Human GH receptor-IGF-1 receptor interaction: implications for GH signaling

Mol Endocrinol. 2014 Nov;28(11):1841-54. doi: 10.1210/me.2014-1174. Epub 2014 Sep 11.

Abstract

GH signaling yields multiple anabolic and metabolic effects. GH binds the transmembrane GH receptor (GHR) to activate the intracellular GHR-associated tyrosine kinase, Janus kinase 2 (JAK2), and downstream signals, including signal transducer and activator of transcription 5 (STAT5) activation and IGF-1 gene expression. Some GH effects are partly mediated by GH-induced IGF-1 via IGF-1 receptor (IGF-1R), a tyrosine kinase receptor. We previously demonstrated in non-human cells that GH causes formation of a GHR-JAK2-IGF-1R complex and that presence of IGF-1R (even without IGF-1 binding) augments proximal GH signaling. In this study, we use human LNCaP prostate cancer cells as a model system to further study the IGF-1R's role in GH signaling. GH promoted JAK2 and GHR tyrosine phosphorylation and STAT5 activation in LNCaP cells. By coimmunoprecipitation and a new split luciferase complementation assay, we find that GH augments GHR/IGF-1R complex formation, which is inhibited by a Fab of an antagonistic anti-GHR monoclonal antibody. Short hairpin RNA-mediated IGF-1R silencing in LNCaP cells reduced GH-induced GHR, JAK2, and STAT5 phosphorylation. Similarly, a soluble IGF-1R extracellular domain fragment (sol IGF-1R) interacts with GHR in response to GH and blunts GH signaling. Sol IGF-1R also markedly inhibits GH-induced IGF-1 gene expression in both LNCaP cells and mouse primary osteoblast cells. On the basis of these and other findings, we propose a model in which IGF-1R augments GH signaling by allowing a putative IGF-1R-associated molecule that regulates GH signaling to access the activated GHR/JAK2 complex and envision sol IGF-1R as a dominant-negative inhibitor of this IGF-1R-mediated augmentation. Physiological implications of this new model are discussed.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Carrier Proteins / metabolism*
  • Cell Line, Tumor
  • Cells, Cultured
  • Growth Hormone / metabolism
  • Humans
  • Immunoprecipitation / methods
  • Insulin-Like Growth Factor I / metabolism
  • Janus Kinase 2 / metabolism
  • Mice
  • Osteoblasts / metabolism
  • Phosphorylation / physiology
  • Protein Interaction Maps / physiology*
  • Receptor, IGF Type 1 / metabolism*
  • STAT5 Transcription Factor / metabolism
  • Signal Transduction / physiology*

Substances

  • Carrier Proteins
  • STAT5 Transcription Factor
  • Insulin-Like Growth Factor I
  • Growth Hormone
  • Receptor, IGF Type 1
  • JAK2 protein, human
  • Janus Kinase 2
  • somatotropin-binding protein