Cavin-1/PTRF mediates insulin-dependent focal adhesion remodeling and ameliorates high-fat diet-induced inflammatory responses in mice

J Biol Chem. 2019 Jul 5;294(27):10544-10552. doi: 10.1074/jbc.RA119.008824. Epub 2019 May 24.

Abstract

Cavin-1/polymerase I and transcript release factor (PTRF) is a requisite component of caveolae, small plasma membrane invaginations that are highly abundant in adipocytes. Cavin-1 is a dynamic molecule whose dissociation from caveolae plays an important role in mechanoprotection and rRNA synthesis. In the former situation, the acute dissociation of cavin-1 from caveolae allows cell membrane expansion that occurs upon insulin-aided lipid uptake into the fat cells. Cavin-1 dissociation from caveolae and membrane flattening alters the cytoskeleton and the interaction of plasma membrane proteins with the extracellular matrix through interactions with focal adhesion structures. Here, using cavin-1 knockout mice, subcellular fractionation, and immunoblotting methods, we addressed the relationship of cavin-1 with focal adhesion complexes following nutritional stimulation. We found that cavin-1 is acutely translocated to focal complex compartments upon insulin stimulation, where it regulates focal complex formation through an interaction with paxillin. We found that loss of cavin-1 impairs focal complex remodeling and focal adhesion formation and causes a mechanical stress response, concomitant with activation of proinflammatory and senescence/apoptosis pathways. We conclude that cavin-1 plays key roles in dynamic remodeling of focal complexes upon metabolic stimulation. This mechanism also underlies the crucial role of caveolae in the long-term healthy expansion of the adipocyte.

Keywords: PTRF; adipocyte; adipose tissue; caveolae; cavin-1; focal adhesion; focal complex; inflammation; insulin; lipid raft; obesity; osmotic swelling; phosphorylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 3T3-L1 Cells
  • Animals
  • Caveolae / metabolism
  • Caveolin 1 / deficiency
  • Caveolin 1 / genetics
  • Caveolin 1 / metabolism*
  • Diet, High-Fat*
  • Focal Adhesions / drug effects*
  • Focal Adhesions / metabolism
  • Inflammation / etiology
  • Inflammation / metabolism*
  • Insulin / pharmacology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Paxillin / metabolism
  • Protein Binding
  • Signal Transduction
  • Stress, Mechanical

Substances

  • Caveolin 1
  • Insulin
  • Paxillin