Thyroid transcription factor-1 regulates feeding behavior via melanocortin pathway in the hypothalamus

Diabetes. 2011 Mar;60(3):710-9. doi: 10.2337/db10-0183. Epub 2011 Jan 31.

Abstract

Objective: α-Melanocyte-stimulating hormone (α-MSH) and agouti-related peptide (AgRP) control energy homeostasis by their opposing actions on melanocortin receptors (MC3/4R) in the hypothalamus. We previously reported that thyroid transcription factor-1 (TTF-1) controls feeding behavior in the hypothalamus. This study aims to identify the function of TTF-1 in the transcriptional regulation of AgRP and α-MSH synthesis for the control of feeding behavior.

Research design and methods: TTF-1 activity in AgRP and pro-opiomelanocortin (POMC) transcription was examined using gel-shift and promoter assays and an in vivo model of TTF-1 synthesis inhibition by intracerebroventricular injection of an antisense (AS) oligodeoxynucleotide (ODN). Double immunohistochemistry was performed to colocalize TTF-1 and AgRP or α-MSH in the hypothalamic arcuate nucleus (ARC). To determine whether TTF-1 action on food intake is mediated through MC3/4R, we measured changes in food intake upon intracerebroventricular injection of MC3/4R antagonists (SHU9119 and AgRP) into rat brain preinjected with the AS ODN.

Results: TTF-1 stimulated AgRP but inhibited POMC transcription by binding to the promoters of these genes. TTF-1 was widely distributed in the hypothalamus, but we identified some cells coexpressing TTF-1 and AgRP or α-MSH in the ARC. In addition, intracerebroventricular administration of leptin decreased TTF-1 expression in the hypothalamus, and AS ODN-induced inhibition of TTF-1 expression decreased food intake and AgRP expression but increased α-MSH expression. Anorexia induced by the AS ODN was attenuated by the administration of MC3/4R antagonists.

Conclusions: TTF-1 transcriptionally regulates synthesis of AgRP and α-MSH in the ARC and affects feeding behavior via the melanocortin pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Agouti-Related Protein / genetics
  • Agouti-Related Protein / metabolism*
  • Agouti-Related Protein / pharmacology
  • Analysis of Variance
  • Animals
  • Arcuate Nucleus of Hypothalamus / drug effects
  • Arcuate Nucleus of Hypothalamus / physiology*
  • Blotting, Western
  • Cell Line
  • Cells, Cultured
  • Eating / drug effects
  • Eating / physiology
  • Electrophoretic Mobility Shift Assay
  • Feeding Behavior / drug effects
  • Feeding Behavior / physiology*
  • Immunohistochemistry
  • In Situ Hybridization
  • Melanocyte-Stimulating Hormones / pharmacology
  • Mice
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Oligodeoxyribonucleotides, Antisense
  • Promoter Regions, Genetic
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Rats
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / physiology*
  • Thyroid Nuclear Factor 1
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • alpha-MSH / genetics
  • alpha-MSH / metabolism*

Substances

  • Agouti-Related Protein
  • Nkx2-1 protein, mouse
  • Nkx2-1 protein, rat
  • Nuclear Proteins
  • Oligodeoxyribonucleotides, Antisense
  • RNA, Messenger
  • Thyroid Nuclear Factor 1
  • Transcription Factors
  • SHU 9119
  • alpha-MSH
  • Melanocyte-Stimulating Hormones