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The impact of cyclin D1 overexpression on the prognosis of ER-positive breast cancers: a meta-analysis

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Abstract

Cyclin D1 (CCND1), a key regulator of cell cycle progression, is overexpressed in many human cancers, including breast cancer. However, the impact of CCND1 overexpression in these cancers remains unclear and controversial. We conducted a systematic literature search in PubMed and EMBASE with the search terms “cyclin D1”, “CCND1”, “breast cancer”, “prognosis”, and potential studies for analysis were selected. Studies with survival data, including progression-free survival (PFS), overall survival (OS) or metastasis-free survival (MFS), were included in this meta-analysis. A total of 33 studies containing 8,537 cases were included. The combined hazard risk (HR) and its 95 % confidence interval (CI) of OS, PFS and MFS were 1.13 (95 % CI 0.87–1.47; P = 0.35), 1.25 (95 % CI 0.95–1.64; P = 0.12), and 1.04 (95 % CI 0.80–1.36; P = 0.76), respectively, for primary breast cancer patients with tumors exhibiting CCND1 overexpression. Interestingly, the impact of CCND1 expression on OS was a 1.67-fold (95 % CI 1.38–2.02; P = 0.00) increased risk for ER-positive breast cancer patients. However, CCND1 overexpression exhibited no association with the PFS or OS of patients who received epirubicin-based neoadjuvant chemotherapy, for which the P values were 0.63 and 0.47, respectively. In summary, CCND1 overexpression impacts the prognosis of ER-positive breast cancer patients, but not patients with unselected primary breast cancer or patients treated with neoadjuvant chemotherapy.

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References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM. GLOBOCAN 2008 v2.0, Cancer incidence and mortality worldwide: IARC CancerBase No. 10 (Internet). Lyon, France: International Agency for Research on Cancer, 2010

  2. Guan X, Wang Y, Xie R, Chen L, Bai J, Lu J, Kuo MT (2010) p27(Kip1) as a prognostic factor in breast cancer: a systematic review and meta-analysis. J Cell Mol Med 14(4):944–953. doi:10.1111/j.1582-4934.2009.00730.x

    Article  PubMed  Google Scholar 

  3. Wang J, Guo Y, Wang B, Bi J, Li K, Liang X, Chu H, Jiang H (2012) Lymphatic microvessel density and vascular endothelial growth factor-C and -D as prognostic factors in breast cancer: a systematic review and meta-analysis of the literature. Mol Biol Rep 39(12):11153–11165. doi:10.1007/s11033-012-2024-y

    Article  PubMed  CAS  Google Scholar 

  4. Kim HS, Moon HG, Han W, Yom CK, Kim WH, Kim JH, Noh DY (2012) COX2 overexpression is a prognostic marker for Stage III breast cancer. Breast Cancer Res Treat 132(1):51–59. doi:10.1007/s10549-011-1521-3

    Article  PubMed  CAS  Google Scholar 

  5. Callagy GM, Webber MJ, Pharoah PD, Caldas C (2008) Meta-analysis confirms BCL2 is an independent prognostic marker in breast cancer. BMC Cancer 8:153. doi:10.1186/1471-2407-8-153

    Article  PubMed  Google Scholar 

  6. Motokura T, Arnold A (1993) Cyclin D and oncogenesis. Curr Opin Genet Dev 3(1):5–10

    Article  PubMed  CAS  Google Scholar 

  7. Strauss M, Lukas J, Bartek J (1995) Unrestricted cell cycling and cancer. Nat Med 1(12):1245–1246

    Article  PubMed  CAS  Google Scholar 

  8. Zwijsen RM, Buckle RS, Hijmans EM, Loomans CJ, Bernards R (1998) Ligand-independent recruitment of steroid receptor coactivators to estrogen receptor by cyclin D1. Genes Dev 12(22):3488–3498

    Article  PubMed  CAS  Google Scholar 

  9. Ahnstrom M, Nordenskjold B, Rutqvist LE, Skoog L, Stal O (2005) Role of cyclin D1 in ErbB2-positive breast cancer and tamoxifen resistance. Breast Cancer Res Treat 91(2):145–151. doi:10.1007/s10549-004-6457-4

    Article  PubMed  Google Scholar 

  10. Bukholm IR, Bukholm G, Nesland JM (2001) Over-expression of cyclin A is highly associated with early relapse and reduced survival in patients with primary breast carcinomas. Int J Cancer 93(2):283–287. doi:10.1002/ijc.1311

    Article  PubMed  CAS  Google Scholar 

  11. Choschzick M, Heilenkotter U, Lebeau A, Jaenicke F, Terracciano L, Bokemeyer C, Sauter G, Simon R (2010) MDM2 amplification is an independent prognostic feature of node-negative, estrogen receptor-positive early-stage breast cancer. Cancer Biomark 8(2):53–60. doi:10.3233/DMA-2011-0806

    PubMed  CAS  Google Scholar 

  12. Garcia V, Garcia JM, Pena C, Silva J, Dominguez G, Lorenzo Y, Diaz R, Espinosa P, de Sola JG, Cantos B, Bonilla F (2008) Free circulating mRNA in plasma from breast cancer patients and clinical outcome. Cancer Lett 263(2):312–320. doi:10.1016/j.canlet.2008.01.008

    Article  PubMed  CAS  Google Scholar 

  13. Guo LL, Gao P, Wu YG, Jian WC, Hao CY, Li H, Lin XY (2007) Alteration of cyclin D1 in Chinese patients with breast carcinoma and its correlation with Ki-67, pRb, and p53. Arch Med Res 38(8):846–852. doi:10.1016/j.arcmed.2007.06.004

    Article  PubMed  CAS  Google Scholar 

  14. Hwang TS, Han HS, Hong YC, Lee HJ, Paik NS (2003) Prognostic value of combined analysis of cyclin D1 and estrogen receptor status in breast cancer patients. Pathol Int 53(2):74–80

    Article  PubMed  CAS  Google Scholar 

  15. Kenny FS, Hui R, Musgrove EA, Gee JM, Blamey RW, Nicholson RI, Sutherland RL, Robertson JF (1999) Overexpression of cyclin D1 messenger RNA predicts for poor prognosis in estrogen receptor-positive breast cancer. Clin Cancer Res 5(8):2069–2076

    PubMed  CAS  Google Scholar 

  16. Lee A, Park WC, Yim HW, Lee MA, Park G, Lee KY (2007) Expression of c-erbB2, cyclin D1 and estrogen receptor and their clinical implications in the invasive ductal carcinoma of the breast. Jpn J Clin Oncol 37(9):708–714. doi:10.1093/jjco/hym082

    Article  PubMed  Google Scholar 

  17. Lim SC (2003) Role of COX-2, VEGF and cyclin D1 in mammary infiltrating duct carcinoma. Oncol Rep 10(5):1241–1249

    PubMed  CAS  Google Scholar 

  18. Lin SY, Xia W, Wang JC, Kwong KY, Spohn B, Wen Y, Pestell RG, Hung MC (2000) Beta-catenin, a novel prognostic marker for breast cancer: its roles in cyclin D1 expression and cancer progression. Proc Natl Acad Sci U S A 97(8):4262–4266. doi:10.1073/pnas.060025397

    Article  PubMed  CAS  Google Scholar 

  19. Lundgren K, Brown M, Pineda S, Cuzick J, Salter J, Zabaglo L, Howell A, Dowsett M, Landberg G (2012) Effects of cyclin D1 gene amplification and protein expression on time to recurrence in postmenopausal breast cancer patients treated with anastrozole or tamoxifen: a TransATAC study. Breast Cancer Res 14(2):R57. doi:10.1186/bcr3161

    Article  PubMed  CAS  Google Scholar 

  20. McIntosh GG, Anderson JJ, Milton I, Steward M, Parr AH, Thomas MD, Henry JA, Angus B, Lennard TW, Horne CH (1995) Determination of the prognostic value of cyclin D1 overexpression in breast cancer. Oncogene 11(5):885–891

    PubMed  CAS  Google Scholar 

  21. Michalides R, Hageman P, van Tinteren H, Houben L, Wientjens E, Klompmaker R, Peterse J (1996) A clinicopathological study on overexpression of cyclin D1 and of p53 in a series of 248 patients with operable breast cancer. Br J Cancer 73(6):728–734

    Article  PubMed  CAS  Google Scholar 

  22. Millar EK, Dean JL, McNeil CM, O’Toole SA, Henshall SM, Tran T, Lin J, Quong A, Comstock CE, Witkiewicz A, Musgrove EA, Rui H, Lemarchand L, Setiawan VW, Haiman CA, Knudsen KE, Sutherland RL, Knudsen ES (2009) Cyclin D1b protein expression in breast cancer is independent of cyclin D1a and associated with poor disease outcome. Oncogene 28(15):1812–1820. doi:10.1038/onc.2009.13

    Article  PubMed  CAS  Google Scholar 

  23. Pelosio P, Barbareschi M, Bonoldi E, Marchetti A, Verderio P, Caffo O, Bevilacqua P, Boracchi P, Buttitta F, Barbazza R, Dalla Palma P, Gasparini G (1996) Clinical significance of cyclin D1 expression in patients with node-positive breast carcinoma treated with adjuvant therapy. Ann Oncol 7(7):695–703

    Article  PubMed  CAS  Google Scholar 

  24. Peurala E, Koivunen P, Haapasaari KM, Bloigu R, Jukkola-Vuorinen A (2013) The prognostic significance and value of cyclin D1, CDK4 and p16 in human breast cancer. Breast Cancer Res 15(1):R5. doi:10.1186/bcr3376

    Article  PubMed  CAS  Google Scholar 

  25. Rudas M, Lehnert M, Huynh A, Jakesz R, Singer C, Lax S, Schippinger W, Dietze O, Greil R, Stiglbauer W, Kwasny W, Grill R, Stierer M, Gnant MF, Filipits M (2008) Cyclin D1 expression in breast cancer patients receiving adjuvant tamoxifen-based therapy. Clin Cancer Res 14(6):1767–1774. doi:10.1158/1078-0432.CCR-07-4122

    Article  PubMed  CAS  Google Scholar 

  26. Takano Y, Takenaka H, Kato Y, Masuda M, Mikami T, Saegusa M, Okayasu I (1999) Cyclin D1 overexpression in invasive breast cancers: correlation with cyclin-dependent kinase 4 and oestrogen receptor overexpression, and lack of correlation with mitotic activity. J Cancer Res Clin Oncol 125(8–9):505–512

    Article  PubMed  CAS  Google Scholar 

  27. Tobin NP, Lundgren KL, Conway C, Anagnostaki L, Costello S, Landberg G (2012) Automated image analysis of cyclin D1 protein expression in invasive lobular breast carcinoma provides independent prognostic information. Hum Pathol 43(11):2053–2061. doi:10.1016/j.humpath.2012.02.015

    Article  PubMed  CAS  Google Scholar 

  28. Umekita Y, Ohi Y, Sagara Y, Yoshida H (2002) Overexpression of cyclinD1 predicts for poor prognosis in estrogen receptor-negative breast cancer patients. Int J Cancer 98(3):415–418. doi:10.1002/ijc.10151

    Article  PubMed  CAS  Google Scholar 

  29. Utsumi T, Yoshimura N, Maruta M, Takeuchi S, Ando J, Mizoguchi Y, Harada N (2000) Correlation of cyclin D1 MRNA levels with clinico-pathological parameters and clinical outcome in human breast carcinomas. Int J Cancer 89(1):39–43. doi:10.1002/(SICI)1097-0215(20000120)89:1<39:AID-IJC7>3.0.CO2-T

    Article  PubMed  CAS  Google Scholar 

  30. van Diest PJ, Michalides RJ, Jannink L, van der Valk P, Peterse HL, de Jong JS, Meijer CJ, Baak JP (1997) Cyclin D1 expression in invasive breast cancer. Correlations and prognostic value. Am J Pathol 150(2):705–711

    PubMed  Google Scholar 

  31. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer 93(4):387–391. doi:10.1038/sj.bjc.6602678

    Article  PubMed  CAS  Google Scholar 

  32. Chen M, Cai E, Huang J, Yu P, Li K (2012) Prognostic value of vascular endothelial growth factor expression in patients with esophageal cancer: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 21(7):1126–1134. doi:10.1158/1055-9965.EPI-12-0020

    Article  PubMed  CAS  Google Scholar 

  33. Parmar MK, Torri V, Stewart L (1998) Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 17(24):2815–2834. doi:10.1002/(SICI)1097-0258(19981230)17:24<2815:AID-SIM110>3.0.CO2-8

    Article  PubMed  CAS  Google Scholar 

  34. Xu XL, Ling ZQ, Chen SZ, Li B, Ji WH, Mao WM (2013) The impact of E-cadherin expression on the prognosis of esophageal cancer: a meta-analysis. Dis Esophagus. doi:10.1111/dote.12024

  35. Tierney JFSL, Ghersi D, Burdett S, Sydes MR (2007) Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8:16

    Article  PubMed  Google Scholar 

  36. Yusuf S, Peto R, Lewis J, Collins R, Sleight P (1985) Beta blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis 27(5):335–371

    Article  PubMed  CAS  Google Scholar 

  37. Dublin EA, Patel NK, Gillett CE, Smith P, Peters G, Barnes DM (1998) Retinoblastoma and p16 proteins in mammary carcinoma: their relationship to cyclin D1 and histopathological parameters. Int J Cancer 79(1):71–75. doi:10.1002/(SICI)1097-0215(19980220)79:1<71:AID-IJC14>3.0.CO2-K

    Article  PubMed  CAS  Google Scholar 

  38. Gillett CE, Smith P, Peters G, Lu X, Barnes DM (1999) Cyclin-dependent kinase inhibitor p27Kip1 expression and interaction with other cell cycle-associated proteins in mammary carcinoma. J Pathol 187(2):200–206. doi:10.1002/(SICI)1096-9896(199901)187:2<200:AID-PATH228>3.0.CO;2-M

    Article  PubMed  CAS  Google Scholar 

  39. Husdal A, Bukholm G, Bukholm IR (2006) The prognostic value and overexpression of cyclin A is correlated with gene amplification of both cyclin A and cyclin E in breast cancer patient. Cell Oncol 28(3):107–116

    PubMed  CAS  Google Scholar 

  40. Lim SC, Lee MS (2002) Significance of E-cadherin/beta-catenin complex and cyclin D1 in breast cancer. Oncol Rep 9(5):915–928

    PubMed  CAS  Google Scholar 

  41. Bostner J, Ahnstrom Waltersson M, Fornander T, Skoog L, Nordenskjold B, Stal O (2007) Amplification of CCND1 and PAK1 as predictors of recurrence and tamoxifen resistance in postmenopausal breast cancer. Oncogene 26(49):6997–7005. doi:10.1038/sj.onc.1210506

    Article  PubMed  CAS  Google Scholar 

  42. Elsheikh S, Green AR, Aleskandarany MA, Grainge M, Paish CE, Lambros MB, Reis-Filho JS, Ellis IO (2008) CCND1 amplification and cyclin D1 expression in breast cancer and their relation with proteomic subgroups and patient outcome. Breast Cancer Res Treat 109(2):325–335. doi:10.1007/s10549-007-9659-8

    Article  PubMed  CAS  Google Scholar 

  43. Rodriguez C, Hughes-Davies L, Valles H, Orsetti B, Cuny M, Ursule L, Kouzarides T, Theillet C (2004) Amplification of the BRCA2 pathway gene EMSY in sporadic breast cancer is related to negative outcome. Clin Cancer Res 10(17):5785–5791. doi:10.1158/1078-0432.CCR-03-0410

    Article  PubMed  CAS  Google Scholar 

  44. Aaltonen K, Amini RM, Landberg G, Eerola H, Aittomaki K, Heikkila P, Nevanlinna H, Blomqvist C (2009) Cyclin D1 expression is associated with poor prognostic features in estrogen receptor positive breast cancer. Breast Cancer Res Treat 113(1):75–82. doi:10.1007/s10549-008-9908-5

    Article  PubMed  CAS  Google Scholar 

  45. Jacquemier J, Charafe-Jauffret E, Monville F, Esterni B, Extra JM, Houvenaeghel G, Xerri L, Bertucci F, Birnbaum D (2009) Association of GATA3, P53, Ki67 status and vascular peritumoral invasion are strongly prognostic in luminal breast cancer. Breast Cancer Res 11(2):R23. doi:10.1186/bcr2249

    Article  PubMed  Google Scholar 

  46. Kreike B, Hart G, Bartelink H, van de Vijver MJ (2010) Analysis of breast cancer related gene expression using natural splines and the Cox proportional hazard model to identify prognostic associations. Breast Cancer Res Treat 122(3):711–720. doi:10.1007/s10549-009-0588-6

    Article  PubMed  Google Scholar 

  47. Perez-Tenorio G, Karlsson E, Waltersson MA, Olsson B, Holmlund B, Nordenskjold B, Fornander T, Skoog L, Stal O (2011) Clinical potential of the mTOR targets S6K1 and S6K2 in breast cancer. Breast Cancer Res Treat 128(3):713–723. doi:10.1007/s10549-010-1058-x

    Article  PubMed  CAS  Google Scholar 

  48. Bonnefoi H, Diebold-Berger S, Therasse P, Hamilton A, van de Vijver M, MacGrogan G, Shepherd L, Amaral N, Duval C, Drijkoningen R, Larsimont D, Piccart M (2003) Locally advanced/inflammatory breast cancers treated with intensive epirubicin-based neoadjuvant chemotherapy: are there molecular markers in the primary tumour that predict for 5-year clinical outcome? Ann Oncol 14(3):406–413

    Article  PubMed  CAS  Google Scholar 

  49. Chen S, Chen CM, Yu KD, Yang WT, Shao ZM (2012) A prognostic model to predict outcome of patients failing to achieve pathological complete response after anthracycline-containing neoadjuvant chemotherapy for breast cancer. J Surg Oncol 105(6):577–585. doi:10.1002/jso.22140

    Article  PubMed  CAS  Google Scholar 

  50. Wachter DL, Fasching PA, Haeberle L, Schulz-Wendtland R, Dimmler A, Koscheck T, Renner SP, Lux MP, Beckmann MW, Hartmann A, Rauh C, Schrauder MG (2013) Prognostic molecular markers and neoadjuvant therapy response in anthracycline-treated breast cancer patients. Arch Gynecol Obstet 287(2):337–344. doi:10.1007/s00404-012-2534-9

    Article  PubMed  CAS  Google Scholar 

  51. Mahdey HM, Ramanathan A, Ismail SM, Abraham MT, Jamaluddin M, Zain RB (2011) Cyclin D1 amplification in tongue and cheek squamous cell carcinoma. Asian Pac J Cancer Prev 12(9):2199–2204

    PubMed  Google Scholar 

  52. Wang MT, Chen G, An SJ, Chen ZH, Huang ZM, Xiao P, Ben XS, Xie Z, Chen SL, Luo DL, Tang JM, Lin JY, Zhang XC, Wu YL (2012) Prognostic significance of cyclinD1 amplification and the co-alteration of cyclinD1/pRb/ppRb in patients with esophageal squamous cell carcinoma. Dis Esophagus 25(7):664–670. doi:10.1111/j.1442-2050.2011.01291.x

    Article  PubMed  Google Scholar 

  53. Brennan DJ, Jirstrom K, Kronblad A, Millikan RC, Landberg G, Duffy MJ, Ryden L, Gallagher WM, O’Brien SL (2006) 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 12(21):6421–6431. doi:10.1158/1078-0432.CCR-06-0480

    Article  PubMed  CAS  Google Scholar 

  54. Muss HB, Bunn JY, Crocker A, Plaut K, Koh J, Heintz N, Rincon M, Weaver DL, Tam D, Beatty B, Kaufman P, Donovan M, Verbel D, Weiss L (2007) Cyclin D-1, interleukin-6, HER-2/neu, transforming growth factor receptor-II and prediction of relapse in women with early stage, hormone receptor-positive breast cancer treated with tamoxifen. Breast J 13(4):337–345. doi:10.1111/j.1524-4741.2007.00440.x

    Article  PubMed  CAS  Google Scholar 

  55. Nielsen NH, Emdin SO, Cajander J, Landberg G (1997) Deregulation of cyclin E and D1 in breast cancer is associated with inactivation of the retinoblastoma protein. Oncogene 14(3):295–304. doi:10.1038/sj.onc.1200833

    Article  PubMed  CAS  Google Scholar 

  56. Reed W, Florems VA, Holm R, Hannisdal E, Nesland JM (1999) Elevated levels of p27, p21 and cyclin D1 correlate with positive oestrogen and progesterone receptor status in node-negative breast carcinoma patients. Virchows Arch 435(2):116–124

    Article  PubMed  CAS  Google Scholar 

  57. Reed W, Sandstad B, Holm R, Nesland JM (2003) The prognostic impact of hormone receptors and c-erbB-2 in pregnancy-associated breast cancer and their correlation with BRCA1 and cell cycle modulators. Int J Surg Pathol 11(2):65–74

    Article  PubMed  CAS  Google Scholar 

  58. Peters MG, Vidal Mdel C, Gimenez L, Mauro L, Armanasco E, Cresta C, Bal de Kier Joffe E, Puricelli L (2004) Prognostic value of cell cycle regulator molecules in surgically resected stage I and II breast cancer. Oncol Rep 12(5):1143–1150

    PubMed  CAS  Google Scholar 

  59. Olsson A, Borgquist S, Butt S, Zackrisson S, Landberg G, Manjer J (2012) Tumour-related factors and prognosis in breast cancer detected by screening. Br J Surg 99(1):78–87. doi:10.1002/bjs.7757

    Article  PubMed  CAS  Google Scholar 

  60. Nicolini A, Campani D, Miccoli P, Spinelli C, Carpi A, Menicagli M, Ferrari P, Gadducci G, Rossi G, Fini M, Giavaresi G, Bonazzi V, Giardino R (2004) Vascular endothelial growth factor (VEGF) and other common tissue prognostic indicators in breast cancer: a case-control study. Int J Biol Markers 19(4):275–281

    PubMed  CAS  Google Scholar 

  61. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lonning PE, Borresen-Dale AL (2001) Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 98(19):10869–10874. doi:10.1073/pnas.191367098

    Article  PubMed  CAS  Google Scholar 

  62. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lonning PE, Brown PO, Borresen-Dale AL, Botstein D (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100(14):8418–8423. doi:10.1073/pnas.0932692100

    Article  PubMed  CAS  Google Scholar 

  63. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406(6797):747–752. doi:10.1038/35021093

    Article  PubMed  CAS  Google Scholar 

  64. Bennis S, Abbass F, Akasbi Y, Znati K, Joutei KA, El Mesbahi O, Amarti A (2012) Prevalence of molecular subtypes and prognosis of invasive breast cancer in north-east of Morocco: retrospective study. BMC Res Notes 5:436. doi:10.1186/1756-0500-5-436

    Article  PubMed  Google Scholar 

  65. Su Y, Zheng Y, Zheng W, Gu K, Chen Z, Li G, Cai Q, Lu W, Shu XO (2011) Distinct distribution and prognostic significance of molecular subtypes of breast cancer in Chinese women: a population-based cohort study. BMC Cancer 11:292. doi:10.1186/1471-2407-11-292

    Article  PubMed  Google Scholar 

  66. Gao CY, Zelenka PS (1997) Cyclins, cyclin-dependent kinases and differentiation. BioEssays 19(4):307–315. doi:10.1002/bies.950190408

    Article  PubMed  Google Scholar 

  67. Stendahl M, Kronblad A, Ryden L, Emdin S, Bengtsson NO, Landberg G (2004) Cyclin D1 overexpression is a negative predictive factor for tamoxifen response in postmenopausal breast cancer patients. Br J Cancer 90(10):1942–1948. doi:10.1038/sj.bjc.6601831

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Jian-Guo Feng at Zhejiang Cancer Hospital (Zhejiang Cancer Research Institute) for data statistics assistance. This study was supported by Province important technology and science (Special feature of major province scientific and technological 2011), No. 2011C13039-1, 2011–2014, and the establishment and NSFC general program, No. 81172081, 2012.01-2015-12.

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The authors declare that they have no conflict of interest.

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  1. Key Laboratory on Diagnosis and Treatment Technology on Thoracic Cancer, Zhejiang Cancer Hospital (Zhejiang Cancer Research Institute), Hangzhou, No. 38 Guangji Road, Banshanqiao District, Hangzhou, 310022, China

    Xiao-Ling Xu, Wei Chen, Bo Li & Wei-Min Mao

  2. Department of Breast Surgery, Lishui Centre Hospital, Lishui, 323000, China

    Shu-Zheng Chen

  3. Department of Breast Surgery, Zhejiang Cancer Hospital, Hangzhou, 310022, China

    Wei-Hui Zheng, Xiang-Hou Xia & Hong-Jian Yang

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Xu, XL., Chen, SZ., Chen, W. et al. The impact of cyclin D1 overexpression on the prognosis of ER-positive breast cancers: a meta-analysis. Breast Cancer Res Treat 139, 329–339 (2013). https://doi.org/10.1007/s10549-013-2563-5

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