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Annual Review of Animal Biosciences

Volume 11, 2023

Animal Models, Zoonotic Reservoirs, and Cross-Species Transmission of Emerging Human-Infecting Coronaviruses

Abstract

Over the past three decades, coronavirus (CoV) diseases have impacted humans more than any other emerging infectious disease. The recent emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of COVID-19 (coronavirus disease 2019), has resulted in huge economic disruptions and loss of human lives. The SARS-CoV-2 genome was found to mutate more rapidly due to sustained transmission in humans and potentially animals, resulting in variants of concern (VOCs) that threaten global human health. However, the primary difficulties are filling in the current knowledge gaps in terms of the origin and modalities of emergence for these viruses. Because many CoVs threatening human health are suspected to have a zoonotic origin, identifying the animal hosts implicated in the spillover or spillback events would be beneficial for current pandemic management and to prevent future outbreaks. In this review, wesummarize the animal models, zoonotic reservoirs, and cross-species transmission of the emerging human CoVs. Finally, we comment on potential sources of SARS-CoV-2 Omicron VOCs and the new SARS-CoV-2 recombinants currently under investigation.

Keyword(s): animal model, coronavirus, cross-species transmission, recombination, surveillance, zoonotic diseases
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/content/journals/10.1146/annurev-animal-020420-025011
2023-02-15
2024-04-29
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Literature Cited

  1. 1.
    Feng Y, Gao GF. 2007. Towards our understanding of SARS-CoV, an emerging and devastating but quickly conquered virus. Comp. Immunol. Microbiol. Infect. Dis. 30:5–6309–27
     [Google Scholar]
  2. 2.
    Zhou G, Yan G 2003. Severe acute respiratory syndrome epidemic in Asia. Emerg. Infect. Dis. 9:121608–10
     [Google Scholar]
  3. 3.
    Cotten M, Watson SJ, Kellam P, Al-Rabeeah AA, Makhdoom HQ et al. 2013. Transmission and evolution of the Middle East respiratory syndrome coronavirus in Saudi Arabia: a descriptive genomic study. Lancet 382:99091993–2002
     [Google Scholar]
  4. 4.
    Wong G, Liu W, Liu Y, Zhou B, Bi Y, Gao GF. 2015. MERS, SARS, and Ebola: the role of super-spreaders in infectious disease. Cell Host Microbe 18:4398–401
     [Google Scholar]
  5. 5.
    World Health Organ 2022. Middle East respiratory syndrome coronavirus (MERS-CoV) https://www.who.int/health-topics/middle-east-respiratory-syndrome-coronavirus-mers
  6. 6.
    Zhu N, Zhang D, Wang W, Li X, Yang B et al. 2020. A novel coronavirus from patients with pneumonia in China, 2019. N. Engl. J. Med. 382:8727–33
     [Google Scholar]
  7. 7.
    Tan W, Zhao X, Ma X, Wang W, Niu P et al. 2020. A novel coronavirus genome identified in a cluster of pneumonia cases—Wuhan, China 2019–2020. CCDC Wkly 2:461–62
     [Google Scholar]
  8. 8.
    Jiang S, Shi Z, Shu Y, Song J, Gao GF et al. 2020. A distinct name is needed for the new coronavirus. Lancet 395:10228949
     [Google Scholar]
  9. 9.
    World Health Organ. 2022. Weekly epidemiological update on COVID-19—15 March 2022 Publ., World Health Organ. Geneva: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19---15-march-2022
  10. 10.
    Petrosillo N, Viceconte G, Ergonul O, Ippolito G, Petersen E. 2020. COVID-19, SARS and MERS: Are they closely related?. Clin. Microbiol. Infect. 26:6729–34
     [Google Scholar]
  11. 11.
    Zhang T, Wu Q, Zhang Z. 2020. Probable pangolin origin of SARS-CoV-2 associated with the COVID-19 outbreak. Curr. Biol. 30:71346–51.e2
     [Google Scholar]
  12. 12.
    Zhou H, Chen X, Hu T, Li J, Song H et al. 2020. A novel bat coronavirus closely related to SARS-CoV-2 contains natural insertions at the S1/S2 cleavage site of the spike protein. Curr. Biol. 30:112196–203.e3
     [Google Scholar]
  13. 13.
    Niu S, Wang J, Bai B, Wu L, Zheng A et al. 2021. Molecular basis of cross-species ACE2 interactions with SARS-CoV-2-like viruses of pangolin origin. EMBO J. 40:16e107786
     [Google Scholar]
  14. 14.
    Andersen KG, Rambaut A, Lipkin WI, Holmes EC, Garry RF. 2020. The proximal origin of SARS-CoV-2. Nat. Med. 26:4450–52
     [Google Scholar]
  15. 15.
    Pormohammad A, Ghorbani S, Khatami A, Farzi R, Baradaran B et al. 2020. Comparison of confirmed COVID-19 with SARS and MERS cases—clinical characteristics, laboratory findings, radiographic signs and outcomes: a systematic review and meta-analysis. Rev. Med. Virol. 30:4e2112
     [Google Scholar]
  16. 16.
    Kim M-N, Kim E-C. 2018. Considering revision the criteria for patients under investigations for MERS-CoV infections: diarrhea or not. J. Korean Med. Sci. 33:53e344
     [Google Scholar]
  17. 17.
    Guan W, Liang W, Zhao Y, Liang H, Chen Z et al. 2020. Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis. Eur. Respir. J. 55:52000547
     [Google Scholar]
  18. 18.
    Parra-Bracamonte GM, Lopez-Villalobos N, Parra-Bracamonte FE. 2020. Clinical characteristics and risk factors for mortality of patients with COVID-19 in a large dataset from Mexico. Ann. Epidemiol. 52:93–98.e2
     [Google Scholar]
  19. 19.
    Ng DL, Al Hosani F, Keating MK, Gerber SI, Jones TL et al. 2016. Clinicopathologic, immunohistochemical, and ultrastructural findings of a fatal case of Middle East respiratory syndrome coronavirus infection in the United Arab Emirates, April 2014. Am. J. Pathol. 186:3652–58
     [Google Scholar]
  20. 20.
    Liu J, Zheng X, Tong Q, Li W, Wang B et al. 2020. Overlapping and discrete aspects of the pathology and pathogenesis of the emerging human pathogenic coronaviruses SARS-CoV, MERS-CoV, and 2019-nCoV. J. Med. Virol. 92:5491–94
     [Google Scholar]
  21. 21.
    Nikolich-Zugich J, Knox KS, Rios CT, Natt B, Bhattacharya D, Fain MJ. 2020. SARS-CoV-2 and COVID-19 in older adults: what we may expect regarding pathogenesis, immune responses, and outcomes. GeroScience 42:2505–14
     [Google Scholar]
  22. 22.
    Centers for Disease Control and Prevention 2019. Coronavirus disease 2019 (COVID-19). https://www.cdc.gov/coronavirus/2019-ncov/index.html
  23. 23.
    Sui J, Aird DR, Tamin A, Murakami A, Yan M et al. 2008. Broadening of neutralization activity to directly block a dominant antibody-driven SARS-coronavirus evolution pathway. PLOS Pathog. 4:11e1000197
     [Google Scholar]
  24. 24.
    Xiong Q, Cao L, Ma C, Liu C, Si J et al. 2022. Close relatives of MERS-CoV in bats use ACE2 as their functional receptors. bioRxiv 477490v1. https://doi.org/10.1101/2022.01.24.477490
  25. 25.
    World Health Organ 2022. Weekly epidemiological update on COVID-19—5 April 2022 Publ. World Health Organ. Geneva: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19---5-april-2022
  26. 26.
    World Health Organ 2022. Weekly epidemiological update on COVID-19—12 April 2022 Publ. World Health Organ. Geneva: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19---12-april-2022
  27. 27.
    Liu Y, Liu J, Plante KS, Plante JA, Xie X, Zhang X et al. 2022. The N501Y spike substitution enhances SARS-CoV-2 infection and transmission. Nature 602:7896294–99
     [Google Scholar]
  28. 28.
    Thakur S, Sasi S, Pillai SG, Nag A, Shukla D et al. 2022. SARS-CoV-2 mutations and their impact on diagnostics, therapeutics and vaccines. Front. Med. 9:815389
     [Google Scholar]
  29. 29.
    Ulrich L, Halwe NJ, Taddeo A, Ebert N, Schön J et al. 2022. Enhanced fitness of SARS-CoV-2 variant of concern Alpha but not Beta. Nature 602:7896307–13
     [Google Scholar]
  30. 30.
    Padilha DA, Filho VB, Moreira RS, Soratto TAT, Maia GA et al. 2022. Emergence of two distinct SARS-CoV-2 Gamma variants and the rapid spread of P.1-like-II SARS-CoV-2 during the second wave of COVID-19 in Santa Catarina, Southern Brazil. Viruses4695
     [Google Scholar]
  31. 31.
    Kim Y-I, Casel MAB, Choi YK. 2022. Transmissibility and pathogenicity of SARS-CoV-2 variants in animal models. J. Microbiol. 60:3255–67
     [Google Scholar]
  32. 32.
    Saville JW, Mannar D, Zhu X, Srivastava SS, Berezuk AM, Demers J-P et al. 2022. Structural and biochemical rationale for enhanced spike protein fitness in Delta and Kappa SARS-CoV-2 variants. Nat. Commun. 13:742
     [Google Scholar]
  33. 33.
    Wei C, Shan K-J, Wang W, Zhang S, Huan Q, Qian W. 2021. Evidence for a mouse origin of the SARS-CoV-2 Omicron variant. J. Genet. Genom. 48:121111–21
     [Google Scholar]
  34. 34.
    Negi SS, Schein CH, Braun W. 2022. Regional and temporal coordinated mutation patterns in SARS-CoV-2 spike protein revealed by a clustering and network analysis. Sci. Rep. 12:1128
     [Google Scholar]
  35. 35.
    Singh DK, Singh B, Ganatra SR, Gazi M, Cole J et al. 2021. Responses to acute infection with SARS-CoV-2 in the lungs of rhesus macaques, baboons and marmosets. Nat. Microbiol. 6:173–86
     [Google Scholar]
  36. 36.
    Blair RV, Vaccari M, Doyle-Meyers LA, Roy CJ, Russell-Lodrigue K et al. 2021. Acute respiratory distress in aged, SARS-CoV-2-infected African Green monkeys but not rhesus macaques. Am. J. Pathol. 191:2274–82
     [Google Scholar]
  37. 37.
    Falzarano D, de Wit E, Feldmann F, Rasmussen AL, Okumura A et al. 2014. Infection with MERS-CoV causes lethal pneumonia in the common marmoset. PLOS Pathog. 10:8e1004250
     [Google Scholar]
  38. 38.
    Coleman CM, Matthews KL, Goicochea L, Frieman MB. 2014. Wild-type and innate immune-deficient mice are not susceptible to the Middle East respiratory syndrome coronavirus. J. Gen. Virol. 95:Pt. 2408–12
     [Google Scholar]
  39. 39.
    McCray PB, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L et al. 2007. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J. Virol. 81:2813–21
     [Google Scholar]
  40. 40.
    Day CW, Baric R, Cai SX, Frieman M, Kumaki Y et al. 2009. A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. Virology 395:2210–22
     [Google Scholar]
  41. 41.
    Li K, Wohlford-Lenane CL, Channappanavar R, Park J-E, Earnest JT et al. 2017. Mouse-adapted MERS coronavirus causes lethal lung disease in human DPP4 knockin mice. PNAS 114:15E3119–28
     [Google Scholar]
  42. 42.
    Bao L, Deng W, Huang B, Gao H, Liu J et al. 2020. The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice. Nature 583:7818830–33
     [Google Scholar]
  43. 43.
    Jiang RD, Liu MQ, Chen Y, Shan C, Zhou YW et al. 2020. Pathogenesis of SARS-CoV-2 in transgenic mice expressing human angiotensin-converting enzyme 2. Cell 182:150–58.e8
     [Google Scholar]
  44. 44.
    Sun S, Gu H, Cao L, Chen Q, Ye Q et al. 2021. Characterization and structural basis of a lethal mouse-adapted SARS-CoV-2. Nat. Commun. 12:15654
     [Google Scholar]
  45. 45.
    Halfmann PJ, Iida S, Iwatsuki-Horimoto K, Maemura T, Kiso M et al. 2022. SARS-CoV-2 Omicron virus causes attenuated disease in mice and hamsters. Nature 603:7902687–92
     [Google Scholar]
  46. 46.
    Zhang YN, Zhang ZR, Zhang HQ, Li N, Zhang QY et al. 2022. Different pathogenesis of SARS-CoV-2 Omicron variant in wild-type laboratory mice and hamsters. Signal Transduct. Target Ther. 7:62
     [Google Scholar]
  47. 47.
    Abdelnabi R, Foo CS, Zhang X, Lemmens V, Maes P et al. 2022. The omicron (B.1.1.529) SARS-CoV-2 variant of concern does not readily infect Syrian hamsters. Antiviral Res. 198:105253
     [Google Scholar]
  48. 48.
    Chu YK, Ali GD, Jia F, Li Q, Kelvin D et al. 2008. The SARS-CoV ferret model in an infection-challenge study. Virology 374:1151–63
     [Google Scholar]
  49. 49.
    Cameron MJ, Kelvin AA, Leon AJ, Cameron CM, Ran L et al. 2012. Lack of innate interferon responses during SARS coronavirus infection in a vaccination and reinfection ferret model. PLOS ONE 7:9e45842
     [Google Scholar]
  50. 50.
    Czub M, Weingartl H, Czub S, He R, Cao J. 2005. Evaluation of modified vaccinia virus Ankara based recombinant SARS vaccine in ferrets. Vaccine 23:172273–79
     [Google Scholar]
  51. 51.
    Ryan KA, Bewley KR, Fotheringham SA, Slack GS, Brown P et al. 2021. Dose-dependent response to infection with SARS-CoV-2 in the ferret model and evidence of protective immunity. Nat. Commun. 12:81
     [Google Scholar]
  52. 52.
    Zaeck LM, Scheibner D, Sehl J, Müller M, Hoffmann D et al. 2021. Light sheet microscopy-assisted 3D analysis of SARS-CoV-2 infection in the respiratory tract of the ferret model. Viruses 13:3529
     [Google Scholar]
  53. 53.
    Raj VS, Smits SL, Provacia LB, van den Brand JMA, Wiersma L et al. 2014. Adenosine deaminase acts as a natural antagonist for dipeptidyl peptidase 4-mediated entry of the Middle East respiratory syndrome coronavirus. J. Virol. 88:31834–38
     [Google Scholar]
  54. 54.
    van den Brand JMA, Haagmans BL, Leijten L, van Riel D, Martina BEE et al. 2008. Pathology of experimental SARS coronavirus infection in cats and ferrets. Vet. Pathol. 45:4551–62
     [Google Scholar]
  55. 55.
    Park SJ, Yu KM, Kim YI, Kim SM, Kim EH et al. 2020. Antiviral efficacies of FDA-approved drugs against SARS-CoV-2 infection in ferrets. mBio 11:3e01114–20
     [Google Scholar]
  56. 56.
    Proud PC, Tsitoura D, Watson RJ, Chua BY, Aram MJ et al. 2020. Prophylactic intranasal administration of a TLR2/6 agonist reduces upper respiratory tract viral shedding in a SARS-CoV-2 challenge ferret model. eBioMedicine 63:103153
     [Google Scholar]
  57. 57.
    Havermalen N, Miazgowicz KL, Milne-Price S, Bushmaker T, Robertson S et al. 2014. Host species restriction of Middle East Respiratory Syndrome coronavirus through its receptor, dipeptidyl peptidase 4. J. Virol. 88:169220–32
     [Google Scholar]
  58. 58.
    ter Meulen J, Bakker ABH, van den Brink EN, Weverling GJ, Martina BEE et al. 2004. Human monoclonal antibody as prophylaxis for SARS coronavirus infection in ferrets. Lancet 363:94272139–41
     [Google Scholar]
  59. 59.
    Lamirande EW, DeDiego ML, Roberts A, Jackson JP, Alvarez E et al. 2008. A live attenuated severe acute respiratory syndrome coronavirus is immunogenic and efficacious in golden Syrian hamsters. J. Virol. 82:157721–24
     [Google Scholar]
  60. 60.
    Roberts A, Vogel L, Guarner J, Hayes N, Murphy B et al. 2005. Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J. Virol. 79:1503–11
     [Google Scholar]
  61. 61.
    Watts DM, Peters CJ, Newman P, Wang N, Yoshikawa N et al. 2008. Evaluation of cotton rats as a model for severe acute respiratory syndrome. Vector Borne Zoonotic Dis. 8:3339–44
     [Google Scholar]
  62. 62.
    Damas J, Hughes GM, Keough KC, Painter CA, Persky NS et al. 2020. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. PNAS 117:3622311–22
     [Google Scholar]
  63. 63.
    Wells HL, Letko M, Lasso G, Ssebide B, Nziza J et al. 2021. The evolutionary history of ACE2 usage within the coronavirus subgenus Sarbecovirus. bioRxiv 190546v2. https://doi.org/10.1101/2020.07.07.190546
  64. 64.
    Chan JFW, Zhang AJ, Yuan S, Poon VKM, Chan CCS et al. 2020. Simulation of the clinical and pathological manifestations of coronavirus disease 2019 (COVID-19) in a golden Syrian hamster model: implications for disease pathogenesis and transmissibility. Clin. Infect. Dis. 71:92428–46
     [Google Scholar]
  65. 65.
    Osterrieder N, Bertzbach LD, Dietert K, Abdelgawad A, Vladimirova D et al. 2020. Age-dependent progression of SARS-CoV-2 infection in Syrian hamsters. Viruses 12:7779
     [Google Scholar]
  66. 66.
    Imai M, Iwatsuki-Horimoto K, Hatta M, Loeber S, Halfmann PJ et al. 2020. Syrian hamsters as a small animal model for SARS-CoV-2 infection and countermeasure development. PNAS 117:2816587–95
     [Google Scholar]
  67. 67.
    Abdelnabi R, Boudewijns R, Foo CS, Seldeslachts L, Sanchez-Felipe L et al. 2021. Comparing infectivity and virulence of emerging SARS-CoV-2 variants in Syrian hamsters. eBioMedicine 68:103403
     [Google Scholar]
  68. 68.
    Mohandas S, Yadav PD, Shete A, Nyayanit D, Sapkal G et al. 2021. SARS-CoV-2 Delta variant pathogenesis and host response in Syrian hamsters. Viruses 13:91773
     [Google Scholar]
  69. 69.
    Yuan S, Ye ZW, Liang R, Tang K, Zhang AJ et al. 2022. The SARS-CoV-2 Omicron (B.1.1.529) variant exhibits altered pathogenicity, transmissibility, and fitness in the golden Syrian hamster model. bioRxiv 476031v1 https://doi.org/10.1101/2022.01.12.476031
  70. 70.
    Liang L, He C, Lei M, Li S, Hao Y et al. 2005. Pathology of guinea pigs experimentally infected with a novel reovirus and coronavirus isolated from SARS patients. DNA Cell Biol. 24:8485–90
     [Google Scholar]
  71. 71.
    Houser KV, Broadbent AJ, Gretebeck L, Vogel L, Lamirande EW et al. 2017. Enhanced inflammation in New Zealand white rabbits when MERS-CoV reinfection occurs in the absence of neutralizing antibody. PLOS Pathog. 13:8e1006565
     [Google Scholar]
  72. 72.
    Vergara-Alert J, van den Brand JMA, Widagdo W, Muñoz M, Raj S et al. 2017. Livestock susceptibility to infection with Middle East respiratory syndrome coronavirus. Emerg. Infect. Dis. 23:2232–40
     [Google Scholar]
  73. 73.
    Mykytyn AZ, Lamers MM, Okba NMA, Breugem TI, Schipper D et al. 2021. Susceptibility of rabbits to SARS-CoV-2. Emerg. Microbes Infect. 10:11–7
     [Google Scholar]
  74. 74.
    Ravichandran S, Coyle EM, Klenow L, Tang J, Grubbs G et al. 2020. Antibody signature induced by SARS-CoV-2 spike protein immunogens in rabbits. Sci. Transl. Med. 12:550eabc3539
     [Google Scholar]
  75. 75.
    Zhao Y, Wang J, Kuang D, Xu J, Yang M et al. 2020. Susceptibility of tree shrew to SARS-CoV-2 infection. Sci. Rep. 10:116007
     [Google Scholar]
  76. 76.
    Fagre A, Lewis J, Eckley M, Zhan S, Rocha SM et al. 2021. SARS-CoV-2 infection, neuropathogenesis and transmission among deer mice: implications for reverse zoonosis to New World rodents. PLOS Pathog. 17:5e1009585
     [Google Scholar]
  77. 77.
    Haverkamp AK, Lehmbecker A, Spitzbarth I, Widagdo W, Haagmans BL et al. 2018. Experimental infection of dromedaries with Middle East respiratory syndrome-coronavirus is accompanied by massive ciliary loss and depletion of the cell surface receptor dipeptidyl peptidase 4. Sci. Rep. 8:19778
     [Google Scholar]
  78. 78.
    de Wit E, van Doremalen N, Falzarano D, Munster VJ. 2016. SARS and MERS: recent insights into emerging coronaviruses. Nat. Rev. Microbiol. 14:8523–34
     [Google Scholar]
  79. 79.
    Hanke L, Vidakovics Perez L, Sheward DJ, Das H, Schulte T et al. 2020. An alpaca nanobody neutralizes SARS-CoV-2 by blocking receptor interaction. Nat. Commun. 11:14420
     [Google Scholar]
  80. 80.
    Shuai L, Zhong G, Yuan Q, Wen Z, Wang C et al. 2021. Replication, pathogenicity, and transmission of SARS-CoV-2 in minks. Natl. Sci. Rev. 8:3nwaa291
     [Google Scholar]
  81. 81.
    Shi J, Wen Z, Zhong G, Yang H, Wang C et al. 2020. Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS-coronavirus 2. Science 368:64941016–20
     [Google Scholar]
  82. 82.
    Bosco-Lauth AM, Hartwig AE, Porter SM, Gordy PW, Nehring M et al. 2020. Experimental infection of domestic dogs and cats with SARS-CoV-2: pathogenesis, transmission, and response to reexposure in cats. PNAS 117:4226382–88
     [Google Scholar]
  83. 83.
    Freuling CM, Breithaupt A, Müller T, Sehl J, Balkema-Buschmann A et al. 2020. Susceptibility of raccoon dogs for experimental SARS-CoV-2 infection. Emerg. Infect. Dis. 26:122982–85
     [Google Scholar]
  84. 84.
    Cool K, Gaudreault NN, Morozov I, Trujillo JD, Meekins DA et al. 2022. Infection and transmission of ancestral SARS-CoV-2 and its alpha variant in pregnant white-tailed deer. Emerg. Microbes Infect. 11:195–112
     [Google Scholar]
  85. 85.
    Hale VL, Dennis PM, McBride DS, Nolting JM, Madden C et al. 2022. SARS-CoV-2 infection in free-ranging white-tailed deer. Nature 602:7897481–86
     [Google Scholar]
  86. 86.
    Schlottau K, Rissmann M, Graaf A, Schön J, Sehl J et al. 2020. SARS-CoV-2 in fruit bats, ferrets, pigs, and chickens: an experimental transmission study. Lancet Microbe 1:5e218–25
     [Google Scholar]
  87. 87.
    Hall JS, Knowles S, Nashold SW, Ip HS, Leon AE et al. 2020. Experimental challenge of a North American bat species, big brown bat (Eptesicus fuscus), with SARS-CoV-2. Transbound. Emerg. Dis. 68:63443–52
     [Google Scholar]
  88. 88.
    Li W, Shi Z, Yu M, Ren W, Smith C et al. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science 310:5748676–79
     [Google Scholar]
  89. 89.
    Lau SKP, Woo PCY, Li KSM, Huang Y, Tsoi H-W et al. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. PNAS 102:3914040–45
     [Google Scholar]
  90. 90.
    Shi Z, Hu Z. 2008. A review of studies on animal reservoirs of the SARS coronavirus. Virus Res. 133:174–87
     [Google Scholar]
  91. 91.
    Xu H, Wang M, Zhang Z, Zou X, Gao Y et al. 2004. An epidemiologic investigation on infection with severe acute respiratory syndrome coronavirus in wild animals traders in Guangzhou. Chin. J. Prev. Med. 38:281–83
     [Google Scholar]
  92. 92.
    Zhong NS, Zheng BJ, Li YM, Poon LLM, Xie ZH et al. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People's Republic of China, in February, 2003. Lancet 362:93931353–58
     [Google Scholar]
  93. 93.
    Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX et al. 2003. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302:5643276–78
     [Google Scholar]
  94. 94.
    Martina BEE, Haagmans BL, Kuiken T, Fouchier RAM, Rimmelzwaan GF et al. 2003. Virology: SARS virus infection of cats and ferrets. Nature 425:6961915
     [Google Scholar]
  95. 95.
    Annan A, Baldwin HJ, Corman VM, Klose SM, Owusu M et al. 2013. Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe. Emerg. Infect. Dis. 19:3456–59
     [Google Scholar]
  96. 96.
    Ithete NL, Stoffberg S, Corman VM, Cottontail VM, Richards LR et al. 2013. Close relative of human Middle East respiratory syndrome coronavirus in bat, South Africa. Emerg. Infect. Dis. 19:101697–99
     [Google Scholar]
  97. 97.
    Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V et al. 2013. Middle East respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg. Infect. Dis. 19:111819–23
     [Google Scholar]
  98. 98.
    Raj VS, Osterhaus AD, Fouchier RA, Haagmans BL. 2014. MERS: emergence of a novel human coronavirus. Curr. Opin. Virol. 5:58–62
     [Google Scholar]
  99. 99.
    Reusken CB, Farag EA, Jonges M, Godeke GJ, El-Sayed AM et al. 2014. Middle East respiratory syndrome coronavirus (MERS-CoV) RNA and neutralising antibodies in milk collected according to local customs from dromedary camels, Qatar, April 2014. Eurosurveillance 19:2320829
     [Google Scholar]
  100. 100.
    Corman VM, Jores J, Meyer B, Younan M, Liljander A et al. 2014. Antibodies against MERS coronavirus in dromedary camels, Kenya, 1992–2013. Emerg. Infect. Dis. 20:81319–22
     [Google Scholar]
  101. 101.
    Chu DKW, Poon LLM, Gomaa MM, Shehata MM, Perera RAPM et al. 2014. MERS coronaviruses in dromedary camels, Egypt. Emerg. Infect. Dis. 20:61049–53
     [Google Scholar]
  102. 102.
    Reusken CBEM, Messadi L, Feyisa A, Ularamu H, Godeke G-J et al. 2014. Geographic distribution of MERS coronavirus among dromedary camels, Africa. Emerg. Infect. Dis. 20:81370–74
     [Google Scholar]
  103. 103.
    Kandeil A, Gomaa M, Shehata M, El-Taweel A, Kayed AE et al. 2019. Middle East respiratory syndrome coronavirus infection in non-camelid domestic mammals. Emerg. Microbes Infect. 8:1103–8
     [Google Scholar]
  104. 104.
    David D, Rotenberg D, Khinich E, Erster O, Bardenstein S et al. 2018. Middle East respiratory syndrome coronavirus specific antibodies in naturally exposed Israeli llamas, alpacas and camels. One Health 5:65–68
     [Google Scholar]
  105. 105.
    Crameri G, Durr PA, Klein R, Foord A, Yu M et al. 2016. Experimental infection and response to rechallenge of alpacas with Middle East respiratory syndrome coronavirus. Emerg. Infect. Dis. 22:61071–74
     [Google Scholar]
  106. 106.
    Hemida MG, Alnaeem A, Chu DK, Perera RA, Chan SM et al. 2017. Longitudinal study of Middle East respiratory syndrome coronavirus infection in dromedary camel herds in Saudi Arabia, 2014–2015. Emerg. Microbes Infect. 6:6e56
     [Google Scholar]
  107. 107.
    Lu R, Zhao X, Li J, Niu P, Yang B et al. 2020. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet 395:10224565–74
     [Google Scholar]
  108. 108.
    Zhou P, Yang XL, Wang XG, Hu B, Zhang L et al. 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579:7798270–73
     [Google Scholar]
  109. 109.
    Lam TTY, Jia N, Zhang YW, Shum MHH, Jiang JF et al. 2020. Identifying SARS-CoV-2-related coronaviruses in Malayan pangolins. Nature 583:7815282–85
     [Google Scholar]
  110. 110.
    Zhou H, Ji J, Chen X, Bi Y, Li J et al. 2021. Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses. Cell 184:174380–91.e14
     [Google Scholar]
  111. 111.
    Li LL, Wang JL, Ma XH, Sun XM, Li JS et al. 2021. A novel SARS-CoV-2 related coronavirus with complex recombination isolated from bats in Yunnan province, China. Emerg. Microbes Infect. 10:11683–90
     [Google Scholar]
  112. 112.
    Temmam S, Vongphayloth K, Baquero E, Munier S, Bonomi M et al. 2022. Bat coronaviruses related to SARS-CoV-2 and infectious for human cells. Nature 604:330–36
     [Google Scholar]
  113. 113.
    Wacharapluesadee S, Tan CW, Maneeorn P, Duengkae P, Zhu F et al. 2021. Evidence for SARS-CoV-2 related coronaviruses circulating in bats and pangolins in Southeast Asia. Nat. Commun. 12:972
     [Google Scholar]
  114. 114.
    Meekins DA, Gaudreault NN, Richt JA. 2021. Natural and experimental SARS-CoV-2 infection in domestic and wild animals. Viruses 13:101993
     [Google Scholar]
  115. 115.
    Prince T, Smith SL, Radford AD, Solomon T, Hughes GL, Patterson EI. 2021. SARS-CoV-2 infections in animals: reservoirs for reverse zoonosis and models for study. Viruses 13:3494
     [Google Scholar]
  116. 116.
    Boklund A, Gortázar C, Pasquali P, Roberts H, Nielsen SS et al. 2021. Monitoring of SARS-CoV-2 infection in mustelids. EFSA J. 19:3e06459
     [Google Scholar]
  117. 117.
    Devaux CA, Pinault L, Delerce J, Raoult D, Levasseur A, Frutos R. 2021. Spread of mink SARS-CoV-2 variants in humans: a model of sarbecovirus interspecies evolution. Front. Microbiol. 12:675528
     [Google Scholar]
  118. 118.
    Hoffmann M, Zhang L, Krüger N, Graichen L, Kleine-Weber H et al. 2021. SARS-CoV-2 mutations acquired in mink reduce antibody-mediated neutralization. Cell Rep. 35:3109017
     [Google Scholar]
  119. 119.
    Pereira F. 2021. SARS-CoV-2 variants lacking ORF8 occurred in farmed mink and pangolin. Gene 784:145596
     [Google Scholar]
  120. 120.
    Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI et al. 2017. Pathways to zoonotic spillover. Nat. Rev. Microbiol. 15:8502–10
     [Google Scholar]
  121. 121.
    Meyerholz DK, Lambertz AM, McCray PB. 2016. Dipeptidyl peptidase 4 distribution in the human respiratory tract. Am. J. Pathol. 186:178–86
     [Google Scholar]
  122. 122.
    Banerjee A, Subudhi S, Rapin N, Lew J, Jain R et al. 2020. Selection of viral variants during persistent infection of insectivorous bat cells with Middle East respiratory syndrome coronavirus. Sci. Rep. 10:17257
     [Google Scholar]
  123. 123.
    Yan H, Jiao H, Liu Q, Zhang Z, Xiong Q et al. 2021. ACE2 receptor usage reveals variation in susceptibility to SARS-CoV and SARS-CoV-2 infection among bat species. Nat. Ecol. Evol. 5:5600–8
     [Google Scholar]
  124. 124.
    Liu K, Tan S, Niu S, Wang J, Wu L et al. 2021. Cross-species recognition of SARS-CoV-2 to bat ACE2. PNAS 118:1e2020216118
     [Google Scholar]
  125. 125.
    Zhao X, Chen D, Szabla R, Zheng M, Li G et al. 2020. Broad and differential animal ACE2 receptor usage by SARS-CoV-2. J. Virol. 94:18e00940–20
     [Google Scholar]
  126. 126.
    de Wit E, Rasmussen AL, Falzarano D, Bushmaker T, Feldmann F et al. 2013. Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. PNAS 110:4116598–603
     [Google Scholar]
  127. 127.
    Gembardt F, Sterner-Kock A, Imboden H, Spalteholz M, Reibitz F et al. 2005. Organ-specific distribution of ACE2 mRNA and correlating peptidase activity in rodents. Peptides 26:71270–77
     [Google Scholar]
  128. 128.
    Reusken CBEM, Schilp C, Raj VS, De Bruin E, Kohl RHG et al. 2016. MERS-CoV infection of alpaca in a region where MERS-CoV is endemic. Emerg. Infect. Dis. 22:61129–31
     [Google Scholar]
  129. 129.
    Wang L, Su S, Bi Y, Wong G, Gao GF. 2018. Bat-origin coronaviruses expand their host range to pigs. Trends Microbiol. 26:6466–70
     [Google Scholar]
  130. 130.
    Anthony SJ, Johnson CK, Greig DJ, Kramer S, Che X et al. 2017. Global patterns in coronavirus diversity. Virus Evol. 3:1vex012
     [Google Scholar]
  131. 131.
    Latinne A, Hu B, Olival KJ, Zhu G, Zhang L et al. 2020. Origin and cross-species transmission of bat coronaviruses in China. Nat. Commun. 11:4235
     [Google Scholar]
  132. 132.
    Iyer SS, He Q, Janczy JR, Elliott EI, Zhong Z et al. 2013. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 39:2311–23
     [Google Scholar]
  133. 133.
    Zhou P, Tachedjian M, Wynne JW, Boyd V, Cui J et al. 2016. Contraction of the type I IFN locus and unusual constitutive expression of IFN-α in bats. PNAS 113:102696–701
     [Google Scholar]
  134. 134.
    Suu-Ire R, Begeman L, Banyard AC, Breed AC, Drosten C et al. 2018. Pathogenesis of bat rabies in a natural reservoir: comparative susceptibility of the straw-colored fruit bat (Eidolon helvum) to three strains of Lagos bat virus. PLOS Negl. Trop. Dis. 12:3e0006311
     [Google Scholar]
  135. 135.
    Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D et al. 2015. Ecological dynamics of emerging bat virus spillover. Proc. Biol. Sci. 282:179820142124
     [Google Scholar]
  136. 136.
    Breed AC, Breed MF, Meers J, Field HE. 2011. Evidence of endemic Hendra virus infection in flying-foxes (Pteropus conspicillatus)—implications for disease risk management. PLOS ONE 6:12e28816
     [Google Scholar]
  137. 137.
    Pourrut X, Délicat A, Rollin PE, Ksiazek TG, Gonzalez J-P, Leroy EM. 2007. Spatial and temporal patterns of Zaire ebolavirus antibody prevalence in the possible reservoir bat species. J. Infect. Dis. 196:Suppl. 2S176–83
     [Google Scholar]
  138. 138.
    Rahman SA, Hassan L, Epstein JH, Mamat ZC, Yatim AM et al. 2013. Risk factors for Nipah virus infection among pteropid bats, Peninsular Malaysia. Emerg. Infect. Dis. 19:151–60
     [Google Scholar]
  139. 139.
    Ji W, Wang W, Zhao X, Zai J, Li X. 2020. Cross-species transmission of the newly identified coronavirus 2019-nCoV. J. Med. Virol. 92:4433–40
     [Google Scholar]
  140. 140.
    Luan J, Jin X, Lu Y, Zhang L 2020. SARS-CoV-2 spike protein favors ACE2 from Bovidae and Cricetidae. J. Med. Virol. 92:91649–56
     [Google Scholar]
  141. 141.
    Xia X. 2020. Extreme genomic CpG deficiency in SARS-CoV-2 and evasion of host antiviral defense. Mol. Biol. Evol. 37:92699–705
     [Google Scholar]
  142. 142.
    Chin. SARS Mol. Epidemiol. Consort. 2004. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303:56641666–69
     [Google Scholar]
  143. 143.
    Ge XY, Li JL, Yang XL, Chmura AA, Zhu G et al. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature 503:7477535–38
     [Google Scholar]
  144. 144.
    Lau SKP, Feng Y, Chen H, Luk HKH, Yang WH et al. 2015. Severe acute respiratory syndrome (SARS) coronavirus ORF8 protein is acquired from SARS-related coronavirus from greater horseshoe bats through recombination. J. Virol. 89:2010532–47
     [Google Scholar]
  145. 145.
    Zhang Z, Shen L, Gu X. 2016. Evolutionary dynamics of MERS-CoV: potential recombination, positive selection and transmission. Sci. Rep. 6:125049
     [Google Scholar]
  146. 146.
    Wang Q, Qi J, Yuan Y, Xuan Y, Han P et al. 2014. Bat origins of MERS-CoV supported by bat coronavirus HKU4 usage of human receptor CD26. Cell Host Microbe 16:3328–37
     [Google Scholar]
  147. 147.
    Frutos R, Serra-Cobo J, Chen T, Devaux CA 2020. COVID-19: time to exonerate the pangolin from the transmission of SARS-CoV-2 to humans. Infect. Genet. Evol. 84:104493
     [Google Scholar]
  148. 148.
    Singh D, Yi SV. 2021. On the origin and evolution of SARS-CoV-2. Exp. Mol. Med. 53:4537–47
     [Google Scholar]
  149. 149.
    Lee J, Hughes T, Lee M-H, Field H, Rovie-Ryan JJ et al. 2020. No evidence of coronaviruses or other potentially zoonotic viruses in Sunda pangolins (Manis javanica) entering the wildlife trade via Malaysia. EcoHealth 17:3406–18
     [Google Scholar]
  150. 150.
    Graham RL, Baric RS. 2010. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J. Virol. 84:73134–46
     [Google Scholar]
  151. 151.
    Simon-Loriere E, Montagutelli X, Lemoine F, Donati F, Touret F et al. 2022. Rapid characterization of a Delta-Omicron SARS-CoV-2 recombinant detected in Europe. Research Square Preprint. https://doi.org/10.21203/rs.3.rs-1502293/v1
  152. 152.
    Gu H, Ng DYM, Liu GYZ, Cheng SSM, Krishnan P et al. 2022. Recombinant BA.1/BA.2 SARS-CoV-2 virus in arriving travelers, Hong Kong. Emerg. Infect. Dis. 28:61276–78
     [Google Scholar]
  153. 153.
    Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M et al. 2019. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLOS Comput. Biol. 15:4e1006650
     [Google Scholar]
  154. 154.
    Du P, Gao GF, Wang Q. 2022. The mysterious origins of the Omicron variant of SARS-CoV-2. Innovation 3:2100206
     [Google Scholar]
  155. 155.
    Prentice JC, Fox NJ, Hutchings MR, White PCL, Davidson RS, Marion G. 2019. When to kill a cull: factors affecting the success of culling wildlife for disease control. J. R. Soc. Interface 16:15220180901
     [Google Scholar]
  156. 156.
    Miguel E, Grosbois V, Caron A, Pople D, Roche B, Donnelly CA. 2020. A systemic approach to assess the potential and risks of wildlife culling for infectious disease control. Commun. Biol. 3:353
     [Google Scholar]
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Animal Models, Zoonotic Reservoirs, and Cross-Species Transmission of Emerging Human-Infecting Coronaviruses
Annual Review of Animal Biosciences 11, 1 (2023); https://doi.org/10.1146/annurev-animal-020420-025011
/content/journals/10.1146/annurev-animal-020420-025011
/content/journals/10.1146/annurev-animal-020420-025011
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