Focal adhesion kinase is activated by microtubule-depolymerizing agents and regulates membrane blebbing in human endothelial cells

J Cell Mol Med. 2020 Jul;24(13):7228-7238. doi: 10.1111/jcmm.15273. Epub 2020 May 26.

Abstract

Microtubule-depolymerizing agents can selectively disrupt tumor vessels via inducing endothelial membrane blebbing. However, the mechanism regulating blebbing is largely unknown. IMB5046 is a newly discovered microtubule-depolymerizing agent. Here, the functions of focal adhesion kinase (FAK) during IMB5046-induced blebbing and the relevant mechanism are studied. We found that IMB5046 induced membrane blebbing and reassembly of focal adhesions in human vascular endothelial cells. Both FAK inhibitor and knock-down expression of FAK inhibited IMB5046-induced blebbing. Mechanism study revealed that IMB5046 induced the activation of FAK via GEF-H1/ Rho/ ROCK/ MLC2 pathway. cRGD peptide, a ligand of integrin, also blocked IMB5046-induced blebbing. After activation, FAK further promoted the phosphorylation of MLC2. This positive feedback loop caused more intensive actomyosin contraction and continuous membrane blebbing. FAK inhibitor blocked membrane blebbing via inhibiting actomyosin contraction, and stimulated stress fibre formation via promoting the phosphorylation of HSP27. Conclusively, these results demonstrate that FAK is a molecular switch controlling endothelial blebbing and stress fibre formation. Our study provides a new molecular mechanism for microtubule-depolymerizing agents to be used as vascular disrupting agents.

Keywords: IMB5046; endothelial cells; focal adhesion kinase; membrane blebbing; microtubule-depolymerizing agents; stress fibres.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Benzoates / pharmacology*
  • Cardiac Myosins / metabolism
  • Cell Surface Extensions / drug effects
  • Cell Surface Extensions / metabolism*
  • Cytoskeleton / drug effects
  • Cytoskeleton / metabolism
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Enzyme Activation / drug effects
  • Focal Adhesion Protein-Tyrosine Kinases / metabolism*
  • Focal Adhesions / drug effects
  • Focal Adhesions / metabolism
  • Heat-Shock Proteins / metabolism
  • Humans
  • Integrins / metabolism
  • Microtubules / metabolism*
  • Models, Biological
  • Molecular Chaperones / metabolism
  • Morpholines / pharmacology*
  • Myosin Light Chains / metabolism
  • Phosphorylation / drug effects
  • Protein Kinase Inhibitors / pharmacology
  • Quinolones / pharmacology
  • Rho Guanine Nucleotide Exchange Factors / metabolism
  • Signal Transduction / drug effects
  • Stress Fibers / drug effects
  • Stress Fibers / metabolism
  • Sulfones / pharmacology
  • rho GTP-Binding Proteins / metabolism
  • rho-Associated Kinases / metabolism

Substances

  • 6-(4-(3-(methylsulfonyl)benzylamino)-5-(trifluoromethyl)pyrimidin-2-ylamino)-3,4-dihydroquinolin-2(1H)-one
  • ARHGEF2 protein, human
  • Benzoates
  • HSPB1 protein, human
  • Heat-Shock Proteins
  • IMB5046
  • Integrins
  • Molecular Chaperones
  • Morpholines
  • Myosin Light Chains
  • Protein Kinase Inhibitors
  • Quinolones
  • Rho Guanine Nucleotide Exchange Factors
  • Sulfones
  • myosin light chain 2
  • Focal Adhesion Protein-Tyrosine Kinases
  • rho-Associated Kinases
  • Cardiac Myosins
  • rho GTP-Binding Proteins