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Kindlin-2 Phase Separation in Response to Flow Controls Vascular Stability.

Nina Ma1,2, Fangfang Wu1,2, Jiayu Liu3

  • 1Department of Pharmacology, Tianjin Key Laboratory of Inflammation Biology, State Key Laboratory of Experimental Hematology, The Province and Ministry Co-sponsored Collaborative Innovation Center for Medical Epigenetics (N.M., F.W., Z.W., L.W., Y.L., X.D., X.W.), School of Basic Medical Sciences, Tianjin Medical University, China.

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|November 4, 2024
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Summary

Mechanical forces alter Kindlin-2’s arginine methylation, impacting its liquid-liquid phase separation (LLPS) and endothelial cell integrity. Targeting this process offers a new strategy for treating atherosclerosis and vascular disorders.

Keywords:
atherosclerosisendothelial cellsfocal adhesionsphase separationprotein-arginine N-methyltransferases

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Area of Science:

  • Biochemistry
  • Cell Biology
  • Vascular Biology

Background:

  • Endothelial barrier function is regulated by shear stress, with atheroprotective and atheroprone patterns influencing endothelial cell (EC) integrity.
  • The precise mechanisms by which distinct blood flow patterns modulate EC integrity remain incompletely understood.
  • Kindlin-2, a focal adhesion and adherens junction protein, is critical for EC integrity and vascular stability.

Purpose of the Study:

  • To investigate the role of Kindlin-2 in regulating endothelial cell integrity under varying shear stress conditions.
  • To elucidate the molecular mechanisms by which mechanical forces influence Kindlin-2 function.
  • To explore Kindlin-2's involvement in atherogenesis.

Main Methods:

  • Utilized EC-specific Kindlin-2 knockout mouse models and atherosclerosis models (ApoE knockout).
  • Applied distinct shear stress patterns (pulsatile and oscillatory) to cultured ECs.
  • Employed live-cell imaging, biochemical assays (co-immunoprecipitation, mass spectrometry), and biophysical techniques (OptoDroplet, FRAP) to study Kindlin-2 localization, liquid-liquid phase separation (LLPS), and post-translational modifications.

Main Results:

  • Kindlin-2 localization and function are modulated by shear stress patterns.
  • Kindlin-2 deficiency in ECs leads to increased vascular permeability and exacerbated atherosclerosis in mice.
  • Oscillatory shear induces arginine methylation of Kindlin-2 via PRMT5, inhibiting its LLPS, impairing focal adhesion and junction maturation.
  • Pharmacological inhibition of arginine methylation reduces EC activation and atherosclerotic plaque formation.

Conclusions:

  • Mechanical forces regulate vascular stability by inducing arginine methylation of Kindlin-2, which affects its LLPS.
  • Kindlin-2's arginine methylation is a key mediator of flow-dependent EC integrity.
  • Targeting Kindlin-2 arginine methylation presents a potential hemodynamic-based therapeutic strategy for vascular disorders and atherosclerosis.