Neurodegeneration, Myelin Loss and Glial Response in the Three-Vessel Global Ischemia Model in Rat

Int J Mol Sci. 2020 Aug 28;21(17):6246. doi: 10.3390/ijms21176246.

Abstract

(1) Background: Although myelin disruption is an integral part of ischemic brain injury, it is rarely the subject of research, particularly in animal models. This study assessed for the first time, myelin and oligodendrocyte loss in a three-vessel model of global cerebral ischemia (GCI), which causes hippocampal damage. In addition, we investigated the relationships between demyelination and changes in microglia and astrocytes, as well as oligodendrogenesis in the hippocampus; (2) Methods: Adult male Wistar rats (n = 15) underwent complete interruption of cerebral blood flow for 7 min by ligation of the major arteries supplying the brain or sham-operation. At 10 and 30 days after the surgery, brain slices were stained for neurodegeneration with Fluoro-Jade C and immunohistochemically to assess myelin content (MBP+ percentage of total area), oligodendrocyte (CNP+ cells) and neuronal (NeuN+ cells) loss, neuroinflammation (Iba1+ cells), astrogliosis (GFAP+ cells) and oligodendrogenesis (NG2+ cells); (3) Results: 10 days after GCI significant myelin and oligodendrocyte loss was found only in the stratum oriens and stratum pyramidale. By the 30th day, demyelination in these hippocampal layers intensified and affected the substratum radiatum. In addition to myelin damage, activation and an increase in the number of microglia and astrocytes in the corresponding layers, a loss of the CA1 pyramidal neurons, and neurodegeneration in the neocortex and thalamus was observed. At a 10-day time point, we observed rod-shaped microglia in the substratum radiatum. Parallel with ongoing myelin loss on the 30th day after ischemia, we found significant oligodendrogenesis in demyelinated hippocampal layers; (4) Conclusions: Our study showed that GCI-simulating cardiac arrest in humans-causes not only the loss of pyramidal neurons in the CA1 field, but also the myelin loss of adjacent layers of the hippocampus.

Keywords: CA1; GCI; global cerebral ischemia; hippocampus; inflammation; myelin; neurodegeneration; oligodendrocyte; oligodendrogenesis; rod-shaped microglia.

MeSH terms

  • 2',3'-Cyclic Nucleotide 3'-Phosphodiesterase / metabolism
  • Animals
  • Antigens / metabolism
  • Antigens, Nuclear / metabolism
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Biomarkers / metabolism*
  • Brain Ischemia / etiology
  • Brain Ischemia / metabolism
  • Brain Ischemia / pathology*
  • Calcium-Binding Proteins / metabolism
  • Glial Fibrillary Acidic Protein / metabolism
  • Male
  • Microfilament Proteins / metabolism
  • Microglia / metabolism
  • Microglia / pathology*
  • Myelin Basic Protein / metabolism
  • Myelin Sheath / metabolism
  • Myelin Sheath / pathology*
  • Nerve Tissue Proteins / metabolism
  • Proteoglycans / metabolism
  • Rats
  • Rats, Wistar

Substances

  • Aif1 protein, rat
  • Antigens
  • Antigens, Nuclear
  • Biomarkers
  • Calcium-Binding Proteins
  • GFAP protein, rat
  • Glial Fibrillary Acidic Protein
  • Mbp protein, rat
  • Microfilament Proteins
  • Myelin Basic Protein
  • Nerve Tissue Proteins
  • Proteoglycans
  • Rbfox3 protein, rat
  • chondroitin sulfate proteoglycan 4
  • 2',3'-Cyclic Nucleotide 3'-Phosphodiesterase
  • Cnp protein, rat