ACE2 receptor usage reveals variation in susceptibility to SARS-CoV and SARS-CoV-2 infection among bat species

Yan, Huan; Jiao, Hengwu; Liu, Qianyun; Zhang, Zhen; Xiong, Qing; Wang, Bing-Jun; Wang, Xin; Guo, Ming; Wang, Lin‐Fa; Lan, Ke; Chen, Yu; Zhao, Huabin

doi:10.1038/s41559-021-01407-1

Cited by 105 publications

(125 citation statements)

References 39 publications

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“…This highlights the remarkable phylogenetic and genomic diversity of bat coronaviruses in a tiny geographic area and to which humans may be routinely exposed. Importantly, in addition to rhinolophids, this broad geographic region in Asia is rich in many other bat families (Anthony et al, 2017) and other wildlife species (Olival et al, 2017) that have been shown to be susceptible to SARS-CoV-2 in vitro (Conceicao et al, 2020;Wu et al, 2020b;Sang et al, 2020;Yan et al, 2021). It is therefore essential that further surveillance efforts should cover a broader range of wild animals in this region to help track ongoing spillovers of relatives of SARS-CoV-2 and SARS-CoV, as well as other pathogenic viruses from animals to humans.…”

Section: Discussionmentioning

confidence: 99%

Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses

Zhou

Chen

et al. 2021

Cell

316

302

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Despite the discovery of animal coronaviruses related to SARS-CoV-2, the evolutionary origins of this virus are elusive. We describe a meta-transcriptomic study of 411 bat samples collected from a small geographical region in Yunnan province, China, between May 2019 and November 2020. We identified 24 full-length coronavirus genomes, including four novel SARS-CoV-2 related and three SARS-CoV related viruses. Rhinolophus pusillus virus RpYN06 was the closest relative of SARS-CoV-2 in most of the genome, although it possessed a more divergent spike gene. The other three SARS-CoV-2 related coronaviruses carried a genetically distinct spike gene that could weakly bind to the hACE2 receptor in vitro . Ecological modeling predicted the co-existence of up to 23 Rhinolophus bat species, with the largest contiguous hotspots extending from South Laos and Vietnam to southern China. Our study highlights the remarkable diversity of bat coronaviruses at the local scale, including close relatives of both SARS-CoV-2 and SARS-CoV.

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Section: Discussionmentioning

confidence: 99%

Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses

Zhou

Chen

et al. 2021

Cell

316

302

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“…XM_010968001.1). We acquired the ACE2 sequences for Carollia perspicillata bats from a study of SARS-CoV and SARS-CoV-2 infection among bats ( 25 ). We obtained the corresponding ACE2 sequences for llamas and Sturnira lilium bats (accession nos.…”

Section: Methodsmentioning

confidence: 99%

Susceptibility of Well-Differentiated Airway Epithelial Cell Cultures from Domestic and Wild Animals to Severe Acute Respiratory Syndrome Coronavirus 2

Gultom¹,

Licheri²,

Laloli³

et al. 2021

Emerg. Infect. Dis.

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Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has spread globally, and the number of worldwide cases continues to rise. The zoonotic origins of SARS-CoV-2 and its intermediate and potential spillback host reservoirs, besides humans, remain largely unknown. Because of ethical and experimental constraints and more important, to reduce and refine animal experimentation, we used our repository of well-differentiated airway epithelial cell (AEC) cultures from various domesticated and wildlife animal species to assess their susceptibility to SARS-CoV-2. We observed that SARS-CoV-2 replicated efficiently only in monkey and cat AEC culture models. Whole-genome sequencing of progeny viruses revealed no obvious signs of nucleotide transitions required for SARS-CoV-2 to productively infect monkey and cat AEC cultures. Our findings, together with previous reports of human-to-animal spillover events, warrant close surveillance to determine the potential role of cats, monkeys, and closely related species as spillback reservoirs for SARS-CoV-2.

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“…Myotis myotis , Tadarida brasiliensis , Eptesicus serotinus , and Nyctalus noctula cells were resistant to infection with both the initial virus and two recently emerged variants. ACE2 from M. myotis and T. brasiliensis , as well as from a species of the Eptesicus genus, permitted S-mediated entry of pseudotyped VSV when ectopically expressed in human cells refractory to SARS-CoV2 infection [22]. This means that when expressed at high levels, ACE2 from these three species interacts with the viral S protein.…”

Section: Discussionmentioning

confidence: 99%

“…and Eptesicus spp. ACE2 facilitate S-mediated entry of pseudo-viruses [22,23]. By contrast, expressing hACE2 in Nn cells, at a higher level than in permissive Caco-TC7 cells, seems sufficient to permit internalization but not replication.…”

Section: Discussionmentioning

confidence: 99%

Species-specific molecular barriers to SARS-CoV-2 replication in bat cells

Aicher

Streicher

Chazal

et al. 2021

Preprint

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Bats are natural reservoirs of numerous coronaviruses, including the potential ancestor of SARS-CoV-2. Knowledge concerning the interaction between coronaviruses and bat cells is sparse. We investigated the susceptibility of primary cells from Rhinolophus ferrumequinum and Myotis species, as well as of established and novel cell lines from Myotis myotis, Eptesicus serotinus, Tadarida brasiliensis and Nyctalus noctula, to SARS-CoV-2 infection. None of these cells were sensitive to infection, not even the ones expressing detectable levels of angiotensin-converting enzyme 2 (ACE2), which serves as the viral receptor in many mammalian species. The resistance to infection was overcome by expression of human ACE2 (hACE2) in three cell lines, suggesting that restriction to viral replication was due to a low expression of bat ACE2 (bACE2) or absence of bACE2 binding in these cells. Infectious virions were produced but not released from hACE2-transduced M. myotis brain cells. E. serotinus brain cells and M. myotis nasal epithelial cells expressing hACE2 efficiently controlled viral replication. This ability to control viral replication correlated with a potent interferon response. Our data highlight the existence of species-specific molecular barriers to viral replication in bat cells. These novel chiropteran cellular models are valuable tools to investigate the evolutionary relationships between bats and coronaviruses.

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ACE2 receptor usage reveals variation in susceptibility to SARS-CoV and SARS-CoV-2 infection among bat species

Cited by 105 publications

References 39 publications

Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses

Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses

Susceptibility of Well-Differentiated Airway Epithelial Cell Cultures from Domestic and Wild Animals to Severe Acute Respiratory Syndrome Coronavirus 2

Species-specific molecular barriers to SARS-CoV-2 replication in bat cells

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