An essential role of Th1 responses and interferon gamma in infection-mediated suppression of neoplastic growth

Cancer Biology and Therapy

Volumn 2, Issue 6, 2003, Pages 687-693

  Rankin, Erinn B ^a   Yu, Duonan ^a   Jiang, Jiu ^a   Shen, Hao ^a   Pearce, Edward J ^a   Goldschmidt, Michael H ^a   Levy, David E ^b   Golovkina, Tatyana V ^c   Hunter, Christopher A ^a   Thomas Tikhonenko, Andrei ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

Angiogenesis; Infection; Interferons; Melanoma

Indexed keywords

COLLAGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; LAMININ; MATRIGEL; PROTEOGLYCAN; VASCULOTROPIN A;

ACUTE DISEASE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BLOOD; C57BL MOUSE; CELL CLONE; CELL TRANSPLANTATION; COMPARATIVE STUDY; CULTURE MEDIUM; DRUG COMBINATION; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; INFECTION; LISTERIA MONOCYTOGENES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; METABOLISM; MOUSE; MOUSE MUTANT; NEOVASCULARIZATION (PATHOLOGY); PATHOGENICITY; PATHOLOGY; TH1 CELL; TIME; TOXOPLASMA; TOXOPLASMOSIS; TUMOR CELL LINE;

ACUTE DISEASE; ANIMALS; CELL LINE, TUMOR; CELL TRANSPLANTATION; CLONE CELLS; COLLAGEN; CULTURE MEDIA, CONDITIONED; CYTOKINES; DRUG COMBINATIONS; INFECTION; INTERFERON TYPE II; INTERLEUKIN-10; LAMININ; LISTERIA MONOCYTOGENES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; PROTEOGLYCANS; TH1 CELLS; TIME FACTORS; TOXOPLASMA; TOXOPLASMOSIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 4444340034     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.2.6.557     Document Type: Article

References (81)

1. Epstein MA, Achong BG, Barr YM. Virus particles in cultured lymphoblasts from Burkitt's lymphoma. Lancet 1964; 1:702.
2. zur Hauzen H. Human Papillomaviruses and Their Possible Role in Squamous-Cell Carcinomas. Curr Top Microbiol Immunol 1977:1-30.
3. Peek RM, Jr., Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2002; 2:28-37. (Pubitemid 37328805)
4. Badawi AF. Molecular and genetic events in schistosomiasis-associated human bladder cancer: Role of oncogenes and tumor suppressor genes. Cancer Lett 1996; 105:123-138. (Pubitemid 26252584)
5. Cohen JI, Wang F, Mannick J, Kieff E. Epstein-Barr virus nuclear protein-2 is a key determinant of lymphocyte transformation. Proc Natl Acad Sci USA 1989; 86:9558-9562. (Pubitemid 20010466)
6. Buendia MA. Hepatitis B viruses and hepatocellular carcinoma. Adv Cancer Res 1992; 59:167-226.
7. Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893 classical article. Clin Orthopaedics & Related Res 1991; 262:3-11.
8. Hibbs JBJr, Lambert LHJr, Remington JS. Resistance to murine tumors conferred by chronic infection with intracellular protozoa, Toxoplasma gondii and Besnoitia jellisoni. J Infect Dis 1971; 124:587-592.
9. North RJ, Kirstein DP. T-cell-mediated concomitant immunity to syngeneic tumors. I. Activated macrophages as the expressors of nonspecific immunity to unrelated tumors and bacterial parasites. J Exp Med 1977; 145:275-292.
10. Youdim S, Sharman M. Resistance to tumor growth mediated by Listeria monocytogenes: Collaborative and suppressive macrophage-lymphocyte interactions in vitro. J Immunol 1976; 117:1860-1865.
11. Keller R, Keist R, Leist TP, van der Meide PH. Resistance to a non-immunogenic tumor, induced by Corynebacterium parvum or Listeria monocytogenes, is abrogated by antiinterferon gamma. Int J Cancer 1990; 46:687-690. (Pubitemid 20355761)
12. Thomas-Tikhonenko A, Hunter CA. Infection and cancer: the common vein. Cytokine Growth Factor Rev 2003; 14:67-77.
13. Chakrabarty AM. Microorganisms and cancer: Quest for a therapy. J Bacteriol 2003; 185:2683-2686.
14. Alexandroff AB, Jackson AM, O'Donnell MA, James K. BCG immunotherapy of bladder cancer: 20 years on. Lancet 1999; 353:1689-1694. (Pubitemid 29224536)
15. Sacks D, Sher A. Evasion of innate immunity by parasitic protozoa. Nat Immunol 2002; 3:1041-1047. (Pubitemid 35363655)
16. Hibbs JBJr, Lambert LHJr, Remington JS. Control of carcinogenesis: A possible role for the activated macrophage. Science 1972; 177:998-1000.
17. Hibbs JBJr, Lambert LHJr, Remington JS. Possible role of macrophage mediated nonspecific cytotoxicity in tumour resistance. Nature New Biology 1972; 235:48-50.
18. Hibbs JBJr. Infection and nitric oxide. J Infect Dis. 2002; 185:S9-S17.
19. Hunter CA, Reichmann G. Immunology of toxoplasma infection. In: Joynson DHM, Wreghitt TG, eds. Toxoplasmosis. A comprehensive clinical guide. Cambridge: Cambridge University Press; 2002:43-57.
20. Hunter CA, Yu D, Gee M et al. Cutting edge: Systemic inhibition of angiogenesis underlies resistance to tumors during acute toxoplasmosis. J Immunol 2001; 166:5878-5881. (Pubitemid 32440710)
21. MacDougall JR, Croy BA, Chapeau C, Clark DA. Demonstration of a splenic cytotoxic effector cell in mice of genotype SCID/SCID.BG/BG. Cell Immunol 1990; 130:106-117. (Pubitemid 20329269)
22. Laubach VE, Shesely EG, Smithies O, Sherman PA. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci USA 1995; 92:10688-10692.
23. Kagi D, Ledermann B, Burki K et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994; 369:31-37. (Pubitemid 24144352)
24. Yamada T, Goto M, Punj V et al. Bacterial redox protein azurin, tumor suppressor protein p53, and regression of cancer. Proc Natl Acad Sci USA 2002; 99:14098-14103. (Pubitemid 35257631)
25. Liekens S, De Clercq E, Neyts J. Angiogenesis: regulators and clinical applications. Biochem Pharmacol 2001; 61:253-270.
26. Pepper MS, Mandriota SJ, Vassalli JD, Orci L, Montesano R. Angiogenesis-regulating cytokines: Activities and interactions. Curr Top Microbiol Immunol 1996; 213:31-67.
27. Fidler IJ. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975; 35:218-224.
28. Goldman LA, Cutrone EC, Kotenko SV, Krause CD, Langer JA. Modifications of vectors pEF-BOS, pcDNA1 and pcDNA3 result in improved convenience and expression. Biotechniques 1996;21:1013-1015. (Pubitemid 26422004)
29. Dalton DK, Pitts-Meek S, Keshav S et al. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 1993; 259:1739-1742. (Pubitemid 23114658)
30. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10- deficient mice develop chronic enterocolitis. Cell 1993; 75:263-274. (Pubitemid 23320290)
31. Marino MW, Dunn A, Grail D et al. Characterization of tumor necrosis factor-deficient mice. Proc Natl Acad Sci USA 1997; 94:8093-8098. (Pubitemid 27343782)
32. Durbin JE, Hackenmiller R, Simon MC, Levy DE. Targeted disruption of the mouse STAT1 results in compromised innate immunity to viral disease. Cell 1996; 84:443-450. (Pubitemid 26058569)
33. Murali-Krishna K, Altman JD, Suresh M et al. Counting antigen-specific CD8 T cells: A reevaluation of bystander activation during viral infection. Immunity 1998; 8:177-187. (Pubitemid 28123745)
34. Spence PM, Sriram V, Van Kaer L, Hobbs JA, Brutkiewicz RR. Generation of cellular immunity to lymphocytic choriomeningitis virus is independent of CD1d1 expression. Immunology 2001; 104:168-174. (Pubitemid 32989518)
35. Grzych JM, Pearce E, Cheever A et al. Egg deposition is the major stimulus for the production of Th2 cytokines in murine schistosomiasis mansoni. J Immunol 1991; 146:1322-7.
36. Ngo C, Gee MS, Akhtar N et al. An in vivo function for the transforming myc protein: Elicitation of the angiogenic phenotype. Cell Growth Differ 2000; 11:201-10. (Pubitemid 30211009)
37. Sevignani C, Wlodarski P, Kirillova J et al. Tumorigenic conversion of p53-deficient colon epithelial cells by an activated Ki-ras gene. J Clinical Inv 1998; 101:1572-80. (Pubitemid 28198485)
38. Zinkernagel RM, Planz O, Ehl S et al. General and specific immunosuppression caused by antiviral T-cell responses. Immunol Rev 1999; 168:305-15. (Pubitemid 29276690)
39. Matloubian M, Concepcion RJ, Ahmed R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J Virol 1994; 68:8056-63. (Pubitemid 24362694)
40. Zajac AJ, Blattman JN, Murali-Krishna K et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med 1998; 188:2205-13. (Pubitemid 29028493)
41. Hoffmann KF, Wynn TA, Dunne DW. Cytokine-mediated host responses during schistosome infections: Walking the fine line between immunological control and immunopathology. Adv Parasitol 2002; 52:265-307. (Pubitemid 36069926)
42. Pearce EJ, MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol 2002; 2:499-511.
43. Pearce EJ, Caspar P, Grzych JM, Lewis FA, Sher A. Downregulation of Th1 cytokine production accompanies induction of Th2 responses by a parasitic helminth, Schistosoma mansoni. J Exp Med 1991; 173:159-66.
44. La Flamme AC. Patton EA, Pearce EJ. Role of gamma interferon in the pathogenesis of severe schistosomiasis in interleukin-4-deficient mice. Infect Immun 2001; 69:7445-52. (Pubitemid 33086569)
45. Wynn TA, Eltoum I, Cheever AW, et al. Analysis of cytokine mRNA expression during primary granuloma formation induced by eggs of Schistosoma mansoni. J Immunol 1993; 151:1430-1440. (Pubitemid 23219280)
46. Kotenko SV. The family of IL-10-related cytokines and their receptors: related, but to what extent? Cytokine Growth Factor Rev 2002; 13:223-240. (Pubitemid 34693176)
47. Neyer LE, Grunig G, Fort M et al. Role of interleukin-10 in regulation of T-cell-dependent and T-cell-independent mechanisms of resistance to Toxoplasma gondii. Infect Immun 1997; 65:1675-1682. (Pubitemid 27193585)
48. Huang S, Xie K, Bucana CD, Ullrich SE, Bar-Eli M. Interleukin 10 suppresses tumor growth and metastasis of human melanoma cells: potential inhibition of angiogenesis. Clin Cancer Res 1996; 2:1969-1979. (Pubitemid 27006629)
49. Cervenak L, Morbidelli L, Donati D et al. Abolished angiogenicity and tumorigenicity of Burkitt lymphoma by interleukin-10. Blood 2000; 96:2568.
50. Silvestre JS, Mallat Z, Duriez M et al. Antiangiogenic effect of interleukin-10 in ischemia-induced angiogenesis in mice hindlimb. Circ Res 2000; 87:448-452.
51. Kerbel RS, Folkman J. Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2002; 2:727-739.
52. Schindler C. Cytokines and JAK-STAT signaling. Exp Cell Res 1999; 253:7-14.
53. Meraz MA, White JM, Sheehan KC et al. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996; 84:431-442. (Pubitemid 26058568)
54. Gresser I, Belardelli F. Endogenous type I interferons as a defense against tumors. Cytokine Growth Factor Rev 2002; 13:111-118. (Pubitemid 34229386)
55. Ramana CV, Gil MP, Schreiber RD, Stark GR. Stat1-dependent and -independent pathways in IFN-γ-dependent signaling. Trends Immunol 2002; 23:96-101. (Pubitemid 34310151)
56. Passaniti A, Taylor RM, Pili R et al. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest 1992; 67:519-528.
57. Auerbach R, Akhtar N, Lewis RL, Shinners BL. Angiogenesis assays: Problems and pitfalls. Cancer & Metastasis Rev 2000; 19:167-172.
58. Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. NEJM 1991; 324:1-8.
59. Burnet FM. Concept of immunological surveillance. Prog Exp Tumor Res 1970; 13:1-27.
60. Pantelouris EM. Absence of thymus in a mouse mutant. Nature 1968; 217:370-371.
61. Stutman O. Immunodepression and malignancy. Adv Cancer Res 1975; 22:261-422.
62. Bosma GC, Custer RP, Bosma MJ. A severe combined immunodeficiency mutation in the mouse. Nature 1983; 301:527-530. (Pubitemid 13160576)
63. Engel AM, Svane IM, Rygaard J, Werdelin O. MCA sarcomas induced in scid mice are more immunogenic than MCA sarcomas induced in congenic, immunocompetent mice. Scand J Immunol 1997; 45:463-470. (Pubitemid 27198705)
64. Dighe AS, Richards E, Old LJ, Schreiber RD. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1994; 1:447-456.
65. Kaplan DH, Shankaran V, Dighe AS et al. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA 1998; 95:7556-7561. (Pubitemid 28293291)
66. Shankaran V, Ikeda H, Bruce AT et al. IFN gamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001; 410:1107-1111. (Pubitemid 32391043)
67. Street SE, Trapani JA, MacGregor D, Smyth MJ. Suppression of lymphoma and epithelial malignancies effected by interferon gamma. J Exp Med 2002; 196:129-134. (Pubitemid 34747318)
68. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Ann Rev Biochem 1998; 67:227-264.
69. Dunn GP, Bruce AT, Ikeda H, Old LJ, Schreiber RD. Cancer immunoediting: from immunosurveillance to tumor escape. Nat Immunol 2002; 3:991-998. (Pubitemid 35363648)
70. Friesel R, Komoriya A, Maciag T. Inhibition of endothelial cell proliferation by gamma-interferon. J Cell Biol 1987; 104:689-696. (Pubitemid 17024724)
71. Norioka K, Borden EC, Auerbach R. Inhibitory effects of cytokines on vascular endothelial cells: synergistic interactions among interferon-gamma, tumor necrosis factor-alpha, and interleukin-1. J Immunotherapy 1992; 12:13-18.
72. Strieter RM, Kunkel SL, Arenberg DA, Burdick MD, Polverini PJ. Interferon gamma-inducible protein 10 (IP-10), a member of the C-X-C chemokine family, is an inhibitor of angiogenesis. Biochem Biophys Res Comm 1995; 210:51-57.
73. Angiolillo AL, Sgadari C, Taub DD et al. Human interferon-inducible protein-10 is a potent inhibitor of angiogenesis in vivo. J Exp Med 1995; 182:155-162.
74. Vicari AP, Caux C. Chemokines in cancer. Cytokine & Growth Factor Rev 2002; 13:143-154.
75. Coughlin CM, Salhany KE, Wysocka M et al. Interleukin-12 and interleukin-18 synergistically induce murine tumor regression which involves inhibition of angiogenesis. J Clin Invest 1998; 101:1441-1452. (Pubitemid 28145262)
76. Coughlin CM, Salhany KE, Gee MS et al. Tumor cell responses to IFN-γ affect tumor-igenicity and response to IL-12 therapy and antiangiogenesis. Immunity 1998; 9:25-34. (Pubitemid 28361292)
77. Sgadari C, Angiolillo AL, Tosato G. Inhibition of angiogenesis by interleukin-12 is mediated by the interferon-inducible protein 10. Blood 1996; 87:3877-3882. (Pubitemid 26129617)
78. Voest EE, Kenyon BM, O'Reilly MS et al. Inhibition of angiogenesis in vivo by interleukin 12. J Natl Cancer Inst 1995; 87:581-586.
79. Qin Z, Schwartzkopff J, Pradera F et al. A critical requirement of interferon gamma-mediated angiostasis for tumor rejection by CD8+ T cells. Cancer Res 2003; 63:4095-4100. (Pubitemid 36917932)
80. Yu D, Thomas-Tikhonenko A. Intratumoral delivery of an interferon gamma retrovirus-producing cells inhibits growth of a murine melanoma by a non-immune mechanism. Cancer Lett 2001; 173:145-154. (Pubitemid 32971932)
81. Shirahata T, Mori A, Ishikawa H, Goto H. Strain differences of interferon-generating capacity and resistance in toxoplasma-infected mice. Microbiol & Immunol 1986; 30:1307-1316. (Pubitemid 17004414)