The SARS-CoV-2 Spike protein has a broad tropism for mammalian ACE2 proteins.

Carina Conceicao1 Nazia Thakur1 Stacey Human1 James T Kelly1 Leanne Logan1 Dagmara Bialy1 Sushant Bhat1 Phoebe Stevenson-Leggett1 Adrian K Zagrajek1 Philippa Hollinghurst1,2 Michal Varga1 Christina Tsirigoti1 Matthew Tully1 Chris Chiu1 Katy Moffat1 Adrian Paul Silesian1 John A Hammond1 Helena J Maier1 Erica Bickerton1 Holly Shelton1 Isabelle Dietrich1 Stephen C Graham3 Dalan Bailey1
Affiliations 3 institutions
  1. The Pirbright Institute, Woking, Surrey, United Kingdom.
  2. Department of Microbial Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom.
  3. Department of Pathology, University of Cambridge, Cambridge, United Kingdom.

Abstract

SARS Coronavirus 2 (SARS-CoV-2) emerged in late 2019, leading to the Coronavirus Disease 2019 (COVID-19) pandemic that continues to cause significant global mortality in human populations. Given its sequence similarity to SARS-CoV, as well as related coronaviruses circulating in bats, SARS-CoV-2 is thought to have originated in Chiroptera species in China. However, whether the virus spread directly to humans or through an intermediate host is currently unclear, as is the potential for this virus to infect companion animals, livestock, and wildlife that could act as viral reservoirs. Using a combination of surrogate entry assays and live virus, we demonstrate that, in addition to human angiotensin-converting enzyme 2 (ACE2), the Spike glycoprotein of SARS-CoV-2 has a broad host tropism for mammalian ACE2 receptors, despite divergence in the amino acids at the Spike receptor binding site on these proteins. Of the 22 different hosts we investigated, ACE2 proteins from dog, cat, and cattle were the most permissive to SARS-CoV-2, while bat and bird ACE2 proteins were the least efficiently used receptors. The absence of a significant tropism for any of the 3 genetically distinct bat ACE2 proteins we examined indicates that SARS-CoV-2 receptor usage likely shifted during zoonotic transmission from bats into people, possibly in an intermediate reservoir. Comparison of SARS-CoV-2 receptor usage to the related coronaviruses SARS-CoV and RaTG13 identified distinct tropisms, with the 2 human viruses being more closely aligned. Finally, using bioinformatics, structural data, and targeted mutagenesis, we identified amino acid residues within the Spike-ACE2 interface, which may have played a pivotal role in the emergence of SARS-CoV-2 in humans. The apparently broad tropism of SARS-CoV-2 at the point of viral entry confirms the potential risk of infection to a wide range of companion animals, livestock, and wildlife.

Supporting text Virus Host Location
Viral Tropism 45 Virus Attachment 55 Amino Acid Substitution 81 Angiotensin-Converting Enzyme 2 177 Animals 1948 Binding Sites 89 Cats 120 Cattle 126 Dogs 176 Guinea Pigs 21 HEK293 Cells 61 Host-Pathogen Interactions 55 Humans 1440 Rabbits 25 Rats 73 SARS-CoV-2 453 Spike Glycoprotein, Coronavirus 274 Viral Zoonoses 65 spike protein, SARS-CoV-2 157

Evidence records

5 total
Experimental Infection
1 records · 1 evidence types
Evidence type
1 records
OVE4381
Key finding

SARS-CoV-2 Spike glycoprotein mediates entry through ACE2 receptors from multiple mammalian species, showing that dog, cat, and cattle ACE2 were most permissive while bat and bird ACE2 were least efficiently used.

Virus
Host
Location
Not specified
Supporting text

Using a combination of surrogate entry assays and live virus, we demonstrate that, in addition to human angiotensin-converting enzyme 2 (ACE2), the Spike glycoprotein of SARS-CoV-2 has a broad host tropism for mammalian ACE2 receptors. Of the 22 different hosts we investigated, ACE2 proteins from dog, cat, and cattle were the most permissive to SARS-CoV-2, while bat and bird ACE2 proteins were the least efficiently used receptors.

Method
surrogate entry assay | live virus infection assay
Experimental system
surrogate entry assay and live-virus infection system using ACE2 from multiple species
Functional Mechanism
4 records · 2 evidence types
Evidence type
3 records
OVE4382
Key finding

SARS-CoV-2 Spike protein uses angiotensin-converting enzyme 2 (ACE2) as its entry receptor across multiple mammalian species, with variable entry efficiency.

Virus
Host
Location
Not specified
Supporting text

Using a combination of surrogate entry assays and live virus, we demonstrate that, in addition to human angiotensin-converting enzyme 2 (ACE2), the Spike glycoprotein of SARS-CoV-2 has a broad host tropism for mammalian ACE2 receptors.

Method
surrogate entry assays | live virus experiment | receptor binding comparison
Receptors
angiotensin-converting enzyme 2 (ACE2)
OVE4383
Key finding

ACE2 proteins from dog, cat, and cattle were the most permissive to SARS-CoV-2 entry, while bat and bird ACE2 proteins were inefficient receptors.

Virus
Host
Location
Not specified
Supporting text

Of the 22 different hosts we investigated, ACE2 proteins from dog, cat, and cattle were the most permissive to SARS-CoV-2, while bat and bird ACE2 proteins were the least efficiently used receptors.

Method
surrogate entry assays | live virus infection assays
Receptors
ACE2
OVE4387
Key finding

SARS-CoV-2 receptor usage likely shifted during zoonotic transmission from bats into humans, suggesting an animal-to-human spillover possibly involving an intermediate reservoir.

Virus
Host
Location
Not specified
Supporting text

The absence of a significant tropism for any of the 3 genetically distinct bat ACE2 proteins we examined indicates that SARS-CoV-2 receptor usage likely shifted during zoonotic transmission from bats into people, possibly in an intermediate reservoir.

Method
ACE2 receptor tropism assay | virus entry assay | comparative genetic analysis
Receptors
ACE2
Evidence type
1 records
OVE4385
Key finding

Amino acid residues within the SARS-CoV-2 Spike–ACE2 interface are implicated in molecular adaptation linked to human emergence.

Virus
Host
Not specified
Location
Not specified
Supporting text

Using bioinformatics, structural data, and targeted mutagenesis, we identified amino acid residues within the Spike-ACE2 interface, which may have played a pivotal role in the emergence of SARS-CoV-2 in humans.

Genes or proteins
Spike | ACE2
Receptors
ACE2
Mechanism types
receptor binding | host-range expansion