Oligomerization-dependent regulation of motility and morphogenesis by the collagen XVIII NC1/endostatin domain

J Cell Biol. 2001 Mar 19;152(6):1233-46. doi: 10.1083/jcb.152.6.1233.

Abstract

Collagen XVIII (c18) is a triple helical endothelial/epithelial basement membrane protein whose noncollagenous (NC)1 region trimerizes a COOH-terminal endostatin (ES) domain conserved in vertebrates, Caenorhabditis elegans and Drosophila. Here, the c18 NC1 domain functioned as a motility-inducing factor regulating the extracellular matrix (ECM)-dependent morphogenesis of endothelial and other cell types. This motogenic activity required ES domain oligomerization, was dependent on rac, cdc42, and mitogen-activated protein kinase, and exhibited functional distinction from the archetypal motogenic scatter factors hepatocyte growth factor and macrophage stimulatory protein. The motility-inducing and mitogen-activated protein kinase-stimulating activities of c18 NC1 were blocked by its physiologic cleavage product ES monomer, consistent with a proteolysis-dependent negative feedback mechanism. These data indicate that the collagen XVIII NC1 region encodes a motogen strictly requiring ES domain oligomerization and suggest a previously unsuspected mechanism for ECM regulation of motility and morphogenesis.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Angiogenesis Inhibitors / genetics
  • Angiogenesis Inhibitors / metabolism
  • Animals
  • Bacterial Proteins*
  • Bacterial Toxins / pharmacology
  • Blotting, Western
  • Cell Movement / drug effects
  • Cell Movement / physiology*
  • Cells, Cultured
  • Collagen / chemistry
  • Collagen / genetics
  • Collagen / metabolism*
  • Collagen Type XVIII
  • Cytotoxins / pharmacology
  • Dimerization
  • Endostatins
  • Endothelium, Vascular / cytology*
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / growth & development
  • Extracellular Matrix / physiology*
  • Humans
  • Mice
  • Mitogen-Activated Protein Kinases / metabolism
  • Morphogenesis
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism*
  • Protein Structure, Tertiary*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • cdc42 GTP-Binding Protein / genetics
  • cdc42 GTP-Binding Protein / metabolism
  • rac GTP-Binding Proteins / genetics
  • rac GTP-Binding Proteins / metabolism
  • rho GTP-Binding Proteins / metabolism

Substances

  • Angiogenesis Inhibitors
  • Bacterial Proteins
  • Bacterial Toxins
  • Collagen Type XVIII
  • Cytotoxins
  • Endostatins
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • toxB protein, Clostridium difficile
  • Collagen
  • Mitogen-Activated Protein Kinases
  • cdc42 GTP-Binding Protein
  • rac GTP-Binding Proteins
  • rho GTP-Binding Proteins