Molecular Oncology
Volume 2, Issue 3 , Pages 223-232 , October 2008

Estradiol–estrogen receptor: A key interplay of the expression of syndecan-2 and metalloproteinase-9 in breast cancer cells

  • Olga Ch. Kousidou

      Affiliations

    • Laboratory of Biochemistry, Section of Organic Chemistry, Biochemistry and Natural Products, Department of Chemistry, University of Patras, 261 10 Patras, Greece
  • ,
  • Aikaterini Berdiaki

      Affiliations

    • Department of Histology, School of Medicine, University of Crete, Heraklion, Greece
  • ,
  • Dimitris Kletsas

      Affiliations

    • Laboratory of Cell Proliferation and Ageing, Institute of Biology, N.C.S.R. “Demokritos”, 153 10 Athens, Greece
  • ,
  • Alexandros Zafiropoulos

      Affiliations

    • Department of Histology, School of Medicine, University of Crete, Heraklion, Greece
  • ,
  • Achilleas D. Theocharis

      Affiliations

    • Laboratory of Biochemistry, Section of Organic Chemistry, Biochemistry and Natural Products, Department of Chemistry, University of Patras, 261 10 Patras, Greece
  • ,
  • George N. Tzanakakis

      Affiliations

    • Department of Histology, School of Medicine, University of Crete, Heraklion, Greece
  • ,
  • Nikos K. Karamanos

      Affiliations

    • Laboratory of Biochemistry, Section of Organic Chemistry, Biochemistry and Natural Products, Department of Chemistry, University of Patras, 261 10 Patras, Greece
    • Corresponding Author InformationCorresponding author. Tel.: +30 2610 997915; fax: +30 2610 997153.

Received 24 April 2008 ,Revised 5 June 2008 ,Accepted 10 June 2008.

References 

  1. Alarid ET, Bakopoulos N, Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol. Endocrinol. 1999;13:1522–1534
  2. Ali S, Coombes RC. Estrogen receptor alpha in human breast cancer: occurrence and significance. J. Mammary Gland Biol. Neoplasia. 2000;5:271–281
  3. Beauvais DLM, Rapraeger A. Syndecans in tumor cell adhesion and signaling. Reprod. Biol. Endocrinol. 2004;2:1–12
  4. Borras M, Hardy L, Lempereur F, El Khissiin AH, Legros N, Gol-Winkler R, et al. Estradiol-induced down-regulation of estrogen receptor. Effect of various modulators of protein synthesis and expression. J. Steroid Biochem. Mol. Biol. 1994;48:325–336
  5. Capony F, Morisset M, Barrett AJ, Capony JP, Broquet P, Vignon F, et al. Phosphorylation, glycosylation, and proteolytic activity of the 52-kD estrogen-induced protein secreted by MCF-7 cells. J. Cell Biol. 1987;104:253–262
  6. Dobra K, Andäng M, Syrokou A, Karamanos NK, Hjerpe A. Differentiation of mesothelioma cells is influenced by the expression of proteoglycans. Exp. Cell Res. 2000;258:12–22
  7. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2002;2:161–174
  8. El Khissiin A, Leclercq G. Implication of proteasome in estrogen receptor degradation. FEBS Lett. 1999;448:160–166
  9. Elkin M, Cohen I, Zcharia E, Orgel A, Guatta-Rangini Z, Peretz T, et al. Regulation of heparanase gene expression by estrogen in breast cancer. Cancer Res. 2003;63:8821–8826
  10. Essner JJ, Chenb E, Ekker SC. Syndecan-2. Int. J. Biochem. Cell Biol. 2006;38:152–156
  11. Fan M, Nakshatri H, Nephew KP. Inhibiting proteasomal proteolysis sustains estrogen receptor-alpha activation. Mol. Endocrinol. 2004;18:2603–2615
  12. Fernandez HA, Kallenbach K, Seghezzi G, Grossi E, Colvin S, Schneider R, et al. Inhibition of endothelial cell migration by gene transfer of tissue inhibitor of metalloproteinases-1. J. Surg. Res. 1999;82:156–162
  13. Gustafsson JA, Warner M. Estrogen receptor beta in the breast: role in estrogen responsiveness and development of breast cancer. J. Steroid Biochem. Mol. Biol. 2000;74:245–248
  14. Han I, Park H, Oh ES. New insights into syndecan-2 expression and tumorigenic activity in colon carcinoma cells. J. Mol. Histol. 2004;35:319–326
  15. Haslam SZ, Nummy KA. The ontogeny and cellular distribution of estrogen receptors in normal mouse mammary gland. J. Steroid Biochem. Mol. Biol. 1992;42:589–595
  16. Haslam SZ, Woodward TL. Reciprocal regulation of extracellular matrix proteins and ovarian steroid activity in the mammary gland. Breast Cancer Res. 2001;3:365–372
  17. Henderson BE, Feigelson HS. Hormonal carcinogenesis. Carcinogenesis. 2000;21:427–433
  18. Jayson GC, Vives C, Paraskeva C, Schofield K, Coutts J, Fleetwood A, et al. Coordinated modulation of the fibroblast growth factor dual receptor mechanism during transformation from human colon adenoma to carcinoma. Int. J. Cancer. 1999;82:298–304
  19. Jensen EV, Jordan VC. The estrogen receptor: a model for molecular medicine. Clin. Cancer Res. 2003;9:1980–1989
  20. Khan SA, Rogers MA, Khurana KK, Meguid MM, Numann PJ. Estrogen receptor expression in benign breast epithelium and breast cancer risk. J. Natl. Cancer Inst. 1998;90:37–42
  21. Kousidou O Ch, Mitropoulou TN, Roussidis AE, Kletsas D, Theocharis AD, Karamanos NK. Genistein suppresses the invasive potential of human breast cancer cells through transcriptional regulation of metalloproteinases and their tissue inhibitors. Int. J. Oncol. 2005;26:1101–1109
  22. Kuiper GGJM, Carlsson B, Grandien K, Enmark E. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta Endocrinology. 1997;138:863–870
  23. Laïos I, Journé F, Nonclercq D, Vidal DS, Toillon RA, Laurent G, et al. Role of the proteasome in the regulation of estrogen receptor alpha turnover and function in MCF-7 breast carcinoma cells. J. Steroid Biochem. Mol. Biol. 2005;94:347–359
  24. Lafleur MA, Handsley MM, Knauper V, Murphy G, Edwards DR. Endothelial tubulogenesis within fibrin gels specifically requires the activity of membrane-type-matrix metalloproteinases (MT-MMPs). J. Cell Sci. 2002;115:3427–3438
  25. Li G, Fridman R, Kim HR. Tissue inhibitor of metalloproteinase-1 inhibits apoptosis of human breast epithelial cells. Cancer Res. 1999;59:6267–6275
  26. Liotta LA, Kohn EC. The microenvironment of the tumour-host interface. Nature. 2001;411:375–379
  27. Losordo DW, Isner JM. Estrogen and angiogenesis: A review. Arterioscler Thromb. Vasc. Biol. 2001;21:6–12
  28. Luparello C, Avanzato G, Carella C, Pucci-Minafra I. Tissue inhibitor of metalloprotease (TIMP)-1 and proliferative behaviour of clonal breast cancer cells. Breast Cancer Res. Treat. 1999;54:235–244
  29. McDonnell DP, Norris JD. Connections and regulation of the human estrogen receptor. Science. 2002;296:1642–1644
  30. Mitropoulou TN, Tzanakakis GN, Kletsas D, Kalofonos HP, Karamanos NK. Letrozole as a potent inhibitor of cell proliferation and expression of metalloproteinases (MMP-2 and MMP-9) by human epithelial breast cancer cells. Int. J. Cancer. 2003;104:155–160
  31. Nilsson U, Garvin S, Dabrosin C. MMP-2 and MMP-9 activity is regulated by estradiol and tamoxifen in cultured human breast cancer cells. Breast Cancer Res. Treat. 2007;102:253–261
  32. Paech K, Webb P, Kuiper GG, Nilsson S, Gustatsson J, Kushner PJ, et al. Differential ligand activation of estrogen receptors ERα and ERβ at AP-1 sites. Science. 1997;277:1508–1510
  33. Palmieri C, Cheng GJ, Saji S, Zelada-Hedman M, Warri A, Weihua Z, et al. Endocrine-Related Cancer. 2002;9:1–13
  34. Pang H, Faber LE. Estrogen and rapamycin effects on cell cycle progression in T47D breast cancer cells. Breast Cancer Res. Treat. 2001;70:21–26
  35. Park H, Kim Y, Lim Y, Han I, Oh ES. Syndecan-2 mediates adhesion and proliferation of colon carcinoma cells. J. Biol. Chem. 2002;277:29730–29736
  36. Rochefort H, Capony F, Garcia M, Cavailles V, Freiss G, Chambon M, et al. Estrogen-induced lysosomal proteases secreted by breast cancer cells: A role in carcinogenesis?. J. Cell. Biochem. 1987;35:17–29
  37. Ruohola JK, Valve EM, Karkkainen MJ, Joukov V, Alitalo K, Harkonen PL. Vascular endothelial growth factors are differentially regulated by steroid hormones and antiestrogens in breast cancer cells. Mol. Cell Endocrinol. 1999;149:29–40
  38. Russo J, Ao X, Grill C, Russo IH. Pattern of distribution of cells positive for estrogen receptor alpha and progesterone receptor in relation to proliferating cells in the mammary gland. Breast Cancer Res. Treat. 1999;53:217–227
  39. Saceda M, Lippman ME, Chambon P, Lindsey RL, Ponglikitmongkol M, Puente M, et al. Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol. Endocr. 1988;2:1157–1162
  40. Shekhar MP, Werdell J, Santner SJ, Pauley RJ, Tait L. Breast stroma plays a dominant regulatory role in breast epithelial growth and differentiation: implications for tumor development and progression. Cancer Res. 2001;61:1320–1326
  41. Shoker BS, Jarvis C, Sibson DR, Walker C, Sloane JR. Oestrogen receptor expression in the normal and pre-cancerous breast. J. Pathol. 1999;188:237–244
  42. Stahtea XN, Roussidis AE, Kanakis I, Tzanakakis GN, Chalkiadakis G, Mavroudis D, et al. Imatinib inhibits colorectal cancer cell growth and suppresses stromal-induced growth stimulation, MT1-MMP expression and pro-MMP2 activation. Int J. Cancer. 2007;121:2808–2814
  43. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 2001;17:463–516
  44. Tateishi Y, Kawabe Y, Chiba T, Murata S, Ichikawa K, Murayama A, et al. Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor. EMBO J. 2004;23:4813–4823
  45. Tkachenko E, Rhodes JM, Simons M. Syndecans: new kids on the signaling block. Circ. Res. 2005;96:488–500
  46. Welgus HG, Stricklin GP. Human skin fibroblast collagenase inhibitor. Comparative studies in human connective tissues, serum, and amniotic fluid. J. Biol. Chem. 1983;258:12259–12264
  47. Wingrove CS, Garr E, Godsland IF, Stevenson JC. 17beta-oestradiol enhances release of matrix metalloproteinase-2 from human vascular smooth muscle cells. Biochim. Biophys. Acta. 1998;1406:169–174

PII: S1574-7891(08)00072-0

doi: 10.1016/j.molonc.2008.06.002

Molecular Oncology
Volume 2, Issue 3 , Pages 223-232 , October 2008