Delivery of CSF-1R to the lumen of macropinosomes promotes its destruction in macrophages

J Cell Sci. 2014 Dec 15;127(Pt 24):5228-39. doi: 10.1242/jcs.154393. Epub 2014 Oct 21.

Abstract

Activation of the macrophage colony stimulating factor-1 receptor (CSF-1R) by CSF-1 stimulates pronounced macropinocytosis and drives proliferation of macrophages. Although the role of macropinocytosis in CSF-1R signaling remains unknown, we show here that, despite internalizing large quantities of plasma membrane, macropinosomes contribute little to the internalization of the CSF-1-CSF-1R complex. Rather, internalization of the CSF-1R in small endocytic vesicles that are sensitive to clathrin disruption, outcompetes macropinosomes for CSF-1R endocytosis. Following internalization, small vesicles carrying the CSF-1R underwent homotypic fusion and then trafficked to newly formed macropinosomes bearing Rab5. As these macropinosomes matured, acquiring Rab7, the CSF-1R was transported into their lumen and degraded. Inhibition of macropinocytosis delayed receptor degradation despite no disruption to CSF-1R endocytosis. These data indicate that CSF-1-stimulated macropinosomes are sites of multivesicular body formation and accelerate CSF-1R degradation. Furthermore, we demonstrate that macropinocytosis and cell growth have a matching dose dependence on CSF-1, suggesting that macropinosomes might be a central mechanism coupling CSF-1R signaling and macrophage growth.

Keywords: CSF-1R; Endocytosis; M-CSF; Macrophage; Macropinosome.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / drug effects
  • Clathrin / metabolism
  • Endocytosis / drug effects
  • Endosomes / drug effects
  • Endosomes / metabolism
  • Humans
  • Macrophage Colony-Stimulating Factor / pharmacology
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Mice, Inbred C57BL
  • Mitogens / pharmacology
  • Models, Biological
  • Pinocytosis* / drug effects
  • Protein Transport / drug effects
  • Proteolysis / drug effects
  • Receptor, Macrophage Colony-Stimulating Factor / metabolism*
  • rab GTP-Binding Proteins / metabolism
  • rab5 GTP-Binding Proteins / metabolism
  • rab7 GTP-Binding Proteins

Substances

  • Clathrin
  • Mitogens
  • rab7 GTP-Binding Proteins
  • rab7 GTP-binding proteins, human
  • rab7 GTP-binding proteins, mouse
  • Macrophage Colony-Stimulating Factor
  • Receptor, Macrophage Colony-Stimulating Factor
  • rab GTP-Binding Proteins
  • rab5 GTP-Binding Proteins