Fibroblast integrin α11β1 is a collagen assembly receptor in mechanoregulated fibrillar adhesions

Matrix Biol. 2024 Dec:134:144-161. doi: 10.1016/j.matbio.2024.10.006. Epub 2024 Oct 13.

Abstract

Solid epithelial cancers with significant desmoplasia are characterized by an excessive deposition of collagen-based matrix, which often supports tumor progression. However, the mechanism of how collagen receptors mediate collagen fibrillogenesis still remains mostly unclear. We show that the collagen-binding integrin α11β1 can co-localize with tensin-1 and deposited collagen I in human pancreatic ductal adenocarcinoma (PDAC) stroma. In addition to the canonical fibrillar adhesion integrin α5β1 expressed by human PDAC cancer-associated fibroblasts (CAFs), tensin-1-positive fibrillar adhesions contained α11β1 but lacked α1β1 and α2β1. CAFs lacking α5β1 expression displayed mechanoregulated and tensin-1 dependent α11β1 fibrillar adhesions, suggesting independent roles of the two integrins with regards to fibrillar adhesions-based de novo fibrillogenesis. Further, we demonstrate that cell surface-associated collagen I assembly necessitated α11β1, but not α5β1 expression. In summary, α11β1 integrin is a novel component of fibrillar adhesions, which is strategically positioned to mediate de novo collagen fibrillogenesis at the cell surface under pro-fibrotic conditions.

Keywords: Cancer-associated fibroblast; Collagen assembly; Fibrillar adhesions; Fibrosis; Integrin.

MeSH terms

  • Cancer-Associated Fibroblasts / metabolism
  • Cancer-Associated Fibroblasts / pathology
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Carcinoma, Pancreatic Ductal* / pathology
  • Cell Adhesion
  • Cell Line, Tumor
  • Collagen Type I / genetics
  • Collagen Type I / metabolism
  • Extracellular Matrix / metabolism
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Humans
  • Integrin alpha5beta1 / genetics
  • Integrin alpha5beta1 / metabolism
  • Integrins* / genetics
  • Integrins* / metabolism
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism
  • Pancreatic Neoplasms* / pathology
  • Receptors, Collagen / genetics
  • Receptors, Collagen / metabolism
  • Tensins / genetics
  • Tensins / metabolism

Substances

  • integrin alpha11beta1
  • Integrins
  • Collagen Type I
  • Integrin alpha5beta1
  • Receptors, Collagen
  • Tensins