Responsiveness of stromal fibroblasts to IFN-γ blocks tumor growth via angiostasis

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6413-6421

  Lu, Yu ^a,b   Yang, Wei ^a,b   Qin, Chuan ^c   Zhang, Lianfeng ^c   Deng, Jingjing ^a,b   Liu, Shubai ^a,b   Qin, Zhihai ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER REGRESSION; CELL INTERACTION; CONTROLLED STUDY; EFFECTOR CELL; FIBROBLAST; IMMUNOCOMPETENT CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STROMA CELL; TUMOR IMMUNITY;

ANIMALS; CELL LINE, TUMOR; CHEMOKINE CXCL12; DOWN-REGULATION; FEMALE; FIBROBLASTS; INTERFERON-GAMMA; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, INTERFERON; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77954233120     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901073     Document Type: Article

References (49)

1. Li, H., X. Fan, and J. Houghton. 2007. Tumor microenvironment: the role of the tumor stroma in cancer. J. Cell Biochem. 101: 805-815.
2. Dvorak, H. F. 1986. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315: 1650-1659.
3. Folkman, J. 1971. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285: 1182-1186.
4. Mueller, M. M., and N. E. Fusenig. 2004. Friends or foes: bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 4: 839-849.
5. Elenbaas, B., and R. A. Weinberg. 2001. Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp. Cell Res. 264: 169-184.
6. Kalluri, R., and M. Zeisberg. 2006. Fibroblasts in cancer. Nat. Rev. Cancer 6: 392-401.
7. Fukumura, D., R. Xavier, T. Sugiura, Y. Chen, E. C. Park, N. Lu, M. Selig, G. Nielsen, T. Taksir, R. K. Jain, and B. Seed. 1998. Tumor induction of VEGF promoter activity in stromal cells. Cell 94: 715-725.
8. Brown, L. F., A. J. Guidi, S. J. Schnitt, L. Van De Water, M. L. Iruela-Arispe, T. K. Yeo, K. Tognazzi, and H. F. Dvorak. 1999. Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin. Cancer Res. 5: 1041-1056.
9. Orimo, A., P. B. Gupta, D. C. Sgroi, F. Arenzana-Seisdedos, T. Delaunay, R. Naeem, V. J. Carey, A. L. Richardson, and R. A. Weinberg. 2005. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121: 335-348.
10. + T cells. Cancer Res. 63: 4095-4100.
11. + T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN γ receptor expression by nonhematopoietic cells. Immunity 12: 677-686.
12. Ibe, S., Z. Qin, T. Schuler, S. Preiss, and T. Blankenstein. 2001. Tumor rejection by disturbing tumor stroma cell interactions. J. Exp. Med. 194: 1549-1559.
13. Li, Z., F. Pradera, T. Kammertoens, B. Li, S. Liu, and Z. Qin. 2007. Cross-talk between T cells and innate immune cells is crucial for IFN-γ-dependent tumor rejection. J. Immunol. 179: 1568-1576.
14. Wu, T. H., C. N. Pabin, Z. Qin, T. Blankenstein, M. Philip, J. Dignam, K. Schreiber, and H. Schreiber. 2004. Long-term suppression of tumor growth by TNF requires a Stat1- and IFN regulatory factor 1-dependent IFN-γ pathway but not IL-12 or IL-18. J. Immunol. 172: 3243-3251.
15. Li, Z., J. Jiang, Z. Wang, J. Zhang, M. Xiao, C. Wang, Y. Lu, and Z. Qin. 2008. Endogenous interleukin-4 promotes tumor development by increasing tumor cell resistance to apoptosis. Cancer Res. 68: 8687-8694.
16. Blankenstein, T. 2005. The role of tumor stroma in the interaction between tumor and immune system. Curr. Opin. Immunol. 17: 180-186.
17. Blankenstein, T., and Z. Qin. 2003. The role of IFN-γ in tumor transplantation immunity and inhibition of chemical carcinogenesis. Curr. Opin. Immunol. 15: 148-154.
18. Valente, G., L. Ozmen, F. Novelli, M. Geuna, G. Palestro, G. Forni, and G. Garotta. 1992. Distribution of interferon-γ receptor in human tissues. Eur. J. Immunol. 22: 2403-2412.
19. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-γ. Annu. Rev. Immunol. 15: 749-795.
20. Ikeda, H., L. J. Old, and R. D. Schreiber. 2002. The roles of IFN γ in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13: 95-109.
21. Takaoka, A., Y. Mitani, H. Suemori, M. Sato, T. Yokochi, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Cross talk between interferon-γ and -α/β signaling components in caveolar membrane domains. Science 288: 2357-2360.
22. Nazareth, M. R., L. Broderick, M. R. Simpson-Abelson, R. J. Kelleher, Jr., S. J. Yokota, and R. B. Bankert. 2007. Characterization of human lung tumor-associated fibroblasts and their ability to modulate the activation of tumor-associated T cells. J. Immunol. 178: 5552-5562.
23. 3 in the disruption of the tumor vasculature induced by TNF and IFN-γ. Nat. Med. 4: 408-414.
24. Oi, V. T., S. L. Morrison, L. A. Herzenberg, and P. Berg. 1983. Immunoglobulin gene expression in transformed lymphoid cells. Proc. Natl. Acad. Sci. USA 80: 825-829.
25. Nanni, P., C. de Giovanni, P. L. Lollini, G. Nicoletti, and G. Prodi. 1983. TS/A: a new metastasizing cell line from a BALB/c spontaneous mammary adenocarcinoma. Clin. Exp. Metastasis 1: 373-380.
26. Asher, A. L., J. J. Mule, A. Kasid, N. P. Restifo, J. C. Salo, C. M. Reichert, G. Jaffe, B. Fendly, M. Kriegler, and S. A. Rosenberg. 1991. Murine tumor cells transduced with the gene for tumor necrosis factor-α: evidence for paracrine immune effects of tumor necrosis factor against tumors. J. Immunol. 146: 3227-3234.
27. Weidner, N. 1995. Current pathologic methods for measuring intratumoral microvessel density within breast carcinoma and other solid tumors. Breast Cancer Res. Treat. 36: 169-180.
28. Drabkin, D. L. 1949. The standardization of hemoglobin measurement. Am. J. Med. Sci. 217: 710.
29. Schurch, W., T. A. Seemayer, and G. Gabbiani. 1998. The myofibroblast: a quarter century after its discovery. Am. J. Surg. Pathol. 22: 141-147.
30. Sugimoto, H., T. M. Mundel, M. W. Kieran, and R. Kalluri. 2006. Identification of fibroblast heterogeneity in the tumor microenvironment. Cancer Biol. Ther. 5: 1640-1646.
31. Grum-Schwensen, B., J. Klingelhofer, C. H. Berg, C. El-Naaman, M. Grigorian, E. Lukanidin, and N. Ambartsumian. 2005. Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res. 65: 3772-3780.
32. Kiaris, H., I. Chatzistamou, G. Trimis, M. Frangou-Plemmenou, A. Pafiti-Kondi, and A. Kalofoutis. 2005. Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer Res. 65: 1627-1630.
33. Vonlaufen, A., S. Joshi, C. Qu, P. A. Phillips, Z. Xu, N. R. Parker, C. S. Toi, R. C. Pirola, J. S. Wilson, D. Goldstein, and M. V. Apte. 2008. Pancreatic stellate cells: partners in crime with pancreatic cancer cells. Cancer Res. 68: 2085-2093.
34. Hwang, R. F., T. Moore, T. Arumugam, V. Ramachandran, K. D. Amos, A. Rivera, B. Ji, D. B. Evans, and C. D. Logsdon. 2008. Cancer-associated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 68: 918-926.
35. Farrar, M. A., and R. D. Schreiber. 1993. The molecular cell biology of interferon-γ and its receptor. Annu. Rev. Immunol. 11: 571-611.
36. Low, S. Q., S. Kitada, and D. A. Lee. 1991. Interferon-γ inhibits collagen synthesis by human Tenon's capsule fibroblasts in vitro. Investig. Ophthalmol. Visual Sci. 32: 2964-2969.
37. Bitterman, P. B., M. D. Wewers, S. I. Rennard, S. Adelberg, and R. G. Crystal. 1986. Modulation of alveolar macrophage-driven fibroblast proliferation by alternative macrophage mediators. J. Clin. Investig. 77: 700-708.
38. Boire, A., L. Covic, A. Agarwal, S. Jacques, S. Sherifi, and A. Kuliopulos. 2005. PAR1 is a matrix metalloprotease-1 receptor that promotes invasion and tumorigenesis of breast cancer cells. Cell 120: 303-313.
39. Stetler-Stevenson, W. G., S. Aznavoorian, and L. A. Liotta. 1993. Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu. Rev. Cell Biol. 9: 541-573.
40. Sternlicht, M. D., A. Lochter, C. J. Sympson, B. Huey, J. P. Rougier, J. W. Gray, D. Pinkel, M. J. Bissell, and Z. Werb. 1999. The stromal proteinase MMP3/ stromelysin-1 promotes mammary carcinogenesis. Cell 98: 137-146.
41. Bristow, R. G., J. Peacock, A. Jang, J. Kim, R. P. Hill, and S. Benchimol. 2003. Resistance to DNA-damaging agents is discordant from experimental metastatic capacity in MEF ras-transformants-expressing gain of function MTp53. Oncogene 22: 2960-2966.
42. Olumi, A. F., G. D. Grossfeld, S. W. Hayward, P. R. Carroll, T. D. Tlsty, and G. R. Cunha. 1999. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 59: 5002-5011.
43. Kuperwasser, C., T. Chavarria, M. Wu, G. Magrane, J. W. Gray, L. Carey, A. Richardson, and R. A. Weinberg. 2004. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl. Acad. Sci. USA 101: 4966-4971.
44. Studebaker, A. W., G. Storci, J. L. Werbeck, P. Sansone, A. K. Sasser, S. Tavolari, T. Huang, M. W. Chan, F. C. Marini, T. J. Rosol, et al. 2008. Fibroblasts isolated from common sites of breast cancer metastasis enhance cancer cell growth rates and invasiveness in an interleukin-6-dependent manner. Cancer Res. 68: 9087-9095.
45. Karnoub, A. E., A. B. Dash, A. P. Vo, A. Sullivan, M. W. Brooks, G. W. Bell, A. L. Richardson, K. Polyak, R. Tubo, and R. A. Weinberg. 2007. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563.
46. Bhowmick, N. A., E. G. Neilson, and H. L. Moses. 2004. Stromal fibroblasts in cancer initiation and progression. Nature 432: 332-337.
47. Schuler, T., S. Kornig, and T. Blankenstein. 2003. Tumor rejection by modulation of tumor stromal fibroblasts. J. Exp. Med. 198: 1487-1493.
48. Studeny, M., F. C. Marini, J. L. Dembinski, C. Zompetta, M. Cabreira-Hansen, B. N. Bekele, R. E. Champlin, and M. Andreeff. 2004. Mesenchymal stem cells: potential precursors for tumor stroma and targeted-delivery vehicles for anticancer agents. J. Natl. Cancer Inst. 96: 1593-1603.
49. Takahashi, K., and S. Yamanaka. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.