The combination of high cyclin E and Skp2 expression in breast cancer is associated with a poor prognosis and the basal phenotype

Human Pathology

Volumn 39, Issue 10, 2008, Pages 1431-1437

  Voduc, David ^a,b   Nielsen, Torsten O ^b,c   Cheang, Maggie C ^b   Foulkes, William D ^d  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c VANCOUVER GENERAL HOSPITAL   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

Basal phenotype; Biomarker; Breast cancer; Immunohistochemistry; Tissue microarray

Indexed keywords

CYCLIN E; CYTOKERATIN 5; CYTOKERATIN 6; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; PROTEIN P27; S PHASE KINASE ASSOCIATED PROTEIN 2;

ADULT; ARTICLE; BASAL CELL; BREAST CANCER; CONTROLLED STUDY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; PROGNOSIS; PROTEIN EXPRESSION; TISSUE MICROARRAY;

BREAST NEOPLASMS; CELL NUCLEUS; CYCLIN E; FEMALE; HUMANS; LYMPH NODES; LYMPHATIC METASTASIS; MIDDLE AGED; PHENOTYPE; PROGNOSIS; PROLIFERATING CELL NUCLEAR ANTIGEN; S-PHASE KINASE-ASSOCIATED PROTEINS; SURVIVAL RATE; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 50649122298     PISSN: 00468177     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.humpath.2008.03.004     Document Type: Article

References (39)

1. Perou C.M., Sorlie T., Eisen M.B., et al. Molecular portraits of human breast tumours. Nature 406 (2000) 747-752
2. Sorlie T., Perou C.M., Tibshirani R., et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 98 (2001) 10869-10874
3. Sorlie T., Tibshirani R., Parker J., et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100 (2003) 8418-8423
4. Carey L.A., Perou C.M., Livasy C.A., et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295 (2006) 2492-2502
5. Nielsen T.O., Hsu F.D., Jensen K., et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 10 (2004) 5367-5374
6. Foulkes W.D., Brunet J.S., Stefansson I.M., et al. The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res 64 (2004) 830-835
7. Signoretti S., Di Marcotullio L., Richardson A., et al. Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J Clin Invest 110 (2002) 633-641
8. Bartek J., and Lukas J. Cell cycle. Order from destruction. Science 294 (2001) 66-67
9. Hunt K.K., and Keyomarsi K. Cyclin E as a prognostic and predictive marker in breast cancer. Semin Cancer Biol 15 (2005) 319-326
10. Keyomarsi K., Tucker S.L., Buchholz T.A., et al. Cyclin E and survival in patients with breast cancer. N Engl J Med 347 (2002) 1566-1575
11. Catzavelos C., Bhattacharya N., Ung Y.C., et al. Decreased levels of the cell-cycle inhibitor p27Kip1 protein: prognostic implications in primary breast cancer. Nat Med 3 (1997) 227-230
12. Chappuis P.O., Kapusta L., Begin L.R., et al. Germline BRCA1/2 mutations and p27(Kip1) protein levels independently predict outcome after breast cancer. J Clin Oncol 18 (2000) 4045-4052
13. Spataro V.J., Litman H., Viale G., et al. Decreased immunoreactivity for p27 protein in patients with early-stage breast carcinoma is correlated with HER-2/neu overexpression and with benefit from one course of perioperative chemotherapy in patients with negative lymph node status: results from International Breast Cancer Study Group Trial V. Cancer 97 (2003) 1591-1600
14. Cariou S., Donovan J.C., Flanagan W.M., Milic A., Bhattacharya N., and Slingerland J.M. Down-regulation of p21WAF1/CIP1 or p27Kip1 abrogates antiestrogen-mediated cell cycle arrest in human breast cancer cells. Proc Natl Acad Sci U S A 97 (2000) 9042-9046
15. Donovan J.C., Milic A., and Slingerland J.M. Constitutive MEK/MAPK activation leads to p27(Kip1) deregulation and antiestrogen resistance in human breast cancer cells. J Biol Chem 276 (2001) 40888-40895
16. Carrano A.C., Eytan E., Hershko A., and Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1 (1999) 193-199
17. Sonoda H., Inoue H., Ogawa K., et al. Significance of skp2 expression in primary breast cancer. Clin Cancer Res 12 (2006) 1215-1220
18. Makretsov N., Gilks C.B., Coldman A.J., Hayes M., and Huntsman D. Tissue microarray analysis of neuroendocrine differentiation and its prognostic significance in breast cancer. Hum Pathol 34 (2003) 1001-1008
19. Kononen J., Bubendorf L., Kallioniemi A., et al. Tissue microarrays for high-throughput molecular profiling of tumor specimens. [see comment]. Nat Med 4 (1998) 844-847
20. Parker R.L., Huntsman D.G., Lesack D.W., et al. Assessment of interlaboratory variation in the immunohistochemical determination of estrogen receptor status using a breast cancer tissue microarray. Am J Clin Pathol 117 (2002) 723-728
21. Liu C.L., Montgomery K.D., Natkunam Y., et al. TMA-Combiner, a simple software tool to permit analysis of replicate cores on tissue microarrays. Mod Pathol 18 (2005) 1641-1648
22. Wang L., and Shao Z.M. Cyclin e expression and prognosis in breast cancer patients: a meta-analysis of published studies. Cancer Invest 24 (2006) 581-587
23. Han S., Park K., Bae B.N., et al. Prognostic implication of cyclin E expression and its relationship with cyclin D1 and p27Kip1 expression on tissue microarrays of node negative breast cancer. J Surg Oncol 83 (2003) 241-247
24. Rudolph P., Kuhling H., Alm P., et al. Differential prognostic impact of the cyclins E and B in premenopausal and postmenopausal women with lymph node-negative breast cancer. Int J Cancer 105 (2003) 674-680
25. Tan P., Cady B., Wanner M., et al. The cell cycle inhibitor p27 is an independent prognostic marker in small (T1a,b) invasive breast carcinomas. Cancer Res 57 (1997) 1259-1263
26. Traub F., Mengel M., Luck H.J., Kreipe H.H., and von Wasielewski R. Prognostic impact of Skp2 and p27 in human breast cancer. Breast Cancer Res Treat 99 (2006) 185-191
27. Keyomarsi K., and Pardee A.B. Redundant cyclin overexpression and gene amplification in breast cancer cells. Proc Natl Acad Sci U S A 90 (1993) 1112-1116
28. Chappuis P.O., Donato E., Goffin J.R., et al. Cyclin E expression in breast cancer: predicting germline BRCA1 mutations, prognosis and response to treatment. Ann Oncol 16 (2005) 735-742
29. Kawamata N., Morosetti R., Miller C.W., et al. Molecular analysis of the cyclin-dependent kinase inhibitor gene p27/Kip1 in human malignancies. Cancer Res 55 (1995) 2266-2269
30. Ponce-Castaneda M.V., Lee M.H., Latres E., et al. p27Kip1: chromosomal mapping to 12p12-12p13.1 and absence of mutations in human tumors. Cancer Res 55 (1995) 1211-1214
31. Alkarain A., and Slingerland J. Deregulation of p27 by oncogenic signaling and its prognostic significance in breast cancer. Breast Cancer Res 6 (2004) 13-21
32. Han S., Park K., Kim H.Y., Lee M.S., Kim H.J., and Kim Y.D. Reduced expression of p27Kip1 protein is associated with poor clinical outcome of breast cancer patients treated with systemic chemotherapy and is linked to cell proliferation and differentiation. Breast Cancer Res Treat 55 (1999) 161-167
33. Barbareschi M., van Tinteren H., Mauri F.A., et al. p27(kip1) expression in breast carcinomas: an immunohistochemical study on 512 patients with long-term follow-up. Int J Cancer 89 (2000) 236-241
34. Barnes A., Pinder S.E., Bell J.A., et al. Expression of p27kip1 in breast cancer and its prognostic significance. J Pathol 201 (2003) 451-459
35. Leivonen M., Nordling S., Lundin J., von Boguslawski K., and Haglund C. p27 expression correlates with short-term, but not with long-term prognosis in breast cancer. Breast Cancer Res Treat 67 (2001) 15-22
36. Dees E.C., and Orlowski R.Z. Targeting the ubiquitin-proteasome pathway in breast cancer therapy. Future Oncol 2 (2006) 121-135
37. Cardoso F., Ross J.S., Picart M.J., Sotiriou C., and Durbecq V. Targeting the ubiquitin-proteasome pathway in breast cancer. Clin Breast Cancer 5 (2004) 148-157
38. Johnson K.R., and Fan W. Reduced expression of p53 and p21WAF1/CIP1 sensitizes human breast cancer cells to paclitaxel and its combination with 5-fluorouracil. Anticancer Res 22 (2002) 3197-3204
39. Smith M.L., and Seo Y.R. Sensitivity of cyclin E-overexpressing cells to cisplatin/taxol combinations. Anticancer Res 20 (2000) 2537-2539