Binding to gangliosides containing N-acetylneuraminic acid is sufficient to mediate the immunomodulatory properties of the nontoxic mucosal adjuvant LT-IIb(T13I)

Clin Vaccine Immunol. 2010 Jun;17(6):969-78. doi: 10.1128/CVI.00076-10. Epub 2010 Apr 14.

Abstract

By use of a mouse mucosal immunization model, LT-IIb(T13I), a nontoxic mutant type II heat-labile enterotoxin, was shown to have potent mucosal and systemic adjuvant properties. In contrast to LT-IIb, which binds strongly to ganglioside receptors decorated with either N-acetylneuraminic acid (NeuAc) or N-glycolylneuraminic acid (NeuGc), LT-IIb(T13I) binds NeuAc gangliosides much less well. Rather, LT-IIb(T13I) binds preferentially to NeuGc gangliosides. To determine if the adjuvant properties of LT-IIb(T13I) are altered in the absence of NeuGc ganglioside receptors, experiments were conducted using a Cmah-null mouse line which is deficient in the synthesis of NeuGc gangliosides. Several immunomodulatory properties of LT-IIb(T13I) were shown to be dependent on NeuGc gangliosides. LT-IIb(T13I) had reduced binding activity for NeuGc-deficient B cells and macrophages; binding to NeuGc-deficient T cells and dendritic cells (DC) was essentially undetectable. Treatment of Cmah-null macrophages with LT-IIb(T13I), however, upregulated the transcription of interleukin-4 (IL-4), IL-6, IL-17, and gamma interferon (IFN-gamma), four cytokines important for promoting immune responses. The production of mucosal IgA and serum IgG against an immunizing antigen was augmented in NeuGc-deficient mice administered LT-IIb(T13I) as a mucosal adjuvant. Notably, NeuGc gangliosides are not expressed in humans. Still, treatment of human monocytes with LT-IIb(T13I) induced the secretion of IL-6, an inflammatory cytokine that mediates differential control of leukocyte activation. These results suggested that NeuAc gangliosides are sufficient to mediate the immunomodulatory properties of LT-IIb(T13I) in mice and in human cells. The nontoxic mutant enterotoxin LT-IIb(T13I), therefore, is potentially a new and safe human mucosal adjuvant.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adjuvants, Immunologic*
  • Animals
  • B-Lymphocytes / chemistry
  • B-Lymphocytes / immunology
  • Bacterial Toxins / immunology*
  • Bacterial Toxins / metabolism*
  • Cytokines / metabolism
  • Enterotoxins / immunology*
  • Enterotoxins / metabolism*
  • Escherichia coli Proteins / immunology*
  • Escherichia coli Proteins / metabolism*
  • Gangliosides / chemistry
  • Gangliosides / immunology
  • Gangliosides / metabolism*
  • Humans
  • Immunity, Mucosal*
  • Immunization
  • Immunologic Factors / immunology
  • Macrophages, Peritoneal / chemistry
  • Macrophages, Peritoneal / immunology
  • Mice
  • Mice, Inbred C57BL
  • Monocytes / chemistry
  • Monocytes / immunology
  • N-Acetylneuraminic Acid / chemistry*
  • Receptors, Cell Surface / metabolism

Substances

  • Adjuvants, Immunologic
  • Bacterial Toxins
  • Cytokines
  • Enterotoxins
  • Escherichia coli Proteins
  • Gangliosides
  • Immunologic Factors
  • Receptors, Cell Surface
  • ganglioside receptor
  • heat-labile enterotoxin, E coli
  • N-Acetylneuraminic Acid