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01-12-2013 | Research Article

Prognostic value of cyclin E expression in breast cancer: a meta-analysis

Authors: Sheng Gao, Jing-Jing Ma, Cheng Lu

Published in: Tumor Biology | Issue 6/2013

Abstract

Cyclin E is an important regulator of cell cycle progression. Various studies examined the relationship between cyclin E overexpression with the clinical outcome in patients with breast cancer but yielded conflicting results. Electronic databases updated to May 2013 were searched to find relevant studies. A meta-analysis was conducted with eligible studies which quantitatively evaluated the relationship between cyclin E overexpression and survival of patients with breast cancer. Survival data were aggregated and quantitatively analyzed. We conducted a final analysis of 7,759 patients from 23 eligible studies and evaluated the correlation between cyclin E overexpression and survival in patients with breast cancer. Combined hazard ratios suggested that cyclin E overexpression had an unfavorable impact on overall survival (OS) (hazard ratio (HR) = 1.30, 95 % confidence interval (CI), 1.12–1.49) and breast cancer-specific survival (BCSS) (HR = 1.48, 95 % CI, 1.03–1.93), but not disease-free survival (HR = 1.11; 95 % CI, 0.96–1.27) in patients with breast cancer. Significantly, risks were found among stage I–II breast cancer for (HR = 1.75; 95 % CI, 1.30–2.19). Cyclin E overexpression is associated with poor OS and BCSS in breast cancer.

Jemal A, Bray F, Center MM, Ferlay J, Ward E, et al. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRef

Saurel CA, Patel TA, Perez EA. Changes to adjuvant systemic therapy in breast cancer: a decade in review. Clin Breast Cancer. 2010;10:196–208.PubMedCrossRef

Colozza M, Azambuja E, Cardoso F, Sotiriou C, Larsimont D, Piccart MJ. Proliferative markers as prognostic and predictive tools in early breast cancer: where are we now? Ann Oncol. 2005;16:1723–39.PubMedCrossRef

Hayes DF. Prognostic and predictive factors revisited. Breast. 2008;14:493–9.CrossRef

Callagy GM, Webber MJ, Pharoah PD, Caldas C. Meta-analysis confirms BCL2 is an independent prognostic marker in breast cancer. BMC Cancer. 2008;8:153.PubMedCrossRef

Tandis SH, Murray T, Bolden S, Wingo PA. Cancer statistics. CA Cancer J Clin. 1998;48:6–29.CrossRef

Qu Z, Weiss JN, MacLellan WR. Regulation of the mammalian cell cycle: a model of the G1-to-S transition. Am J Physiol Cell Physiol. 2003;284:349–64.CrossRef

Bortner DM, Rosenberg MP. Induction of mammary gland hyperplasia and carcinomas in transgenic mice expressing human cyclin E. Mol Cell Biol. 1997;17:453–9.PubMed

Ohtsubo M, Theodoras AM, Schumacher J, Roberts JM, Pagano M. Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol. 1995;15:2612–24.PubMed

10.

Ekholm-Reed S, Mendez J, Tedesco D, Zetterberg A, Stillman B, Reed SI. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol. 2004;165:789–800.PubMedCrossRef

11.

Berglund P, Landberg G. Cyclin E overexpression reduces infiltrative growth in breast cancer. Cell Cycle. 2006;5(6):606–9.PubMedCrossRef

12.

Altman DG. Systematic reviews of evaluations of prognostic variables. BMJ. 2001;323(7306):224–8.PubMedCrossRef

13.

Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815–34.PubMedCrossRef

14.

Yusuf S, Peto R, Lewis J, et al. Blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis. 1985;27:335–71.PubMedCrossRef

15.

DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.PubMedCrossRef

16.

Egger M, Smith GD, Schneider M. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–34.PubMedCrossRef

17.

Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.PubMedCrossRef

18.

Porter PL, Malone KE, Heagerty PJ, Alexander GM, Gatti LA, et al. Expression of cell cycle regulators p27Kip1 and cyclin E, alone and in combination, correlate with survival in young breast cancer patients. Nat Med. 1997;3(2):222–5.PubMedCrossRef

19.

Donnellan R, Kleinschmidt I, Chetty R. Cyclin E immunoexpression in breast ductal carcinoma: pathologic correlations and prognostic implications. Hum Pathol. 2001;32(1):89–94.PubMedCrossRef

20.

Kim HK, Park IA, Heo DS, Noh DY, Choe KJ, et al. Cyclin E overexpression as an independent risk factor of visceral relapse in breast cancer. Eur J Surg Oncol. 2001;27(5):464–71.PubMedCrossRef

21.

Bukholm IR, Bukholm G, Nesland JM. Overexpression of cyclin A is highly associated with early relapse and reduced survival in patients with primary breast carcinomas. Int J Cancer. 2001;93(2):283–7.PubMedCrossRef

22.

Keyomarsi K, Tucker SL, Buchholz TA, Callister M, Ding Y, et al. Cyclin E and survival in patients with breast cancer. N Engl J Med. 2002;347(20):1566–75.PubMedCrossRef

23.

Span PN, Tjan-Heijnen V, Manders P, Beex LV, Sweep CG. Cyclin-E is a strong predictor of endocrine therapy failure in human breast cancer. Oncogene. 2003;22(31):4898–904.PubMedCrossRef

24.

Han S, Park K, Bae BN, Kim KH, Kim HJ, Kim YD, 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. 2003;83(4):241–7.PubMedCrossRef

25.

Rudolph P, Kuhling H, Alm P, Ferno M, Baldetorp B, 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. 2003;105(5):674–80.PubMedCrossRef

26.

Peters MG, Vidal Mdel C, Gimenez L, Mauro L, Armanasco E, et al. Prognostic value of cell cycle regulator molecules in surgically resected stage I and II breast cancer. Oncol Rep. 2004;12(5):1143–50.PubMed

27.

Foulkes WD, Brunet JS, Stefansson IM, Straume O, Chappuis PO, et al. The prognostic implication of the basal-like (cyclin E high/p27low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res. 2004;64(3):830–5.PubMedCrossRef

28.

Lindahl T, Landberg G, Ahlgren J, Nordgren H, Norberg T, et al. Overexpression of cyclin E protein is associated with specific mutation types in the p53 gene and poor survival in human breast cancer. Carcinogenesis. 2004;25(3):375–80.PubMedCrossRef

29.

Chappuis PO, Donato E, Goffin JR, Wong N, Bégin LR, Kapusta LR, et al. Cyclin E expression in breast cancer: predicting germline BRCA1 mutations, prognosis and response to treatment. Ann Oncol. 2005;16(5):735–42.PubMedCrossRef

30.

Arnes JB, Brunet JS, Stefansson I, Bégin LR, Wong N, Chappuis PO, et al. Placental cadherin and the basal epithelial phenotype of BRCA1-related breast cancer. Clin Cancer Res. 2005;11(11):4003–11.PubMedCrossRef

31.

Brennan DJ, Jirstrom K, Kronblad A, Millikan RC, Landberg G, Duffy MJ, et al. CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clin Cancer Res. 2006;12(21):6421–31.PubMedCrossRef

32.

Callagy GM, Pharoah PD, Pinder SE, Hsu FD, Nielsen TO, Ragaz J, et al. Bcl-2 is a prognostic marker in breast cancer independently of the Nottingham Prognostic Index. Clin Cancer Res. 2006;12(8):2468–75.PubMedCrossRef

33.

Desmedt C, Ouriaghli FE, Durbecq V, Soree A, Colozza MA, Azambuja E, et al. Impact of cyclins E, neutrophil elastase and proteinase 3 expression levels on clinical outcome in primary breast cancer patients. Int J Cancer. 2006;119(11):2539–45.PubMedCrossRef

34.

Sieuwerts AM, Look MP, Meijer-van Gelder ME, Timmermans M, Trapman AM, Garcia RR, et al. Which cyclin E prevails as prognostic marker for breast cancer? Results from a retrospective study involving 635 lymph node-negative breast cancer patients. Clin Cancer Res. 2006;12(11 Pt 1):3319–28.PubMedCrossRef

35.

Porter PL, Barlow WE, Yeh IT, Lin MG, Yuan XP, Donato E, et al. p27(Kip1) and cyclin E expression and breast cancer survival after treatment with adjuvant chemotherapy. J Natl Cancer Inst. 2006;98(23):1723–31.PubMedCrossRef

36.

Potemski P, Pluciennik E, Bednarek AK, Kusinska R, Jesionek-Kupnicka D, Pasz-Walczak G, et al. Cyclin E expression in operable breast cancer quantified using real-time RT-PCR: a comparative study with immunostaining. Jpn J Clin Oncol. 2006;36(3):142–9.PubMedCrossRef

37.

Somlo G, Chu P, Frankel P, Ye W, Groshen S, Doroshow JH, et al. Molecular profiling including epidermal growth factor receptor and p21 expression in high-risk breast cancer patients as indicators of outcome. Ann Oncol. 2008;19(11):1853–9.PubMedCrossRef

38.

Potemski P, Kusińska R, Pasz-Walczak G, Piekarski JH, Watała C, Płuciennik E, et al. Prognostic relevance of cyclin E expression in operable breast cancer. Med Sci Monit. 2009;15(2):MT34–40.PubMed

39.

Sgambato A, Camerini A, Collecchi P, Graziani C, Bevilacqua G, Capodanno A, et al. Cyclin E correlates with manganese superoxide dismutase expression and predicts survival in early breast cancer patients receiving adjuvant epirubicin-based chemotherapy. Cancer Sci. 2009;100(6):1026–33.PubMedCrossRef

40.

Lemée F, Bergoglio V, Fernandez-Vidal A, Machado-Silva A, Pillaire MJ, Bieth A, et al. DNA polymerase theta up-regulation is associated with poor survival in breast cancer, perturbs DNA replication, and promotes genetic instability. Proc Natl Acad Sci U S A. 2010;107(30):13390–5.PubMedCrossRef

41.

Koff A, Giordano A, Desai D, Yamashita K, Harper JW, et al. Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science. 1992;257:1689–94.PubMedCrossRef

42.

Sauer K, Lehner CF. The role of cyclin E in the regulation of entry into S phase. Prog Cell Cycle Res. 1995;1:125–39.PubMedCrossRef

43.

Malumbres M, Barbacid M. To cycle or not cycle: a critical decision in cancer. Nat Rev Cancer. 2001;1:222–31.PubMedCrossRef

44.

Clurman BE, Sheaff RJ, Thress K, Groudine M, Roberts JM. Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev. 1996;10:1979–90.PubMedCrossRef

45.

Moberg KH, Bell DW, Wahrer DC, Haber DA, Hariharan IK. Archipelago regulates Cyclin E levels in Drosophila and is mutated in human cancer cell lines. Nature. 2001;413:311–6.PubMedCrossRef

46.

Wingate H, Puskas A, Duong M, Bui T, Richardson D, et al. Low molecular weight cyclin E is specific in breast cancer and is associated with mechanisms of tumor progression. Cell Cycle. 2009;8:1062–8.PubMedCrossRef

47.

Wang L, Shao ZM. Cyclin E expression and prognosis in breast cancer patients: a meta-analysis of published studies. Cancer Invest. 2006;24:581–7.PubMedCrossRef

48.

Begg CB, Berlin JA. Publication bias: a problem in interpreting medical data. J R Stat Soc A. 1988;151:419–63.CrossRef

Title: Prognostic value of cyclin E expression in breast cancer: a meta-analysis
Authors: Sheng Gao
Jing-Jing Ma
Cheng Lu
Publication date: 01-12-2013
Publisher: Springer Netherlands
Published in: Tumor Biology / Issue 6/2013
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI: https://doi.org/10.1007/s13277-013-0915-8

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