Interferon-γ-inducible protein 10 (IP-10) is an angiostatic factor that inhibits human non-small cell lung cancer (NSCLC) tumorigenesis and spontaneous metastases

Journal of Experimental Medicine

Volumn 184, Issue 3, 1996, Pages 981-992

  Arenberg, Douglas A ^a   Kunkel, Steven L ^a   Polverini, Peter J ^b   Morris, Susan B ^a   Burdick, Marie D ^a   Glass, Mary C ^a   Taub, Dennis T ^c   Iannettoni, Mark D ^d   Whyte, Richard I ^d   Strieter, Robert M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; PROTEIN;

ANGIOGENESIS; ARTICLE; CANCER INHIBITION; COMBINED IMMUNODEFICIENCY; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; LUNG NON SMALL CELL CANCER; LUNG SQUAMOUS CELL CARCINOMA; METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

EID: 9544257385     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.184.3.981     Document Type: Article

References (60)

1. Beckett, W.S. 1993. Epidemiology and etiology of lung cancer. Clin. Chest Med. 14:1-15.
2. Faber, L.P. 1991. Lung cancer. In American Cancer Society Textbook of Clinical Oncology. A.I. Holleb, D.J. Fink, and G.P. Murphy, editors. American Cancer Society, Atlanta. 194-212.
3. Garfinkel, A. 1991. Cancer Statistics and Trends. In American Cancer Society Textbook of Clinical Oncology. A.I. Holleb, D.J. Fink, and G.P. Murphy, editors. American Cancer Society, Atlanta, GA. 2-9.
4. Carney, D.N. 1988. Cancers of the lungs. 2nd ed. In Pulmonary Diseases and Disorders. A.P. Fishman, editor. McGraw-Hill, New York. 1885-2068.
5. Gimbrone, M.A., S.B. Leapman, R.S. Cotran, and J. Folkman. 1972. Tumor dormancy in vivo by prevention of neovascularization. J. Exp Med. 136:261-276.
6. Folkman, J., and R. Cotran. 1976. Relation of vascular proliferation to tumor growth. International Reviews of Exp. Pathol. 16:207-248.
7. Kim, J.K., B. Li, J. Winer, M. Armanini, N. Gillett, H.S. Phillips, and N. Ferrara. 1993. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature (Lond.). 362:841-844.
8. Smith, D.R., P.J. Polverini, S.L. Kunkel, M.B. Orringer, R.I. Whyte, M.D. Burdick, C.A. Wilke, and R.M. Strieter. 1994. Inhibition of IL-8 attenuates angiogenesis in bronchogenic carcinoma. J. Exp. Med. 179:1409-1415.
9. Ueki, N., M. Nakazato, T. Ohkawa, T. Ikeda, Y. Amuro, T. Hada, and K. Higashino. 1992. Excessive production of TGF-β can play an important role in the development of tumorigenesis by its action for angiogenesis: validity of neutralizing antibodies to block tumor growth. Biochem Biophys. Acta. 1137:189-196.
10. Matsuzaki, K., Y. Yoshitake, Y. Matuo, H. Sasaki, and K. Nishikawa. 1989. Monoclonal antibodies against heparin binding growth factor II/basic fibroblast growth factor that block its biological activity: invalidity of the antibodies for tumor angiogenesis. Proc. Natl. Acad. Sci. USA. 86:9911-9915.
11. Rastinejad, F., P.J. Polverini, and N.P. Bouck. 1989. Regulation of the activity of a new inhibitor of angiogenesis by a cancer suppressor gene. Cell. 56:345-355.
12. O'Reilly, M.S., L. Holmgren, Y. Shing, C. Chen, R.A. Rosenthal, M. Moses, W.S. Lane, Y. Cao, E.H. Sage, and J. Folkman. 1994. Angiostatin: a novel angiogenesis inhibitor that mediates suppression of metastases by a Lewis lung carcinoma. Cell. 79:315-328.
13. Good, D.J., P.J. Polverini, F. Rastinejad, M.M. Le Beau, R.S. Lemons, W.A. Frazier, and N.P. Bouck. 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.
14. Van Meir, E.G., P.J. Polverini, V.R. Chazin, H.J. Su Huang, N. de Tribolet, and W.K. Cavence. 1994. Release of an inhibitor of angiogenesis upon induction of wild type p53 expression in glioblastoma cells. Nat. Genet. 8:171-176.
15. Majewski, S., A. Szmurlo, M. Marczak, S. Jablonska, and W. Bollag. 1994. Synergistic effect of retinoids and interferon alpha on tumor-induced angiogenesis: anti-angiogenic effect on HPV-harboring tumor-cell lines. Int. J. Cancer. 57:81-85.
16. Miller, J.W., W.G. Stinson, and J. Folkman. 1993. Regression of experimental iris neovascularization with systemic alpha-interferon. Ophthalmology. 100:9-14.
17. Clark, R.A. 1993. Basics of cutaneous wound repair. J. Dermatol. Surg. Oncol. 19:693-706.
18. Stout, A.J., I. Gresser, and W.D. Thompson. 1993. Inhibition of wound healing in mice by local interferon alpha/beta injection. Int. J. Exp. Pathol. 74:79-85.
19. Brem, H., I. Gresser, J. Grosfeld, and J. Folkman. 1993. The combination of antiangiogenic agents to inhibit primary tumor growth and metastasis. J. Pediatr. Surg. 28:1253-1257.
20. Kaplan, G., A.D. Luster, G. Hancock, and Z.A. Cohn. 1987. The expression of a gamma interferon-induced protein (IP-10) in delayed immune responses in human skin. J. Exp. Med. 166:1098-1108.
21. Boorsma, D.M., P. de Haan, R. Willemze, and T.J. Stoof. 1994. Human growth factor (huGRO), interleukin-8 (IL-8) and interferon- gamma-inducible protein (gamma-IP-10) gene expression in cultured normal human keratinocytes. Arch. Dermatol. Res. 286:471-475.
22. Gomez-Chiarri, M., T.A. Hamilton, J. Egido, and S.N. Emancipator. 1993. Expression of IP-10, a lipopolysaccharide- and interferon-gamma- inducible protein, in murine mesangial cells in culture. Am. J. Pathol. 1422:433-439.
23. Gattass, C.R., L.B. King, A.D. Luster, and J.D. Ashwell. 1994. Constitutive expression of interferon gamma-inducible protein 10 in lymphoid organs and inducible expression in T cells and thymocytes. J. Exp. Med. 179:1373-1378.
24. Strieter, R.M., S.L. Kunkel, D.A. Arenberg, M.D. Burdick, and P.J. Polverini. 1995. Interferon gamma-inducible protein 10 (IP-10), a member of the C-X-C chemokine family, is an inhibitor of angiogenesis. Biochem. Biophys. Res. Commun. 210:51-57.
25. Strieter, R.M., P.J. Polverini, S.L. Kunkel, D.A. Arenberg, M.D. Burdick, J. Kasper, J. Dzuiba, J.V. Damme, A. Walz, D. Marriott et al. 1995. The functional role of the 'ELR' motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem. 270:27348-27357.
26. Luster, A.D., S.M. Greenberg, and P. Leder. 1995. The IP-10 chemokine binds to a specific cell surface heparan sulfate shared with platelet factor 4 and inhibits endothelial cell proliferation. J. Exp. Med. 182:219-232.
27. Angiolillo, A.L., C. Sgadari, D.T. Taub, F. Liao, J.M. Farber, S. Maheshwari, H.K. Kleinman, G.H. Reaman, and G. Tosato. 1995. Human Interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med. 182:155-162.
28. Bacon, K.B., J. Westwick, and R.D.R. Camp. 1989. Potent and specific inhibition of IL-8, IL-1alpha, and IL-1beta-induced in vitro human lymphocyte migration by calcium channel antagonists. Biochem. Biophy. Res. Commun. 165: 349-354.
29. Standiford, T.J., S.L. Kunkel, M.A. Basha, S.W. Chensue, J.P. Lynch III, G.B. Toews, J. Westwick, and R.M. Strieter. 1990. Interleukin-8 gene expression by a pulmonary epithelial cell line: a model for cytokine networks in the lung. J. Clin. Invest. 86:1945-1953.
30. Rolfe, M.W., S.L. Kunkel, T.J. Standiford, S.W. Chensue, R.M. Allen, H.L. Evanoff, S.H. Phan, and R.M Strieter. 1991. Pulmonary fibroblast expression of interleukin-8: a model for alveolar macrophage-derived cytokine networking. Am. J. Respir. Cell. Mol. Biol. 5:493-501.
31. Smith, D.R., S.L. Kunkel, T.J. Standiford, S.W. Chensue, M.W. Rolfe, M.B. Orringer, R.I. Whyte, M.D. Burdick, J.M. Danforth, A.R. Gilbert, and R.M. Strieter. 1993. The production of Interleukin-1 receptor antagonist by human bronchogenic carcinoma. Am. J. Pathol. 143:794-803.
32. Koch, A.E., S.J. Leibovich, and P.J. Polverini. 1986. Stimulation of neovascularization by human rheumatoid synovial tissue macrophages. Arthritis Rheum. 29:471-479.
33. Polverini, P.J., P.S. Cotran, M.A. Gimbrone, and E.R. Unanue. 1977. Activated macrophages induce vascular proliferation. Nature (Lond.). 269:804-806.
34. Koch, A.E., J. Burrows, M. Cho, P.J. Polverini, and J. Leibovich. 1991. Thiol-containing compounds inhibit the production of monocyte/macrophage-derived angiogenic activity. Agents Actions. 34:350-357.
35. Koch, A.E., J. Burrows, M. Cho, P.J. Polverini, and J. Leibovich. 1991. Thiol-containing compounds inhibit the production of monocyte/macrophage-derived angiogenic activity. Agents Actions. 34:350-357.
36. Luster, A.D., J.C. Unkeless, and J.V. Ravetch. 1985. Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature (Lond.). 315:672-676.
37. Oppenheim, J.J., O.C. Zachariae, N. Mukaida, and K. Matsushima. 1991. Properties of the novel proinflammatory supergene "intercrine" cytokine family. Annu. Rev. Immunol. 9: 617-648.
38. Miller, M.D., and M.S. Krangel. 1992. Biology and biochemistry of the chemokines: a family of chemotactic and inflammatory cytokines. Crit. Rev. Immunol. 12:17-46.
39. Maione, T.E., G.S. Gray, J. Petro, A.J. Hunt, A.L. Donner, S.I. Bauer, H.F. Carson, and R.J. Sharpe. 1990. Inhibition of angiogenesis by recombinant human platelet factor-4. Science (Wash. DC). 247:77-79.
40. Maione, T.E., G.S. Gray, A.J. Hunt, H.F. Carson, and R.J. Sharpe. 1990. Inhibition of tumor growth in mice by an analogue of platelet factor 4 that lack affinity for heparin and retains potent angiostatic activity. Cancer Res. 51:2077-2083.
41. Hu, D.E., Y. Hori, and T.P.D. Fan. 1993. Interleukin-8 stimulates angiogenesis in rats. Inflammation. 17:135-143.
42. Koch, A.E., P.J. Polverini, S.L. Kunkel, L.A. Harlow, L.A. DiPietro, V.M. Elner, S.G. Elner, and R.M. Strieter. 1992. Interleukin-8 (IL-8) as a macrophage-derived mediator of angiogenesis. Science (Wash. DC). 258:1798-1801.
43. Strieter, R.M., S.L. Kunkel, V.M. Elner, C.L. Martonyl, A.E. Koch, P.J. Polverini, and S.G. Elner. 1992. Interleukin-8: a corneal factor that induces neovascularization. Am. J. Pathol. 141:1279-1284.
44. Tsuruoka, N., M. Sugiyama, Y. Tawaragi, M. Tsujimoto, T. Nishihara, T. Goto, and N. Sato. 1988. Inhibition of in vitro angiogenesis by lymphotoxin and interferon- gamma. Biochem Biophys. Res. Commun. 155:429-35.
45. Symington, F.W. 1989. Lymphotoxin, tumor necrosis factor and gamma interferon are cytostatic for normal human keratinocytes. J. Invest. Dermatol. 92:798-805.
46. Demaeyer, E., and J. Demaeyer-Guignard. 1988. Interferons and other regulatory cytokines. Wiley, New York.
47. Sidky, Y.A., and E.C. Borden. 1987. Inhibition of angiogenesis by interferons: effects on tumor- and lymphocyte-induced vascular responses. Cancer Res. 47:5155-5161.
48. Pober, J.S., M.A. Gimbrone, Jr., R.S. Cotran, C.S. Reiss, S.J. Burakoff, W. Fiers, and K.A. Ault. 1983. Ia expression by vascular endothelium is inducible by activated T cells and by human gamma interferon. J. Exp. Med. 157:1339-1353.
49. Schnyder-Candrian, S., R.M. Strieter, S.L. Kunkel, and A. Walz. 1995. Interferon-a and interferon-g downregulate the production of interleukin-8 and ENA-78 in human monocytes. J. Leuk. Biol. In press.
50. Gusella, G.L., T. Musso, M.C. Bosco, I. Espinoza-Delgado, K. Matsushima, and L. Varesio. 1993. IL-2 up-regulates but IFN-g suppresses IL-8 expression in human monocytes. J. Immunol. 151:2725-2732.
51. Folkman, J. 1995. Clinical applications of research on angiogenesis. N. Eng. J. Med. 333:1757-1763.
52. Dameron, K.M., O.V. Volpert, M.A. Tainsky, and N. Bouck. 1994. Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science (Wash. DC). 265: 1582-1584.
53. Minna, J.D. 1991. Neoplasms of the lung. 12th ed. In Principles of Internal Medicine. K.J. Isselbacher, editor. McGraew-Hill, New York. 1102-1110.
54. Yuan, A., Y. Pan-Chyr, Y. Chong-Jen, Y. Lee, Y. Yu-Tuang, C. Chi-Long, L. Lee, K. Sow-Hsong, and E. Kwen-Tay. 1995. Tumor angiogenesis correlates with histologic type and metastasis in non-small cell lung cancer. Am. J. Respir. Crit. Care Med. 152:2157-2162.
55. Momiki, S., M. Baba, J. Caamano, T. Iizasa, M. Nakajima, Y. Yamaguchi, and A.J.P. Klein-Szanto. 1991. In vivo and in vitro invasiveness of human lung carcinoma cell lines. Invasion Metastasis. 11:66-75.
56. Zucker, S., R.M. Lysik, M. Malik, B.A. Bauer, J. Caamano, and A.J.P. Klein-Szanto. 1992. Secretion of gelatinases and tissue inhibitors of metalloproteinases by human lung cancer cell lines and revertant cell lines: not an invariant correlation with metastasis. Int. J. Cancer. 52:366-371.
57. Mette, S.A., J. Pilewski, C.A. Buck, and S.M. Albelda. 1993. Distribution of integrin cell adhesion receptors on normal bronchial epithelial cells and lung cancer cells in vitro and in vivo. Am. J. Respir. Cell. Mol. Biol. 8:562-572.
58. Caamano, J., B. Ruggeri, S. Momiki, A. Sickler, S.Y. Zhang, and A.J.P. Klein-Szant. 1991. Detection of p53 in primary lung tumors and nonsmall cell lung carcinoma cell lines. Am. J. Pathol. 139:839-845.
59. Maione, T.E., G.S. Gray, A.J. Hunt, and R.J. Sharpe. 1991. Inhibition of tumor growth in mice by an analogue of platelet factor 4 that lacks affinity for heparin and retains potent angiostatic activity. Cancer Res. 51:2077-2083.
60. Luster, A.D., and P. Leder. 1993. IP-10, a CXC chemokine, elicits a potent thymus-dependent anti-tumor response in vivo. J. Exp. Med. 178:1057-1065.