Fibroblast activation protein (FAP) is essential for the migration of bone marrow mesenchymal stem cells through RhoA activation

PLoS One. 2014 Feb 13;9(2):e88772. doi: 10.1371/journal.pone.0088772. eCollection 2014.

Abstract

Background: The ability of human bone marrow mesenchymal stem cells (BM-MSCs) to migrate and localize specifically to injured tissues is central in developing therapeutic strategies for tissue repair and regeneration. Fibroblast activation protein (FAP) is a cell surface serine protease expressed at sites of tissue remodeling during embryonic development. It is also expressed in BM-MSCs, but not in normal tissues or cells. The function of FAP in BM-MSCs is not known.

Principal findings: We found that depletion of FAP proteins significantly inhibited the migration of BM-MSCs in a transwell chemotaxis assay. Such impaired migration ability of BM-MSCs could be rescued by re-expressing FAP in these cells. We then demonstrated that depletion of FAP activated intracellular RhoA GTPase. Consistently, inhibition of RhoA activity using a RhoA inhibitor rescued its migration ability. Inhibition of FAP activity with an FAP-specific inhibitor did not affect the activation of RhoA or the migration of BM-MSCs. Furthermore, the inflammatory cytokines interleukin-1beta (IL-1β) and transforming growth factor-beta (TGF-β) upregulated FAP expression, which coincided with better BM-MSC migration.

Conclusions: Our results indicate FAP plays an important role in the migration of BM-MSCs through modulation of RhoA GTPase activity. The peptidase activity of FAP is not essential for such migration. Cytokines IL-1β and TGF-β upregulate the expression level of FAP and thus enhance BM-MSC migration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / drug effects
  • Bone Marrow Cells / metabolism
  • Cell Line
  • Chemotaxis
  • Endopeptidases
  • Enzyme Inhibitors / pharmacology
  • Gelatinases / antagonists & inhibitors
  • Gelatinases / deficiency
  • Gelatinases / genetics*
  • Gene Expression Regulation
  • Genetic Complementation Test
  • Humans
  • Interleukin-1beta / pharmacology
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics*
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / metabolism*
  • Primary Cell Culture
  • Serine Endopeptidases / deficiency
  • Serine Endopeptidases / genetics*
  • Signal Transduction
  • Transforming Growth Factor beta / pharmacology
  • rhoA GTP-Binding Protein / antagonists & inhibitors
  • rhoA GTP-Binding Protein / genetics*
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Enzyme Inhibitors
  • Interleukin-1beta
  • Membrane Proteins
  • Transforming Growth Factor beta
  • RHOA protein, human
  • Endopeptidases
  • Serine Endopeptidases
  • fibroblast activation protein alpha
  • Gelatinases
  • rhoA GTP-Binding Protein

Grants and funding

The work was supported by (NRPGMNRPGM-98LC009), National Science Council (NSC 98-3112-B-400-013), Taiwan and National Health Research Institutes, Taiwan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.