Plasticity response in the contralesional hemisphere after subtle neurotrauma: gene expression profiling after partial deafferentation of the hippocampus

PLoS One. 2013 Jul 25;8(7):e70699. doi: 10.1371/journal.pone.0070699. Print 2013.

Abstract

Neurotrauma or focal brain ischemia are known to trigger molecular and structural responses in the uninjured hemisphere. These responses may have implications for tissue repair processes as well as for the recovery of function. To determine whether the plasticity response in the uninjured hemisphere occurs even after a subtle trauma, we subjected mice to a partial unilateral deafferentation of the hippocampus induced by stereotactically performed entorhinal cortex lesion (ECL). The expression of selected genes was assessed by quantitative real-time PCR in the hippocampal tissue at the injured side and the contralesional side at day 4 and 14 after injury. We observed that expression of genes coding for synaptotagmin 1, ezrin, thrombospondin 4, and C1q proteins, that have all been implicated in the synapse formation, re-arrangement and plasticity, were upregulated both in the injured and the contralesional hippocampus, implying a plasticity response in the uninjured hemisphere. Several of the genes, the expression of which was altered in response to ECL, are known to be expressed in astrocytes. To test whether astrocyte activation plays a role in the observed plasticity response to ECL, we took advantage of mice deficient in two intermediate filament (nanofilament) proteins glial fibrillary acidic protein (GFAP) and vimentin (GFAP(-/-)Vim(-/-) ) and exhibiting attenuated astrocyte activation and reactive gliosis. The absence of GFAP and vimentin reduced the ECL-induced upregulation of thrombospondin 4, indicating that this response to ECL depends on astrocyte activation and reactive gliosis. We conclude that even a very limited focal neurotrauma triggers a distinct response at the contralesional side, which at least to some extent depends on astrocyte activation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Afferent Pathways / injuries
  • Afferent Pathways / metabolism*
  • Animals
  • Astrocytes / metabolism
  • Astrocytes / pathology
  • Cerebrum / injuries
  • Cerebrum / metabolism*
  • Craniocerebral Trauma / metabolism*
  • Craniocerebral Trauma / physiopathology
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism
  • Entorhinal Cortex / injuries
  • Entorhinal Cortex / metabolism*
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Glial Fibrillary Acidic Protein
  • Hippocampus / injuries
  • Hippocampus / metabolism*
  • Male
  • Mice
  • Mice, Knockout
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / genetics
  • Neuronal Plasticity*
  • Stereotaxic Techniques
  • Synaptotagmin I / genetics
  • Synaptotagmin I / metabolism
  • Thrombospondins / genetics
  • Thrombospondins / metabolism
  • Vimentin / deficiency
  • Vimentin / genetics

Substances

  • Cytoskeletal Proteins
  • Glial Fibrillary Acidic Protein
  • Nerve Tissue Proteins
  • Synaptotagmin I
  • Syt1 protein, mouse
  • Thrombospondins
  • Vimentin
  • ezrin
  • glial fibrillary astrocytic protein, mouse
  • thrombospondin 4

Grants and funding

This work was supported by the Swedish Medical Research Council (project 11548), AFA Insurance, ALF Göteborg (project 11392), Sten A. Olsson Foundation for Research and Culture, VINNOVA Health Program, the Swedish Stroke Foundation, the Swedish Society of Medicine, the Free Mason Foundation, Wilhelm and Martina Lundgren Foundations, NanoNet COST Action (BM1002), the EU FP 7 Program EduGlia (237956) and the EU FP 7 Program TargetBraIn (279017). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.