Modulation of hippocampal neuronal resilience during aging by the Hsp70/Hsp90 co-chaperone STI1

J Neurochem. 2020 Jun;153(6):727-758. doi: 10.1111/jnc.14882. Epub 2019 Oct 31.

Abstract

Chaperone networks are dysregulated with aging, but whether compromised Hsp70/Hsp90 chaperone function disturbs neuronal resilience is unknown. Stress-inducible phosphoprotein 1 (STI1; STIP1; HOP) is a co-chaperone that simultaneously interacts with Hsp70 and Hsp90, but whose function in vivo remains poorly understood. We combined in-depth analysis of chaperone genes in human datasets, analysis of a neuronal cell line lacking STI1 and of a mouse line with a hypomorphic Stip1 allele to investigate the requirement for STI1 in aging. Our experiments revealed that dysfunctional STI1 activity compromised Hsp70/Hsp90 chaperone network and neuronal resilience. The levels of a set of Hsp90 co-chaperones and client proteins were selectively affected by reduced levels of STI1, suggesting that their stability depends on functional Hsp70/Hsp90 machinery. Analysis of human databases revealed a subset of co-chaperones, including STI1, whose loss of function is incompatible with life in mammals, albeit they are not essential in yeast. Importantly, mice expressing a hypomorphic STI1 allele presented spontaneous age-dependent hippocampal neurodegeneration and reduced hippocampal volume, with consequent spatial memory deficit. We suggest that impaired STI1 function compromises Hsp70/Hsp90 chaperone activity in mammals and can by itself cause age-dependent hippocampal neurodegeneration in mice. Cover Image for this issue: doi: 10.1111/jnc.14749.

Keywords: HOP/STI1; Hsp70/Hsp90; aging; neurodegeneration.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / physiology
  • Aging / genetics
  • Aging / metabolism*
  • Animals
  • Embryonic Stem Cells / metabolism
  • Gene Knockout Techniques / methods
  • HSP70 Heat-Shock Proteins / genetics
  • HSP70 Heat-Shock Proteins / metabolism*
  • HSP90 Heat-Shock Proteins / genetics
  • HSP90 Heat-Shock Proteins / metabolism*
  • Heat-Shock Proteins / deficiency*
  • Heat-Shock Proteins / genetics
  • Hippocampus / cytology
  • Hippocampus / metabolism*
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism*
  • Neurons / metabolism

Substances

  • HSP70 Heat-Shock Proteins
  • HSP90 Heat-Shock Proteins
  • Heat-Shock Proteins
  • Molecular Chaperones
  • Stip1 protein, mouse