Interferon consensus sequence binding protein-deficient mice display impaired resistance to intracellular infection due to a primary defect in interleukin 12 p40 induction

Journal of Experimental Medicine

Volumn 186, Issue 9, 1997, Pages 1523-1534

  Scharton Kersten, Tanya ^a   Contursi, Cristina ^b   Masumi, Atsuko ^b   Sher, Alan ^a   Ozato, Keiko ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GAMMA INTERFERON; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; INTERLEUKIN 12; MESSENGER RNA; PARASITE ANTIGEN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; IMMUNE DEFICIENCY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ACUTE DISEASE; ANIMALS; CARRIER PROTEINS; CONSENSUS SEQUENCE; FEMALE; IMMUNITY, NATURAL; INTERFERON REGULATORY FACTORS; INTERFERON TYPE II; INTERLEUKIN-12; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REPRESSOR PROTEINS; RNA, MESSENGER; SPLEEN; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0030664056     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.9.1523     Document Type: Article

References (55)

1. Driggers, P.H., D.L. Ennist, S.L. Gleason, W.-H. Mak, M.S. Marks, B.-Z. Levi, J.R. Flanagan, E. Appella, and K. Ozato. 1990. An interferon-γ-regulated protein that binds the interferon-inducible enhancer element of major histocompatibility complex class I genes. Proc. Natl. Acad. Sci. USA. 87: 3743-3747.
2. Miyamoto, M., T. Fujita, Y. Kimura, M. Maruyama, H. Harada, Y. Sudo, T. Miyata, and T. Taniguchi. 1988. Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-β gene regulatory elements. Cell. 54:903-913.
3. Harada, H., T. Fujita, M. Miyamoto, Y. Kimura, M. Maruyama, A. Fuira, T. Miyata, and T. Taniguchi. 1989. Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell. 58:729-739.
4. Veals, S.A., C. Schindler, D. Leonard, X. Fu, R. Aebersold, J.E. Darnell, Jr., and D.E. Levy. 1992. Subunit of-γ-interferon-responsive transcription factor is related to interferon regulatory factor and Myb families of DNA binding proteins. Mol. Cell. Biol. 12:3315-3324.
5. Au, W.C., P.A. Moore, W. Lowther, Y.T. Juang, and P.M. Pitha. 1995. Identification of a member of the interferon regulatory factor family that binds to the interferon-stimulated response element and activates expression of interferon-induced genes. Proc. Natl. Acad. Sci. USA. 92:11657-11661.
6. Eisenbeis, C.F., H. Singh, and U. Storb. 1995. Pip, a novel IRF family member, is a lymphoid-specific, PU.1-dependent transcriptional activator. Genes Dev. 9:1377-1387.
7. Kanno, Y., C.A. Kozak, C. Schindler, P.H. Driggers, D.L. Ennist, S.L. Gleason, J.E. Darnell, and K. Ozato. 1993. The genomic structure of the murine ICSBP reveals the presence of the gamma interferon-responsive element, to which an ISGF3α subunit or similar molecule binds. Mol. Cell. Biol. 13:3951-3963.
8. Nelson, N., Y. Kanno, C. Hong, C. Contursi, T. Fujita, B.J. Fowlkes, E. O'Connell, J. Hu-Li, W.E. Paul, D. Jankovic et al. 1996. Expression of interferon regulatory factor family proteins in lymphocytes. Induction of Stat1 and ICSBP expression by T cell activation. J. Immunol. 156:3711-3720.
9. Politis, A.D., K. Ozato, J.E. Coligan, and S.N. Vogel. 1994. Regulation of induced nuclear expression of IFN consensus sequence binding protein in murine peritoneal macrophages. J. Immunol. 152:2270-2278.
10. Darnell, J.E., Jr., I.M. Kerr, and G.R. Stark. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science (Wash. DC). 14:1415-1421.
11. Levy, D.E., D.J. Lew, T. Decker, D.S. Kessler, and J.E. Darnell, Jr. 1990. Synergistic interaction between interteron-γ and interferon-α through induced synthesis of one subunit of the transcription factor ISGF3. EMBO J. 9:1105-1111.
12. Matsuyama, T., T. Kimura, M. Kitagawa, K. Pfeffer, T. Kawakami, N. Watanabe, T. M. Kündig, R. Amakawa, K. Kishihara, A. Wakeham et al. 1993. Targeted disruption of IRF-1 or IRF-2 results in abnormal type I IFN gene induction and aberrant lymphocyte development. Cell. 75:83-97.
13. Holtschke, T., J. Löhler, Y. Kanno, T. Fehr, N. Giese, R. Rosenbauer, J. Lou, K.-P. Knobeloch, L. Gabriele, J.F. Waring et al. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell. 87:307-317.
14. -/- mice. J. Immunol. 156:636-643.
15. Mittrücker, H.W., T. Matsuyama, A. Grossman, T. Kündig, J. Potter, A. Shahinan, A. Wakeham, B. Patterson, P. Ohashi, and T.W. Mak. 1997. Requirement for the transcription factor LSIRF/IRF4 for mature B and T lymphocyte function. Science (Wash. DC). 275:540-543.
16. Fehr, T., G. Schoedon, B. Odermatt, T. Holtschke, M. Schneemann, M. F. Bachmann, T. W. Mak, I. Horak, and R.M. Zinkernagel. 1997. Crucial role of interferon consensus sequence binding protein, but neither of interferon regulator factor 1 nor of nitric oxide synthesis for protection against murine listeriosis. J. Exp. Med. 183:147-157.
17. Lohoff, M., D. Ferrick, H.-W. Mittrucker, G.S. Duncan, S. Bischof, M. Rollinghoff, and T.W. Mak. 1997. Interferon regulatory factor-1 is required for a T helper 1 immune response in vivo. Immunity. 6:681-689.
18. Taki, S., T. Sato, K. Ogasawara, T. Fukuda, M. Sato, S. Hida, G. Suauki, M. Mitsuyama, E.-H. Shin, S. Kojima, T. Taniguchi, and Y. Asano. 1997. Multistage regulation of Th1-type immune responses by the transcription factor IRF-1. Immunity. 6:673-679.
19. Müller, U., U. Steinhoff, L.F. Reis, S. Hemmi, J. Pavlovic, R.M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science (Wash. DC). 264:1918-1921.
20. Huang, S., W. Hendriks, A. Althage, S. Hemmi, G. Bluethmann, R. Kamijo, J. Vilcek, R. M. Zinkernagel, and M. Aguet. 1993. Immune response in mice that lack the interferon-γ receptor. Science (Wash. DC). 259:1742-1745.
21. Ma, X., M. Aste-Amezaga, and G. Trinchieri. 1996. Regulation of interleukin-12 production. Ann. NY Acad. Sci. 795: 12-25.
22. Trinchieri, G. 1997. Cytokines acting on or secreted by macrophages during intracellular infection (IL-10, IL-12, IFN-γ). Curr. Opin. Immunol. 9:17-23.
23. + T cells occurs through macrophage production of IL-12. Science (Wash. DC). 260:547-549.
24. Manetti, R., F. Gerosa, M.G. Giudizi, R. Biagiotti, P. Parronchi, M.P. Piccinni, S. Sampognaro, E. Maggi, S. Romagnani, and G. Trinchieri. 1994. Interleukin-12 induces stable priming for interferon-γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 cell clones. J. Exp. Med. 179: 1273-1283.
25. Farrar, M.A., and R.D. Schreiber. 1993. The molecular cell biology of interferon-γ and its receptor. Ann. Rev. Immunol. 11:571-611.
26. Ma, X., J. Chow, G. Gri, G. Carra, F. Gerosa, S. Wolf, R. Dzialo, and G. Trinchieri. 1996. The interleukin 12 p40 gene promoter is primed by interferon-γ in monocytic cells. J. Exp. Med. 183:147-157.
27. Scharton-Kersten, T.M., T.A. Wynn, E.Y. Denkers, S. Bala, E. Grunvald, S. Hieny, R.T. Gazzinelli, and A. Sher. 1996. In the absence of endogenous interferon-γ mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J. Immunol. 157:4045-4054.
28. Scharton-Kersten, T., E.Y. Denkers, R. Gazzinelli, and A. Sher. 1996. Role of IL-12 in induction of cell-mediated immunity to Toxoplasma gondii. Res. Immunol. 146:539-545.
29. Subauste, C.S., Remington, J.S. 1991. Role of gamma interferon in Toxoplasma gondii infection. Eur. J. Clin. Microbiol. Infect. Dis. 10:58-67.
30. Magram, J., S.E. Connaughton, R.R. Warrier, D.M. Carvajal, C.-Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D.A. Faherty, and M.K. Gately. 1996. IL-12-deficient mice are defective in IFN-γ production and type I cytokine responses. Immunity. 4:471-481.
31. Dalton, K.K., S. Pitts-Meek, S. Keshav, L.S. Figari, A. Bradley, and T.A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science (Wash. DC). 259:1739-1742.
32. Leiby, D.A., A.H. Fortier, R.M. Crawford, R.D. Schreiber, and C.A. Nacy. 1992. In vivo modulation of the murine response to Francisella tularensis LVS by administration of anti-cytokine antibodies. Infect. Immun. 60:84-89.
33. Powrie, F., S. Menon, and R.L. Coffman. 1993. Interleukin-4 and interleukin-10 synergize to inhibit cell-mediated immunity in vivo. Eur. J. Immunol. 23:3043-3049.
34. Pfefferkorn, E.R., and L.C. Pfefferkorn. 1977. Specific labeling of intracellular Toxoplasma gondii with uracil. J. Protozool. 24:449-453.
35. McLeod, R., and J.S. Remington. 1979. A method to evaluate the capacity of monocytes and macrophages to inhibit multiplication of an intracellular pathogen. J. Immunol. Methods. 27:19-29.
36. Curry, R.C., P.A. Keiner, and G.L. Spitalny. 1987. A sensitive immunochemical assay for biologically active muIFN-γ. J. Immunol. Methods. 104:137-142.
37. Vieira, L.Q., B.D. Hondowicz, L.C. Afonso, M. Wysocka, G. Trinchieri, and P. Scott. 1994. Infection with Leishmania major induces IL-12 production in vivo. Immunol. Lett. 40: 157-161.
38. Gazzinelli, R.T., I. Eltoum, T.A. Wynn, and A. Sher. 1993. Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-α and correlates with the down-regulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J. Immunol. 151:1672-1682.
39. Wang, A.M., and D.F. Mark. 1990. Quantitative PCR. In PCR Protocols. M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White, editors. Academic Press, New York. 70-75.
40. Scharton-Kersten, T.M., G. Yap, J. Magram, and A. Sher. 1997. Inducible nitric oxide is essential for host defense against chronic but not acute infection with the intracellular pathogen, Toxoplasma gondii. J. Exp. Med. 185:1261-1273.
41. Sayles, P.C., and L.L. Johnson. 1997. Exacerbation of Toxoplasmosis in neutrophil depleted mice. Nat. Immunity. In press.
42. Grunvald, E., M. Chiramonte, S. Hieny, M. Wysocka, G. Trinchieri, S.N. Vogel, R.T. Gazzinelli, and A. Sher. 1996. Biochemical characterization and protein kinase C dependency of monokine-inducing activities of Toxoplasma gondii. Infect. Immun. 64:2010-2018.
43. D'Andrea, A., M. Aste-Amezaga, N.M. Valiante, X. Ma, M. Kubin, and G. Trinchieri. 1993. Interleukin-10 (IL-10) inhibits human lymphocyte interferon-γ production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 178: 1041-1048.
44. D'Andrea, A., X. Ma, M. Aste-Amezaga, C. Paganin, and G. Trinchieri. 1995. Stimulatory and inhibitory effects of interleukin (IL)-4 and IL-13 on the production of cytokines by human peripheral blood mononuclear cells: priming for IL-12 and tumor necrosis factor-α production. J. Exp. Med. 181: 537-546.
45. Nathan, C. 1995. Natural resistance and nitric oxide. Cell. 82:873-876.
46. Gollob, J.A., H. Kawasaki, and J. Ritz. 1997. Interferon-γ and interleukin-4 regulate T cell interleukin-12 responsiveness through the differential modulation of high affinity interleukin-12 receptor expression. Eur. J. Immunol. 27:647-652.
47. Murphy, T., M. Cleveland, P. Kulesza, J. Magram, and K. Murphy. 1995. Regulation of interleukin 12 p40 expression through an NF-κB half-site. Mol. Cell. Biol. 15:5258-5267.
48. Flesch, I.E., and S.H. Kaufmann. 1995. Differential induction of IL12 synthesis by Mycobacterium bovis BCG and Listeria monocytes. Res. Immunol. 146:520-526.
49. Screpanti, I., L. Romani, P. Musiani, A. Modesti, L. Fattori, D. Lazzaro, C. Sellitto, S. Scarpa, D. Bellavia, G. Lattanzio et. al. 1995. Lymphoproliferative disorder and imbalanced T-helper response in C/EBPβ-deficient mice. EMBO (Eur. Mol. Biol. Organ.) J. 14:1932-1941.
50. Isshiki, H., S. Akira, O. Tanabe, T. Nakajima, T. Shimamoto, T. Hirano, and T. Kishimoto. 1990. Constitutive and IL-1 inducible factors interact with the IL-1 responsive element in the IL-6 gene. Mol. Cell. Biol. 10:2757-2764.
51. Nelson, N.J., M.S. Marks, P.H. Driggers, and K. Ozato. 1993. ICSBP, a member of the IRF family, suppresses IFN induced gene transcription. Mol. Cell. Biol. 21:1066-1081.
52. Shi, Y., E. Seto, L. Chang, and T. Shenk, 1991. Transriptional repression by YY1, a human GLI-druppel-related protein, and relief of repression by adenovirus E1A protein. Cell. 67:377-388.
53. Tripp, C.S., M.K. Gately, J. Hakimi, P. Ling, and E.R. Unanue. 1994. Neutralization of IL-12 decreases resistance to Listeria in SCID and CB-17 mice: reversal by IFN. J. Immunol. 152:1883-1887.
54. Li, Z-Y., C.L. Manthey, P.Y. Perera, A. Sher, and S.N. Vogel. 1994. Toxoplasma gondii soluble antigen induces a subset of lps-inducible genes and tyrosine phosphoproteins in peritoneal macrophages. Infect. Immun. 62:3434-3440.
55. Reis e Sousa, C., S. Hieny, T. Scharton-Kersten, D. Jankovic, H. Charest, R.N. Germain, and A. Sher. In vivo microbial stimulation induces rapid CD40L-independent production of IL-12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. In press.