Single-nucleus transcriptomic landscape of primate hippocampal aging

Protein Cell. 2021 Sep;12(9):695-716. doi: 10.1007/s13238-021-00852-9. Epub 2021 May 30.

Abstract

The hippocampus plays a crucial role in learning and memory, and its progressive deterioration with age is functionally linked to a variety of human neurodegenerative diseases. Yet a systematic profiling of the aging effects on various hippocampal cell types in primates is still missing. Here, we reported a variety of new aging-associated phenotypic changes of the primate hippocampus. These include, in particular, increased DNA damage and heterochromatin erosion with time, alongside loss of proteostasis and elevated inflammation. To understand their cellular and molecular causes, we established the first single-nucleus transcriptomic atlas of primate hippocampal aging. Among the 12 identified cell types, neural transiently amplifying progenitor cell (TAPC) and microglia were most affected by aging. In-depth dissection of gene-expression dynamics revealed impaired TAPC division and compromised neuronal function along the neurogenesis trajectory; additionally elevated pro-inflammatory responses in the aged microglia and oligodendrocyte, as well as dysregulated coagulation pathways in the aged endothelial cells may contribute to a hostile microenvironment for neurogenesis. This rich resource for understanding primate hippocampal aging may provide potential diagnostic biomarkers and therapeutic interventions against age-related neurodegenerative diseases.

Keywords: aging; hippocampus; primate; single-cell RNA sequencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / genetics*
  • Amyloid beta-Peptides / genetics
  • Amyloid beta-Peptides / metabolism
  • Animals
  • DNA Damage
  • Endothelial Cells / cytology
  • Endothelial Cells / metabolism
  • Female
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental
  • Heterochromatin / chemistry
  • Heterochromatin / metabolism
  • High-Throughput Nucleotide Sequencing
  • Hippocampus / cytology
  • Hippocampus / growth & development
  • Hippocampus / metabolism*
  • Humans
  • Inflammation
  • Long Interspersed Nucleotide Elements
  • Macaca mulatta / genetics*
  • Macaca mulatta / growth & development
  • Macaca mulatta / metabolism
  • Male
  • Microglia / cytology
  • Microglia / metabolism
  • Nerve Tissue Proteins / classification
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism
  • Neurogenesis / genetics*
  • Neurons / cytology
  • Neurons / metabolism
  • Oligodendroglia / cytology
  • Oligodendroglia / metabolism
  • Single-Cell Analysis
  • Transcriptome*

Substances

  • Amyloid beta-Peptides
  • Heterochromatin
  • Nerve Tissue Proteins