Unacylated-Ghrelin Impairs Hippocampal Neurogenesis and Memory in Mice and Is Altered in Parkinson's Dementia in Humans

Cell Rep Med. 2020 Oct 20;1(7):100120. doi: 10.1016/j.xcrm.2020.100120.

Abstract

Blood-borne factors regulate adult hippocampal neurogenesis and cognition in mammals. We report that elevating circulating unacylated-ghrelin (UAG), using both pharmacological and genetic methods, reduced hippocampal neurogenesis and plasticity in mice. Spatial memory impairments observed in ghrelin-O-acyl transferase-null (GOAT-/-) mice that lack acyl-ghrelin (AG) but have high levels of UAG were rescued by acyl-ghrelin. Acyl-ghrelin-mediated neurogenesis in vitro was dependent on non-cell-autonomous BDNF signaling that was inhibited by UAG. These findings suggest that post-translational acylation of ghrelin is important to neurogenesis and memory in mice. To determine relevance in humans, we analyzed circulating AG:UAG in Parkinson disease (PD) patients diagnosed with dementia (PDD), cognitively intact PD patients, and controls. Notably, plasma AG:UAG was only reduced in PDD. Hippocampal ghrelin-receptor expression remained unchanged; however, GOAT+ cell number was reduced in PDD. We identify UAG as a regulator of hippocampal-dependent plasticity and spatial memory and AG:UAG as a putative circulating diagnostic biomarker of dementia.

Keywords: AG:UAG; BDNF; GOAT; Parkinson disease dementia; acyl-ghrelin; adult hippocampal neurogenesis; biomarker; ghrelin; memory; unacylated-ghrelin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyltransferases / deficiency
  • Acyltransferases / genetics*
  • Animals
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • Cognition / physiology
  • Disease Models, Animal
  • Female
  • Gene Expression Regulation
  • Ghrelin / analogs & derivatives*
  • Ghrelin / genetics*
  • Ghrelin / metabolism
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Humans
  • Male
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurogenesis / genetics
  • Neuronal Plasticity / genetics
  • Neurons / metabolism
  • Neurons / pathology
  • Parkinson Disease / genetics*
  • Parkinson Disease / metabolism
  • Parkinson Disease / pathology
  • Primary Cell Culture
  • Rats
  • Signal Transduction
  • Spatial Memory / physiology
  • Supranuclear Palsy, Progressive / genetics*
  • Supranuclear Palsy, Progressive / metabolism
  • Supranuclear Palsy, Progressive / pathology

Substances

  • Bdnf protein, mouse
  • Brain-Derived Neurotrophic Factor
  • Ghrelin
  • Membrane Proteins
  • acyl-ghrelin
  • Acyltransferases
  • MBOAT4 protein, human
  • Mboat4 protein, mouse

Supplementary concepts

  • Progressive supranuclear palsy atypical