The SARS-CoV-2 Spike protein has a broad tropism for mammalian ACE2 proteins
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...
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| Vydané v: | PLoS biology Ročník 18; číslo 12; s. e3001016 |
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| Hlavní autori: | , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
Public Library of Science
21.12.2020
Public Library of Science (PLoS) |
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| ISSN: | 1545-7885, 1544-9173, 1545-7885 |
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| 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. |
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| AbstractList | 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.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. 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. A study using a combination of surrogate entry assays and live virus suggests that SARS-CoV-2 may have a broad host-range, revealing that the virus's spike protein can use a broad range of host ACE2 receptors to enter cells and that the sequence of this protein might have changed during the zoonotic jump into humans. To this end, we synthesised expression constructs for human ACE2 as well as orthologues from 22 other vertebrate species, including 9 companion animals (dogs, cats, rabbits, guinea pigs, hamsters, horses, rats, ferrets, and chinchilla), 7 livestock species (chickens, cattle, sheep, goats, pigs, turkeys, and buffalo), 4 bat species (horseshoe bat, fruit bat, little brown bat, and flying fox bat), and 2 species confirmed or suspected to be associated with coronavirus outbreaks (civet and pangolin). There is 62% to 99% sequence identity between these proteins at the amino acid level (76% to 99% when excluding the 2 bird sequences), and their phylogenetic relationships are largely consistent with vertebrate phylogeny, although the guinea pig sequence was more divergent than predicted (Fig 1A). Examining the conservation of amino acids at the SARS-CoV-2 binding site on the surface of the ACE2 protein revealed a high degree of variation across mammalian taxa (Fig 1B and 1C), suggesting that SARS-CoV-2 receptor binding may vary between potential hosts. The cause of this poor expression is unknown, potentially arising due to errors in the ACE2 sequences available for these species (see Methods; Phylogenetic analysis). Since the available sequence accuracy for these 2 genes would need to be explored further, these 2 ACE2 proteins were excluded from our subsequent experiments. 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. To this end, we synthesised expression constructs for human ACE2 as well as orthologues from 22 other vertebrate species, including 9 companion animals (dogs, cats, rabbits, guinea pigs, hamsters, horses, rats, ferrets, and chinchilla), 7 livestock species (chickens, cattle, sheep, goats, pigs, turkeys, and buffalo), 4 bat species (horseshoe bat, fruit bat, little brown bat, and flying fox bat), and 2 species confirmed or suspected to be associated with coronavirus outbreaks (civet and pangolin). There is 62% to 99% sequence identity between these proteins at the amino acid level (76% to 99% when excluding the 2 bird sequences), and their phylogenetic relationships are largely consistent with vertebrate phylogeny, although the guinea pig sequence was more divergent than predicted (Fig 1A). Examining the conservation of amino acids at the SARS-CoV-2 binding site on the surface of the ACE2 protein revealed a high degree of variation across mammalian taxa (Fig 1B and 1C), suggesting that SARS-CoV-2 receptor binding may vary between potential hosts. The cause of this poor expression is unknown, potentially arising due to errors in the ACE2 sequences available for these species (see Methods; Phylogenetic analysis). Since the available sequence accuracy for these 2 genes would need to be explored further, these 2 ACE2 proteins were excluded from our subsequent experiments. |
| Audience | Academic |
| Author | Dietrich, Isabelle Moffat, Katy Thakur, Nazia Shelton, Holly Chiu, Chris Tully, Matthew Graham, Stephen C. Maier, Helena J. Human, Stacey Hammond, John A. Bialy, Dagmara Tsirigoti, Christina Stevenson-Leggett, Phoebe Conceicao, Carina Zagrajek, Adrian K. Bailey, Dalan Logan, Leanne Kelly, James T. Hollinghurst, Philippa Bickerton, Erica Varga, Michal Silesian, Adrian Paul Bhat, Sushant |
| AuthorAffiliation | 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 University of Wisconsin-Madison, UNITED STATES 3 Department of Pathology, University of Cambridge, Cambridge, United Kingdom |
| AuthorAffiliation_xml | – name: 3 Department of Pathology, University of Cambridge, Cambridge, United Kingdom – name: 2 Department of Microbial Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom – name: University of Wisconsin-Madison, UNITED STATES – name: 1 The Pirbright Institute, Woking, Surrey, United Kingdom |
| Author_xml | – sequence: 1 givenname: Carina surname: Conceicao fullname: Conceicao, Carina – sequence: 2 givenname: Nazia orcidid: 0000-0002-4450-5911 surname: Thakur fullname: Thakur, Nazia – sequence: 3 givenname: Stacey orcidid: 0000-0003-4735-2065 surname: Human fullname: Human, Stacey – sequence: 4 givenname: James T. orcidid: 0000-0002-8307-507X surname: Kelly fullname: Kelly, James T. – sequence: 5 givenname: Leanne surname: Logan fullname: Logan, Leanne – sequence: 6 givenname: Dagmara surname: Bialy fullname: Bialy, Dagmara – sequence: 7 givenname: Sushant orcidid: 0000-0003-1869-6176 surname: Bhat fullname: Bhat, Sushant – sequence: 8 givenname: Phoebe orcidid: 0000-0002-6509-3354 surname: Stevenson-Leggett fullname: Stevenson-Leggett, Phoebe – sequence: 9 givenname: Adrian K. surname: Zagrajek fullname: Zagrajek, Adrian K. – sequence: 10 givenname: Philippa surname: Hollinghurst fullname: Hollinghurst, Philippa – sequence: 11 givenname: Michal orcidid: 0000-0002-7437-1723 surname: Varga fullname: Varga, Michal – sequence: 12 givenname: Christina surname: Tsirigoti fullname: Tsirigoti, Christina – sequence: 13 givenname: Matthew orcidid: 0000-0002-1395-1775 surname: Tully fullname: Tully, Matthew – sequence: 14 givenname: Chris surname: Chiu fullname: Chiu, Chris – sequence: 15 givenname: Katy orcidid: 0000-0003-0120-7196 surname: Moffat fullname: Moffat, Katy – sequence: 16 givenname: Adrian Paul orcidid: 0000-0002-4100-9269 surname: Silesian fullname: Silesian, Adrian Paul – sequence: 17 givenname: John A. orcidid: 0000-0002-2213-3248 surname: Hammond fullname: Hammond, John A. – sequence: 18 givenname: Helena J. surname: Maier fullname: Maier, Helena J. – sequence: 19 givenname: Erica orcidid: 0000-0002-4012-1283 surname: Bickerton fullname: Bickerton, Erica – sequence: 20 givenname: Holly surname: Shelton fullname: Shelton, Holly – sequence: 21 givenname: Isabelle orcidid: 0000-0002-6300-109X surname: Dietrich fullname: Dietrich, Isabelle – sequence: 22 givenname: Stephen C. orcidid: 0000-0003-4547-4034 surname: Graham fullname: Graham, Stephen C. – sequence: 23 givenname: Dalan orcidid: 0000-0002-5640-2266 surname: Bailey fullname: Bailey, Dalan |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33347434$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2020 Public Library of Science 2020 Conceicao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2020 Conceicao et al 2020 Conceicao et al |
| Copyright_xml | – notice: COPYRIGHT 2020 Public Library of Science – notice: 2020 Conceicao et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2020 Conceicao et al 2020 Conceicao et al |
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| DOI | 10.1371/journal.pbio.3001016 |
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| Snippet | 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... To this end, we synthesised expression constructs for human ACE2 as well as orthologues from 22 other vertebrate species, including 9 companion animals (dogs,... |
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| SubjectTerms | ACE2 Amino acid sequence Amino Acid Substitution Amino acids Angiotensin converting enzyme Angiotensin-converting enzyme 2 Angiotensin-Converting Enzyme 2 - metabolism Animals Binding Sites Biology and life sciences Cats Cattle Conserved sequence Coronaviruses COVID-19 Divergence Dogs Flight Genetic aspects Goats Guinea Pigs Hamsters Health aspects HEK293 Cells Horses Host-Pathogen Interactions Host-virus relationships Humans Identification and classification Livestock Mammals Medicine and health sciences Middle East respiratory syndrome Phylogeny Physiological aspects Proteins Rabbits Rats Research and Analysis Methods SARS-CoV-2 - physiology Severe acute respiratory syndrome Severe acute respiratory syndrome coronavirus 2 Sheep Species Spike Glycoprotein, Coronavirus - metabolism Spike protein Swine Tropism Tropisms Vertebrates Viral diseases Viral Tropism Viral Zoonoses - virology Virus Attachment Zoonoses |
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| Title | The SARS-CoV-2 Spike protein has a broad tropism for mammalian ACE2 proteins |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/33347434 https://www.proquest.com/docview/2479139588 https://www.proquest.com/docview/2472112967 https://pubmed.ncbi.nlm.nih.gov/PMC7751883 https://doaj.org/article/f8b27b647dac40929bfb2e5622149f2e http://dx.doi.org/10.1371/journal.pbio.3001016 |
| Volume | 18 |
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