SPSB1, a Novel Negative Regulator of the Transforming Growth Factor-β Signaling Pathway Targeting the Type II Receptor

J Biol Chem. 2015 Jul 17;290(29):17894-17908. doi: 10.1074/jbc.M114.607184. Epub 2015 Jun 1.

Abstract

Appropriate cellular signaling is essential to control cell proliferation, differentiation, and cell death. Aberrant signaling can have devastating consequences and lead to disease states, including cancer. The transforming growth factor-β (TGF-β) signaling pathway is a prominent signaling pathway that has been tightly regulated in normal cells, whereas its deregulation strongly correlates with the progression of human cancers. The regulation of the TGF-β signaling pathway involves a variety of physiological regulators. Many of these molecules act to alter the activity of Smad proteins. In contrast, the number of molecules known to affect the TGF-β signaling pathway at the receptor level is relatively low, and there are no known direct modulators for the TGF-β type II receptor (TβRII). Here we identify SPSB1 (a Spry domain-containing Socs box protein) as a novel regulator of the TGF-β signaling pathway. SPSB1 negatively regulates the TGF-β signaling pathway through its interaction with both endogenous and overexpressed TβRII (and not TβRI) via its Spry domain. As such, TβRII and SPSB1 co-localize on the cell membrane. SPSB1 maintains TβRII at a low level by enhancing the ubiquitination levels and degradation rates of TβRII through its Socs box. More importantly, silencing SPSB1 by siRNA results in enhanced TGF-β signaling and migration and invasion of tumor cells.

Keywords: SPSB; protein degradation; receptor modification; receptor regulation; signal transduction; transforming growth factor beta (TGF-B).

MeSH terms

  • Animals
  • Cell Line
  • Cell Line, Tumor
  • Cell Movement
  • Gene Silencing
  • HEK293 Cells
  • Humans
  • Mice
  • NIH 3T3 Cells
  • Neoplasm Invasiveness / genetics
  • Neoplasm Invasiveness / pathology
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Protein Interaction Maps
  • Protein Serine-Threonine Kinases / analysis
  • Protein Serine-Threonine Kinases / metabolism*
  • Receptor, Transforming Growth Factor-beta Type II
  • Receptors, Transforming Growth Factor beta / analysis
  • Receptors, Transforming Growth Factor beta / metabolism*
  • Signal Transduction*
  • Suppressor of Cytokine Signaling Proteins / analysis
  • Suppressor of Cytokine Signaling Proteins / genetics
  • Suppressor of Cytokine Signaling Proteins / metabolism*
  • Transcriptional Activation
  • Transforming Growth Factor beta / metabolism*
  • Ubiquitination

Substances

  • Receptors, Transforming Growth Factor beta
  • SPSB1 protein, human
  • SSB-1 protein, mouse
  • Suppressor of Cytokine Signaling Proteins
  • Transforming Growth Factor beta
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type II