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The biological role and regulation of versican levels in cancer

  • Carmela RicciardelliEmail author
  • Andrew J. Sakko
  • Miranda P. Ween
  • Darryl L. Russell
  • David J. Horsfall
NON-THEMATIC REVIEW

Abstract

Increased expression of the proteoglycan, versican is strongly associated with poor outcome for many different cancers. Depending on the cancer type, versican is expressed by either the cancer cells themselves or by stromal cells surrounding the tumor. Versican plays diverse roles in cell adhesion, proliferation, migration and angiogenesis, all features of invasion and metastasis. These wide ranging functions have been attributed to the central glycosaminoglycan-binding region of versican, and to the N-(G1) and C-(G3) terminal globular domains which collectively interact with a large number of extracellular matrix and cell surface structural components. Here we review the recently identified mechanisms responsible for the regulation of versican expression and the biological roles that versican plays in cancer invasion and metastasis. The regulation of versican expression may represent one mechanism whereby cancer cells alter their surrounding microenvironment to facilitate the malignant growth and invasion of several tumor types. A greater understanding of the regulation of versican expression may contribute to the development of therapeutic methods to inhibit versican function and tumor invasion.

Keywords

Versican Cancer invasion Extracellular matrix Tumor stroma 

Notes

Acknowledgements

This work was supported by the National Health Medical Research Council Grants #519228 and #349457, University of Adelaide Faculty of Health Sciences (Hilda Farmer Research Fellowship to CR) and the Cancer Council South Australia grants and fellowships (W Bruce Hall Cancer Research Fellowship to AJS and Senior Research Fellowship to CR).

Conflicts of interest

There are no conflicts of interest to declare.

References

  1. 1.
    Bryant, R. J., & Hamdy, F. C. (2008). Screening for prostate cancer: an update. European Urology, 53(1), 37–44.PubMedCrossRefGoogle Scholar
  2. 2.
    Lapointe, J., Li, C., Higgins, J. P., van de Rijn, M., Bair, E., Montgomery, K., et al. (2004). Gene expression profiling identifies clinically relevant subtypes of prostate cancer. The Proceedings of the National Academy of Science USA, 101(3), 811–816.CrossRefGoogle Scholar
  3. 3.
    Hezel, A. F., Kimmelman, A. C., Stanger, B. Z., Bardeesy, N., & Depinho, R. A. (2006). Genetics and biology of pancreatic ductal adenocarcinoma. Genes and Development, 20(10), 1218–1249.PubMedCrossRefGoogle Scholar
  4. 4.
    Mangiola, A., de Bonis, P., Maira, G., Balducci, M., Sica, G., Lama, G., et al. (2008). Invasive tumor cells and prognosis in a selected population of patients with glioblastoma multiforme. Cancer, 113(4), 841–846.PubMedCrossRefGoogle Scholar
  5. 5.
    Kung, H. C., Hoyert, D. L., Xu, J., & Murphy, S. L. (2008). Deaths: final data for 2005. National Vital Statistics Reports, 56(10), 1–120.PubMedGoogle Scholar
  6. 6.
    Friedl, P., & Wolf, K. (2008). Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Research, 68(18), 7247–7249.PubMedCrossRefGoogle Scholar
  7. 7.
    Wolf, K., Wu, Y. I., Liu, Y., Geiger, J., Tam, E., Overall, C., et al. (2007). Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. National Cell Biology, 9(8), 893–904.CrossRefGoogle Scholar
  8. 8.
    Nabeshima, K., Inoue, T., Shimao, Y., Kataoka, H., & Koono, M. (1999). Cohort migration of carcinoma cells: differentiated colorectal carcinoma cells move as coherent cell clusters or sheets. Histology and Histopathology, 14(4), 1183–1197.PubMedGoogle Scholar
  9. 9.
    Larue, L., & Bellacosa, A. (2005). Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3’ kinase/AKT pathways. Oncogene, 24(50), 7443–7454.PubMedCrossRefGoogle Scholar
  10. 10.
    Moschos, S. J., Drogowski, L. M., Reppert, S. L., & Kirkwood, J. M. (2007). Integrins and cancer. Oncology (Williston Park), 21(9 Suppl 3), 13–20.Google Scholar
  11. 11.
    Alexandrova, A. Y. (2008). Evolution of cell interactions with extracellular matrix during carcinogenesis. Biochemistry (Moscow), 73(7), 733–741.CrossRefGoogle Scholar
  12. 12.
    Schamhart, D. H., & Kurth, K. H. (1997). Role of proteoglycans in cell adhesion of prostate cancer cells: from review to experiment. Urological Research, 25(Suppl 2), S89–96.PubMedCrossRefGoogle Scholar
  13. 13.
    Cattaruzza, S., & Perris, R. (2005). Proteoglycan control of cell movement during wound healing and cancer spreading. Matrix Biology, 24(6), 400–417.PubMedCrossRefGoogle Scholar
  14. 14.
    Cattaruzza, S., Nicolosi, P. A., & Perris, R. (2008). Proteoglycans in the control of tumor growth and metastasis formation. Connective Tissue Research, 49(3), 225–229.PubMedCrossRefGoogle Scholar
  15. 15.
    Naso, M. F., Zimmermann, D. R., & Iozzo, R. V. (1994). Characterization of the complete genomic structure of the human versican gene and functional analysis of its promoter. Journal of Biological Chemistry, 269(52), 32999–33008.PubMedGoogle Scholar
  16. 16.
    Zimmermann, D. R., & Ruoslahti, E. (1989). Multiple domains of the large fibroblast proteoglycan, versican. The EMBO Journal, 8(10), 2975–2981.PubMedGoogle Scholar
  17. 17.
    LeBaron, R. G. (1996). Versican. Perspectives on Developmental Neurobiology, 3(4), 261–271.PubMedGoogle Scholar
  18. 18.
    LeBaron, R. G., Zimmermann, D. R., & Ruoslahti, E. (1992). Hyaluronate binding properties of versican. Journal of Biological Chemistry, 267(14), 10003–10010.PubMedGoogle Scholar
  19. 19.
    Matsumoto, K., Shionyu, M., Go, M., Shimizu, K., Shinomura, T., Kimata, K., et al. (2003). Distinct interaction of versican/PG-M with hyaluronan and link protein. Journal of Biological Chemistry, 278(42), 41205–41212.PubMedCrossRefGoogle Scholar
  20. 20.
    Wight, T. N. (2002). Versican: a versatile extracellular matrix proteoglycan in cell biology. Current Opinions in Cell Biology, 14(5), 617–623.CrossRefGoogle Scholar
  21. 21.
    Wu, Y. J., La Pierre, D. P., Wu, J., Yee, A. J., & Yang, B. B. (2005). The interaction of versican with its binding partners. Cell Research, 15(7), 483–494.PubMedCrossRefGoogle Scholar
  22. 22.
    Yamagata, M., Yamada, K. M., Yoneda, M., Suzuki, S., & Kimata, K. (1986). Chondroitin sulfate proteoglycan (PG-M-like proteoglycan) is involved in the binding of hyaluronic acid to cellular fibronectin. Journal of Biological Chemistry, 261(29), 13526–13535.PubMedGoogle Scholar
  23. 23.
    Aspberg, A., Adam, S., Kostka, G., Timpl, R., & Heinegard, D. (1999). Fibulin-1 is a ligand for the C-type lectin domains of aggrecan and versican. Journal of Biological Chemistry, 274(29), 20444–20449.PubMedCrossRefGoogle Scholar
  24. 24.
    Aspberg, A., Miura, R., Bourdoulous, S., Shimonaka, M., Heinegard, D., Schachner, M., et al. (1997). The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. The Proceedings of the National Academy of Science USA, 94(19), 10116–10121.CrossRefGoogle Scholar
  25. 25.
    Olin, A. I., Morgelin, M., Sasaki, T., Timpl, R., Heinegard, D., & Aspberg, A. (2001). The proteoglycans aggrecan and Versican form networks with fibulin-2 through their lectin domain binding. Journal of Biological Chemistry, 276(2), 1253–1261.PubMedCrossRefGoogle Scholar
  26. 26.
    Kawashima, H., Li, Y. F., Watanabe, N., Hirose, J., Hirose, M., & Miyasaka, M. (1999). Identification and characterization of ligands for L-selectin in the kidney. I. Versican, a large chondroitin sulfate proteoglycan, is a ligand for L-selectin. International Immunology, 11(3), 393–405.PubMedCrossRefGoogle Scholar
  27. 27.
    Kawashima, H., Hirose, M., Hirose, J., Nagakubo, D., Plaas, A. H., & Miyasaka, M. (2000). Binding of a large chondroitin sulfate/dermatan sulfate proteoglycan, versican, to L-selectin, P-selectin, and CD44. Journal of Biological Chemistry, 275(45), 35448–35456.PubMedCrossRefGoogle Scholar
  28. 28.
    Kawashima, H., Atarashi, K., Hirose, M., Hirose, J., Yamada, S., Sugahara, K., et al. (2002). Oversulfated chondroitin/dermatan sulfates containing GlcAbeta 1/IdoAalpha 1–3GalNAc(4,6-O-disulfate) interact with L- and P-selectin and chemokines. Journal of Biological Chemistry.Google Scholar
  29. 29.
    Hirose, J., Kawashima, H., Yoshie, O., Tashiro, K., & Miyasaka, M. (2001). Versican interacts with chemokines and modulates cellular responses. Journal of Biological Chemistry, 276(7), 5228–5234.PubMedCrossRefGoogle Scholar
  30. 30.
    Wu, Y., Chen, L., Zheng, P. S., Yang, B. B. (2002). Beta1-integrin mediated Glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican. Journal of Biological Chemistry.Google Scholar
  31. 31.
    Cattaruzza, S., Schiappacassi, M., Ljungberg-Rose, A., Spessotto, P., Perissinotto, D., Morgelin, M., et al. (2002). Distribution of PG-M/versican variants in human tissues and de novo expression of isoform V3 upon endothelial cell activation, migration, and neoangiogenesis in vitro. Journal of Biological Chemistry, 277(49), 47626–47635.PubMedCrossRefGoogle Scholar
  32. 32.
    Perissinotto, D., Iacopetti, P., Bellina, I., Doliana, R., Colombatti, A., Pettway, Z., et al. (2000). Avian neural crest cell migration is diversely regulated by the two major hyaluronan-binding proteoglycans PG-M/versican and aggrecan. Development, 127(13), 2823–2842.PubMedGoogle Scholar
  33. 33.
    Sheng, W., Wang, G., Wang, Y., Liang, J., Wen, J., Zheng, P. S., et al. (2005). The roles of versican V1 and V2 isoforms in cell proliferation and apoptosis. Molecular Biology of the Cell, 16(3), 1330–1340.PubMedCrossRefGoogle Scholar
  34. 34.
    Wu, Y., Sheng, W., Chen, L., Dong, H., Lee, V., Lu, F., et al. (2004). Versican V1 isoform induces neuronal differentiation and promotes neurite outgrowth. Molecular Biology of the Cell, 15(5), 2093–2104.PubMedCrossRefGoogle Scholar
  35. 35.
    Schmalfeldt, M., Bandtlow, C. E., Dours-Zimmermann, M. T., Winterhalter, K. H., & Zimmermann, D. R. (2000). Brain derived versican V2 is a potent inhibitor of axonal growth. Journal of Cell Science, 113( Pt 5), 807–816.PubMedGoogle Scholar
  36. 36.
    Sakko, A. J., Ricciardelli, C., Mayne, K., Tilley, W. D., LeBaron, R. G., & Horsfall, D. J. (2001). Versican accumulation in human prostatic fibroblast cultures is enhanced by prostate cancer cell-derived transforming growth factor beta1. Cancer Research, 61(3), 926–930.PubMedGoogle Scholar
  37. 37.
    Ricciardelli, C., Brooks, J. H., Suwiwat, S., Sakko, A. J., Mayne, K., Raymond, W. A., et al. (2002). 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, 8(4), 1054–1060.PubMedGoogle Scholar
  38. 38.
    Nikitovic, D., Zafiropoulos, A., Katonis, P., Tsatsakis, A., Theocharis, A. D., Karamanos, N. K., et al. (2006). Transforming growth factor-beta as a key molecule triggering the expression of versican isoforms v0 and v1, hyaluronan synthase-2 and synthesis of hyaluronan in malignant osteosarcoma cells. International Union of Biochemistry and Molecular Biology Life, 58(1), 47–53.PubMedCrossRefGoogle Scholar
  39. 39.
    Arslan, F., Bosserhoff, A. K., Nickl-Jockschat, T., Doerfelt, A., Bogdahn, U., & Hau, P. (2007). The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-beta2. British Journal of Cancer, 96(10), 1560–1568.PubMedCrossRefGoogle Scholar
  40. 40.
    Lemire, J. M., Merrilees, M. J., Braun, K. R., & Wight, T. N. (2002). Overexpression of the V3 variant of versican alters arterial smooth muscle cell adhesion, migration, and proliferation in vitro. Journal of Cell Physiology, 190(1), 38–45.CrossRefGoogle Scholar
  41. 41.
    Serra, M., Miquel, L., Domenzain, C., Docampo, M. J., Fabra, A., Wight, T. N., et al. (2005). V3 versican isoform expression alters the phenotype of melanoma cells and their tumorigenic potential. International Journal of Cancer, 114(6), 879–886.CrossRefGoogle Scholar
  42. 42.
    Miquel-Serra, L., Serra, M., Hernandez, D., Domenzain, C., Docampo, M. J., Rabanal, R. M., et al. (2006). V3 versican isoform expression has a dual role in human melanoma tumor growth and metastasis. Laboratory Investigation, 86(9), 889–901.PubMedCrossRefGoogle Scholar
  43. 43.
    Paulus, W., Baur, I., Dours-Zimmermann, M. T., & Zimmermann, D. R. (1996). Differential expression of versican isoforms in brain tumors. Journal of Neuropathology and Experimental Neurology, 55(5), 528–533.PubMedCrossRefGoogle Scholar
  44. 44.
    Nara, Y., Kato, Y., Torii, Y., Tsuji, Y., Nakagaki, S., Goto, S., et al. (1997). Immunohistochemical localization of extracellular matrix components in human breast tumours with special reference to PG-M/versican. Histochemical Journal, 29(1), 21–30.PubMedCrossRefGoogle Scholar
  45. 45.
    Rottiers, P., Verfaillie, T., Contreras, R., Revets, H., Desmedt, M., Dooms, H., et al. (1998). Differentiation of EL4 lymphoma cells by tumoral environment is associated with inappropriate expression of the large chondroitin sulfate proteoglycan PG-M and the tumor-associated antigen HTgp-175. International Journal of Cancer, 78(4), 503–510.CrossRefGoogle Scholar
  46. 46.
    Ricciardelli, C., Mayne, K., Sykes, P. J., Raymond, W. A., McCaul, K., Marshall, V. R., et al. (1998). Elevated levels of versican but not decorin predict disease progression in early-stage prostate cancer. Clinical Cancer Research, 4(4), 963–971.PubMedGoogle Scholar
  47. 47.
    Touab, M., Villena, J., Barranco, C., Arumi-Uria, M., & Bassols, A. (2002). Versican is differentially expressed in human melanoma and may play a role in tumor development. American Journal of Pathology, 160(2), 549–557.PubMedGoogle Scholar
  48. 48.
    Voutilainen, K., Anttila, M., Sillanpaa, S., Tammi, R., Tammi, M., Saarikoski, S., et al. (2003). Versican in epithelial ovarian cancer: relation to hyaluronan, clinicopathologic factors and prognosis. International Journal of Cancer, 107(3), 359–364.CrossRefGoogle Scholar
  49. 49.
    Casey, R. C., Oegema Jr., T. R., Skubitz, K. M., Pambuccian, S. E., Grindle, S. M., & Skubitz, A. P. (2003). Cell membrane glycosylation mediates the adhesion, migration, and invasion of ovarian carcinoma cells. Clinical and Experimental Metastasis, 20(2), 143–152.PubMedCrossRefGoogle Scholar
  50. 50.
    Mukaratirwa, S., Koninkx, J. F., Gruys, E., & Nederbragt, H. (2005). Mutual paracrine effects of colorectal tumour cells and stromal cells: modulation of tumour and stromal cell differentiation and extracellular matrix component production in culture. International Journal of Experimental Pathology, 86(4), 219–229.PubMedCrossRefGoogle Scholar
  51. 51.
    Suwiwat, S., Ricciardelli, C., Tammi, R., Tammi, M., Auvinen, P., Kosma, V. M., et al. (2004). 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, 10(7), 2491–2498.PubMedCrossRefGoogle Scholar
  52. 52.
    Pirinen, R., Leinonen, T., Bohm, J., Johansson, R., Ropponen, K., Kumpulainen, E., et al. (2005). Versican in nonsmall cell lung cancer: relation to hyaluronan, clinicopathologic factors, and prognosis. Human Pathology, 36(1), 44–50.PubMedCrossRefGoogle Scholar
  53. 53.
    Pukkila, M., Kosunen, A., Ropponen, K., Virtaniemi, J., Kellokoski, J., Kumpulainen, E., et al. (2007). High stromal versican expression predicts unfavourable outcome in oral squamous cell carcinoma. Journal of Clinical Pathology, 60(3), 267–272.PubMedCrossRefGoogle Scholar
  54. 54.
    Skandalis, S. S., Kletsas, D., Kyriakopoulou, D., Stavropoulos, M., & Theocharis, D. A. (2006). The greatly increased amounts of accumulated versican and decorin with specific post-translational modifications may be closely associated with the malignant phenotype of pancreatic cancer. Biochimica and Biophysica Acta, 1760(8), 1217–1225.Google Scholar
  55. 55.
    Lancaster, J. M., Dressman, H. K., Clarke, J. P., Sayer, R. A., Martino, M. A., Cragun, J. M., et al. (2006). Identification of genes associated with ovarian cancer metastasis using microarray expression analysis. International Journal of Gynecological Cancer, 16(5), 1733–1745.PubMedCrossRefGoogle Scholar
  56. 56.
    Castronovo, V., Kischel, P., Guillonneau, F., de Leval, L., Defechereux, T., De Pauw, E., et al. (2007). Identification of specific reachable molecular targets in human breast cancer using a versatile ex vivo proteomic method. Proteomics, 7(8), 1188–1196.PubMedCrossRefGoogle Scholar
  57. 57.
    Makatsori, E., Lamari, F. N., Theocharis, A. D., Anagnostides, S., Hjerpe, A., Tsegenidis, T., et al. (2003). Large matrix proteoglycans, versican and perlecan, are expressed and secreted by human leukemic monocytes. Anticancer Research, 23(4), 3303–3309.PubMedGoogle Scholar
  58. 58.
    Hanekamp, E. E., Gielen, S. C., Smid-Koopman, E., Kuhne, L. C., de Ruiter, P. E., Chadha-Ajwani, S., et al. (2003). Consequences of loss of progesterone receptor expression in development of invasive endometrial cancer. Clinical Cancer Research, 9(11), 4190–4199.PubMedGoogle Scholar
  59. 59.
    Pukkila, M. J., Kosunen, A. S., Virtaniemi, J. A., Kumpulainen, E. J., Johansson, R. T., Kellokoski, J. K., et al. (2004). Versican expression in pharyngeal squamous cell carcinoma: an immunohistochemical study. Journal of Clinical Pathology, 57(7), 735–739.PubMedCrossRefGoogle Scholar
  60. 60.
    Kodama, J., Hasengaowa, , Kusumoto, T., Seki, N., Matsuo, T., Nakamura, K., et al. (2007). Versican expression in human cervical cancer. European Journal of Cancer, 43(9), 1460–1466.PubMedCrossRefGoogle Scholar
  61. 61.
    Kodama, J., Hasengaowa, , Kusumoto, T., Seki, N., Matsuo, T., Ojima, Y., et al. (2007). Prognostic significance of stromal versican expression in human endometrial cancer. Annals of Oncology, 18(2), 269–274.PubMedCrossRefGoogle Scholar
  62. 62.
    Brown, L. F., Guidi, A. J., Schnitt, S. J., Van De Water, L., Iruela-Arispe, M. L., Yeo, T. K., et al. (1999). Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clinical Cancer Research, 5(5), 1041–1056.PubMedGoogle Scholar
  63. 63.
    Mauri, P., Scarpa, A., Nascimbeni, A. C., Benazzi, L., Parmagnani, E., Mafficini, A., et al. (2005). Identification of proteins released by pancreatic cancer cells by multidimensional protein identification technology: a strategy for identification of novel cancer markers. Journal of The Federation of American Societies for Experimental Biology, 19(9), 1125–1127.Google Scholar
  64. 64.
    Ang, L. C., Zhang, Y., Cao, L., Yang, B. L., Young, B., Kiani, C., et al. (1999). Versican enhances locomotion of astrocytoma cells and reduces cell adhesion through its G1 domain. Journal of Neuropathology and Experimental Neurology, 58(6), 597–605.PubMedCrossRefGoogle Scholar
  65. 65.
    Cattaruzza, S., Schiappacassi, M., Kimata, K., Colombatti, A., Perris, R. (2004). The globular domains of PGM/versican modulate the proliferation-apoptosis equilibrium and invasive capabilities of tumor cells. Journal of The Federation of American Societies for Experimental Biology.Google Scholar
  66. 66.
    Zheng, P. S., Wen, J., Ang, L. C., Sheng, W., Viloria-Petit, A., Wang, Y., et al. (2004). Versican/PG-M G3 domain promotes tumor growth and angiogenesis. Journal of The Federation of American Societies for Experimental Biology.Google Scholar
  67. 67.
    Paris, S., Sesboue, R., Chauzy, C., Maingonnat, C., & Delpech, B. (2006). Hyaluronectin modulation of lung metastasis in nude mice. European Journal of Cancer, 42(18), 3253–3259.PubMedCrossRefGoogle Scholar
  68. 68.
    Ricciardelli, C., Russell, D. L., Ween, M. P., Mayne, K., Suwiwat, S., Byers, S., et al. (2007). Formation of hyaluronan– and versican–rich pericellular matrix by prostate cancer cells promotes cell motility. Journal of Biological Chemistry, 282(14), 10814–10825.PubMedCrossRefGoogle Scholar
  69. 69.
    Creighton, C. J., Bromberg-White, J. L., Misek, D. E., Monsma, D. J., Brichory, F., Kuick, R., et al. (2005). Analysis of tumor-host interactions by gene expression profiling of lung adenocarcinoma xenografts identifies genes involved in tumor formation. Molecular Cancer Research, 3(3), 119–129.PubMedCrossRefGoogle Scholar
  70. 70.
    LaPierre, D. P., Lee, D. Y., Li, S. Z., Xie, Y. Z., Zhong, L., Sheng, W., et al. (2007). The ability of versican to simultaneously cause apoptotic resistance and sensitivity. Cancer Research, 67(10), 4742–4750.PubMedCrossRefGoogle Scholar
  71. 71.
    Yee, A. J., Akens, M., Yang, B. L., Finkelstein, J., Zheng, P. S., Deng, Z., et al. (2007). The effect of versican G3 domain on local breast cancer invasiveness and bony metastasis. Breast Cancer Research, 9(4), R47.PubMedCrossRefGoogle Scholar
  72. 72.
    Sakko, A. J., Ricciardelli, C., Mayne, K., Suwiwat, S., LeBaron, R. G., Marshall, V. R., et al. (2003). Modulation of Prostate Cancer Cell Attachment to Matrix by Versican. Cancer Research, 63(16), 4786–4791.PubMedGoogle Scholar
  73. 73.
    Yamagata, M., Saga, S., Kato, M., Bernfield, M., & Kimata, K. (1993). Selective distributions of proteoglycans and their ligands in pericellular matrix of cultured fibroblasts. Implications for their roles in cell-substratum adhesion. Journal of Cell Science, 106( Pt 1), 55–65.PubMedGoogle Scholar
  74. 74.
    Yamagata, M., & Kimata, K. (1994). Repression of a malignant cell-substratum adhesion phenotype by inhibiting the production of the anti-adhesive proteoglycan, PG-M/versican. Journal of Cell Science, 107( Pt 9), 2581–2590.PubMedGoogle Scholar
  75. 75.
    Simpson, M. A., Reiland, J., Burger, S. R., Furcht, L. T., Spicer, A. P., Oegema Jr., T. R., et al. (2001). Hyaluronan synthase elevation in metastatic prostate carcinoma cells correlates with hyaluronan surface retention, a prerequisite for rapid adhesion to bone marrow endothelial cells. Journal of Biological Chemistry, 276(21), 17949–17957.PubMedCrossRefGoogle Scholar
  76. 76.
    Draffin, J. E., McFarlane, S., Hill, A., Johnston, P. G., & Waugh, D. J. (2004). CD44 potentiates the adherence of metastatic prostate and breast cancer cells to bone marrow endothelial cells. Cancer Research, 64(16), 5702–5711.PubMedCrossRefGoogle Scholar
  77. 77.
    Zhang, Y., Cao, L., Yang, B. L., & Yang, B. B. (1998). The G3 domain of versican enhances cell proliferation via epidermial growth factor-like motifs. Journal of Biological Chemistry, 273(33), 21342–21351.PubMedCrossRefGoogle Scholar
  78. 78.
    Yang, B. L., Zhang, Y., Cao, L., & Yang, B. B. (1999). Cell adhesion and proliferation mediated through the G1 domain of versican. Journal of Cell Biochemistry, 72(2), 210–220.CrossRefGoogle Scholar
  79. 79.
    Sandy, J. D., Westling, J., Kenagy, R. D., Iruela-Arispe, M. L., Verscharen, C., Rodriguez-Mazaneque, J. C., et al. (2001). Versican V1 proteolysis in human aorta in vivo occurs at the Glu441-Ala442 bond, a site that is cleaved by recombinant ADAMTS-1 and ADAMTS-4. Journal of Biological Chemistry, 276(16), 13372–13378.PubMedCrossRefGoogle Scholar
  80. 80.
    Russell, D. L., Doyle, K. M., Ochsner, S. A., Sandy, J. D., & Richards, J. S. (2003). Processing and localization of ADAMTS-1 and proteolytic cleavage of versican during cumulus matrix expansion and ovulation. Journal of Biological Chemistry, 278(43), 42330–42339.PubMedCrossRefGoogle Scholar
  81. 81.
    Kern, C. B., Twal, W. O., Mjaatvedt, C. H., Fairey, S. E., Toole, B. P., Iruela-Arispe, M. L., et al. (2006). Proteolytic cleavage of versican during cardiac cushion morphogenesis. Developmental Dynamics, 235(8), 2238–2247.PubMedCrossRefGoogle Scholar
  82. 82.
    Westling, J., Gottschall, P. E., Thompson, V. P., Cockburn, A., Perides, G., Zimmermann, D. R., et al. (2004). ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate binding protein. Biochemical Journal, 377(Pt 3), 787–795.PubMedGoogle Scholar
  83. 83.
    Perides, G., Asher, R. A., Lark, M. W., Lane, W. S., Robinson, R. A., & Bignami, A. (1995). Glial hyaluronate-binding protein: a product of metalloproteinase digestion of versican? Biochemical Journal, 312( Pt 2), 377–384.PubMedGoogle Scholar
  84. 84.
    Passi, A., Negrini, D., Albertini, R., Miserocchi, G., & De Luca, G. (1999). The sensitivity of versican from rabbit lung to gelatinase A (MMP-2) and B (MMP-9) and its involvement in the development of hydraulic lung edema. Federation of European Biochemical Societies Letters, 456(1), 93–96.PubMedGoogle Scholar
  85. 85.
    Halpert, I., Sires, U. I., Roby, J. D., Potter-Perigo, S., Wight, T. N., Shapiro, S. D., et al. (1996). Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. The Proceedingsof the National Academy of Science USA, 93(18), 9748–9753.CrossRefGoogle Scholar
  86. 86.
    Kenagy, R. D., Fischer, J. W., Davies, M. G., Berceli, S. A., Hawkins, S. M., Wight, T. N., et al. (2002). Increased plasmin and serine proteinase activity during flow-induced intimal atrophy in baboon PTFE grafts. Arteriosclerosis, Thrombosis, and Vascular Biology, 22(3), 400–404.PubMedCrossRefGoogle Scholar
  87. 87.
    Jonsson-Rylander, A. C., Nilsson, T., Fritsche-Danielson, R., Hammarstrom, A., Behrendt, M., Andersson, J. O., et al. (2005). Role of ADAMTS-1 in atherosclerosis: remodeling of carotid artery, immunohistochemistry, and proteolysis of versican. Arteriosclerosis, Thrombosis, and Vascular Biology, 25(1), 180–185.PubMedGoogle Scholar
  88. 88.
    Kenagy, R. D., Plaas, A. H., & Wight, T. N. (2006). Versican degradation and vascular disease. Trends in Cardiovascular Medicine, 16(6), 209–215.PubMedCrossRefGoogle Scholar
  89. 89.
    Rahmani, M., Wong, B. W., Ang, L., Cheung, C. C., Carthy, J. M., Walinski, H., et al. (2006). Versican: signaling to transcriptional control pathways. Canadian Journal of Physiological Pharmacology, 84(1), 77–92.CrossRefGoogle Scholar
  90. 90.
    Yoon, H., Liyanarachchi, S., Wright, F. A., Davuluri, R., Lockman, J. C., de la Chapelle, A., et al. (2002). Gene expression profiling of isogenic cells with different TP53 gene dosage reveals numerous genes that are affected by TP53 dosage and identifies CSPG2 as a direct target of p53. The Proceedings of the National Academy of Science USA, 99(24), 15632–15637.CrossRefGoogle Scholar
  91. 91.
    Willert, J., Epping, M., Pollack, J. R., Brown, P. O., & Nusse, R. (2002). A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Developmental Biology, 2, 8.PubMedCrossRefGoogle Scholar
  92. 92.
    Rahmani, M., Read, J. T., Carthy, J. M., McDonald, P. C., Wong, B. W., Esfandiarei, M., et al. (2005). Regulation of the versican promoter by the beta-catenin-T-cell factor complex in vascular smooth muscle cells. Journal of Biological Chemistry, 280(13), 13019–13028.PubMedCrossRefGoogle Scholar
  93. 93.
    Haase, H. R., Clarkson, R. W., Waters, M. J., & Bartold, P. M. (1998). Growth factor modulation of mitogenic responses and proteoglycan synthesis by human periodontal fibroblasts. Journal of Cell Physiology, 174(3), 353–361.CrossRefGoogle Scholar
  94. 94.
    Kahari, V. M., Larjava, H., & Uitto, J. (1991). Differential regulation of extracellular matrix proteoglycan (PG) gene expression. Transforming growth factor-beta 1 up-regulates biglycan (PGI), and versican (large fibroblast PG) but down-regulates decorin (PGII) mRNA levels in human fibroblasts in culture. Journal of Biological Chemistry, 266(16), 10608–10615.PubMedGoogle Scholar
  95. 95.
    Asher, R. A., Morgenstern, D. A., Shearer, M. C., Adcock, K. H., Pesheva, P., & Fawcett, J. W. (2002). Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. Journal of Neuroscience, 22(6), 2225–2236.PubMedGoogle Scholar
  96. 96.
    Cross, N. A., Chandrasekharan, S., Jokonya, N., Fowles, A., Hamdy, F. C., Buttle, D. J., et al. (2005). The expression and regulation of ADAMTS−1, −4, −5, −9, and −15, and TIMP−3 by TGFbeta1 in prostate cells: relevance to the accumulation of versican. Prostate, 63(3), 269–275.PubMedCrossRefGoogle Scholar
  97. 97.
    Koninger, J., Giese, T., di Mola, F. F., Wente, M. N., Esposito, I., Bachem, M. G., et al. (2004). Pancreatic tumor cells influence the composition of the extracellular matrix. Biochemical and Biophysical Research Communications, 322(3), 943–949.PubMedCrossRefGoogle Scholar
  98. 98.
    Berdiaki, A., Zafiropoulos, A., Fthenou, E., Katonis, P., Tsatsakis, A., Karamanos, N. K., et al. (2008). Regulation of hyaluronan and versican deposition by growth factors in fibrosarcoma cell lines. Biochimica and Biophysica Acta, 1780(2), 194–202.Google Scholar
  99. 99.
    Schonherr, E., Jarvelainen, H. T., Sandell, L. J., & Wight, T. N. (1991). Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. Journal of Biological Chemistry, 266(26), 17640–17647.PubMedGoogle Scholar
  100. 100.
    Schonherr, E., Kinsella, M. G., & Wight, T. N. (1997). Genistein selectively inhibits platelet-derived growth factor-stimulated versican biosynthesis in monkey arterial smooth muscle cells. Archives of Biochemistry and Biophysics, 339(2), 353–361.PubMedCrossRefGoogle Scholar
  101. 101.
    Evanko, S. P., Johnson, P. Y., Braun, K. R., Underhill, C. B., Dudhia, J., & Wight, T. N. (2001). Platelet-derived growth factor stimulates the formation of versican-hyaluronan aggregates and pericellular matrix expansion in arterial smooth muscle cells. Archives of Biochemistry and Biophysics, 394(1), 29–38.PubMedCrossRefGoogle Scholar
  102. 102.
    Syrokou, A., Tzanakakis, G. N., Hjerpe, A., & Karamanos, N. K. (1999). Proteoglycans in human malignant mesothelioma. Stimulation of their synthesis induced by epidermal, insulin and platelet-derived growth factors involves receptors with tyrosine kinase activity. Biochimie, 81(7), 733–744.PubMedCrossRefGoogle Scholar
  103. 103.
    Potter-Perigo, S., Baker, C., Tsoi, C., Braun, K. R., Isenhath, S., Altman, G. M., et al. (2004). Regulation of proteoglycan synthesis by leukotriene d4 and epidermal growth factor in bronchial smooth muscle cells. American Journal of Respiratory Cell Molecular Biology, 30(1), 101–108.CrossRefGoogle Scholar
  104. 104.
    Qwarnstrom, E. E., Jarvelainen, H. T., Kinsella, M. G., Ostberg, C. O., Sandell, L. J., Page, R. C., et al. (1993). Interleukin-1 beta regulation of fibroblast proteoglycan synthesis involves a decrease in versican steady-state mRNA levels. Biochemical Journal, 294( Pt 2), 613–620.PubMedGoogle Scholar
  105. 105.
    Lemire, J. M., Chan, C. K., Bressler, S., Miller, J., LeBaron, R. G., & Wight, T. N. (2007). Interleukin-1beta selectively decreases the synthesis of versican by arterial smooth muscle cells. Journal of Cell Biochemistry, 101(3), 753–766.CrossRefGoogle Scholar
  106. 106.
    Tufvesson, E., & Westergren-Thorsson, G. (2000). Alteration of proteoglycan synthesis in human lung fibroblasts induced by interleukin-1beta and tumor necrosis factor-alpha. Journal of Cell Biochemistry, 77(2), 298–309.CrossRefGoogle Scholar
  107. 107.
    Russell, D. L., Ochsner, S. A., Hsieh, M., Mulders, S., & Richards, J. S. (2003). Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology, 144(3), 1020–1031.PubMedCrossRefGoogle Scholar
  108. 108.
    Read, J. T., Rahmani, M., Boroomand, S., Allahverdian, S., McManus, B. M., & Rennie, P. S. (2007). Androgen receptor regulation of the versican gene through an androgen response element in the proximal promoter. Journal of Biological Chemistry, 282(44), 31954–31963.PubMedCrossRefGoogle Scholar
  109. 109.
    Sakko, A. J., Ricciardelli, C., Mayne, K., Dours-Zimmermann, M. T., Zimmermann, D. R., Neufing, P., et al. (2007). Changes in steroid receptors and proteoglycan expression in the guinea pig prostate stroma during puberty and hormone manipulation. Prostate, 67(3), 288–300.PubMedCrossRefGoogle Scholar
  110. 110.
    Adany, R., Heimer, R., Caterson, B., Sorrell, J. M., & Iozzo, R. V. (1990). Altered expression of chondroitin sulfate proteoglycan in the stroma of human colon carcinoma. Hypomethylation of PG-40 gene correlates with increased PG-40 content and mRNA levels. Journal of Biological Chemistry, 265(19), 11389–11396.PubMedGoogle Scholar
  111. 111.
    Toyota, M., Ho, C., Ahuja, N., Jair, K. W., Li, Q., Ohe-Toyota, M., et al. (1999). Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Research, 59(10), 2307–2312.PubMedGoogle Scholar
  112. 112.
    Shimizu-Hirota, R., Sasamura, H., Mifune, M., Nakaya, H., Kuroda, M., Hayashi, M., et al. (2001). Regulation of vascular proteoglycan synthesis by angiotensin II type 1 and type 2 receptors. Journal of the American Society of Nephrology, 12(12), 2609–2615.PubMedGoogle Scholar
  113. 113.
    Burgess, J. K., Oliver, B. G., Poniris, M. H., Ge, Q., Boustany, S., Cox, N., et al. (2006). A phosphodiesterase 4 inhibitor inhibits matrix protein deposition in airways in vitro. Journal of Allergy Clinical Immunology, 118(3), 649–657.CrossRefGoogle Scholar
  114. 114.
    Todorova, L., Gurcan, E., Miller-Larsson, A., & Westergren-Thorsson, G. (2006). Lung fibroblast proteoglycan production induced by serum is inhibited by budesonide and formoterol. American Journal of Respiratory Cell Molecular Biology, 34(1), 92–100.CrossRefGoogle Scholar
  115. 115.
    Jaworski, D. M., Kelly, G. M., Piepmeier, J. M., & Hockfield, S. (1996). BEHAB (brain enriched hyaluronan binding) is expressed in surgical samples of glioma and in intracranial grafts of invasive glioma cell lines. Cancer Research, 56(10), 2293–2298.PubMedGoogle Scholar
  116. 116.
    Matthews, R. T., Gary, S. C., Zerillo, C., Pratta, M., Solomon, K., Arner, E. C., et al. (2000). Brain-enriched hyaluronan binding (BEHAB)/brevican cleavage in a glioma cell line is mediated by a disintegrin and metalloproteinase with thrombospondin motifs (ADAMTS) family member. Journal of Biological Chemistry, 275(30), 22695–22703.PubMedCrossRefGoogle Scholar
  117. 117.
    Nutt, C. L., Matthews, R. T., & Hockfield, S. (2001). Glial tumor invasion: a role for the upregulation and cleavage of BEHAB/brevican. Neuroscientist, 7(2), 113–122.PubMedCrossRefGoogle Scholar
  118. 118.
    Viapiano, M. S., Hockfield, S., & Matthews, R. T. (2008). BEHAB/brevican requires ADAMTS-mediated proteolytic cleavage to promote glioma invasion. Journal of Neurooncology, 88(3), 261–272.CrossRefGoogle Scholar
  119. 119.
    Casey, R. C., Koch, K. A., Oegema Jr., T. R., Skubitz, K. M., Pambuccian, S. E., Grindle, S. M., et al. (2003). Establishment of an in vitro assay to measure the invasion of ovarian carcinoma cells through mesothelial cell monolayers. Clinical and Experimental Metastasis, 20(4), 343–356.PubMedCrossRefGoogle Scholar
  120. 120.
    Nakamura, J. L., Haas-Kogan, D. A., & Pieper, R. O. (2007). Glioma invasiveness responds variably to irradiation in a co-culture model. International Journal of Radiation Oncology Biology Physics, 69(3), 880–886.Google Scholar
  121. 121.
    Almholt, K., Juncker-Jensen, A., Laerum, O. D., Dano, K., Johnsen, M., Lund, L. R., et al. (2008). Metastasis is strongly reduced by the matrix metalloproteinase inhibitor Galardin in the MMTV-PymT transgenic breast cancer model. Molecular Cancer Therapies, 7(9), 2758–2767.CrossRefGoogle Scholar
  122. 122.
    Vankemmelbeke, M. N., Jones, G. C., Fowles, C., Ilic, M. Z., Handley, C. J., Day, A. J., et al. (2003). Selective inhibition of ADAMTS−1, −4 and −5 by catechin gallate esters. European Journal of Biochemistry, 270(11), 2394–2403.PubMedCrossRefGoogle Scholar
  123. 123.
    Knudson, W., & Knudson, C. B. (1991). Assembly of a chondrocyte-like pericellular matrix on non-chondrogenic cells. Role of the cell surface hyaluronan receptors in the assembly of a pericellular matrix. Journal of Cell Science, 99( Pt 2), 227–235.PubMedGoogle Scholar
  124. 124.
    Evanko, S. P., Angello, J. C., & Wight, T. N. (1999). Formation of hyaluronan– and versican–rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 19(4), 1004–1013.PubMedGoogle Scholar
  125. 125.
    Zeng, C., Toole, B. P., Kinney, S. D., Kuo, J. W., & Stamenkovic, I. (1998). Inhibition of tumor growth in vivo by hyaluronan oligomers. International Journal of Cancer, 77(3), 396–401.CrossRefGoogle Scholar
  126. 126.
    du Cros, D. L., Lebaron, R. G., & Couchman, J. R. (1995). Association of versican with dermal matrices and its potential role in hair follicle development and cycling. Journal of Investagative Dermatology, 105(3), 426–431.CrossRefGoogle Scholar
  127. 127.
    Ricciardelli, C., Choong, C. S., Buchanan, G., Vivekanandan, S., Neufing, P., Stahl, J., et al. (2005). Androgen receptor levels in prostate cancer epithelial and peritumoral stromal cells identify non-organ confined disease. Prostate, 63(1), 19–28.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Carmela Ricciardelli
    • 1
    • 2
    Email author
  • Andrew J. Sakko
    • 1
    • 2
    • 3
  • Miranda P. Ween
    • 1
  • Darryl L. Russell
    • 1
  • David J. Horsfall
    • 2
  1. 1.Research Centre for Reproductive Health, Discipline of Obstetrics and GynaecologyUniversity of AdelaideAdelaideAustralia
  2. 2.Dame Roma Mitchell Cancer Research LaboratoriesUniversity of Adelaide, Hanson InstituteAdelaideAustralia
  3. 3.Novozymes Biopharma AU LimitedThebartonAustralia

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