Differential Smad2/3 linker phosphorylation is a crosstalk mechanism of Rho/ROCK and canonical TGF-β3 signaling in tenogenic differentiation

Sci Rep. 2024 May 6;14(1):10393. doi: 10.1038/s41598-024-60717-z.

Abstract

The transforming growth factor (TGF)-β3 is a well-known inducer for tenogenic differentiation, signaling via the Smad2/3 pathway. Furthermore, other factors like extracellular matrix or mechanical force can induce tenogenic differentiation and possibly alter the response to TGF-β3 by signaling via the Rho/ROCK pathway. The aim of this study was to investigate the interplay of Rho/ROCK and TGF-β3/Smad signaling in tenogenic differentiation, with the Smad2/3 molecule hypothesized as a possible interface. Cultured as monolayers or on collagen I matrices, mesenchymal stromal cells (MSC) were treated with the ROCK inhibitor Y-27632 (10 µM), TGF-β3 (10 ng/ml) or both combined. Control cells were cultured accordingly, without Y-27632 and/or without TGF-β3. At different time points, MSC were analyzed by real-time RT-PCR, immunofluorescence, and Western blot. Cultivation of MSC on collagen matrices and ROCK inhibition supported tenogenic differentiation and fostered the effect of TGF-β3. The phosphorylation of the linker region of Smad2 was reduced by cultivation on collagen matrices, but not by ROCK inhibition. The latter, however, led to increased phosphorylation of the linker region of Smad3. In conclusion, collagen matrices and the Rho/ROCK signaling pathway influence the TGF-β3/Smad2/3 pathway by regulating different phosphorylation sites of the Smad linker region.

Keywords: Linker phosphorylation; Mesenchymal stem cells; Smad; Tenogenic differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amides / pharmacology
  • Cell Differentiation* / drug effects
  • Cells, Cultured
  • Humans
  • Mesenchymal Stem Cells* / cytology
  • Mesenchymal Stem Cells* / drug effects
  • Mesenchymal Stem Cells* / metabolism
  • Phosphorylation
  • Pyridines / pharmacology
  • Signal Transduction*
  • Smad2 Protein* / metabolism
  • Smad3 Protein* / metabolism
  • Transforming Growth Factor beta3* / metabolism
  • rho GTP-Binding Proteins / metabolism
  • rho-Associated Kinases* / metabolism

Substances

  • rho-Associated Kinases
  • Smad2 Protein
  • Smad3 Protein
  • Transforming Growth Factor beta3
  • SMAD3 protein, human
  • SMAD2 protein, human
  • Y 27632
  • Pyridines
  • Amides
  • rho GTP-Binding Proteins