|
|
||||
|
|
||||
|
||||
Tumor Biology |
Departments of Pathology, Division of Neuropathology, and Cell Biology (T.A.R., C.Y.F., C.L.G.), and the Medical Scientist Training Program (T.A.R.), University of Alabama at Birmingham, Birmingham, AL 35294 USA
2 Address correspondence to Candece L. Gladson, The University of Alabama at Birmingham, LHRB 567, 701 South 19th Street, Birmingham, AL 35294, USA (gladson{at}uab.edu).
Abstract
Angiogenesis is necessary for tumor growth beyond a volume of approximately 2 mm3. This observation, along with the accessibility of tumor vessels to therapeutic targeting, has resulted in a research focus on inhibitors of angiogenesis. A number of endogenous inhibitors of angiogenesis are found in the body. Some of these are synthesized by specific cells in different organs, and others are created by extracellular proteolytic cleavage of plasma-derived or extracellular matrix-localized proteins. In this review, we focus on angiostatin, endostatin, PEX, pigment epithelial-derived factor, and thrombospondin (TSP)-1 and -2, either because these molecules are expressed in malignant glioma biopsies or because animal studies in malignant glioma models have suggested that their therapeutic administration could be efficacious. We review the known mechanisms of action, potential receptors, expression in glioma biopsy samples, and studies testing their potential therapeutic efficacy in animal models of malignant glioma. Two conclusions can be made regarding the mechanisms of action of these inhibitors: (1) Several of these inhibitors appear to mediate their antiangiogenic effect through multiple protein-protein interactions that inhibit the function of proangiogenic molecules rather than through a specific receptor-mediated signaling event, and (2) TSP-1 and TSP-2 appear to mediate their antiangiogenic effect, at least in part, through a specific receptor, CD36, which initiates the antiangiogenic signal. Although not proven in gliomas, evidence suggests that expression of specific endogenous inhibitors of angiogenesis in certain organs may be part of a host antitumor response. The studies reviewed here suggest that new antiangiogenic therapies for malignant gliomas offer exciting promise as nontoxic, growth-inhibitory agents.
References
Abdollahi, A., Hahnfeldt, P., Maercker, C., Grone, H.J., Debus, J., Ansorge, W., Folkman, J., Hlatky, L., and Huber, P.E. (2004) Endostatin's antian giogenic signaling network. Mol. Cell 13,649 -663.[CrossRef][ISI][Medline]
Adams, J.C., and Lawler, J. (2004) The thrombospondins. Int. J. Biochem. Cell Biol. 36,961 -968.[CrossRef][ISI][Medline]
Allport, J.R., Shinde Patil, V.R., and Weissleder, R. (2004) Murine neuro nal progenitor cells are preferentially recruited to tumor vasculature via alpha (4)-integrin and SDF-1 alpha-dependent mechanisms. Cancer Biol. Ther. 3, 838-844.[ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
Bein, K., and Simons, M. (2000) Thrombospondin type 1
repeats inter act with matrix metalloproteinase 2. Regulation of
metalloproteinase activity. J. Biol. Chem.
275,32167
-32173.
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 angiogen esis, cell proliferation, and invasion by a naturally
occurring fragment of human metalloproteinase-2. Cancer
Res. 61,8730
-8736.
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.
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) Combinato rial 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.
Bertin, N., Clezardin, P., Kubiak, R., and Frappart, L.
(1997) Thrombospon din-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.
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.[CrossRef][ISI][Medline]
Boehm, T., Folkman, J., Browder, T., and O'Reilly, M.S. (1997) Antiangio genic therapy of experimental cancer does not induce acquired drug resistance. Nature 390,404 -407.[CrossRef][Medline]
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.[CrossRef][Medline]
Bouck, N. (2002) PEDF: Anti-angiogenic guardian of ocular function. Trends Mol. Med. 8, 330-334.[CrossRef][ISI][Medline]
Brooks, P.C. (1996) Role of integrins in angiogenesis. Eur. J. Cancer 32A,2423 -2429.[CrossRef]
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.[CrossRef][ISI][Medline]
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) Local ization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell 85,683 -693.[CrossRef][ISI][Medline]
Brooks, P.C., Silletti, S., von Schalscha, T.L., Friedlander, M., and Cheresh, D.A. (1998) Disruption of angiogenesis by PEX, a noncatalytic metallo proteinase fragment with integrin binding activity. Cell 92,391 -400.[CrossRef][ISI][Medline]
Chakravarti, A., Zhai, G., Suzuki, Y., Sarkesh, S., Black, P.M.,
Muzikansky, A., and Loeffler, J.S. (2004) The prognostic
significance of phospha tidylinositol 3-kinase pathway activation in human
gliomas. J. Clin. Oncol.
22,1926
-1933.
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.
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.
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.
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.
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 epithe lium-derived factor (PEDF) in neuroblastoma: A multifunctional mediator of Schwann cell antitumor activity. J. Cell Sci. 114,4421 -4428.
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.
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.
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.
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.[CrossRef][ISI][Medline]
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 osteo pontin
versus vitronectin. Cancer Res.
62,5336
-5343.
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.
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.[CrossRef][ISI][Medline]
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.[ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
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.[CrossRef][ISI][Medline]
Giancotti, F.G., and Ruoslahti, E. (1999) Integrin
signaling. Science 285,1028
-1032.
Gingras, M.C., Roussel, E., Bruner, J.M., Branch, C.D., and Moser, R.P. (1995) Comparison of cell adhesion molecule expression between glio blastoma multiforme and autologous normal brain tissue. J. Neuroimmunol. 57,143 -153.[CrossRef][ISI][Medline]
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.[ISI][Medline]
Gladson, C.L., and Cheresh, D.A. (1991) Glioblastoma expression of vitro nectin and the alpha v beta 3 integrin. Adhesion mechanism for trans formed glial cells. J. Clin. Invest. 88,1924 -1932.
Gladson, C.L., Wilcox, J.N., Sanders, L., Gillespie, G.Y., and Cheresh, D.A. (1995) Cerebral microenvironment influences expression of the vitro nectin gene in astrocytic tumors. J. Cell Sci. 108,945 -956.
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.
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 glio blastoma multiforme pathophysiology. Mol. Biol. Cell 4,121 -133.[Abstract]
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 indistin guishable from a fragment of thrombospondin.
Proc. Natl. Acad. Sci. USA
87,6624
-6628.
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.
Groft, L.L., Muzik, H., Rewcastle, N.B., Johnston, R.N., Knauper, V., Laf leur, 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.[CrossRef][ISI][Medline]
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.
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.[CrossRef][ISI][Medline]
Guo, N., Krutzsch, H.C., Inman, J.K., and Roberts, D.D.
(1997) Thrombo spondin 1 and type I repeat peptides of
thrombospondin 1 specifically induce apoptosis of endothelial cells.
Cancer Res. 57,1735
-1742.
Hagedorn, M., Zilberberg, L., Wilting, J., Canron, X., Carrabba,
G., Gius sani, 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.
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.[CrossRef][ISI][Medline]
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 endo thelial growth factor by tissue inhibitor of
metalloproteinase-2: Effect on in vivo mammary tumor growth and angiogenesis.
Cancer Res. 61,3450
-3457.
Hanahan, D., and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86,353 -364.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
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.[CrossRef][ISI][Medline]
Hecker, T.P., and Gladson, C.L. (2003) Focal adhesion kinase in cancer. Front. Biosci. 8,s705 -s714.[ISI][Medline]
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.
Hynes, R.O. (1992) Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.[CrossRef][ISI][Medline]
Iruela-Arispe, M.L., Lombardo, M., Krutzsch, H.C., Lawler, J., and
Roberts, D.D. (1999) Inhibition of angiogenesis by
thrombospondin-1 is medi ated by 2 independent regions within the type 1
repeats. Circulation
100,1423
-1431.
Jansen, M., de Witt Hamer, P.C., Witmer, A.N., Troost, D., and van Noor den, C.J. (2004) Current perspectives on antiangiogenesis strategies in the treatment of malignant gliomas. Brain Res. Brain. Res. Rev. 45,143 -163.[CrossRef][Medline]
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.
Jiang, Y., Goldberg, I.D., and Shi, Y.E. (2002) Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 21,2245 -2252.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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. Bio technol. 19, 35-39.
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.
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 end ostatin receptors. Mol. Cell. 7,811 -822.[CrossRef][ISI][Medline]
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 glio blastoma independently of p53 expression.
Am. J. Pathol. 162,19
-27.
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.[CrossRef][ISI][Medline]
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. Neuropa thology 20,161 -169.
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.
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.
Kim, Y.M., Jang, J.W., Lee, O.H., Yeon, J., Choi, E.Y., Kim, K.W.,
Lee, S.T., and Kwon, Y.G. (2000b) Endostatin inhibits endothelial
and tumor cel lular invasion by blocking the activation and catalytic activity
of matrix metalloproteinase 2. Cancer Res.
60,5410
-5413.
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.
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.
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.
Levchenko, T., Bratt, A., Arbiser, J.L., and Holmgren, L. (2004) Angiomotin expression promotes hemangioendothelioma invasion. Oncogene 23,1469 -1473.[CrossRef][ISI][Medline]
Liekens, S., De Clercq, E., and Neyts, J. (2001) Angiogenesis: Regulators and clinical applications. Biochem. Pharmacol. 61,253 -270.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
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.[ISI][Medline]
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.
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 thrombospon din. A process facilitated by cell-surface proteoglycans.
J. Biol. Chem. 270,9543
-9549.
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.
Moser, T.L., Stack, M.S., Asplin, I., Enghild, J.J., Hojrup, P.,
Everitt, L., Hub chak, 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.
Moser, T.L., Kenan, D.J., Ashley, T.A., Roy, J.A., Goodman, M.D.,
Misra, U.K., Cheek, D.J., and Pizzo, S.V. (2001) Endothelial cell
surface F1-F0 ATP synthase is active in ATP synthesis
and is inhibited by angiostatin. Proc. Natl. Acad. Sci.
USA 98,6656
-6661.
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.[CrossRef][ISI][Medline]
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.[ISI][Medline]
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 thrombospon din type 1 repeats inhibits experimental angiogenesis. Oncogene 15,2145 -2150.[CrossRef][ISI][Medline]
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-termi nal 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.[CrossRef][ISI][Medline]
Nor, J.E., Mitra, R.S., Sutorik, M.M., Mooney, D.J., Castle, V.P., and Pol verini, P.J. (2000) Thrombospondin-1 induces endothelial cell apopto sis and inhibits angiogenesis by activating the caspase death pathway. J. Vasc. Res. 37,209 -218.[CrossRef][ISI][Medline]
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) Angio statin: A novel angiogenesis inhibitor that mediates the suppression of metastases by Lewis lung carcinoma. Cell 79,315 -328.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
Paulus, W., Baur, I., Schuppan, D., and Roggendorf, W. (1993) Character ization of integrin receptors in normal and neoplastic human brain. Am. J. Pathol. 143,154 -163.[Abstract]
Peroulis, I., Jonas, N., and Saleh, M. (2002) Antiangiogenic activity of end ostatin inhibits C6 glioma growth. Int. J. Cancer 97,839 -845.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
Qiao, D., Meyer, K., Mundhenke, C., Drew, S.A., and Friedl, A.
(2003) Hep aran 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.
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
Reiher, F.K., Volpert, O.V., Jimenez, B., Crawford, S.E., Dinney, C.P., Hen kin, 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.[CrossRef][ISI][Medline]
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.
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.
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.
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.[CrossRef][ISI][Medline]
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) Antian giogenic therapy by local intracerebral
microinfusion improves treatment efficiency and survival in an orthotopic
human glioblastoma model. Clin. Cancer Res.
10,1255
-1262.
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.
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) End ostatin reduces vascularization, blood flow, and
growth in a rat gliosar coma. Neuro-Oncol.
4, 1-8.
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.
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.
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.
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.[CrossRef][ISI][Medline]
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.
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.[CrossRef][ISI][Medline]
Tarui, T., Miles, L.A., and Takada, Y. (2001) Specific
interaction of angio statin with integrin alpha(v)beta(3) in endothelial
cells. J. Biol. Chem.
276,39562
-39568.
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) Throm bospondin-1 is downregulated by anoxia and
suppresses tumorigenicity of human glioblastoma cells. J. Exp.
Med. 191,1789
-1798.
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.
Tombran-Tink, J., Mazuruk, K., Rodriguez, I.R., Chung, D., Linker, T., Eng lander, E., and Chader, G.J. (1996) Organization, evolutionary con servation, expression and unusual Alu density of the human gene for pigment epithelium-derived factor, a unique neurotrophic serpin. Mol. Vis. 2,11 .[Medline]
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.[ISI][Medline]
Troyanovsky, B., Levchenko, T., Månsson, G., Matvijenko, O.,
and Hol mgren, L. (2001) Angiomotin: An angiostatin binding
protein that regulates endothelial cell migration and tube formation.
J. Cell Biol. 152,1247
-1254.
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
Wang, S., Herndon, M.E., Ranganathan, S., Godyna, S., Lawler, J., Argraves, W.S., and Liau, G. (2004b) Internalization but not binding of thrombo spondin-1 to low density lipoprotein receptor-related protein-1 requires heparan sulfate proteoglycans. J. Cell. Biochem. 91,766 -776.[CrossRef][ISI][Medline]
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.[CrossRef][ISI][Medline]
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.
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.
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. Biochem istry 42,3160 -3167.
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.
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. Chin. Med. J. 113,996 -1001.[Medline]
This article has been cited by other articles:
![]() |
M. N. Rudzinski, L. Chen, and M. R. Hernandez Antiangiogenic Characteristics of Astrocytes From Optic Nerve Heads With Primary Open-angle Glaucoma Arch Ophthalmol, May 1, 2008; 126(5): 679 - 685. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. Benny, S.-K. Kim, K. Gvili, I. S. Radzishevsky, A. Mor, L. Verduzco, L. G. Menon, P. M. Black, M. Machluf, and R. S. Carroll In vivo fate and therapeutic efficacy of PF-4/CTF microspheres in an orthotopic human glioblastoma model FASEB J, February 1, 2008; 22(2): 488 - 499. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. C. Brown, I. Staniszewska, P. Lazarovici, G. P. Tuszynski, L. Del Valle, and C. Marcinkiewicz Regulatory effect of nerve growth factor in {alpha}9{beta}1 integrin-dependent progression of glioblastoma Neuro-oncol, January 1, 2008; 10(6): 968 - 980. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. A. N. Mustafa, P. C. Burgers, L. J. Dekker, H. Charif, M. K. Titulaer, P. A. E. S. Smitt, T. M. Luider, and J. M. Kros Identification of Glioma Neovascularization-related Proteins by Using MALDI-FTMS and Nano-LC Fractionation to Microdissected Tumor Vessels Mol. Cell. Proteomics, July 1, 2007; 6(7): 1147 - 1157. [Abstract] [Full Text] [PDF] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
|