Deep spatial profiling of human COVID-19 brains reveals neuroinflammation with distinct microanatomical microglia-T-cell interactions

Immunity. 2021 Jul 13;54(7):1594-1610.e11. doi: 10.1016/j.immuni.2021.06.002. Epub 2021 Jun 9.

Abstract

COVID-19 can cause severe neurological symptoms, but the underlying pathophysiological mechanisms are unclear. Here, we interrogated the brain stems and olfactory bulbs in postmortem patients who had COVID-19 using imaging mass cytometry to understand the local immune response at a spatially resolved, high-dimensional, single-cell level and compared their immune map to non-COVID respiratory failure, multiple sclerosis, and control patients. We observed substantial immune activation in the central nervous system with pronounced neuropathology (astrocytosis, axonal damage, and blood-brain-barrier leakage) and detected viral antigen in ACE2-receptor-positive cells enriched in the vascular compartment. Microglial nodules and the perivascular compartment represented COVID-19-specific, microanatomic-immune niches with context-specific cellular interactions enriched for activated CD8+ T cells. Altered brain T-cell-microglial interactions were linked to clinical measures of systemic inflammation and disturbed hemostasis. This study identifies profound neuroinflammation with activation of innate and adaptive immune cells as correlates of COVID-19 neuropathology, with implications for potential therapeutic strategies.

Keywords: COVID-19; SARS-CoV-2; T cells; brain autopsy; encephalopathy; high-dimensional imaging; mass cytometry; microglia; neuroinflammation; single-cell analysis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood-Brain Barrier / immunology
  • Blood-Brain Barrier / metabolism
  • Blood-Brain Barrier / pathology
  • Brain / immunology*
  • Brain / metabolism
  • Brain / pathology
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / metabolism
  • COVID-19 / immunology*
  • COVID-19 / pathology
  • Cell Communication
  • Central Nervous System / immunology
  • Central Nervous System / metabolism
  • Central Nervous System / pathology
  • Humans
  • Immune Checkpoint Proteins / metabolism
  • Inflammation
  • Lymphocyte Activation
  • Microglia / immunology*
  • Multiple Sclerosis / immunology
  • Multiple Sclerosis / pathology
  • Olfactory Bulb / immunology
  • Olfactory Bulb / metabolism
  • Olfactory Bulb / pathology
  • Respiratory Insufficiency / immunology
  • Respiratory Insufficiency / pathology
  • SARS-CoV-2
  • Spike Glycoprotein, Coronavirus / metabolism
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism

Substances

  • Immune Checkpoint Proteins
  • Spike Glycoprotein, Coronavirus
  • spike protein, SARS-CoV-2