Endogenous inhibitors of angiogenesis in malignant gliomas: Nature's antiangiogenic therapy

Neuro-Oncology

Volumn 7, Issue 2, 2005, Pages 106-121

  Rege, Tanya A ^a,b   Fears, Constance Y ^a   Gladson, Candece L ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHOXYESTRADIOL; 4 DEDIMETHYLAMINOSANCYCLINE; ALGINIC ACID; ANGIOGENESIS INHIBITOR; ANGIOSTATIN; CARBOPLATIN; CD36 ANTIGEN; CILENGITIDE; ENDOSTATIN; ETOPOSIDE; GELATINASE A; HEMOPEXIN; MATRIX PROTEIN; PIGMENT EPITHELIUM DERIVED FACTOR; PROTEOCHONDROITIN SULFATE; PROTEOHEPARAN SULFATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; THROMBOCYTE FACTOR 4; THROMBOSPONDIN 1; THROMBOSPONDIN 2; THYMIDINE KINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TISSUE INHIBITOR OF METALLOPROTEINASE 4; TISSUE PLASMINOGEN ACTIVATOR; UNINDEXED DRUG; VASCULOTROPIN; VERY LATE ACTIVATION ANTIGEN 5; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; CANCER SURVIVAL; CLINICAL TRIAL; GLIOBLASTOMA; HUMAN; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR GROWTH; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ANGIOGENESIS INHIBITORS; ANGIOSTATINS; ANIMALS; BRAIN NEOPLASMS; ENDOSTATINS; EYE PROTEINS; GLIOMA; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; NERVE GROWTH FACTORS; PEPTIDE FRAGMENTS; SERPINS; SIGNAL TRANSDUCTION; THROMBOSPONDIN 1; THROMBOSPONDINS;

EID: 17844405022     PISSN: 15228517     EISSN: None     Source Type: Journal    
DOI: 10.1215/S115285170400119X     Document Type: Review

References (135)

1. Abdollahi, A., Hahnfeldt, P., Maercker, C., Grone, H.J., Debus, J., Ansorge, W., Folkman, J., Hlatky, L., and Huber, P.E. (2004) Endostatin's antiangiogenic signaling network. Mol. Cell 13, 649-663.
2. Adams, J.C., and Lawler, J. (2004) The thrombospondins. Int. J. Biochem. Cell Biol. 36, 961-968.
3. Allport, J.R., Shinde Patil, V.R., and Weissleder, R. (2004) Murine neuronal progenitor cells are preferentially recruited to tumor vasculature via alpha (4)-integrin and SDF-1 alpha-dependent mechanisms. Cancer Biol. Ther. 3, 838-844.
4. Annabi, B., Naud, E., Lee, Y.T., Eliopoulos, N., and Galipeau, J. (2004) Vascular progenitors derived from murine bone marrow stromal cells are regulated by fibroblast growth factor and are avidly recruited by vascularizing tumors. J. Cell. Biochem. 91, 1146-1158.
5. Armstrong, L.C., Bjorkblom, B., Hankenson, K.D., Siadak, A.W., Stiles, C.E., and Bornstein, P. (2002) Thrombospondin 2 inhibits microvascular endothelial cell proliferation by a caspase-independent mechanism. Mol. Biol. Cell 13, 1893-1905.
6. Bein, K., and Simons, M. (2000) Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity. J. Biol. Chem. 275, 32167-32173.
7. Bello, L., Lucini, V., Carrabba, G., Giussani, C., Machluf, M., Pluderi, M., Nikas, D., Zhang, J., Tomei, G., Villani, R.M., Carroll, R.S., Bikfalvi, A., and Black, P.M. (2001a) Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2. Cancer Res. 61, 8730-8736.
8. Bello, L., Carrabba, G., Giussani, C., Lucini, V., Cerutti, F., Scaglione, F., Landre, J., Pluderi, M., Tomei, G., Villani, R., Carroll, R.S., Black, P.M., and Bikfalvi, A. (2001b) Low-dose chemotherapy combined with an antiangiogenic drug reduces human glioma growth in vivo. Cancer Res. 61, 7501-7506.
9. Bello, L., Lucini, V., Costa, F., Pluderi, M., Giussani, C., Acerbi, F., Carrabba, G., Pannacci, M., Caronzolo, D., Grosso, S., Shinkaruk, S., Colleoni, F., Canron, X., Tomei, G., Deleris, G., and Bikfalvi, A. (2004) Combinatorial administration of molecules that simultaneously inhibit angiogenesis and invasion leads to increased therapeutic efficacy in mouse models of malignant glioma. Clin. Cancer Res. 10, 4527-4537.
10. Bertin, N., Clezardin, P., Kubiak, R., and Frappart, L. (1997) Thrombospondin-1 and -2 messenger RNA expression in normal, benign, and neoplastic human breast tissues: Correlation with prognostic factors, tumor angiogenesis, and fibroblastic desmoplasia. Cancer Res. 57, 396-399.
11. Bikfalvi, A. (2004) Recent developments in the inhibition of angiogenesis: Examples from studies on platelet factor-4 and the VEGF/VEGFR system. Biochem. Pharmacol. 68, 1017-1021.
12. Boehm, T., Folkman, J., Browder, T., and O'Reilly, M.S. (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature 390, 404-407.
13. Bogdanov, A., Jr., Marecos, E., Cheng, H.C., Chandrasekaran, L., Krutzsch, H.C., Roberts, D.D., and Weissleder, R. (1999) Treatment of experimental brain tumors with thrombospondin-1 derived peptides: An in vivo imaging study. Neoplasia 1, 438-445.
14. Bouck, N. (2002) PEDF: Anti-angiogenic guardian of ocular function. Trends Mol. Med. 8, 330-334.
15. Brooks, P.C. (1996) Role of integrins in angiogenesis. Eur. J. Cancer 32A, 2423-2429.
16. Brooks, P.C., Montgomery, A.M., Rosenfeld, M., Reisfeld, R.A., Hu, T., Klier, G., and Cheresh, D.A. (1994) Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 79, 1157-1164.
17. Brooks, P.C., Stromblad, S., Sanders, L.C., von Schalscha, T.L., Aimes, R.T., Stetler-Stevenson, W.G., Quigley, J.P., and Cheresh, D.A. (1996) Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85, 683-693.
18. Brooks, P.C., Silletti, S., von Schalscha, T.L., Friedlander, M., and Cheresh, D.A. (1998) Disruption of angiogenesis by PEX, a noncatalytic metalloproteinase fragment with integrin binding activity. Cell 92, 391-400.
19. Chakravarti, A., Zhai, G., Suzuki, Y., Sarkesh, S., Black, P.M., Muzikansky, A., and Loeffler, J.S. (2004) The prognostic significance of phosphatidylinositol 3-kinase pathway activation in human gliomas. J. Clin. Oncol. 22, 1926-1933.
20. Chekenya, M., Hjelstuen, M., Enger, P.O., Thorsen, F., Jacob, A.L., Probst, B., Haraldseth, O., Pilkington, G., Butt, A., Levine, J.M., and Bjerkvig, R. (2002) NG2 proteoglycan promotes angiogenesis-dependent tumor growth in CNS by sequestering angiostatin. FASEB J. 16, 586-588.
21. Chen, H., Strickland, D.K., and Mosher, D.F. (1996a) Metabolism of thrombospondin 2. Binding and degradation by 3T3 cells and glycos-aminoglycan-variant Chinese hamster ovary cells. J. Biol. Chem. 271, 15993-15999.
22. Chen, H., Sottile, J., Strickland, D.K., and Mosher, D.F. (1996b) Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteoglycans and low-density-lipoprotein receptor-related protein: Localization of the functional activity to the trimeric N-terminal heparin-binding region of thrombospondin-1. Biochem. J. 318, 959-963.
23. Choe, G., Horvath, S., Cloughesy, T.F., Crosby, K., Seligson, D., Palotie, A., Inge, L., Smith, B.L., Sawyers, C.L., and Mischel, P.S. (2003) Analysis of the phosphatidylinositol 3′-kinase signaling pathway in glioblastoma patients in vivo. Cancer Res. 63, 2742-2746.
24. Crawford, S.E., Stellmach, V., Ranalli, M., Huang, X., Huang, L., Volpert, O., De Vries, G.H., Abramson, L.P., and Bouck, N. (2001) Pigment epithelium-derived factor (PEDF) in neuroblastoma: A multifunctional mediator of Schwann cell antitumor activity. J. Cell Sci. 114, 4421-4428.
25. Dameron, K.M., Volpert, O.V., Tainsky, M.A., and Bouck, N. (1994) The p53 tumor suppressor gene inhibits angiogenesis by stimulating the production of thrombospondin. Cold Spring Harb. Symp. Quant. Biol. 59, 483-489.
26. Dawson, D.W., Pearce, S.F., Zhong, R., Silverstein, R.L., Frazier, W.A., and Bouck, N.P. (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol. 138, 707-717.
27. Dawson, D.W., Volpert, O.V., Gillis, P., Crawford, S.E., Xu, H., Benedict, W., and Bouck, N.P. (1999) Pigment epithelium-derived factor: A potent inhibitor of angiogenesis. Science 285, 245-248.
28. de Fraipont, F., Keramidas, M., El Atifi, M., Chambaz, E.M., Berger, F., and Feige, J.J. (2004) Expression of the thrombospondin 1 fragment 167-569 in C6 glioma cells stimulates tumorigenicity despite reduced neovascularization. Oncogene 23, 3642-3649.
29. Ding, Q., Stewart, J., Jr., Prince, C.W., Chang, P.L., Trikha, M., Han, X., Grammer, J.R., and Gladson, C.L. (2002) Promotion of malignant astrocytoma cell migration by osteopontin expressed in the normal brain: Differences in integrin signaling during cell adhesion to osteopontin versus vitronectin. Cancer Res. 62, 5336-5343.
30. Emonard, H., Bellon, G., Troeberg, L., Berton, A., Robinet, A., Henriet, P., Marbaix, E., Kirkegaard, K., Patthy, L., Eeckhout, Y., Nagase, H., Hornebeck, W., and Courtoy, P.J. (2004) The low density lipoprotein receptor-related protein mediates endocytic clearance of proMMP-2: TIMP-2 complex through a thrombospondin-independent mechanism. J. Biol. Chem. 279, 54944-54951.
31. Eriksson, K., Magnusson, P., Dixelius, J., Claesson-Welsh, L., and Cross, M.J. (2003) Angiostatin and endostatin inhibit endothelial cell migration in response to FGF and VEGF without interfering with specific intracellular signal transduction pathways. FEBS Lett. 536, 19-24.
32. Fears, C.Y., Sontheimer, H.W., Bullard, D.C., and Gladson, C.L. (2004) Could labeled neuronal progenitor cells be used to target glioma tumor endothelium? Cancer Biol. Ther. 3, 845-846.
33. Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., and Mothes, W. (2000) Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J. 19, 1187-1194.
34. Ferreras, M., Felbor, U., Lenhard, T., Olsen, B.R., and Delaisse, J. (2000) Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett. 486, 247-251.
35. Filleur, S., Volpert, O.V., Degeorges, A., Voland, C., Reiher, F., Clezardin, P., Bouck, N., and Cabon, F. (2001) In vivo mechanisms by which tumors producing thrombospondin 1 bypass its inhibitory effects. Genes Dev. 15, 1373-1382.
36. Geiger, J.H., and Cnudde, S.E. (2004) What the structure of angiostatin may tell us about its mechanism of action. J. Thromb. Haemost. 2, 23-34.
37. Giancotti, F.G., and Ruoslahti, E. (1999) Integrin signaling. Science 285, 1028-1032.
38. Gingras, M.C., Roussel, E., Bruner, J.M., Branch, C.D., and Moser, R.P. (1995) Comparison of cell adhesion molecule expression between glioblastoma multiforme and autologous normal brain tissue. J. Neuroimmunol. 57, 143-153.
39. Gladson, C.L. (1996) Expression of integrin alpha v beta 3 in small blood vessels of glioblastoma tumors. J. Neuropath. Exp. Neurol. 55, 1143-1149.
40. Gladson, C.L., and Cheresh, D.A. (1991) Glioblastoma expression of vitro-nectin and the alpha v beta 3 integrin. Adhesion mechanism for transformed glial cells. J. Clin. Invest. 88, 1924-1932.
41. Gladson, C.L., Wilcox, J.N., Sanders, L., Gillespie, G.Y., and Cheresh, D.A. (1995) Cerebral microenvironment influences expression of the vitronectin gene in astrocytic tumors. J. Cell Sci. 108, 945-956.
42. Godyna, S., Liau, G., Popa, I., Stefansson, S., and Argraves, W.S. (1995) Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J. Cell Biol. 129, 1403-1410.
43. Goldman, C.K., Kim, J., Wong, W.L., King, V., Brock, T., and Gillespie, G.Y. (1993) Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glioma cells: A model of glioblastoma multiforme pathophysiology. Mol. Biol. Cell 4, 121-133.
44. Good, D.J., Polverini, P.J., Rastinejad, F., Le Beau, M.M., Lemons, R.S., Frazier, W.A., and Bouck, N.P. (1990) A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc. Natl. Acad. Sci. USA 87, 6624-6628.
45. Griscelli, F., Li, H., Bennaceur-Griscelli, A., Soria, J., Opolon, P., Soria, C., Perricaudet, M., Yeh, P., and Lu, H. (1998) Angiostatin gene transfer: Inhibition of tumor growth in vivo by blockage of endothelial cell proliferation associated with a mitosis arrest. Proc. Natl. Acad. Sci. USA 95, 6367-6372.
46. Groft, L.L., Muzik, H., Rewcastle, N.B., Johnston, R.N., Knauper, V., Lafleur, M.A., Forsyth, P.A., and Edwards, D.R. (2001) Differential expression and localization of TIMP-1 and TIMP-4 in human gliomas. Br. J. Cancer 85, 55-63.
47. Guan, M., Yam, H.F., Su, B., Chan, K.P., Pang, C.P., Liu, W.W., Zhang, W.Z., and Lu, Y. (2003) Loss of pigment epithelium derived factor expression in glioma progression. J. Clin. Pathol. 56, 277-282.
48. Guan, M., Pang, C.P., Yam, H.F., Cheung, K.F., Liu, W.W., and Lu, Y. (2004) Inhibition of glioma invasion by overexpression of pigment epithelium-derived factor. Cancer Gene Ther. 11, 325-332.
49. Guo, N., Krutzsch, H.C., Inman, J.K., and Roberts, D.D. (1997) Thrombospondin 1 and type I repeat peptides of thrombospondin 1 specifically induce apoptosis of endothelial cells. Cancer Res. 57, 1735-1742.
50. Hagedorn, M., Zilberberg, L., Wilting, J., Canron, X., Carrabba, G., Giussani, C., Pluderi, M., Bello, L., and Bikfalvi, A. (2002) Domain swapping in a COOH-terminal fragment of platelet factor 4 generates potent angiogenesis inhibitors. Cancer Res. 62, 6884-6890.
51. Hahn, W., Ho, S.H., Jeong, J.G., Hahn, E.Y., Kim, S., Yu, S.S., Kim, S., and Kim, J.M. (2004) Viral vector-mediated transduction of a modified thrombospondin-2 cDNA inhibits tumor growth and angiogenesis. Gene Ther. 11, 739-745.
52. Hajitou, A., Sounni, N.E., Devy, L., Grignet-Debrus, C., Lewalle, J.M., Li, H., Deroanne, C.F., Lu, H., Colige, A., Nusgens, B.V., Frankenne, F., Maron, A., Yeh, P., Perricaudet, M., Chang, Y., Soria, C., Calberg-Bacq, C.M., Foidart, J.M., and Noel, A. (2001) Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: Effect on in vivo mammary tumor growth and angiogenesis. Cancer Res. 61, 3450-3457.
53. Hanahan, D., and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364.
54. Harada, H., Nakagawa, K., Saito, M., Kohno, S., Nagato, S., Furukawa, K., Kumon, Y., Hamada, K., and Ohnishi, T. (2003) Introduction of wild-type p53 enhances thrombospondin-1 expression in human glioma cells. Cancer Lett. 191, 109-119.
55. Haskell, H., Natarajan, M., Hecker, T.P., Ding, Q., Stewart, J., Jr., Grammer, J.R., and Gladson, C.L. (2003) Focal adhesion kinase is expressed in the angiogenic blood vessels of malignant astrocytic tumors in vivo and promotes capillary tube formation of brain microvascular endothelial cells. Clin. Cancer Res. 9, 2157-2165.
56. Hawighorst, T., Velasco, P., Streit, M., Hong, Y.K., Kyriakides, T.R., Brown, L.F., Bornstein, P., and Detmar, M. (2001) Thrombospondin-2 plays a protective role in multistep carcinogenesis: A novel host anti-tumor defense mechanism. EMBO J. 20, 2631-2640.
57. Hecker, T.P., and Gladson, C.L. (2003) Focal adhesion kinase in cancer. Front. Biosci. 8, s705-s714.
58. Hsu, S.C., Volpert, O.V., Steck, P.A., Mikkelsen, T., Polverini, P.J., Rao, S., Chou, P., and Bouck, N.P. (1996) Inhibition of angiogenesis in human glioblastomas by chromosome 10 induction of thrombospondin-1. Cancer Res. 56, 5684-5691.
59. Hynes, R.O. (1992) Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
60. Iruela-Arispe, M.L., Lombardo, M., Krutzsch, H.C., Lawler, J., and Roberts, D.D. (1999) Inhibition of angiogenesis by thrombospondin-1 is mediated by 2 independent regions within the type 1 repeats. Circulation 100, 1423-1431.
61. Jansen, M., de Witt Hamer, P.C., Witmer, A.N., Troost, D., and van Noorden, C.J. (2004) Current perspectives on antiangiogenesis strategies in the treatment of malignant gliomas. Brain Res. Brain. Res. Rev. 45, 143-163.
62. Janssen, M.L., Oyen, W.J., Dijkgraaf, I., Massuger, L.F., Frielink, C., Edwards, D.S., Rajopadhye, M., Boonstra, H., Corstens, F.H., and Boerman, O.C. (2002) Tumor targeting with radiolabeled alpha(v)beta(3) integrin binding peptides in a nude mouse model. Cancer Res. 62, 6146-6151.
63. Jiang, Y., Goldberg, I.D., and Shi, Y.E. (2002) Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 21, 2245-2252.
64. Jimenez, B., Volpert, O.V., Crawford, S.E., Febbraio, M., Silverstein, R.L., and Bouck, N. (2000) Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat. Med. 6, 41-48.
65. Jimenez, B., Volpert, O.V., Reiher, F., Chang, L., Munoz, A., Karin, M., and Bouck, N. (2001) c-Jun N-terminal kinase activation is required for the inhibition of neovascularization by thrombospondin-1. Oncogene 20, 3443-3448.
66. Joe, Y.A., Hong, Y.K., Chung, D.S., Yang, Y.J., Kang, J.K., Lee, Y.S., Chang, S.I., You, W.K., Lee, H., and Chung, S.I. (1999) Inhibition of human malignant glioma growth in vivo by human recombinant plasminogen kringles 1-3. Int. J. Cancer 82, 694-699.
67. Joki, T., Machluf, M., Atala, A., Zhu, J., Seyfried, N.T., Dunn, I. F., Abe, T., Carroll, R.S., and Black, P.M. (2001) Continuous release of endostatin from microencapsulated engineered cells for tumor therapy. Nat. Biotechnol. 19, 35-39.
68. Kanamori, M., Vanden Berg, S.R., Bergers, G., Berger, M.S., and Pieper, R.O. (2004) Integrin beta3 overexpression suppresses tumor growth in a human model of gliomagenesis: Implications for the role of beta3 overexpression in glioblastoma multiforme. Cancer Res. 64, 2751-2758.
69. Karumanchi, S.A., Jha, V., Ramchandran, R., Karihaloo, A., Tsiokas, L., Chan, B., Dhanabal, M., Hanai, J.I., Venkataraman, G., Shriver, Z., Keiser, N., Kalluri, R., Zeng, H., Mukhopadhyay, D., Chen, R.L., Lander, A.D., Hagihara, K., Yamaguchi, Y., Sasisekharan, R., Cantley, L., and Sukhatme, V.P. (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol. Cell. 7, 811-822.
70. Kaur, B., Brat, D.J., Calkins, C.C., and Van Meir, E.G. (2003) Brain angiogenesis inhibitor 1 is differentially expressed in normal brain and glioblastoma independently of p53 expression. Am. J. Pathol. 162, 19-27.
71. Kawahara, N., Ono, M., Taguchi, K., Okamoto, M., Shimada, M., Takenaka, K., Hayashi, K., Mosher, D.F., Sugimachi, K., Tsuneyoshi, M., and Kuwano, M. (1998) Enhanced expression of thrombospondin-1 and hypovascularity in human cholangiocarcinoma. Hepatology 28, 1512-1517.
72. Kawataki, T., Naganuma, H., Sasaki, A., Yoshikawa, H., Tasaka, K., and Nukui, H. (2000) Correlation of thrombospondin-1 and transforming growth factor-beta expression with malignancy of glioma. Neuropathology 20, 161-169.
73. Kazuno, M., Tokunaga, T., Oshika, Y., Tanaka, Y., Tsugane, R., Kijima, H., Yamazaki, H., Ueyama, Y., and Nakamura, M. (1999) Thrombospondin-2 (TSP2) expression is inversely correlated with vascularity in glioma. Eur. J. Cancer 35, 502-506.
74. Kim, S., Bell, K., Mousa, S.A., and Varner, J.A. (2000a) Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am. J. Pathol. 156, 1345-1362.
75. Kim, Y.M., Jang, JW., Lee, O.H., Yeon, J., Choi, E.Y., Kim, K.W., Lee, S.T., and Kwon, Y.G. (2000b) Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase 2. Cancer Res. 60, 5410-5413.
76. Kim, Y.M., Hwang, S., Kim, Y.M., Pyun, B.J., Kim, T.Y., Lee, S.T., Gho, Y.S., and Kwon, Y.G. (2002) Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 277, 27872-27879.
77. Kragh, M., Quistorff, B., Tenan, M., Van Meir, E.G., and Kristjansen, P.E. (2002) Overexpression of thrombospondin-1 reduces growth and vascular index but not perfusion in glioblastoma. Cancer Res. 62, 1191-1195.
78. Lampert, K., Machein, U., Machein, M.R., Conca, W., Peter, H.H., and Volk, B. (1998) Expression of matrix metalloproteinases and their tissue inhibitors in human brain tumors. Am. J. Pathol. 153, 429-437.
79. Levchenko, T., Bratt, A., Arbiser, J.L., and Holmgren, L. (2004) Angiomotin expression promotes hemangioendothelioma invasion. Oncogene 23, 1469-1473.
80. Liekens, S., De Clercq, E., and Neyts, J. (2001) Angiogenesis: Regulators and clinical applications. Biochem. Pharmacol. 61, 253-270.
81. Lu, W., Zhou, X., Hong, B., Liu, J., and Yue, Z. (2004) Suppression of invasion in human U87 glioma cells by adenovirus-mediated co-transfer of TIMP-2 and PTEN gene. Cancer Lett. 214, 205-213.
82. Ma, H.I., Lin, S.Z., Chiang, Y.H., Li, J., Chen, S.L., Tsao, Y.P., and Xiao, X. (2002) Intratumoral gene therapy of malignant brain tumor in a rat model with angiostatin delivered by adeno-associated viral (AAV) vector. Gene Ther. 9, 2-11.
83. MacDonald, N.J., Shivers, W.Y., Narum, D.L., Plum, S.M., Wingard, J.N., Fuhrmann, S.R., Liang, H., Holland-Linn, J., Chen, D.H., and Sim, B.K. (2001) Endostatin binds tropomyosin. A potential modulator of the antitumor activity of endostatin. J. Biol. Chem. 276, 25190-25196.
84. Matsuzawa, K., Fukuyama, K., Hubbard, S.L., Dirks, P.B., and Rutka, J.T. (1996) Transfection of an invasive human astrocytoma cell line with a TIMP-1 cDNA: Modulation of astrocytoma invasive potential. J. Neuropathol. Exp. Neurol. 55, 88-96.
85. Meyer, C., Notari, L., and Becerra, S.P. (2002) Mapping the type I collagen-binding site on pigment epithelium-derived factor. Implications for its antiangiogenic activity. J. Biol. Chem. 277, 45400-45407.
86. Mikhailenko, I., Kounnas, M.Z., and Strickland, D.K. (1995) Low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor mediates the cellular internalization and degradation of thrombospondin. A process facilitated by cell-surface proteoglycans. J. Biol. Chem. 270, 9543-9549.
87. Morimoto, T., Aoyagi, M., Tamaki, M., Yoshino, Y., Hori, H., Duan, L., Yano, T., Shibata, M., Ohno, K., Hirakawa, K., and Yamaguchi, N. (2002) Increased levels of tissue endostatin in human malignant gliomas. Clin. Cancer Res. 8, 2933-2938.
88. Moser, T.L., Stack, M.S., Asplin, I., Enghild, J.J., Hojrup, P., Everitt, L., Hubchak, S., Schnaper, H.W., and Pizzo, S.V. (1999) Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc. Natl. Acad. Sci. USA 96, 2811-2816.
89. 0 ATP synthase is active in ATP synthesis and is inhibited by angiostatin. Proc. Natl. Acad. Sci. USA 98, 6656-6661.
90. Murphy, A.N., Unsworth, E.J., and Stetler-Stevenson, W.G. (1993) Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation. J. Cell Physiol. 157, 351-358.
91. Nakagawa, T., Kubota, T., Kabuto, M., Sato, K., Kawano, H., Hayakawa, T., and Okada, Y. (1994) Production of matrix metalloproteinases and tissue inhibitor of metalloproteinases-1 by human brain tumors. J. Neurosurg. 81, 69-77.
92. Nishimori, H., Shiratsuchi, T., Urano, T., Kimura, Y., Kiyono, K., Tatsumi, K., Yoshida, S., Ono, M., Kuwano, M., Nakamura, Y., and Tokino, T. (1997) A novel brain-specific p53-target gene, BAI1, containing thrombospondin type 1 repeats inhibits experimental angiogenesis. Oncogene 15, 2145-2150.
93. Noh, Y.H., Matsuda, K., Hong, Y.K., Kunstfeld, R., Riccardi, L., Koch, M., Oura, H., Dadras, S.S., Streit, M., and Detmar, M. (2003) An N-terminal 80 kDa recombinant fragment of human thrombospondin-2 inhibits vascular endothelial growth factor induced endothelial cell migration in vitro and tumor growth and angiogenesis in vivo. J. Invest. Dermatol. 121, 1536-1543.
94. Nor, J.E., Mitra, R.S., Sutorik, M.M., Mooney, D.J., Castle, V.P., and Polverini, P.J. (2000) Thrombospondin-1 induces endothelial cell apoptosis and inhibits angiogenesis by activating the caspase death pathway. J. Vasc. Res. 37, 209-218.
95. O'Reilly, M.S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R.A., Moses, M., Lane, W.S., Cao, Y., Sage, E.H., and Folkman, J. (1994) Angiostatin: A novel angiogenesis inhibitor that mediates the suppression of metastases by Lewis lung carcinoma. Cell 79, 315-328.
96. O'Reilly, M.S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W.S., Flynn, E., Birkhead, J.R., Olsen, B.R., and Folkman, J. (1997) Endostatin: An endogenous inhibitor of angiogenesis and tumor growth. Cell 88, 277-285.
97. Parthymou, A., Kardamakis, D., Pavlopoulos, I., and Papadimitriou, E. (2004) Irradiated C6 glioma cells induce angiogenesis in vivo and activate endothelial cells in vitro. Int. J. Cancer 110, 807-814.
98. Paulus, W., Baur, I., Schuppan, D., and Roggendorf, W. (1993) Characterization of integrin receptors in normal and neoplastic human brain. Am. J. Pathol. 143, 154-163.
99. Peroulis, I., Jonas, N., and Saleh, M. (2002) Antiangiogenic activity of endostatin inhibits C6 glioma growth. Int. J. Cancer 97, 839-845.
100. Pijuan-Thompson, V., Grammer, J.R., Stewart, J., Silverstein, R.L., Pearce, S.F., Tuszynski, G.P., Murphy-Ullrich, J.E., and Gladson, C.L. (1999) Retinoic acid alters the mechanism of attachment of malignant astrocytoma and neuroblastoma cells to thrombospondin-1. Exp. Cell Res. 249, 86-101.
101. Qiao, D., Meyer, K., Mundhenke, C., Drew, S.A., and Friedl, A. (2003) Heparan sulfate proteoglycans as regulators of fibroblast growth factor-2 signaling in brain endothelial cells. Specific role for glypican-1 in glioma angiogenesis. J. Biol. Chem. 278, 16045-16053.
102. Rastinejad, F., Polverini, P.J., and Bouck, N.P. (1989) Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene. Cell 56, 345-355.
103. Read, T.A., Sorensen, D.R., Mahesparan, R., Enger, P.O., Timpl, R., Olsen, B.R., Hjelstuen, M.H., Haraldseth, O., and Bjerkvig, R. (2001) Local endostatin treatment of gliomas administered by microencapsulated producer cells. Nat. Biotechnol. 19, 29-34.
104. Rege, T.A., Stewart, J., Jr., Henkin, J., Silverstein, R.L., and Gladson, C.L. (2004) TSP-1 and type 1 repeat domain peptides induce apoptosis of human brain microvascular endothelial cells. Abstract 217. Presented at Second National Meeting of the American Society for Matrix Biology, November 10-13, 2004, San Diego, Calif.
105. Reiher, F.K., Volpert, O.V., Jimenez, B., Crawford, S.E., Dinney, C.P., Henkin, J., Haviv, F., Bouck, N.P., and Campbell, S.C. (2002) Inhibition of tumor growth by systemic treatment with thrombospondin-1 peptide mimetics. Int. J. Cancer 98, 682-689.
106. Reinmuth, N., Liu, W., Ahmad, S.A., Fan, F., Stoeltzing, O., Parikh, A.A., Bucana, C.D., Gallick, G.E., Nickols, M.A., Westlin, W.F., and Ellis, L.M. (2003) Alphavbeta3 integrin antagonist S247 decreases colon cancer metastasis and angiogenesis and improves survival in mice. Cancer Res. 63, 2079-2087.
107. Rodriguez-Manzaneque, J.C., Lane, T.F., Ortega, M.A., Hynes, R.O., Lawler, J., and Iruela-Arispe, M.L. (2001) Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc. Natl. Acad. Sci. USA 98, 12485-12490.
108. Rofstad, E.K., Henriksen, K., Galappathi, K., and Mathiesen, B. (2003) Antiangiogenic treatment with thrombospondin-1 enhances primary tumor radiation response and prevents growth of dormant pulmonary micrometastases after curative radiation therapy in human melanoma xenografts. Cancer Res. 63, 4055-4061.
109. Sasaki, T., Larsson, H., Kreuger, J., Salmivirta, M., Claesson-Welsh, L., Lindahl, U., Hohenester, E., and Timpl, R. (1999) Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J. 18, 6240-6248.
110. Schmidt, N.O., Ziu, M., Carrabba, G., Giussani, C., Bello, L., Sun, Y., Schmidt, K., Albert, M., Black, P.M., and Carroll, R.S. (2004) Antiangiogenic therapy by local intracerebral microinfusion improves treatment efficiency and survival in an orthotopic human glioblastoma model. Clin. Cancer Res. 10, 1255-1262.
111. Schrappe, M., Klier, F.G., Spiro, R.C., Waltz, T.A., Reisfeld, R.A., and Gladson, C.L. (1991) Correlation of chondroitin sulfate proteoglycan expression on proliferating brain capillary endothelial cells with the malignant phenotype of astroglial cells. Cancer Res. 51, 4986-4993.
112. Sorensen, D.R., Read, T.A., Porwol, T., Olsen, B.R., Timpl, R., Sasaki, T., Iversen, P.O., Benestad, H.B., Sim, B.K., and Bjerkvig, R. (2002) Endostatin reduces vascularization, blood flow, and growth in a rat gliosarcoma. Neuro-Oncol. 4, 1-8.
113. Steinfeld, R., Van den Berghe, H., and David, G. (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133, 405-416.
114. Stellmach, V., Crawford, S.E., Zhou, W., and Bouck, N. (2001) Prevention of ischemia-induced retinopathy by the natural ocular antiangiogenic agent pigment epithelium-derived factor. Proc. Natl. Acad. Sci. USA 98, 2593-2597.
115. Streit, M., Riccardi, L., Velasco, P., Brown, L.F., Hawighorst, T., Bornstein, P., and Detmar, M. (1999) Thrombospondin-2: A potent endogenous inhibitor of tumor growth and angiogenesis. Proc. Natl. Acad. Sci. USA 96, 14888-14893.
116. Strik, H.M., Schluesener, H.J., Seid, K., Meyermann, R., and Deininger, M.H. (2001) Localization of endostatin in rat and human gliomas. Cancer 91, 1013-1019.
117. Sudhakar, A., Sugimoto, H., Yang, C., Lively, J., Zeisberg, M., and Kalluri, R. (2003) Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proc. Natl. Acad. Sci. USA 100, 4766-4771.
118. Tanaka, T., Manome, Y., Wen, P., Kufe, D.W., and Fine, H.A. (1997) Viral vector-mediated transduction of a modified platelet factor 4 cDNA inhibits angiogenesis and tumor growth. Nat. Med. 3, 437-442.
119. Tarui, T., Miles, L.A., and Takada, Y. (2001) Specific interaction of angiostatin with integrin alpha(v)beta(3) in endothelial cells. J. Biol. Chem. 276, 39562-39568.
120. Tenan, M., Fulci, G., Albertoni, M., Diserens, A.C., Hamou, M.F., El Atifi-Borel, M., Feige, J.J., Pepper, M.S., and Van Meir, E.G. (2000) Thrombospondin-1 is downregulated by anoxia and suppresses tumorigenicity of human glioblastoma cells. J. Exp. Med. 191, 1789-1798.
121. Tolsma, S.S., Volpert, O.V., Good, D.J., Frazier, W.A., Polverini, P.J., and Bouck, N. (1993) Peptides derived from two separate domains of the matrix protein thrombospondin-1 have anti-angiogenic activity. J. Cell Biol. 122, 497-511.
122. Tombran-Tink, J., Mazuruk, K., Rodriguez, I.R., Chung, D., Linker, T., Englander, E., and Chader, G.J. (1996) Organization, evolutionary conservation, expression and unusual Alu density of the human gene for pigment epithelium-derived factor, a unique neurotrophic serpin. Mol. Vis. 2, 11.
123. Tomii, Y., Kamochi, J., Yamazaki, H., Sawa, N., Tokunaga, T., Ohnishi, Y., Kijima, H., Ueyama, Y., Tamaoki, N., and Nakamura, M. (2002) Human thrombospondin 2 inhibits proliferation of microvascular endothelial cells. Int. J. Oncol. 20, 339-342.
124. Troyanovsky, B., Levchenko, T., Månsson, G., Matvijenko, O., and Holmgren, L. (2001) Angiomotin: An angiostatin binding protein that regulates endothelial cell migration and tube formation. J. Cell Biol. 152, 1247-1254.
125. Volpert, O.V., Tolsma, S.S., Pellerin, S., Feige, J.J., Chen, H., Mosher, D.F., and Bouck, N. (1995) Inhibition of angiogenesis by thrombospondin-2. Biochem. Biophys. Res. Commun. 217, 326-332.
126. Volpert, O.V., Zaichuk, T., Zhou, W., Reiher, F., Ferguson, T.A., Stuart, P.M., Amin, M., and Bouck, N.P. (2002a) Inducer-stimulated Fas targets activated endothelium for destruction by anti-angiogenic thrombospondin-1 and pigment epithelium-derived factor. Nat. Med. 8, 349-357.
127. Volpert, O.V., Pili, R., Sikder, H.A., Nelius, T., Zaichuk, T., Morris, C., Shiflett, C.B., Devlin, M.K., Conant, K., and Alani, R.M. (2002b) Id1 regulates angiogenesis through transcriptional repression of thrombospondin-1. Cancer Cell 2, 473-483.
128. Wang, H., Wang, H., Zhang, W., Huang, H.J., Liao, W.S., and Fuller, G.N. (2004a) Analysis of the activation status of Akt, NFkappaB, and Stat3 in human diffuse gliomas. Lab. Invest. 84, 941-951.
129. Wang, S., Herndon, M.E., Ranganathan, S., Godyna, S., Lawler, J., Argraves, W.S., and Liau, G. (2004b) Internalization but not binding of thrombospondin-1 to low density lipoprotein receptor-related protein-1 requires heparan sulfate proteoglycans. J. Cell. Biochem. 91, 766-776.
130. Watnick, R.S., Cheng, Y.N., Rangarajan, A., Ince, T.A., and Weinberg, R.A. (2003) Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 3, 219-231.
131. Wen, W., Moses, M.A., Wiederschain, D., Arbiser, J.L., and Folkman, J. (1999) The generation of endostatin is mediated by elastase. Cancer Res. 59, 6052-6056.
132. Yang, Z., Strickland, D.K., and Bornstein, P. (2001) Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2. J. Biol. Chem. 276, 8403-8408.
133. Yasui, N., Mori, T., Morito, D., Matsushita, O., Kourai, H., Nagata, K., and Koide, T. (2003) Dual-site recognition of different extracellular matrix components by anti-angiogenic/neurotrophic serpin, PEDF. Biochemistry 42, 3160-3167.
134. Zaichuk, T.A., Shroff, E.H., Emmanuel, R., Filleur, S., Nelius, T., and Volpert, O.V. (2004) Nuclear factor of activated T cells balances angiogenesis activation and inhibition. J. Exp. Med. 199, 1513-1522.
135. Zhang, X., Wu, J., Fei, Z., Gao, D., Li, X., Liu, X., Liang, J., and Wang, X. (2000) Angiostatin K(1-3) gene for treatment of human gliomas: An experimental study. Clin. Med. J. 113, 996-1001.