Poststroke Sonic Hedgehog Agonist Treatment Improves Functional Recovery by Enhancing Neurogenesis and Angiogenesis

Stroke. 2017 Jun;48(6):1636-1645. doi: 10.1161/STROKEAHA.117.016650. Epub 2017 May 9.

Abstract

Background and purpose: Because of the limitation in treatment window of the r-tPA (recombinant tissue-type plasminogen activator), the development of delayed treatment for stroke is needed. In this study, we examined the efficacy of delayed poststroke treatment (post 3-8 days) of the sonic hedgehog pathway agonist on functional recovery and the underlying mechanisms.

Methods: We evaluated functional recovery at 1 month after stroke using locomotion analysis and Barnes maze test for cognitive function. We used a genetically inducible neural stem cell-specific reporter mouse line (nestin-CreERT2-R26R-YFP) to label and track their proliferation, survival, and differentiation in ischemic brain. Brain tissue damage, angiogenesis, and cerebral blood flow recovery was evaluated using magnetic resonance imaging techniques and immunostaining.

Results: Our results show that delayed treatment of sonic hedgehog pathway agonist in stroke mice results in enhanced functional recovery both in locomotor function and in cognitive function at 1 month after stroke. Furthermore, using the Nestincre-ERT2-YFP mice, we showed that poststroke sonic hedgehog pathway agonist treatment increased surviving newly born cells derived from both subventricular zone and subgranular zone neural stem cells, total surviving DCX+ (Doublecortin) neuroblast cells, and neurons (NeuN+/YFP+) in the ischemic brain. Sonic hedgehog pathway agonist treatment also improved the brain tissue repair in ischemic region supported by our T2-weighted magnetic resonance imaging, cerebral blood flow map by arterial spin labeling, and immunohistochemistry (α-smooth muscle actin and CD31 immunostaining).

Conclusions: These data confirm an important role for the hedgehog pathway in poststroke brain repair and functional recovery, suggesting a prolonged treatment window for potential treatment strategy to modulate sonic hedgehog pathway after stroke.

Keywords: animals; brain; nestin; neurogenesis; stroke.

MeSH terms

  • Animals
  • Behavior, Animal
  • Brain Ischemia / drug therapy*
  • Disease Models, Animal
  • Doublecortin Protein
  • Hedgehog Proteins / administration & dosage
  • Hedgehog Proteins / agonists*
  • Hedgehog Proteins / pharmacology*
  • Male
  • Maze Learning
  • Mice
  • Mice, Inbred C57BL
  • Motor Activity
  • Neovascularization, Physiologic / drug effects*
  • Nestin
  • Neural Stem Cells
  • Neurogenesis / drug effects*
  • Recovery of Function / drug effects*
  • Stroke / drug therapy*

Substances

  • Dcx protein, mouse
  • Doublecortin Protein
  • Hedgehog Proteins
  • Nestin
  • Shh protein, mouse