Implication of anti-inflammatory macrophages in regenerative moto-neuritogenesis: promotion of myoblast migration and neural chemorepellent semaphorin 3A expression in injured muscle

Int J Biochem Cell Biol. 2014 Sep:54:272-85. doi: 10.1016/j.biocel.2014.05.032. Epub 2014 Jun 2.

Abstract

Regenerative mechanisms that regulate intramuscular motor innervation are thought to reside in the spatiotemporal expression of axon-guidance molecules. Our previous studies proposed a heretofore unexplored role of resident myogenic stem cell (satellite cell)-derived myoblasts as a key presenter of a secreted neural chemorepellent semaphorin 3A (Sema3A); hepatocyte growth factor (HGF) triggered its expression exclusively at the early-differentiation phase. In order to verify this concept, the present study was designed to clarify a paracrine source of HGF release. In vitro experiments demonstrated that activated anti-inflammatory macrophages (CD206-positive M2) produce HGF and thereby promote myoblast chemoattraction and Sema3A expression. Media from pro-inflammatory macrophage cultures (M1) did not show any significant effect. M2 also enhanced the expression of myoblast-differentiation markers in culture, and infiltrated predominantly at the early-differentiation phase (3-5 days post-injury); M2 were confirmed to produce HGF as monitored by in vivo/ex vivo immunocytochemistry of CD11b/CD206/HGF-positive cells and by HGF in situ hybridization of cardiotoxin- or crush-injured tibialis anterior muscle, respectively. These studies advance our understanding of the stage-specific activation of Sema3A expression signaling. Findings, therefore, encourage the idea that M2 contribute to spatiotemporal up-regulation of extracellular Sema3A concentrations by producing HGF that, in turn, stimulates a burst of Sema3A secretion by myoblasts that are recruited to site of injury. This model may ensure a coordinated delay in re-attachment of motoneuron terminals onto damaged fibers early in muscle regeneration, and thus synchronize the recovery of muscle-fiber integrity and the early resolution of inflammation after injury.

Keywords: Activated macrophage; Hepatocyte growth factor; Migration; Regenerative moto-neuritogenesis; Semaphorin 3A.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / metabolism
  • Blotting, Western
  • Cell Differentiation*
  • Cell Movement*
  • Cells, Cultured
  • Hepatocyte Growth Factor / metabolism
  • In Situ Hybridization
  • Macrophages / cytology
  • Macrophages / drug effects
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Motor Neurons / cytology*
  • Motor Neurons / drug effects
  • Motor Neurons / immunology
  • Motor Neurons / metabolism
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / injuries
  • Muscle, Skeletal / metabolism*
  • Myoblasts, Skeletal / cytology
  • Myoblasts, Skeletal / drug effects
  • Myoblasts, Skeletal / metabolism*
  • Nerve Regeneration / physiology*
  • Neurogenesis / physiology
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Reverse Transcriptase Polymerase Chain Reaction
  • Semaphorin-3A / genetics
  • Semaphorin-3A / metabolism*
  • Signal Transduction

Substances

  • Anti-Inflammatory Agents
  • RNA, Messenger
  • Sema3a protein, mouse
  • Semaphorin-3A
  • Hepatocyte Growth Factor