A mouse-adapted model of SARS-CoV-2 to test COVID-19 countermeasures

Nature. 2020 Oct;586(7830):560-566. doi: 10.1038/s41586-020-2708-8. Epub 2020 Aug 27.

Abstract

Coronaviruses are prone to transmission to new host species, as recently demonstrated by the spread to humans of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of the coronavirus disease 2019 (COVID-19) pandemic1. Small animal models that recapitulate SARS-CoV-2 disease are needed urgently for rapid evaluation of medical countermeasures2,3. SARS-CoV-2 cannot infect wild-type laboratory mice owing to inefficient interactions between the viral spike protein and the mouse orthologue of the human receptor, angiotensin-converting enzyme 2 (ACE2)4. Here we used reverse genetics5 to remodel the interaction between SARS-CoV-2 spike protein and mouse ACE2 and designed mouse-adapted SARS-CoV-2 (SARS-CoV-2 MA), a recombinant virus that can use mouse ACE2 for entry into cells. SARS-CoV-2 MA was able to replicate in the upper and lower airways of both young adult and aged BALB/c mice. SARS-CoV-2 MA caused more severe disease in aged mice, and exhibited more clinically relevant phenotypes than those seen in Hfh4-ACE2 transgenic mice, which express human ACE2 under the control of the Hfh4 (also known as Foxj1) promoter. We demonstrate the utility of this model using vaccine-challenge studies in immune-competent mice with native expression of mouse ACE2. Finally, we show that the clinical candidate interferon-λ1a (IFN-λ1a) potently inhibits SARS-CoV-2 replication in primary human airway epithelial cells in vitro-both prophylactic and therapeutic administration of IFN-λ1a diminished SARS-CoV-2 replication in mice. In summary, the mouse-adapted SARS-CoV-2 MA model demonstrates age-related disease pathogenesis and supports the clinical use of pegylated IFN-λ1a as a treatment for human COVID-196.

Publication types

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

MeSH terms

  • Aging / immunology
  • Angiotensin-Converting Enzyme 2
  • Animals
  • Betacoronavirus* / drug effects
  • Betacoronavirus* / immunology
  • Betacoronavirus* / pathogenicity
  • COVID-19
  • COVID-19 Vaccines
  • Coronavirus Infections / drug therapy*
  • Coronavirus Infections / genetics
  • Coronavirus Infections / immunology
  • Coronavirus Infections / prevention & control*
  • Disease Models, Animal*
  • Female
  • Forkhead Transcription Factors / genetics
  • Humans
  • Interferon-alpha / administration & dosage
  • Interferon-alpha / pharmacology
  • Interferon-alpha / therapeutic use
  • Interferons / administration & dosage
  • Interferons / pharmacology*
  • Interferons / therapeutic use*
  • Interleukins / administration & dosage
  • Interleukins / pharmacology*
  • Interleukins / therapeutic use*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Transgenic
  • Models, Molecular
  • Pandemics / prevention & control*
  • Peptidyl-Dipeptidase A / genetics
  • Peptidyl-Dipeptidase A / metabolism
  • Pneumonia, Viral / drug therapy*
  • Pneumonia, Viral / genetics
  • Pneumonia, Viral / immunology
  • Pneumonia, Viral / prevention & control*
  • Receptors, Virus / genetics
  • Receptors, Virus / metabolism
  • SARS-CoV-2
  • Viral Vaccines / immunology*

Substances

  • COVID-19 Vaccines
  • FOXJ1 protein, mouse
  • Forkhead Transcription Factors
  • interferon-lambda, human
  • Interferon-alpha
  • Interleukins
  • Receptors, Virus
  • Viral Vaccines
  • Interferons
  • Peptidyl-Dipeptidase A
  • ACE2 protein, human
  • Ace2 protein, mouse
  • Angiotensin-Converting Enzyme 2