Blocking glutamate carboxypeptidase II inhibits glutamate excitotoxicity and regulates immune responses in experimental autoimmune encephalomyelitis

FEBS J. 2016 Sep;283(18):3438-56. doi: 10.1111/febs.13816. Epub 2016 Aug 11.

Abstract

Experimental autoimmune encephalomyelitis (EAE) is an inflammatory disease in the murine central nervous system (CNS) and recapitulates the clinical and pathological features of human multiple sclerosis (MS). Glutamate carboxipeptidase II (GCPII), an enzyme expressed exclusively on astrocytes, is known to affect the disease progression of various neurological disorders by producing glutamate. Despite several findings indicating possible link between glutamate and MS/EAE, however, the involvement of astrocyte or GCPII on glutamate excitotoxicity has not received much attention in MS/EAE. When we examined GCPII expression during EAE progression in this study, we observed significantly elevated GCPII expression in peak stage of disease localized mainly in astrocytes. Intrigued by these results, we tried a potent GCPII inhibitor, 2-phosphonomethyl pentanedioic acid (2-PMPA), on EAE mice and noticed markedly attenuated EAE clinical signs along with significantly inhibited infiltration of inflammatory cells into CNS. Furthermore, 2-PMPA dampened the function of Th1 cell lineage and down-regulated mGluR1 expression in both periphery and CNS contributing to glutamate-mediated immune regulation. Our observations identify a sequence of events triggering EAE through GCPII overexpression, which may offer a novel therapeutic approach to the treatment of MS.

Keywords: 2-phosphonomethyl pentanedioic acid; experimental autoimmune encephalomyelitis (EAE); glutamate carboxypeptidase II; glutamate excitotoxicity; metabotropic glutamate receptors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / pharmacology
  • Animals
  • Astrocytes / drug effects
  • Astrocytes / enzymology
  • Disease Progression
  • Encephalomyelitis, Autoimmune, Experimental / drug therapy*
  • Encephalomyelitis, Autoimmune, Experimental / enzymology*
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Female
  • Glutamate Carboxypeptidase II / antagonists & inhibitors*
  • Glutamate Carboxypeptidase II / metabolism
  • Glutamic Acid / metabolism
  • Humans
  • Immunohistochemistry
  • Mice
  • Mice, Inbred C57BL
  • Organophosphorus Compounds / pharmacology*
  • Protease Inhibitors / pharmacology
  • Rats, Inbred Lew
  • Receptors, Metabotropic Glutamate / agonists
  • Receptors, Metabotropic Glutamate / antagonists & inhibitors
  • Receptors, Metabotropic Glutamate / metabolism
  • Spinal Cord / drug effects
  • Spinal Cord / enzymology
  • Spinal Cord / immunology
  • Th1 Cells / drug effects
  • Th1 Cells / immunology
  • Xanthenes / pharmacology

Substances

  • 2-(phosphonomethyl)pentanedioic acid
  • Amino Acids
  • Excitatory Amino Acid Antagonists
  • LY 341495
  • Organophosphorus Compounds
  • Protease Inhibitors
  • Receptors, Metabotropic Glutamate
  • Xanthenes
  • metabotropic glutamate receptor 3
  • metabotropic glutamate receptor type 1
  • Glutamic Acid
  • Glutamate Carboxypeptidase II