Biofunctionalization of a generic collagenous triple helix with the α2β1 integrin binding site allows molecular force measurements

Int J Biochem Cell Biol. 2011 May;43(5):721-31. doi: 10.1016/j.biocel.2011.01.013. Epub 2011 Jan 22.

Abstract

The integrin α2β1 plays an important role in force-transmitting cell-matrix interactions. It recognizes the peptide sequence GFOGER (O=4-hydroxy-proline) presented as trimer within a collagenous triple-helical framework. We produced the recombinant non-hydroxylated mini-collagen, termed FC3, which harbors the α2β1 integrin recognition site. FC3 consists of a foldon-stabilized host triple helix of three chains with 10 GPP-repeats, into which the integrin binding motif was inserted. The triple-helical structure could further be stabilized by covalently cross-linking the three chains. Unlike collagen-I, FC3 lacks binding sites for matrix proteins and cellular receptors other than the collagen-binding integrins. It showed a preference for α2β1 over α1β1 integrin, especially when the chains were neither cross-linked nor prolyl-hydroxylated. Using FC3 as substratum for primary skin fibroblasts, we showed that the loss of α2β1 integrin could not be compensated by other collagen-binding integrins, suggesting a major role of α2β1 integrin in exerting sufficient mechanical force to induce or sustain cell spreading. Atomic force microscopy revealed that a single α2β1 integrin can withstand tensile forces of up to approximately 160pN before it releases FC3. Moreover, FC3 is fully competent to agonistically elicit α2β1 integrin-induced cell reactions, such as recruitment of α2β1 integrin into focal adhesions and lamellipodia formation. The biofunctionalized mini-collagen sheds light on the molecular forces of the α2β1 integrin-collagen interaction, which affects tissue homeostasis by contracting the connective tissue and by contributing to interstitial tissue pressure regulation. Additionally, biofunctionalized mini-collagens can be useful in force-resistant cell attachment to biomedical materials.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Biomechanical Phenomena
  • Cattle
  • Cell Line, Tumor
  • Collagen Type I / biosynthesis
  • Collagen Type I / chemistry*
  • Collagen Type I / metabolism*
  • Extracellular Matrix / metabolism
  • Humans
  • Integrin alpha2beta1 / metabolism*
  • Microscopy, Atomic Force
  • Protein Structure, Secondary
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Repetitive Sequences, Amino Acid

Substances

  • Collagen Type I
  • Integrin alpha2beta1
  • Recombinant Proteins