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CpG oligonucleotides can prophylactically immunize against Th2-mediated schistosome egg-induced pathology by an IL-12-independent mechanism

J Immunol. 2000 Jan 15;164(2):973-85. doi: 10.4049/jimmunol.164.2.973.

Abstract

Using a Schistosoma mansoni egg-induced granuloma model, we examined the ability of CpG oligodeoxynucleotides (ODN) to suppress Th2-type cytokine expression and to prophylactically immunize against Th2-dependent pulmonary pathology. The mechanism was examined by studying Th2 response regulation in cytokine-deficient mice. Surprisingly, our findings revealed several functions of CpG DNA that were completely IL-12 independent. Most striking was the marked suppression in Th2 cytokine expression and granulomatous inflammation observed in egg/CpG-sensitized IL-12-deficient mice. Immune deviation was not dependent on NK or B cells. However, a role for IL-10, B7.1, and CD40 expression in Th2 response inhibition was suggested. Indeed, CpG ODN up-regulated all three elements in both wild-type and IL-12-deficient mice. The role of IL-10 was demonstrated in mice exhibiting combined deficiencies in IL-12 and IL-10. Here, a marked increase in egg-specific IL-4/IL-5-producing cells confirmed a role for both cytokines in Th2 response inhibition. Nevertheless, the frequency of Th2-producing cells was again reduced by CpG ODN. However, in marked contrast to IL-12-deficient animals, a significant increase in IFN-gamma-producing cells likely explains the reduced Th2 response in IL-10/IL-12-deficient mice. Thus, a novel IL-12-independent type 1-inducing pathway was revealed in the combined absence of IL-12 and IL-10. Together, these data demonstrate 1) that the Th1-promoting activity of CpG DNA is controlled by IL-12 and IL-10, and 2) that Th2 response inhibition by CpG ODN involves IL-12-independent changes in IL-10 and costimulatory molecule expression. These findings illustrate the utility of CpG DNA as adjuvants for vaccines designed to prevent Th2-dependent immunopathology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adjuvants, Immunologic / administration & dosage
  • Animals
  • Antigens, Helminth / administration & dosage
  • Antigens, Helminth / immunology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology
  • B7-1 Antigen / biosynthesis
  • CD40 Antigens / biosynthesis
  • CpG Islands / immunology*
  • Cytokines / biosynthesis
  • Epitopes, T-Lymphocyte / immunology
  • Female
  • G(M1) Ganglioside / biosynthesis
  • Granuloma, Respiratory Tract / genetics
  • Granuloma, Respiratory Tract / immunology*
  • Granuloma, Respiratory Tract / parasitology
  • Granuloma, Respiratory Tract / pathology*
  • Immunoglobulin Isotypes / biosynthesis
  • Immunoglobulin Isotypes / metabolism
  • Immunosuppressive Agents / administration & dosage
  • Injections, Intraperitoneal
  • Interferon-gamma / biosynthesis
  • Interferon-gamma / genetics
  • Interferon-gamma / physiology
  • Interleukin-10 / biosynthesis
  • Interleukin-10 / deficiency
  • Interleukin-10 / genetics
  • Interleukin-12 / biosynthesis
  • Interleukin-12 / deficiency
  • Interleukin-12 / genetics
  • Interleukin-12 / physiology*
  • Killer Cells, Natural / immunology
  • Killer Cells, Natural / metabolism
  • Lung / immunology
  • Lung / metabolism
  • Lymphopenia / genetics
  • Lymphopenia / immunology
  • Macrophage Activation / genetics
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oligonucleotides / administration & dosage
  • Oligonucleotides / immunology*
  • Ovum / immunology*
  • RNA, Messenger / biosynthesis
  • Schistosoma mansoni / immunology*
  • Th2 Cells / immunology*
  • Th2 Cells / metabolism
  • Th2 Cells / parasitology
  • Up-Regulation / immunology

Substances

  • Adjuvants, Immunologic
  • Antigens, Helminth
  • B7-1 Antigen
  • CD40 Antigens
  • Cytokines
  • Epitopes, T-Lymphocyte
  • Immunoglobulin Isotypes
  • Immunosuppressive Agents
  • Oligonucleotides
  • RNA, Messenger
  • Interleukin-10
  • Interleukin-12
  • G(M1) Ganglioside
  • asialo GM1 ganglioside
  • Interferon-gamma