Developmental endothelial locus-1 is a homeostatic factor in the central nervous system limiting neuroinflammation and demyelination

Mol Psychiatry. 2015 Jul;20(7):880-888. doi: 10.1038/mp.2014.146. Epub 2014 Nov 11.

Abstract

Inflammation in the central nervous system (CNS) and disruption of its immune privilege are major contributors to the pathogenesis of multiple sclerosis (MS) and of its rodent counterpart, experimental autoimmune encephalomyelitis (EAE). We have previously identified developmental endothelial locus-1 (Del-1) as an endogenous anti-inflammatory factor, which inhibits integrin-dependent leukocyte adhesion. Here we show that Del-1 contributes to the immune privilege status of the CNS. Intriguingly, Del-1 expression decreased in chronic-active MS lesions and in the inflamed CNS in the course of EAE. Del-1-deficiency was associated with increased EAE severity, accompanied by increased demyelination and axonal loss. As compared with control mice, Del-1(-/-) mice displayed enhanced disruption of the blood-brain barrier and increased infiltration of neutrophil granulocytes in the spinal cord in the course of EAE, accompanied by elevated levels of inflammatory cytokines, including interleukin-17 (IL-17). The augmented levels of IL-17 in Del-1-deficiency derived predominantly from infiltrated CD8(+) T cells. Increased EAE severity and neutrophil infiltration because of Del-1-deficiency was reversed in mice lacking both Del-1 and IL-17 receptor, indicating a crucial role for the IL-17/neutrophil inflammatory axis in EAE pathogenesis in Del-1(-/-) mice. Strikingly, systemic administration of Del-1-Fc ameliorated clinical relapse in relapsing-remitting EAE. Therefore, Del-1 is an endogenous homeostatic factor in the CNS protecting from neuroinflammation and demyelination. Our findings provide mechanistic underpinnings for the previous implication of Del-1 as a candidate MS susceptibility gene and suggest that Del-1-centered therapeutic approaches may be beneficial in neuroinflammatory and demyelinating disorders.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, N.I.H., Intramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Axons / drug effects
  • Axons / metabolism*
  • Axons / pathology
  • Blood-Brain Barrier / drug effects
  • Blood-Brain Barrier / metabolism*
  • Blood-Brain Barrier / pathology
  • Calcium-Binding Proteins
  • Capillary Permeability / drug effects
  • Capillary Permeability / physiology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Adhesion Molecules
  • Encephalomyelitis, Autoimmune, Experimental / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental / metabolism
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Female
  • Granulocytes / drug effects
  • Granulocytes / metabolism
  • Granulocytes / pathology
  • Homeostasis / drug effects
  • Homeostasis / physiology
  • Intercellular Signaling Peptides and Proteins
  • Interleukin-17 / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myelin Sheath / drug effects
  • Myelin Sheath / metabolism*
  • Myelin Sheath / pathology
  • Neuroimmunomodulation / drug effects
  • Neuroimmunomodulation / physiology*
  • Neutrophils / drug effects
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Receptors, Interleukin-17 / genetics
  • Receptors, Interleukin-17 / metabolism
  • Severity of Illness Index
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism*
  • Spinal Cord / pathology

Substances

  • Calcium-Binding Proteins
  • Carrier Proteins
  • Cell Adhesion Molecules
  • Edil3 protein, mouse
  • Il17ra protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Interleukin-17
  • Receptors, Interleukin-17