Deficiency in prohormone convertase PC1 impairs prohormone processing in Prader-Willi syndrome

J Clin Invest. 2017 Jan 3;127(1):293-305. doi: 10.1172/JCI88648. Epub 2016 Dec 12.

Abstract

Prader-Willi syndrome (PWS) is caused by a loss of paternally expressed genes in an imprinted region of chromosome 15q. Among the canonical PWS phenotypes are hyperphagic obesity, central hypogonadism, and low growth hormone (GH). Rare microdeletions in PWS patients define a 91-kb minimum critical deletion region encompassing 3 genes, including the noncoding RNA gene SNORD116. Here, we found that protein and transcript levels of nescient helix loop helix 2 (NHLH2) and the prohormone convertase PC1 (encoded by PCSK1) were reduced in PWS patient induced pluripotent stem cell-derived (iPSC-derived) neurons. Moreover, Nhlh2 and Pcsk1 expression were reduced in hypothalami of fasted Snord116 paternal knockout (Snord116p-/m+) mice. Hypothalamic Agrp and Npy remained elevated following refeeding in association with relative hyperphagia in Snord116p-/m+ mice. Nhlh2-deficient mice display growth deficiencies as adolescents and hypogonadism, hyperphagia, and obesity as adults. Nhlh2 has also been shown to promote Pcsk1 expression. Humans and mice deficient in PC1 display hyperphagic obesity, hypogonadism, decreased GH, and hypoinsulinemic diabetes due to impaired prohormone processing. Here, we found that Snord116p-/m+ mice displayed in vivo functional defects in prohormone processing of proinsulin, pro-GH-releasing hormone, and proghrelin in association with reductions in islet, hypothalamic, and stomach PC1 content. Our findings suggest that the major neuroendocrine features of PWS are due to PC1 deficiency.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Diabetes Mellitus / genetics
  • Diabetes Mellitus / metabolism
  • Diabetes Mellitus / pathology
  • Female
  • Growth Hormone-Releasing Hormone / genetics
  • Growth Hormone-Releasing Hormone / metabolism*
  • Humans
  • Hyperphagia / genetics
  • Hyperphagia / metabolism
  • Hyperphagia / pathology
  • Hypogonadism / genetics
  • Hypogonadism / metabolism
  • Hypogonadism / pathology
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology
  • Male
  • Mice, Knockout
  • Neurons / metabolism*
  • Neurons / pathology
  • Obesity / genetics
  • Obesity / metabolism
  • Obesity / pathology
  • Prader-Willi Syndrome / genetics
  • Prader-Willi Syndrome / metabolism*
  • Prader-Willi Syndrome / pathology
  • Proinsulin / genetics
  • Proinsulin / metabolism*
  • Proprotein Convertase 1 / deficiency*
  • Protein Precursors / genetics
  • Protein Precursors / metabolism*
  • RNA, Small Nucleolar / genetics
  • RNA, Small Nucleolar / metabolism

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Nhlh2 protein, mouse
  • Protein Precursors
  • RNA, Small Nucleolar
  • SNORD116 RNA, human
  • SNORD116 RNA, mouse
  • pro-growth hormone releasing hormone, mouse
  • NHLH2 protein, human
  • Growth Hormone-Releasing Hormone
  • Proinsulin
  • PCSK1 protein, human
  • Pcsk1 protein, mouse
  • Proprotein Convertase 1