Synergistic down-regulation of urokinase plasminogen activator receptor and matrix metalloproteinase-9 in SNB19 glioblastoma cells efficiently inhibits glioma cell invasion, angiogenesis, and tumor growth

Cancer Research

Volumn 63, Issue 10, 2003, Pages 2454-2461

  Lakka, Sajani S ^a   Gondi, Christopher S ^a   Yanamandra, Niranjan ^a   Dinh, Dzung H ^a   Olivero, William C ^a   Gujrati, Meena ^a   Rao, Jasti S ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ANTISENSE OLIGONUCLEOTIDE; GELATINASE B; GROWTH HORMONE; UROKINASE RECEPTOR;

ADENOVIRUS 5; ANGIOGENESIS; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INVASION; CARCINOGENICITY; CONTROLLED STUDY; CYTOMEGALOVIRUS; EMBRYO; GENE THERAPY; GLIOMA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; RAT; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR GROWTH; TUMOR VOLUME; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING;

ADENOVIRIDAE; ANIMALS; CELL DIVISION; CELL MOVEMENT; DNA, ANTISENSE; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; GLIOBLASTOMA; HUMANS; MATRIX METALLOPROTEINASE 9; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CELL SURFACE; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 0038181212     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Mignatti, P., and Rifkin, D. B. Biology and biochemistry of proteinases in tumor invasion. Physiol. Rev., 73: 161-195, 1993.
2. Blasi, F. Proteolysis, cell adhesion, chemotaxis, and invasiveness are regulated by the u-PA-u-PAR-PAI-1 system. Thromb. Haemost., 82: 298-304, 1999.
3. Crowley, C. W., Cohen, R. L., Lucas, B. K., Liu, G., Shuman, M. A., and Levinson, A. D. Prevention of metastasis by inhibition of the urokinase receptor. Proc. Natl. Acad. Sci. USA, 90: 5021-5025, 1993.
4. Min, H. Y., Doyle, L. V., Vitt, C. R., Zandonella, C. L., Stratton-Thomas, J. R., Shuman, M. A., and Rosenberg, S. Urokinase receptor antagonists inhibit angiogenesis and primary tumor growth in syngeneic mice. Cancer Res., 56: 2428-2433, 1996.
5. Yu, W., Kim, J., and Ossowski, L. Reduction in surface urokinase receptor forces malignant cells into a protracted state of dormancy. J. Cell Biol., 137: 767-777, 1997.
6. Yamamoto, M., Sawaya, R., Mohanam, S., Rao, V. H., Bruner, J. M., Nicolson, G. L., and Rao, J. S. Expression and localization of urokinase-type plasminogen activator receptor in human gliomas. Cancer Res., 54: 5016-5020, 1994.
7. Gladson, C. L., Pijuan-Thompson, V., Olman, M. A., Gillespie, G. Y., and Yacoub, I. Z. Up-regulation of urokinase and urokinase receptor genes in malignant astrocytoma. Am. J. Pathol., 146: 1150-1160, 1995.
8. Mohanam, S., Chintala, S. K., Go, Y., Bhattacharya, A., Venkaiah, B., Boyd, D., Gokaslan, Z. L., Sawaya, R., and Rao, J. S. In vitro inhibition of human glioblastoma cell line invasiveness by antisense uPA receptor. Oncogene. 14: 1351-1359, 1997.
9. Go, Y., Chintala, S. K., Mohanam, S., Gokaslan, Z., Venkaiah, B., Bjerkvig, R., Oka, K., Nicolson, G. L., Sawaya, R., and Rao, J. S. Inhibition of in vivo tumorigenicity and invasiveness of a human glioblastoma cell line transfected with antisense uPAR vectors. Clin. Exp. Metastasis, 15: 440-446, 1997.
10. Mohanam, S., Chintala, S. K., Mohan, P. M., Sawaya, R., Lagos, G. K., Gokaslan, Z. L., Kouraklis, G. P., and Rao, J. S. Increased invasion of neuroglioma cells transfected with urokinase plasminogen activator receptor cDNA. Int. J. Oncol., 13: 1285-1290, 1998.
11. Mohan, P. M., Chintala, S. K., Mohanam, S., Gladson, C. L., Kim, E. S., Gokaslan, Z. L., Lakka, S. S., Roth, J. A., Fang, B., Sawaya, R., Kyritsis, A. P., and Rao, J. S. Adenovirus-mediated delivery of antisense gene to urokinase-type plasminogen activator receptor suppresses glioma invasion and tumor growth. Cancer Res., 59: 3369-3373, 1999.
12. Chapman, H. A., Wei, Y., Simon, D. I., and Waltz, D. A. Role of urokinase receptor and caveolin in regulation of integrin signaling. Thromb. Haemost., 82: 291-297, 1999.
13. Irigoyen, J. P., Munoz-Canoves, P., Montero, L., Koziczak, M., and Nagamine, Y. The plasminogen activator system: biology and regulation. Cell Mol. Life Sci., 56: 104-132, 1999.
14. Rao, N. K., Shi, G. P., and Chapman, H. A. Urokinase receptor is a multifunctional protein: influence of receptor occupancy on macrophage gene expression. J. Clin. Investig., 96: 465-474, 1995.
15. Ruoslahti, E. Integrins. J. Clin. Investig., 87: 1-5, 1991.
16. Forsyth, P. A., Wong, H., Laing, T. D., Rewcastle, N. B., Morris, D. G., Muzik, H., Leco, K. J., Johnston, R. N., Brasher, P. M., Sutherland, G., and Edwards, D. R. Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas. Br. J. Cancer, 79: 1828-1835, 1999.
17. Rao, J. S., Steck, P. A., Mohanam, S., Stetler-Stevenson, W. G., Liotta, L. A., and Sawaya, R. Elevated levels of M(r) 92, 000 type IV collagenase in human brain tumors. Cancer Res, 53: 2208-2211, 1993.
18. Sawaya, R., Go, Y., Kyritisis, A. P., Uhm, J., Venkaiah, B., Mohanam, S., Gokaslan, Z. L., and Rao, J. S. Elevated levels of Mr 92,000 type IV collagenase during tumor growth in vivo. Biochem. Biophys. Res. Commun., 251: 632-636, 1998.
19. Chintala, S. K., Tonn, J. C., and Rao, J. S. Matrix metalloproteinases and their biological function in human gliomas. Int. J. Dev. Neurosci., 17: 495-502, 1999.
20. Chandrasekar, N., Jasti, S., Alfred-Yung, W. K., Ali-Osman, F., Dinh, D. H., Olivero, W. C., Gujrati, M., Kyritsis, A. P., Nicolson, G. L., Rao, J. S., and Mohanam, S. Modulation of endothelial cell morphogenesis in vitro by MMP-9 during glial-endothelial cell interactions. Clin. Exp. Metastasis, 18: 337-342, 2000.
21. Kondraganti, S., Mohanam, S., Chintala, S. K., Kin, Y., Jasti, S. L., Nirmala, C., Lakka, S. S., Adachi, Y., Kyritsis, A. P., Ali-Osman, F., Sawaya, R., Fuller, G. N., and Rao, J. S. Selective suppression of matrix metalloproteinase-9 in human glioblastoma cells by antisense gene transfer impairs glioblastoma cell invasion. Cancer Res., 60: 6851-6855, 2000.
22. Lakka, S. S., Jasti, S. L., Gondi, C., Boyd, D., Chandrasekar, N., Dinh, D. H., Olivero, W. C., Gujrati, M., and Rao, J. S. Downregulation of MMP-9 in ERK-mutated stable transfectants inhibits glioma invasion in vitro. Oncogene, 21: 5601-5608, 2002.
23. Giese, A., and Westphal, M. Glioma invasion in the central nervous system. Neurosurgery, 39: 235-250, 1996.
24. Anderson, W. F. Excitement in gene therapy! Hum. Gene Ther., 12: 1483-1484, 2001.
25. Graham, F. L., and Prevec, L. Manipulation of adenovirus vectors. In: E. J. Murray (ed.), Methods in Molecular Biology, pp. 109-127. Clifton, NJ: The Humana Press. 1991.
26. Hollas, W., Soravia, E., Mazar, A., Henkin, J., Blasi, F., and Boyd, D. Decreased urokinase receptor expression by overexpression of the plasminogen activator in a colon cancer cell line. Biochem. J., 285: 629-634, 1992.
27. Pedersen, H., Brunner, N., Francis, D., Osterlind, K., Ronne, E., Hansen, H. H., Dano, K., and Grondahl-Hansen, J. Prognostic impact of urokinase, urokinase receptor, and type 1 plasminogen activator inhibitor in squamous and large cell lung cancer tissue. Cancer Res., 54: 4671-4675, 1994.
28. Stahl, A., and Mueller, B. M. Binding of urokinase to its receptor promotes migration and invasion of human melanoma cells in vitro. Cancer Res., 54: 3066-3071, 1994.
29. Reiter, L. S., Kruithof, E. K., Cajot, J. F., and Sordat, B. The role of the urokinase receptor in extracellular matrix degradation by HT29 human colon carcinoma cells. Int. J. Cancer, 53: 444-450, 1993.
30. Mohanam, S., Sawaya, R., McCutcheon, I., Ali-Osman, F., Boyd, D., and Rao, J. S. Modulation of in vitro invasion of human glioblastoma cells by urokinase-type plasminogen activator receptor antibody. Cancer Res., 53: 4143-4147, 1993.
31. Bourguignon, L. Y., Gunja-Smith, Z., Iida, N., Zhu, H. B., Young, L. J., Muller, W. J., and Cardiff, R. D. CD44v(3, 8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J. Cell. Physiol., 176: 206-215, 1998.
32. Waltz, D. A., Fujita, R. M., Yang, X., Natkin, L., Zhuo, S., Gerard, C. J., Rosenberg, S., and Chapman, H. A. Nonproteolytic role for the urokinase receptor in cellular migration in vivo. Am. J. Respir. Cell Mol. Biol., 22: 316-322, 2000.
33. Legrand, C., Gilles, C., Zahm, J. M., Polette, M., Buisson, A. C., Kaplan, H., Birembaut, P., and Tournier, J. M. Airway epithelial cell migration dynamics. MMP-9 role in cell-extracellular matrix remodeling. J. Cell Biol., 146: 517-529, 1999.
34. Ratzinger, G., Stoitzner, P., Ebner, S., Lutz, M. B., Layton, G. T., Rainer, C., Senior, R. M., Shipley, J. M., Fritsch, P., Schuler, G., and Romani, N. Matrix metalloproteinases 9 and 2 are necessary for the migration of Langerhans cells and dermal dendritic cells from human and murine skin. J. Immunol., 168: 4361-4371, 2002.
35. Kin, Y., Chintala, S. K., Go, Y., Sawaya, R., Mohanam, S., Kyritsis, A. P., and Rao, J. S. A novel role for the urokinase-type plasminogen activator receptor in apoptosis of malignant gliomas. Int. J. Oncol., 17: 61-65, 2000.
36. Li, H., Lu, H., Griscelli, F., Opolon, P., Sun, L. Q., Ragot, T., Legrand, Y., Belin, D., Soria, J., Soria, C., Perricaudet, M., and Yeh, P. Adenovirus-mediated delivery of a uPA/uPAR antagonist suppresses angiogenesis-dependent tumor growth and dissemination in mice. Gene Ther., 5: 1105-1113, 1998.
37. Evans, C. P., Elfman, F., Parangi, S., Conn, M., Cunha, G., and Shuman, M. A. Inhibition of prostate cancer neovascularization and growth by urokinase-plasminogen activator receptor blockade. Cancer Res., 57: 3594-3599, 1997.
38. Guo, Y., Higazi, A. A., Arakelian, A., Sachais, B. S., Cines, D., Goldfarb, R. H., Jones, T. R., Kwaan, H., Mazar, A. P., and Rabbani, S. A. A peptide derived from the nonreceptor binding region of urokinase plasminogen activator (uPA) inhibits tumor progression and angiogenesis and induces tumor cell death in vivo. FASEB J., 14: 1400-1410, 2000.
39. Mishima, K., Mazar, A. P., Gown, A., Skelly, M., Ji, X. D., Wang, X. D., Jones, T. R., Cavenee, W. K., and Huang, H. J. A peptide derived from the non-receptor-binding region of urokinase plasminogen activator inhibits glioblastoma growth and angiogenesis in vivo in combination with cisplatin. Proc. Natl. Acad. Sci. USA, 97: 8484-8489, 2000.
40. Coussens, L. M., Tinkle, C. L., Hanahan, D., and Werb, Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell, 103: 481-490, 2000.
41. Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z., and Hanahan, D. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat. Cell Biol., 2: 737-744, 2000.
42. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., and Werb, Z. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell, 93: 411-422, 1998.
43. Rabbani, S. A., and Mazar, A. P. The role of the plasminogen activation system in angiogenesis and metastasis. Surg. Oncol. Clin. N. Am., 10: 393-415, 2001.
44. Kjoller, L. The urokinase plasminogen activator receptor in the regulation of the actin cytoskeleton and cell motility. J. Biol. Chem., 383: 5-19, 2002.
45. Chapman, H. A., and Wei, Y. Protease crosstalk with integrins: the urokinase receptor paradigm. Thromb. Haemost., 86: 124-129, 2001.
46. Clezardin, P. Recent insights into the role of integrins in cancer metastasis. Cell Mol. Life Sci., 54: 541-548, 1998.
47. Lund, L. R., Romer, J., Bugge, T. H., Nielsen, B. S., Frandsen, T. L., Degen, J. L., Stephens, R. W., and Dano, K. Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J., 18: 4645-4656, 1999.
48. Vlachaki, M., Hernandez-Garcia, A., Ittmann, M., Chhikara, M., Aguilar, L., Zhu, Z., The, B., Butler, E., Woo, S., Thompson, T., Barrera-Saldana, H., and Aguilar-Cordova, E. Impact of preimmunization on adenoviral vector expression and toxicity in a subcutaneous mouse cancer model. Mol. Ther., 6: 342-348, 2002.