Endogenous Mobilization of Bone-Marrow Cells Into the Murine Retina Induces Fusion-Mediated Reprogramming of Müller Glia Cells

EBioMedicine. 2018 Apr:30:38-51. doi: 10.1016/j.ebiom.2018.02.023. Epub 2018 Feb 28.

Abstract

Müller glial cells (MGCs) represent the most plastic cell type found in the retina. Following injury, zebrafish and avian MGCs can efficiently re-enter the cell cycle, proliferate and generate new functional neurons. The regenerative potential of mammalian MGCs, however, is very limited. Here, we showed that N-methyl-d-aspartate (NMDA) damage stimulates murine MGCs to re-enter the cell cycle and de-differentiate back to a progenitor-like stage. These events are dependent on the recruitment of endogenous bone marrow cells (BMCs), which, in turn, is regulated by the stromal cell-derived factor 1 (SDF1)-C-X-C motif chemokine receptor type 4 (CXCR4) pathway. BMCs mobilized into the damaged retina can fuse with resident MGCs, and the resulting hybrids undergo reprogramming followed by re-differentiation into cells expressing markers of ganglion and amacrine neurons. Our findings constitute an important proof-of-principle that mammalian MGCs retain their regenerative potential, and that such potential can be activated via cell fusion with recruited BMCs. In this perspective, our study could contribute to the development of therapeutic strategies based on the enhancement of mammalian endogenous repair capabilities.

Keywords: Bone-marrow cells; Cell fusion-mediated reprogramming; Endogenous migration; Müller glial cells; NMDA-damage; Retinal damage; SDF1/CXCR4 pathway.

MeSH terms

  • Amacrine Cells / cytology
  • Amacrine Cells / drug effects
  • Animals
  • Bone Marrow Cells / cytology*
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / metabolism
  • Cell Dedifferentiation / drug effects
  • Cell Fusion
  • Cell Proliferation / drug effects
  • Cellular Reprogramming* / drug effects
  • Chemokine CXCL12 / metabolism
  • Mice, Transgenic
  • N-Methylaspartate / toxicity
  • Neuroglia / cytology*
  • Neuroglia / drug effects
  • Receptors, CXCR4 / metabolism
  • Retina / cytology*
  • Retinal Ganglion Cells / cytology
  • Retinal Ganglion Cells / drug effects
  • Signal Transduction

Substances

  • Chemokine CXCL12
  • Cxcl12 protein, mouse
  • Receptors, CXCR4
  • N-Methylaspartate