Interleukin-12: A bridge between innate resistance and adaptive immunity with a role in infection and acquired immunodeficiency (original) (raw)

References

  1. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, Loudon R, Sherman F, Perussia B, Trinchieri G: Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 170:827–846, 1989
    PubMed Google Scholar
  2. Stern AS, Podlaski FJ, Hulmes JD, Pan YE, Quinn PM, Wolitzky AG, Familletti PC, Stremlo DL, Truitt T, Chizzonite R, Gately MK: Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc Natl Acad Sci USA 87:6808–6812, 1990
    PubMed Google Scholar
  3. Wolf SF, Temple PA, Kobayashi M, Young D, Dicig M, Lowe L, Dzialo R, Fitz L, Ferenz C, Hewick RM, Kelleher K, Herrmann SH, Clark SC, Azzoni L, Chan SH, Trinchieri G, Perussia B: 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, 1991
    PubMed Google Scholar
  4. Gubler U, Chua AO, Schoenhaut DS, Dwyer CM, McComas W, Motyka R, Nabavi N, Wolitzky AG, Quinn PM, Familletti PC, Gately MK: Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc Natl Acad Sci USA 88:4143–4147, 1991
    PubMed Google Scholar
  5. Podlaski FJ, Nanduri VB, Hulmes JD, Pan Y-C E, Levin W, Danho W, Chizzonite R, Gately MK, Stern AS: Molecular characterization of interleukin 12. Arch Biochem Biophys 294:230–237, 1992
    PubMed Google Scholar
  6. Sieburth D, Jabs EW, Warrington JA, Li X, Lasota J, FaForgia S, Kelleher K, Huebner K, Wasmuth JJ, Wolf SF: Assignment of genes encoding a unique cytokine (IL12) composed of two unrelated subunits to chromosomes 3 and 5. Genomics 14:59–62, 1992
    PubMed Google Scholar
  7. Schoenhaut DS, Chau AO, Wolitzky AG, Quinn PM, Dwyer CM, McComas W, Familletti PC, Gately MK, Gubler U: Cloning and expression of murine IL-12. J Immunol 148:3433–3440, 1992
    PubMed Google Scholar
  8. Valiante NM, Rengaraju M, Trinchieri G: Role of the production of natural killer cell stimulatory factor (NKSF/IL-12) in the ability of B cell lines to stimulate T and NK cell proliferation. Cellular Immunology 145:187–198, 1992
    PubMed Google Scholar
  9. D'Andrea A, Rengaraju M, Valiante NM, Chehimi J, Kubin M, Aste-Amezaga M, Chan SH, Kobayashi M, Young D, Nickbarg E, Chizzonite R, Wolf SF, Trinchieri G: Production of natural killer cell stimulatory factor (NKSF/IL-12) by peripheral blood mononuclear cells. J Exp Med 176:1387–1398, 1992
    PubMed Google Scholar
  10. Mattner F, Fischer S, Guckes S, Jin S, Kaulen H, Schmitt E, Rüde E, Germann T: The interleukin-12 subunit p40 specifically inhibits effects of the interleukin-12 heterodimer. Eur J Immunol 23:2202–2208, 1993
    PubMed Google Scholar
  11. Merberg DM, Wolf SF, Clark SC: Sequence similarity between NKSF and the IL-6/G-CSF family. Immunol Today 13:77–78, 1992
    Google Scholar
  12. Gearing DP, Cosman D: Homology of the p40 subunit of Natural Killer cell Stimulatory Factor (NKSF) with the extracellular domain of the interleukin-6 receptor. Cell 66:9–10, 1991
    PubMed Google Scholar
  13. Hibi M, Murakami M, Saito M, Hirano T, Taga T, Kishimoto T: Molecular cloning and expression of an IL-6 signal transducer, gp130. Cell 63:1149–1157, 1990
    PubMed Google Scholar
  14. Davis S, Aldrich TH, Ip NY, Stahl N, Scherer S, Farrugella T, Di Stefano PS, Curtis R, Panayotatos N, Gascan H, Chevalier S, Yancopoulos GD: Released form of CNTF receptor alpha component as a soluble mediator of CNTF responses. Science 259:1736–1739, 1993
    PubMed Google Scholar
  15. Chizzonite R, Truitt T, Desai BB, Nunes P, Podlaski FJ, Stern AS, Gately MK: IL-12 receptor. I. Characterization of the receptor on PHA-activated human lymphoblasts. J Immunol 148:3117–3124, 1992
    PubMed Google Scholar
  16. Desai BB, Quinn PM, Wolitzky AG, Mongini PKA, Chizzonite R, Gately MK: The IL-12 receptor. II. Distribution and regulation of receptor expression. J Immunol 148:3125–3132, 1992
    PubMed Google Scholar
  17. Tripp CS, Wolf SF, Unanue ER: Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc Natl Acad Sci USA 90:3725–3729, 1993
    PubMed Google Scholar
  18. Gazzinelli RT, Hieny S, Wynn TA, Wolf S, Sher A: Interleukin-12 is required for the T-lymphocyte independent induction of interferon-γ by an intracellular parasite and induces resistance in T-deficient hosts. Proc Natl Acad Sci USA 90:6115–6119, 1993
    PubMed Google Scholar
  19. Reiner LS, Zheng S, Wang Z, Stowring L, Locksley RM: Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. J Exp Med 179:447–456, 1994
    PubMed Google Scholar
  20. Kubin M, Chow JM, Trichieri G: Differential regulation of interleukin-12, tumor necrosis factor-α, and interleukin-1β production in human myeloid leukemia cell lines and peripheral blood mononuclear cells. Blood (in press), 1994
  21. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G: Interleukin-10 inhibits human lymphocyte IFN-γ production by suppressing natural killer cell stimulatory factor/interleukin-12 synthesis in accessory cells. J Exp Med 178:1041–1048, 1993
    PubMed Google Scholar
  22. Trinchieri G: Interleukin-12 and its role in the generation of TH1 cells. Immunol Today 14:335–338, 1993
    PubMed Google Scholar
  23. Murphy EE, Terres G, Macatonia SE, Hsieh C, Mattson J, Lanier L, Wysocka M, Trinchieri G, Murphy K, O'Garra A: B7 and IL-12 cooperate for proliferation and IFN-γ production by mouse Th1 clones that are unresponsive to B7 costimulation. J Exp Med (in press), 1994
  24. Ogawa M: Differentiation and proliferation of hematopoietic stem cells. Blood 81:2844–2853, 1993
    PubMed Google Scholar
  25. Jacobsen SE, Veiby OP, Smeland EB: Cytotoxic lymphocyte maturation factor (interleukin 12) is a synergistic growth factor for hematopoietic stem cells. J Exp Med 178:413–418, 1993
    PubMed Google Scholar
  26. Ploemacher RE, van Soest PL, Boudewijn A, Neben S: Interleukin-12 enhances interleukin-3 dependent multilineage hematopoietic colony formation stimulated by interleukin-11 or steel factor. Leukemia 7:1374–1380, 1993
    PubMed Google Scholar
  27. Ploemacher RE, van Soest PL, Voorwinden H, Boudewijn A: Interleukin-12 synergizes with interleukin-3 and steel factor to enhance recovery of murine hemopoietic stem cells in liquid culture. Leukemia 7:1381–1388, 1993
    PubMed Google Scholar
  28. Bellone G, Trinchieri G: Dual stimulatory and inhibitory effects of natural killer cell stimulatory factor (NKSF/IL-12) on human hematopoiesis (submitted for publication), 1994
  29. Chan SH, Perussia B, Gupta JW, Kobayashi M, Pospśil M, Young HA, Wolf SF, Young D, Clark SC, Trinchieri G: Induction of IFN-γ production by NK cell stimulatory factor (NKSF): Characterization of the responder cells and synergy with other inducers. J Exp Med 173:869–879, 1991
    PubMed Google Scholar
  30. Kubin M, Kamoun M, Trinchieri G: Interleukin-12 synergizes with B7/CD28 interaction in inducing efficient proliferation and cytokine production of human T cells. J Exp Med (in press), 1994
  31. Aste-Amezaga M, D'Andrea A, Kubin M, Trinchieri G: Cooperation of natural killer cell stimulatory factor/interleukin-12 with other stimuli in the induction of cytokines and cytotoxic cell-associated molecules in human T and NK cells. Cell Immunol (in press), 1994
  32. Chan SH, Kobayashi M, Santoli D, Perussia B, Trinchieri G: Mechanisms of INF-γ induction by natural killer cell stimulatory factor (NKSF/IL-12): Role of transcription and mRNA stability in the synergistic interaction between NKSF and IL-2. J Immunol 148:92–98, 1992
    PubMed Google Scholar
  33. Valiante NM, Trinchieri G: Identification of a novel signal transduction surface molecule on human cytotoxic lymphocytes. J Exp Med 1978:1397–1406, 1993
    Google Scholar
  34. Naume B, Johnsen A, Espevik T, Sundan A: Gene expression and secretion of cytokines and cytokine receptors from highly purified CD56+ natural killer cells stimulated with interleukin-2, interleukin-7 and interleukin-12. Eur J Immunol 23:1831–1838, 1993
    PubMed Google Scholar
  35. Perussia B, Chan S, D'Andrea A, Tsuji K, Santoli D, Pospisil M, Young D, Wolf S, Trinchieri G: Natural killer cell stimulatory factor or IL-12 has differential effects on the proliferation of TCRαβ+, TCRγδ+ T lymphocytes and NK cells. J Immunol 149:3495–3502, 1992
    PubMed Google Scholar
  36. Chehimi J, Starr S, Frank I, Rengaraju M, Jackson SJ, Lianes C, Kobayashi M, Perussia B, Young D, Nickbarg E, Wolf SF, Trinchieri G: Natural killer cell stimulatory factor (NKSF) increases the cytotoxic activity of NK cells from both healthy donors and HIV-infected patients. J Exp Med 175:789–796, 1992
    PubMed Google Scholar
  37. Chehimi J, Valiante NM, D'Andrea A, Rengaraju M, Rosado Z, Kobayashi M, Perussia B, Wolf S, Starr SE, Trinchieri G: Enhancing effect of natural killer cell stimulatory factor (NKSF/IL-12) on cell-mediated cytotoxicity against tumor-derived and virus-infected cells. Eur J Immunol 23:1826–1830, 1993
    PubMed Google Scholar
  38. Lieberman M, Sigal R, Williams N, Daly J: Natural killer cell stimulatory factor (NKSF) augments natural killer cell and antibody-dependent tumoricidal response against colon carcinoma cell lines. J Surg Res 50:410–415, 1991
    PubMed Google Scholar
  39. Cesano A, Visonneau S, Clark SC, Santoli D: Cellular and molecular mechanisms of activation of MHC nonrestricted cytotoxic cells by IL-12. J Immunol 151:2943–2957, 1993
    PubMed Google Scholar
  40. Salcedo TW, Azzoni L, Wolf SF, Perussia B: Modulation of perform and granzyme messenger RNA expression in human natural killer cells. J Immunol 151:2511–2520, 1993
    PubMed Google Scholar
  41. Robertson MJ, Soiffer RJ, Wolf SF, Manley TJ, Donahue C, Young D, Herrmann SH, Ritz J: Response of human natural killer (NK) cells to NK cell stimulatory factor (NKSF): Cytolytic activity and proliferation of NK cells are differentially regulated by NKSF. J Exp Med 175:779–788, 1992
    PubMed Google Scholar
  42. Rabinowich H, Herberman RB, Whiteside TL: Differential effects of IL-12 and IL-2 on expression and function of cellular adhesion molecules on purified human natural killer cells. Cell Immunol 152:481–498, 1993
    PubMed Google Scholar
  43. Mehrotra PT, Wu D, Crim JA, Mostowski HS, Siegel JP: Effects of IL-12 on the generation of cytotoxic activity in human CD8+ T lymphocytes. J Immunol 151:2444–2452, 1993
    PubMed Google Scholar
  44. Gately MK, Wolitzky AG, Quinn PM, Chizzonite R: Regulation of human cytolytic lymphocyte responses by interleukin-12. Cell Immunol 143:127–142, 1992
    PubMed Google Scholar
  45. Gerosa F, Tommasi M, Benati C, Gandini G, Libonati M, Tridente G, Carra G, Trinchieri G: Differential effects of tyrosine kinase inhibition in CD69 antigen expression and lytic activity induced by rIL-2, rIL-12 and rIFN-α in human NK cells. Cell Immunol 150:382–390, 1993
    PubMed Google Scholar
  46. Brunda MJ, Luistro L, Warrier RR, Wright RB, Hubbard BR, Murphy M, Wolf SF, Gately MK: Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med 178:1223–1230, 1993
    PubMed Google Scholar
  47. Tahara H, Zeh HJ, III, Storkus WJ, Pappo I, Watkins SC, Gubler U, Wolf SF, Robbins PD, Lotze MT: Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma_in vivo_. Cancer Res 54:182–189, 1994
    PubMed Google Scholar
  48. Gately MK, Desai BB, Wolitzky AG, Quinn PM, Dwyer CM, Podlaski FJ, Familletti PC, Sinigaglia F, Chizzonite R, Gubler U, Stern AS: Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J Immunol 147:874–882, 1991
    PubMed Google Scholar
  49. Naume B, Gately M, Espevik T: A comparative study of IL-12 (cytotoxic lymphocyte maturation factor)-, IL-2-, and IL-7-induced effects on immunom agnetically purified CD56+ NK cells. J Immunol 148:2429–2436, 1992
    PubMed Google Scholar
  50. Naume B, Gately MK, Desai BB, Sundan A, Espevik T: Synergistic effects of interleukin 4 and interleukin 12 on NK cell proliferation. Cytokine 5:38–46, 1993
    PubMed Google Scholar
  51. Romagnani S: Human TH1 ad TH2 subsets: Doubt no more, Immunol Today 12:256–257, 1991
    PubMed Google Scholar
  52. Manetti R, Parronchi P, Giudizi MG, Piccinni M-P, Maggi E, Trinchieri G, Romagnani S: 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, 1993
    PubMed Google Scholar
  53. Kiniwa M, Gately M, Gubler U, Chizzonite R, Fargeas C, Delespesse G: Recombinant interleukin-12 suppresses the synthesis of immunoglobulin E by interleukin-4 stimulated human lymphocytes. J Clin Invest 90:262–266, 1992
    PubMed Google Scholar
  54. Manetti R, Gerosa F, Giudizi MG, Biagiotti R, Parronchi P, Piccinni M, Sampognaro S, Maggi E, Romagnani S, Trinchieri G: 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, 1994
    PubMed Google Scholar
  55. Wu CY, Demeure C, Kiniwa M, Gately M, Delespesse G: Il-12 induces the production of IFN-gamma by neonatal human CD4 T cells. J Immunol 151:1938–1949, 1993
    PubMed Google Scholar
  56. Hsieh C, Macatonia SE, Tripp CS, Wolf SF, O'Garra A, Murphy KM:Listeria -induced Th1 development of αβ-TCR transgenic CD4+ T cells occurs through macrophage production of IL-12. Science 260:547–549, 1993
    PubMed Google Scholar
  57. Macatonia SE, Hsieh C, Murphy KM, O'Garra A: Dendritic cells and macrophages are required for Th1 development of CD4+ T cells from αβ-TCR transgenic mice: IL-12 substitution for macrophages to stimulate IFN-γ production is IFN-γ-dependent. Int Immunol 5:1119–1128, 1993
    PubMed Google Scholar
  58. Seder RA, Gazzinelli R, Sher A, Paul WE: IL-12 acts directly on CD4+ T cells to enhance priming for IFNγ production and diminishes IL-4 inhibition of such priming. Proc Natl Acad Sci USA 90:10188–10192, 1993
    PubMed Google Scholar
  59. Trinchieri G, Kubin M, Bellone G, Cassatella MC: Cytokine cross-talk between phagocytic cells and lymphocytes: relevance for differentiation/activation of phagocytic cells and regulation of adaptive immunity. J Cell Biochem 53:301–308, 1993
    PubMed Google Scholar
  60. Romagnani S: Induction of TH1 and TH2 responses: A key role for the “natural” immune response? Immunol Today 13:379–381, 1992
    PubMed Google Scholar
  61. Scott P: IL-12: Initiation cytokine for cell-mediated immunity. Science 260:496–497, 1993
    PubMed Google Scholar
  62. Locksley RM: Interleukin 12 in host defense against microbial pathogens. Proc Natl Acad Sci USA 90:5879–5880, 1993
    PubMed Google Scholar
  63. Bancroft GJ, Schreiber RD, Unanue ER: Natural immunity: A T-cell-independent pathway of macrophage activation, defined in the scid mouse. Immunol Rev 124:5–24, 1991
    PubMed Google Scholar
  64. Gazzinelli RT, Wysocka M, Hayashi S, Deukers EY, Hieny S, Caspar P, Trinchieri G, Sher A: Parasite induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with_Toxoplasma gondii_ (submitted for publication), 1994
  65. Heinzel FP, Schoenhaut DS, Rerko RM, Rosser LE, Gately MK: Recombinant interleukin 12 cures mice infected with_Leishmania major_. J Exp Med 177:1505–1509, 1993
    PubMed Google Scholar
  66. Sypek JP, Chung CL, Mayor SEH, Subramanyam JM, Goldman SJ, Sieburth DS, Wolf SF, Schaub RG: Resolution of cutaneous leishmaniasis: Interleukin-12 initiates a protective T helper type 1 immune response. J Exp Med 177:1797–1802, 1993
    PubMed Google Scholar
  67. Afonso LCC, Scharton TM, Vieira LQ, Wysocka M, Trinchieri G, Scott P: IL-12 functions as an effective adjuvant in a vaccine against_Leishmania major_ by directing the development of leishmanial specific CD4+ Th1 cells. Science 263:235–237, 1994
    PubMed Google Scholar
  68. Salk J, Bretscher PA, Salk PL, Clerici M, Shearer G: A strategy for prophylactic vaccination against HIV. Science 160:1740–1742, 1993
    Google Scholar
  69. Resenberg ZF, Fauci AS: The immunopathogenesis of HIV infection. Adv Immunol 47:377–431, 1989
    PubMed Google Scholar
  70. Levy JA: Pathogenesis of human immunodeficiency virus infection. Microbiol Rev 57:183–289, 1993
    PubMed Google Scholar
  71. Fauci AS; Multifactoral nature of human immunodeficiency virus disease: implications for therapy. Science 262:1011–1018, 1993
    PubMed Google Scholar
  72. Miedema F, Petit A, Terpstra F, Eeftinck Schattenkerk J, DeWolf F, Ai B, Roos M, Lange J, Danner S, Goudsmit J, Schellekens P: Immunological abnormalities in human immunodeficiency virus (HIV)-infected asymptomatic homosexual men: HIV affects the immune system before CD4+ T helper cell depletion occurs. J Clin Invest 82:1908–1914, 1988
    PubMed Google Scholar
  73. Clerici M, Giorgi JV, Chou CC, Gudeman VK, Zack JA, Gupta P, Ho NN, Nishanian PG, Bezzofsky JA, Shearer GM: Cell-mediated immune response to human immunodeficiency virus (HIV) type 1 in seronegative homosexual men with recent sexual exposure to HIV. J Infect Dis 165:1012–1119, 1992
    PubMed Google Scholar
  74. Poli G, Fauci AS: Multifactorial nature of human immunodeficiency virus disease: implications for therapy. AIDS Res Hum Retrovirus 8:191–197, 1993
    Google Scholar
  75. Clerici M, Shearer GM: A Th1-Th2 switch is a critical step in the etiology of HIV infection. Immunol Today 14:107–111, 1993
    PubMed Google Scholar
  76. Clerici M, Lucey DR, Berzofsky JA, Pinto LA, Wynn TA, Blatt SP, Dolan MJ, Hendrix CW, Wolf SF, Shearer GM: Restoration of HIV-specific cell-mediated immune responses by interleukin-12 in vitro. Science 262:1721–1724, 1993
    PubMed Google Scholar
  77. Chehimi J, Starr S, Frank I, D'Andrea A, MacGregor RR, Sennelier J, Trinchieri G: Impaired interleukin-12 production in HIV-infected patients. J Exp Med 179:1361–1366, 1994
    PubMed Google Scholar
  78. Maggi E, Macchia D, Parronchi P, Mazzetti M, Ravina A, Milo D, Romagnani S: Reduced production of interleukin 2 and interferon-gamma and enhanced helper activity for IgG synthesis by cloned CD4+ T cells from patients with AIDS. Eur J Immunol 17:1685–1690, 1987
    PubMed Google Scholar
  79. Shearer GM, Clerici M: T helper cell immune dysfunction in asymptomatic, HIV-1-seropositive individuals: the role of Th1-Th2 cross-regulation. Chem Immunol 54:21–43, 1992
    PubMed Google Scholar
  80. Meyaard L, Otto SA, de Jong R, Miedema F: Preferential outgrowth of Th2 cells after HIV infection. IX International Conference on AIDS, Berlin, 1993, p 32, abstr, WS-A16-13
  81. Graziosi C, Pantaleo G, Gantt KR, Demarest JF, Fauci AS: Comparative analysis of cytokine expression in peripheral blood and lymphoid organs of patients with HIV-1 infection by quantitative PCR. First National Conference on Human Retroviruses, Washington, DC, 1993, p 109, abstr 308
  82. Fan J, Bass HZ, Fahey JL: Elevated IFN-γ and decreased IL-2 gene expression are associated with HIV infection. J Immunol 154:5031–5040, 1993
    Google Scholar
  83. Tyring SK, Cauda R, Tumbarello M, Ortona L, Kennedy RC, Chanh TC, Kanda P: Synthetic peptides corresponding to sequences in HIV envelope gp41 and gp120 enhance in vitro production of interleukin-1 and tumor necrosis factor but depress production of interferon-α, interferon-γ and interleukin-2. Viral Immunol 4:33–42, 1991
    PubMed Google Scholar
  84. Murray HW, Rubin BY, Masur H, Roberts RB: Impaired production of lymphokines and immune (gamma) interferon in the acquired immunodeficiency syndrome. N Engl J Med 310;883–889, 1984
    PubMed Google Scholar
  85. Fuchs D, Hausen A, Reibnegger G, Werner ER, Werner-Felmayer G, Dierich MP, Wachter H: Interferon-gamma concentrations are increased in sera from individuals infected with human immunodeficiency virus type 1. J Acquir Immune Defic Syndr 2:158–165, 1989
    PubMed Google Scholar
  86. Myeaard L, Schuitemaker H, Miedema F: T-cell dysfunction in HIV infection: anergy due to defective antigenpresenting cell function? Immunol Today 14:161–164, 1993
    PubMed Google Scholar
  87. Heagy W, Groopman J, Schindler J, Finberg R: Use of IFN-γ in patients with AIDS. J Acq Immun Defic Syndr 3:584–590, 1990
    Google Scholar
  88. Germann T, Gately MK, Schoenhaut DS, Lohoff M, Mattner F, Fischer S, Jin S, Schmitt E, Rüde E: Interleukin-12/T cell stimulating factor, a cytokine with multiple effects on T helper type 1 (Th1) but not on Th2 cells. Eur J Immunol 23:1762–1770, 1993
    PubMed Google Scholar
  89. Quill H, Bhandoola A, Trinchieri G, Haluskey J, Peritt D: Induction of IL-12 responsiveness is impaired in anergic T lymphocytes. J Exp Med 179:1065–1070, 1994
    PubMed Google Scholar
  90. Gajewski TF, Lancki DW, Stack L, Fitch FW: “Anergy” of Th0 helper T lymphocytes induces downregulation of Th1 characteristics and a transition to a Th2-like phenotype. J Exp Med 179:481–492, 1994
    PubMed Google Scholar
  91. Chomarat P, Rissoan MC, Banphereau J, Miossec P: Interferon gamma inhibits interleukin 10 production by monocytes. J Exp Med 177:523–527, 1993
    PubMed Google Scholar

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