Inhibition of invasion, angiogenesis, tumor growth, and metastasis by adenovirus-mediated transfer of antisense uPAR and MMP-9 in non-small cell lung cancer cells

Molecular Cancer Therapeutics

Volumn 4, Issue 9, 2005, Pages 1399-1408

  Rao, Jasti S ^a   Gondi, Christopher ^a   Chetty, Chandramu ^a   Chittivelu, Subramanyam ^a   Joseph, Pushpa A ^a   Lakka, Sajani S ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE B; UROKINASE; CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; PLASMINOGEN ACTIVATOR, UROKINASE RECEPTORS;

ADENOVIRUS VECTOR; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CANCER REGRESSION; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENE THERAPY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; METASTASIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; STATISTICAL MODEL; STATISTICAL SIGNIFICANCE; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ZYMOGRAPHY; ADENOVIRUS; ANIMAL; CELL CULTURE; CELL PROLIFERATION; GENE TRANSFER; GENE VECTOR; GENETICS; LUNG TUMOR; METABOLISM; MOUSE; MOUSE MUTANT; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; VASCULARIZATION;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; DNA, ANTISENSE; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; LUNG NEOPLASMS; MATRIX METALLOPROTEINASE 9; MICE; MICE, SCID; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, CELL SURFACE; TUMOR CELLS, CULTURED;

EID: 33644683515     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-05-0082     Document Type: Article

References (64)

1. Shottenfeld D. Epidemiology of lung cancer. In: Pass HI, Mitchell JB, Johnson DH, Turrisi AT, Minna JD, editors. Lung cancer. Philadelphia: Lippincott Williams & Wilkins; 2003. p. 367-88.
2. Liotta LA, Stetler-Stevenson WG. Tumor invasion and metastasis: an imbalance of positive and negative regulation. Cancer Res 1991;51: 5054-9s.
3. MacKay AR, Corbitt RH, Hartzler JL, Thorgeirsson UP. Basement membrane type IV collagen degradation: evidence for the involvement of a proteolytic cascade independent of metalloproteinases. Cancer Res 1990; 50:5997-6001.
4. Dano K, Behrendt N, Brunner N, Ellis V, Ploug M, Pyke C. The urokinse receptor. Protein structure and role in plasminogen activation and cancer invasion. Fibrinolysis 1994;8:189-203.
5. Vassalli JD. The urokinase receptor. Fibrinolysis 1994;8:172-81.
6. Chapman HA. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr Opin Cell Biol 1997;9: 714-24.
7. Wei Y, Lukashev M, Simon DI, et al. Regulation of integrin function by the urokinase receptor. Science 1996;273:1551-5.
8. Wei Y, Waltz DA, Rao N, Drummond RJ, Rosenberg S, Chapman HA. Identification of the urokinase receptor as an adhesion receptor for vitronectin. J Biol Chem 1994;269:32380-8.
9. Ossowski L, Aguirre-Ghiso JA. Urokinase receptor and integrin partnership: coordination of signaling for cell adhesion, migration and growth. Curr Opin Cell Biol 2000;12:613-20.
10. Bolon I, Gouyer V, Devouassoux M, et al. Expression of c-ets-1, collagenase 1, and urokinase-type plasminogen activator genes in lung carcinomas. Am J Pathol 1995;147:1298-310.
11. Bolon I, Devouassoux M, Robert C, Moro D, Brambilla C, Brambilla E. Expression of urokinase-type plasminogen activator, stromelysin 1, stromelysin 3, and matrilysin genes in lung carcinomas. Am J Pathol 1997;150:1619-29.
12. Robert C, Bolon I, Gazzeri S, Veyrenc S, Brambilla C, Brambilla E. Expression of plasminogen activator inhibitors 1 and 2 in lung cancer and their role in tumor progression. Clin Cancer Res 1999;5:2094-102.
13. Ignar DM, Andrews JL, Witherspoon SM, et al. Inhibition of establishment of primary and micrometastatic tumors by a urokinase plasminogen activator receptor antagonist. Clin Exp Metastasis 1998; 16: 9-20.
14. Stamenkovic I. Extracellular matrix remodelling: the role of matrix metalloproteinases. J Pathol 2003;200:448-64.
15. Vihinen P, Kahari VM. Matrix metalloproteinases in cancer: prognostic markers and therapeutic targets. Int J Cancer 2002;99:157-66.
16. Brown PD, Bloxidge RE, Stuart NS, Gatter KC, Carmichael J. Association between expression of activated 72-kilodalton gelatinase and tumor spread in non-small-cell lung carcinoma. J Natl Cancer Inst 1993;85:574-8.
17. Gonzalez-Avila G, Iturria C, Vadillo F, Teran L, Selman M, Perez-Tamayo R. 72-kD (MMP-2) and 92-kD (MMP-9) type IV collagenase production and activity in different histologic types of lung cancer cells. Pathobiology 1998;66:5-16.
18. Urbanski SJ, Edwards DR, Maitland A, Leco KJ, Watson A, Kossakowska AE. Expression of metalloproteinases and their inhibitors in primary pulmonary carcinomas. Br J Cancer 1992;66:1188-94.
19. Kodate M, Kasai T, Hashimoto H, Yasumoto K, Iwata Y, Manabe H. Expression of matrix metal lo proteinase (gelatinase) in T1 adenocarcinoma of the lung. Pathol Int 1997;47:461-9.
20. Nawrocki B, Polette M, Marchand V, et al. Expression of matrix metalloproteinases and their inhibitors in human bronchopulmonary carcinomas: quantificative and morphological analyses. Int J Cancer 1997;72:556-64.
21. Suzuki M, Iizasa T, Fujisawa T, et al. Expression of matrix metalloproteinases and tissue inhibitor of matrix metalloproteinases in non-small-cell lung cancer. Invasion Metastasis 1998;18:134-41.
22. Sienel W, Hellers J, Morresi-Hauf A, et al. Prognostic impact of matrix metalloproteinase-9 in operable non-small cell lung cancer. Int J Cancer 2003;103:647-51.
23. Lakka SS, Rajagopal R, Rajan MK, et al. Adenovirus-mediated antisense urokinase-type plasminogen activator receptor gene transfer reduces tumor cell invasion and metastasis in non-small cell lung cancer cell lines. Clin Cancer Res 2001;7:1087-93.
24. Lakka SS, Gondi CS, Yanamandra N, et al. 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 Res 2003;63:2454-61.
25. Palmer GD, Gouze E, Gouze JN, Betz OB, Evans CH, Ghivizzani SC. Gene transfer to articular chondrocytes with recombinant adenovirus. Methods Mol Biol 2003;215:235-46.
26. Mueller-Klieser W. Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am J Physiol 1997;273:C1109-23.
27. Bugge TH, Kombrinck KW, Xiao Q, et al. Growth and dissemination of Lewis lung carcinoma in plasminogen-deficient mice. Blood 1997;90: 4522-31.
28. Anderson IC, Shipp MA, Docherty AJP, Teicher BA. Combination therapy including a gelatinase inhibitor and cytotoxic agent reduces local invasion and metastasis of murine Lewis lung carcinoma. Cancer Res 1996;56:715-8.
29. Andreasen PA, Kjoller L, Christensen L, Duffy MJ. The urokinase-type plasminogen activator system in cancer metastasis: a review. Int J Cancer 1997;72:1-22.
30. Sato H, Kida Y, Mai M, et al. Expression of genes encoding type IV collagen-degrading metalloproteinases and tissue inhibitors of metalloproteinases in various human tumor cells. Oncogene 1992;7:77-83.
31. Muller D, Breathnach R, Engelmann A, et al. Expression of collagenase-related metalloproteinase genes in human lung or head and neck tumours. Int J Cancer 1991 Jun 19;48:550-6.
32. Kerbel RS, Rak J, Kobayashi H, Man MS, St Croix B, Graham CH. Multicellular resistance: a new paradigm to explain aspects of acquired drug resistance of solid tumors. Cold Spring Harb Symp Quant Biol 1994; 59:661-72.
33. Phillips RM, Clayton MR. Plateau-phase cultures: an experimental model for identifying drugs which are bioactivated within the microenvironment of solid tumours. Br J Cancer 1997;75:196-201.
34. Bredin CG, Liu Z, Hauzenberger D, Klominek J. Growth-factor-dependent migration of human lung-cancer cells. Int J Cancer 1999;82: 338-45.
35. Vignaud JM, Martinet Y, Martinet N. Role of growth factors in the stromal reaction in non-small cell lung carcinoma. In: Brambilla C, Brambilla E, editors. Lung tumors. Fundamental biology and clinical management. New York: Marcel Dekker, Inc.; 1998. p. 347-64.
36. Taipale J, Keski-Oja J. Growth factors in the extracellular matrix. FASEB J 1997; 11:51-9.
37. Bredin CG, Liu Z, Klominek J. Growth factor-enhanced expression and activity of matrix metalloproteases in human non-small cell lung cancer cell lines. Anticancer Res 2003;23:4877-84.
38. Pei XH, Nakanishi Y, Takayama K, Bai F, Hare N. Granulocyte, granulocyte-macrophage, and macrophage colony-stimulating factors can stimulate the invasive capacity of human lung cancer cells. Br J Cancer 1999;79:40-6.
39. Li H, Lu H, Griscelli F, et al. Adenovirus-mediated delivery of a uPA/ uPAR antagonist suppresses angiogenesis-dependent tumor growth and dissemination in mice. Gene Ther 1998;5:1105-13.
40. Li H, Griscelli F, Lindenmeyer F, et al. Systemic delivery of antiangiogenic adenovirus AdmATF induces liver resistance to metastasis and prolongs survival of mice. Hum Gene Ther 1999; 10:3045-53.
41. Kim J, Yu W, Kovalski K, Ossowski L. Requirement for specific proteases in cancer cell intravasation as revealed by a novel semiquantitative PCR-based assay. Cell 1998;94:353-62.
42. Mira E, Lacalle RA, Buesa JM, et al. Secreted MMP9 promotes angiogenesis more efficiently than constitutive active MMP9 bound to the tumor cell surface. J Cell Sci 2004; 117:1847-57.
43. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295:2387-92.
44. Bonomi P. Matrix metalloproteinases and matrix metalloproteinase inhibitors in lung cancer. Semin Oncol 2002;29:78-86.
45. Yamamoto A, Yano S, Shiraga M, et al. A third-generation matrix metalloproteinase (MMP) inhibitor (ONO-4817) combined with docetaxel suppresses progression of lung micrometastasis of MMP-expressing tumor cells in nude mice. Int J Cancer 2003;103:822-8.
46. Liu J, Tsao MS, Pagura M, et al. Early combined treatment with carboplatin and the MMP inhibitor, prinomastat, prolongs survival and reduces systemic metastasis in an aggressive orthotopic lung cancer model. Lung Cancer 2003;42:335-44.
47. McCawley LJ, Crawford HC, King LE, Jr., Mudgett J, Matrisian LM. A protective role for matrix metalloproteinase-3 in squamous cell carcinoma. Cancer Res 2004;64:6965-72.
48. Bissell MJ, Radisky D. Putting tumours in context. Nat Rev Cancer 2001;1:46-54.
49. Fibbi G, Caldini R, Chevanne M, et al. Urokinase-dependent angiogenesis in vitro and diacylglycerol production are blocked by antisense oligonucleotides against the urokinase receptor. Lab Invest 1998;78:1109-19.
50. Koolwijk P, van Erck MG, de Vree WJ, et al. Cooperative effect of TNFa, bFGF, and VEGF on the formation of tubular structures of human microvascular endothelial cells in a fibrin matrix. Role of urokinase activity. J Cell Biol 1996;132:1177-88.
51. Koolwijk P, Sidenius N, Peters E, et al. Proteolysis of the urokinase-type plasminogen activator receptor by metalloproteinase-12: implication for angiogenesis in fibrin matrices. Blood 2001;97:3123-31.
52. Mazer AP, Henkin J, Goldfarb RH. The urokinase plasminogen activator system in cancer: implications for tumor angiogenesis and metastasis. Angiogenesis 1999;3:15-32.
53. Lu H, Mabilat C, Yeh P, et al. Blockage of urokinase receptor reduces in vitro the motility and the deformability of endothelial cells. FEBS Lett 1996;380:21-4.
54. Min HY, Doyle LV, Vitt CR, et al. Urokinase receptor antagonists inhibit angiogenesis and primary tumor growth in syngeneic mice. Cancer Res 1996;56:2428-33.
55. Yasunaga C, Nakashima Y, Sueishi K. A role of fibrinolytic activity in angiogenesis. Quantitative assay using in vitro method. Lab Invest 1989; 61:698-704.
56. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res 1998;58:1048-51.
57. Vu TH, Shipley JM, Bergers G, et al. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 1998;93:411-22.
58. Stetler-Stevenson WG. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest 1999;103:1237-41.
59. Pinto CA, Carvalho PE, Antonangelo L, et al. Morphometric evaluation of tumor matrix metalloproteinase 9 predicts survival after surgical resection of adenocarcinoma of the lung. Clin Cancer Res 2003;9:3098-104.
60. O'Reilly MS, Holmgren L, Shing Y, et al. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 1994;79:315-28.
61. Engbring JA, Kleinman HK. The basement membrane matrix in malignancy. J Pathol 2003;200:465-70.
62. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001; 17:463-516.
63. Rabbani SA, Mazer AP. The role of the plasminogen activation system in angiogenesis and metastasis. Surg Oncol Clin N Am 2001;10: 393-415.
64. Lund LR, Romer J, Bugge TH, et al. Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J 1999; 18:4645-56.