Sex-biased islet β cell dysfunction is caused by the MODY MAFA S64F variant by inducing premature aging and senescence in males

Cell Rep. 2021 Oct 12;37(2):109813. doi: 10.1016/j.celrep.2021.109813.

Abstract

A heterozygous missense mutation of the islet β cell-enriched MAFA transcription factor (p.Ser64Phe [S64F]) is found in patients with adult-onset β cell dysfunction (diabetes or insulinomatosis), with men more prone to diabetes than women. This mutation engenders increased stability to the unstable MAFA protein. Here, we develop a S64F MafA mouse model to determine how β cell function is affected and find sex-dependent phenotypes. Heterozygous mutant males (MafAS64F/+) display impaired glucose tolerance, while females are slightly hypoglycemic with improved blood glucose clearance. Only MafAS64F/+ males show transiently higher MafA protein levels preceding glucose intolerance and sex-dependent changes to genes involved in Ca2+ signaling, DNA damage, aging, and senescence. MAFAS64F production in male human β cells also accelerate cellular senescence and increase senescence-associated secretory proteins compared to cells expressing MAFAWT. These results implicate a conserved mechanism of accelerated islet aging and senescence in promoting diabetes in MAFAS64F carriers in a sex-biased manner.

Keywords: MAFA; beta cell; cellular senescence; diabetes; islet biology; sexual dimorphism.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Blood Glucose / metabolism
  • Calcium Signaling
  • Cell Line
  • Cellular Senescence*
  • DNA Damage
  • Diabetes Mellitus, Type 2 / genetics
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetes Mellitus, Type 2 / pathology
  • Disease Models, Animal
  • Female
  • Genetic Predisposition to Disease
  • Humans
  • Insulin / blood
  • Insulin-Secreting Cells / metabolism*
  • Insulin-Secreting Cells / pathology
  • Maf Transcription Factors, Large / genetics
  • Maf Transcription Factors, Large / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mutation, Missense
  • Phenotype
  • Sex Characteristics
  • Sex Factors

Substances

  • Blood Glucose
  • Insulin
  • MAFA protein, human
  • Maf Transcription Factors, Large
  • Mafa protein, mouse