Critical role of CCL22/CCR4 axis in the maintenance of immune homeostasis during apoptotic cell clearance by splenic CD8α(+) CD103(+) dendritic cells

Immunology. 2016 Jun;148(2):174-86. doi: 10.1111/imm.12596. Epub 2016 Mar 30.

Abstract

Macrophages and dendritic cells (DCs) in murine spleen are essential for the maintenance of immune homeostasis by elimination of blood-borne foreign particles and organisms. It has been reported that splenic DCs, especially CD8α(+) CD103(+) DCs, are responsible for tolerance to apoptosis-associated antigens. However, the molecular mechanism by which these DCs maintain immune homeostasis by blood-borne apoptotic cell clearance remains elusive. Here, we found that the CCL22/CCR4 axis played a critical role in the maintenance of immune homeostasis during apoptotic cell clearance by splenic CD8α(+) CD103(+) DCs. The present results revealed that systemic administration of apoptotic cells rapidly induced a large number of CCL22 and CCR4(+) regulatory T (Treg) cells in the spleen of C57BL/6J mice. Further study demonstrated that CD8α(+) CD103(+) DCs dominantly produce much higher CCL22 than CD8α(+) CD103(-) DCs. Moreover, the transient deletion of CD8α(+) CD103(+) DCs caused a decrease in CCL22 levels together with CCR4(+) Treg cell percentage. Subsequently, the levels of some pro-inflammatory cytokines, such as interleukin-17 and interferon-γ in the spleen with the absence of CD8α(+) CD103(+) DCs increased in response to the administration of apoptotic cells. Hence, intravenous injection of apoptotic cells induced a subsequent increase in CCL22 expression and CCR4(+) Treg cells, which contribute to the maintenance of immune homeostasis at least partially by splenic CD8α(+) CD103(+) DCs.

Keywords: CCL22; CCR4+ regulatory T cells; CD8α+ CD103+ dendritic cells; spleen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / metabolism
  • Apoptosis / immunology*
  • CD8 Antigens / metabolism
  • Cells, Cultured
  • Chemokine CCL22 / metabolism*
  • Dendritic Cells / immunology*
  • Homeostasis / immunology
  • Integrin alpha Chains / metabolism
  • Interferon-gamma / metabolism
  • Interleukin-17 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Receptors, CCR4 / metabolism*
  • Spleen / pathology
  • T-Lymphocytes, Regulatory / immunology*

Substances

  • Antigens, CD
  • CD8 Antigens
  • CD8alpha antigen
  • Ccl22 protein, mouse
  • Ccr4 protein, mouse
  • Chemokine CCL22
  • Integrin alpha Chains
  • Interleukin-17
  • Receptors, CCR4
  • alpha E integrins
  • Interferon-gamma