Protein kinase Cβ as a therapeutic target stabilizing blood-brain barrier disruption in experimental autoimmune encephalomyelitis

Proc Natl Acad Sci U S A. 2013 Sep 3;110(36):14735-40. doi: 10.1073/pnas.1302569110. Epub 2013 Aug 19.

Abstract

Disruption of the blood-brain barrier (BBB) is a hallmark of acute inflammatory lesions in multiple sclerosis (MS) and its animal model experimental autoimmune encephalomyelitis. This disruption may precede and facilitate the infiltration of encephalitogenic T cells. The signaling events that lead to this BBB disruption are incompletely understood but appear to involve dysregulation of tight-junction proteins such as claudins. Pharmacological interventions aiming at stabilizing the BBB in MS might have therapeutic potential. Here, we show that the orally available small molecule LY-317615, a synthetic bisindolylmaleimide and inhibitor of protein kinase Cβ, which is clinically under investigation for the treatment of cancer, suppresses the transmigration of activated T cells through an inflamed endothelial cell barrier, where it leads to the induction of the tight-junction molecules zona occludens-1, claudin 3, and claudin 5 and other pathways critically involved in transendothelial leukocyte migration. Treatment of mice with ongoing experimental autoimmune encephalomyelitis with LY-317615 ameliorates inflammation, demyelination, axonal damage, and clinical symptoms. Although LY-317615 dose-dependently suppresses T-cell proliferation and cytokine production independent of antigen specificity, its therapeutic effect is abrogated in a mouse model requiring pertussis toxin. This abrogation indicates that the anti-inflammatory and clinical efficacy is mainly mediated by stabilization of the BBB, thus suppressing the transmigration of encephalitogenic T cells. Collectively, our data suggest the involvement of endothelial protein kinase Cβ in stabilizing the BBB in autoimmune neuroinflammation and imply a therapeutic potential of BBB-targeting agents such as LY-317615 as therapeutic approaches for MS.

Keywords: CNS; EAE; enzastaurin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood-Brain Barrier / drug effects*
  • Blood-Brain Barrier / immunology
  • Cell Proliferation / drug effects
  • Claudin-3 / immunology
  • Claudin-3 / metabolism
  • Claudin-5 / immunology
  • Claudin-5 / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism
  • Demyelinating Diseases / immunology
  • Demyelinating Diseases / prevention & control
  • Dose-Response Relationship, Drug
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Encephalomyelitis, Autoimmune, Experimental / prevention & control*
  • Endothelial Cells / drug effects
  • Endothelial Cells / immunology
  • Endothelial Cells / metabolism
  • Female
  • Gene Expression Profiling
  • Immunohistochemistry
  • Indoles / immunology
  • Indoles / pharmacology*
  • Inflammation / immunology
  • Inflammation / metabolism
  • Inflammation / prevention & control
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred Strains
  • Microscopy, Confocal
  • Protein Kinase C beta / antagonists & inhibitors*
  • Protein Kinase C beta / immunology
  • Protein Kinase C beta / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Tight Junctions / drug effects
  • Tight Junctions / immunology
  • Tight Junctions / metabolism
  • Transendothelial and Transepithelial Migration / drug effects
  • Transendothelial and Transepithelial Migration / immunology
  • Zonula Occludens-1 Protein / immunology
  • Zonula Occludens-1 Protein / metabolism

Substances

  • Claudin-3
  • Claudin-5
  • Cytokines
  • Indoles
  • Zonula Occludens-1 Protein
  • Protein Kinase C beta
  • enzastaurin

Associated data

  • GEO/GSE48572