Altered cell and RNA isoform diversity in aging Down syndrome brains

Proc Natl Acad Sci U S A. 2021 Nov 23;118(47):e2114326118. doi: 10.1073/pnas.2114326118.

Abstract

Down syndrome (DS), trisomy of human chromosome 21 (HSA21), is characterized by lifelong cognitive impairments and the development of the neuropathological hallmarks of Alzheimer's disease (AD). The cellular and molecular modifications responsible for these effects are not understood. Here we performed single-nucleus RNA sequencing (snRNA-seq) employing both short- (Illumina) and long-read (Pacific Biosciences) sequencing technologies on a total of 29 DS and non-DS control prefrontal cortex samples. In DS, the ratio of inhibitory-to-excitatory neurons was significantly increased, which was not observed in previous reports examining sporadic AD. DS microglial transcriptomes displayed AD-related aging and activation signatures in advance of AD neuropathology, with increased microglial expression of C1q complement genes (associated with dendritic pruning) and the HSA21 transcription factor gene RUNX1 Long-read sequencing detected vast RNA isoform diversity within and among specific cell types, including numerous sequences that differed between DS and control brains. Notably, over 8,000 genes produced RNAs containing intra-exonic junctions, including amyloid precursor protein (APP) that had previously been associated with somatic gene recombination. These and related results illuminate large-scale cellular and transcriptomic alterations as features of the aging DS brain.

Keywords: Down syndrome; gene recombination; intra-exonic junctions; microglia; single-nucleus RNA sequencing.

Publication types

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

MeSH terms

  • Aging / physiology*
  • Alzheimer Disease / metabolism
  • Amyloid beta-Protein Precursor / metabolism
  • Brain / metabolism
  • Chromosomes, Human, Pair 21
  • Core Binding Factor Alpha 2 Subunit / metabolism
  • Down Syndrome / genetics
  • Down Syndrome / metabolism*
  • Gene Expression
  • Humans
  • Microglia
  • RNA / metabolism
  • RNA Isoforms / metabolism*
  • Sequence Analysis, RNA
  • Up-Regulation

Substances

  • Amyloid beta-Protein Precursor
  • Core Binding Factor Alpha 2 Subunit
  • RNA Isoforms
  • RUNX1 protein, human
  • RNA