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...

Celý popis

Uložené v:
Podrobná bibliografia
Vydané v:PLoS biology Ročník 18; číslo 12; s. e3001016
Hlavní autori: Conceicao, Carina, Thakur, Nazia, Human, Stacey, Kelly, James T., Logan, Leanne, Bialy, Dagmara, Bhat, Sushant, Stevenson-Leggett, Phoebe, Zagrajek, Adrian K., Hollinghurst, Philippa, Varga, Michal, Tsirigoti, Christina, Tully, Matthew, Chiu, Chris, Moffat, Katy, Silesian, Adrian Paul, Hammond, John A., Maier, Helena J., Bickerton, Erica, Shelton, Holly, Dietrich, Isabelle, Graham, Stephen C., Bailey, Dalan
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Public Library of Science 21.12.2020
Public Library of Science (PLoS)
Predmet:
ISSN:1545-7885, 1544-9173, 1545-7885
On-line prístup:Získať plný text
Tagy: Pridať tag
Žiadne tagy, Buďte prvý, kto otaguje tento záznam!
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.
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
BookMark eNqVk11v0zAUhiM0xD7gHyCIxA1cpPgjiW0ukKpqwKSKSevYreXYJ61LEgc7RfDvcdd0WqcJgXLhyH7e18evfU6To851kCQvMZpgyvD7tdv4TjWTvrJuQhHCCJdPkhNc5EXGOC-O7v0fJ6chrBEiRBD-LDmmlOYsp_lJMr9eQbqYXi2ymbvJSLro7XdIe-8GsF26UiFVaeWdMungXW9Dm9bOp61qW9VY1aXT2TnZ4-F58rRWTYAX43iWfPt0fj37ks0vP1_MpvNMl6IYssJg4KJSORGlgLqo8hoQcAOlZgQIplQbSirEdWlIaVDNS8YoL4khvMBM0bPk9c63b1yQYxBBkpwJTEXBeSQudoRxai17b1vlf0unrLydcH4plR-sbkDWvCKsKnNmlM6RIKKqKwJFSQjORU0gen0cd9tULRgN3eBVc2B6uNLZlVy6n5KxAsdaosHb0cC7HxsIg2xt0NA0qgO3ua2bYBzDYBF98wB9_HQjtVTxALarXdxXb03ltCwQj4WLrdfkESp-Blqr42OqbZw_ELw7EERmgF_DUm1CkBeLq_9gv_47e3lzyL66H_ZdyvsXG4F8B2jvQvBQ3yEYyW1j7BOT28aQY2NE2YcHMm0HNVi3vTLb_F38BwiCEH8
CitedBy_id crossref_primary_10_1038_s41392_022_01039_2
crossref_primary_10_1099_jgv_0_001859
crossref_primary_10_1016_j_cell_2021_06_008
crossref_primary_10_1016_j_micinf_2021_104843
crossref_primary_10_1016_j_cell_2021_08_017
crossref_primary_10_1099_jgv_0_001735
crossref_primary_10_1128_AAC_00772_21
crossref_primary_10_1016_j_ijbiomac_2022_11_311
crossref_primary_10_1099_jgv_0_001584
crossref_primary_10_1177_11786302221107786
crossref_primary_10_3389_fphar_2022_842512
crossref_primary_10_1016_j_chphi_2023_100443
crossref_primary_10_1016_j_cell_2021_01_037
crossref_primary_10_1093_molbev_msac156
crossref_primary_10_1134_S1062359021150103
crossref_primary_10_1128_CMR_00299_20
crossref_primary_10_3389_fimmu_2022_978619
crossref_primary_10_1002_jmv_70049
crossref_primary_10_1016_j_nmni_2021_100889
crossref_primary_10_1038_s41467_021_26809_4
crossref_primary_10_1038_s42003_022_03325_9
crossref_primary_10_1038_s41598_025_95644_0
crossref_primary_10_1172_JCI183161
crossref_primary_10_1128_jvi_00256_22
crossref_primary_10_1038_s41598_022_23339_x
crossref_primary_10_1128_spectrum_03244_24
crossref_primary_10_1186_s13102_024_00817_5
crossref_primary_10_1038_s41467_024_53029_3
crossref_primary_10_1016_j_jiph_2023_09_004
crossref_primary_10_1111_tbed_14232
crossref_primary_10_1016_j_str_2022_09_003
crossref_primary_10_1590_1519_6984_264946
crossref_primary_10_36233_0372_9311_628
crossref_primary_10_1128_jvi_00608_22
crossref_primary_10_1088_1742_6596_2868_1_012029
crossref_primary_10_3389_fmicb_2023_1228128
crossref_primary_10_1016_j_virol_2021_10_005
crossref_primary_10_1099_jgv_0_001799
crossref_primary_10_1038_s41579_022_00841_7
crossref_primary_10_1080_22221751_2021_1898291
crossref_primary_10_1016_j_idc_2022_01_004
crossref_primary_10_1038_s41380_022_01831_0
crossref_primary_10_1002_cti2_1350
crossref_primary_10_1111_irv_12892
crossref_primary_10_1099_jgv_0_002092
crossref_primary_10_1093_ve_veaf059
crossref_primary_10_3748_wjg_v29_i3_425
crossref_primary_10_1073_pnas_2317026121
crossref_primary_10_1016_j_tice_2024_102711
crossref_primary_10_1007_s00705_025_06339_w
crossref_primary_10_1099_jgv_0_002022
crossref_primary_10_1111_jvp_13429
crossref_primary_10_1128_Spectrum_01199_21
crossref_primary_10_1016_j_celrep_2021_109292
crossref_primary_10_1371_journal_ppat_1012044
crossref_primary_10_1038_s41392_022_00907_1
crossref_primary_10_1016_j_aca_2022_339777
crossref_primary_10_1093_jimmun_vkae006
crossref_primary_10_1017_ash_2021_222
crossref_primary_10_1128_jvi_00455_22
crossref_primary_10_1007_s10311_021_01211_0
crossref_primary_10_1002_hsr2_1052
crossref_primary_10_1016_j_coviro_2023_101365
crossref_primary_10_1038_s41467_023_38717_w
crossref_primary_10_1007_s10072_021_05505_7
crossref_primary_10_1016_j_smhs_2023_03_004
crossref_primary_10_3389_fmicb_2021_725074
crossref_primary_10_3389_fmicb_2022_840757
crossref_primary_10_3389_fendo_2022_799521
crossref_primary_10_1016_j_virol_2022_01_014
crossref_primary_10_1038_s44161_022_00177_8
crossref_primary_10_3389_fgene_2021_571707
crossref_primary_10_1042_BCJ20200908
crossref_primary_10_1016_j_jbc_2021_101175
crossref_primary_10_1016_j_tim_2022_07_004
crossref_primary_10_1128_spectrum_01789_21
crossref_primary_10_1186_s42522_021_00039_6
crossref_primary_10_1111_tbed_14557
crossref_primary_10_1038_s41586_022_04532_4
crossref_primary_10_1016_j_sbi_2023_102619
crossref_primary_10_1007_s11030_022_10552_z
crossref_primary_10_1155_2023_3324790
crossref_primary_10_1016_j_heliyon_2023_e19345
crossref_primary_10_1111_sji_13275
crossref_primary_10_25122_jml_2024_0166
crossref_primary_10_1038_s41579_021_00652_2
crossref_primary_10_1016_j_vaccine_2022_03_064
crossref_primary_10_1016_j_vas_2023_100303
crossref_primary_10_14348_molcells_2021_0026
crossref_primary_10_1016_j_jenvman_2021_112277
crossref_primary_10_1089_ars_2021_0017
crossref_primary_10_3389_fmicb_2023_1199561
crossref_primary_10_3389_fmicb_2022_933983
crossref_primary_10_1080_14760584_2023_2211153
crossref_primary_10_1371_journal_ppat_1011206
crossref_primary_10_1007_s00018_021_04096_y
crossref_primary_10_1007_s00705_021_05166_z
crossref_primary_10_1371_journal_ppat_1012653
crossref_primary_10_1128_msphere_00558_22
crossref_primary_10_15212_ZOONOSES_2024_0028
crossref_primary_10_3389_fmicb_2023_1073789
crossref_primary_10_1126_science_abh0117
crossref_primary_10_1073_pnas_2121644119
crossref_primary_10_1007_s11684_024_1066_6
crossref_primary_10_1038_s41598_023_50952_1
crossref_primary_10_1016_j_cell_2021_05_031
crossref_primary_10_1038_s41467_022_31276_6
Cites_doi 10.1038/s41423-020-0400-4
10.1093/protein/gzs051
10.1107/S0907444910007493
10.1093/bioinformatics/btu739
10.1038/s41586-020-2180-5
10.1128/JVI.01248-18
10.1126/science.abb7015
10.1038/s41564-020-0688-y
10.1371/journal.ppat.0030005
10.1128/JVI.00442-08
10.1101/gr.849004
10.1016/j.cell.2020.02.052
10.1126/science.1116480
10.1093/nar/gkw408
10.1371/journal.ppat.1008815
10.1093/nar/25.17.3389
10.1056/NEJMoa1401505
10.1038/s41586-020-2324-7
10.2807/1560-7917.ES.2020.25.23.2001005
10.1038/s41586-020-2012-7
10.1126/science.1118391
10.1128/JVI.00737-08
10.1128/JVI.00940-20
10.1038/s41586-020-2179-y
10.1038/s41467-020-15562-9
10.1073/pnas.2002589117
10.1128/JVI.02792-12
10.1126/science.abb2762
10.1016/j.cell.2020.03.045
10.1016/j.chom.2020.03.023
10.1128/JVI.02615-14
10.1016/S2666-5247(20)30089-6
10.1093/molbev/msw054
10.1128/JVI.01085-07
10.1093/nar/gkf436
10.1016/j.virol.2009.09.023
10.1074/jbc.M111.325803
10.1128/JVI.78.20.11429-11433.2004
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
DBID AAYXX
CITATION
CGR
CUY
CVF
ECM
EIF
NPM
IOV
ISN
ISR
3V.
7QG
7QL
7SN
7SS
7T5
7TK
7TM
7X7
7XB
88E
8FD
8FE
8FH
8FI
8FJ
8FK
ABUWG
AEUYN
AFKRA
ATCPS
AZQEC
BBNVY
BENPR
BHPHI
C1K
CCPQU
DWQXO
FR3
FYUFA
GHDGH
GNUQQ
H94
HCIFZ
K9.
LK8
M0S
M1P
M7N
M7P
P64
PATMY
PHGZM
PHGZT
PIMPY
PJZUB
PKEHL
PPXIY
PQEST
PQGLB
PQQKQ
PQUKI
PYCSY
RC3
7X8
5PM
DOA
CZG
DOI 10.1371/journal.pbio.3001016
DatabaseName CrossRef
Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
Gale In Context: Opposing Viewpoints
Gale In Context: Canada
Gale In Context: Science
ProQuest Central (Corporate)
Animal Behavior Abstracts
Bacteriology Abstracts (Microbiology B)
Ecology Abstracts
Entomology Abstracts (Full archive)
Immunology Abstracts
Neurosciences Abstracts
Nucleic Acids Abstracts
Health & Medical Collection
ProQuest Central (purchase pre-March 2016)
Medical Database (Alumni Edition)
Technology Research Database
ProQuest SciTech Collection
ProQuest Natural Science Collection
Hospital Premium Collection
Hospital Premium Collection (Alumni Edition)
ProQuest Central (Alumni) (purchase pre-March 2016)
ProQuest Central (Alumni)
ProQuest One Sustainability
ProQuest Central UK/Ireland
Agricultural & Environmental Science Collection
ProQuest Central Essentials
Biological Science Collection (subscription)
ProQuest Central - New (Subscription)
Natural Science Collection
Environmental Sciences and Pollution Management
ProQuest One Community College
ProQuest Central
Engineering Research Database
Health Research Premium Collection
Health Research Premium Collection (Alumni)
ProQuest Central Student
AIDS and Cancer Research Abstracts
SciTech Premium Collection
ProQuest Health & Medical Complete (Alumni)
Biological Sciences
Health & Medical Collection (Alumni Edition)
PML(ProQuest Medical Library)
Algology Mycology and Protozoology Abstracts (Microbiology C)
Biological Science Database
Biotechnology and BioEngineering Abstracts
Environmental Science Database (subscripiton)
ProQuest Central Premium
ProQuest One Academic
Publicly Available Content Database (subscription)
ProQuest Health & Medical Research Collection
ProQuest One Academic Middle East (New)
ProQuest One Health & Nursing
ProQuest One Academic Eastern Edition (DO NOT USE)
ProQuest One Applied & Life Sciences
ProQuest One Academic (retired)
ProQuest One Academic UKI Edition
Environmental Science Collection
Genetics Abstracts
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
PLoS Biology
DatabaseTitle CrossRef
MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
Publicly Available Content Database
ProQuest Central Student
ProQuest Central Essentials
Nucleic Acids Abstracts
SciTech Premium Collection
Environmental Sciences and Pollution Management
ProQuest One Applied & Life Sciences
ProQuest One Sustainability
Health Research Premium Collection
Natural Science Collection
Health & Medical Research Collection
Biological Science Collection
ProQuest Central (New)
ProQuest Medical Library (Alumni)
ProQuest Biological Science Collection
ProQuest One Academic Eastern Edition
ProQuest Hospital Collection
Health Research Premium Collection (Alumni)
Biological Science Database
Ecology Abstracts
Neurosciences Abstracts
ProQuest Hospital Collection (Alumni)
Biotechnology and BioEngineering Abstracts
Environmental Science Collection
Entomology Abstracts
ProQuest Health & Medical Complete
ProQuest One Academic UKI Edition
Environmental Science Database
Engineering Research Database
ProQuest One Academic
ProQuest One Academic (New)
Technology Research Database
ProQuest One Academic Middle East (New)
ProQuest Health & Medical Complete (Alumni)
ProQuest Central (Alumni Edition)
ProQuest One Community College
ProQuest One Health & Nursing
ProQuest Natural Science Collection
ProQuest Central
ProQuest Health & Medical Research Collection
Genetics Abstracts
Health and Medicine Complete (Alumni Edition)
ProQuest Central Korea
Bacteriology Abstracts (Microbiology B)
Algology Mycology and Protozoology Abstracts (Microbiology C)
Agricultural & Environmental Science Collection
AIDS and Cancer Research Abstracts
ProQuest SciTech Collection
ProQuest Medical Library
Animal Behavior Abstracts
Immunology Abstracts
ProQuest Central (Alumni)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic


CrossRef

MEDLINE
Publicly Available Content Database

Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 3
  dbid: PIMPY
  name: Publicly Available Content Database (subscription)
  url: http://search.proquest.com/publiccontent
  sourceTypes: Aggregation Database
DeliveryMethod fulltext_linktorsrc
Discipline Biology
DocumentTitleAlternate SARS-CoV-2 host range
EISSN 1545-7885
ExternalDocumentID 2479139588
oai_doaj_org_article_f8b27b647dac40929bfb2e5622149f2e
PMC7751883
A650814997
33347434
10_1371_journal_pbio_3001016
Genre Research Support, Non-U.S. Gov't
Journal Article
Comparative Study
GeographicLocations United Kingdom
United States--US
China
GeographicLocations_xml – name: United Kingdom
– name: China
– name: United States--US
GrantInformation_xml – fundername: Medical Research Council
  grantid: MR/P021735/1
– fundername: Wellcome Trust
– fundername: Wellcome Trust
  grantid: 098406/Z/12/B
– fundername: Biotechnology and Biological Sciences Research Council
  grantid: BBS/E/I/00007039
– fundername: Biotechnology and Biological Sciences Research Council
  grantid: BBS/E/I/00007038
– fundername: Biotechnology and Biological Sciences Research Council
  grantid: BBS/E/I/00007034
– fundername: Biotechnology and Biological Sciences Research Council
  grantid: BBS/E/I/COV07001
– fundername: Biotechnology and Biological Sciences Research Council
  grantid: BBS/E/I/00007037
– fundername: ;
  grantid: BBS/E/I/00007034
– fundername: ;
  grantid: BB/R019843/1
– fundername: ;
  grantid: BBS/E/I/00007030
– fundername: ;
  grantid: MR/P021735/1
– fundername: ;
  grantid: BBS/E/I/00007039
– fundername: ;
  grantid: 971555
– fundername: ;
  grantid: 098406/Z/12/B
GroupedDBID ---
123
29O
2WC
36B
53G
5VS
7X7
7XC
88E
8FE
8FH
8FI
8FJ
AAFWJ
AAUCC
AAWOE
AAYXX
ABDBF
ABIVO
ABUFD
ABUWG
ACCTH
ACGFO
ACIHN
ACPRK
ACUHS
ADBBV
AEAQA
AENEX
AEUYN
AFFHD
AFKRA
AFPKN
AFRAH
AFXKF
AHMBA
AKRSQ
ALMA_UNASSIGNED_HOLDINGS
AOIJS
ATCPS
B0M
BAIFH
BAWUL
BBNVY
BBTPI
BCNDV
BENPR
BHPHI
BPHCQ
BVXVI
BWKFM
CCPQU
CITATION
CS3
DIK
DU5
E3Z
EAD
EAP
EAS
EBD
EBS
EJD
EMB
EMK
EMOBN
EPL
ESX
F5P
FPL
FYUFA
GROUPED_DOAJ
GX1
HCIFZ
HMCUK
HYE
IAG
IAO
IGS
IHR
IOV
ISE
ISN
ISR
ITC
KQ8
LK8
M1P
M48
M7P
O5R
O5S
OK1
OVT
P2P
PATMY
PHGZM
PHGZT
PIMPY
PJZUB
PPXIY
PQGLB
PQQKQ
PROAC
PSQYO
PV9
PYCSY
QF4
QN7
RNS
RPM
RZL
SJN
SV3
TR2
TUS
UKHRP
WOW
XSB
YZZ
~8M
.GJ
ADRAZ
ADXHL
ALIPV
C1A
CGR
CUY
CVF
ECM
EIF
IPNFZ
NPM
RIG
WOQ
3V.
7QG
7QL
7SN
7SS
7T5
7TK
7TM
7XB
8FD
8FK
AZQEC
C1K
DWQXO
FR3
GNUQQ
H94
K9.
M7N
P64
PKEHL
PQEST
PQUKI
RC3
7X8
5PM
-
AAPBV
ABFLS
ABPTK
ADACO
AGJBV
BBAFP
CZG
M~E
PRINS
ZA5
ID FETCH-LOGICAL-c695t-5d1e89ba42969ef5b4fe0e8de6c72e2133cd32b08c6d26d0f86773862d28517a3
IEDL.DBID DOA
ISICitedReferencesCount 155
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000601328800004&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1545-7885
1544-9173
IngestDate Fri Nov 26 17:12:51 EST 2021
Tue Oct 14 18:42:16 EDT 2025
Tue Nov 04 02:01:11 EST 2025
Sun Nov 09 11:08:59 EST 2025
Sat Nov 29 14:32:13 EST 2025
Tue Nov 11 10:54:14 EST 2025
Tue Nov 04 18:14:01 EST 2025
Thu Nov 13 16:12:31 EST 2025
Thu Nov 13 16:11:54 EST 2025
Thu Nov 13 16:12:36 EST 2025
Mon Jul 21 05:35:04 EDT 2025
Tue Nov 18 20:05:49 EST 2025
Sat Nov 29 06:28:47 EST 2025
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 12
Language English
License This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Creative Commons Attribution License
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c695t-5d1e89ba42969ef5b4fe0e8de6c72e2133cd32b08c6d26d0f86773862d28517a3
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 14
ObjectType-Article-2
ObjectType-Feature-1
content type line 23
The authors have declared that no competing interests exist.
ORCID 0000-0003-4547-4034
0000-0002-7437-1723
0000-0002-8307-507X
0000-0002-1395-1775
0000-0002-6509-3354
0000-0002-5640-2266
0000-0003-1869-6176
0000-0002-6300-109X
0000-0002-4450-5911
0000-0002-4100-9269
0000-0002-4012-1283
0000-0003-4735-2065
0000-0002-2213-3248
0000-0003-0120-7196
OpenAccessLink https://doaj.org/article/f8b27b647dac40929bfb2e5622149f2e
PMID 33347434
PQID 2479139588
PQPubID 1436341
ParticipantIDs plos_journals_2479139588
doaj_primary_oai_doaj_org_article_f8b27b647dac40929bfb2e5622149f2e
pubmedcentral_primary_oai_pubmedcentral_nih_gov_7751883
proquest_miscellaneous_2472112967
proquest_journals_2479139588
gale_infotracmisc_A650814997
gale_infotracacademiconefile_A650814997
gale_incontextgauss_ISR_A650814997
gale_incontextgauss_ISN_A650814997
gale_incontextgauss_IOV_A650814997
pubmed_primary_33347434
crossref_primary_10_1371_journal_pbio_3001016
crossref_citationtrail_10_1371_journal_pbio_3001016
PublicationCentury 2000
PublicationDate 2020-12-21
PublicationDateYYYYMMDD 2020-12-21
PublicationDate_xml – month: 12
  year: 2020
  text: 2020-12-21
  day: 21
PublicationDecade 2020
PublicationPlace United States
PublicationPlace_xml – name: United States
– name: San Francisco
– name: San Francisco, CA USA
PublicationTitle PLoS biology
PublicationTitleAlternate PLoS Biol
PublicationYear 2020
Publisher Public Library of Science
Public Library of Science (PLoS)
Publisher_xml – name: Public Library of Science
– name: Public Library of Science (PLoS)
References J Shi (pbio.3001016.ref022) 2020; 368
Q. Wang (pbio.3001016.ref006) 2020; 181
M Letko (pbio.3001016.ref009) 2020; 5
C Woolsey (pbio.3001016.ref037) 2020
M. Hoffmann (pbio.3001016.ref008) 2020; 181
H Ashkenazy (pbio.3001016.ref050) 2016; 44
IG Barr (pbio.3001016.ref039) 2020; 25
EI Azhar (pbio.3001016.ref003) 2014; 370
AG Wrobel (pbio.3001016.ref012) 2020
A Roberts (pbio.3001016.ref025) 2007; 3
X Ou (pbio.3001016.ref038) 2020; 11
K Wu (pbio.3001016.ref013) 2012; 287
P Zhou (pbio.3001016.ref001) 2020; 579
SF Sia (pbio.3001016.ref027) 2020
B.D. Griffin (pbio.3001016.ref028) 2020
J Birch (pbio.3001016.ref043) 2013; 87
R Yan (pbio.3001016.ref011) 2020; 367
Y.I. Kim (pbio.3001016.ref021) 2020; 27
Y. Liu (pbio.3001016.ref032) 2020
Y Qiu (pbio.3001016.ref014) 2020
K Katoh (pbio.3001016.ref049) 2002; 30
J Lan (pbio.3001016.ref010) 2020; 581
N Saitou (pbio.3001016.ref051) 1987; 4
J Netland (pbio.3001016.ref023) 2008; 82
F Li (pbio.3001016.ref019) 2005; 309
W Li (pbio.3001016.ref002) 2005; 310
Y Qiao (pbio.3001016.ref018) 2020; 16
Y Li (pbio.3001016.ref031) 2020
BE Suzek (pbio.3001016.ref048) 2015; 31
Sit THC (pbio.3001016.ref040) 2020
N Abdullah (pbio.3001016.ref015) 2018; 92
F Li (pbio.3001016.ref020) 2008; 82
J Shang (pbio.3001016.ref005) 2020; 581
CW Day (pbio.3001016.ref024) 2009; 395
W Tai (pbio.3001016.ref029) 2020; 17
H Ishikawa (pbio.3001016.ref045) 2012; 25
S. Lu (pbio.3001016.ref035) 2020
A.T. Huang (pbio.3001016.ref004) 2020
X Zhao (pbio.3001016.ref033) 2020; 94
F Li (pbio.3001016.ref007) 2015; 89
N Thakur (pbio.3001016.ref044) 2020
K Schlottau (pbio.3001016.ref034); 1
N Oreshkova (pbio.3001016.ref042) 2020; 25
P Emsley (pbio.3001016.ref046) 2010; 66
S Kumar (pbio.3001016.ref052) 2016; 33
Q. Zhang (pbio.3001016.ref041) 2020
VJ Munster (pbio.3001016.ref036) 2020; 585
GE Crooks (pbio.3001016.ref053) 2004; 14
S Matsuyama (pbio.3001016.ref017) 2020; 117
W Li (pbio.3001016.ref016) 2004; 78
KH 3rd Dinnon (pbio.3001016.ref026) 2020
SF Altschul (pbio.3001016.ref047) 1997; 25
W Ren (pbio.3001016.ref030) 2008; 82
References_xml – volume: 17
  start-page: 613
  issue: 6
  year: 2020
  ident: pbio.3001016.ref029
  article-title: Characterization of the receptor-binding domain (RBD) of 2019 novel coronavirus: implication for development of RBD protein as a viral attachment inhibitor and vaccine
  publication-title: Cell Mol Immunol
  doi: 10.1038/s41423-020-0400-4
– volume: 25
  start-page: 813
  issue: 12
  year: 2012
  ident: pbio.3001016.ref045
  article-title: Generation of a dual-functional split-reporter protein for monitoring membrane fusion using self-associating split GFP
  publication-title: Protein Eng Des Sel
  doi: 10.1093/protein/gzs051
– volume: 66
  start-page: 486
  issue: Pt 4
  year: 2010
  ident: pbio.3001016.ref046
  article-title: Features and development of Coot
  publication-title: Acta Crystallogr D Biol Crystallogr
  doi: 10.1107/S0907444910007493
– volume: 31
  start-page: 926
  issue: 6
  year: 2015
  ident: pbio.3001016.ref048
  article-title: UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btu739
– volume: 581
  start-page: 215
  issue: 7807
  year: 2020
  ident: pbio.3001016.ref010
  article-title: Structure of the SARS-CoV-2 spike receptor-binding domain bound to the ACE2 receptor
  publication-title: Nature
  doi: 10.1038/s41586-020-2180-5
– year: 2020
  ident: pbio.3001016.ref037
  article-title: Establishment of an African green monkey model for COVID-19
  publication-title: bioRxiv
– volume: 25
  issue: 25
  year: 2020
  ident: pbio.3001016.ref039
  article-title: SARS-CoV-2 does not replicate in embryonated hen's eggs or in MDCK cell lines
  publication-title: Euro Surveill
– volume: 92
  issue: 23
  year: 2018
  ident: pbio.3001016.ref015
  article-title: Structure-Guided Identification of a Nonhuman Morbillivirus with Zoonotic Potential
  publication-title: J Virol
  doi: 10.1128/JVI.01248-18
– year: 2020
  ident: pbio.3001016.ref028
  article-title: North American deer mice are susceptible to SARS-CoV-2
  publication-title: bioRxiv
– volume: 368
  start-page: 1016
  issue: 6494
  year: 2020
  ident: pbio.3001016.ref022
  article-title: Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2
  publication-title: Science
  doi: 10.1126/science.abb7015
– volume: 5
  start-page: 562
  issue: 4
  year: 2020
  ident: pbio.3001016.ref009
  article-title: Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses
  publication-title: Nat Microbiol
  doi: 10.1038/s41564-020-0688-y
– volume: 3
  start-page: e5
  issue: 1
  year: 2007
  ident: pbio.3001016.ref025
  article-title: A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice
  publication-title: PLoS Pathog
  doi: 10.1371/journal.ppat.0030005
– volume: 4
  start-page: 406
  issue: 4
  year: 1987
  ident: pbio.3001016.ref051
  article-title: The neighbor-joining method: a new method for reconstructing phylogenetic trees
  publication-title: Mol Biol Evol
– volume: 82
  start-page: 6984
  issue: 14
  year: 2008
  ident: pbio.3001016.ref020
  article-title: Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections
  publication-title: J Virol
  doi: 10.1128/JVI.00442-08
– volume: 14
  start-page: 1188
  issue: 6
  year: 2004
  ident: pbio.3001016.ref053
  article-title: WebLogo: a sequence logo generator
  publication-title: Genome Res
  doi: 10.1101/gr.849004
– volume: 181
  start-page: 271
  issue: 2
  year: 2020
  ident: pbio.3001016.ref008
  article-title: SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor
  publication-title: Cell
  doi: 10.1016/j.cell.2020.02.052
– volume: 309
  start-page: 1864
  issue: 5742
  year: 2005
  ident: pbio.3001016.ref019
  article-title: Structure of SARS coronavirus spike receptor-binding domain complexed with receptor
  publication-title: Science
  doi: 10.1126/science.1116480
– year: 2020
  ident: pbio.3001016.ref031
  article-title: SARS-CoV-2 and three related coronaviruses utilize multiple ACE2 orthologs and are potently blocked by an improved ACE2-Ig
  publication-title: J Virol
– volume: 44
  start-page: W344
  issue: W1
  year: 2016
  ident: pbio.3001016.ref050
  article-title: ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkw408
– year: 2020
  ident: pbio.3001016.ref004
  article-title: A systematic review of antibody mediated immunity to coronaviruses: antibody kinetics, correlates of protection, and association of antibody responses with severity of disease
  publication-title: medRxiv
– year: 2020
  ident: pbio.3001016.ref032
  article-title: Functional and Genetic Analysis of Viral Receptor ACE2 Orthologs Reveals a Broad Potential Host Range of SARS-CoV-2
  publication-title: bioRxiv
– year: 2020
  ident: pbio.3001016.ref026
  article-title: A mouse-adapted model of SARS-CoV-2 to test COVID-19 countermeasures
  publication-title: Nature
– year: 2020
  ident: pbio.3001016.ref035
  article-title: Comparison of SARS-CoV-2 infections among 3 species of non-human primates
  publication-title: bioRxiv
– volume: 16
  start-page: e1008815
  issue: 8
  year: 2020
  ident: pbio.3001016.ref018
  article-title: Global exploration of the metabolic requirements of gallid alphaherpesvirus 1
  publication-title: PLoS Pathog.
  doi: 10.1371/journal.ppat.1008815
– year: 2020
  ident: pbio.3001016.ref044
  article-title: Micro-fusion inhibition tests: quantifying antibody neutralization of virus-mediated cell-cell fusion
  publication-title: J Gen Virol
– year: 2020
  ident: pbio.3001016.ref040
  article-title: Ranawaka APM Perera, Leo LM Poon, and Malik Peiris, Canine SARS-CoV-2 infection
  publication-title: PREPRINT (Version 1) available at Research Square
– volume: 25
  start-page: 3389
  issue: 17
  year: 1997
  ident: pbio.3001016.ref047
  article-title: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/25.17.3389
– volume: 370
  start-page: 2499
  issue: 26
  year: 2014
  ident: pbio.3001016.ref003
  article-title: Evidence for camel-to-human transmission of MERS coronavirus
  publication-title: N Engl J Med
  doi: 10.1056/NEJMoa1401505
– volume: 585
  start-page: 268
  issue: 7824
  year: 2020
  ident: pbio.3001016.ref036
  article-title: Respiratory disease in rhesus macaques inoculated with SARS-CoV-2
  publication-title: Nature
  doi: 10.1038/s41586-020-2324-7
– volume: 25
  issue: 23
  year: 2020
  ident: pbio.3001016.ref042
  article-title: SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020
  publication-title: Euro Surveill
  doi: 10.2807/1560-7917.ES.2020.25.23.2001005
– volume: 579
  start-page: 270
  issue: 7798
  year: 2020
  ident: pbio.3001016.ref001
  article-title: A pneumonia outbreak associated with a new coronavirus of probable bat origin
  publication-title: Nature
  doi: 10.1038/s41586-020-2012-7
– volume: 310
  start-page: 676
  issue: 5748
  year: 2005
  ident: pbio.3001016.ref002
  article-title: Bats are natural reservoirs of SARS-like coronaviruses
  publication-title: Science
  doi: 10.1126/science.1118391
– volume: 82
  start-page: 7264
  issue: 15
  year: 2008
  ident: pbio.3001016.ref023
  article-title: Severe acute respiratory syndrome coronavirus infection causes neuronal death in the absence of encephalitis in mice transgenic for human ACE2
  publication-title: J Virol
  doi: 10.1128/JVI.00737-08
– volume: 94
  issue: 18
  year: 2020
  ident: pbio.3001016.ref033
  article-title: Broad and Differential Animal Angiotensin-Converting Enzyme 2 Receptor Usage by SARS-CoV-2
  publication-title: J Virol
  doi: 10.1128/JVI.00940-20
– volume: 581
  start-page: 221
  issue: 7807
  year: 2020
  ident: pbio.3001016.ref005
  article-title: Structural basis of receptor recognition by SARS-CoV-2
  publication-title: Nature
  doi: 10.1038/s41586-020-2179-y
– volume: 11
  start-page: 1620
  issue: 1
  year: 2020
  ident: pbio.3001016.ref038
  article-title: Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV
  publication-title: Nat Commun.
  doi: 10.1038/s41467-020-15562-9
– volume: 117
  start-page: 7001
  issue: 13
  year: 2020
  ident: pbio.3001016.ref017
  article-title: Enhanced isolation of SARS-CoV-2 by TMPRSS2-expressing cells
  publication-title: Proc Natl Acad Sci U S A
  doi: 10.1073/pnas.2002589117
– volume: 87
  start-page: 4756
  issue: 8
  year: 2013
  ident: pbio.3001016.ref043
  article-title: Characterization of ovine Nectin-4, a novel peste des petits ruminants virus receptor
  publication-title: J Virol
  doi: 10.1128/JVI.02792-12
– volume: 367
  start-page: 1444
  issue: 6485
  year: 2020
  ident: pbio.3001016.ref011
  article-title: Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2
  publication-title: Science
  doi: 10.1126/science.abb2762
– volume: 181
  start-page: 894
  issue: 4
  year: 2020
  ident: pbio.3001016.ref006
  article-title: Structural and Functional Basis of SARS-CoV-2 Entry by Using Human ACE2
  publication-title: Cell
  doi: 10.1016/j.cell.2020.03.045
– volume: 27
  start-page: 704
  issue: 5
  year: 2020
  ident: pbio.3001016.ref021
  article-title: Infection and Rapid Transmission of SARS-CoV-2 in Ferrets
  publication-title: Cell Host Microbe
  doi: 10.1016/j.chom.2020.03.023
– year: 2020
  ident: pbio.3001016.ref027
  article-title: Pathogenesis and transmission of SARS-CoV-2 in golden hamsters
  publication-title: Nature
– volume: 89
  start-page: 1954
  issue: 4
  year: 2015
  ident: pbio.3001016.ref007
  article-title: Receptor recognition mechanisms of coronaviruses: a decade of structural studies
  publication-title: J Virol
  doi: 10.1128/JVI.02615-14
– year: 2020
  ident: pbio.3001016.ref012
  article-title: SARS-CoV-2 and bat RaTG13 spike glycoprotein structures inform on virus evolution and furin-cleavage effects
  publication-title: Nat Struct Mol Biol
– volume: 1
  start-page: e218
  issue: 5
  ident: pbio.3001016.ref034
  article-title: SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study
  publication-title: Lancet Microbe. 2020
  doi: 10.1016/S2666-5247(20)30089-6
– volume: 33
  start-page: 1870
  issue: 7
  year: 2016
  ident: pbio.3001016.ref052
  article-title: MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
  publication-title: Mol Biol Evol
  doi: 10.1093/molbev/msw054
– year: 2020
  ident: pbio.3001016.ref041
  article-title: SARS-CoV-2 neutralizing serum antibodies in cats: a serological investigation
  publication-title: bioRxiv
– volume: 82
  start-page: 1899
  issue: 4
  year: 2008
  ident: pbio.3001016.ref030
  article-title: Difference in receptor usage between severe acute respiratory syndrome (SARS) coronavirus and SARS-like coronavirus of bat origin
  publication-title: J Virol
  doi: 10.1128/JVI.01085-07
– volume: 30
  start-page: 3059
  issue: 14
  year: 2002
  ident: pbio.3001016.ref049
  article-title: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
  publication-title: Nucleic Acids Res
  doi: 10.1093/nar/gkf436
– volume: 395
  start-page: 210
  issue: 2
  year: 2009
  ident: pbio.3001016.ref024
  article-title: A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo
  publication-title: Virology
  doi: 10.1016/j.virol.2009.09.023
– volume: 287
  start-page: 8904
  issue: 12
  year: 2012
  ident: pbio.3001016.ref013
  article-title: Mechanisms of host receptor adaptation by severe acute respiratory syndrome coronavirus
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M111.325803
– year: 2020
  ident: pbio.3001016.ref014
  article-title: Predicting the angiotensin converting enzyme 2 (ACE2) utilizing capability as the receptor of SARS-CoV-2
  publication-title: Microbes Infect
– volume: 78
  start-page: 11429
  issue: 20
  year: 2004
  ident: pbio.3001016.ref016
  article-title: Efficient replication of severe acute respiratory syndrome coronavirus in mouse cells is limited by murine angiotensin-converting enzyme 2
  publication-title: J Virol
  doi: 10.1128/JVI.78.20.11429-11433.2004
SSID ssj0022928
Score 2.6597729
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,...
SourceID plos
doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e3001016
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
SummonAdditionalLinks – databaseName: ProQuest Central - New (Subscription)
  dbid: BENPR
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV3db9MwELegA4kXvscKAxmExFO2xk7j5Al1VSeQpjK1MO0tsmN7i1iTkLRI_PfcJW4gaHxIvMa_RMnd-XxnX35HyGvfKC0jbTxlITcJpGaehGXCYxKCZzG2QaQaTZ-I-Tw6P49P3YZb7coqtz6xcdS6SHGP_JAFAhksx1H0tvziYdcoPF11LTRukh1kKgsGZOdoNj9ddCkXi5vuqkg5A9NacPfzHBf-odPVQamy4oC3XGu9xanh8O889aC8KurrwtBfqyl_Wp6O7_3vh90nd11gSietJT0gN0z-kNxuW1V-e0ROwJ7ocrJYetPizGN0WWafDW1YHrKcXsqaSqqqQmq6rooyq1cUomG6kqtVs5FCJ9MZ28Lrx-TT8ezj9J3nOjF4aRiP195Y-yaKlYTFK4yNHavAmpEBFYepYIZBnptqztQoSkPNQj2yyJLHIVnSDCI6IfkuGeRFbvYIFViIE9hYY9tr38aRlWAgQivIVCVnZkj4VgVJ6mjKsVvGVdKcvQlIV1qBJKi4xCluSLzurrKl6fgL_gi122GRZLu5UFQXiZuziY0UEyoMhJYppMEsVlYxAwEjg7TS4qu-QttIkEYjxzqdC7mp6-T9h7NkgoEvoGLxO9By_i-gRQ_0xoFsARJJpfuBAuSKHF495H4PCR4j7Q3voTFvBVMnP0wQ7twa6fXDL7thfCgW6OWm2DQYhqF7CE9_0s6HTric8wAC1WBIRG-m9KTfH8mzy4bqXOCpYMSf_vm1npE7DLdBfPAx_j4ZrKuNeU5upV_XWV29cD7hO97-aCk
  priority: 102
  providerName: ProQuest
– databaseName: Public Library of Science (PLoS) Journals Open Access
  dbid: FPL
  link: http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV3fb9MwELaggMQLv2GFgQxC4imjsdPYeSzVKpCqMq0w7c2yY5tFrEnUtEj899wlaSDTKuA1_hxZ353tu_jymZC3oTNWS-sC4yE3ibRlgYZtImAagmcx9pE0taXnYrGQ5-fJye9E8coJPhfh-5bTo9JkxRFvNNFukluMxzGWcM1O5l2CxRIm29_j9vXsbT-1Sn-3Fg_Ky6K6LtC8Wi_5xwY0u_-_Q39A7rWhJp00vvGQ3HD5I3KnuXzy52MyBw-hy8npMpgWZwGjyzL77mit25Dl9EJXVFOzLrSlm3VRZtWKQnxLV3q1qj-N0Mn0mO3g1RPydXb8ZfoxaO9WCNI4GW-CsQ2dTIyG7ShOnB-byLuRA6PFqWCOQeaaWs7MSKaxZbEdedS945D-WAYxmtD8KRnkRe4OCBVYWhP5xOJF1qFPpNdgcmEN5J6aMzckfEe5Slvhcbz_4lLVp2kCEpCGEIU8qZanIQm6XmUjvPEX_Ae0ZodF2ez6ARhEtbNQeWmYMHEkrE4hsWWJ8YY5CAEZJIoeh_oGfUGhMEaOlTff9Laq1KfPZ2qCoSygErEPtFz8C-i0B3rXgnwBjKS6_SUCeEVVrh7ysIeENSDtNR-g8-6IqRSLBOq9jqWEnjuHvr75ddeML8WSu9wV2xrDMBiP4e3PGv_vyOWcRxB6RkMiejOjx36_Jc8uavFyged8kj_fP-IX5C7DjxohrBjhIRls1lv3ktxOf2yyav2qnvG_ABJbUwY
  priority: 102
  providerName: Public Library of Science
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
WOSCitedRecordID wos000601328800004&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
journalDatabaseRights – providerCode: PRVAON
  databaseName: DOAJ Directory of Open Access Journals
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: DOA
  dateStart: 20030101
  isFulltext: true
  titleUrlDefault: https://www.doaj.org/
  providerName: Directory of Open Access Journals
– providerCode: PRVPQU
  databaseName: Biological Science Database
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: M7P
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/biologicalscijournals
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Environmental Science Database (subscripiton)
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: PATMY
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/environmentalscience
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Health & Medical Collection
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: 7X7
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: https://search.proquest.com/healthcomplete
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: ProQuest Central
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: BENPR
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: https://www.proquest.com/central
  providerName: ProQuest
– providerCode: PRVPQU
  databaseName: Publicly Available Content Database (subscription)
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: PIMPY
  dateStart: 20031001
  isFulltext: true
  titleUrlDefault: http://search.proquest.com/publiccontent
  providerName: ProQuest
– providerCode: PRVATS
  databaseName: Public Library of Science (PLoS) Journals Open Access
  customDbUrl:
  eissn: 1545-7885
  dateEnd: 99991231
  omitProxy: false
  ssIdentifier: ssj0022928
  issn: 1545-7885
  databaseCode: FPL
  dateStart: 20030101
  isFulltext: true
  titleUrlDefault: http://www.plos.org/publications/
  providerName: Public Library of Science
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1Nj9MwELWggMQF8b2FpTIIiVN2GzuNnWO3asVKpUQtrMopsmObjdgmVdMi8e-ZSdJqgxYtBy451C-R-mbimUkmbwh571ttlDTW0w5qk0AZ5ikIEx5TkDyLgQukriw9FbOZXC6j-NqoL-wJq-WBa-JOndRM6DAQRqVQi7BIO80sRG0Gub1jFndfyHr2xVRTarGomqqKUjNwOwvefDTHhX_a2OhkrbPihNcaa62gVGn3H3bozvqqKG9KP__sorwWliaPyaMmn6TD-n88IXds_pQ8qCdM_npGpuAGdDGcL7xRceExulhnPyytxBmynF6qkiqqN4UydLsp1lm5opDE0pVararnH3Q4GrM9vHxOvk7GX0YfvWaAgpeG0WDrDYxvZaQVxJwwsm6gA2f7FiwTpoJZBuVpajjTfZmGhoWm71DcjkONYxgkYkLxF6STF7k9IlRg_0zgIoPTqn0XSafArsJoKDAVZ7ZL-J7BJG3UxXHIxVVSvTITUGXUhCTIe9Lw3iXe4ax1ra5xC_4MjXPAojZ29QN4TNJ4THKbx3TJOzRtguoXObbXfFe7skzOP18kQ8xXARWJv4EWs38BzVugDw3IFcBIqprvHoBXlN5qIY9bSLjR09byEfrinpgyYYFAUdeBlHDm3j9vXn57WMaLYl9dbotdhWGYcYdw9Ze1Ox_I5ZwHkF8GXSJajt5iv72SZ5eVQrnAl3mSv_of5npNHjJ8xuHDBuIfk852s7NvyP305zYrNz1yVyxFdZQ9cu9sPIvnvWorgOMknvawlzeGlfj8U_ztN9oVX8w
linkProvider Directory of Open Access Journals
linkToHtml http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V3db9MwELdGAcEL37DCAINAPGVr7DROHhAqZdOmlYLWbepbsGN7i1iT0rSg_VP8jdzloyNofLzsgdf4bDnnu_Odff4dIS9co7QMtHGUhdjEk5o5ErYJh0lwnkXXeoEqVnoghsNgPA4_rpDv9VsYTKusbWJhqHUW4xn5BvMEIlh2g-DN9IuDVaPwdrUuoVGKxa45_QYhW_565x2s70vGtjb3-9tOVVXAif2wO3e62jVBqCQYYj80tqs8azoGpuvHghkGMVusOVOdIPY183XHIuIbB8dfM6xjLzmMe4lchu4CU8jE-CzAY2FRyxUBbsCICF491ePC3agkY32qkmydl8huja2wqBiw3Bda05MsP8_p_TV386fNcOvm_8bGW-RG5XbTXqknt8mKSe-Qq2UhztO7ZADaQke9vZHTzw4dRkfT5LOhBYZFktJjmVNJ1SyTms5n2TTJJxR8fTqRk0lxTER7_U1Wk-f3yMGF_Mp90kqz1KwSKjDNyLOhxqLerg0DK0H8hVYQh0vOTJvwesmjuAJhx1ogJ1FxsyggGCsZEqGgRJWgtImz7DUtQUj-Qv8WpWlJixDixYdsdhRVFimygWJC-Z7QMoYgn4XKKmbAHWYQNFuc6nOUxQhBQlLMQjqSizyPdj4cRj1064EqFL8jGg3_hWivQfSqIrIZcCSW1fMQ4CsilDUo1xqUYA_jRvMqKk_NmDw6E3noWSvF-c3Pls04KKYfpiZbFDQMAxMfRn9Q6t-SuZxzD9xwr01EQzMb3G-2pMlxAeQu8M4z4A__PK2n5Nr2_vtBNNgZ7j4i1xke-LhgTd010prPFuYxuRJ_nSf57ElhjSj5dNF6-wNftMMq
linkToPdf http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMw1V1Lb9NAEF6VFBAX3tBAgQWBOLlN1o7XPiCUpomIGoUooVVvZte721o0dogTUP8av44Zv8CoPC49cM1-Xm1mZ2bn28cMIS_bWirhKW1JA9zEEYpZApYJiwkInnnHOJ7MZnrEx2Pv-NifbJBv5VsYvFZZ-sTMUaskxD3yXeZwzGDZAcJmimsRk_3B28VnCytI4UlrWU4jV5EDff4V6Fv6ZrgPc_2KsUH_Q--dVVQYsELX76ysjmprz5cCnLLra9ORjtEtDUN3Q840A_4WKpvJlhe6irmqZTD7mw0kQDGsaS9s6PcK2eQQZIB1be71x5NpRfeYn1V2xXQ34FK4XTzcs3l7t9CTnYWMkh07z_NWWxiz-gHVKtFYnCXpRSHwrzc5f1oaB7f-Z6HeJjeLgJx2cwu6QzZ0fJdcy0t0nt8jI7AjOutOZ1YvObIYnS2iT5pm2S2imJ6KlAoql4lQdLVMFlE6p8AC6FzM59kGEu32-qyEp_fJ4aX8lQekESex3iKU4wUkx_gKy323je8ZAYbBlQSGLmymm8Qupz8Ii_TsWCXkLMjOHDnQtFwgASpNUChNk1jVV4s8Pclf8HuoWRUWk4tnPyTLk6DwVYHxJOPSdbgSIdB_5ksjmYZAmQGdNjjUF6iXAaYPiVFnTsQ6TYPh-6OgiwE_oHz-O9Bs_C-gaQ30ugCZBCQSiuLhCMgVc5fVkNs1JHjKsNa8hYZUCiYNfqg_fFkayMXNz6tm7BQvJsY6WWcYhpTFhd4f5rZYCde2bQcCdKdJeM1Ka9Kvt8TRaZbineNpqGc_-vOwnpHrYK7BaDg-eExuMNwJaoObbW-Txmq51k_I1fDLKkqXTwvXRMnHyzbc79wjzUs
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+SARS-CoV-2+Spike+protein+has+a+broad+tropism+for+mammalian+ACE2+proteins&rft.jtitle=PLoS+biology&rft.au=Conceicao%2C+Carina&rft.au=Thakur%2C+Nazia&rft.au=Human%2C+Stacey&rft.au=Kelly%2C+James+T&rft.date=2020-12-21&rft.pub=Public+Library+of+Science&rft.issn=1544-9173&rft.volume=18&rft.issue=12&rft_id=info:doi/10.1371%2Fjournal.pbio.3001016&rft.externalDocID=A650814997
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1545-7885&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1545-7885&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1545-7885&client=summon