MCSF orchestrates branching morphogenesis in developing submandibular gland tissue

J Cell Sci. 2017 May 1;130(9):1559-1569. doi: 10.1242/jcs.196907. Epub 2017 Mar 27.

Abstract

The importance of macrophages in tissue development and regeneration has been strongly emphasized. However, the specific roles of macrophage colony-stimulating factor (MCSF), the key regulator of macrophage differentiation, in glandular tissue development have been unexplored. Here, we disclose new macrophage-independent roles of MCSF in tissue development. We initially found that MCSF is markedly upregulated at embryonic day (E)13.5, at a stage preceding the colonization of macrophages (at E15.5), in mouse submandibular gland (SMG) tissue. Surprisingly, MCSF-induced branching morphogenesis was based on a direct effect on epithelial cells, as well as indirectly, by modulating the expression of major growth factors of SMG growth, FGF7 and FGF10, via the phosphoinositide 3-kinase (PI3K) pathway. Additionally, given the importance of neurons in SMG organogenesis, we found that MCSF-induced SMG growth was associated with regulation of neurturin expression and neuronal network development during early SMG development in an in vitro organogenesis model as well as in vivo These results indicate that MCSF plays pleiotropic roles and is an important regulator of early SMG morphogenesis.

Keywords: 3D culture; Branching morphogenesis; Fibroblast growth factor; Macrophage colony-stimulating factor; Neurturin; Salivary gland.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Epithelium / drug effects
  • Epithelium / embryology
  • Epithelium / metabolism
  • Fibroblast Growth Factor 10 / metabolism
  • Fibroblast Growth Factor 7 / metabolism
  • Macrophage Colony-Stimulating Factor / pharmacology*
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Mice, Inbred ICR
  • Morphogenesis / drug effects*
  • Neuronal Outgrowth / drug effects
  • Neurturin / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Signal Transduction / drug effects
  • Submandibular Gland / drug effects
  • Submandibular Gland / growth & development*
  • Submandibular Gland / metabolism

Substances

  • Fibroblast Growth Factor 10
  • Neurturin
  • Nrtn protein, mouse
  • Fibroblast Growth Factor 7
  • Macrophage Colony-Stimulating Factor
  • Phosphatidylinositol 3-Kinases