Modulation of the interleukin-6 receptor subunit glycoprotein 130 complex and its signaling by LMO4 interaction

J Biol Chem. 2005 Apr 1;280(13):12747-57. doi: 10.1074/jbc.M500175200. Epub 2005 Jan 27.

Abstract

The interleukin (IL)-6-type cytokines play major roles in a variety of biological processes by signaling through a common receptor subunit, glycoprotein (gp) 130. We performed yeast two-hybrid screening to identify new binding partners of the activated gp130 and the associated Janus kinases. LMO4, a LIM domain-containing protein that belongs to a family of oncogenes, was identified in this assay. Further studies show that LMO4 associates with gp130 and Janus kinase1 in several mammalian cell types. It also interacts with protein-tyrosine phosphatase 2 (SHP2) and suppressor of cytokine signaling 3 (SOCS3). The binding domains involved in these interactions were mapped, and the interactions were shown to be in a direct manner by in vitro binding assays. It is likely that LMO4 exists in the gp130 complex. The cellular localization of LMO4 was detected primarily in the nucleus with a substantial amount also detected in the cytoplasm in several cell types. The effect of LMO4 in IL-6 signaling was subsequently examined. Overexpression of LMO4 enhanced the transcriptional activity and target gene expression of Stat 3 (signal transducers and activators of transcription 3). Consistent with this, silencing LMO4 expression in stable cell lines expressing the small interfering RNA of LMO4 decreased Stat3 activity. Furthermore, the half-life of gp130 was shortened, and the production of acute phase proteins induced by IL-6 was reduced. Together, our data reveal a positive regulatory role of LMO4 in IL-6 signaling, possibly by acting as a scaffold for stabilization of the gp130 complex. These studies may open up a link between the oncogenic effect of LMO proteins and their regulatory role in cytokine signaling in general.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • Antigens, CD / chemistry*
  • Antigens, CD / physiology*
  • Blotting, Northern
  • COS Cells
  • Cell Line
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Cytokine Receptor gp130
  • Cytokines / metabolism
  • Cytoplasm / metabolism
  • DNA-Binding Proteins / metabolism
  • Down-Regulation
  • Gene Silencing
  • Genes, Reporter
  • Glutathione Transferase / metabolism
  • Homeodomain Proteins / chemistry
  • Homeodomain Proteins / physiology*
  • Humans
  • Immunoprecipitation
  • Intracellular Signaling Peptides and Proteins
  • LIM Domain Proteins
  • Membrane Glycoproteins / chemistry*
  • Membrane Glycoproteins / physiology*
  • Microscopy, Fluorescence
  • Phosphorylation
  • Plasmids / metabolism
  • Protein Binding
  • Protein Phosphatase 2
  • Protein Structure, Tertiary
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / chemistry
  • RNA, Small Interfering / metabolism
  • STAT3 Transcription Factor
  • Signal Transduction*
  • Trans-Activators / metabolism
  • Transcription Factors / chemistry
  • Transcription Factors / physiology*
  • Transfection
  • Two-Hybrid System Techniques
  • Tyrosine / chemistry
  • Tyrosine / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, CD
  • Cytokines
  • DNA-Binding Proteins
  • Homeodomain Proteins
  • IL6ST protein, human
  • Intracellular Signaling Peptides and Proteins
  • LIM Domain Proteins
  • LMO4 protein, human
  • Membrane Glycoproteins
  • RNA, Small Interfering
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Trans-Activators
  • Transcription Factors
  • Cytokine Receptor gp130
  • Tyrosine
  • Glutathione Transferase
  • Protein Phosphatase 2
  • PTPN11 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases