The taming of IL-12: Suppressing the production of proinflammatory cytokines

Journal of Leukocyte Biology

Volumn 65, Issue 5, 1999, Pages 543-551

  Sutterwala, Fayyaz S ^a   Mosser, David M ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Lipopolysaccharide; Macrophage; Phagocytes; Receptors; Th1

Indexed keywords

CYTOKINE; INTERLEUKIN 12;

ANIMAL CELL; ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; CELLULAR IMMUNITY; COVALENT BOND; DENDRITIC CELL; EXTRACELLULAR MATRIX; GENETIC TRANSCRIPTION; IMMUNOREGULATION; INFLAMMATION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION;

EID: 0032934002     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.65.5.543     Document Type: Review

References (82)

1. Wolf, S. F., Temple, P. A., Kobayashi, M., Young, D., Dicig, M., Lowe, L., Dzialo, R., Fitz, L., Ferenz, C., Hewick, R. M., Kelleher, K., Herrmann, S. H., Clark, S. C., Azzoni, L., Chan, S. H., Trinchieri, G., Perussia, B. (1991) Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 146, 3074-3081.
2. Gubler, U., Chua, A. O., Schoenhaut, D. S., Dwyer, C. M., McComas, W., Motyka, R., Nabavi, N., Wolitzky, A. G., Quinn, P. M., Familletti, P. C., Gately, M. K. (1991) Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. USA 88, 4143-4147.
3. Kobayashi, M., Fitz, L., Ryan, M., Hewick, R. M., Clark, S. C., Chan, S., Loudon, R., Sherman, F., Perussia, B., Trinchieri, G. (1989) Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biological effects on human lymphocytes. J. Exp. Med. 170, 827-839.
4. D'Andrea, A., Rengaraju, M., Valiante, N. M., Chehimi, J., Kubin, M., Aste, M., Chan, S. H., Kobayashi, M., Young, D., Nickbarg, E., Chizzonite, R., Wolf, S. F., Trinchieri, G. (1992) Production of natural killer cell stimulatory factor (NKSF/IL-12) by peripheral blood mononuclear cells. J. Exp. Med. 176, 1387-1398.
5. + T cells. J. Immunol. 154, 5071-5079.
6. Cassatella, M. A., Meda, L., Gasperini, S., D'Andrea, A., Ma, X., Trinchieri, G. (1995) Interleukin-12 production by human polymorpho-nuclear leukocytes. Eur. J. Immunol. 25, 1-5.
7. Cleveland, M. G., Gorham, J. D., Murphy, T. L., Tuomanen, E., Murphy, K. M. (1996) Lipoteichoic acid preparations of gram-positive bacteria induce interleukin-12 through a CD14-dependent pathway. Infect. Immun. 64, 1906-1912.
8. Oswald, I. P., Dozois, C. M., Petit, J. F., Lemaire, G. (1997) Interleukin-12 synthesis is a required step in trehalose dimycolate-induced activation of mouse peritoneal macrophages. Infect. Immun. 65, 1364-1369.
9. Camargo, M. M., Almeida, I. C., Pereira, M. E., Ferguson, M. A., Travassos, L. R., Gazzinelli, R. T. (1997) Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes initiate the synthesis of proinflammatory cytokines by macrophages. J. Ilmmunol. 158, 5890-5901.
10. Grunvald, E., Chiaramonte, M., Hieny, S., Wysocka, M., Trinchieri, G., Vogel, S. N., Gazzinelli, R. T., Sher, A. (1996) Biochemical characterization and protein kinase C dependency of monokine-inducing activities of Toxoplasma gondii. Infect. Immun. 64, 2010-2018.
11. Skeiky, Y. A., Guderian, J. A., Benson, D. R., Bacelar, O., Carvalho, E. M., Kubin, M., Badaro, R., Trinchieri, G., Reed, S. G. (1995) A recombinant Leishmania antigen that stimulates human peripheral blood mononuclear cells to express a Th1-type cytokine profile and to produce interleukin-12. J. Exp. Med. 181, 1527-1537.
12. Sato, Y., Roman, M., Tighe, H., Lee, D., Corr, M., Nguyen, M. D., Silverman, G. J., Lotz, M., Carson, D. A., Raz, E. (1996) Immunostimulatory DNA sequences necessary for effective intradermal gene immunization. Science 273, 352-354.
13. Hodge-Dufour, J., Noble, P. W., Horton, M. R., Bao, C., Wysoka, M., Burdick, M. D., Stricter, R. M., Trinchieri, G., Puré, E. (1997) Induction of IL-12 and chemokines by hyaluronan requires adhesion-dependent priming of resident but not elicited macrophages. J. Immunol. 159, 2492-2500.
14. Shu, U., Kiniwa, M., Wu, C. Y., Maliszewski, C., Vezzio, N., Hakimi, J., Gately, M., Delespesse, G. (1995) Activated T cells induce interleukin-12 production by monocytes via CD40-CD40 ligand interaction. Eur. J. Ilmmunol. 25, 1125-1128.
15. Koch, F., Stanzl, U., Jennewein, P., Janke, K., Heufler, C., Kampgen, E., Romani, N., Schuler, G. (1996) High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J. Exp. Med. 184, 741-746.
16. Cella, M., Scheidegger, D., Palmer-Lehmann, K., Lane, P., Lanzavecchia, A., Alber, G. (1996) Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J. Exp. Med. 184, 747-752.
17. Trinchieri, G., Gerosa, F. (1996) Immunoregulation by interleukin-12. J. Leukoc. Biol. 59, 505-511.
18. + T cells through IL-12 produced by Listeria-induced macrophages. Science 260, 547-549.
19. Manetti, R., Parronchi, P., Giudizi, M. G., Piccini, M.-P., Maggi, E., Trinchieri, G., Romagnani, S. (1993) Natural killer cell stimulatory factor (NKSF/IL-12) induces Th1-type specific immune responses and inhibits the development of IL-4 producing Th cells. J. Exp. Med. 177, 1199-1204.
20. Magram, J., Connaughton, S. E., Warrier, R. R., Carvajal, D. M., Wu, C. Y., Ferrante, J., Stewart, C., Sarmiento, U., Faherty, D. A., Gately, M. K. (1996) IL-12-deficient mice are defective in IFN-γ production and type 1 cytokine responses. Immunity 4, 471-481.
21. Chan, S. H., Perussia, B., Gupta, J. W., Kobayashi, M., Pospisil, M., Young, H. A., Wolf, S. F., Young, D., Clark, S. C., Trinchieri, G. (1991) Induction of IFN-γ production by natural killer cell stimulatory factor (NKSF): characterization of the responder cells and synergy with other inducers. J. Exp. Med. 173, 869-879.
22. Heinzel, F. P., Schoenhaut, D. S., Rerko, R. M., Rosser, L. E., Gately, M. K. (1993) Recombinant interleukin-12 cures mice infected with Leishmania major. J. Exp. Med. 177, 1505-1512.
23. Sypek, J. P., Chung, C. L., Mayor, S. E. H., Subramanyam, J. M., Goldman, S. J., Sieburth, D. S., Wolf, S. F., Schaub, R. G. (1993) Resolution of cutaneous leishmaniasis: interleukin-12 initiates a protective T helper type 1 immune response. J. Exp. Med. 177, 1797-1802.
24. Cooper, A. M., Roberts, A. D., Rhoades, E. R., Callahan, J. E., Getzy, D. M., Orme, I. M. (1995) The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 84, 423-432.
25. Gazzinelli, R. T., Wysocka, M., Hayasi, S., Denkers, E. Y., Hieny, S., Caspar, P., Trinchieri, G., Sher, A. (1994) Parasite-induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol. 153, 2533-2543.
26. Mattner, F., Magram, J., Ferrante, J., Launois, P., Dipadova, K., Behin, R., Gately, M. K., Louis, J. A., Alber, G. (1996) Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur. J. Immunol. 26, 1553-1559.
27. Scharton-Kerston, T., Afonso, L. C. C., Wysocka, M., Trinchieri, G., Scott, P. (1995) Interleukin-12 is required for natural killer cell activation and subsequent T helper 1 cell development in experimental leishmaniasis. J. Immunol. 154, 5320-5330.
28. Tripp, C. S., Gately, M. K., Hakimi, J., Ling, P., Unanue, E. R. (1994) Neutralization of IL-12 decreases resistance to Listeria in SCID and C.B-17 mice. Reversal by interferon-γ. J. Immunol. 152, 1883-1887.
29. Afonso, L. C., Scharton, T. M., Vieira, L. Q., Wysocka, M., Trinchieri, G., Scott, P. (1994) The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science 263, 235-237.
30. Wysocka, M., Marek, M., Vieira, L. Q., Ozmen, L., Garotta, G., Scott, P., Trinchieri, G. (1995) Interleukin-12 is required for interferon-γ production and lethality in lipopolysaccharide-induced shock in mice. Eur. J. Immunol. 25, 672-676.
31. Trembleau, S., Penna, G., Bosi, E., Mortara, A., Gately, M. K., Adorini, L. (1995) Interleukin-12 administration induces T helper type 1 cells and accelerates autoimmune diabetes in NOD mice. J. Exp. Med. 181, 817-821.
32. Leonard, J. P., Waldburger, K. E., Goldman, S. J. (1995) Prevention of experimental autoimmune encephalomyelitis by antibodies against interleukin-12. J. Exp. Med. 181, 381-386.
33. Germann, T., Szeliga, J., Hess, H., Storkel, S., Podlaski, F. J., Gately, M. K., Schmitt, E., Rude, E. (1995) Administration of interleukin 12 in combination with type II collagen induces severe arthritis in DBA/1 mice. Proc. Natl. Acad. Sci. USA. 92, 4823-1827.
34. Ma, X., Neurath, M., Gri, G., Trinchieri, G. (1997) Identification and characterization of a novel Ets-2-related nuclear complex implicated in the activation of the human interleukin-12 p40 gene promoter. J. Biol. Chem. 272, 10389-10395.
35. Murphy, T. L., Cleveland, M. G., Kulesza, P., Magram, J., Murphy, K. M. (1995) Regulation of interleukin 12 p40 expression through an NF-κB half-site. Mol. Cell Biol. 15, 5258-5267.
36. Gri, G., Savio, D., Trinchieri, G., Ma, X. (1998) Synergistic regulation of the human interleukin-12 p40 promoter by NFκB and Ets transcription factors in Epstein-Barr virus-transformed B cells and macrophages. J. Biol. Chem. 273, 6431-6438.
37. Plevy, S. E., Gemberling, J. H., Hsu, S., Dorner, A. J., Smale, S. T. (1997) Multiple control elements mediate activation of the murine and human interleukin 12 p40 promoters: evidence of functional synergy between C/EBP and Rel proteins. Mol. Cell. Biol. 17, 4572-4588.
38. Hayes, M. P., Wang, J., Norcross, M. A. (1995) Regulation of interleukin-12 expression in human monocytes: selective priming by IFN-γ of LPS inducible p35 and p40 genes. Blood 86, 646-650.
39. Snijders, A., Hilkens, C. M., van der Pouw Kraan, T. C., Engel, M., Aarden, L. A., Kapsenberg, M. L. (1996) Regulation of bioactive IL-12 production in lipopolysaccharide-stimulated human monocytes is determined by the expression of the p35 subunit. J. Immunol. 156, 1207-1212.
40. Hayes, M. P., Murphy, F. J., Burd, P. R. (1998) Interferon-γ-dependent inducible expression of the human IL-12 p35 gene in monocytes initiates from a TATA-containing promoter distinct from the CpG-rich promoter active in Epstein-Barr virus-transformed lymphoblastoid cells. Blood 91, 4645-4651.
41. Tone, Y., Thompson, A., Babik, J. M., Nolan, K. F., Tone, M., Raven, C., Waldmann, H. (1996) Structure and chromosomal location of the mouse interleukin 12 p35 and p40 subunit genes. Eur. J. Immunol. 26, 1222-1227.
42. Yashimoto, T., Kojima, K., Funakoshi, T., Endo, Y., Fujita, T., Nariuchi, H. (1996) Molecular cloning and characterization of murine IL-12 genes. J. Immunol. 156, 1082-1088.
43. Ma, X., Chow, J. M., Gri, G., Carra, G., Gerosa, F., Wolf, S. F., Dzialo, R., Trinchieri, G. (1996) The interleukin-12 p40 gene promoter is primed by interferon-γ in monocytic cells. J. Exp. Med. 183, 147-157.
44. Munder, M., Mallo, M., Eichmann, K., Modolell, M. (1998) Murine macrophages secrete interferon γ upon combined stimulation with interleukin (IL)-12 and IL-18: a novel pathway of autocrine macrophage activation. J. Exp. Med. 187, 2103-2108.
45. Carrera, L., Gazzinelli, R. T., Badolato, R., Hieny, S., Muller, W., Kuhn, R., Sacks, D. L. (1996) Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J. Exp. Med. 183, 515-526.
46. Belkaid, Y., Butcher, B., Sacks, D. L. (1998) Analysis of cytokine production by inflammatory mouse macrophages at the single-cell level: selective impairment of IL-12 induction in Leishmania-infected cells. Eur. J. Immunol. 28, 1389-1400.
47. Weinheber, N., Wolfram, M., Harbecke, D., Aebischer, T. (1998) Phagocytosis of Leishmania mexicana amastigotes by macrophages leads to a sustained suppression of IL-12 production. Eur. J. Immunol. 28, 2467-2477.
48. Karp, C. L., Wysocka, M., Wahl, L. M., Ahearn, J. M., Cuomo, P. J., Sherry, B., Trinchieri, G., Griffin, D. E. (1996) Mechanism of suppression of cell-mediated immunity by measles virus. Science 273, 228-231.
49. Chehimi, J., Starr, S. E., Frank, I., D'Andrea, A., Ma, X., MacGregor, R. R., Sennelier, J., Trinchieri, G. (1994) Impaired interleukin 12 production in human immunodeficiency virus-infected patients. J. Exp. Med. 179, 1361-1366.
50. Chougnet, C., Wynn, T. A., Clerici, M., Landay, A. L., Kessler, H. A., Rusnak, J., Melcher, G. P., Sher, A., Shearer, G. M. (1996) Molecular analysis of decreased interleukin-12 production in persons infected with human immunodeficiency virus. J. Infect. Dis. 174, 46-53.
51. + T cells during the initiation of infection. J. Exp. Med. 179, 447-456.
52. Mosser, D. M., Springer, T. S., Diamond, M. S. (1992) Leishmania promastigotes require opsonic complement to bind to the human leukocyte integrin Mac-1 (CD11b/CD18). J. Cell Biol. 116, 511-520.
53. Tamashiro, V. G., Perez, H. H., Griffin, D. E. (1987) Prospective study of the magnitude and duration of changes in tuberculin reactivity during uncomplicated and complicated measles. Pediatr. Infect. Dis. J. 6, 451-454.
54. Clerici, M., Shearer, G. M. (1993) A TH1 → TH2 switch is a critical step in the etiology of HIV infection. Immunol. Today 14, 107-111.
55. Stoiber, H., Clivio, A., Dierich, M. P. (1997) Role of complement in HIV infection. Annu. Rev. Immunol. 15, 649-674.
56. Gazzinelli, R. T., Bala, S., Stevens, R., Baseler, M., Wahl, L., Kovacs, J., Sher, A. (1995) HIV infection suppresses Type 1 lymphokine and IL-12 responses to Toxoplasma gondii but fails to inhibit the synthesis of other parasite-induced monokines. J. Immunol. 155, 1565-1574.
57. Sutterwala, F. S., Noel, G. J., Clynes, R., Mosser, D. M. (1997) Selective suppression of IL-12 induction after macrophage receptor ligation. J. Exp. Med. 185, 1977-1985.
58. Marth, T., Kelsall, B. L. (1997) Regulation of interleukin-12 by complement receptor 3 signaling. J. Exp. Med. 185, 1987-1995.
59. Feldman, G. M., Chuang, E. J., Finbloom, D. S. (1995) IgG immune complexes inhibit IFN-γ-induced transcription of the FcγRI gene in human monocytes by preventing the tyrosine phosphorylation of the p91 (Stat1) transcription factor. J. Immunol. 154, 318-325.
60. 2+ response amplitude and duration. Nature 386, 855-858.
61. 2 agonists prevent Th1 development by selective inhibition of interleukin-12. J. Clin. Invest. 100, 1513-1519.
62. 2 is a potent inhibitor of human IL-12 production. J. Exp. Med. 181, 775-779.
63. Sutterwala, F. S., Noel, G. J., Salgame, P., Mosser, D. M. (1998) Reversal of proinflammatory responses by ligating the macrophage FcγRI. J. Exp. Med. 188, 217-222.
64. Berger, S., Chandra, R., Ballo, H., Hildenbrand, R., Stutte, H. J. (1997) Immune complexes are potent inhibitors of interleukin-12 secretion by human monocytes. Eur. J. Immunol. 27, 2994-3000.
65. Gavin, A. I., Barnes, N., Dijstelbloem, H. M., Hogarth, P. M. (1998) Identification of the mouse IgG3 receptor: implications for antibody effector functions at the interface between innate and acquired immunity. J. Immunol. 160, 20-23.
66. Heijnen, I. A. F., van Vugt, M. J., Fanger, N. A., Graziano, R. F., de Wit, T. P. M., Hofhuis, F. M. A., Guyre, P. M., Capel, P. J. A., Verbeek, J. S., van de Winkle, J. G. (1996) Antigen targeting to myeloid-specific human FcγRI/CD64 triggers enhanced antibody responses in transgenic mice. J. Clin. Invest. 97, 331-338.
67. Tripp, C. S., Beckerman, K. P., Unanue, E. R. (1995) Immune complexes inhibit antimicrobial responses through interleukin-10 production: effects in severe combined immunodeficient mice during Listeria infection. J. Clin. Invest. 95, 1628-1634.
68. Esparza, I., Green, R., Schreiber, R. D. (1983) Inhibition of macrophage tumoricidal activity by immune complexes and altered erythrocytes. J. Immunol. 131, 2117-2121.
69. Virgin, H. W., Kurt-Jones, E. A., Wittenberg, G. F., Unanue, E. R. (1985) Immune complex effects on murine macrophages: II. Immune complex effects on activated macrophages cytotoxicity, membrane IL-1 and antigen presentation. J. Immunol. 135, 3744-3749.
70. Harrison, T. S., Levitz, S. M. (1996) Role of IL-12 in peripheral blood mononuclear cell responses to fungi in persons with and without HIV infection. J. Immunol. 156, 4492-4497.
71. Zhou, P., Sieve, M. C., Bennett, J., Kwon-Chung, K. J., Tewari, R. P., Gazzinelli, R. T., Sher, A., Seder, R. A. (1995) IL-12 prevents mortality in mice infected with Histoplasma capsulatum through the induction of IFN-γ. J. Immunol. 155, 785-799.
72. 3: involvment of NFκB downregulation in transcriptional repression of the p40 gene. J. Clin. Invest. 101, 252-262.
73. + lymphocytes. J. Immunol. 158, 5589-5595.
74. Visser, J., van Boxel-Dezaire, A., Methorst, D., Brunt, T., de Kloet, E. R., Nagelkerken, L. (1998) Differential regulation of interleukin-10 (IL-10) and IL-12 by glucocorticoids in vitro. Blood 91, 4255-4264.
75. Cousens, L. P., Orange, J. S., Su, H. C., Biron, C. A. (1997) Interferon-α/β inhibition of interleukin 12 and interferon-γ production in vitro and endogenously during viral infection. Proc. Natl. Acad. Sci. USA. 94, 634-639.
76. McRae, B. L., Semnani, R. T., Hayes, M. P., van Seventer, G. A. (1998) Type I IFNs inhibit human dendritic cell IL-12 production and Th1 cell development. J. Immunol. 160, 4298-4304.
77. Maksymowych, W. P., Avina-Zubieta, A., Luong, M. H., Russell, A. S. (1995) An open study of pentoxifylline in the treatment of severe refractory rheumatoid arthritis. J. Rheumatol. 22, 625-629.
78. Rieckmann, P., Weber, F., Gunther, A., Martin, S., Bitsch, A., Broocks, A., Kitze, B., Weber, T., Borner, T., Poser, S. (1996) Pentoxifylline, a phosphodiesterase inhibitor, induces immune deviation in patients with multiple sclerosis. J. Neuroimmunol. 64, 193-200.
79. Moller, D. R., Wysocka, M., Greenlee, B. M., Ma, X., Wahl, L., Trinchieri, G., Karp, C. L. (1997) Inhibition of human interleukin-12 production by pentoxifylline. Immunology 91, 197-203.
80. Moller, D. R., Wysocka, M., Greenlee, B. M., Ma, X., Wahl, L., Flockhart, D. A., Trinchieri, G., Karp, C. L. (1997) Inhibition of IL-12 production by thalidomide. J. Immunol. 159, 5157-5161.
81. Ballow, M. (1997) Mechanisms of action of intravenous immune serum globulin in autoimmune and inflammatory diseases. J. Allergy Clin. Immunol. 100, 151-157.
82. Andersson, J., Skansen-Saphir, U., Sparrelid, E., Andersson, U. (1996) Intravenous immune globulin affects cytokine production in T lymphocytes and monocytes/macrophages. Clin. Exp. Immunol. 104, S10-S20.