Altered TGF-β endocytic trafficking contributes to the increased signaling in Marfan syndrome

Biochim Biophys Acta Mol Basis Dis. 2018 Feb;1864(2):554-562. doi: 10.1016/j.bbadis.2017.11.015. Epub 2017 Nov 23.

Abstract

The main cardiovascular alteration in Marfan syndrome (MFS) is the formation of aortic aneurysms in which augmented TGF-β signaling is reported. However, the primary role of TGF-β signaling as a molecular link between the genetic mutation of fibrillin-1 and disease onset is controversial. The compartmentalization of TGF-β endocytic trafficking has been shown to determine a signaling response in which clathrin-dependent internalization leads to TGF-β signal propagation, and caveolin-1 (CAV-1) associated internalization leads to signal abrogation. We here studied the contribution of endocytic trafficking compartmentalization to increased TGF-β signaling in vascular smooth muscle cells (VSMC) from MFS patients. We examined molecular components involved in clathrin- (SARA, SMAD2) and caveolin-1- (SMAD7, SMURF2) dependent endocytosis. Marfan VSMC showed higher recruitment of SARA and SMAD2 to membranes and their increased interaction with TGF-β receptor II, as well as higher colocalization of SARA with the early endosome marker EEA1. We assessed TGF-β internalization using a biotinylated ligand (b-TGF-β), which colocalized equally with either EEA1 or CAV-1 in VSMC from Marfan patients and controls. However, in Marfan cells, colocalization of b-TGF-β with SARA and EEA1 was increased and accompanied by decreased colocalization with CAV-1 at EEA1-positive endosomes. Moreover, Marfan VSMC showed higher transcriptional levels and membrane enrichment of RAB5. Our results indicate that increased RAB5-associated SARA localization to early endosomes facilitates its TGF-β receptor binding and phosphorylation of signaling mediator SMAD2 in Marfan VSMC. This is accompanied by a reduction of TGF-β sorting into multifunctional vesicles containing cargo from both internalization pathways.

Keywords: Endocytosis; Human vascular smooth muscle cells; Marfan syndrome; Membrane trafficking; TGF-β signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Caveolin 1 / metabolism
  • Clathrin / metabolism
  • Cytosol / metabolism
  • Endocytosis*
  • Female
  • Gene Expression Profiling
  • Humans
  • Male
  • Marfan Syndrome / metabolism*
  • Middle Aged
  • Muscle, Smooth, Vascular / cytology
  • Myocytes, Smooth Muscle / metabolism*
  • Phosphorylation
  • Protein Transport
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction*
  • Smad2 Protein / metabolism
  • Transforming Growth Factor beta1 / metabolism*
  • Young Adult
  • rab5 GTP-Binding Proteins / metabolism

Substances

  • CAV1 protein, human
  • Caveolin 1
  • Clathrin
  • Receptors, Transforming Growth Factor beta
  • SMAD2 protein, human
  • Smad2 Protein
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • RAB5C protein, human
  • rab5 GTP-Binding Proteins