1887

Abstract

Coronaviruses (CoVs) have been studied for over 60 years, but have only recently gained notoriety as deadly human pathogens with the emergence of severe respiratory syndrome CoV and Middle East respiratory syndrome virus. The rapid emergence of these viruses has demonstrated the need for good models to study severe CoV respiratory infection and pathogenesis. There are, currently, different methods and models for the study of CoV disease. The available genetic methods for the study and evaluation of CoV genetics are reviewed here. There are several animal models, both mouse and alternative animals, for the study of severe CoV respiratory disease that have been examined, each with different pros and cons relative to the actual pathogenesis of the disease in humans. A current limitation of these models is that no animal model perfectly recapitulates the disease seen in humans. Through the review and analysis of the available disease models, investigators can employ the most appropriate available model to study various aspects of CoV pathogenesis and evaluate possible antiviral treatments that may potentially be successful in future treatment and prevention of severe CoV respiratory infections.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.069732-0
2015-03-01
2020-01-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/3/494.html?itemId=/content/journal/jgv/10.1099/vir.0.069732-0&mimeType=html&fmt=ahah

References

  1. Abdul-Rasool S., Fielding B. C.. ( 2010;). Understanding human coronavirus HCoV-NL63. . Open Virol J 4:, 76–84. [CrossRef][PubMed]
    [Google Scholar]
  2. Almazán F., Dediego M. L., Galán C., Escors D., Alvarez E., Ortego J., Sola I., Zuñiga S., Alonso S.. & other authors ( 2006;). Construction of a severe acute respiratory syndrome coronavirus infectious cDNA clone and a replicon to study coronavirus RNA synthesis. . J Virol 80:, 10900–10906. [CrossRef][PubMed]
    [Google Scholar]
  3. Assiri A., McGeer A., Perl T. M., Price C. S., Al Rabeeah A. A., Cummings D. A., Alabdullatif Z. N., Assad M., Almulhim A.. & other authors ( 2013;). Hospital outbreak of Middle East respiratory syndrome coronavirus. . N Engl J Med 369:, 407–416. [CrossRef][PubMed]
    [Google Scholar]
  4. Baas T., Roberts A., Teal T. H., Vogel L., Chen J., Tumpey T. M., Katze M. G., Subbarao K.. ( 2008;). Genomic analysis reveals age-dependent innate immune responses to severe acute respiratory syndrome coronavirus. . J Virol 82:, 9465–9476. [CrossRef][PubMed]
    [Google Scholar]
  5. Burrell L. M., Johnston C. I., Tikellis C., Cooper M. E.. ( 2004;). ACE2, a new regulator of the renin–angiotensin system. . Trends Endocrinol Metab 15:, 166–169. [CrossRef][PubMed]
    [Google Scholar]
  6. Casais R., Thiel V., Siddell S. G., Cavanagh D., Britton P.. ( 2001;). Reverse genetics system for the avian coronavirus infectious bronchitis virus. . J Virol 75:, 12359–12369. [CrossRef][PubMed]
    [Google Scholar]
  7. Chen H. I., Kao S. J., Wang D., Lee R. P., Su C. F.. ( 2003;). Acute respiratory distress syndrome. . J Biomed Sci 10:, 588–592. [CrossRef][PubMed]
    [Google Scholar]
  8. Chen J., Lau Y. F., Lamirande E. W., Paddock C. D., Bartlett J. H., Zaki S. R., Subbarao K.. ( 2010;). Cellular immune responses to severe acute respiratory syndrome coronavirus (SARS-CoV) infection in senescent BALB/c mice: CD4+ T cells are important in control of SARS-CoV infection. . J Virol 84:, 1289–1301. [CrossRef][PubMed]
    [Google Scholar]
  9. Chu Y. K., Ali G. D., Jia F., Li Q., Kelvin D., Couch R. C., Harrod K. S., Hutt J. A., Cameron C.. & other authors ( 2008;). The SARS-CoV ferret model in an infection-challenge study. . Virology 374:, 151–163. [CrossRef][PubMed]
    [Google Scholar]
  10. Clay C. C., Donart N., Fomukong N., Knight J. B., Overheim K., Tipper J., Van Westrienen J., Hahn F., Harrod K. S.. ( 2014;). Severe acute respiratory syndrome-coronavirus infection in aged nonhuman primates is associated with modulated pulmonary and systemic immune responses. . Immun Ageing 11:, 4. [CrossRef][PubMed]
    [Google Scholar]
  11. Coleman C. M., Matthews K. L., Goicochea L., Frieman M. B.. ( 2014;). Wild-type and innate immune-deficient mice are not susceptible to the Middle East respiratory syndrome coronavirus. . J Gen Virol 95:, 408–412. [CrossRef][PubMed]
    [Google Scholar]
  12. Day C. W., Baric R., Cai S. X., Frieman M., Kumaki Y., Morrey J. D., Smee D. F., Barnard D. L.. ( 2009;). A new mouse-adapted strain of SARS-CoV as a lethal model for evaluating antiviral agents in vitro and in vivo. . Virology 395:, 210–222. [CrossRef][PubMed]
    [Google Scholar]
  13. De Albuquerque N., Baig E., Ma X., Zhang J., He W., Rowe A., Habal M., Liu M., Shalev I.. & other authors ( 2006;). Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice. . J Virol 80:, 10382–10394. [CrossRef][PubMed]
    [Google Scholar]
  14. de Haan C. A., Masters P. S., Shen X., Weiss S., Rottier P. J.. ( 2002;). The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. . Virology 296:, 177–189. [CrossRef][PubMed]
    [Google Scholar]
  15. de Lang A., Baas T., Teal T., Leijten L. M., Rain B., Osterhaus A. D., Haagmans B. L., Katze M. G.. ( 2007;). Functional genomics highlights differential induction of antiviral pathways in the lungs of SARS-CoV-infected macaques. . PLoS Pathog 3:, e112. [CrossRef][PubMed]
    [Google Scholar]
  16. de Wit E., Prescott J., Baseler L., Bushmaker T., Thomas T., Lackemeyer M. G., Martellaro C., Milne-Price S., Haddock E.. & other authors ( 2013a;). The Middle East respiratory syndrome coronavirus (MERS-CoV) does not replicate in Syrian hamsters. . PLoS ONE 8:, e69127. [CrossRef][PubMed]
    [Google Scholar]
  17. de Wit E., Rasmussen A. L., Falzarano D., Bushmaker T., Feldmann F., Brining D. L., Fischer E. R., Martellaro C., Okumura A.. & other authors ( 2013b;). Middle East respiratory syndrome coronavirus (MERS-CoV) causes transient lower respiratory tract infection in rhesus macaques. . Proc Natl Acad Sci U S A 110:, 16598–16603. [CrossRef][PubMed]
    [Google Scholar]
  18. C., Va J., De Adjounian F. C., Ferrari M. F. R., Yuan L., Silver X., Torres R., Raizada M. K.. ( 2006;). ACE2 gene transfer attenuates hypertension-linked pathophysiological changes in the SHR. . Physiol Genomics 2:, 12–19.
    [Google Scholar]
  19. Drosten C., Günther S., Preiser W., van der Werf S., Brodt H.-R., Becker S., Rabenau H., Panning M., Kolesnikova L.. & other authors ( 2003;). Identification of a novel coronavirus in patients with severe acute respiratory syndrome. . N Engl J Med 348:, 1967–1976. [CrossRef][PubMed]
    [Google Scholar]
  20. Dufour J. H., Dziejman M., Liu M. T., Leung J. H., Lane T. E., Luster A. D.. ( 2002;). IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. . J Immunol 168:, 3195–3204. [CrossRef][PubMed]
    [Google Scholar]
  21. Enjuanes L., Almazán F., Sola I., Zuñiga S.. ( 2006;). Biochemical aspects of coronavirus replication and virus–host interaction. . Annu Rev Microbiol 60:, 211–230. [CrossRef][PubMed]
    [Google Scholar]
  22. Eriksson K. K., Cervantes-Barragán L., Ludewig B., Thiel V.. ( 2008;). Mouse hepatitis virus liver pathology is dependent on ADP-ribose-1″-phosphatase, a viral function conserved in the alpha-like supergroup. . J Virol 82:, 12325–12334. [CrossRef][PubMed]
    [Google Scholar]
  23. Falzarano D., de Wit E., Feldmann F., Rasmussen A. L., Okumura A., Peng X., Thomas M. J., van Doremalen N., Haddock E.. & other authors ( 2014;). Infection with MERS-CoV causes lethal pneumonia in the common marmoset. . PLoS Pathog 10:, e1004250. [CrossRef][PubMed]
    [Google Scholar]
  24. Farcas G. A., Poutanen S. M., Mazzulli T., Willey B. M., Butany J., Asa S. L., Faure P., Akhavan P., Low D. E., Kain K. C.. ( 2005;). Fatal severe acute respiratory syndrome is associated with multiorgan involvement by coronavirus. . J Infect Dis 191:, 193–197. [CrossRef][PubMed]
    [Google Scholar]
  25. Fischer F., Stegen C. F., Koetzner C. A., Masters P. S.. ( 1997;). Analysis of a recombinant mouse hepatitis virus expressing a foreign gene reveals a novel aspect of coronavirus transcription. . J Virol 71:, 5148–5160.[PubMed]
    [Google Scholar]
  26. Frieman M., Baric R.. ( 2008;). Mechanisms of severe acute respiratory syndrome pathogenesis and innate immunomodulation. . Microbiol Mol Biol Rev 72:, 672–685. [CrossRef][PubMed]
    [Google Scholar]
  27. Ge X.-Y., Li J.-L., Yang X.-L., Chmura A. A., Zhu G., Epstein J. H., Mazet J. K., Hu B., Zhang W.. & other authors ( 2013;). Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. . Nature 503:, 535–538. [CrossRef][PubMed]
    [Google Scholar]
  28. Glass W. G., Subbarao K., Murphy B., Murphy P. M.. ( 2004;). Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. . J Immunol 173:, 4030–4039. [CrossRef][PubMed]
    [Google Scholar]
  29. Greenough T. C., Carville A., Coderre J., Somasundaran M., Sullivan J. L., Luzuriaga K., Mansfield K.. ( 2005;). Pneumonitis and multi-organ system disease in common marmosets (Callithrix jacchus) infected with the severe acute respiratory syndrome-associated coronavirus. . Am J Pathol 167:, 455–463. [CrossRef][PubMed]
    [Google Scholar]
  30. Gu J., Gong E., Zhang B., Zheng J., Gao Z., Zhong Y., Zou W., Zhan J., Wang S.. & other authors ( 2005;). Multiple organ infection and the pathogenesis of SARS. . J Exp Med 202:, 415–424. [CrossRef][PubMed]
    [Google Scholar]
  31. Haagmans B. L., Kuiken T., Martina B. E., Fouchier R. A., Rimmelzwaan G. F., van Amerongen G., van Riel D., de Jong T., Itamura S.. & other authors ( 2004;). Pegylated interferon-alpha protects type 1 pneumocytes against SARS coronavirus infection in macaques. . Nat Med 10:, 290–293. [CrossRef][PubMed]
    [Google Scholar]
  32. Haagmans B. L., Andeweg A. C., Osterhaus A. D. M. E.. ( 2009;). The application of genomics to emerging zoonotic viral diseases. . PLoS Pathog 5:, e1000557. [CrossRef][PubMed]
    [Google Scholar]
  33. Hogan R. J., Gao G., Rowe T., Bell P., Flieder D., Paragas J., Kobinger G. P., Wivel N. A., Crystal R. G.. & other authors ( 2004;). Resolution of primary severe acute respiratory syndrome-associated coronavirus infection requires Stat1. . J Virol 78:, 11416–11421. [CrossRef][PubMed]
    [Google Scholar]
  34. Huang K.-J., Su I.-J., Theron M., Wu Y.-C., Lai S.-K., Liu C.-C., Lei H.-Y.. ( 2005;). An interferon-gamma-related cytokine storm in SARS patients. . J Med Virol 75:, 185–194. [CrossRef][PubMed]
    [Google Scholar]
  35. Hussain S., Perlman S., Gallagher T. M.. ( 2008;). Severe acute respiratory syndrome coronavirus protein 6 accelerates murine hepatitis virus infections by more than one mechanism. . J Virol 82:, 7212–7222. [CrossRef][PubMed]
    [Google Scholar]
  36. Imai Y., Kuba K., Ohto-Nakanishi T., Penninger J. M.. ( 2010;). Angiotensin-converting enzyme 2 (ACE2) in disease pathogenesis. . Circ J 74:, 405–410. [CrossRef][PubMed]
    [Google Scholar]
  37. Jones B. M., Ma E. S. K., Peiris J. S. M., Wong P. C., Ho J. C. M., Lam B., Lai K. N., Tsang K. W. T.. ( 2004;). Prolonged disturbances of in vitro cytokine production in patients with severe acute respiratory syndrome (SARS) treated with ribavirin and steroids. . Clin Exp Immunol 135:, 467–473. [CrossRef][PubMed]
    [Google Scholar]
  38. Kebaabetswe L. P., Haick A. K., Miura T. A.. ( 2013;). Differentiated phenotypes of primary murine alveolar epithelial cells and their susceptibility to infection by respiratory viruses. . Virus Res 175:, 110–119. [CrossRef][PubMed]
    [Google Scholar]
  39. Khanolkar A., Hartwig S. M., Haag B. A., Meyerholz D. K., Epping L. L., Haring J. S., Varga S. M., Harty J. T.. ( 2009;). Protective and pathologic roles of the immune response to mouse hepatitis virus type 1: implications for severe acute respiratory syndrome. . J Virol 83:, 9258–9272. [CrossRef][PubMed]
    [Google Scholar]
  40. Khanolkar A., Fulton R. B., Epping L. L., Pham N.-L., Tifrea D., Varga S. M., Harty J. T.. ( 2010;). T cell epitope specificity and pathogenesis of mouse hepatitis virus-1-induced disease in susceptible and resistant hosts. . J Immunol 185:, 1132–1141. [CrossRef][PubMed]
    [Google Scholar]
  41. Koetzner C. A., Parker M. M., Ricard C. S., Sturman L. S., Masters P. S.. ( 1992;). Repair and mutagenesis of the genome of a deletion mutant of the coronavirus mouse hepatitis virus by targeted RNA recombination. . J Virol 66:, 1841–1848.[PubMed]
    [Google Scholar]
  42. Kuo L., Godeke G.-J. J., Raamsman M. J. B., Masters P. S., Rottier P. J.. ( 2000;). Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. . J Virol 74:, 1393–1406. [CrossRef][PubMed]
    [Google Scholar]
  43. Kuri T., Eriksson K. K., Putics A., Züst R., Snijder E. J., Davidson A. D., Siddell S. G., Thiel V., Ziebuhr J., Weber F.. ( 2011;). The ADP-ribose-1″-monophosphatase domains of severe acute respiratory syndrome coronavirus and human coronavirus 229E mediate resistance to antiviral interferon responses. . J Gen Virol 92:, 1899–1905. [CrossRef][PubMed]
    [Google Scholar]
  44. Lai C. J., Zhao B. T., Hori H., Bray M.. ( 1991;). Infectious RNA transcribed from stably cloned full-length cDNA of dengue type 4 virus. . Proc Natl Acad Sci U S A 88:, 5139–5143. [CrossRef][PubMed]
    [Google Scholar]
  45. Lamirande E. W., DeDiego M. L., Roberts A., Jackson J. P., Alvarez E., Sheahan T., Shieh W.-J., Zaki S. R., Baric R.. & other authors ( 2008;). A live attenuated severe acute respiratory syndrome coronavirus is immunogenic and efficacious in golden Syrian hamsters. . J Virol 82:, 7721–7724. [CrossRef][PubMed]
    [Google Scholar]
  46. Lau S. K. P., Li K. S. M., Huang Y., Shek C.-T., Tse H., Wang M., Choi G. K. Y., Xu H., Lam C. S. F.. & other authors ( 2010;). Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. . J Virol 84:, 2808–2819. [CrossRef][PubMed]
    [Google Scholar]
  47. Law A. H. Y., Lee D. C. W., Cheung B. K. W., Yim H. C. H., Lau A. S. Y.. ( 2007;). Role for nonstructural protein 1 of severe acute respiratory syndrome coronavirus in chemokine dysregulation. . J Virol 81:, 416–422. [CrossRef][PubMed]
    [Google Scholar]
  48. Lawler J. V., Endy T. P., Hensley L. E., Garrison A., Fritz E. A., Lesar M., Baric R. S., Kulesh D. A., Norwood D. A.. & other authors ( 2006;). Cynomolgus macaque as an animal model for severe acute respiratory syndrome. . PLoS Med 3:, e149. [CrossRef][PubMed]
    [Google Scholar]
  49. Leibowitz J. L., Srinivasa R., Williamson S. T., Chua M. M., Liu M., Wu S., Kang H., Ma X.-Z., Zhang J.. & other authors ( 2010;). Genetic determinants of mouse hepatitis virus strain 1 pneumovirulence. . J Virol 84:, 9278–9291. [CrossRef][PubMed]
    [Google Scholar]
  50. Leparc-Goffart I., Hingley S. T., Chua M. M., Phillips J., Lavi E., Weiss S. R.. ( 1998;). Targeted recombination within the spike gene of murine coronavirus mouse hepatitis virus-A59: Q159 is a determinant of hepatotropism. . J Virol 72:, 9628–9636.[PubMed]
    [Google Scholar]
  51. Li F.. ( 2008;). Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. . J Virol 82:, 6984–6991. [CrossRef][PubMed]
    [Google Scholar]
  52. Li W., Moore M. J., Vasilieva N., Sui J., Wong S. K., Berne M. A., Somasundaran M., Sullivan J. L., Luzuriaga K.. & other authors ( 2003;). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. . Nature 426:, 450–454. [CrossRef][PubMed]
    [Google Scholar]
  53. Li C. K., Wu H., Yan H., Ma S., Wang L., Zhang M., Tang X., Temperton N. J., Weiss R. A.. & other authors ( 2008;). T cell responses to whole SARS coronavirus in humans. . J Immunol 181:, 5490–5500. [CrossRef][PubMed]
    [Google Scholar]
  54. Makino S., Keck J. G., Stohlman S. A., Lai M. M.. ( 1986;). High-frequency RNA recombination of murine coronaviruses. . J Virol 57:, 729–737.[PubMed]
    [Google Scholar]
  55. Martina B. E. E., Haagmans B. L., Kuiken T., Fouchier R. A., Rimmelzwaan G. F., Van Amerongen G., Peiris J. S., Lim W., Osterhaus A. D.. ( 2003;). Virology: SARS virus infection of cats and ferrets. . Nature 425:, 915. [CrossRef][PubMed]
    [Google Scholar]
  56. Masters P. S., Koetzner C. A., Kerr C. A., Heo Y.. ( 1994;). Optimization of targeted RNA recombination and mapping of a novel nucleocapsid gene mutation in the coronavirus mouse hepatitis virus. . J Virol 68:, 328–337.[PubMed]
    [Google Scholar]
  57. McAuliffe J., Vogel L., Roberts A., Fahle G., Fischer S., Shieh W. J., Butler E., Zaki S., St Claire M.. & other authors ( 2004;). Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys. . Virology 330:, 8–15. [CrossRef][PubMed]
    [Google Scholar]
  58. McCray P. B. Jr, Pewe L., Wohlford-Lenane C., Hickey M., Manzel L., Shi L., Netland J., Jia H. P., Halabi C.. & other authors ( 2007;). Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. . J Virol 81:, 813–821. [CrossRef][PubMed]
    [Google Scholar]
  59. Memish Z. A., Zumla A. I., Al-Hakeem R. F., Al-Rabeeah A. A., Stephens G. M.. ( 2013;). Family cluster of Middle East respiratory syndrome coronavirus infections. . N Engl J Med 368:, 2487–2494. [CrossRef][PubMed]
    [Google Scholar]
  60. Mesel-Lemoine M., Millet J., Vidalain P.-O., Law H., Vabret A., Lorin V., Escriou N., Albert M. L., Nal B., Tangy F.. ( 2012;). A human coronavirus responsible for the common cold massively kills dendritic cells but not monocytes. . J Virol 86:, 7577–7587. [CrossRef][PubMed]
    [Google Scholar]
  61. Munster V. J., de Wit E., Feldmann H.. ( 2013;). Pneumonia from human coronavirus in a macaque model. . N Engl J Med 368:, 1560–1562. [CrossRef][PubMed]
    [Google Scholar]
  62. Nagata N., Iwata N., Hasegawa H., Fukushi S., Yokoyama M., Harashima A., Sato Y., Saijo M., Morikawa S., Sata T.. ( 2007;). Participation of both host and virus factors in induction of severe acute respiratory syndrome (SARS) in F344 rats infected with SARS coronavirus. . J Virol 81:, 1848–1857. [CrossRef][PubMed]
    [Google Scholar]
  63. Nagata N., Iwata N., Hasegawa H., Fukushi S., Harashima A., Sato Y., Saijo M., Taguchi F., Morikawa S., Sata T.. ( 2008;). Mouse-passaged severe acute respiratory syndrome-associated coronavirus leads to lethal pulmonary edema and diffuse alveolar damage in adult but not young mice. . Am J Pathol 172:, 1625–1637. [CrossRef][PubMed]
    [Google Scholar]
  64. Nagata N., Iwata-Yoshikawa N., Taguchi F.. ( 2010;). Studies of severe acute respiratory syndrome coronavirus pathology in human cases and animal models. . Vet Pathol 47:, 881–892. [CrossRef][PubMed]
    [Google Scholar]
  65. Perlman S., Dandekar A. A.. ( 2005;). Immunopathogenesis of coronavirus infections: implications for SARS. . Nat Rev Immunol 5:, 917–927. [CrossRef][PubMed]
    [Google Scholar]
  66. Pewe L., Zhou H., Netland J., Tangudu C., Olivares H., Shi L., Look D., Gallagher T., Perlman S.. ( 2005;). A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. . J Virol 79:, 11335–11342. [CrossRef][PubMed]
    [Google Scholar]
  67. Pfefferle S., Krähling V., Ditt V., Grywna K., Mühlberger E., Drosten C.. ( 2009;). Reverse genetic characterization of the natural genomic deletion in SARS-Coronavirus strain Frankfurt-1 open reading frame 7b reveals an attenuating function of the 7b protein in-vitro and in-vivo. . Virol J 6:, 131. [CrossRef][PubMed]
    [Google Scholar]
  68. Plant E. P., Rakauskaite R., Taylor D. R., Dinman J. D.. ( 2010;). Achieving a golden mean: mechanisms by which coronaviruses ensure synthesis of the correct stoichiometric ratios of viral proteins. . J Virol 84:, 4330–4340. [CrossRef][PubMed]
    [Google Scholar]
  69. Raaben M., Groot Koerkamp M. J., Rottier P. J., de Haan C. A.. ( 2009a;). Type I interferon receptor-independent and -dependent host transcriptional responses to mouse hepatitis coronavirus infection in vivo. . BMC Genomics 10:, 350. [CrossRef][PubMed]
    [Google Scholar]
  70. Raaben M., Prins H.-J., Martens A. C., Rottier P. J. M., de Haan C. A.. ( 2009b;). Non-invasive imaging of mouse hepatitis coronavirus infection reveals determinants of viral replication and spread in vivo. . Cell Microbiol 11:, 825–841. [CrossRef][PubMed]
    [Google Scholar]
  71. Raj V. S., Smits S. L., Provacia L. B., van den Brand J. M., Wiersma L., Ouwendijk W. J., Bestebroer T. M., Spronken M. I., van Amerongen G.. & other authors ( 2014;). Adenosine deaminase acts as a natural antagonist for dipeptidyl peptidase 4-mediated entry of the Middle East respiratory syndrome coronavirus. . J Virol 88:, 1834–1838. [CrossRef][PubMed]
    [Google Scholar]
  72. Rest J. S., Mindell D. P.. ( 2003;). SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of host-shifting. . Infect Genet Evol 3:, 219–225. [CrossRef][PubMed]
    [Google Scholar]
  73. Roberts A., Paddock C., Vogel L., Butler E., Zaki S., Subbarao K.. ( 2005a;). Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. . J Virol 79:, 5833–5838. [CrossRef][PubMed]
    [Google Scholar]
  74. Roberts A., Vogel L., Guarner J., Hayes N., Murphy B., Zaki S., Subbarao K.. ( 2005b;). Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. . J Virol 79:, 503–511. [CrossRef][PubMed]
    [Google Scholar]
  75. Roberts A., Thomas W. D., Guarner J., Lamirande E. W., Babcock G. J., Greenough T. C., Vogel L., Hayes N., Sullivan J. L.. & other authors ( 2006;). Therapy with a severe acute respiratory syndrome-associated coronavirus-neutralizing human monoclonal antibody reduces disease severity and viral burden in golden Syrian hamsters. . J Infect Dis 193:, 685–692. [CrossRef][PubMed]
    [Google Scholar]
  76. Roberts A., Deming D., Paddock C. D., Cheng A., Yount B., Vogel L., Herman B. D., Sheahan T., Heise M.. & other authors ( 2007;). A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. . PLoS Pathog 3:, e5. [CrossRef][PubMed]
    [Google Scholar]
  77. Rockx B., Baas T., Zornetzer G. A., Haagmans B., Sheahan T., Frieman M., Dyer M. D., Teal T. H., Proll S.. & other authors ( 2009;). Early upregulation of acute respiratory distress syndrome-associated cytokines promotes lethal disease in an aged-mouse model of severe acute respiratory syndrome coronavirus infection. . J Virol 83:, 7062–7074. [CrossRef][PubMed]
    [Google Scholar]
  78. Roth-Cross J. K., Martínez-Sobrido L., Scott E. P., García-Sastre A., Weiss S. R.. ( 2007;). Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. . J Virol 81:, 7189–7199. [CrossRef][PubMed]
    [Google Scholar]
  79. Roth-Cross J. K., Stokes H., Chang G., Chua M. M., Thiel V., Weiss S. R., Gorbalenya A. E., Siddell S. G.. ( 2009;). Organ-specific attenuation of murine hepatitis virus strain A59 by replacement of catalytic residues in the putative viral cyclic phosphodiesterase ns2. . J Virol 83:, 3743–3753. [CrossRef][PubMed]
    [Google Scholar]
  80. Rowe T., Gao G., Hogan R. J., Crystal R. G., Voss T. G., Grant R. L., Bell P., Kobinger G. P., Wivel N. A., Wilson J. M.. ( 2004;). Macaque model for severe acute respiratory syndrome. . J Virol 78:, 11401–11404. [CrossRef][PubMed]
    [Google Scholar]
  81. Sawicki S. G., Sawicki D. L.. ( 1990;). Coronavirus transcription: subgenomic mouse hepatitis virus replicative intermediates function in RNA synthesis. . J Virol 64:, 1050–1056.[PubMed]
    [Google Scholar]
  82. Schaecher S. R., Stabenow J., Oberle C., Schriewer J., Buller R. M., Sagartz J. E., Pekosz A.. ( 2008;). An immunosuppressed Syrian golden hamster model for SARS-CoV infection. . Virology 380:, 312–321. [CrossRef][PubMed]
    [Google Scholar]
  83. Scobey T., Yount B. L., Sims A. C., Donaldson E. F., Agnihothram S. S., Menachery V. D., Graham R. L., Swanstrom J., Bove P. F.. & other authors ( 2013;). Reverse genetics with a full-length infectious cDNA of the Middle East respiratory syndrome coronavirus. . Proc Natl Acad Sci U S A 110:, 16157–16162. [CrossRef][PubMed]
    [Google Scholar]
  84. See H., Wark P.. ( 2008;). Innate immune response to viral infection of the lungs. . Paediatr Respir Rev 9:, 243–250. [CrossRef][PubMed]
    [Google Scholar]
  85. Seok J., Warren H. S., Cuenca A. G., Mindrinos M. N., Baker H. V., Xu W., Richards D. R., McDonald-Smith G. P., Gao H.. & other authors ( 2013;). Genomic responses in mouse models poorly mimic human inflammatory diseases. . Proc Natl Acad Sci U S A 110:, 3507–3512. [CrossRef][PubMed]
    [Google Scholar]
  86. Smits S. L., de Lang A., van den Brand J. M. A., Leijten L. M., van IJcken W. F., Eijkemans M. J. C., van Amerongen G., Kuiken T., Andeweg A. C.. & other authors ( 2010;). Exacerbated innate host response to SARS-CoV in aged non-human primates. . PLoS Pathog 6:, e1000756. [CrossRef][PubMed]
    [Google Scholar]
  87. Subbarao K., McAuliffe J., Vogel L., Fahle G., Fischer S., Tatti K., Packard M., Shieh W. J., Zaki S., Murphy B.. ( 2004;). Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. . J Virol 78:, 3572–3577. [CrossRef][PubMed]
    [Google Scholar]
  88. Tangudu C., Olivares H., Netland J., Perlman S., Gallagher T.. ( 2007;). Severe acute respiratory syndrome coronavirus protein 6 accelerates murine coronavirus infections. . J Virol 81:, 1220–1229. [CrossRef][PubMed]
    [Google Scholar]
  89. Tekes G., Hofmann-Lehmann R., Stallkamp I., Thiel V., Thiel H.-J.. ( 2008;). Genome organization and reverse genetic analysis of a type I feline coronavirus. . J Virol 82:, 1851–1859. [CrossRef][PubMed]
    [Google Scholar]
  90. Thiel V., Herold J., Schelle B., Siddell S. G.. ( 2001;). Infectious RNA transcribed in vitro from a cDNA copy of the human coronavirus genome cloned in vaccinia virus. . J Gen Virol 82:, 1273–1281.[PubMed]
    [Google Scholar]
  91. Tseng C.-T. K., Huang C., Newman P., Wang N., Narayanan K., Watts D. M., Makino S., Packard M. M., Zaki S. R.. & other authors ( 2007;). Severe acute respiratory syndrome coronavirus infection of mice transgenic for the human angiotensin-converting enzyme 2 virus receptor. . J Virol 81:, 1162–1173. [CrossRef][PubMed]
    [Google Scholar]
  92. Tu C., Crameri G., Kong X., Chen J., Sun Y., Yu M., Xiang H., Xia X., Liu S.. & other authors ( 2004;). Antibodies to SARS coronavirus in civets. . Emerg Infect Dis 10:, 2244–2248. [CrossRef][PubMed]
    [Google Scholar]
  93. van den Brand J. M., Haagmans B. L., Leijten L., van Riel D., Martina B. E., Osterhaus A. D., Kuiken T.. ( 2008;). Pathology of experimental SARS coronavirus infection in cats and ferrets. . Vet Pathol 45:, 551–562. [CrossRef][PubMed]
    [Google Scholar]
  94. van den Brand J. M., Haagmans B. L., van Riel D., Osterhaus A. D., Kuiken T.. ( 2014;). The pathology and pathogenesis of experimental severe acute respiratory syndrome and influenza in animal models. . J Comp Pathol 151:, 83–112. [CrossRef][PubMed]
    [Google Scholar]
  95. Vennema H., Heijnen L., Zijderveld A., Horzinek M. C., Spaan W. J.. ( 1990;). Intracellular transport of recombinant coronavirus spike proteins: implications for virus assembly. . J Virol 64:, 339–346.[PubMed]
    [Google Scholar]
  96. Versteeg G. A., Bredenbeek P. J., van den Worm S. H., Spaan W. J.. ( 2007;). Group 2 coronaviruses prevent immediate early interferon induction by protection of viral RNA from host cell recognition. . Virology 361:, 18–26. [CrossRef][PubMed]
    [Google Scholar]
  97. Wang L.-F., Shi Z., Zhang S., Field H., Daszak P., Eaton B. T.. ( 2006;). Review of bats and SARS. . Emerg Infect Dis 12:, 1834–1840. [CrossRef][PubMed]
    [Google Scholar]
  98. Weiss S. R., Leibowitz J. L.. ( 2007;). Pathogenesis of murine coronavirus infections. . In Nidoviruses, pp. 259–279. Edited by Pearlman S., Gallagher T. M., Snijder E. J... Washington, DC:: American Society for Microbiology;.
    [Google Scholar]
  99. Whitman L., Zhou H., Perlman S., Lane T. E.. ( 2009;). IFN-gamma-mediated suppression of coronavirus replication in glial-committed progenitor cells. . Virology 384:, 209–215. [CrossRef][PubMed]
    [Google Scholar]
  100. Wood J. L. N., Leach M., Waldman L., Macgregor H., Fooks A. R., Jones K. E., Restif O., Dechmann D., Hayman D. T. S.. & other authors ( 2012;). A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study. . Philos Trans R Soc Lond B Biol Sci 367:, 2881–2892. [CrossRef][PubMed]
    [Google Scholar]
  101. Wu D., Tu C., Xin C., Xuan H., Meng Q., Liu Y., Yu Y., Guan Y., Jiang Y.. & other authors ( 2005;). Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates. . J Virol 79:, 2620–2625. [CrossRef][PubMed]
    [Google Scholar]
  102. Yao Y., Bao L., Deng W., Xu L., Li F., Lv Q., Yu P., Chen T., Xu Y.. & other authors ( 2014;). An animal model of MERS produced by infection of rhesus macaques with MERS coronavirus. . J Infect Dis 209:, 236–242. [CrossRef][PubMed]
    [Google Scholar]
  103. Yoshikawa T., Hill T., Li K., Peters C. J., Tseng C.-T. K.. ( 2009;). Severe acute respiratory syndrome (SARS) coronavirus-induced lung epithelial cytokines exacerbate SARS pathogenesis by modulating intrinsic functions of monocyte-derived macrophages and dendritic cells. . J Virol 83:, 3039–3048. [CrossRef][PubMed]
    [Google Scholar]
  104. Yoshikawa T., Hill T. E., Yoshikawa N., Popov V. L., Galindo C. L., Garner H. R., Peters C. J., Tseng C.-T. K.. ( 2010;). Dynamic innate immune responses of human bronchial epithelial cells to severe acute respiratory syndrome-associated coronavirus infection. . PLoS ONE 5:, e8729. [CrossRef][PubMed]
    [Google Scholar]
  105. Youn S., Leibowitz J. L., Collisson E. W.. ( 2005;). In vitro assembled, recombinant infectious bronchitis viruses demonstrate that the 5a open reading frame is not essential for replication. . Virology 332:, 206–215. [CrossRef][PubMed]
    [Google Scholar]
  106. Yount B., Curtis K. M., Baric R. S.. ( 2000;). Strategy for systematic assembly of large RNA and DNA genomes: transmissible gastroenteritis virus model. . J Virol 74:, 10600–10611. [CrossRef][PubMed]
    [Google Scholar]
  107. Yount B., Denison M. R., Weiss S. R., Baric R. S.. ( 2002;). Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. . J Virol 76:, 11065–11078. [CrossRef][PubMed]
    [Google Scholar]
  108. Yount B., Curtis K. M., Fritz E. A., Hensley L. E., Jahrling P. B., Prentice E., Denison M. R., Geisbert T. W., Baric R. S.. ( 2003;). Reverse genetics with a full-length infectious cDNA of severe acute respiratory syndrome coronavirus. . Proc Natl Acad Sci U S A 100:, 12995–13000. [CrossRef][PubMed]
    [Google Scholar]
  109. Zhang Y., Li J., Zhan Y., Wu L., Yu X., Zhang W., Ye L., Xu S., Sun R.. & other authors ( 2004;). Analysis of serum cytokines in patients with severe acute respiratory syndrome. . Infect Immun 72:, 4410–4415. [CrossRef][PubMed]
    [Google Scholar]
  110. Zhang C.-Y., Wei J.-F., He S.-H.. ( 2006;). Adaptive evolution of the spike gene of SARS coronavirus: changes in positively selected sites in different epidemic groups. . BMC Microbiol 6:, 88. [CrossRef][PubMed]
    [Google Scholar]
  111. Zhao X., Nicholls J. M., Chen Y.-G.. ( 2008;). Severe acute respiratory syndrome-associated coronavirus nucleocapsid protein interacts with Smad3 and modulates transforming growth factor-beta signaling. . J Biol Chem 283:, 3272–3280. [CrossRef][PubMed]
    [Google Scholar]
  112. Zhao J., Zhao J., Van Rooijen N., Perlman S.. ( 2009;). Evasion by stealth: inefficient immune activation underlies poor T cell response and severe disease in SARS-CoV-infected mice. . PLoS Pathog 5:, e1000636. [CrossRef][PubMed]
    [Google Scholar]
  113. Zhao J. J., Zhao J., Perlman S.. ( 2010;). T cell responses are required for protection from clinical disease and for virus clearance in severe acute respiratory syndrome coronavirus-infected mice. . J Virol 84:, 9318–9325. [CrossRef][PubMed]
    [Google Scholar]
  114. Zhao L., Rose K. M., Elliott R., Van Rooijen N., Weiss S. R.. ( 2011;). Cell-type-specific type I interferon antagonism influences organ tropism of murine coronavirus. . J Virol 85:, 10058–10068. [CrossRef][PubMed]
    [Google Scholar]
  115. Zhao L., Jha B. K., Wu A., Elliott R., Ziebuhr J., Gorbalenya A. E., Silverman R. H., Weiss S. R.. ( 2012;). Antagonism of the interferon-induced OAS–RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. . Cell Host Microbe 11:, 607–616. [CrossRef][PubMed]
    [Google Scholar]
  116. Zhao J., Li K., Wohlford-Lenane C., Agnihothram S. S., Fett C., Zhao J., Gale M. J. Jr, Baric R. S., Enjuanes L.. & other authors ( 2014;). Rapid generation of a mouse model for Middle East respiratory syndrome. . Proc Natl Acad Sci U S A 111:, 4970–4975. [CrossRef][PubMed]
    [Google Scholar]
  117. Zhou W., Wang W., Wang H., Lu R., Tan W.. ( 2013;). First infection by all four non-severe acute respiratory syndrome human coronaviruses takes place during childhood. . BMC Infect Dis 13:, 433. [CrossRef][PubMed]
    [Google Scholar]
  118. Zúñiga S., Sola I., Alonso S., Enjuanes L.. ( 2004;). Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. . J Virol 78:, 980–994. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.069732-0
Loading
/content/journal/jgv/10.1099/vir.0.069732-0
Loading

Data & Media loading...

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error