Shp2E76K mutant confers cytokine-independent survival of TF-1 myeloid cells by up-regulating Bcl-XL

J Biol Chem. 2007 Dec 14;282(50):36463-73. doi: 10.1074/jbc.M705789200. Epub 2007 Oct 17.

Abstract

Shp2 has been known to mediate growth factor-stimulated cell proliferation, but its role in cell survival is less clear. Gain-of-function Shp2 mutants such as Shp2E76K are associated with myeloid leukemias. We found that Shp2E76K could transform cytokine-dependent human TF-1 myeloid cells into cytokine independence and further characterized the Shp2E76K-induced cell survival mechanism in this study. Expression of Shp2E76K suppressed the cytokine withdrawal-induced intrinsic/mitochondrial apoptosis pathway, which is controlled by the Bcl-2 family proteins. Analysis of Bcl-2 family proteins showed that Bcl-XL and Mcl-1 were up-regulated in Shp2E76K-transformed TF-1 (TF-1/Shp2E76K) cells. Knockdown of Bcl-XL but not Mcl-1 with short hairpin RNAs prevented Shp2E76K-induced cytokine-independent survival. Roscovitine, which down-regulated Mcl-1, also did not prevent cytokine-independent survival of TF-1/Shp2E76K cells, whereas the Bcl-XL inhibitor HA14-1 did. Ras and mitogen-activated protein kinases Erk1 and Erk2 (Erk1/2) were constitutively activated in TF-1/Shp2E76K cells, whereas little active Akt was detected under cytokine-free conditions. Shp2E76K-induced Bcl-XL expression was suppressed by Mek inhibitors and by a dominant-negative Mek1 mutant but not by the phosphoinositide 3-phosphate inhibitor LY294002 and the Akt inhibitor API-2. Inhibition of Erk1/2 blocked cytokine-independent survival of TF-1/Shp2E76K cells, whereas inhibition of Akt had a minimal effect on cytokine-independent survival of TF-1/Shp2E76K cells. These results show that Shp2E76K can evoke constitutive Erk1/2 activation in TF-1 cells. Furthermore, Shp2E76K induces cytokine-independent survival of TF-1 cells by a novel mechanism involving up-regulation of Bcl-XL through the Erk1/2 pathway.

Publication types

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

MeSH terms

  • Amino Acid Substitution
  • Apoptosis / genetics
  • Apoptosis / physiology
  • Benzopyrans / pharmacology
  • Cell Line
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Chlorpropamide / analogs & derivatives
  • Chlorpropamide / pharmacology
  • Chromones / pharmacology
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Elafin / antagonists & inhibitors
  • Elafin / genetics
  • Elafin / metabolism
  • Enzyme Activation / drug effects
  • Enzyme Activation / genetics
  • Granulocyte-Macrophage Colony-Stimulating Factor / metabolism*
  • Granulocyte-Macrophage Colony-Stimulating Factor / pharmacology
  • Humans
  • Interleukin-3 / metabolism*
  • Interleukin-3 / pharmacology
  • Leukemia, Myeloid / enzymology
  • Leukemia, Myeloid / genetics
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / genetics
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mitogen-Activated Protein Kinase 1 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / antagonists & inhibitors
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Morpholines / pharmacology
  • Mutation, Missense
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Myeloid Progenitor Cells / enzymology*
  • Neoplasm Proteins / biosynthesis
  • Neoplasm Proteins / genetics
  • Nitriles / pharmacology
  • Oncogene Protein p21(ras) / antagonists & inhibitors
  • Oncogene Protein p21(ras) / genetics
  • Oncogene Protein p21(ras) / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / metabolism*
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Purines / pharmacology
  • Roscovitine
  • Up-Regulation* / drug effects
  • Up-Regulation* / genetics
  • bcl-X Protein / biosynthesis*
  • bcl-X Protein / genetics

Substances

  • API 2
  • BCL2L1 protein, human
  • Benzopyrans
  • Chromones
  • Elafin
  • IL3 protein, human
  • Interleukin-3
  • Morpholines
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Neoplasm Proteins
  • Nitriles
  • PI3 protein, human
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins c-bcl-2
  • Purines
  • bcl-X Protein
  • ethyl 2-amino-6-bromo-4-(1-cyano-2-ethoxy-2-oxoethyl)-4H-chromene-3-carboxylate
  • Roscovitine
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Oncogene Protein p21(ras)
  • Chlorpropamide