Neurogenic Niche Conversion Strategy Induces Migration and Functional Neuronal Differentiation of Neural Precursor Cells Following Brain Injury

Stem Cells Dev. 2020 Feb 15;29(4):235-248. doi: 10.1089/scd.2019.0147. Epub 2020 Jan 6.

Abstract

Glial scars formed after brain injuries provide permissive cues for endogenous neural precursor/stem cells (eNP/SCs) to undergo astrogenesis rather than neurogenesis. Following brain injury, eNP/SCs from the subventricular zone leave their niche, migrate to the injured cortex, and differentiate into reactive astrocytes that contribute to glial scar formation. In vivo neuronal reprogramming, directly converting non-neuronal cells such as reactive astrocytes or NG2 glia into neurons, has greatly improved brain injury repair strategies. However, reprogramming carries a high risk of future clinical applications such as tumorigenicity, involving virus. In this study, we constructed a neural matrix to alter the adverse niche at the injured cortex, enabling eNP/SCs to differentiate into functional neurons. We found that the neural matrix functioned as a "glial trap" that largely concentrated and limited reactive astrocytes to the core of the lesion area, thus altering the adverse niche. The eNP/SCs migrated toward the injured cortex and differentiated into functional neurons. In addition, regenerated neurites extended across the boundary of the injured cortex. Mice treated with the neural matrix demonstrated significant behavioral recovery. For the first time, we induced eNP/SC-derived functional neurons in the cortex after brain injury without the use of viruses, microRNAs, or small molecules. Our novel strategy of applying this "glial trap" to obtain functional neurons in the injured cortex may provide a safer and more natural therapeutic alternative to reprogramming in future clinical applications.

Keywords: brain injury; endogenous neural precursor/stem cells; functional neurons; glial trap; neural matrix; neural regeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Injuries, Traumatic / drug therapy*
  • Brain Injuries, Traumatic / metabolism
  • Brain Injuries, Traumatic / pathology
  • Brain-Derived Neurotrophic Factor / chemistry
  • Brain-Derived Neurotrophic Factor / pharmacology
  • Cell Differentiation / drug effects
  • Cell Movement / drug effects
  • Cellular Reprogramming / drug effects*
  • Cerebral Cortex / drug effects*
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / pathology
  • Chemokine CXCL12 / chemistry
  • Chemokine CXCL12 / pharmacology
  • Chondroitin ABC Lyase / chemistry
  • Chondroitin ABC Lyase / pharmacology
  • Disease Models, Animal
  • Immobilized Proteins / chemistry
  • Immobilized Proteins / pharmacology
  • Lateral Ventricles / cytology
  • Lateral Ventricles / physiology
  • Maze Learning / physiology
  • Mice
  • Mice, Transgenic
  • Nerve Growth Factor / chemistry
  • Nerve Growth Factor / pharmacology
  • Neural Stem Cells / cytology
  • Neural Stem Cells / drug effects
  • Neural Stem Cells / physiology
  • Neurogenesis / drug effects*
  • Neurogenesis / physiology
  • Neuroglia / cytology
  • Neuroglia / drug effects
  • Neuroglia / physiology
  • Neurons / cytology
  • Neurons / drug effects*
  • Neurons / physiology
  • Olfactory Bulb / cytology
  • Olfactory Bulb / physiology
  • Rotarod Performance Test
  • Stem Cell Niche / drug effects

Substances

  • Bdnf protein, mouse
  • Brain-Derived Neurotrophic Factor
  • Chemokine CXCL12
  • Cxcl12 protein, mouse
  • Immobilized Proteins
  • Nerve Growth Factor
  • Chondroitin ABC Lyase