M2-like macrophages are responsible for collagen degradation through a mannose receptor-mediated pathway

J Cell Biol. 2013 Sep 16;202(6):951-66. doi: 10.1083/jcb.201301081. Epub 2013 Sep 9.

Abstract

Tissue remodeling processes critically depend on the timely removal and remodeling of preexisting collagen scaffolds. Nevertheless, many aspects related to the turnover of this abundant extracellular matrix component in vivo are still incompletely understood. We therefore took advantage of recent advances in optical imaging to develop an assay to visualize collagen turnover in situ and identify cell types and molecules involved in this process. Collagen introduced into the dermis of mice underwent cellular endocytosis in a partially matrix metalloproteinase-dependent manner and was subsequently routed to lysosomes for complete degradation. Collagen uptake was predominantly executed by a quantitatively minor population of M2-like macrophages, whereas more abundant Col1a1-expressing fibroblasts and Cx3cr1-expressing macrophages internalized collagen at lower levels. Genetic ablation of the collagen receptors mannose receptor (Mrc1) and urokinase plasminogen activator receptor-associated protein (Endo180 and Mrc2) impaired this intracellular collagen degradation pathway. This study demonstrates the importance of receptor-mediated cellular uptake to collagen turnover in vivo and identifies a key role of M2-like macrophages in this process.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis
  • Blotting, Western
  • CX3C Chemokine Receptor 1
  • Cell Proliferation
  • Cells, Cultured
  • Collagen / metabolism*
  • Collagen Type I / physiology*
  • Collagen Type I, alpha 1 Chain
  • Endocytosis / physiology
  • Female
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Immunoenzyme Techniques
  • Lysosomes / metabolism
  • Macrophages / cytology
  • Macrophages / metabolism*
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • RNA, Messenger / genetics
  • Real-Time Polymerase Chain Reaction
  • Receptors, Cell Surface / physiology*
  • Receptors, Chemokine / physiology*
  • Receptors, Immunologic
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction

Substances

  • CX3C Chemokine Receptor 1
  • Collagen Type I
  • Collagen Type I, alpha 1 Chain
  • Cx3cr1 protein, mouse
  • MRC1 protein, mouse
  • Membrane Glycoproteins
  • Mrc2 protein, mouse
  • RNA, Messenger
  • Receptors, Cell Surface
  • Receptors, Chemokine
  • Receptors, Immunologic
  • Green Fluorescent Proteins
  • Collagen