Sphingosine 1-phosphate receptor modulation suppresses pathogenic astrocyte activation and chronic progressive CNS inflammation

Proc Natl Acad Sci U S A. 2017 Feb 21;114(8):2012-2017. doi: 10.1073/pnas.1615413114. Epub 2017 Feb 6.

Abstract

Multiple sclerosis (MS) is an autoimmune inflammatory demyelinating disease of the CNS that causes disability in young adults as a result of the irreversible accumulation of neurological deficits. Although there are potent disease-modifying agents for its initial relapsing-remitting phase, these therapies show limited efficacy in secondary progressive MS (SPMS). Thus, there is an unmet clinical need for the identification of disease mechanisms and potential therapeutic approaches for SPMS. Here, we show that the sphingosine 1-phosphate receptor (S1PR) modulator fingolimod (FTY720) ameliorated chronic progressive experimental autoimmune encephalomyelitis in nonobese diabetic mice, an experimental model that resembles several aspects of SPMS, including neurodegeneration and disease progression driven by the innate immune response in the CNS. Indeed, S1PR modulation by FTY720 in murine and human astrocytes suppressed neurodegeneration-promoting mechanisms mediated by astrocytes, microglia, and CNS-infiltrating proinflammatory monocytes. Genome-wide studies showed that FTY720 suppresses transcriptional programs associated with the promotion of disease progression by astrocytes. The study of the molecular mechanisms controlling these transcriptional modules may open new avenues for the development of therapeutic strategies for progressive MS.

Keywords: EAE; astrocytes; multiple sclerosis; secondary progression; sphingolipid metabolism.

Publication types

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

MeSH terms

  • Animals
  • Astrocytes / drug effects*
  • Astrocytes / metabolism
  • Cell Line, Tumor
  • Disease Progression
  • Encephalomyelitis, Autoimmune, Experimental / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Female
  • Fingolimod Hydrochloride / pharmacology
  • Fingolimod Hydrochloride / therapeutic use
  • Humans
  • Immunosuppressive Agents / pharmacology*
  • Immunosuppressive Agents / therapeutic use
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Microglia / metabolism
  • Monocytes / immunology
  • Monocytes / metabolism
  • Multiple Sclerosis, Chronic Progressive / drug therapy*
  • Multiple Sclerosis, Chronic Progressive / pathology
  • Primary Cell Culture
  • Receptors, Lysosphingolipid / metabolism*
  • Sphingosine / metabolism
  • Sphingosine-1-Phosphate Receptors
  • Transcriptome / drug effects

Substances

  • Immunosuppressive Agents
  • Receptors, Lysosphingolipid
  • S1PR1 protein, human
  • S1pr1 protein, mouse
  • Sphingosine-1-Phosphate Receptors
  • Fingolimod Hydrochloride
  • Sphingosine