Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014 (2014), Article ID 124321, 13 pages
http://dx.doi.org/10.1155/2014/124321
Review Article

The Motile Breast Cancer Phenotype Roles of Proteoglycans/Glycosaminoglycans

1Laboratory of Anatomy-Histology-Embryology, Medical School, University of Crete, 71003 Heraklion, Greece
2Dipartimento di Scienze Chirurgiche e Morfologiche, Università degli Studi dell’Insubria, Via J.H. Dunant 5, 21100 Varese, Italy

Received 9 May 2014; Accepted 2 July 2014; Published 22 July 2014

Academic Editor: Ilona Kovalszky

Copyright © 2014 Dragana Nikitovic et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Nikitovic, A. Papoutsidakis, N. K. Karamanos, and G. N. Tzanakakis, “Lumican affects tumor cell functions, tumor-ECM interactions, angiogenesis and inflammatory response,” Matrix Biology, vol. 35, pp. 206–214, 2014. View at Publisher · View at Google Scholar
  2. D. Nikitovic, K. Kouvidi, N. K. Karamanos, and G. N. Tzanakakis, “The roles of hyaluronan/RHAMM/CD44 and their respective interactions along the insidious pathways of fibrosarcoma progression,” BioMed Research International, vol. 2013, Article ID 929531, 12 pages, 2013. View at Publisher · View at Google Scholar
  3. D. Nikitovic, M. Mytilinaiou, A. Berdiaki, N. K. Karamanos, and G. N. Tzanakakis, “Heparan sulfate proteoglycans and heparin regulate melanoma cell functions,” Biochimica et Biophysica Acta, vol. 1840, no. 8, pp. 2471–2481, 2014. View at Google Scholar
  4. K. Kouvidi, A. Berdiaki, D. Nikitovic et al., “Role of Receptor for Hyaluronic Acid-mediated Motility (RHAMM) in Low Molecular Weight Hyaluronan (LMWHA)-mediated fibrosarcoma cell adhesion,” Journal of Biological Chemistry, vol. 286, no. 44, pp. 38509–38520, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Mytilinaiou, A. Bano, D. Nikitovic et al., “Syndecan-2 is a key regulator of transforming growth factor beta 2/smad2-mediated adhesion in fibrosarcoma cells,” IUBMB Life, vol. 65, no. 2, pp. 134–143, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. G. Chalkiadaki, D. Nikitovic, P. Katonis et al., “Low molecular weight heparin inhibits melanoma cell adhesion and migration through a PKCa/JNK signaling pathway inducing actin cytoskeleton changes,” Cancer Letters, vol. 312, no. 2, pp. 235–244, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. J. D. S. Antonio and R. V. Iozzo, “Glycosaminoglycans: Structure and Biological Functions,” eLS, 2001. View at Google Scholar
  8. A. Syrokou, G. Tzanakakis, T. Tsegenidis, A. Hjerpe, and N. K. Karamanos, “Effects of glycosaminoglycans on proliferation of epithelial and fibroblast human malignant mesothelioma cells: a structure-function relationship,” Cell Proliferation, vol. 32, no. 2-3, pp. 85–99, 1999. View at Publisher · View at Google Scholar · View at Scopus
  9. T. N. Mitropoulou, G. N. Tzanakakis, D. Nikitovic, A. Tsatsakis, and N. K. Karamanos, “In vitro effects of genistein on the synthesis and distribution of glycosaminoglycans / proteoglycans by estrogen receptor-positive and -negative human breast cancer epithelial cells,” Anticancer Research, vol. 22, no. 5, pp. 2841–2846, 2002. View at Google Scholar · View at Scopus
  10. C. B. N. Mendes de Aguiar, B. Lobão-Soares, M. Alvarez-Silva, and A. Gonçalves Trentin, “Glycosaminoglycans modulate C6 glioma cell adhesion to extracellular matrix components and alter cell proliferation and cell migration,” BMC Cell Biology, vol. 6, article 31, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Afratis, C. Gialeli, D. Nikitovic et al., “Glycosaminoglycans: key players in cancer cell biology and treatment,” The FEBS Journal, vol. 279, no. 7, pp. 1177–1197, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. A. D. Theocharis, S. S. Skandalis, G. N. Tzanakakis, and N. K. Karamanos, “Proteoglycans in health and disease: novel roles for proteoglycans in malignancy and their pharmacological targeting,” FEBS Journal, vol. 277, no. 19, pp. 3904–3923, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. R. V. Iozzo, “Matrix proteoglycans: from molecular design to cellular function,” Annual Review of Biochemistry, vol. 67, pp. 609–652, 1998. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Schaefer and R. M. Schaefer, “Proteoglycans: from structural compounds to signaling molecules,” Cell and Tissue Research, vol. 339, no. 1, pp. 237–246, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. P. P. Provenzano, K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely, “Collagen reorganization at the tumor-stromal interface facilitates local invasion,” BMC Medicine, vol. 4, article 38, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. K. R. Levental, H. Yu, L. Kass et al., “Matrix crosslinking forces tumor progression by enhancing integrin signaling,” Cell, vol. 139, no. 5, pp. 891–906, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Lu, V. M. Weaver, and Z. Werb, “The extracellular matrix: a dynamic niche in cancer progression,” Journal of Cell Biology, vol. 196, no. 4, pp. 395–406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. R. V. Iozzo, “The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins,” Journal of Biological Chemistry, vol. 274, no. 27, pp. 18843–18846, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. J. L. Andres, D. DeFalcis, M. Noda, and J. Massague, “Binding of two growth factor families to separate domains of the proteoglycan betaglycan,” Journal of Biological Chemistry, vol. 267, no. 9, pp. 5927–5930, 1992. View at Google Scholar · View at Scopus
  20. M. Bernfield, R. Kokenyesi, M. Kato et al., “Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans,” Annual Review of Cell Biology, vol. 8, pp. 365–393, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Leivonen, J. Lundin, S. Nordling, K. von Boguslawski, and C. Haglund, “Prognostic value of syndecan-1 expression in breast cancer,” Oncology, vol. 67, no. 1, pp. 11–18, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. M. J. Stanley, M. W. Stanley, R. D. Sanderson, and R. Zera, “Syndecan-1 expression is induced in the stroma of infiltrating breast carcinoma,” American Journal of Clinical Pathology, vol. 112, no. 3, pp. 377–383, 1999. View at Google Scholar · View at Scopus
  23. T. Maeda, C. M. Alexander, and A. Friedl, “Induction of syndecan-1 expression in stromal fibroblasts promotes proliferation of human breast cancer cells,” Cancer Research, vol. 64, no. 2, pp. 612–621, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. M. V. Dhodapkar, T. Kelly, A. Theus, A. B. Athota, B. Barlogie, and R. D. Sanderson, “Elevated levels of shed syndecan-1 correlate with tumour mass and decreased matrix metalloproteinase-9 activity in the serum of patients with multiple myeloma,” British Journal of Haematology, vol. 99, no. 2, pp. 368–371, 1997. View at Google Scholar · View at Scopus
  25. Y. Yang, S. Yaccoby, W. Liu et al., “Soluble syndecan-1 promotes growth of myeloma tumors in vivo,” Blood, vol. 100, no. 2, pp. 610–617, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. M. E. Lendorf, T. Manon-Jensen, P. Kronqvist, H. A. B. Multhaupt, and J. R. Couchman, “Syndecan-1 and syndecan-4 are independent indicators in breast carcinoma,” Journal of Histochemistry and Cytochemistry, vol. 59, no. 6, pp. 615–629, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. F. Baba, K. Swartz, R. van Buren et al., “Syndecan-1 and syndecan-4 are overexpressed in an estrogen receptor-negative, highly proliferative breast carcinoma subtype,” Breast Cancer Research and Treatment, vol. 98, no. 1, pp. 91–98, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. C. J. Malavaki, A. E. Roussidis, C. Gialeli et al., “Imatinib as a key inhibitor of the platelet-derived growth factor receptor mediated expression of cell surface heparan sulfate proteoglycans and functional properties of breast cancer cells,” FEBS Journal, vol. 280, no. 10, pp. 2477–2489, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Mundhenke, K. Meyer, S. Drew, and A. Friedl, “Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 receptor binding in breast carcinomas,” American Journal of Pathology, vol. 160, no. 1, pp. 185–194, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Barbareschi, P. Maisonneuve, D. Aldovini et al., “High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis,” Cancer, vol. 98, no. 3, pp. 474–483, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Bernfield, M. Götte, P. W. Park et al., “Functions of cell surface heparan sulfate proteoglycans,” Annual Review of Biochemistry, vol. 68, pp. 729–777, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Lundström, L. Sahlin, L. Skoog et al., “Expression of Syndecan-1 in histologically normal breast tissue from postmenopausal women with breast cancer according to mammographic density,” Climacteric, vol. 9, no. 4, pp. 277–282, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Löfgren, L. Sahlin, S. Jiang et al., “Expression of syndecan-1 in paired samples of normal and malignant breast tissue from postmenopausal women,” Anticancer Research, vol. 27, no. 5, pp. 3045–3050, 2007. View at Google Scholar · View at Scopus
  34. M. Götte, C. Kersting, M. Ruggiero et al., “Predictive value of syndecan-1 expression for the response to neoadjuvant chemotherapy of primary breast cancer,” Anticancer Research, vol. 26, no. 1, pp. 621–627, 2006. View at Google Scholar · View at Scopus
  35. A. M. Tokes, A. M. Szasz, A. Farkas et al., “Stromal matrix protein expression following preoperative systemic therapy in breast cancer,” Clinical Cancer Research, vol. 15, no. 2, pp. 731–739, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Filmus, M. Capurro, and J. Rast, “Glypicans,” Genome Biology, vol. 9, no. 5, article 224, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Y. Xiang, V. Ladeda, and J. Filmus, “Glypican-3 expression is silenced in human breast cancer,” Oncogene, vol. 20, no. 50, pp. 7408–7412, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. A. D. Gonzalez, M. Kaya, W. Shi et al., “OCI-5/GPC3, a glypican encoded by a gene that is mutated in the Simpson-Golabi-Behmel overgrowth syndrome, induces apoptosis in a cell line-specific manner,” Journal of Cell Biology, vol. 141, no. 6, pp. 1407–1414, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. K. Matsuda, H. Maruyama, F. Guo et al., “Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells,” Cancer Research, vol. 61, no. 14, pp. 5562–5569, 2001. View at Google Scholar · View at Scopus
  40. T. N. Wight, “Versican: a versatile extracellular matrix proteoglycan in cell biology,” Current Opinion in Cell Biology, vol. 14, no. 5, pp. 617–623, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. A. R. Jeffs, A. C. Glover, L. J. Slobbe et al., “A gene expression signature of invasive potential in metastatic melanoma cells,” PLoS ONE, vol. 4, no. 12, Article ID e8461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Nara, Y. Kato, Y. Torii et al., “Immunohistochemical localization of extracellular matrix components in human breast tumours with special reference to PG-M/versican,” Histochemical Journal, vol. 29, no. 1, pp. 21–30, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Ricciardelli, J. H. Brooks, S. Suwiwat et al., “Regulation of stromal versican expression by breast cancer cells and importance to relapse-free survival in patients with node-negative primary breast cancer,” Clinical Cancer Research, vol. 8, no. 4, pp. 1054–1060, 2002. View at Google Scholar · View at Scopus
  44. C. Ricciardelli, K. Mayne, P. J. Sykes et al., “Elevated levels of versican but not decorin predict disease progression in early-stage prostate cancer,” Clinical Cancer Research, vol. 4, no. 4, pp. 963–971, 1998. View at Google Scholar · View at Scopus
  45. S. Suwiwat, C. Ricciardelli, R. Tammi et al., “Expression of extracellular matrix components versican, chondroitin sulfate, tenascin, and hyaluronan, and their association with disease outcome in node-negative breast cancer,” Clinical Cancer Research, vol. 10, no. 7, pp. 2491–2498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Canavese, G. Candelaresi, I. Castellano, and M. P. Mano, “Expression of proteoglycan versican in in situ breast lesions: relations between stromal changes, histotype, and invasion,” Pathology Research and Practice, vol. 207, no. 2, pp. 97–103, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. A. J. M. Yee, M. Akens, B. L. Yang, J. Finkelstein, P. Zheng, and Z. Deng, “The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis,” Breast Cancer Research, vol. 9, no. 4, article R42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. W. W. Du, B. B. Yang, T. A. Shatseva et al., “Versican G3 promotes mouse mammary tumor cell growth, migration, and metastasis by influencing EGF receptor signaling,” PLoS ONE, vol. 5, no. 11, Article ID e13828, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. W. W. Du, B. B. Yang, B. L. Yang et al., “Versican G3 domain modulates breast cancer cell apoptosis: a mechanism for breast cancer cell response to chemotherapy and egfr therapy,” PLoS ONE, vol. 6, no. 11, Article ID e26396, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Kischel, D. Waltregny, B. Dumont et al., “Versican overexpression in human breast cancer lesions: known and new isoforms for stromal tumor targeting,” International Journal of Cancer, vol. 126, no. 3, pp. 640–650, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. P. A. McEwan, P. G. Scott, P. N. Bishop, and J. Bella, “Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans,” Journal of Structural Biology, vol. 155, no. 2, pp. 294–305, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. L. Schaefer and R. V. Iozzo, “Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction,” Journal of Biological Chemistry, vol. 283, no. 31, pp. 21305–21309, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Leygue, L. Snell, H. Dotzlaw et al., “Lumican and decorin are differentially expressed in human breast carcinoma,” The Journal of Pathology, vol. 192, pp. 313–320, 2000. View at Google Scholar
  54. P. Boström, A. Sainio, T. Kakko, M. Savontaus, M. Söderström, and H. Järveläinen, “Localization of decorin gene expression in normal human breast tissue and in benign and malignant tumors of the human breast,” Histochemistry and Cell Biology, vol. 139, no. 1, pp. 161–171, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Troup, C. Njue, E. V. Kliewer et al., “Reduced expression of the small leucine-rich proteoglycans, lumican, and decorin is associated with poor outcome in node-negative invasive breast cancer,” Clinical Cancer Research, vol. 9, no. 1, pp. 207–214, 2003. View at Google Scholar · View at Scopus
  56. C. C. Reed, A. Waterhouse, S. Kirby et al., “Decorin prevents metastatic spreading of breast cancer,” Oncogene, vol. 24, no. 6, pp. 1104–1110, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Santra, I. Eichstetter, and R. V. Iozzo, “An anti-oncogenic role for decorin: down-regulation of ErbB2 leads to growth suppression and cytodifferentiation of mammary carcinoma cells,” The Journal of Biological Chemistry, vol. 275, no. 45, pp. 35153–35161, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Leygue, L. Snell, H. Dotzlaw et al., “Expression of lumican in human breast carcinoma,” Cancer Research, vol. 58, no. 7, pp. 1348–1352, 1998. View at Google Scholar · View at Scopus
  59. R. H. Tammi, A. Kultti, V. Kosma, R. Pirinen, P. Auvinen, and M. I. Tammi, “Hyaluronan in human tumors: pathobiological and prognostic messages from cell-associated and stromal hyaluronan,” Seminars in Cancer Biology, vol. 18, no. 4, pp. 288–295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. B. P. Toole, T. N. Wight, and M. I. Tammi, “Hyaluronan-cell interactions in cancer and vascular disease,” Journal of Biological Chemistry, vol. 277, no. 7, pp. 4593–4596, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Jojovic, B. Delpech, P. Prehm, and U. Schumacher, “Expression of hyaluronate and hyaluronate synthase in human primary tumours and their metastases in scid mice,” Cancer Letters, vol. 188, no. 1-2, pp. 181–189, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Auvinen, R. Tammi, J. Parkkinen et al., “Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival,” The American Journal of Pathology, vol. 156, no. 2, pp. 529–536, 2000. View at Publisher · View at Google Scholar · View at Scopus
  63. J. X. Tan, X. Y. Wang, H. Y. Li et al., “HYAL1 overexpression is correlated with the malignant behavior of human breast cancer,” International Journal of Cancer, vol. 128, no. 6, pp. 1303–1315, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Wells, J. Grahovac, S. Wheeler, B. Ma, and D. Lauffenburger, “Targeting tumor cell motility as a strategy against invasion and metastasis,” Trends in Pharmacological Sciences, vol. 34, no. 5, pp. 283–289, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. A. J. Ridley, “Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking,” Trends in Cell Biology, vol. 16, no. 10, pp. 522–529, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. A. K. Howe, “Regulation of actin-based cell migration by cAMP/PKA,” Biochimica et Biophysica Acta, vol. 1692, no. 2-3, pp. 159–174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Gehler, S. M. Ponik, K. M. Riching, and P. J. Keely, “Bi-Directional signaling: Extracellular matrix and integrin regulation of breast tumor progression,” Critical Reviews in Eukaryotic Gene Expression, vol. 23, no. 2, pp. 139–157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. J. Zhao and J. Guan, “Signal transduction by focal adhesion kinase in cancer,” Cancer and Metastasis Reviews, vol. 28, no. 1-2, pp. 35–49, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Hannigan, A. A. Troussard, and S. Dedhar, “Integrin-linked kinase: a cancer therapeutic target unique among its ILK,” Nature Reviews Cancer, vol. 5, no. 1, pp. 51–63, 2005. View at Publisher · View at Google Scholar · View at Scopus
  70. P. Savagner, “The epithelial-mesenchymal transition (EMT) phenomenon,” Annals of Oncology, vol. 21, supplement 7, pp. vii89–vii92, 2010. View at Publisher · View at Google Scholar · View at Scopus
  71. M. J. C. Hendrix, E. A. Seftor, Y. Chu, K. T. Trevor, and R. E. B. Seftor, “Role of intermediate filaments in migration, invasion and metastasis,” Cancer and Metastasis Reviews, vol. 15, no. 4, pp. 507–525, 1996. View at Publisher · View at Google Scholar · View at Scopus
  72. V. Quaranta, “Motility cues in the tumor microenvironment,” Differentiation, vol. 70, no. 9-10, pp. 590–598, 2002. View at Publisher · View at Google Scholar · View at Scopus
  73. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Publisher · View at Google Scholar · View at Scopus
  74. A. V. Marusyk, A. Almendro, and K. Polyak, “Intra-tumour heterogeneity: a looking glass for cancer?” Nature Reviews Cancer, vol. 12, no. 5, pp. 323–334, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Marcucci, M. Bellone, C. A. Caserta, and A. Corti, “Pushing tumor cells towards a malignant phenotype: stimuli from the microenvironment, intercellular communications and alternative roads,” International Journal of Cancer, vol. 135, no. 6, pp. 1265–1276, 2014. View at Publisher · View at Google Scholar
  76. J. P. Thiery, H. Acloque, R. Y. J. Huang, and M. A. Nieto, “Epithelial-mesenchymal transitions in development and disease,” Cell, vol. 139, no. 5, pp. 871–890, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Morel, M. Lièvre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux, “Generation of breast cancer stem cells through epithelial-mesenchymal transition,” PLoS ONE, vol. 3, no. 8, Article ID e2888, 2008. View at Publisher · View at Google Scholar · View at Scopus
  78. M. L. Ackland, D. F. Newgreen, M. Fridman et al., “Epidermal growth factor-induced epithelio-mesenchymal transition in human breast carcinoma cells,” Laboratory Investigation, vol. 83, no. 3, pp. 435–448, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Giampieri, C. Manning, S. Hooper, L. Jones, C. S. Hill, and E. Sahai, “Localized and reversible TGFβ signalling switches breast cancer cells from cohesive to single cell motility,” Nature Cell Biology, vol. 11, no. 11, pp. 1287–1296, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. A. Wicki, F. Lehembre, N. Wick, B. Hantusch, D. Kerjaschki, and G. Christofori, “Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton,” Cancer Cell, vol. 9, no. 4, pp. 261–272, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. M. Marsan, G. van den Eynden, R. Limame et al., “A core invasiveness gene signature reflects epithelial-to-mesenchymal transition but not metastatic potential in breast cancer cell lines and tissue samples,” PLoS ONE, vol. 21, Article ID e89262, 2014. View at Google Scholar
  82. D. Gao, L. T. Vahdat, S. Wong, J. C. Chang, and V. Mittal, “Microenvironmental regulation of epithelial-mesenchymal transitionsin cancer,” Cancer Research, vol. 72, no. 19, pp. 4883–4889, 2012. View at Publisher · View at Google Scholar · View at Scopus
  83. Q. Zheng, A. Safina, and A. V. Bakin, “Role of high-molecular weight tropomyosins in TGF-β-mediated control of cell motility,” International Journal of Cancer, vol. 122, no. 1, pp. 78–90, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Kim, B. C. Litzenburger, X. Cui et al., “Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-κB and snail,” Molecular and Cellular Biology, vol. 27, no. 8, pp. 3165–3175, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. H. Porsch, B. Bernert, M. Mehić, A. D. Theocharis, C. Heldin, and P. Heldin, “Efficient TGFβ-induced epithelial-mesenchymal transition depends on hyaluronan synthase HAS2,” Oncogene, vol. 32, pp. 4355–4365, 2013. View at Publisher · View at Google Scholar · View at Scopus
  86. H. C. Lien, Y. H. Lee, Y. M. Jeng, C. H. Lin, Y. S. Lu, and Y. T. Yao, “Differential expression of hyaluronan synthase 2 in breast carcinoma and its biological significance,” Histopathology, 2014. View at Publisher · View at Google Scholar
  87. A. K. Kiemer, K. Takeuchi, and M. P. Quinlan, “Identification of genes involved in epithelial-mesenchymal transition and tumor progression,” Oncogene, vol. 20, no. 46, pp. 6679–6688, 2001. View at Publisher · View at Google Scholar · View at Scopus
  88. C. Thomas and A. E. Karnoub, “Lysyl oxidase at the crossroads of mesenchymal stem cells and epithelial-mesenchymal transition,” Oncotarget, vol. 4, no. 3, pp. 376–377, 2013. View at Google Scholar · View at Scopus
  89. S. Maschler, S. Grunert, A. Danielopol, H. Beug, and G. Wirl, “Enhanced tenascin-C expression and matrix deposition during Ras/TGF-β-induced progression of mammary tumor cells,” Oncogene, vol. 23, no. 20, pp. 3622–3633, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. D. Loussouarn, L. Campion, C. Sagan et al., “Prognostic impact of syndecan-1 expression in invasive ductal breast carcinomas,” British Journal of Cancer, vol. 98, no. 12, pp. 1993–1998, 2008. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Götte, C. Kersting, I. Radke, L. Kiesel, and P. Wülfing, “An expression signature of syndecan-1 (CD138), E-cadherin and c-met is associated with factors of angiogenesis and lymphangiogenesis in ductal breast carcinoma in situ,” Breast Cancer Research, vol. 9, no. 1, article R8, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Gao, N. Joshi, H. Choi et al., “Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition,” Cancer Research, vol. 72, no. 6, pp. 1384–1394, 2012. View at Publisher · View at Google Scholar · View at Scopus
  93. C. Gialeli, A. D. Theocharis, and N. K. Karamanos, “Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting,” The FEBS Journal, vol. 278, no. 1, pp. 16–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  94. R. V. Iozzo, “The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth,” Critical Reviews in Biochemistry and Molecular Biology, vol. 32, no. 2, pp. 141–174, 1997. View at Google Scholar · View at Scopus
  95. S. Sarrazin, W. C. Lamanna, and J. D. Esko, “Heparan sulfate proteoglycans,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 7, Article ID a004952, 2011. View at Publisher · View at Google Scholar · View at Scopus
  96. D. M. Beauvais and A. C. Rapraeger, “Syndecans in tumor cell adhesion and signaling,” Reproductive Biology and Endocrinology, vol. 2, article 3, 2004. View at Publisher · View at Google Scholar · View at Scopus
  97. J. R. Couchman, “Syndecans: proteoglycan regulators of cell-surface microdomains?” Nature Reviews Molecular Cell Biology, vol. 4, no. 12, pp. 926–937, 2003. View at Publisher · View at Google Scholar · View at Scopus
  98. J. R. Couchman, “Transmembrane signaling proteoglycans,” Annual Review of Cell and Developmental Biology, vol. 26, pp. 89–114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Manon-Jensen, Y. Itoh, and J. R. Couchman, “Proteoglycans in health and disease: the multiple roles of syndecan shedding,” FEBS Journal, vol. 277, no. 19, pp. 3876–3889, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. X. Xian, S. Gopal, and J. R. Couchman, “Syndecans as receptors and organizers of the extracellular matrix,” Cell and Tissue Research, vol. 339, no. 1, pp. 31–46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. A. I. Tsonis, N. Afratis, C. Gialeli et al., “Evaluation of the coordinated actions of estrogen receptors with epidermal growth factor receptor and insulin-like growth factor receptor in the expression of cell surface heparan sulfate proteoglycans and cell motility in breast cancer cells,” FEBS Journal, vol. 280, no. 10, pp. 2248–2259, 2013. View at Publisher · View at Google Scholar · View at Scopus
  102. G. W. Yip, M. Smollich, and M. Götte, “Therapeutic value of glycosaminoglycans in cancer,” Molecular Cancer Therapeutics, vol. 5, no. 9, pp. 2139–2148, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. C. Y. Fears and A. Woods, “The role of syndecans in disease and wound healing,” Matrix Biology, vol. 25, no. 7, pp. 443–456, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. K. Lambaerts, S. A. Wilcox-Adelman, and P. Zimmermann, “The signaling mechanisms of syndecan heparan sulfate proteoglycans,” Current Opinion in Cell Biology, vol. 21, no. 5, pp. 662–669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  105. S. A. Ibrahim, G. W. Yip, C. Stock et al., “Targeting of syndecan-1 by microRNA miR-10b promotes breast cancer cell motility and invasiveness via a Rho-GTPase- and E-cadherin-dependent mechanism,” International Journal of Cancer, vol. 131, no. 6, pp. E884–E896, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. D. M. Beauvais and A. C. Rapraeger, “Syndecan-1-mediated cell spreading requires signaling by αvβ3 integrins in human breast carcinoma cells,” Experimental Cell Research, vol. 286, no. 2, pp. 219–232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  107. D. M. Beauvais and A. C. Rapraeger, “Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation,” Journal of Cell Science, vol. 123, no. 21, pp. 3796–3807, 2010. View at Publisher · View at Google Scholar · View at Scopus
  108. H. Hassan, B. Greve, M. S. G. Pavao, L. Kiesel, S. A. Ibrahim, and M. Götte, “Syndecan-1 modulates β-integrin-dependent and interleukin-6-dependent functions in breast cancer cell adhesion, migration, and resistance to irradiation,” FEBS Journal, vol. 280, no. 10, pp. 2216–2227, 2013. View at Publisher · View at Google Scholar · View at Scopus
  109. E. Tkachenko, J. M. Rhodes, and M. Simons, “Syndecans: new kids on the signaling block,” Circulation Research, vol. 96, no. 5, pp. 488–500, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. O. C. Kousidou, A. Berdiaki, D. Kletsas et al., “Estradiol-estrogen receptor: a key interplay of the expression of syndecan-2 and metalloproteinase-9 in breast cancer cells,” Molecular Oncology, vol. 2, no. 3, pp. 223–232, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. A. Yoneda, M. E. Lendorf, J. R. Couchman, and H. A. B. Multhaupt, “Breast and ovarian cancers: a survey and possible roles for the cell surface heparan sulfate proteoglycans,” Journal of Histochemistry and Cytochemistry, vol. 60, no. 1, pp. 9–21, 2012. View at Publisher · View at Google Scholar · View at Scopus
  112. E. J. Davies, F. H. Blackhall, J. H. Shanks et al., “Distribution and clinical significance of heparan sulfate proteoglycans in ovarian cancer,” Clinical Cancer Research, vol. 10, no. 15, pp. 5178–5186, 2004. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Woods and J. R. Couchman, “Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component,” Molecular Biology of the Cell, vol. 5, no. 2, pp. 183–192, 1994. View at Publisher · View at Google Scholar · View at Scopus
  114. A. Woods, R. L. Longley, S. Tumova, and J. R. Couchman, “Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts,” Archives of Biochemistry and Biophysics, vol. 374, no. 1, pp. 66–72, 2000. View at Publisher · View at Google Scholar · View at Scopus
  115. A. C. Rapraeger, “Syndecan-regulated receptor signaling,” Journal of Cell Biology, vol. 149, no. 5, pp. 995–997, 2000. View at Publisher · View at Google Scholar · View at Scopus
  116. A. Woods, “Syndecans: transmembrane modulators of adhesion and matrix assembly,” Journal of Clinical Investigation, vol. 107, no. 8, pp. 935–941, 2001. View at Publisher · View at Google Scholar · View at Scopus
  117. L. A. Cary, J. F. Chang, and J. Guan, “Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn,” Journal of Cell Science, vol. 109, no. 7, pp. 1787–1794, 1996. View at Google Scholar · View at Scopus
  118. R. L. Longley, A. Woods, A. Fleetwood, G. J. Cowling, J. T. Gallagher, and J. R. Couchman, “Control of morphology, cytoskeleton and migration by syndecan-4,” Journal of Cell Science, vol. 112, no. 20, pp. 3421–3431, 1999. View at Google Scholar · View at Scopus
  119. W. Huang, R. Chiquet-Ehrismann, J. V. Moyano, A. Garcia-Pardo, and G. Orend, “Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation,” Cancer Research, vol. 61, no. 23, pp. 8586–8594, 2001. View at Google Scholar · View at Scopus
  120. G. Vollmer, M. I. Tan, W. Wunsche, and K. Frank, “Expression of tenascin-C by human endometrial adenocarcinoma and stroma cells: heterogeneity of splice variants and induction by TGF-β,” Biochemistry and Cell Biology, vol. 75, no. 6, pp. 759–769, 1997. View at Publisher · View at Google Scholar · View at Scopus
  121. M. Kato, S. Saunders, H. Nguyen, and M. Bernfield, “Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells,” Molecular Biology of the Cell, vol. 6, no. 5, pp. 559–576, 1995. View at Publisher · View at Google Scholar · View at Scopus
  122. A. J. McFall and A. C. Rapraeger, “Identification of an adhesion site within the syndecan-4 extracellular protein domain,” The Journal of Biological Chemistry, vol. 272, no. 20, pp. 12901–12904, 1997. View at Publisher · View at Google Scholar · View at Scopus
  123. A. J. McFall and A. C. Rapraeger, “Characterization of the high affinity cell-binding domain in the cell surface proteoglycan syndecan-4,” Journal of Biological Chemistry, vol. 273, no. 43, pp. 28270–28276, 1998. View at Publisher · View at Google Scholar · View at Scopus
  124. V. Nikolova, C. Koo, S. A. Ibrahim et al., “Differential roles for membrane-bound and soluble syndecan-1 (CD138) in breast cancer progression,” Carcinogenesis, vol. 30, no. 3, pp. 397–407, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. I. Vlodavsky, M. Elkin, and N. Ilan, “Impact of heparanase and the tumor microenvironment on cancer metastasis and angiogenesis: basic aspects and clinical applications,” Rambam Maimonides Medical Journal, vol. 2, no. 1, Article ID e0019, 2011. View at Publisher · View at Google Scholar
  126. M. G. Peters, E. Farías, L. Colombo, J. Filmus, L. Puricelli, and E. Bal de Kier Joffé, “Inhibition of invasion and metastasis by glypican-3 in a syngeneic breast cancer model,” Breast Cancer Research and Treatment, vol. 80, no. 2, pp. 221–232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  127. I. Stigliano, L. Puricelli, J. Filmus, M. C. Sogayar, E. B. de Kier Joffé, and M. G. Peters, “Glypican-3 regulates migration, adhesion and actin cytoskeleton organization in mammary tumor cells through Wnt signaling modulation,” Breast Cancer Research and Treatment, vol. 114, no. 2, pp. 251–262, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. G. K. Yiu, A. Kaunisto, Y. R. Chin, and A. Toker, “NFAT promotes carcinoma invasive migration through glypican-6,” Biochemical Journal, vol. 440, no. 1, pp. 157–166, 2011. View at Publisher · View at Google Scholar · View at Scopus
  129. Y. J. Wu, D. P. La Pierre, J. Wu, A. J. Yee, and B. B. Yang, “The interaction of versican with its binding partners,” Cell Research, vol. 15, no. 7, pp. 483–494, 2005. View at Publisher · View at Google Scholar · View at Scopus
  130. A. D. Theocharis, “Versican in health and disease,” Connective Tissue Research, vol. 49, no. 3-4, pp. 230–234, 2008. View at Publisher · View at Google Scholar · View at Scopus
  131. S. S. Skandalis, V. T. Labropoulou, P. Ravazoula et al., “Versican but not decorin accumulation is related to malignancy in mammographically detected high density and malignant-appearing microcalcifications in non-palpable breast carcinomas,” BMC Cancer, vol. 11, article 314, 2011. View at Publisher · View at Google Scholar · View at Scopus
  132. W. W. Du, L. Fang, W. Yang et al., “The role of versican G3 domain in regulating breast cancer cell motility including effects on osteoblast cell growth and differentiation in vitro—evaluation towards understanding breast cancer cell bone metastasis,” BMC Cancer, vol. 12, article 341, 2012. View at Publisher · View at Google Scholar · View at Scopus
  133. S. S. Skandalis, N. Afratis, G. Smirlaki, D. Nikitovic, A. D. Theocharis, and G. N. Tzanakakis, “Cross-talk between estradiol receptor and EGFR/IGF-IR signaling pathways in estrogen-responsive breast cancers: focus on the role and impact of proteoglycans,” Matrix Biology, vol. 35, pp. 182–193, 2014. View at Google Scholar
  134. J. Zhu, S. Goldoni, G. Bix et al., “Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis,” Journal of Biological Chemistry, vol. 280, no. 37, pp. 32468–32479, 2005. View at Publisher · View at Google Scholar · View at Scopus
  135. R. V. Iozzo, S. Buraschi, M. Genua et al., “Decorin antagonizes IGF receptor I (IGF-IR) function by interfering with IGF-IR activity and attenuating downstream signaling,” The Journal of Biological Chemistry, vol. 286, no. 40, pp. 34712–34721, 2011. View at Publisher · View at Google Scholar · View at Scopus
  136. B. Vuillermoz, A. Khoruzhenko, M. D'Onofrio et al., “The small leucine-rich proteoglycan lumican inhibits melanoma progression,” Experimental Cell Research, vol. 296, no. 2, pp. 294–306, 2004. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Brezillon, C. Zeltz, L. Schneider et al., “Lumican inhibits B16F1 melanoma cell lung metastasis,” Journal of Physiology and Pharmacology, vol. 60, pp. 15–22, 2009. View at Google Scholar · View at Scopus
  138. C. Zeltz, S. Brézillon, J. Käpylä et al., “Lumican inhibits cell migration through α2Β1 integrin,” Experimental Cell Research, vol. 316, no. 17, pp. 2922–2931, 2010. View at Publisher · View at Google Scholar · View at Scopus
  139. A. Korpetinou, S. S. Skandalis, A. Moustakas et al., “Serglycin is implicated in the promotion of aggressive phenotype of breast cancer cells,” PLoS ONE, vol. 8, Article ID e78157, 2013. View at Google Scholar
  140. N. Montgomery, A. Hill, S. McFarlane et al., “CD44 enhances invasion of basal-like breast cancer cells by upregulating serine protease and collagen-degrading enzymatic expression and activity,” Breast Cancer Research, vol. 14, no. 3, article R84, 2012. View at Publisher · View at Google Scholar · View at Scopus
  141. L. E. Dickinson, C. C. Ho, G. M. Wang, K. J. Stebe, and S. Gerecht, “Functional surfaces for high-resolution analysis of cancer cell interactions on exogenous hyaluronic acid,” Biomaterials, vol. 31, no. 20, pp. 5472–5478, 2010. View at Publisher · View at Google Scholar · View at Scopus
  142. C. Yang, M. Cao, H. Liu et al., “The high and low molecular weight forms of hyaluronan have distinct effects on CD44 clustering,” The Journal of Biological Chemistry, vol. 287, no. 51, pp. 43094–43107, 2012. View at Publisher · View at Google Scholar · View at Scopus
  143. L. Y. W. Bourguignon, G. Wong, C. A. Earle, and W. Xia, “Interaction of low molecular weight hyaluronan with CD44 and toll-like receptors promotes the actin filament-associated protein 110-actin binding and MyD88-NFκB signaling leading to proinflammatory cytokine/chemokine production and breast tumor invasion,” Cytoskeleton, vol. 68, no. 12, pp. 671–693, 2011. View at Publisher · View at Google Scholar · View at Scopus
  144. P. G. Dedes, C. Gialeli, A. I. Tsonis et al., “Expression of matrix macromolecules and functional properties of breast cancer cells are modulated by the bisphosphonate zoledronic acid,” Biochimica et Biophysica Acta, vol. 1820, no. 12, pp. 1926–1939, 2012. View at Publisher · View at Google Scholar · View at Scopus
  145. A. C. Rapraeger, “Synstatin: A selective inhibitor of the syndecan-1-coupled IGF1R-αvβ3 integrin complex in tumorigenesis and angiogenesis,” The FEBS Journal, vol. 280, no. 10, pp. 2207–2215, 2013. View at Publisher · View at Google Scholar · View at Scopus
  146. D. Liu, Z. Shriver, G. Venkataraman, Y. El Shabrawi, and R. Sasisekharan, “Tumor cell surface heparan sulfate as cryptic promoters or inhibitors of tumor growth and metastasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 2, pp. 568–573, 2002. View at Publisher · View at Google Scholar · View at Scopus
  147. C. Y. Pumphrey, A. M. Theus, S. Li, R. S. Parrish, and R. D. Sanderson, “Neoglycans, carbodiimide-modified glycosaminoglycans: a new class of anticancer agents that inhibit cancer cell proliferation and induce apoptosis,” Cancer Research, vol. 62, no. 13, pp. 3722–3728, 2002. View at Google Scholar · View at Scopus