Profound Treg perturbations correlate with COVID-19 severity

Proc Natl Acad Sci U S A. 2021 Sep 14;118(37):e2111315118. doi: 10.1073/pnas.2111315118.

Abstract

The hallmark of severe COVID-19 is an uncontrolled inflammatory response, resulting from poorly understood immunological dysfunction. We hypothesized that perturbations in FoxP3+ T regulatory cells (Treg), key enforcers of immune homeostasis, contribute to COVID-19 pathology. Cytometric and transcriptomic profiling revealed a distinct Treg phenotype in severe COVID-19 patients, with an increase in Treg proportions and intracellular levels of the lineage-defining transcription factor FoxP3, correlating with poor outcomes. These Tregs showed a distinct transcriptional signature, with overexpression of several suppressive effectors, but also proinflammatory molecules like interleukin (IL)-32, and a striking similarity to tumor-infiltrating Tregs that suppress antitumor responses. Most marked during acute severe disease, these traits persisted somewhat in convalescent patients. A screen for candidate agents revealed that IL-6 and IL-18 may individually contribute different facets of these COVID-19-linked perturbations. These results suggest that Tregs may play nefarious roles in COVID-19, by suppressing antiviral T cell responses during the severe phase of the disease, and by a direct proinflammatory role.

Keywords: COVID-19; FoxP3; Tregs; tumor Tregs.

Publication types

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

MeSH terms

  • Adult
  • Aged
  • CD4-Positive T-Lymphocytes / virology
  • COVID-19 / etiology*
  • Female
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation
  • Humans
  • Inflammation / metabolism
  • Inflammation / virology
  • Interleukin-18 / genetics
  • Interleukin-18 / metabolism
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Lymphocytes, Tumor-Infiltrating / physiology
  • Male
  • Middle Aged
  • Severity of Illness Index
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / physiology*
  • T-Lymphocytes, Regulatory / virology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • IL18 protein, human
  • IL2RA protein, human
  • IL6 protein, human
  • Interleukin-18
  • Interleukin-2 Receptor alpha Subunit
  • Interleukin-6
  • Transcription Factors