Src family kinase-independent signal transduction and gene induction by leukemia inhibitory factor

J Biol Chem. 2003 Jul 25;278(30):27750-7. doi: 10.1074/jbc.M303670200. Epub 2003 May 21.

Abstract

Members of the interleukin-6 (IL-6) family of cytokines exert their biological effects via binding to their cognate ligand-binding receptor subunit on a target cell. The subsequent recruitment of the common signal transducer glycoprotein 130 and activation of the JAK/STAT and SHP-2/Ras/mitogen-activated protein kinase (MAPK) pathways are responsible for the majority of cellular responses elicited by IL-6 cytokines. Several types of experiments suggest that the Src family of kinases (SFK) also participates in IL-6 family cytokine-mediated signaling events. SYF cells, which lack expression of SFKs Src, Yes, and Fyn, were used to determine the role of SFKs in IL-6 family cytokine signaling and gene induction. SYF and wild type (WT) control fibroblasts displayed similar activation of signaling intermediates following stimulation with leukemia inhibitory factor (LIF). LIF-stimulated tyrosine phosphorylation of SHP-2 and subsequent activation of MAPK in SYF cells were identical to that seen in LIF-stimulated WT cells. Both LIF-stimulated tyrosine phosphorylation of STAT1 and STAT3, as well as LIF-stimulated DNA binding activity of STAT-containing nuclear complexes were indistinguishable when compared in SYF and WT cells. In addition, the phosphatidylinositol 3-kinase-sensitive Akt kinase and p38 MAPK were activated by LIF in both SYF and WT cells. Furthermore, LIF-stimulated expression of c-fos, egr-1, and suppressor of cytokine signaling-3 was retained in SYF cells. The IL-6 family cytokine oncostatin M was also capable of activating MAPK, STAT3, STAT1, Akt, and p38 in both WT and SYF cells. These results demonstrate that IL-6 family cytokines can activate a full repertoire of signaling pathways and induce gene expression independent of SFKs.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • Cytokines / metabolism
  • DNA-Binding Proteins / metabolism
  • Dose-Response Relationship, Drug
  • Early Growth Response Protein 1
  • Electrophoresis, Polyacrylamide Gel
  • Enzyme Activation
  • Fibroblasts / metabolism
  • Growth Inhibitors / metabolism
  • Growth Inhibitors / physiology*
  • Humans
  • Immediate-Early Proteins*
  • Immunoblotting
  • Interleukin-6 / metabolism
  • Leukemia Inhibitory Factor
  • Ligands
  • Lymphokines / metabolism
  • Lymphokines / physiology*
  • MAP Kinase Signaling System
  • Mice
  • Mice, Inbred C57BL
  • Mitogen-Activated Protein Kinases / metabolism
  • Oncostatin M
  • Peptides / metabolism
  • Phosphorylation
  • Precipitin Tests
  • Protein Binding
  • Protein Serine-Threonine Kinases*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • Proto-Oncogene Proteins c-fos / metabolism
  • STAT1 Transcription Factor
  • STAT3 Transcription Factor
  • Signal Transduction*
  • Time Factors
  • Trans-Activators / metabolism
  • Transcription Factors / metabolism
  • p38 Mitogen-Activated Protein Kinases
  • src-Family Kinases / metabolism*

Substances

  • Cytokines
  • DNA-Binding Proteins
  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Egr1 protein, mouse
  • Growth Inhibitors
  • Immediate-Early Proteins
  • Interleukin-6
  • LIF protein, human
  • Leukemia Inhibitory Factor
  • Lif protein, mouse
  • Ligands
  • Lymphokines
  • OSM protein, human
  • Osm protein, mouse
  • Peptides
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-fos
  • STAT1 Transcription Factor
  • STAT1 protein, human
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Stat1 protein, mouse
  • Stat3 protein, mouse
  • Trans-Activators
  • Transcription Factors
  • Oncostatin M
  • src-Family Kinases
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases