Mechanisms of glioma invasion: Role of matrix-metalloproteinases

Canadian Journal of Neurological Sciences

Volumn 24, Issue 1, 1997, Pages 3-15

  Uhm, J H ^a   Dooley, N P ^a   Villemure, J G ^a   Yong, V W ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX METALLOPROTEINASE; PROTEINASE C; UNCLASSIFIED DRUG;

CANCER INVASION; GLIOMA; HUMAN; MOLECULAR BIOLOGY; PRIORITY JOURNAL; REVIEW;

EID: 0031049327     PISSN: 03171671     EISSN: None     Source Type: Journal    
DOI: 10.1017/S0317167100021028     Document Type: Review

References (143)

1. Dedhar S. Integrins and tumor invasion. BioEssays 1990; 12: 583-590.
2. Ruoslahti E. Control of cell motility and tumour invasion by extracellular matrix interactions. Br J Cancer 1992; 66: 239-242.
3. Furcht LT, Skubitz AP, Fields GB. Tumor cell invasion, matrix metalloproteinases, and the dogma [editorial; comment]. Lab Invest 1994; 70: 781-783.
4. Stetler-Stevenson WG, Liotta LA, Kleiner DE, Jr. Extracellular matrix 6: role of matrix metalloproteinases in tumor invasion and metastasis. FASEB J 1993; 7: 1434-1441.
5. Mignatti P, Rifkin DB. Biology and biochemistry of proteinases in tumor invasion. Physiol Rev 1993; 73: 161-195.
6. MacDougall JR, Matrisian LM. Contributions of tumor and stromal matrix metalloproteases to tumor progression, invasion and metastasis. Cancer and Metast Rev 1995; 14: 351-362.
7. DeClerck YA, Yean TD, Chan D, Shimada H, Langley, KE. Inhibition of tumor invasion of smooth muscle cell layers by recombinant human metalloproteinase inhibitor. Cancer Res 1991; 51: 2151-2157.
8. Vaithilingam IS, McDonald W, Brown NK, et al. Serum proteolytic activity during the growth of C6 astrocytoma. J Neurosurg 1992; 77: 595-600.
9. Nakagawa T, Kubota T, Kabuto M, et al. Production of matrix metalloproteinases and tissue inhibitor of metalloproteinases-1 by human brain tumors. J Neurosurg 1994: 81: 69-77.
10. Del Maestro RF, Lopez-Torres M, McDonald WB, et al. The effect of tumor necrosis factor-α on human malignant glial cells. J Neurosurg 1992; 76: 652-659.
11. Yamamoto M, Sawaya R, Mohanam S, et al. Expression and cellular localization of messenger RNA for plasminogen activator inhibitor type 1 in human astrocytomas in vivo. Cancer Res 1994; 54: 3329-3332.
12. Rao JS, Steck PA, Mohanam S, Stetler-Stevenson WG, Liotta LA. Elevated levels of Mr 92,000 Type IV collagenase in human brain tumors. Cancer Res 1993; 53: 2208-2211.
13. Rao JS, Steck PA, Tofilon P, et al. Role of plasminogen activator and of 92-KDa type IV collagenase in glioblastoma invasion using an in vitro matrigel model. J Neurooncol 1994; 18: 129-138.
14. Couldwell WT, de Tribolet N, Antel JP, Gauthier T, Kuppner MC. Adhesion molecules and malignant gliomas: implications for tumorigenesis. J Neurosurg 1992; 76: 782-791.
15. Berens ME, Rutka JT, Rosenblum ML. Brain tumor epidemiology, growth, and invasion. Neurosurg Clin North Am 1990; 1: 1-18.
16. Barker FG II, Israel MA. The molecular biology of brain tumors. Neurol Clin 1995; 13: 701-722.
17. Wang X, Fu X, Brown PD, Crimmin MJ, Hoffman RM. Matrix metalloproteinase inhibitor BB-94 (Batimastat) inhibits human colon tumor growth and spread in a patient-like orthotopic model in nude mice. Cancer Res 1994; 54: 4726-4728.
18. Chirivi RGS, Garofalo A, Crimmin MJ, et al. Inhibition of the metastatic spread and growth of B16-B16 murine melanoma by a synthetic matrix metalloproteinase inhibitor. Int J Cancer 1994; 58: 460-464.
19. Taraboletti G, Garofalo A, Belotti D, et al. Inhibition of angiogenesis and murine hemangioma growth by Batimastat, a synthetic inhibitor of matrix metalloproteinases. J Natl Cancer Inst 1995; 87: 293-298.
20. Sledge GWJ, Qulali M, Goulet R, Bone, EA, Fife R. Effect of matrix metalloproteinase inhibitor Batismatat on breast cancer regrowth and metastasis in athymic mice. J. Natl Cancer Inst 1995; 87: 1546-1550.
21. Watson SA, Morris TM, Robinson G, et al. Inhibition of organ invasion by the matrix metalloproteinase inhibitor Batismatat (BB-94) in two human colon carcinoma metastasis models. Cancer Res 1995; 55: 3629-3633.
22. Davies B, Brown PD, East N, Crimmin MJ, Balkwill FK. A synthetic metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts. Cancer Res 1994; 54: 2087-2091.
23. Brown PD. Matrix metalloproteinase inhibitors: a novel class of anticancer agents. Adv Enz Regul 1995; 35: 293-301.
24. Moscatelli D, Rifkin DB. Membrane and matrix localization of proteinases: a common theme in tumor cell invasion and angiogenesis. Biochim Biophys Acta 1988; 948: 67-85.
25. Vassalli J-D, Pepper MS. Membrane proteases in focus. Nature 1994; 370: 14-15.
26. Yamamoto M, Sawaya R, Mohanam S, et al. Expression and localization of urokinase-type plasminogen activator in human astrocytomas in vivo. Cancer Res 1994; 54: 3656-3661.
27. Mohanam S, Sawaya R, McCutcheon I, et al. Modulation of in vitro invasion of human glioblastoma cells by urokinase-type plasminogen activator receptor antibody. Cancer Res 1993; 53: 4143-4147.
28. Mikkelsen T, Yan P-S, Ho K-L, et al. Immunolocalization of cathepsin B in human glioma: implications for tumor invasion and angiogenesis. J Neurosurg 1995; 83: 285-290.
29. Rempel SA, Rosenblum ML, Mikkelsen T, et al. Cathepsin B expression and localization in glioma progression and invasion. Cancer Res 1994; 54: 6027-6031.
30. Matrisian LM The matrix-degrading metalloproteinases. BioEssays 1992; 14: 455-463.
31. Jeffrey JJ. Collagen degradation. In: Diegelmann RF, Lindblad WJ, eds. Wound Healing: Biochemical and Clinical Aspects. Philadelphia: WB Saunders Company, 1992: 177-194.
32. Delasse J-M, Vaes G. Mechanism of mineral solubilization and matrix degradation in osteoclastic bone resorption. In: Rifkin BR, Gay CV, eds. Biology and Physiology of the Osteoclast, Boca Raton. FL: CRC Press 1992: 290-314.
33. Liotta LA, Tryggvason K, Garbisa S, et al. Metastatic potential correlates with enzymatic degradation of basement membrane collagen Nature 1980; 284: 67-68.
34. Sato H, Takino T, Okada Y, et al. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature 1994; 370: 61-65.
35. Basset P, Wolf C, Chambon P. Expression of the stromelysin-3 gene in fibroblastic cells of invasive carcinomas of the breast and other human tissues: a review. Breast Cancer Res Treat 1993; 24: 185-193.
36. Heino J. Biology of tumor cell invasion: interplay of cell adhesion and matrix degradation. Int J Cancer 1996; 65: 717-722.
37. Abe T, Mori T, Kohno K, et al. Expression of 72 kDa type IV collagenase and invasion activity of human glioma cells. Clin Exp Metastasis 1994; 12: 296-304.
38. Apodaca G, Rutka JT, Bouhana K, et al. Expression of metalloproteinases and metalloproteinase inhibitors by fetal astrocytes and glioma cells. Cancer Res 1990; 50: 2322-2329.
39. Uhm JH, Dooley NP, Villemure J-G, Yong, VW. Glioma invasion in vitro: regulation by matrix metalloprotease-2 and protein kinase C. Clin Exp Metast 1996 14: 421-433.
40. Yamamoto M, Mohanam S, Sawaya R, et al. Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res 1996; 56: 384-392.
41. Rutka JT, Matsuzawa K, Hubbard SL, et al. Expression of TIMP-1, TIMP-2, 72- and 92-kDa type IV collagenase transcripts in human astrocytoma cell lines; correlation with astrocytoma cell invasiveness. Int J Oncology 1995; 6: 877-884.
42. Sawaya RE, Yamamoto M, Gokaslan ZL, et al. Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin Exp Metastasis 1996; 14: 35-42.
43. Takino T, Sato H, Shinagawa A, Seiki M. Identification of the second membrane-type matrix metalloproteinase (MT-MMP-2) gene from a human placenta eDNA library. J Biol Chem 1995; 270: 23013-23020.
44. Yu M, Sato H, Seiki M. Thompson EW. Complex regulation of membrane-type matrix metalloproteinase expression and matrix metalloproteinase-2 activation by Concanavalin A in MDA-MB-231 human breast cancer cells. Cancer Res 1995; 55: 3272-3277.
45. Lewalle JM, Munaut C, Pichot B, et al. Plasma membrane-dependent activation of gelatinase A in human vascular endothelial cells. J Cell Physiol 1995; 165: 478-483.
46. Strongin AY, Collier I, Bannikov G, et al. Mechanism of cell surface activation of 72 kDa type IV collagenase: isolation of the activated form of the membrane metalloprotease. J Biol Chem 1995; 270: 5331-5338.
47. Matrisian LM. Matrix metalloproteinase gene expression. Ann NY Acad Sci 1994; 732: 42-50.
48. Hu E, Mueller E, Oliviero S, et al. Targeted disruption of the c-fos gene demonstrates c-fos-dependent and -independent pathways for gene expression stimulated by growth factors or oncogenes. EMBO J 1994; 13: 3094-3103.
49. Wasylyk C, Flores P, Gutman A, Wasylyk B. PEA3 is a nuclear target for transcription activation by non-nuclear oncogenes. EMBO J 1989; 8: 3371-3378.
50. von Deimling A, Louis DN, Wiestler OD. Molecular pathways in the formation of gliomas. Glia 1995; 15: 328-338.
51. Collins VP. Gene amplification in human gliomas. Glia 1995; 15: 289-296.
52. Cavenee WK, White RL. The genetic basis of cancer. Sci Am 1995; 272: 72-79.
53. Dalrymple SJ, Jenkins RB. Molecular genetics of astrocytomas and meningiomas. Curr Opin Neurol 1994; 7: 477-483.
54. Lund-Johansen M, Bjerkvig R, Humphrey P, et al. Effect of epidermal growth factor on glioma cell growth, migration, and invasion in vitro. Cancer Res 1990; 50: 6039-6044.
55. Lund-Johansen M, Forsberg K, Bjerkvig R, Laerum OD. Effects of growth factors on a human cell line during invasion into rat brain aggregates in culture. Acta Neuropathol 1992; 84: 190-197.
56. Engerbraaten O, Bjerkvig R, Pedersen P-H, Laerum OD. Effects of EGF, bFGF, NGF and PDGF(bb) on cell proliferative, migratory, and invasive capacities of human brain-tumour biopsies in vitro. Int J Cancer 1993 53: 209-214.
57. Pedersen PH, Ness GO, Engebraaten O, et al. Heterogenous response to the growth factors [EGF, PDGF(bb), TGF-alpha, bFGF, IL-2] on glioma spheroid growth, migration and invasion. Int J Cancer 1994; 56: 255-261.
58. Takahashi JA, Fukumoto M, Igarshi K, et al. Correlation of basic fibroblast growth factor expression levels with the degree of malignancy and vascularity in human gliomas. J Neurosurg 1992; 76: 792-798.
59. Takahashi JA, Mori H, Fukumoto M, et al. Gene expression of fibroblast growth factors in human gliomas and meningiomas: demonstration of cellular source of basic fibroblast growth factor mRNA and peptide in tumor tissues. Proc Natl Acad Sci USA 1990; 87: 5710-5714.
60. Zagzag D, Miller DC, Sato Y, Rifkin DB, Burstein DE. Immunohistochemical localization of basic fibroblast growth factor in astrocytomas. Cancer Res 1990; 50: 7393-7398.
61. Morrison RS, Yamaguchi F, Saya H, et al. Basic fibroblast growth factor and fibroblast growth factor receptor I are implicated in the growth of human astrocytomas. J Neurooncol 1994; 18: 207-216.
62. Ueba T, Takahashi JA, Fukumoto M, et al. Expression of fibroblast growth factor receptor-1 in human glioma and meningioma tissues. Neurosurgery 1994; 34: 221-225.
63. Chicoine MR, Madsen CL, Silbergeld DL. Modification of human locomotion in vitro by cytokines EGF, bFGF, PDGFbb, NGF, and TNF alpha. Neurosurgery 1995; 36: 1165-1170.
64. Gately S, Tsanaclis AM, Takano S, Klagsbrun M, Brem S. Cells transfected with the basic fibroblast growth factor gene fused to a signal sequence are invasive in vitro and in situ in the brain. Neurosurgery 1995; 36: 780-788.
65. Nerlov C, Rorth P, Blasi F, Johansen M. Essential AP-1 and PEA3 binding elements in the human urokinase enhancer display cell type-specific activity. Oncogene 1991; 6: 1583-1592.
66. Flaumenhaft R, Moscatelli D, Saksela O, Rifkin DB. Role of extracellular matrix in the action of basic fibroblast growth factor: matrix as a source of growth factor for long-term stimulation of plasminogen activator production and DNA synthesis. J Cell Physiol 1989; 140: 75-81.
67. Landau BJ, Kwaan HC, Verrusio EN, Brem SS. Elevated levels of urokinase-type plasminogen activator and plasminogen activator inhibitor type-1 in malignant human brain tumors. Cancer Res 1994; 54: 1105-1108.
68. Rucklidge GJ, Edvardsen K, Bock E. Cell-adhesion molecules and metalloproteinases: a linked role in tumour cell invasiveness. Biochem Soc Trans 1994; 22: 63-68.
69. r 72,000 type IV collagenase in human colonie adenocarcinoma. Cancer Res 1991; 51: 439-444.
70. Overall CM, Wrana JL, Sodek J. Transcriptional and post-transcriptional regulation of 72-kDa gelatinase/type IV collagenase by transforming growth factor-beta 1 in human fibroblasts. Comparisons with collagenase and tissue inhibitor of matrix metalloproteinase gene expression. J Biol Chem 1991; 266: 14064-14071.
71. Sato H, Seiki M. Membrane-type matrix metalloproteinases (MT-MMPs) in tumor metastasis. J Biochem 1996; 119: 209-215.
72. Tokuraku M, Sato H, Murakami S, et al. Activation of the precursor of gelatinase A/72 kDa type IV collagenase/MMP-2 in lung carcinomas correlates with the expression of membrane-type metalloproteinase (MT-MMP) and with lymph node metastasis. Int J Cancer 1995; 64: 355-359.
73. Nomura H, Sato H, Seiki M, Mai M, Okada Y. Expression of membrane-type matrix metalloproteinase in human gastric carcinomas. Cancer Res 1995; 55: 3263-3266.
74. Foda HD, George S, Conner C, et al. Activation of human umbilical vein endothelial cell progelatinase A by phorbol myristate acetate: a protein kinase C-dependent mechanism involving a membrane-type matrix metalloproteinase. Lab Invest 1996; 74: 538-545.
75. Yamada T, Yoshiyama Y, Sato H, et al. White matter microglia produce membrane-type matrix metalloprotease, an activator of gelatinase A, in human brain tissues. Acta Neuropathol 1995; 90: 421-424.
76. Boone TC, Johnson MJ, DeClerck YA, Langley KE. cDNA cloning and expression of a metalloproteinase inhibitor related to tissue inhibitor of metalloproteinases. Proc Natl Acad Sci USA 1990; 87: 2800-2804.
77. DeClerck YA, Yean TD, Ratzkin, BJ, Lu HS, Langley KE. Purification and characterization of two related but distinct metalloproteinase inhibitors secreted by bovine aortic endothelial cells. J Biol Chem 1989; 264: 17445-17453.
78. Murphy G, Cawston T, Reynolds J. An inhibitor of collagenase from human amniotic fluid: purification, characterization and action on metalloproteinases. Biochem J 1981; 195: 167-170.
79. Stetler-Stevenson WG, Krutzsch HC, Liotta LA. Tissue inhibitor of metalloproteinase (TIMP-2): a new member of the metalloproteinase inhibitor family. J Biol Chem 1989; 264: 17374-17378.
80. Goldberg GI, Marmer BL, Grant GA, et al. Human 72K type IV collagenase forms a complex with a tissue inhibitor of metalloproteinases designated TIMP-2. Proc Natl Acad Sci USA 1989; 86: 8207-8211.
81. Goldberg GI, Strongin A, Collier IE, Genrich LT, Marmer BL. Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinase prevents dimerization, complex formation with interstitial collagenase and activation of the proenzyme with stromelysin. J Biol Chem 1992; 267: 4583-4591.
82. DeClerck YA, Imren S. Protease inhibitors: role and potential therapeutic use in human cancer. Eur J Cancer 1994; 30A: 2170-2180.
83. Matsuzawa K, Fukuyama K, Hubbard SL, Dirks PB, Rutka JT. Transfection of an invasive human astrocytoma cell line with a TIMP-1 cDNA: modulation of astrocytoma invasive potential. J Neuropathol Exp Neurol 1996; 55: 88-96.
84. Nakano A, Tani E, Miyazaki K, Yamamoto Y, Furuyama J-I. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gliomas. J Neurosurg 1995; 83: 298-307.
85. DeClerck YA, Perez N, Shimada H, et al. Inhibition of invasion and metastasis in cells transfected with an inhibitor of metalloproteinases. Cancer Res 1992; 52: 701-708.
86. Mohanam S, Wang SW, Rayford A, et al. Expression of tissue inhibitors of metalloproteinases: negative regulators of human glioblastoma invasion in vivo. Clin Exp Metastasis 1995; 13: 57-62.
87. Kossakowska AE, Urbanski SJ, Edwards DR: Tissue inhibitor of metalloproteinases-1 (TIMP-1) RNA is expressed at elevated levels in malignant non-Hodgkin's lymphomas. Blood 1991; 77: 2475-2481.
88. Kossakowska AE, Urbanski SJ, Watson A, Hayden LJ, Edwards DR. Patterns of expression of metalloproteinases and their inhibitors in human malignant lymphomas. Oncol Res 1993; 5: 19-28.
89. Visscher DW, Hoyhtya M, Ottosen SK, et al. Enhanced expression of tissue inhibitor of metalloproteinase-2 (TIMP-2) in the stroma of breast carcinoma correlates with tumour recurrence. Int J Cancer 1994; 59: 339-344.
90. Fridman R, Bird RE, Hoyhtya M, et al. Expression of human recombinant 72 kDa gelatinase and tissue inhibitor of metalloproteinase-2 (TIMP-2): characterization of complex and free enzyme. Biochem J 1993; 289: 411-416.
91. Gasson JC, Golde DW, Kaufman SE, et al. Molecular characterization and expression of the gene encoding human erythroid-potentiating activity. Nature 1985; 315: 768-771.
92. Stetler-Stevenson WG, Bersch N, Golde DE. Tissue inhibitor of metalloproteinase-2 (TIMP-2) has erythroid potentiating activity. FEBS Lett 1992; 296: 231-234.
93. Avalos BR, Kaufman SE, Tomonaga M, et al. K562 cells produce and respond to human erythroid-potentiating activity. Blood 1988; 71: 1720-1725.
94. Bertaux B, Hornebeck W, Eisen AZ, Dubertret L. Growth stimulation of human keratinocytes by tissue inhibitor of metalloproteinases. J Invest Dermatol 1991; 97: 679-685.
95. Hayakawa T, Yamashita K, Tanzawa K, Uchijima E, Iwata K. Growth-promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. FEBS Lett 1992; 298: 29-32.
96. Murate T, Yamashita K, Ohashi H, et al. Erythroid potentiating activity of tissue inhibitor of metalloproteinases on the differentiation of erythropoietin-responsive mouse erythroleukemia cell line, ELM-I-1-3, is closely related to its cell growth potentiating activity. Exp Hematol 1993; 21: 169-176.
97. Nemeth JA, Goolsby, CL. TIMP-2, a growth-stimulatory protein from SV40-transformed human fibroblasts. Exp Cell Res 1993; 207: 376-382.
98. Overall CM. Regulation of tissue inhibitor of matrix metalloproteinase expression. In: Greenwald RA and Golub LM, eds. Inhibition of Matrix Metalloproteinases: Therapeutic Potential. New York: The New York Academy of Sciences, 1994: 51-64.
99. Weinstein IB. The role of protein kinase C in growth control and the concept of carcinogenesis as a progressive disorder in signal transduction. Adv in Second Messenger Phosphoprotein Res 1990; 24: 307-316.
100. Schwartz GK, Jiang J, Kelsen D, Albino AP. Protein kinase C: a novel target for inhibiting gastric cancer cell invasion. J Natl Cancer Inst 1994; 85: 402-407.
101. Baltuch GH, Dooley NP, Rostworowski KM, Villemure J-G, Yong VW. Protein kinase C isoform α overexpression in C6 glioma cells and its role in cell proliferation. J Neurooncol 1995; 24: 241-250.
102. Baltuch GH, Dooley NP, Villemure J-G, Yong VW. Protein kinase C and growth regulation of malignant gliomas, Can J Neurol Sci 1995; 22: 264-271.
103. Baltuch GH, Dooley NP, Couldwell WT, Yong VW. Staurosporine differentially inhibits glioma versus non-glioma cell lines. J Neurooncol 1993; 16: 141-147.
104. Couldwell WT, Antel JP, Apuzzo MLJ, Yong VW. Inhibition of growth of established human glioma lines by modulators of the protein kinase C system. J Neurosurg 1990; 73: 594-600.
105. Couldwell WT, Uhm JH, Antel JP, Yong VW. Enhanced protein kinase C activity correlates with the growth rate of malignant gliomas in vitro. Neurosurgery 1991; 29: 880-887.
106. Couldwell WT, Antel JP, Yong VW. Protein kinase C (PKC) activity correlates with growth rate of gliomas. II: Effects of glioma mitogens and modulators of PKC. Neurosurgery 1992; 31: 717-724.
107. Ahmad S, Mineta T, Martuza RL, Glazer RI. Antisense expression of protein kinase Ca inhibits the growth and tumorigenicity of human glioblastoma cells. Neurosurgery 1994; 35: 904-909.
108. Glazer RI, Ahmad S, Yazaki T, Martuza RL, Dean N. Inhibition of glioblastoma U-87 in vivo by a protein kinase Cα (PKCα) antisense phosphorothioate oligodeoxynucleotide (S-oligo). Proc Am Assoc Cancer Res 1996; 37: (Abstract).
109. Gopalakrishna R, Barsky SH. Tumor promoter-induced membrane-bound kinase C regulates hematogenous metastasis. Proc Natl Acad Sci USA 1988; 85; 612-616.
110. Takenaga K, Takahashi K. Effects of 12-O-tetradecanylphorbol-13-acetate on adhesiveness and lung-colonizing ability of Lewis lung carcinoma cells. Cancer Res 1986; 40: 375-380.
111. 2+ mobilization and protein kinase C activation in the induction of spontaneous metastasis by mouse mammary adenocarcinoma cells. Cancer Res 1989; 49: 2597-2602.
112. Nabeshima K, Komada N, Kishi J, et al. TPA-enhanced invasion of matrigel associated with augmentation of cell motility but no metalloproteinase activity in a highly metastatic variant (L-10) of human rectal adenocarcinoma cell line RCM-1. Int J Cancer 1993; 55: 974-981.
113. Schwartz GK, Redwood SM, Ohnuma T, et al. Inhibition of invasion of invasive human bladder carcinoma cells by protein kinase C inhibitor staurosporine. J Natl Cancer Inst 1990; 82: 1753-1756.
114. Lamph WW, Wamsley P, Sassone-Corsi P, Verma IM. Induction of proto-oncogene jun/AP-1 by serum and TPA. Nature 1988; 334: 629-631.
115. Overall CM, Sodek J. Concanavalin A produces a matrix-degradative phenotype in human fibroblasts. Induction and endogenous activation of collagenase, 72-kDa gelatinase, and Pump-1 is accompanied by the suppression of the tissue inhibitor of matrix metalloproteinases. J Biol Chem 1990; 265: 21141-21151.
116. Lim Y-T, Sugiura Y, Laug WE, et al. Independent regulation of matrix metalloproteinases and plasminogen activators in human fibrosarcoma cells. J Cell Physiol 1996; 167: 333-340.
117. DiBattista JA, Pelletier JP, Zafarullah M, et al. Coordinate regulation of matrix metalloproteases and tissue inhibitor of metalloproteinase expression in human synovial fibroboasts. J Rheumatol 1995; 43 (Suppl): 123-128.
118. Ries C, Kolb H, Petrides PE. Regulation of 92-kD gelatinase release in HL-60 leukemia cells: tumor necrosis factor-alpha as an autocrine stimulus for basal- and phorbol ester-induced secretion. Blood 1994; 83: 3638-3646.
119. Juarez J, Clayman G, Nakajima M, et al. Role and regulation of expression of 92-kDa type-IV collagenase (MMP-9) in 2 invasive squamous-cell-carcinoma cell lines of the oral cavity. Int J Cancer 1993; 55: 10-18.
120. Sanz L, Berra E, Municio MM, et al. Zeta PKC plays a critical role during stromelysin promoter activation by platelet-derived growth factor through a novel palindromic element. J Biol Chem 1994; 269: 10044-10049.
121. Nerlov C, Rorth P, Blasi F, Johnsen M. Essential AP-1 and PEA3 binding elements in the human urokinase enhancer display cell type-specific activity. Oncogene 1990; 5: 75-83.
122. Honn KV, Timar J, Rozhin J, et al. A lipoxygenase metabolite, 12-(S)-HETE, stimulates protein kinase C-mediated release of cathepsin B from malignant cells. Exp Cell Res 1994; 214: 120-130.
123. Kent KC, Mii S, Harrington EO, et al. Requirement for protein kinase C activation in basic fibroblast growth factor-induced human endothelial cell proliferation. Circulation Res 1995; 77: 231-238.
124. Hu DE, Fan TP. Protein kinase C inhibitor calphostin C prevents cytokine-induced angiogenesis in the rat. Inflammation 1995; 19: 39-53.
125. Tsopanoglou NE, Haralabopoulos GC, Maragoudakis ME. Opposing effects on modulationof angiogenesis by protein kinase C and cAMP-mediated pathways. J Vasc Res 1994: 31: 195-204.
126. Davis CM, Danehower SC, Laurenza A, Molony JL. Identification of a role of the vitronectin receptor and protein kinase C in the induction of endothelial cell vascular formation. J Cell Biochem 1993; 51: 206-218.
127. Stanimirovic DB, Ball R, Durkin JP. Evidence for the role of protein kinase C in astrocyte-induced proliferation of rat cerebromicrovascular endothelial cells. Neurosci Lett 1995; 197: 219-222.
128. Couldwell WT, Hinton DR, He SK, et al. Protein kinase C inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Lett 1994; 345: 43-46.
129. Ikemoto H, Tani E, Matsumoto T, Nakano A, Furuyama J-I. Apoptosis of human glioma cells in response to calphostin C, a specific protein kinase C inhibitor. J Neurosurg 1995; 83: 1008-1016.
130. Dooley NP, Baltuch GH, Groome N, Villemure J-G, Yong, VW. Apoptosis is induced in A172 human glioma line by antisense oligonucleotides to protein kinase C α and is enhanced by cycloheximide (submitted).
131. Basu A. The potential of protein kinase C as a target for anticancer treatment. Pharmac Ther 1993; 59: 257-280.
132. Baltuch G, Shenouda G, Langleben A. Villemure J-G. High-dose tamoxifen in the treatment of recurrent high grade glioma: a report of clinical stabilization and tumour regression. Can J Neurol Sci 1993; 20: 168-170.
133. Bradshaw D, Hill CH, Nixon JS, Wilkinson SE. Therapeutic potential of protein kinase C inhibitors. Agents Actions 1993; 38: 135-147.
134. Couldwell WT, Hinton DR, Surnock AA, et al. Treatment of recurrent malignant gliomas with chronic oral high-dose tamoxifen. Clin Cancer Res 1996; 2: 619-622.
135. Baltuch GH, Couldwell WT, Viilemure J-G, Yong, VW. Protein kinase C inhibitors suppress cell growth in established and low passage glioma cell lines. A comparison between staurosporine and tamoxifen. Neurosurgery 1993; 33: 495-501.
136. O'Brian CA, Liskamp RM, Solomon DH, Weinstein IB. Inhibition of protein kinase C by tamoxifen. Cancer Res 1985; 45: 2462-2465.
137. Pollack IF, Randall MS, Kristofic MP, et al. Effect of tamoxifen on DNA synthesis and proliferation of human malignant glioma lines in vitro. Cancer Res 1990; 50: 7134-7138.
138. Couldwell WT, Weiss MH, DeGiorgio CM, et al. Clincal and radiographic response in a minority of patients with recurrent malignant gliomas treated with high-dose tamoxifen. Neurosurgery 1993; 32: 485-490.
139. Brown PD. Synthetic matrix metalloproteinase inhibitors: From cancer models to cancer patients. Proc Am Assoc Cancer Res 1996; 37: 633-634.
140. Crissman J Metastases from metastasis: clinical relevance in human cancer. In: Goldfarb R, ed. Fundamental Aspects of Cancer. Dordrecht, Netherlands: Kluwer Academic Publishers, 1989: 156-161.
141. Kono S, Sci DM, Rao JS, Bruner JM, Sawaya R. Immunohistochemical localization of plasminogen activator inhibitor type 1 in human brain tumors. J Neuropathol Exp Neurol 1994; 53: 256-262.
142. Vaithilingam IS, McDonald W, Malott DW, Del Maestro RF. An extracellular proteasome-like structure from C6 astrocytoma cells with serine collagenase IV activity and metallo-dependent activity on α -casein and β-insulin. J Biol Chem 1995; 270: 4588-4593.
143. Woessner JF, Jr. The family of matrix metalloproteinases. Ann NY Acad Sci 1994; 732: 11-21.