Konstadoulakis MM, et al. Can expression of apoptosis genes, bcl-2 and bax, predict survival and responsiveness to chemotherapy in node-negative breast cancer patients? J Surg Res 2001; 99:161–8. <https://doi.org/10.1006/jsre.2001.6084>
34. Le Doussal V, Tubiana-Hulin M, Friedman S, et al. Prognostic value of histologic grade nuclear components of Scarff-Bloom-Richardson (SBR): an improved score modification based on multivariate analysis of 1262 invasive ductal breast carcinomas. Cancer 1989; 64:1914–21. <https://doi.org/10.1002/1097-0142(19891101)64:9<1914::AID-CNCR2820640926>3.0.CO;2-G>
35. Linjawi A, Kontogiannea M, Halwani F, Edwardes M, Meterissian S. Prognostic significance of p53, bcl-2, and Bax expression in early breast cancer. J Am Coll Surg 2004; 198:83–90. <https://doi.org/10.1016/j.jamcollsurg.2003.08.008>
36. Megha T, Ferrari F, Arcuri F, et al. Cellular kinetics and expression of bcl-2 and p53 in ductal carcinoma of the breast. Oncol Rep 2000; 7:473–8.
37. Molino A, Micciolo R, Turazza M, et al. Ki-67 immunostaining in 322 primary breast cancers: association with clinical and pathological variables and prognosis. Int J Cancer 1997; 74:433–7. <https://doi.org/10.1002/(SICI)1097-0215(19970822)74:4<433::AID-IJC12>3.0.CO;2-A>
38. Neri A, Marrelli D, Roviello F, et al. Bcl-2 expression correlates with lymphovascular invasion and long-term prognosis in breast cancer. Breast Cancer Res Treat 2006; 99:77–83. <https://doi.org/10.1007/s10549-006-9183-2>
39. Pernick NL, Biernat L, Du W, Visscher DW. Clinicopathologic analysis of Fas, Fas ligand, and other biomarkers in locally advanced breast carcinoma. Breast J 2000; 6:233–41. <https://doi.org/10.1046/j.1524-4741.2000.98087.x>
40. Pertschuk LP, Kim DS, Nayer K, et al. Immunocytochemical estrogen and progestin receptor assays in breast cancer with monoclonal antibodies. Histopathologic, demographic, and biochemical correlations and relationship to endocrine response and survival. Cancer 1990; 66:1663–70. <https://doi.org/10.1002/1097-0142(19901015)66:8<1663::AID-CNCR2820660802>3.0.CO;2-C>
41. Reed JC. Balancing cell life and death: Bax, apoptosis, and breast cancer. J Clin Invest 1996; 97:2403–4. <https://doi.org/10.1172/JCI118684> <PubMed>
42. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 1994; 124:1–6. <https://doi.org/10.1083/jcb.124.1.1> <PubMed>
43. Reed JC. Mechanisms of apoptosis. Am J Pathol 2000; 157:1415–30. <https://doi.org/10.1016/S0002-9440(10)64779-7> <PubMed>
44. Remmele W, Stegner HE. Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Pathologe 1987; 8:138–40.
45. Rolland P, Spendlove I, Madjid Z, et al. The p53 positive Bcl-2 negative phenotype is an independent marker of prognosis in breast cancer. Int J Cancer 2007; 120:1311–7. <https://doi.org/10.1002/ijc.22430>
46. 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; 14:1604–10. <https://doi.org/10.1200/JCO.1996.14.5.1604>
47. Silvestrini R, Veneroni S, Daidone MG, et al. The Bcl-2 protein: a prognostic indicator strongly related to p53 protein in lymph node-negative breast cancer patients. J Natl Cancer Inst 1994; 86:499–504. <https://doi.org/10.1093/jnci/86.7.499>
48. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER- 2/neu oncogene. Science 1987; 235:177–82. <https://doi.org/10.1126/science.3798106>
49. Smith JA, Gamez-Araugo JJ, Gallager HS, et al. Carcinoma of the breast: analysis of total lymph node involvement versus level of metastasis. Cancer 1977; 39: 527–32. <https://doi.org/10.1002/1097-0142(197702)39:2<527::AID-CNCR2820390221>3.0.CO;2-N>
50. Teixeira C, Reed JC, Pratt MA. Estrogen promotes chemotherapeutic drug resistance by a mechanism involving Bcl-2 proto-oncogene expression in human breast cancer cell. Cancer Res 1995; 55:3902–7.
51. Tsujimoto Y, Croce CM. Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 1986; 83:5214–8. <https://doi.org/10.1073/pnas.83.14.5214> <PubMed>
52. Tsutsui S, Kataoka A, Ohno S, Murakami S, Kinoshita J, Hachitanda Y. Prognostic and predictive value of epidermal growth factor receptor in recurrent breast cancer. Clin Cancer Res 2002; 8:3454–60.
53. Umekita Y, Ohi Y, Sagara Y, Yoshida H. Overexpression of cyclin D1 predicts for poor prognosis in estrogen receptor-negative breast cancer patients. Int J Cancer 2002; 98:415–8. <https://doi.org/10.1002/ijc.10151>
54. Veronesi U, Cascinelli N, Greco M, et al. Prognosis of breast cancer patients after mastectomy and dissection of internal mammary nodes. Ann Surg 1985; 202: 702–7. <https://doi.org/10.1097/00000658-198512000-00007> <PubMed>
55. Veronesi U, Galimberti V, Zurrida S, et al. Prognostic significance of number and level of axillary nodal metastases in breast cancer. Breast 1993; 2:224–8. <https://doi.org/10.1016/0960-9776(93)90004-Y>
56. Zapata JM, Krajewska M, Krajewski S, et al. Expression of multiple apoptosis-regulatory genes in human breast cancer cell lines and primary tumors. Breast Cancer Res Treat 1998; 47:129–40. <https://doi.org/10.1023/A:1005940832123>
57. Zhang GJ, Kimijima I, Abe R, et al. Apoptotic index correlated to Bcl-2 and p53 protein expression, histological grade and prognosis in invasive breast cancers. Anticancer Res 1998; 18:1989–98.
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