RNA editing regulates host immune response and T cell homeostasis in SARS-CoV-2 infection

PLoS One. 2024 Aug 23;19(8):e0307450. doi: 10.1371/journal.pone.0307450. eCollection 2024.

Abstract

Adenosine to inosine (A-to-I) RNA editing by ADAR1 has been implicated in maintaining self-tolerance, preventing autoimmunity, and mediating antiviral immunity. Foreign viral double-stranded RNA triggers rapid interferon response and activates ADAR1 in the host immune system. Emerging data points to a role of ADAR1 A-to-I editing in the inflammatory response associated with severe COVID-19 disease. We identify A-to-I editing events within human whole transcriptome data from SARS-CoV-2 infected individuals, non-infected individuals, and individuals with other viral illnesses from nasopharyngeal swabs. High levels of RNA editing in host cells are associated with low SARS-CoV-2 viral load (p = 9.27 E-06), suggesting an inhibitory effect of ADAR1 on viral infection. Additionally, we find differentially expressed genes associated with RNA-modifications and interferon response. Single cell RNA-sequencing analysis of SARS-CoV-2 infected nasopharyngeal swabs reveals that cytotoxic CD8 T cells upregulate ADAR1 in COVID-19 positive samples (p = 0.0269). We further reveal ADAR1 expression increases with CD4 and CD8 T cell activation, and knockdown of ADAR1 leads to apoptosis and aberrant IL-2 secretion. Together, our data suggests A-to-I RNA editing is required to maintain healthy homeostasis of activated T cells to combat SARS-CoV-2 infection.

MeSH terms

  • Adenosine / metabolism
  • Adenosine Deaminase* / genetics
  • Adenosine Deaminase* / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • COVID-19* / genetics
  • COVID-19* / immunology
  • COVID-19* / virology
  • Homeostasis*
  • Humans
  • Inosine / metabolism
  • Lymphocyte Activation / immunology
  • RNA Editing*
  • RNA-Binding Proteins* / genetics
  • RNA-Binding Proteins* / metabolism
  • SARS-CoV-2* / immunology
  • SARS-CoV-2* / physiology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Viral Load

Substances

  • Adenosine Deaminase
  • ADAR protein, human
  • RNA-Binding Proteins
  • Inosine
  • Adenosine