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01-06-2009 | NON-THEMATIC REVIEW

The biological role and regulation of versican levels in cancer

Authors: Carmela Ricciardelli, Andrew J. Sakko, Miranda P. Ween, Darryl L. Russell, David J. Horsfall

Published in: Cancer and Metastasis Reviews | Issue 1-2/2009

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.

Bryant, R. J., & Hamdy, F. C. (2008). Screening for prostate cancer: an update. European Urology, 53(1), 37–44.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

Friedl, P., & Wolf, K. (2008). Tube travel: the role of proteases in individual and collective cancer cell invasion. Cancer Research, 68(18), 7247–7249.PubMedCrossRef

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.CrossRef

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.PubMed

Larue, L., & Bellacosa, A. (2005). Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3’ kinase/AKT pathways. Oncogene, 24(50), 7443–7454.PubMedCrossRef

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.

11.

Alexandrova, A. Y. (2008). Evolution of cell interactions with extracellular matrix during carcinogenesis. Biochemistry (Moscow), 73(7), 733–741.CrossRef

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.PubMedCrossRef

13.

Cattaruzza, S., & Perris, R. (2005). Proteoglycan control of cell movement during wound healing and cancer spreading. Matrix Biology, 24(6), 400–417.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

16.

Zimmermann, D. R., & Ruoslahti, E. (1989). Multiple domains of the large fibroblast proteoglycan, versican. The EMBO Journal, 8(10), 2975–2981.PubMed

17.

LeBaron, R. G. (1996). Versican. Perspectives on Developmental Neurobiology, 3(4), 261–271.PubMed

18.

LeBaron, R. G., Zimmermann, D. R., & Ruoslahti, E. (1992). Hyaluronate binding properties of versican. Journal of Biological Chemistry, 267(14), 10003–10010.PubMed

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.PubMedCrossRef

20.

Wight, T. N. (2002). Versican: a versatile extracellular matrix proteoglycan in cell biology. Current Opinions in Cell Biology, 14(5), 617–623.CrossRef

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.PubMedCrossRef

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.PubMed

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.

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.PubMedCrossRef

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.

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.PubMedCrossRef

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMed

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.PubMed

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.

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.PubMedCrossRef

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.

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.

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.PubMed

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.CrossRef

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.PubMedCrossRef

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.PubMed

88.

Kenagy, R. D., Plaas, A. H., & Wight, T. N. (2006). Versican degradation and vascular disease. Trends in Cardiovascular Medicine, 16(6), 209–215.PubMedCrossRef

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.CrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMed

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMed

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.CrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.PubMed

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.CrossRef

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.CrossRef

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.

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.CrossRef

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.PubMedCrossRef

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.PubMed

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.PubMed

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.CrossRef

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.CrossRef

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.PubMedCrossRef

Title: The biological role and regulation of versican levels in cancer
Authors: Carmela Ricciardelli
Andrew J. Sakko
Miranda P. Ween
Darryl L. Russell
David J. Horsfall
Publication date: 01-06-2009
Publisher: Springer US
Published in: Cancer and Metastasis Reviews / Issue 1-2/2009
Print ISSN: 0167-7659
Electronic ISSN: 1573-7233
DOI: https://doi.org/10.1007/s10555-009-9182-y

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