Lipocalin-2 protein deficiency ameliorates experimental autoimmune encephalomyelitis: the pathogenic role of lipocalin-2 in the central nervous system and peripheral lymphoid tissues

J Biol Chem. 2014 Jun 13;289(24):16773-89. doi: 10.1074/jbc.M113.542282. Epub 2014 May 7.

Abstract

Lipocalin-2 (LCN2) plays an important role in cellular processes as diverse as cell growth, migration/invasion, differentiation, and death/survival. Furthermore, recent studies indicate that LCN2 expression and secretion by glial cells are induced by inflammatory stimuli in the central nervous system. The present study was undertaken to examine the regulation of LCN2 expression in experimental autoimmune encephalomyelitis (EAE) and to determine the role of LCN2 in the disease process. LCN2 expression was found to be strongly increased in spinal cord and secondary lymphoid tissues after EAE induction. In spinal cords astrocytes and microglia were the major cell types expressing LCN2 and its receptor 24p3R, respectively, whereas in spleens, LCN2 and 24p3R were highly expressed in neutrophils and dendritic cells, respectively. Furthermore, disease severity, inflammatory infiltration, demyelination, glial activation, the expression of inflammatory mediators, and the proliferation of MOG-specific T cells were significantly attenuated in Lcn2-deficient mice as compared with wild-type animals. Myelin oligodendrocyte glycoprotein-specific T cells in culture exhibited an increased expression of Il17a, Ifng, Rorc, and Tbet after treatment with recombinant LCN2 protein. Moreover, LCN2-treated glial cells expressed higher levels of proinflammatory cytokines, chemokines, and MMP-9. Adoptive transfer and recombinant LCN2 protein injection experiments suggested that LCN2 expression in spinal cord and peripheral immune organs contributes to EAE development. Taken together, these results imply LCN2 is a critical mediator of autoimmune inflammation and disease development in EAE and suggest that LCN2 be regarded a potential therapeutic target in multiple sclerosis.

Keywords: Astrocyte; Autoimmune Disease; Central Nervous System; EAE; LCN2; Microglia; Multiple Sclerosis; Neuroinflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute-Phase Proteins / genetics
  • Acute-Phase Proteins / metabolism*
  • Animals
  • Astrocytes / metabolism
  • Cells, Cultured
  • Dendritic Cells / metabolism
  • Encephalomyelitis, Autoimmune, Experimental / metabolism*
  • Gene Deletion
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism
  • Interleukin-17 / genetics
  • Interleukin-17 / metabolism
  • Lipocalin-2
  • Lipocalins / genetics
  • Lipocalins / metabolism*
  • Lymphoid Tissue / metabolism*
  • Lymphoid Tissue / pathology
  • Matrix Metalloproteinase 9 / genetics
  • Matrix Metalloproteinase 9 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Myelin Sheath / genetics
  • Myelin Sheath / metabolism
  • Neutrophils / metabolism
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / genetics
  • Nuclear Receptor Subfamily 1, Group F, Member 3 / metabolism
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism
  • Spinal Cord / metabolism*
  • Spinal Cord / pathology
  • T-Lymphocytes / metabolism

Substances

  • 24p3 receptor, mouse
  • Acute-Phase Proteins
  • Il17a protein, mouse
  • Interleukin-17
  • Lipocalin-2
  • Lipocalins
  • Nuclear Receptor Subfamily 1, Group F, Member 3
  • Oncogene Proteins
  • Receptors, Cell Surface
  • Rorc protein, mouse
  • Lcn2 protein, mouse
  • Interferon-gamma
  • Matrix Metalloproteinase 9
  • Mmp9 protein, mouse