The NMDA receptor functions independently and as an LRP1 co-receptor to promote Schwann cell survival and migration

J Cell Sci. 2015 Sep 15;128(18):3478-88. doi: 10.1242/jcs.173765. Epub 2015 Aug 13.

Abstract

NMDA receptors (NMDA-Rs) are ionotropic glutamate receptors, which associate with LDL-receptor-related protein-1 (LRP1) to trigger cell signaling in response to protein ligands in neurons. Here, we demonstrate for the first time that the NMDA-R is expressed by rat Schwann cells and functions independently and with LRP1 to regulate Schwann cell physiology. The NR1 (encoded by GRIN1) and NR2b (encoded by GRIN2B) NMDA-R subunits were expressed by cultured Schwann cells and upregulated in sciatic nerves following crush injury. The ability of LRP1 ligands to activate ERK1/2 (also known as MAPK3 and MAPK1, respectively) and promote Schwann cell migration required the NMDA-R. NR1 gene silencing compromised Schwann cell survival. Injection of the LRP1 ligands tissue-type plasminogen activator (tPA, also known as PLAT) or MMP9-PEX into crush-injured sciatic nerves activated ERK1/2 in Schwann cells in vivo, and the response was blocked by systemic treatment with the NMDA-R inhibitor MK801. tPA was unique among the LRP1 ligands examined because tPA activated cell signaling and promoted Schwann cell migration by interacting with the NMDA-R independently of LRP1, albeit with delayed kinetics. These results define the NMDA-R as a Schwann cell signaling receptor for protein ligands and a major regulator of Schwann cell physiology, which may be particularly important in peripheral nervous system (PNS) injury.

Keywords: LRP1; MMP9; NMDA receptor; Peripheral nerve; Schwann cell; Tissue-type plasminogen activator; α2-macroglobulin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Dizocilpine Maleate / pharmacology
  • Low Density Lipoprotein Receptor-Related Protein-1 / metabolism*
  • MAP Kinase Signaling System
  • Matrix Metalloproteinase 9 / metabolism
  • Peripheral Nerve Injuries / metabolism
  • RNA Interference
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Schwann Cells / physiology*
  • Sciatic Nerve
  • Signal Transduction
  • Tissue Plasminogen Activator / metabolism

Substances

  • Low Density Lipoprotein Receptor-Related Protein-1
  • Receptors, N-Methyl-D-Aspartate
  • Dizocilpine Maleate
  • Tissue Plasminogen Activator
  • Matrix Metalloproteinase 9
  • Mmp9 protein, rat