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Oligogenesis and oligodendrocyte progenitor maturation vary in different brain regions and partially correlate with local angiogenesis after ischemic stroke.

ABSTRACT: Oligogenesis plays an important role in functional recovery after ischemic stroke. We tested the hypothesis that oligogenesis and the maturation of oligodendrocyte progenitor cells (OPCs) vary in different brain regions using a rat transient middle cerebral artery occlusion (tMCAO) model. Compared to Day 1, olig2(+) OPCs and oligodendrocytes (OLGs) increased in the peri-infarct basal ganglia (BG) 7 (44%) and 14 (61%) days after 2 hours of MCAO; OPCs (PDGFRα(+)) and OLGs (CC1(+)) increased in this region 14 days after tMCAO by 139% and 126%, respectively. Although the olig2(+) cells and OLGs did not increase significantly in the peri-infarct cortex (CTX), the OPCs increased in this region by 95% at Day 14 vs. Day 1 after tMCAO. The numbers of OPCs and OLGs remained low after an initial reduction at Day 1 in the peri-infarct corpus callosum (CC). Correlation analyses showed that the numbers of olig2(+) cells (r=0.73, P=0.03) and OLGs (r=0.74, P=0.02) correlated with local vessel density; however, the number of OPCs did not correlate with vessel density (r=0.43, P=0.24). Our data show that oligogenesis and the maturation of OPCs differ in various brain regions and the difference in regional angiogenic response is one of the potential reasons.

SUBMITTER: Jiang L

PROVIDER: S-EPMC3196661 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Oligogenesis and oligodendrocyte progenitor maturation vary in different brain regions and partially correlate with local angiogenesis after ischemic stroke.

Jiang Lidan L Shen Fanxia F Degos Vincent V Schonemann Marcus M Pleasure Samuel J SJ Mellon Synthia H SH Young William L WL Su Hua H

Translational stroke research 20110901 3

Oligogenesis plays an important role in functional recovery after ischemic stroke. We tested the hypothesis that oligogenesis and the maturation of oligodendrocyte progenitor cells (OPCs) vary in different brain regions using a rat transient middle cerebral artery occlusion (tMCAO) model. Compared to Day 1, olig2(+) OPCs and oligodendrocytes (OLGs) increased in the peri-infarct basal ganglia (BG) 7 (44%) and 14 (61%) days after 2 hours of MCAO; OPCs (PDGFRα(+)) and OLGs (CC1(+)) increased in thi ...[more]

PMID: 22022343

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Project description:IntroductionRemyelination of demyelinated axons can occur as an endogenous repair mechanism in multiple sclerosis (MS), but its efficacy varies between both MS individuals and lesions. The molecular and cellular mechanisms that drive remyelination remain poorly understood. Here, we studied the relation between microglia activation and remyelination activity in MS.MethodsWe correlated regenerative (CD163+) and inflammatory (iNOS+) microglia with BCAS1+ oligodendrocytes, subdivided into early-stage (<3 processes) and late-stage (≥3 processes) cells in brain donors with high or low remyelinating potential in remyelinated lesions and active lesions with ramified/amoeboid (non-foamy) or foamy microglia. A cohort of MS donors categorized as efficiently remyelinating donors (ERDs; n=25) or poorly remyelinating donors (PRDs; n=17) was included, based on their proportion of remyelinated lesions at autopsy.Results and discussionWe hypothesized more CD163+ microglia and BCAS1+ oligodendrocytes in remyelinated and active non-foamy lesions from ERDs and more iNOS+ microglia with fewer BCAS1+ oligodendrocytes in active foamy lesions from PRDs. For CD163+ microglia, however, no differences were observed between MS lesions and MS donor groups. In line with our hypothesis, we found that INOS+ microglia were significantly increased in PRDs compared to ERDs within remyelinated lesions. MS lesions, more late-stage BCAS1+ oligodendrocytes were detected in active lesions with non-foamy or foamy microglia in comparison with remyelinated lesions. Although no differences were found for early-stage BCAS1+ oligodendrocytes between MS lesions, we did find significantly more early-stage BCAS1+ oligodendrocytes in PRDs vs ERDs in remyelinated lesions. Interestingly, a positive correlation was identified between iNOS+ microglia and the presence of early-stage BCAS1+ oligodendrocytes. These findings suggest that impaired maturation of early-stage BCAS1+ oligodendrocytes, encountering inflammatory microglia, may underlie remyelination deficits and unsuccessful lesion repair in MS.

Project description:Premature birth or complications during labor can cause temporary disruption of cerebral blood flow, often followed by long-term disturbances in brain development called hypoxic-ischemic (HI) encephalopathy. Diffuse damage to the white matter is the most frequently detected pathology in this condition. We hypothesized that oligodendrocyte progenitor cell (OPC) differentiation disturbed by mild neonatal asphyxia may affect the viability, maturation, and physiological functioning of oligodendrocytes. To address this issue, we studied the effect of temporal HI in the in vivo model in P7 rats with magnetic resonance imaging (MRI), microscopy techniques and biochemical analyses. Moreover, we recreated the injury in vitro performing the procedure of oxygen-glucose deprivation on rat neonatal OPCs to determine its effect on cell viability, proliferation, and differentiation. In the in vivo model, MRI evaluation revealed changes in the volume of different brain regions, as well as changes in the directional diffusivity of water in brain tissue that may suggest pathological changes to myelinated neuronal fibers. Hypomyelination was observed in the cortex, striatum, and CA3 region of the hippocampus. Severe changes to myelin ultrastructure were observed, including delamination of myelin sheets. Interestingly, shortly after the injury, an increase in oligodendrocyte proliferation was observed, followed by an overproduction of myelin proteins 4 weeks after HI. Results verified with the in vitro model indicate, that in the first days after damage, OPCs do not show reduced viability, intensively proliferate, and overexpress myelin proteins and oligodendrocyte-specific transcription factors. In conclusion, despite the increase in oligodendrocyte proliferation and myelin protein expression after HI, the production of functional myelin sheaths in brain tissue is impaired. Presented study provides a detailed description of oligodendrocyte pathophysiology developed in an effect of HI injury, resulting in an altered CNS myelination. The described models may serve as useful tools for searching and testing effective of effective myelination-supporting therapies for HI injuries.

Dataset Information

Oligogenesis and oligodendrocyte progenitor maturation vary in different brain regions and partially correlate with local angiogenesis after ischemic stroke.

Publications

Oligogenesis and oligodendrocyte progenitor maturation vary in different brain regions and partially correlate with local angiogenesis after ischemic stroke.

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