Dab2 inhibits the cholesterol-dependent activation of JNK by TGF-β

Mol Biol Cell. 2014 May;25(10):1620-8. doi: 10.1091/mbc.E13-09-0537. Epub 2014 Mar 19.

Abstract

Transforming growth factor-β (TGF-β) ligands activate Smad-mediated and noncanonical signaling pathways in a cell context-dependent manner. Localization of signaling receptors to distinct membrane domains is a potential source of signaling output diversity. The tumor suppressor/endocytic adaptor protein disabled-2 (Dab2) was proposed as a modulator of TGF-β signaling. However, the molecular mechanism(s) involved in the regulation of TGF-β signaling by Dab2 were not known. Here we investigate these issues by combining biophysical studies of the lateral mobility and endocytosis of the type I TGF-β receptor (TβRI) with TGF-β phosphoprotein signaling assays. Our findings demonstrate that Dab2 interacts with TβRI to restrict its lateral diffusion at the plasma membrane and enhance its clathrin-mediated endocytosis. Small interfering RNA-mediated knockdown of Dab2 or Dab2 overexpression shows that Dab2 negatively regulates TGF-β-induced c-Jun N-terminal kinase (JNK) activation, whereas activation of the Smad pathway is unaffected. Moreover, activation of JNK by TGF-β in the absence of Dab2 is disrupted by cholesterol depletion. These data support a model in which Dab2 regulates the domain localization of TβRI in the membrane, balancing TGF-β signaling via the Smad and JNK pathways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / biosynthesis
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Apoptosis Regulatory Proteins
  • Cell Line, Tumor
  • Cell Membrane / physiology
  • Cholesterol / metabolism*
  • Clathrin
  • Endocytosis / physiology*
  • Enzyme Activation
  • Humans
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / biosynthesis*
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Protein Transport / physiology
  • RNA Interference
  • RNA, Small Interfering
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction
  • Smad Proteins / metabolism
  • Transforming Growth Factor beta / metabolism*
  • Tumor Suppressor Proteins / biosynthesis
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • Clathrin
  • DAB2 protein, human
  • RNA, Small Interfering
  • Receptors, Transforming Growth Factor beta
  • Smad Proteins
  • Transforming Growth Factor beta
  • Tumor Suppressor Proteins
  • Cholesterol
  • JNK Mitogen-Activated Protein Kinases