Rai1 haploinsufficiency causes reduced Bdnf expression resulting in hyperphagia, obesity and altered fat distribution in mice and humans with no evidence of metabolic syndrome

Hum Mol Genet. 2010 Oct 15;19(20):4026-42. doi: 10.1093/hmg/ddq317. Epub 2010 Jul 27.

Abstract

Smith-Magenis syndrome (SMS) is a genetic disorder caused by haploinsufficiency of the retinoic acid induced 1 (RAI1) gene. In addition to intellectual disabilities, behavioral abnormalities and sleep disturbances, a majority of children with SMS also have significant early-onset obesity. To study the role of RAI1 in obesity, we investigated the growth and obesity phenotype in a mouse model haploinsufficient for Rai1. Data show that Rai1(+/-) mice are hyperphagic, have an impaired satiety response and have altered abdominal and subcutaneous fat distribution, with Rai1(+/-) female mice having a higher proportion of abdominal fat when compared with wild-type female mice. Expression analyses revealed that Bdnf (brain-derived neurotrophic factor), a gene previously associated with hyperphagia and obesity, is downregulated in the Rai1(+/-) mouse hypothalamus, and reporter studies show that RAI1 directly regulates the expression of BDNF. Even though the Rai1(+/-) mice are significantly obese, serum analyses do not reveal any evidence of metabolic syndrome. Supporting these findings, a caregiver survey revealed that even though a high incidence of abdominal obesity is observed in females with SMS, they did not exhibit a higher incidence of indicators of metabolic syndrome above the general population. We conclude that Rai1 haploinsufficiency represents a single-gene model of obesity with hyperphagia, abnormal fat distribution and altered hypothalamic gene expression associated with satiety, food intake, behavior and obesity. Linking RAI1 and BDNF provides a more thorough understanding of the role of Rai1 in growth and obesity and insight into the complex pathogenicity of obesity, behavior and sex-specific differences in adiposity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Fat Distribution*
  • Brain-Derived Neurotrophic Factor / genetics*
  • Brain-Derived Neurotrophic Factor / metabolism
  • Disease Models, Animal
  • Female
  • Gene Expression
  • HEK293 Cells
  • Haploinsufficiency*
  • Humans
  • Hyperphagia / genetics*
  • Mice
  • Mice, Knockout
  • Microarray Analysis
  • Obesity / genetics*
  • Polymerase Chain Reaction
  • Satiety Response
  • Smith-Magenis Syndrome / genetics
  • Smith-Magenis Syndrome / metabolism
  • Trans-Activators / genetics*
  • Transcription Factors / genetics*

Substances

  • Brain-Derived Neurotrophic Factor
  • RAI1 protein, human
  • Rai1 protein, mouse
  • Trans-Activators
  • Transcription Factors