A myosin-Va tail fragment sequesters dynein light chains leading to apoptosis in melanoma cells

Cell Death Dis. 2013 Mar 21;4(3):e547. doi: 10.1038/cddis.2013.45.

Abstract

Previous studies proposed that myosin-Va regulates apoptosis by sequestering pro-apoptotic Bmf to the actin cytoskeleton through dynein light chain-2 (DLC2). Adhesion loss or other cytoskeletal perturbations would unleash Bmf, allowing it to bind and inhibit pro-survival Bcl2 proteins. Here, we demonstrated that overexpression of a myosin-Va medial tail fragment (MVaf) harboring the binding site for DLC2 dramatically decreased melanoma cell viability. Morphological and molecular changes, including surface blebbing, mitochondrial outer membrane permeabilization, cytochrome-c and Smac release, as well as caspase-9/-3 activation and DNA fragmentation indicated that melanoma cells died of apoptosis. Immobilized MVaf interacted directly with DLCs, but complexed MVaf/DLCs did not interact with Bmf. Overexpression of DLC2 attenuated MVaf-induced apoptosis. Thus, we suggest that, MVaf induces apoptosis by sequestering DLC2 and DLC1, thereby unleashing the pair of sensitizer and activator BH3-only proteins Bmf and Bim. Murine embryonic fibroblasts (MEFs) lacking Bim and Bmf or Bax and Bak were less sensitive to apoptosis caused by MVaf expression than wild-type MEFs, strengthening the putative role of the intrinsic apoptotic pathway in this response. Finally, MVaf expression attenuated B16-F10 solid tumor growth in mice, suggesting that this peptide may be useful as an apoptosis-inducing tool for basic and translational studies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Apoptosis / drug effects
  • Apoptosis Regulatory Proteins / deficiency
  • Apoptosis Regulatory Proteins / genetics
  • Bcl-2-Like Protein 11
  • Cell Line, Tumor
  • Cytoplasmic Dyneins / genetics*
  • Cytoplasmic Dyneins / metabolism
  • DNA Fragmentation / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Melanoma / genetics*
  • Melanoma / metabolism
  • Melanoma / pathology
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics
  • Mice
  • Mice, Knockout
  • Myosin Heavy Chains / genetics*
  • Myosin Heavy Chains / metabolism
  • Myosin Type V / genetics*
  • Myosin Type V / metabolism
  • Neoplasm Transplantation
  • Peptide Fragments / genetics*
  • Peptide Fragments / metabolism
  • Peptide Fragments / pharmacology
  • Protein Binding
  • Proto-Oncogene Proteins / deficiency
  • Proto-Oncogene Proteins / genetics
  • Signal Transduction / drug effects
  • Skin Neoplasms / genetics*
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • bcl-2 Homologous Antagonist-Killer Protein / deficiency
  • bcl-2 Homologous Antagonist-Killer Protein / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • BMF protein, human
  • Bak1 protein, mouse
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Membrane Proteins
  • Peptide Fragments
  • Proto-Oncogene Proteins
  • bcl-2 Homologous Antagonist-Killer Protein
  • MYO5A protein, human
  • DYNLL1 protein, human
  • Myosin Type V
  • Myosin Heavy Chains
  • Cytoplasmic Dyneins
  • DYNLL2 protein, human