Seasonal leptin resistance is associated with impaired signalling via JAK2-STAT3 but not ERK, possibly mediated by reduced hypothalamic GRB2 protein

J Comp Physiol B. 2012 May;182(4):553-67. doi: 10.1007/s00360-011-0637-4. Epub 2011 Dec 24.

Abstract

The Siberian hamster, Phodopus sungorus, undergoes a striking seasonal cycle of leptin sensitivity and body weight regulation, but the molecular mechanism and relevance to human leptin insensitivity are unknown. Here we show that nuclear translocation of phospho-STAT3 in the hypothalamus is rapidly stimulated by leptin to a greater extent in hamsters held in short-day length (SD) as compared to long-day length (LD). Intriguingly, effects of leptin on STAT3 appeared to be in part limited to nuclear translocation of phospho-STAT3 associated with the cell surface rather than phosphorylation of STAT3. The number of phospho-ERK cells within the hypothalamus was unaffected by either photoperiod or leptin. However, proximal to ERK phosphorylation, hypothalamic SH2-containing tyrosine phosphatase (SHP2) and the small growth factor receptor-binding protein (GRB2), which act as competitive negative modulators on binding of SOCS3 to leptin receptor (LRb)-associated Tyr⁹⁸⁵, were increased in SD compared to LD. Our findings suggest that activation of STAT3 by leptin may be dependent on interaction of stimulatory SHP2/GRB2 as well as inhibitory SOCS3 on the level of competitive binding to LRb-associated Tyr⁹⁸⁵. This hypothetical mechanism may represent the molecular identity of seasonally induced adjustments in leptin sensitivity and may be applied to investigating leptin sensitivity in other rodent models.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Nucleus
  • Cricetinae
  • Female
  • GRB2 Adaptor Protein / metabolism*
  • Gene Expression Regulation
  • Hypothalamus / cytology
  • Hypothalamus / metabolism*
  • Janus Kinase 2 / metabolism*
  • Leptin / metabolism*
  • Male
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons / cytology
  • Neurons / metabolism
  • Phodopus / metabolism*
  • Photoperiod
  • Protein Isoforms / metabolism
  • Protein Transport
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / genetics
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / metabolism
  • RNA, Messenger / metabolism
  • Receptors, Leptin / metabolism
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction*
  • Suppressor of Cytokine Signaling Proteins / metabolism

Substances

  • GRB2 Adaptor Protein
  • Leptin
  • Nerve Tissue Proteins
  • Protein Isoforms
  • RNA, Messenger
  • Receptors, Leptin
  • STAT3 Transcription Factor
  • Suppressor of Cytokine Signaling Proteins
  • Janus Kinase 2
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11