YIPF5 mutations cause neonatal diabetes and microcephaly through endoplasmic reticulum stress

J Clin Invest. 2020 Dec 1;130(12):6338-6353. doi: 10.1172/JCI141455.

Abstract

Neonatal diabetes is caused by single gene mutations reducing pancreatic β cell number or impairing β cell function. Understanding the genetic basis of rare diabetes subtypes highlights fundamental biological processes in β cells. We identified 6 patients from 5 families with homozygous mutations in the YIPF5 gene, which is involved in trafficking between the endoplasmic reticulum (ER) and the Golgi. All patients had neonatal/early-onset diabetes, severe microcephaly, and epilepsy. YIPF5 is expressed during human brain development, in adult brain and pancreatic islets. We used 3 human β cell models (YIPF5 silencing in EndoC-βH1 cells, YIPF5 knockout and mutation knockin in embryonic stem cells, and patient-derived induced pluripotent stem cells) to investigate the mechanism through which YIPF5 loss of function affects β cells. Loss of YIPF5 function in stem cell-derived islet cells resulted in proinsulin retention in the ER, marked ER stress, and β cell failure. Partial YIPF5 silencing in EndoC-βH1 cells and a patient mutation in stem cells increased the β cell sensitivity to ER stress-induced apoptosis. We report recessive YIPF5 mutations as the genetic cause of a congenital syndrome of microcephaly, epilepsy, and neonatal/early-onset diabetes, highlighting a critical role of YIPF5 in β cells and neurons. We believe this is the first report of mutations disrupting the ER-to-Golgi trafficking, resulting in diabetes.

Keywords: Cell Biology; Cell stress; Diabetes; Genetics; Human stem cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Diabetes Mellitus* / embryology
  • Diabetes Mellitus* / genetics
  • Diabetes Mellitus* / pathology
  • Endoplasmic Reticulum Stress / genetics*
  • Female
  • Genetic Diseases, Inborn* / embryology
  • Genetic Diseases, Inborn* / genetics
  • Genetic Diseases, Inborn* / pathology
  • Human Embryonic Stem Cells / metabolism
  • Human Embryonic Stem Cells / pathology
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology
  • Infant, Newborn
  • Infant, Newborn, Diseases* / embryology
  • Infant, Newborn, Diseases* / genetics
  • Infant, Newborn, Diseases* / pathology
  • Insulin-Secreting Cells / metabolism
  • Insulin-Secreting Cells / pathology
  • Male
  • Microcephaly* / embryology
  • Microcephaly* / genetics
  • Microcephaly* / pathology
  • Mutation*
  • Neurons / metabolism
  • Neurons / pathology
  • Vesicular Transport Proteins* / genetics
  • Vesicular Transport Proteins* / metabolism

Substances

  • Vesicular Transport Proteins
  • YIPF5 protein, human