Maintenance of intestinal Th17 cells and reduced microbial translocation in SIV-infected rhesus macaques treated with interleukin (IL)-21

PLoS Pathog. 2013;9(7):e1003471. doi: 10.1371/journal.ppat.1003471. Epub 2013 Jul 4.

Abstract

In pathogenic HIV and SIV infections of humans and rhesus macaques (RMs), preferential depletion of CD4⁺ Th17 cells correlates with mucosal immune dysfunction and disease progression. Interleukin (IL)-21 promotes differentiation of Th17 cells, long-term maintenance of functional CD8⁺ T cells, and differentiation of memory B cells and antibody-secreting plasma cells. We hypothesized that administration of IL-21 will improve mucosal function in the context of pathogenic HIV/SIV infections. To test this hypothesis, we infected 12 RMs with SIV(mac239) and at day 14 post-infection treated six of them with rhesus rIL-21-IgFc. IL-21-treatment was safe and did not increase plasma viral load or systemic immune activation. Compared to untreated animals, IL-21-treated RMs showed (i) higher expression of perforin and granzyme B in total and SIV-specific CD8⁺ T cells and (ii) higher levels of intestinal Th17 cells. Remarkably, increased levels of Th17 cells were associated with reduced levels of intestinal T cell proliferation, microbial translocation and systemic activation/inflammation in the chronic infection. In conclusion, IL-21-treatment in SIV-infected RMs improved mucosal immune function through enhanced preservation of Th17 cells. Further preclinical studies of IL-21 may be warranted to test its potential use during chronic infection in conjunction with antiretroviral therapy.

Publication types

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

MeSH terms

  • Animals
  • Bacterial Translocation / drug effects*
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Differentiation / drug effects
  • Down-Regulation / drug effects
  • Female
  • Granzymes / biosynthesis
  • Granzymes / genetics
  • Granzymes / metabolism
  • Immunity, Mucosal / drug effects*
  • Immunoglobulin Fc Fragments / adverse effects
  • Immunoglobulin Fc Fragments / genetics
  • Immunoglobulin Fc Fragments / therapeutic use*
  • Interleukins / adverse effects
  • Interleukins / genetics
  • Interleukins / therapeutic use*
  • Intestinal Mucosa / drug effects*
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / pathology
  • Intestinal Mucosa / virology
  • Macaca mulatta
  • Perforin / biosynthesis
  • Perforin / genetics
  • Perforin / metabolism
  • Random Allocation
  • Recombinant Fusion Proteins / adverse effects
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / therapeutic use
  • Simian Acquired Immunodeficiency Syndrome / drug therapy*
  • Simian Acquired Immunodeficiency Syndrome / immunology
  • Simian Acquired Immunodeficiency Syndrome / metabolism
  • Simian Acquired Immunodeficiency Syndrome / virology
  • Simian Immunodeficiency Virus / drug effects*
  • Simian Immunodeficiency Virus / isolation & purification
  • Simian Immunodeficiency Virus / physiology
  • Th17 Cells / drug effects*
  • Th17 Cells / immunology
  • Th17 Cells / pathology
  • Th17 Cells / virology
  • Up-Regulation / drug effects
  • Viral Load / drug effects

Substances

  • Immunoglobulin Fc Fragments
  • Interleukins
  • Recombinant Fusion Proteins
  • Perforin
  • Granzymes
  • interleukin-21