Calmodulin-mediated activation of Akt regulates survival of c-Myc-overexpressing mouse mammary carcinoma cells

J Biol Chem. 2004 Sep 10;279(37):38903-11. doi: 10.1074/jbc.M405314200. Epub 2004 Jul 9.

Abstract

c-Myc-overexpressing mammary epithelial cells are proapoptotic; their survival is strongly promoted by epidermal growth factor (EGF). We now demonstrate that EGF-induced Akt activation and survival in transgenic mouse mammary tumor virus-c-Myc mouse mammary carcinoma cells are both calcium/calmodulin-dependent. Akt activation is abolished by the phospholipase C-gamma inhibitor U-73122, by the intracellular calcium chelator BAPTA-AM, and by the specific calmodulin antagonist W-7. These results implicate calcium/calmodulin in the activation of Akt in these cells. In addition, Akt activation by serum and insulin is also inhibited by W-7. EGF-induced and calcium/calmodulin-mediated Akt activation occurs in both tumorigenic and non-tumorigenic mouse and human mammary epithelial cells, independent of their overexpression of c-Myc. These results imply that calcium/calmodulin may be a common regulator of Akt activation, irrespective of upstream receptor activator, mammalian species, and transformation status in mammary epithelial cells. However, only c-Myc-overexpressing mouse mammary carcinoma cells (but not normal mouse mammary epithelial cells) undergo apoptosis in the presence of the calmodulin antagonist W-7, indicating the vital selective role of calmodulin for survival of these cells. Calcium/calmodulin-regulated Akt activation is mediated directly by neither calmodulin kinases nor phosphatidylinositol 3-kinase (PI-3 kinase). Pharmacological inhibitors of calmodulin kinase kinase and calmodulin kinases II and III do not inhibit EGF-induced Akt activation, and calmodulin antagonist W-7 does not inhibit phosphotyrosine-associated PI-3 kinase activation. Akt is, however, co-immunoprecipitated with calmodulin in an EGF-dependent manner, which is inhibited by calmodulin antagonist W-7. We conclude that calmodulin may serve a vital regulatory function to direct the localization of Akt to the plasma membrane for its activation by PI-3 kinase.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Apoptosis
  • Blotting, Western
  • Calmodulin / metabolism*
  • Cell Line, Tumor
  • Cell Survival
  • Chelating Agents / pharmacology
  • Dose-Response Relationship, Drug
  • Egtazic Acid / analogs & derivatives*
  • Egtazic Acid / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Estrenes / pharmacology
  • Humans
  • Mice
  • Mice, Transgenic
  • Models, Biological
  • Neurons / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphodiesterase Inhibitors / pharmacology
  • Phospholipase C gamma
  • Precipitin Tests
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Transport
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-akt
  • Proto-Oncogene Proteins c-myc / metabolism*
  • Pyrrolidinones / pharmacology
  • Signal Transduction
  • Sulfonamides / pharmacology
  • Time Factors
  • Type C Phospholipases / pharmacology

Substances

  • Calmodulin
  • Chelating Agents
  • Enzyme Inhibitors
  • Estrenes
  • Phosphodiesterase Inhibitors
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-myc
  • Pyrrolidinones
  • Sulfonamides
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • 1,2-bis(2-aminophenoxy)ethane N,N,N',N'-tetraacetic acid acetoxymethyl ester
  • Egtazic Acid
  • W 7
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Type C Phospholipases
  • Phospholipase C gamma