Table of Contents Author Guidelines Submit a Manuscript
Journal of Oncology
Volume 2010, Article ID 586905, 13 pages
http://dx.doi.org/10.1155/2010/586905
Review Article

Extracellular Matrix Proteins and Tumor Angiogenesis

1Department of Biomedical Sciences, University of Guelph, Guelph, ON, Canada N1G 2W1
2CIHR Group in Matrix Biology, University of Toronto, ON, Canada M5G 1G6
3Department of Pathobiology, University of Guelph, Guelph, ON, Canada N1G 2W1

Received 2 November 2009; Accepted 26 May 2010

Academic Editor: Kalpna Gupta

Copyright © 2010 N. E. Campbell 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. Radisky, C. Hagios, and M. J. Bissell, “Tumors are unique organs defined by abnormal signaling and context,” Seminars in Cancer Biology, vol. 11, no. 2, pp. 87–95, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Brekken, O. S. Bruland, and C. de Lange Davies, “Interstitial fluid pressure in human osteosarcoma xenografts: significance of implantation site and the response to intratumoral injection of hyaluronidase,” Anticancer Research, vol. 20, no. 5, pp. 3503–3512, 2000. View at Google Scholar · View at Scopus
  3. D. Fukumura, F. Yuan, W. L. Monsky, Y. Chen, and R. K. Jain, “Effect of host microenvironment on the microcirculation of human colon adenocarcinoma,” American Journal of Pathology, vol. 151, no. 3, pp. 679–688, 1997. View at Google Scholar · View at Scopus
  4. J. J. Killion, R. Radinsky, and I. J. Fidler, “Orthotopic models are necessary to predict therapy of transplantable tumors in mice,” Cancer and Metastasis Reviews, vol. 17, no. 3, pp. 279–284, 1998. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Greenaway, R. Moorehead, P. Shaw, and J. Petrik, “Epithelial-stromal interaction increases cell proliferation, survival and tumorigenicity in a mouse model of human epithelial ovarian cancer,” Gynecologic Oncology, vol. 108, no. 2, pp. 385–394, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Wernert, “The multiple roles of tumour stroma,” Virchows Archiv, vol. 430, no. 6, pp. 433–443, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. J. Folkman, “Tumor angiogenesis: therapeutic implications,” New England Journal of Medicine, vol. 285, no. 21, pp. 1182–1186, 1971. View at Google Scholar · View at Scopus
  8. J. Folkman and M. Klagsbrun, “Angiogenic factors,” Science, vol. 235, no. 4787, pp. 442–447, 1987. View at Google Scholar · View at Scopus
  9. J. Folkman, K. Watson, D. Ingber, and D. Hanahan, “Induction of angiogenesis during the transition from hyperplasia to neoplasia,” Nature, vol. 339, no. 6219, pp. 58–61, 1989. View at Google Scholar · View at Scopus
  10. P. Carmeliet, “Angiogenesis in health and disease,” Nature Medicine, vol. 9, no. 6, pp. 653–660, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Ferrara, K. Houck, L. Jakeman, and D. W. Leung, “Molecular and biological properties of the vascular endothelial growth factor family of proteins,” Endocrine Reviews, vol. 13, no. 1, pp. 18–32, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. Z. Galzie, A. R. Kinsella, and J. A. Smith, “Fibroblast growth factors and their receptors,” Biochemistry and Cell Biology, vol. 75, no. 6, pp. 669–685, 1997. View at Google Scholar · View at Scopus
  13. A. Compagni, P. Wilgenbus, M.-A. Impagnatiello, M. Cotten, and G. Christofori, “Fibroblast growth factors are required for efficient tumor angiogenesis,” Cancer Research, vol. 60, no. 24, pp. 7163–7169, 2000. View at Google Scholar · View at Scopus
  14. P. Gerwins, E. Sköldenberg, and L. Claesson-Welsh, “Function of fibroblast growth factors and vascular endothelial growth factors and their receptors in angiogenesis,” Critical Reviews in Oncology/Hematology, vol. 34, no. 3, pp. 185–194, 2000. View at Publisher · View at Google Scholar · View at Scopus
  15. S. A. Rabbani, “Metalloproteases and urokinase in angiogenesis and tumor progression,” In Vivo, vol. 12, no. 1, pp. 135–142, 1998. View at Google Scholar
  16. J. P. Geisler, G. A. Miller, J. R. Broshears, and K. J. Manahan, “Vascular endothelial growth factor staining and elevated INR in advanced epithelial ovarian carcinoma,” Journal of Surgical Oncology, vol. 96, no. 6, pp. 514–517, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. D. R. Senger, S. J. Galli, A. M. Dvorak, C. A. Perruzzi, V. Susan Harvey, and H. F. Dvorak, “Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid,” Science, vol. 219, no. 4587, pp. 983–985, 1983. View at Google Scholar · View at Scopus
  18. L. De Cecco, L. Marchionni, M. Gariboldi et al., “Gene expression profiling of advanced ovarian cancer: characterization of a molecular signature involving fibroblast growth factor 2,” Oncogene, vol. 23, no. 49, pp. 8171–8183, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Salgado, I. Benoy, P. Vermeulen, P. van Dam, E. van Marck, and L. Dirix, “Circulating basic fibroblast growth factor is partly derived from the tumour in patients with colon, cervical and ovarian cancer,” Angiogenesis, vol. 7, no. 1, pp. 29–32, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. A. M. Di Blasio, C. Carniti, P. Vigano, and M. Vignali, “Basic fibroblast growth factor and ovarian cancer,” Journal of Steroid Biochemistry and Molecular Biology, vol. 53, no. 1–6, pp. 375–379, 1995. View at Publisher · View at Google Scholar · View at Scopus
  21. M. K. Whitworth, A. C. Backen, A. R. Clamp et al., “Regulation of fibroblast growth factor-2 activity by human ovarian cancer tumor endothelium,” Clinical Cancer Research, vol. 11, no. 12, pp. 4282–4288, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Klagsbrun and P. A. D'Amore, “Regulators of angiogenesis,” Annual Review of Physiology, vol. 53, pp. 217–239, 1991. View at Google Scholar · View at Scopus
  23. J. Sottile, “Regulation of angiogenesis by extracellular matrix,” Biochimica et Biophysica Acta, vol. 1654, no. 1, pp. 13–22, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Rouet, Y. Hamma-Kourbali, E. Petit et al., “A synthetic glycosaminoglycan mimetic binds vascular endothelial growth factor and modulates angiogenesis,” Journal of Biological Chemistry, vol. 280, no. 38, pp. 32792–32800, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. 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
  26. M. I. Góth, E. Hubina, S. Raptis, G. M. Nagy, and B. E. Tóth, “Physiological and pathological angiogenesis in the endocrine system,” Microscopy Research and Technique, vol. 60, no. 1, pp. 98–106, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. R. V. Iozzo and J. D. San Antonio, “Heparan sulfate proteoglycans: heavy hitters in the angiogenesis arena,” Journal of Clinical Investigation, vol. 108, no. 3, pp. 349–355, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. R. Sasisekharan, M. A. Moses, M. A. Nugent, C. L. Cooney, and R. Langer, “Heparinase inhibits neovascularization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 4, pp. 1524–1528, 1994. View at Google Scholar · View at Scopus
  29. A. Walker, J. E. Turnbull, and J. T. Gallagher, “Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor,” Journal of Biological Chemistry, vol. 269, no. 2, pp. 931–935, 1994. View at Google Scholar · View at Scopus
  30. S. A. Karumanchi, V. Jha, R. Ramchandran et al., “Cell surface glypicans are low-affinity endostatin receptors,” Molecular Cell, vol. 7, no. 4, pp. 811–822, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. T. M. Mundel and R. Kalluri, “Type IV collagen-derived angiogenesis inhibitors,” Microvascular Research, vol. 74, no. 2-3, pp. 85–89, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. M. S. Pepper, “Extracellular proteolysis and angiogenesis,” Thrombosis and Haemostasis, vol. 86, no. 1, pp. 346–355, 2001. View at Google Scholar · View at Scopus
  33. O. Saksela and D. B. Rifkin, “Release of basic fibroblast growth factor-heparan sulfate complexes from endothelial cells by plasminogen activator-mediated proteolytic activity,” Journal of Cell Biology, vol. 110, no. 3, pp. 767–775, 1990. View at Google Scholar · View at Scopus
  34. B. Kaur, D. J. Brat, N. S. Devi, and E. G. Van Meir, “Vasculostatin, a proteolytic fragment of brain angiogenesis inhibitor 1, is an antiangiogenic and antitumorigenic factor,” Oncogene, vol. 24, no. 22, pp. 3632–3642, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. H. A. Hanford, C. A. Wong, H. Kassan et al., “Angiostatin4.5-mediated apoptosis of vascular endothelial cells,” Cancer Research, vol. 63, no. 14, pp. 4275–4280, 2003. View at Google Scholar · View at Scopus
  36. J. Folkman, “Tumor suppression by p53 is mediated in part by the antiangiogenic activity of endostatin and tumstatin,” Science's STKE, vol. 2006, no. 354, article pe35, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. J. T. Yang, H. Rayburn, and R. O. Hynes, “Embryonic mesodermal defects in α5 integrin-deficient mice,” Development, vol. 119, no. 4, pp. 1093–1105, 1993. View at Google Scholar · View at Scopus
  38. K. L. Goh, J. T. Yang, and R. O. Hynes, “Mesodermal defects and cranial neural crest apoptosis in α5 integrin-null embryos,” Development, vol. 124, no. 21, pp. 4309–4319, 1997. View at Google Scholar · View at Scopus
  39. S. E. Francis, K. L. Goh, K. Hodivala-Dilke et al., “Central roles of α5β1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 6, pp. 927–933, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Marcinkiewicz, P. H. Weinreb, J. J. Calvete et al., “Obtustatin: a potent selective inhibitor of α1β1 integrin in vitro and angiogenesis in vivo,” Cancer Research, vol. 63, no. 9, pp. 2020–2023, 2003. View at Google Scholar · View at Scopus
  41. K. Tashiro, G. C. Sephel, B. Weeks et al., “A synthetic peptide containing the IKVAV sequence from the A chain of laminin mediates cell attachment, migration, and neurite outgrowth,” Journal of Biological Chemistry, vol. 264, no. 27, pp. 16174–16182, 1989. View at Google Scholar · View at Scopus
  42. M. C. Kibbey, D. S. Grant, and H. K. Kleinman, “Role of the SIKVAV site of laminin in promotion of angiogenesis and tumor growth: an in vivo Matrigel model,” Journal of the National Cancer Institute, vol. 84, no. 21, pp. 1633–1638, 1992. View at Google Scholar · View at Scopus
  43. K. M. Malinda, M. Nomizu, M. Chung et al., “Identification of laminin α1 and β1 chain peptides active for endothelial cell adhesion, tube formation, and aortic sprouting,” FASEB Journal, vol. 13, no. 1, pp. 53–62, 1999. View at Google Scholar · View at Scopus
  44. A. Mettouchi, S. Klein, W. Guo et al., “Integrin-specific activation of Rac controls progression through the G1 phase of the cell cycle,” Molecular Cell, vol. 8, no. 1, pp. 115–127, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. M. S. Pepper, “Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 21, no. 7, pp. 1104–1117, 2001. View at Google Scholar · View at Scopus
  46. T. Itoh, M. Tanioka, H. Yoshida, T. Yoshioka, H. Nishimoto, and S. Itohara, “Reduced angiogenesis and tumor progression in gelatinase A-deficient mice,” Cancer Research, vol. 58, no. 5, pp. 1048–1051, 1998. View at Google Scholar · View at Scopus
  47. J. Fang, Y. Shing, D. Wiederschain et al., “Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 8, pp. 3884–3889, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Zhang, L. Meng, Q. Wang et al., “Enhanced in vitro invasiveness of ovarian cancer cells through up-regulation of VEGF and induction of MMP-2,” Oncology Reports, vol. 15, no. 4, pp. 831–836, 2006. View at Google Scholar · View at Scopus
  49. S. Lee, S. M. Jilan, G. V. Nikolova, D. Carpizo, and M. Luisa Iruela-Arispe, “Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors,” Journal of Cell Biology, vol. 169, no. 4, pp. 681–691, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Hollborn, C. Stathopoulos, A. Steffen, P. Wiedemann, L. Kohen, and A. Bringmann, “Positive feedback regulation between MMP-9 and VEGF in human RPE cells,” Investigative Ophthalmology and Visual Science, vol. 48, no. 9, pp. 4360–4367, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. L. J. A. C. Hawinkels, K. Zuidwijk, H. W. Verspaget et al., “VEGF release by MMP-9 mediated heparan sulphate cleavage induces colorectal cancer angiogenesis,” European Journal of Cancer, vol. 44, no. 13, pp. 1904–1913, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. T. Onguchi, K. Y. Han, J.-H. Chang, and D. T. Azar, “Membrane type-1 matrix metalloproteinase potentiates basic fibroblast growth factor-induced corneal neovascularization,” American Journal of Pathology, vol. 174, no. 4, pp. 1564–1571, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. N. E. Sounni, L. Devy, A. Hajitou et al., “MTI-MMP expression promotes tumor growth and angiogenesis through an up-regulation of vascular endothelial growth factor expression,” FASEB Journal, vol. 16, no. 6, pp. 555–564, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. E. I. Deryugina, L. Soroceanu, and A. Y. Strongin, “Up-regulation of vascular endothelial growth factor by membrane-type 1 matrix metalloproteinase stimulates human glioma xenograft growth and angiogenesis,” Cancer Research, vol. 62, no. 2, pp. 580–588, 2002. View at Google Scholar · View at Scopus
  55. J. C. Rodríguez-Manzaneque, T. F. Lane, M. A. Ortega, R. O. Hynes, J. Lawler, and M. L. Iruela-Arispe, “Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 22, pp. 12485–12490, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. A. J. Trimboli, C. Z. Cantemir-Stone, F. Li et al., “Pten in stromal fibroblasts suppresses mammary epithelial tumours,” Nature, vol. 461, no. 7267, pp. 1084–1091, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. R. Kalluri, “Basement membranes: structure, assembly and role in tumour angiogenesis,” Nature Reviews Cancer, vol. 3, no. 6, pp. 422–433, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. M. S. O'Reilly, L. Holmgren, Y. Shing et al., “Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma,” Cell, vol. 79, no. 2, pp. 315–328, 1994. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Ikenaka, H. Yoshiji, S. Kuriyama et al., “Tissue inhibitor of metalloproteinases-1 (TIMP-1) inhibits tumor growth and angiogenesis in the TIMP-1 transgenic mouse model,” International Journal of Cancer, vol. 105, no. 3, pp. 340–346, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. D.-W. Seo, H. Li, L. Guedez et al., “TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism,” Cell, vol. 114, no. 2, pp. 171–180, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. P. Valente, G. Fassina, A. Melchiori et al., “TIMP-2 over-expression reduces invasion and angiogenesis and protects B16F10 melanoma cells from apoptosis,” International Journal of Cancer, vol. 75, no. 2, pp. 246–253, 1998. View at Publisher · View at Google Scholar · View at Scopus
  62. A. L. Feldman, W. G. Stetler-Stevenson, N. G. Costouros et al., “Modulation of tumor-host interactions, angiogenesis, and tumor growth by tissue inhibitor of metalloproteinase 2 via a novel mechanism,” Cancer Research, vol. 64, no. 13, pp. 4481–4486, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Hajitou, N.-E. Sounni, L. Devy et al., “Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: effect on in vivo mammary tumor growth and angiogenesis,” Cancer Research, vol. 61, no. 8, pp. 3450–3457, 2001. View at Google Scholar · View at Scopus
  64. D.-W. Seo, S. H. Kim, S.-H. Eom et al., “TIMP-2 disrupts FGF-2-induced downstream signaling pathways,” Microvascular Research, vol. 76, no. 3, pp. 145–151, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. W. W. Spurbeck, C. Y. C. Ng, T. S. Strom, E. F. Vanin, and A. M. Davidoff, “Enforced expression of tissue inhibitor of matrix metalloproteinase-3 affects functional capillary morphogenesis and inhibits tumor growth in a murine tumor model,” Blood, vol. 100, no. 9, pp. 3361–3368, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. K.-H. Kang, S.-Y. Park, S. B. Rho, and J.-H. Lee, “Tissue inhibitor of metalloproteinases-3 interacts with angiotensin II type 2 receptor and additively inhibits angiogenesis,” Cardiovascular Research, vol. 79, no. 1, pp. 150–160, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Chetty, S. S. Lakka, P. Bhoopathi, S. Kunigal, R. Geiss, and J. S. Rao, “Tissue inhibitor of metalloproteinase 3 suppresses tumor angiogenesis in matrix metalloproteinase 2-down-regulated lung cancer,” Cancer Research, vol. 68, no. 12, pp. 4736–4745, 2008. View at Publisher · View at Google Scholar · View at Scopus
  68. W. Cruz-Muñoz, I. Kim, and R. Khokha, “TIMP-3 deficiency in the host, but not in the tumor, enhances tumor growth and angiogenesis,” Oncogene, vol. 25, no. 4, pp. 650–655, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. M. L. Corcoran and W. G. Stetler-Stevenson, “Tissue inhibitor of metalloproteinase-2 stimulates fibroblast proliferation via a cAMP-dependent mechanism,” Journal of Biological Chemistry, vol. 270, no. 22, pp. 13453–13459, 1995. View at Publisher · View at Google Scholar · View at Scopus
  70. S. E. Hoegy, H.-R. Oh, M. L. Corcoran, and W. G. Stetler-Stevenson, “Tissue inhibitor of metalloproteinases-2 (TIMP-2) suppresses TKR-growth factor signaling independent of metalloproteinase inhibition,” Journal of Biological Chemistry, vol. 276, no. 5, pp. 3203–3214, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. J. Oh, B.-W. Seo, T. Diaz et al., “Tissue inhibitors of metalloproteinase 2 inhibits endothelial cell migration through increased expression of RECK,” Cancer Research, vol. 64, no. 24, pp. 9062–9069, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. C. A. Fernández, C. Butterfield, G. Jackson, and M. A. Moses, “Structural and functional uncoupling of the enzymatic and angiogenic inhibitory activities of tissue inhibitor of metalloproteinase-2 (TIMP-2): loop 6 is a novel angiogenesis inhibitor,” Journal of Biological Chemistry, vol. 278, no. 42, pp. 40989–40995, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. J. R. Dunn, J. E. Reed, D. G. du Plessis et al., “Expression of ADAMTS-8, a secreted protease with antiangiogenic properties, is downregulated in brain tumours,” British Journal of Cancer, vol. 94, no. 8, pp. 1186–1193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  74. P. Göoz, M. Göoz, A. Baldys, and S. Hoffman, “ADAM-17 regulates endothelial cell morphology, proliferation, and in vitro angiogenesis,” Biochemical and Biophysical Research Communications, vol. 380, no. 1, pp. 33–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Sharghi-Namini, H. Fan, K. N. Sulochana et al., “The first but not the second thrombospondin type 1 repeat of ADAMTS5 functions as an angiogenesis inhibitor,” Biochemical and Biophysical Research Communications, vol. 371, no. 2, pp. 215–219, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. F. Vázquez, G. Hastings, M.-A. Ortega et al., “METH-1, a human ortholog of ADAMTS-1, and METH-2 are members of a new family of proteins with angio-inhibitory activity,” Journal of Biological Chemistry, vol. 274, no. 33, pp. 23349–23357, 1999. View at Publisher · View at Google Scholar · View at Scopus
  77. A. Luque, D. R. Carpizo, and M. L. Iruela-Arispe, “ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165,” Journal of Biological Chemistry, vol. 278, no. 26, pp. 23656–23665, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. O. L. Podhajcer, L. G. Benedetti, M. R. Girotti, F. Prada, E. Salvatierra, and A. S. Llera, “The role of the matricellular protein SPARC in the dynamic interaction between the tumor and the host,” Cancer and Metastasis Reviews, vol. 27, no. 4, pp. 691–705, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. A. Chlenski, S. Liu, L. J. Guerrero et al., “SPARC expression is associated with impaired tumor growth, inhibited angiogenesis and changes in the extracellular matrix,” International Journal of Cancer, vol. 118, no. 2, pp. 310–316, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. C. K. Yunker, W. Golembieski, N. Lemke et al., “SPARC-induced increase in glioma matrix and decrease in vascularity are associated with reduced VEGF expression and secretion,” International Journal of Cancer, vol. 122, no. 12, pp. 2735–2743, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. A. Chlenski, L. J. Guerrero, Q. Yang et al., “SPARC enhances tumor stroma formation and prevents fibroblast activation,” Oncogene, vol. 26, no. 31, pp. 4513–4522, 2007. View at Publisher · View at Google Scholar · View at Scopus
  82. C. Kupprion, K. Motamed, and E. H. Sage, “SPARC (BM-40, osteonectin) inhibits the mitogenic effect of vascular endothelial growth factor on microvascular endothelial cells,” Journal of Biological Chemistry, vol. 273, no. 45, pp. 29635–29640, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. P. Nyberg, L. Xie, and R. Kalluri, “Endogenous inhibitors of angiogenesis,” Cancer Research, vol. 65, no. 10, pp. 3967–3979, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Folkman, “Endogenous angiogenesis inhibitors,” APMIS, vol. 112, no. 7-8, pp. 496–507, 2004. View at Publisher · View at Google Scholar · View at Scopus
  85. D. J. Good, P. J. Polverini, F. Rastinejad et al., “A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 17, pp. 6624–6628, 1990. View at Google Scholar · View at Scopus
  86. B. Schmierer and C. S. Hill.
  87. L. David, J.-J. Feige, and S. Bailly, “Emerging role of bone morphogenetic proteins in angiogenesis,” Cytokine and Growth Factor Reviews, vol. 20, no. 3, pp. 203–212, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. M. M. L. Deckers, R. L. van Bezooijen, D. E. R. van Geertje Horst et al., “Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A,” Endocrinology, vol. 143, no. 4, pp. 1545–1553, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Rothhammer, F. Bataille, T. Spruss, G. Eissner, and A.-K. Bosserhoff, “Functional implication of BMP4 expression on angiogenesis in malignant melanoma,” Oncogene, vol. 26, no. 28, pp. 4158–4170, 2007. View at Publisher · View at Google Scholar · View at Scopus
  90. J. R. Mathura Jr., N. Jafari, J. T. Chang et al., “Bone morphogenetic proteins-2 and-4: negative growth regulators in adult retinal pigmented epithelium,” Investigative Ophthalmology and Visual Science, vol. 41, no. 2, pp. 592–600, 2000. View at Google Scholar · View at Scopus
  91. R. Kane, C. Godson, and C. O'Brien, “Chordin-like 1, a bone morphogenetic protein-4 antagonist, is upregulated by hypoxia in human retinal pericytes and plays a role in regulating angiogenesis,” Molecular Vision, vol. 14, pp. 1138–1148, 2008. View at Google Scholar · View at Scopus
  92. P. ten Dijke and H. M. Arthur.
  93. C. Morrissey, L. G. Brown, T. E. M. Pitts, R. L. Vessella, and E. Corey, “Bone morphogenetic protein 7 is expressed in prostate cancer metastases and its effects on prostate tumor cells depend on cell phenotype and the tumor microenvironment,” Neoplasia, vol. 12, no. 2, pp. 192–205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. E. M. Langenfeld, Y. Kong, and J. Langenfeld, “Bone morphogenetic protein 2 stimulation of tumor growth involves the activation of Smad-1/5,” Oncogene, vol. 25, no. 5, pp. 685–692, 2006. View at Publisher · View at Google Scholar · View at Scopus
  95. J. M. Bailey, P. K. Singh, and M. A. Hollingsworth, “Cancer metastasis facilitated by developmental pathways: sonic hedgehog, notch, and bone morphogenic proteins,” Journal of Cellular Biochemistry, vol. 102, no. 4, pp. 829–839, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Takiguchi, M. Kobayashi, R. Suzuki et al., “Recombinant human bone morphogenetic protein-2 stimulates osteoblast differentiation and suppresses matrix metalloproteinase-1 production in human bone cells isolated from mandibulae,” Journal of Periodontal Research, vol. 33, no. 8, pp. 476–485, 1998. View at Google Scholar · View at Scopus
  97. T. Kumagai, T. Shimizu, and K. Takeda, “Bone morphogenetic protein-2 suppresses invasiveness of TSU-Pr1 cells with the inhibition of MMP-9 secretion,” Anticancer Research, vol. 26, no. 1, pp. 293–298, 2006. View at Google Scholar · View at Scopus
  98. T. C. Otto, R. R. Bowers, and M. D. Lane.
  99. T. G. Shepherd, M. L. Mujoomdar, and M. W. Nachtigal, “Constitutive activation of BMP signalling abrogates experimental metastasis of OVCA429 cells via reduced cell adhesion,” Journal of Ovarian Research, vol. 3, no. 1, article 5, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. N. L. Baenziger, G. N. Brodie, and P. W. Majerus, “A thrombin-sensitive protein of human platelet membranes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 68, no. 1, pp. 240–243, 1971. View at Google Scholar · View at Scopus
  101. N. L. Baenziger, G. N. Brodie, and P. W. Majerus, “Isolation and properties of a thrombin-sensitive protein of human platelets,” Journal of Biological Chemistry, vol. 247, no. 9, pp. 2723–2731, 1972. View at Google Scholar · View at Scopus
  102. J. W. Lawler and H. S. Slayter, “The release of heparin binding peptides from platelet thrombospondin by proteolytic action of thrombin, plasmin and trypsin,” Thrombosis Research, vol. 22, no. 3, pp. 267–279, 1981. View at Google Scholar · View at Scopus
  103. V. M. Dixit, G. A. Grant, S. A. Santoro, and W. A. Frazier, “Isolation and characterization of a heparin-binding domain from the amino terminus of platelet thrombospondin,” Journal of Biological Chemistry, vol. 259, no. 16, pp. 10100–10105, 1984. View at Google Scholar · View at Scopus
  104. G. O. Gogstad, N. O. Solum, and M. B. Krutnes, “Heparin-binding platelet proteins demonstrated by crossed affinity immunoelectrophoresis,” British Journal of Haematology, vol. 53, no. 4, pp. 563–573, 1983. View at Google Scholar · View at Scopus
  105. J. Lahav, M. A. Schwartz, and R. O. Hynes, “Analysis of platelet adhesion with a radioactive chemical crosslinking reagent: interaction of thrombospondin with fibronectin and collagen,” Cell, vol. 31, no. 1, pp. 253–262, 1982. View at Google Scholar · View at Scopus
  106. J. Lahav, J. Lawler, and M. A. Gimbrone, “Thrombospondin interactions with fibronectin and fibrinogen. Mutual inhibition in binding,” European Journal of Biochemistry, vol. 145, no. 1, pp. 151–156, 1984. View at Google Scholar · View at Scopus
  107. L. L. K. Leung and R. L. Nachman, “Complex formation of platelet thrombospondin with fibrinogen,” Journal of Clinical Investigation, vol. 70, no. 3, pp. 542–549, 1982. View at Google Scholar · View at Scopus
  108. G. P. Tuszynski, S. Srivastava, H. I. Switalska, J. C. Holt, C. S. Cierniewski, and S. Niewiarowski, “The interaction of human platelet thrombospondin with fibrinogen: thrombospondin purification and specificity of interaction,” Journal of Biological Chemistry, vol. 260, no. 22, pp. 12240–12245, 1985. View at Google Scholar · View at Scopus
  109. R. L. Silverstein, L. L. K. Leung, P. C. Harpel, and R. L. Nachman, “Platelet thrombospondin forms a trimolecular complex with plasminogen and histidine-rich glycoprotein,” Journal of Clinical Investigation, vol. 75, no. 6, pp. 2065–2073, 1985. View at Google Scholar · View at Scopus
  110. L. L. K. Leung, R. L. Nachman, and P. C. Harpel, “Complex formation of platelet thrombospondin with histidine-rich glycoprotein,” Journal of Clinical Investigation, vol. 73, no. 1, pp. 5–12, 1984. View at Google Scholar · View at Scopus
  111. S. M. Mumby, G. J. Raugi, and P. Bornstein, “Interactions of thrombospondin with extracellular matrix proteins: selective binding to type V collagen,” Journal of Cell Biology, vol. 98, no. 2, pp. 646–652, 1984. View at Google Scholar · View at Scopus
  112. J. Lawler and E. R. Simons, “Cooperative binding of calcium to thrombospondin. The effect of calcium on the circular dichroism and limited tryptic digestion of thrombospondin,” Journal of Biological Chemistry, vol. 258, no. 20, pp. 12098–12101, 1983. View at Google Scholar · View at Scopus
  113. D. R. Phillips, L. K. Jennings, and H. R. Prasanna, “Ca2+-mediated association of glycoprotein G (thrombin sensitive protein, thrombospondin) with human platelets,” Journal of Biological Chemistry, vol. 255, no. 24, pp. 11629–11632, 1980. View at Google Scholar · View at Scopus
  114. J. Lahav, “The functions of thrombospondin and its involvement in physiology and pathophysiology,” Biochimica et Biophysica Acta, vol. 1182, no. 1, pp. 1–14, 1993. View at Publisher · View at Google Scholar · View at Scopus
  115. G. J. Raugi, S. M. Mumby, D. Abbott-Brown, and P. Bornstein, “Thrombospondin: synthesis and secretion by cells in culture,” Journal of Cell Biology, vol. 95, no. 1, pp. 351–354, 1982. View at Google Scholar · View at Scopus
  116. E. A. Jaffe, J. T. Ruggiero, L. L. K. Leung, M. J. Doyle, P. J. McKeown-Longo, and D. F. Mosher, “Cultured human fibroblasts synthesize and secrete thrombospondin and incorporate it into extracellular matrix,” Proceedings of the National Academy of Sciences of the United States of America, vol. 80, no. 4, pp. 998–1002, 1983. View at Google Scholar · View at Scopus
  117. P. J. McKeown-Longo, R. Hanning, and D. F. Mosher, “Binding and degradation of platelet thrombospondin by cultured fibroblasts,” Journal of Cell Biology, vol. 98, no. 1, pp. 22–28, 1984. View at Google Scholar · View at Scopus
  118. J. McPherson, H. Sage, and P. Bornstein, “Isolation and characterization of a glycoprotein secreted by aortic endothelial cells in culture. Apparent identity with platelet thrombospondin,” Journal of Biological Chemistry, vol. 256, no. 21, pp. 11330–11336, 1981. View at Google Scholar · View at Scopus
  119. D. F. Mosher, M. J. Doyle, and E. A. Jaffe, “Synthesis and secretion of thrombospondin by cultured human endothelial cells,” Journal of Cell Biology, vol. 93, no. 2, pp. 343–348, 1982. View at Google Scholar · View at Scopus
  120. J. Lawler, “The structural and functional properties of thrombospondin,” Blood, vol. 67, no. 5, pp. 1197–1209, 1986. View at Google Scholar · View at Scopus
  121. J. Lawler, L. H. Derick, J. E. Connolly, J. H. Chen, and F. C. Chao, “The structure of human platelet thrombospondin,” Journal of Biological Chemistry, vol. 260, no. 6, pp. 3762–3772, 1985. View at Google Scholar · View at Scopus
  122. J. Lawler, H. S. Slayter, and J. E. Coligan, “Isolation and characterization of a high molecular weight glycoprotein from human blood platelets,” Journal of Biological Chemistry, vol. 253, no. 23, pp. 8609–8616, 1978. View at Google Scholar · View at Scopus
  123. J. Lawler, F. C. Chao, and P. H. Fang, “Observation of a high molecular weight platelet protein released by thrombin,” Thrombosis and Haemostasis, vol. 37, no. 2, pp. 355–357, 1977. View at Google Scholar
  124. P. Bornstein, “Thrombospondins: structure and regulation of expression,” FASEB Journal, vol. 6, no. 14, pp. 3290–3299, 1992. View at Google Scholar · View at Scopus
  125. J. E. Coligan and H. S. Slayter, “Structure of thrombospondin,” Journal of Biological Chemistry, vol. 259, no. 6, pp. 3944–3948, 1984. View at Google Scholar · View at Scopus
  126. J. Lawler and R. O. Hynes, “The structure of human thrombospondin, an adhesive glycoprotein with multiple calcium-binding sites and homologies with several different proteins,” Journal of Cell Biology, vol. 103, no. 5, pp. 1635–1648, 1986. View at Google Scholar · View at Scopus
  127. J. Lawler, M. Duquette, L. Urry, K. McHenry, and T. F. Smith, “The evolution of the thrombospondin gene family,” Journal of Molecular Evolution, vol. 36, no. 6, pp. 509–516, 1993. View at Publisher · View at Google Scholar · View at Scopus
  128. J. C. Adams, “Thrombospondins: multifunctional regulators of cell interactions,” Annual Review of Cell and Developmental Biology, vol. 17, pp. 25–51, 2001. View at Publisher · View at Google Scholar · View at Scopus
  129. P. Bornstein and E. H. Sage, “Thrombospondins,” Methods in Enzymology, vol. 245, pp. 62–85, 1994. View at Publisher · View at Google Scholar · View at Scopus
  130. J. Adams and J. Lawler, “The thrombospondin family,” Current Biology, vol. 3, no. 3, pp. 188–190, 1993. View at Google Scholar · View at Scopus
  131. G. Taraboletti, D. Roberts, L. A. Liotta, and R. Giavazzi, “Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor,” Journal of Cell Biology, vol. 111, no. 2, pp. 765–772, 1990. View at Publisher · View at Google Scholar · View at Scopus
  132. R. A. Majack, L. V. Goodman, and V. M. Dixit, “Cell surface thrombospondin is functionally essential for vascular smooth muscle cell proliferation,” Journal of Cell Biology, vol. 106, no. 2, pp. 415–422, 1988. View at Google Scholar · View at Scopus
  133. G. Taraboletti, D. D. Roberts, and L. A. Liotta, “Thrombodspondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains,” Journal of Cell Biology, vol. 105, no. 5, pp. 2409–2415, 1987. View at Google Scholar · View at Scopus
  134. T. Vogel, N. Guo, H. C. Krutzsch et al., “Modulation of endothelial cell proliferation, adhesion, and motility by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin,” Journal of Cellular Biochemistry, vol. 53, no. 1, pp. 74–84, 1993. View at Google Scholar · View at Scopus
  135. N. V. Ketis, J. Lawler, R. L. Hoover, and M. J. Karnosvky, “Effects of heat shock on the expression of thrombospondin by endothelial cells in culture,” Journal of Cell Biology, vol. 106, no. 3, pp. 893–904, 1988. View at Google Scholar · View at Scopus
  136. N. V. Ketis and J. Lawler, “Effects of thrombospondin antibody on the recovery of endothelial cells from hyperthermia,” Journal of Cell Science, vol. 96, no. 2, pp. 263–270, 1990. View at Google Scholar · View at Scopus
  137. C. Kreis, M. La Fleur, C. Menard, R. Paquin, and A. D. Beaulieu, “Thrombospondin and fibronectin are synthesized by neutrophils in human inflammatory joint disease and in a rabbit model of in vivo neutrophil activation,” Journal of Immunology, vol. 143, no. 6, pp. 1961–1968, 1989. View at Google Scholar · View at Scopus
  138. E. A. Jaffe, J. T. Ruggiero, and D. J. Falcone, “Monocytes and macrophages synthesize and secrete thrombospondin,” Blood, vol. 65, no. 1, pp. 79–84, 1985. View at Google Scholar · View at Scopus
  139. K. S. O'Shea, L.-H. J. Liu, L. H. Kinnunen, and V. M. Dixit, “Role of the extracellular matrix protein thrombospondin in the early development of the mouse embryo,” Journal of Cell Biology, vol. 111, no. 6, pp. 2713–2723, 1990. View at Publisher · View at Google Scholar · View at Scopus
  140. P. Bornstein, A. Agah, and T. R. Kyriakides, “The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury,” International Journal of Biochemistry and Cell Biology, vol. 36, no. 6, pp. 1115–1125, 2004. View at Publisher · View at Google Scholar · View at Scopus
  141. B. Ren, K. O. Yee, J. Lawler, and R. Khosravi-Far, “Regulation of tumor angiogenesis by thrombospondin-1,” Biochimica et Biophysica Acta, vol. 1765, no. 2, pp. 178–188, 2006. View at Publisher · View at Google Scholar · View at Scopus
  142. H. Chen, M. E. Herndon, and J. Lawler, “The cell biology of thrombospondin-1,” Matrix Biology, vol. 19, no. 7, pp. 597–614, 2000. View at Publisher · View at Google Scholar · View at Scopus
  143. J. Lawler, “Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth,” Journal of Cellular and Molecular Medicine, vol. 6, no. 1, pp. 1–12, 2002. View at Google Scholar · View at Scopus
  144. V. Zabrenetzky, C. C. Harris, P. S. Steeg, and D. D. Roberts, “Expression of the extracellular matrix molecule thrombospondin inversely correlates with malignant progression in melanoma, lung and breast carcinoma,” International Journal of Cancer, vol. 59, no. 2, pp. 191–195, 1994. View at Publisher · View at Google Scholar · View at Scopus
  145. D. L. Weinstat-Saslow, V. S. Zabrenetzky, K. VanHoutte, W. A. Frazier, D. D. Roberts, and P. S. Steeg, “Transfection of thrombospondin 1 complementary DNA into a human breast carcinoma cell line reduces primary tumor growth, metastatic potential, and angiogenesis,” Cancer Research, vol. 54, no. 24, pp. 6504–6511, 1994. View at Google Scholar · View at Scopus
  146. N. Sheibani and W. A. Frazier, “Thrombospondin 1 expression in transformed endothelial cells restores a normal phenotype and suppresses their tumorigenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 15, pp. 6788–6792, 1995. View at Publisher · View at Google Scholar · View at Scopus
  147. K. Bleuel, S. Popp, N. E. Fusenig, E. J. Stanbridge, and P. Boukamp, “Tumor suppression in human skin carcinoma cells by chromosome 15 transfer or thrombospondin-1 overexpression through halted tumor vascularization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 5, pp. 2065–2070, 1999. View at Publisher · View at Google Scholar · View at Scopus
  148. S. C. Hsu, O. V. Volpert, P. A. Steck et al., “Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1,” Cancer Research, vol. 56, no. 24, pp. 5684–5691, 1996. View at Google Scholar · View at Scopus
  149. M. Streit, P. Velasco, L. F. Brown et al., “Overexpression of thrombospondin-1 decreases angiogenesis and inhibits the growth of human cutaneous squamous cell carcinomas,” American Journal of Pathology, vol. 155, no. 2, pp. 441–452, 1999. View at Google Scholar · View at Scopus
  150. A. Fontana, S. Filleur, J. Guglielmi et al., “Human breast tumors override the antiangiogenic effect of stromal thrombospondin-1 in vivo,” International Journal of Cancer, vol. 116, no. 5, pp. 686–691, 2005. View at Publisher · View at Google Scholar · View at Scopus
  151. G. D. Grossfeld, D. A. Ginsberg, J. P. Stein et al., “Thrombospondin-1 expression in bladder cancer: association with p53 alterations, tumor angiogenesis, and tumor progression,” Journal of the National Cancer Institute, vol. 89, no. 3, pp. 219–227, 1997. View at Google Scholar · View at Scopus
  152. A. A. Alvarez, J. R. Axelrod, R. S. Whitaker et al., “Thrombospondin-1 expression in epithelial ovarian carcinoma: association with p53 status, tumor angiogenesis, and survival in platinum-treated patients,” Gynecologic Oncology, vol. 82, no. 2, pp. 273–278, 2001. View at Publisher · View at Google Scholar · View at Scopus
  153. L. Yao, Y.-L. Zhao, S. Itoh, S. Wada, L. Yue, and I. Furuta, “Thrombospondin-1 expression in oral squamous cell carcinomas: correlations with tumor vascularity, clinicopathological features and survival,” Oral Oncology, vol. 36, no. 6, pp. 539–544, 2000. View at Publisher · View at Google Scholar · View at Scopus
  154. K. Tanaka, H. Sonoo, J. Kurebayashi et al., “Inhibition of infiltration and angiogenesis by thrombospondin-1 in papillary thyroid carcinoma,” Clinical Cancer Research, vol. 8, no. 5, pp. 1125–1131, 2002. View at Google Scholar · View at Scopus
  155. J. Kodama, I. Hashimoto, N. Seki et al., “Thrombospondin-1 and -2 messenger RNA expression in invasive cervical cancer: correlation with angiogenesis and prognosis,” Clinical Cancer Research, vol. 7, no. 9, pp. 2826–2831, 2001. View at Google Scholar · View at Scopus
  156. N. Kawahara, M. Ono, K.-I. Taguhi et al., “Enhanced expression of thrombospondin-1 and hypovascularity in human cholangiocarcinoma,” Hepatology, vol. 28, no. 6, pp. 1512–1517, 1998. View at Google Scholar · View at Scopus
  157. J. Kodama, I. Hashimoto, N. Seki et al., “Thrombospondin-1 and -2 messenger RNA expression in epithelial ovarian tumor,” Anticancer Research, vol. 21, no. 4, pp. 2983–2987, 2001. View at Google Scholar · View at Scopus
  158. J. Folkman, “Anti-angiogenesis: new concept for therapy of solid tumors,” Annals of Surgery, vol. 175, no. 3, pp. 409–416, 1972. View at Google Scholar · View at Scopus
  159. B. A. Teicher, “A systems approach to cancer therapy,” Cancer and Metastasis Reviews, vol. 15, no. 2, pp. 247–272, 1996. View at Publisher · View at Google Scholar · View at Scopus
  160. D. Fukumura and R. K. Jain, “Imaging angiogenesis and the microenvironment,” APMIS, vol. 116, no. 7-8, pp. 695–715, 2008. View at Publisher · View at Google Scholar · View at Scopus
  161. C. Lu, A. A. Kamat, Y. G. Lin et al., “Dual targeting of endothelial cells and pericytes in antivascular therapy for ovarian carcinoma,” Clinical Cancer Research, vol. 13, no. 14, pp. 4209–4217, 2007. View at Publisher · View at Google Scholar · View at Scopus
  162. G. M. Tozer, C. Kanthou, G. Lewis, V. E. Prise, B. Vojnovic, and S. A. Hill, “Tumour vascular disrupting agents: combating treatment resistance,” British Journal of Radiology, vol. 81, pp. S12–S20, 2008. View at Publisher · View at Google Scholar · View at Scopus
  163. D. Fukumura and R. K. Jain, “Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization,” Microvascular Research, vol. 74, no. 2-3, pp. 72–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  164. R. K. Jain, “Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy,” Nature Medicine, vol. 7, no. 9, pp. 987–989, 2001. View at Publisher · View at Google Scholar · View at Scopus
  165. P. V. Dickson, J. B. Hamner, T. L. Sims et al., “Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy,” Clinical Cancer Research, vol. 13, no. 13, pp. 3942–3950, 2007. View at Publisher · View at Google Scholar · View at Scopus
  166. R. Yap, D. Veliceasa, U. Emmenegger et al., “Metronomic low-dose chemotherapy boosts CD95-dependent antiangiogenic effect of the thrombospondin peptide ABT-510: a complementation antiangiogenic strategy,” Clinical Cancer Research, vol. 11, no. 18, pp. 6678–6685, 2005. View at Publisher · View at Google Scholar · View at Scopus
  167. J. Greenaway, J. Lawler, R. Moorehead, P. Bornstein, J. Lamarre, and J. Petrik, “Thrombospondin-1 inhibits VEGF levels in the ovary directly by binding and internalization via the low density lipoprotein receptor-related protein-1 (LRP-1),” Journal of Cellular Physiology, vol. 210, no. 3, pp. 807–818, 2007. View at Publisher · View at Google Scholar · View at Scopus
  168. J. Greenaway, J. Henkin, J. Lawler, R. Moorehead, and J. Petrik, “ABT-510 induces tumor cell apoptosis and inhibits ovarian tumor growth in an orthotopic, syngeneic model of epithelial ovarian cancer,” Molecular Cancer Therapeutics, vol. 8, no. 1, pp. 64–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  169. K. Bein and M. Simons, “Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity,” Journal of Biological Chemistry, vol. 275, no. 41, pp. 32167–32173, 2000. View at Google Scholar · View at Scopus
  170. X. Qian, V. L. Rothman, R. F. Nicosia, and G. P. Tuszynski, “Expression of thrombospondin-1 in human pancreatic adenocarcinomas: role in matrix metalloproteinase-9 production,” Pathology and Oncology Research, vol. 7, no. 4, pp. 251–259, 2001. View at Google Scholar · View at Scopus
  171. A. Agah, T. R. Kyriakides, J. Lawler, and P. Bornstein, “The lack of thrombospondin-1 (TSP1) dictates the course of wound healing in double-TSP1/TSP2-null mice,” American Journal of Pathology, vol. 161, no. 3, pp. 831–839, 2002. View at Google Scholar · View at Scopus
  172. M. E. Herndon, C. S. Stipp, and A. D. Lander, “Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding,” Glycobiology, vol. 9, no. 2, pp. 143–155, 1999. View at Publisher · View at Google Scholar · View at Scopus
  173. C. A. Elzie and J. E. Murphy-Ullrich, “The N-terminus of thrombospondin: the domain stands apart,” International Journal of Biochemistry and Cell Biology, vol. 36, no. 6, pp. 1090–1101, 2004. View at Publisher · View at Google Scholar · View at Scopus
  174. M. A. Ferrari do Outeiro-Bernstein, S. S. Nunes, A. C. M. Andrade, T. R. Alves, C. Legrand, and V. Morandi, “A recombinant NH2-terminal heparin-binding domain of the adhesive glycoprotein, thrombospondin-1, promotes endothelial tube formation and cell survival: a possible role for syndecan-4 proteoglycan,” Matrix Biology, vol. 21, no. 4, pp. 311–324, 2002. View at Publisher · View at Google Scholar · View at Scopus
  175. P. K. Anonick, J. K. Yoo, D. J. Webb, and S. L. Gonias, “Characterization of the antiplasmin activity of human thrombospondin-1 in solution,” Biochemical Journal, vol. 289, no. 3, pp. 903–909, 1993. View at Google Scholar · View at Scopus
  176. P. J. Hogg, “Thrombospondin 1 as an enzyme inhibitor,” Thrombosis and Haemostasis, vol. 72, no. 6, pp. 787–792, 1994. View at Google Scholar