A truncating mutation of Alms1 reduces the number of hypothalamic neuronal cilia in obese mice

Dev Neurobiol. 2013 Jan;73(1):1-13. doi: 10.1002/dneu.22031. Epub 2012 Jul 20.

Abstract

Primary cilia are ubiquitous cellular antennae whose dysfunction collectively causes various disorders, including vision and hearing impairment, as well as renal, skeletal, and central nervous system anomalies. One ciliopathy, Alström syndrome, is closely related to Bardet-Biedl syndrome (BBS), sharing amongst other phenotypic features morbid obesity. As the cellular and molecular links between weight regulation and cilia are poorly understood, we used the obese mouse strain foz/foz, bearing a truncating mutation in the Alström syndrome protein (Alms1), to help elucidate why it develops hyperphagia, leading to early onset obesity and metabolic anomalies. Our in vivo studies reveal that Alms1 localizes at the base of cilia in hypothalamic neurons, which are implicated in the control of satiety. Alms1 is lost from this location in foz/foz mice, coinciding with a strong postnatal reduction (∼70%) in neurons displaying cilia marked with adenylyl cyclase 3 (AC3), a signaling protein implicated in obesity. Notably, the reduction in AC3-bearing cilia parallels the decrease in cilia containing two appetite-regulating proteins, Mchr1 and Sstr3, as well as another established Arl13b ciliary marker, consistent with progressive loss of cilia during development. Together, our results suggest that Alms1 maintains the function of neuronal cilia implicated in weight regulation by influencing the maintenance and/or stability of the organelle. Given that Mchr1 and Sstr3 localization to remaining cilia is maintained in foz/foz animals but known to be lost from BBS knockout mice, our findings suggest different molecular etiologies for the satiety defects associated with the Alström syndrome and BBS ciliopathies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-Ribosylation Factors / metabolism
  • Adenylyl Cyclases / metabolism
  • Adipose Tissue / metabolism
  • Adipose Tissue / pathology
  • Age Factors
  • Animals
  • Animals, Newborn
  • Cell Cycle Proteins
  • Cells, Cultured
  • Cilia* / genetics
  • Cilia* / metabolism
  • Cilia* / pathology
  • DNA-Binding Proteins / genetics*
  • DNA-Binding Proteins / metabolism
  • Diabetes Mellitus, Experimental / genetics*
  • Diabetes Mellitus, Experimental / pathology
  • Embryo, Mammalian
  • Female
  • Gene Expression Regulation, Developmental / genetics
  • Hippocampus / pathology
  • Hypothalamus / pathology*
  • Mice
  • Mice, Inbred NOD
  • Microtubule-Associated Proteins / metabolism
  • Mutation / genetics*
  • Neurons / metabolism
  • Neurons / pathology
  • Neurons / ultrastructure*
  • RNA, Messenger / metabolism
  • Receptors, Somatostatin / metabolism

Substances

  • Alms1 protein, mouse
  • Arl13b protein, mouse
  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Mchr1 protein, mouse
  • Microtubule-Associated Proteins
  • Mtap2 protein, mouse
  • RNA, Messenger
  • Receptors, Somatostatin
  • somatostatin receptor 3
  • ADP-Ribosylation Factors
  • Adenylyl Cyclases
  • adenylate cyclase 3