Astrocytes initiate inflammation in the injured mouse spinal cord by promoting the entry of neutrophils and inflammatory monocytes in an IL-1 receptor/MyD88-dependent fashion

Brain Behav Immun. 2010 May;24(4):540-53. doi: 10.1016/j.bbi.2009.11.007. Epub 2009 Nov 22.

Abstract

CNS injury stimulates the expression of several proinflammatory cytokines and chemokines, some of which including MCP-1 (also known as CCL2), KC (CXCL1), and MIP-2 (CXCL2) act to recruit Gr-1(+) leukocytes at lesion sites. While earlier studies have reported that neutrophils and monocytes/macrophages contribute to secondary tissue loss after spinal cord injury (SCI), recent work has shown that depletion of Gr-1(+) leukocytes compromised tissue healing and worsened functional recovery. Here, we demonstrate that astrocytes distributed throughout the spinal cord initially contribute to early neuroinflammation by rapidly synthesizing MCP-1, KC, and MIP-2, from 3 up to 12h post-SCI. Chemokine expression by astrocytes was followed by the infiltration of blood-derived immune cells, such as type I "inflammatory" monocytes and neutrophils, into the lesion site and nearby damaged areas. Interestingly, astrocytes from mice deficient in MyD88 signaling produced significantly less MCP-1 and MIP-2 and were unable to synthesize KC. Analysis of the contribution of MyD88-dependent receptors revealed that the astrocytic expression of MCP-1, KC, and MIP-2 was mediated by the IL-1 receptor (IL-1R1), and not by TLR2 or TLR4. Flow cytometry analysis of cells recovered from the spinal cord of MyD88- and IL-1R1-knockout mice confirmed the presence of significantly fewer type I "inflammatory" monocytes and the almost complete absence of neutrophils at 12h and 4days post-SCI. Together, these results indicate that MyD88/IL-1R1 signals regulate the entry of neutrophils and, to a lesser extent, type I "inflammatory" monocytes at sites of SCI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / immunology*
  • Astrocytes / metabolism
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism*
  • Chemokine CXCL1 / genetics
  • Chemokine CXCL1 / metabolism*
  • Chemokine CXCL2 / genetics
  • Chemokine CXCL2 / metabolism*
  • Disease Models, Animal
  • Flow Cytometry
  • Fluorescent Antibody Technique
  • In Situ Hybridization
  • Mice
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / immunology
  • Myeloid Differentiation Factor 88 / deficiency*
  • Neutrophils / immunology
  • Polymerase Chain Reaction
  • RNA, Messenger
  • Receptors, Interleukin-1 Type I / deficiency*
  • Spinal Cord / cytology
  • Spinal Cord Injuries / immunology*
  • Spinal Cord Injuries / metabolism
  • Time Factors
  • Toll-Like Receptor 2 / deficiency
  • Toll-Like Receptor 4 / deficiency

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Chemokine CXCL1
  • Chemokine CXCL2
  • Cxcl1 protein, mouse
  • Cxcl2 protein, mouse
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • RNA, Messenger
  • Receptors, Interleukin-1 Type I
  • Tlr2 protein, mouse
  • Tlr4 protein, mouse
  • Toll-Like Receptor 2
  • Toll-Like Receptor 4