Regulation of Nur77 nuclear export by c-Jun N-terminal kinase and Akt

Oncogene. 2006 May 18;25(21):2974-86. doi: 10.1038/sj.onc.1209358.

Abstract

Proapoptotic nuclear receptor family member Nur77 translocates from the nucleus to the mitochondria, where it interacts with Bcl-2 to trigger apoptosis. Nur77 translocation is induced by certain apoptotic stimuli, including the synthetic retinoid-related 6-[3-(1-adamantyl)-4-hydroxyphenyl]-2-naphthalenecarboxylic acid (AHPN)/CD437 class. In this study, we investigated the molecular mechanism by which AHPN/CD437 analog (E)-4-[3-(1-adamantyl)-4-hydroxyphenyl]-3-chlorocinnamic acid (3-Cl-AHPC) induces Nur77 nuclear export. Our results demonstrate that 3-Cl-AHPC effectively activated Jun N-terminal kinase (JNK), which phosphorylates Nur77. Inhibition of JNK activation by a JNK inhibitor suppressed 3-Cl-AHPC-induced Nur77 nuclear export and apoptosis. In addition, several JNK upstream activators, including the phorbol ester TPA, anisomycin and MAPK kinase kinase-1 (MEKK1), phosphorylated Nur77 and induced its nuclear export. However, Nur77 phosphorylation by JNK, although essential, was not sufficient for inducing Nur77 nuclear export. Induction of Nur77 nuclear export by MEKK1 required a prolonged MEKK1 activation and was attenuated by Akt activation. Expression of constitutively active Akt prevented MEKK1-induced Nur77 nuclear export. Conversely, transfection of dominant-negative Akt or treatment with a phosphatidylinositol 3-kinase (PI3-K) inhibitor accelerated MEKK1-induced Nur77 nuclear export. Furthermore, mutation of an Akt phosphorylation residue Ser351 in Nur77 abolished the effect of Akt or the PI3-K inhibitor. Together, our results demonstrate that both activation of JNK and inhibition of Akt play a role in translocation of Nur77 from the nucleus to the cytoplasm.

Publication types

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

MeSH terms

  • Adamantane / analogs & derivatives*
  • Adamantane / pharmacology
  • Anisomycin / pharmacology
  • Apoptosis / drug effects
  • Cell Line, Tumor / drug effects
  • Cell Line, Tumor / metabolism
  • Cell Line, Tumor / ultrastructure
  • Cell Nucleus / metabolism
  • Cinnamates / pharmacology*
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Enzyme Activation / drug effects
  • Flavonoids / pharmacology
  • Humans
  • Imidazoles / pharmacology
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / physiology*
  • MAP Kinase Kinase 7 / genetics
  • MAP Kinase Kinase 7 / pharmacology
  • MAP Kinase Kinase Kinase 1 / physiology*
  • Mutagenesis, Site-Directed
  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • Phosphatidylinositol 3-Kinases / physiology
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation / drug effects
  • Protein Processing, Post-Translational* / drug effects
  • Protein Transport / drug effects
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / physiology*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Pyridines / pharmacology
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism*
  • Receptors, Steroid / genetics
  • Receptors, Steroid / metabolism*
  • Recombinant Fusion Proteins / pharmacology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • 4-(3-(1-adamantyl)-4-hydroxyphenyl)-3-chlorocinnamic acid
  • Cinnamates
  • DNA-Binding Proteins
  • Flavonoids
  • Imidazoles
  • NR4A1 protein, human
  • Nuclear Receptor Subfamily 4, Group A, Member 1
  • Phosphoinositide-3 Kinase Inhibitors
  • Proto-Oncogene Proteins c-bcl-2
  • Pyridines
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, Steroid
  • Recombinant Fusion Proteins
  • Transcription Factors
  • Anisomycin
  • AKT1 protein, human
  • Proto-Oncogene Proteins c-akt
  • JNK Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 1
  • MAP3K1 protein, human
  • MAP Kinase Kinase 7
  • MAP2K7 protein, human
  • Tetradecanoylphorbol Acetate
  • SB 203580
  • Adamantane
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one