ORAI1 Limits SARS-CoV-2 Infection by Regulating Tonic Type I IFN Signaling

J Immunol. 2022 Jan 1;208(1):74-84. doi: 10.4049/jimmunol.2100742. Epub 2021 Nov 24.

Abstract

ORAI1 and stromal interaction molecule 1 (STIM1) are the critical mediators of store-operated Ca2+ entry by acting as the pore subunit and an endoplasmic reticulum-resident signaling molecule, respectively. In addition to Ca2+ signaling, STIM1 is also involved in regulation of the type I IFN (IFN-I) response. To examine their potential role in severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection, we generated ORAI1 and STIM1 knockout human HEK293-angiotensin-converting enzyme 2 cells and checked their responses. STIM1 knockout cells showed strong resistance to SARS-CoV-2 infection as a result of enhanced IFN-I response. On the contrary, ORAI1 deletion induced high susceptibility to SARS-CoV-2 infection. Mechanistically, ORAI1 knockout cells showed reduced homeostatic cytoplasmic Ca2+ concentration and severe impairment in tonic IFN-I signaling. Transcriptome analysis showed downregulation of multiple antiviral signaling pathways in ORAI1 knockout cells, likely because of reduced expression of the Ca2+-dependent transcription factors of the AP-1 family and MEF2C Accordingly, modulation of homeostatic Ca2+ concentration by pretreatment with ORAI1 blocker or agonist could influence baseline IFNB expression and resistance to SARS-CoV-2 infection in a human lung epithelial cell line. Our results identify a novel role of ORAI1-mediated Ca2+ signaling in regulating the tonic IFN-I levels, which determine host resistance to SARS-CoV-2 infection.

Publication types

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

MeSH terms

  • A549 Cells
  • Angiotensin-Converting Enzyme 2 / genetics
  • Angiotensin-Converting Enzyme 2 / metabolism
  • COVID-19 / immunology
  • COVID-19 / metabolism*
  • Calcium Signaling
  • Clustered Regularly Interspaced Short Palindromic Repeats
  • Disease Resistance
  • Disease Susceptibility
  • Gene Expression Profiling
  • HEK293 Cells
  • Humans
  • Interferon Type I / metabolism*
  • Lung / immunology*
  • Lung / virology
  • MEF2 Transcription Factors / genetics
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism*
  • ORAI1 Protein / genetics
  • ORAI1 Protein / metabolism*
  • Respiratory Mucosa / metabolism*
  • SARS-CoV-2 / physiology*
  • Stromal Interaction Molecule 1 / genetics
  • Stromal Interaction Molecule 1 / metabolism*
  • Transcription Factor AP-1 / genetics

Substances

  • Interferon Type I
  • MEF2 Transcription Factors
  • Neoplasm Proteins
  • ORAI1 Protein
  • ORAI1 protein, human
  • STIM1 protein, human
  • Stromal Interaction Molecule 1
  • Transcription Factor AP-1
  • Angiotensin-Converting Enzyme 2