PPAR-γ activation enhances myelination and neurological recovery in premature rabbits with intraventricular hemorrhage

Proc Natl Acad Sci U S A. 2021 Sep 7;118(36):e2103084118. doi: 10.1073/pnas.2103084118.

Abstract

Intraventricular hemorrhage (IVH) results in periventricular inflammation, hypomyelination of the white matter, and hydrocephalus in premature infants. No effective therapy exists to prevent these disorders. Peroxisome proliferator activated receptor-γ (PPAR-γ) agonists reduce inflammation, alleviate free radical generation, and enhance microglial phagocytosis, promoting clearance of debris and red blood cells. We hypothesized that activation of PPAR-γ would enhance myelination, reduce hydrocephalus, and promote neurological recovery in newborns with IVH. These hypotheses were tested in a preterm rabbit model of IVH; autopsy brain samples from premature infants with and without IVH were analyzed. We found that IVH augmented PPAR-γ expression in microglia of both preterm human infants and rabbit kits. The treatment with PPAR-γ agonist or PPAR-γ overexpression by adenovirus delivery further elevated PPAR-γ levels in microglia, reduced proinflammatory cytokines, increased microglial phagocytosis, and improved oligodendrocyte progenitor cell (OPC) maturation in kits with IVH. Transcriptomic analyses of OPCs identified previously unrecognized PPAR-γ-induced genes for purinergic signaling, cyclic adenosine monophosphate generation, and antioxidant production, which would reprogram these progenitors toward promoting myelination. RNA-sequencing analyses of microglia revealed PPAR-γ-triggered down-regulation of several proinflammatory genes and transcripts having roles in Parkinson's disease and amyotrophic lateral sclerosis, contributing to neurological recovery in kits with IVH. Accordingly, PPAR-γ activation enhanced myelination and neurological function in kits with IVH. This also enhanced microglial phagocytosis of red blood cells but did not reduce hydrocephalus. Treatment with PPAR-γ agonist might enhance myelination and neurological recovery in premature infants with IVH.

Keywords: PPAR-γ; microglia; myelin; oligodendrocyte.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Transport Systems, Acidic / deficiency
  • Amino Acid Transport Systems, Acidic / metabolism
  • Animals
  • Animals, Newborn
  • Antiporters / deficiency
  • Antiporters / metabolism
  • Cerebral Intraventricular Hemorrhage / metabolism*
  • Cerebral Intraventricular Hemorrhage / pathology
  • Disease Models, Animal
  • Hereditary Central Nervous System Demyelinating Diseases / metabolism
  • Humans
  • Infant, Premature
  • Microglia / metabolism
  • Mitochondrial Diseases / metabolism
  • Myelin Proteins / biosynthesis*
  • Oligodendroglia / pathology
  • PPAR gamma / agonists
  • PPAR gamma / metabolism*
  • Psychomotor Disorders / metabolism
  • Rabbits
  • Rosiglitazone / pharmacology
  • Sequence Analysis, RNA / methods

Substances

  • Amino Acid Transport Systems, Acidic
  • Antiporters
  • Myelin Proteins
  • PPAR gamma
  • Rosiglitazone

Supplementary concepts

  • Hypomyelination, Global Cerebral