Oncogenic inhibition by a deleted in liver cancer gene requires cooperation between tensin binding and Rho-specific GTPase-activating protein activities

Proc Natl Acad Sci U S A. 2007 May 22;104(21):9012-7. doi: 10.1073/pnas.0703033104. Epub 2007 May 15.

Abstract

The three deleted in liver cancer genes (DLC1-3) encode Rho-GTPase-activating proteins (RhoGAPs) whose expression is frequently down-regulated or silenced in a variety of human malignancies. The RhoGAP activity is required for full DLC-dependent tumor suppressor activity. Here we report that DLC1 and DLC3 bind to human tensin1 and its chicken homolog. The binding has been mapped to the tensin Src homology 2 (SH2) and phosphotyrosine binding (PTB) domains at the C terminus of tensin proteins. Distinct DLC1 sequences are required for SH2 and PTB binding. DCL binding to both domains is constitutive under basal conditions. The SH2 binding depends on a tyrosine in DCL1 (Y442) but is phosphotyrosine-independent, a highly unusual feature for SH2 binding. DLC1 competed with the binding of other proteins to the tensin C terminus, including beta 3-integrin binding to the PTB domain. Point mutation of a critical tyrosine residue (Y442F) in DLC1 rendered the protein deficient for binding the tensin SH2 domain and binding full-length tensin. The Y442F protein was diffusely cytoplasmic, in contrast to the localization of wild-type DLC1 to focal adhesions, but it retained the ability to reduce the intracellular levels of Rho-GTP. The Y442F mutant displayed markedly reduced biological activity, as did a mutant that was RhoGAP-deficient. The results suggest that DLC1 is a multifunctional protein whose biological activity depends on cooperation between its tensin binding and RhoGAP activities, although neither activity depends on the other.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Cell Line
  • GTPase-Activating Proteins / metabolism*
  • Humans
  • Integrins / metabolism
  • Mice
  • Microfilament Proteins / metabolism*
  • Mutation / genetics
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Phosphotyrosine / metabolism
  • Protein Binding
  • Tensins
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Tyrosine / genetics
  • Tyrosine / metabolism
  • src Homology Domains

Substances

  • GTPase-Activating Proteins
  • Integrins
  • Microfilament Proteins
  • Oncogene Proteins
  • STARD8 protein, human
  • TNS1 protein, human
  • Tensins
  • Tns1 protein, mouse
  • Tumor Suppressor Proteins
  • rho GTPase-activating protein
  • Phosphotyrosine
  • Tyrosine