Interleukin-1 participates in the classical and alternative activation of microglia/macrophages after spinal cord injury

J Neuroinflammation. 2012 Apr 7:9:65. doi: 10.1186/1742-2094-9-65.

Abstract

Background: Microglia and macrophages (MG/MΦ) have a diverse range of functions depending on unique cytokine stimuli, and contribute to neural cell death, repair, and remodeling during central nervous system diseases. While IL-1 has been shown to exacerbate inflammation, it has also been recognized to enhance neuroregeneration. We determined the activating phenotype of MG/MΦ and the impact of IL-1 in an in vivo spinal cord injury (SCI) model of IL-1 knock-out (KO) mice. Moreover, we demonstrated the contribution of IL-1 to both the classical and alternative activation of MG in vitro using an adult MG primary culture.

Methods: SCI was induced by transection of the spinal cord between the T9 and T10 vertebra in wild-type and IL-1 KO mice. Locomotor activity was monitored and lesion size was determined for 14 days. TNFα and Ym1 levels were monitored to determine the MG/MΦ activating phenotype. Primary cultures of MG were produced from adult mice, and were exposed to IFNγ or IL-4 with and without IL-1β. Moreover, cultures were exposed to IL-4 and/or IL-13 in the presence and absence of IL-1β.

Results: The locomotor activity and lesion area of IL-1 KO mice improved significantly after SCI compared with wild-type mice. TNFα production was significantly suppressed in IL-1 KO mice. Also, Ym1, an alternative activating MG/MΦ marker, did not increase in IL-1 KO mice, suggesting that IL-1 contributes to both the classical and alternative activation of MG/MΦ. We treated primary MG cultures with IFNγ or IL-4 in the presence and absence of IL-1β. Increased nitric oxide and TNFα was present in the culture media and increased inducible NO synthase was detected in cell suspensions following co-treatment with IFNγ and IL-1β. Expression of the alternative activation markers Ym1 and arginase-1 was increased after exposure to IL-4 and further increased after co-treatment with IL-4 and IL-1β. The phenotype was not observed after exposure of cells to IL-13.

Conclusions: We demonstrate here in in vivo experiments that IL-1 suppressed SCI in a process mediated by the reduction of inflammatory responses. Moreover, we suggest that IL-1 participates in both the classical and alternative activation of MG in in vivo and in vitro systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arginase / metabolism
  • CD11b Antigen / metabolism
  • Cells, Cultured
  • Central Nervous System / pathology
  • Cytokines / pharmacology
  • Disease Models, Animal
  • Doxorubicin / analogs & derivatives
  • Doxorubicin / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Gene Expression Regulation / genetics
  • Glial Fibrillary Acidic Protein / metabolism
  • Interleukin-1 / deficiency
  • Interleukin-1 / metabolism*
  • Interleukin-1alpha / deficiency
  • Interleukin-1beta / deficiency
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / drug effects
  • Microglia / metabolism*
  • Microtubule-Associated Proteins / metabolism
  • Motor Activity / physiology
  • Myelin Basic Protein / metabolism
  • Nitric Oxide / metabolism
  • Spinal Cord Injuries / genetics
  • Spinal Cord Injuries / pathology*
  • Spinal Cord Injuries / physiopathology

Substances

  • CD11b Antigen
  • Cytokines
  • Glial Fibrillary Acidic Protein
  • Interleukin-1
  • Interleukin-1alpha
  • Interleukin-1beta
  • Microtubule-Associated Proteins
  • Mtap2 protein, mouse
  • Myelin Basic Protein
  • N-(3-pyridylmethyl)adriamycin
  • Nitric Oxide
  • Doxorubicin
  • Arginase