Unique charge-dependent constraint on collagen recognition by integrin α10β1

Matrix Biol. 2017 May:59:80-94. doi: 10.1016/j.matbio.2016.08.010. Epub 2016 Aug 25.

Abstract

The collagen-binding integrins recognise collagen through their inserted (I) domain, where co-ordination of a Mg2+ ion in the metal ion-dependent site is reorganised by ligation by a collagen glutamate residue found in specific collagen hexapeptide motifs. Here we show that GROGER, found in the N-terminal domain of collagens I and III, is only weakly recognised by α10β1, an important collagen receptor on chondrocytes, contrasting with the other collagen-binding integrins. Alignment of I domain sequence and molecular modelling revealed a clash between a unique arginine residue (R215) in α10β1 and the positively-charged GROGER. Replacement of R215 with glutamine restored binding. Substituting arginine at the equivalent locus (Q214) in integrins α1 and α2 I domains impaired their binding to GROGER. Collagen II, abundant in cartilage, lacks GROGER. GRSGET is uniquely expressed in the C-terminus of collagen II, but this motif is similarly not recognised by α10β1. These data suggest an evolutionary imperative to maintain accessibility of the terminal domains of collagen II in tissues such as cartilage, perhaps during endochondral ossification, where α10β1 is the main collagen-binding integrin.

Keywords: C2C12 cells; Cartilage; GROGER; Integrin I domain; Triple-helical peptides.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Animals
  • Binding Sites
  • Cations, Divalent
  • Cell Line
  • Collagen Type II / chemistry*
  • Collagen Type II / genetics
  • Collagen Type II / metabolism
  • Edetic Acid / chemistry
  • Gene Expression
  • Humans
  • Integrin alpha Chains / chemistry*
  • Integrin alpha Chains / genetics
  • Integrin alpha Chains / metabolism
  • Magnesium / chemistry*
  • Mice
  • Models, Molecular
  • Muscle Fibers, Skeletal / cytology
  • Muscle Fibers, Skeletal / metabolism
  • Peptides / chemical synthesis
  • Peptides / metabolism*
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Static Electricity

Substances

  • Cations, Divalent
  • Collagen Type II
  • Integrin alpha Chains
  • Peptides
  • Recombinant Proteins
  • integrin alpha 10
  • Edetic Acid
  • Magnesium