Ras-mediated apoptosis of PC CL 3 rat thyroid cells induced by RET/PTC oncogenes

Oncogene. 2003 Jan 16;22(2):246-55. doi: 10.1038/sj.onc.1206112.

Abstract

RET gene rearrangements, which generate chimeric RET/PTC oncogenes, are early events in the evolution of thyroid papillary carcinomas. Expression of RET/PTC oncogenes promotes neoplastic transformation of cultured thyroid cells and of thyroid glands in transgenic mice. Notwithstanding these oncogenic effects, we have found that the expression of two RET/PTC oncogenes (H4-RET and RFG-RET) induces apoptosis of rat thyroid PC CL 3 cells. Promotion of thyroid cell death depends on the kinase activity of RET/PTC and on the phosphorylation of a tyrosine residue (tyrosine 1062) that maps in the carboxy-terminus of the RET protein. Tyrosine 1062 is essential for RET/PTC-mediated activation of the Ras/ERK pathway. Inhibition of Ras/ERK by a dominant negative Ras or by the MEKI inhibitor, PD98059, obstructed RET/PTC-mediated apoptosis. We also show that signals transmitted by tyrosine 1062 mediate proapoptotic events like Bcl-2 down regulation and Bax upregulation, and that adoptive overexpression of Bcl-2 overcomes RET/PTC-induced apoptosis. Thus, gene rearrangements that generate RET/PTC oncogenes subvert RET function by converting it into a chronically active kinase that is constitutively phosphorylated on tyrosine 1062. In turn, Y1062 phosphorylation transmits not only mitogenic but also proapoptotic signals to thyroid cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / physiology*
  • Cell Differentiation / physiology
  • Cells, Cultured
  • Drosophila Proteins*
  • Enzyme Inhibitors / pharmacology
  • Feedback, Physiological
  • Flavonoids / pharmacology
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation
  • Oncogene Proteins / genetics
  • Oncogene Proteins / metabolism*
  • Oncogene Proteins, Fusion
  • Phosphoprotein Phosphatases / genetics
  • Phosphoprotein Phosphatases / metabolism
  • Protein Phosphatase 2
  • Protein Phosphatase 2C
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Proto-Oncogene Proteins c-ret
  • Rats
  • Rats, Inbred F344
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Saccharomyces cerevisiae Proteins*
  • Signal Transduction
  • Thyroid Gland / pathology*
  • Thyroid Gland / physiology
  • Tyrosine / metabolism
  • Up-Regulation
  • bcl-2-Associated X Protein
  • ras Proteins / genetics
  • ras Proteins / metabolism*

Substances

  • Bax protein, rat
  • Drosophila Proteins
  • Enzyme Inhibitors
  • Flavonoids
  • Oncogene Proteins
  • Oncogene Proteins, Fusion
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Recombinant Proteins
  • Saccharomyces cerevisiae Proteins
  • bcl-2-Associated X Protein
  • Tyrosine
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins c-ret
  • RET-PTC oncoprotein, rat
  • Receptor Protein-Tyrosine Kinases
  • Ret protein, Drosophila
  • Ret protein, rat
  • Ret-Ptc1 oncoprotein, mouse
  • Mitogen-Activated Protein Kinases
  • PTC1 protein, S cerevisiae
  • Phosphoprotein Phosphatases
  • Protein Phosphatase 2
  • Protein Phosphatase 2C
  • ras Proteins
  • 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one