Prader-Willi Critical Region, a Non-Translated, Imprinted Central Regulator of Bone Mass: Possible Role in Skeletal Abnormalities in Prader-Willi Syndrome

PLoS One. 2016 Jan 29;11(1):e0148155. doi: 10.1371/journal.pone.0148155. eCollection 2016.

Abstract

Prader-Willi Syndrome (PWS), a maternally imprinted disorder and leading cause of obesity, is characterised by insatiable appetite, poor muscle development, cognitive impairment, endocrine disturbance, short stature and osteoporosis. A number of causative loci have been located within the imprinted Prader-Willi Critical Region (PWCR), including a set of small non-translated nucleolar RNA's (snoRNA). Recently, micro-deletions in humans identified the snoRNA Snord116 as a critical contributor to the development of PWS exhibiting many of the classical symptoms of PWS. Here we show that loss of the PWCR which includes Snord116 in mice leads to a reduced bone mass phenotype, similar to that observed in humans. Consistent with reduced stature in PWS, PWCR KO mice showed delayed skeletal development, with shorter femurs and vertebrae, reduced bone size and mass in both sexes. The reduction in bone mass in PWCR KO mice was associated with deficiencies in cortical bone volume and cortical mineral apposition rate, with no change in cancellous bone. Importantly, while the length difference was corrected in aged mice, consistent with continued growth in rodents, reduced cortical bone formation was still evident, indicating continued osteoblastic suppression by loss of PWCR expression in skeletally mature mice. Interestingly, deletion of this region included deletion of the exclusively brain expressed Snord116 cluster and resulted in an upregulation in expression of both NPY and POMC mRNA in the arcuate nucleus. Importantly, the selective deletion of the PWCR only in NPY expressing neurons replicated the bone phenotype of PWCR KO mice. Taken together, PWCR deletion in mice, and specifically in NPY neurons, recapitulates the short stature and low BMD and aspects of the hormonal imbalance of PWS individuals. Moreover, it demonstrates for the first time, that a region encoding non-translated RNAs, expressed solely within the brain, can regulate bone mass in health and disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Base Sequence*
  • Bone Density
  • Bone and Bones / abnormalities
  • Bone and Bones / metabolism*
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation, Developmental
  • Genomic Imprinting*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Molecular Sequence Data
  • Neurons / metabolism
  • Neurons / pathology
  • Neuropeptide Y / genetics
  • Neuropeptide Y / metabolism
  • Prader-Willi Syndrome / genetics*
  • Prader-Willi Syndrome / metabolism
  • Prader-Willi Syndrome / pathology
  • Proprotein Convertases / genetics
  • Proprotein Convertases / metabolism
  • RNA, Small Nucleolar / genetics*
  • RNA, Small Nucleolar / metabolism
  • Sequence Deletion*
  • Signal Transduction

Substances

  • Neuropeptide Y
  • RNA, Small Nucleolar
  • Proprotein Convertases

Grants and funding

This study was supported by the National Health and Medical Research Council (NHMRC) of Australia project grant #1028882 by providing funds for reagents.