Complete protection against severe acute respiratory syndrome coronavirus-mediated lethal respiratory disease in aged mice by immunization with a mouse-adapted virus lacking E protein

Journal of Virology

Volumn 87, Issue 12, 2013, Pages 6551-6559

  Fett, Craig ^a   DeDiego, Marta L ^b   Regla Nava, Jose A ^b   Enjuanes, Luis ^b   Perlman, Stanley ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; VIRUS ENVELOPE PROTEIN;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; IMMUNOGENICITY; INFECTION PREVENTION; INFLAMMATORY CELL; LETHALITY; LUNG EDEMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEVERE ACUTE RESPIRATORY SYNDROME; VACCINATION; VIRAL CLEARANCE; VIRUS ATTENUATION; VIRUS VIRULENCE;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; GENE DELETION; HUMANS; IMMUNIZATION; LUNG; MICE; MICE, INBRED BALB C; SARS VIRUS; SEVERE ACUTE RESPIRATORY SYNDROME; SURVIVAL ANALYSIS; VACCINATION; VIRAL ENVELOPE PROTEINS; VIRAL LOAD; VIRAL VACCINES;

ANIMALIA; CORONAVIRUS; MUS; SARS CORONAVIRUS;

EID: 84878553478     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00087-13     Document Type: Article

References (42)

1. Peiris JS, Guan Y, Yuen KY. 2004. Severe acute respiratory syndrome.Nat. Med. 10:S88 -S97.
2. Perlman S, Netland J. 2009. Coronaviruses post-SARS: update on replication and pathogenesis. Nat. Rev. Microbiol. 7:439-450.
3. Hon CC, Lam TY, Shi ZL, Drummond AJ, Yip CW, Zeng F, Lam PY, Leung FC. 2008. Evidence of the recombinant origin of a bat severe acute respiratory syndrome (SARS)-like coronavirus and its implications on the direct ancestor of SARS coronavirus. J. Virol. 82:1819 -1826.
4. Lau SK, Li KS, Huang Y, Shek CT, Tse H, Wang M, Choi GK, Xu H, Lam CS, Guo R, Chan KH, Zheng BJ, Woo PC, Yuen KY. 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.
5. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc. Natl. Acad. Sci. U. S. A. 102:14040 -14045.
6. Lau SK, Woo PC, Li KS, Huang Y, Wang M, Lam CS, Xu H, Guo R, Chan KH, Zheng BJ, Yuen KY. 2007. Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology 367:428-439.
7. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367:1814 -1820.
8. Chen J, Subbarao K. 2007. The immunobiology of SARS. Annu. Rev. Immunol. 25:443-472.
9. Enjuanes L, Dediego ML, Alvarez E, Deming D, Sheahan T, Baric R. 2008. Vaccines to prevent severe acute respiratory syndrome coronavirusinduced disease. Virus Res. 133:45-62.
10. Yang ZY, Werner HC, Kong WP, Leung K, Traggiai E, Lanzavecchia A, Nabel GJ. 2005. Evasion of antibody neutralization in emerging severe acute respiratory syndrome coronaviruses. Proc. Natl. Acad. Sci. U. S. A. 102:797-801.
11. Deming D, Sheahan T, Heise M, Yount B, Davis N, Sims A, Suthar M, Harkema J, Whitmore A, Pickles R, West A, Donaldson E, Curtis K, Johnston R, Baric R. 2006. Vaccine efficacy in senescent mice challenged with recombinant SARS-CoV bearing epidemic and zoonotic spike variants. PLoS Med. 3:e525. doi:10.1371/journal.pmed.0030525.
12. Oh H-L, Gan S, Bertoletti A, Tan Y-J. 2012. Understanding the T cell immune response in SARS coronavirus infection. Emerg. Microbes Infect. 1:e23-e28.
13. Yasui F, Kai C, Kitabatake M, Inoue S, Yoneda M, Yokochi S, Kase R, Sekiguchi S, Morita K, Hishima T, Suzuki H, Karamatsu K, Yasutomi Y, Shida H, Kidokoro M, Mizuno K, Matsushima K, Kohara M. 2008. Prior immunization with severe acute respiratory syndrome (SARS)-associated coronavirus (SARS-CoV) nucleocapsid protein causes severe pneumonia in mice infected with SARS-CoV. J. Immunol. 181:6337-6348.
14. Masters PS. 2006. The molecular biology of coronaviruses. Adv. Virus Res. 66:193-292.
15. DeDiego ML, Alvarez E, Almazan F, Rejas MT, Lamirande E, Roberts A, Shieh WJ, Zaki SR, Subbarao K, Enjuanes L. 2007. A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J. Virol. 81:1701-1713.
16. Yount B, Roberts RS, Lindesmith L, Baric RS. 2006. Rewiring the severe acute respiratory syndrome coronavirus (SARS-CoV) transcription circuit: engineering a recombination-resistant genome. Proc. Natl. Acad. Sci. U. S. A. 103:12546 -12551.
17. DeDiego ML, Pewe L, Alvarez E, Rejas MT, Perlman S, Enjuanes L. 2008. Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376:379 -389.
18. Kuo L, Masters PS. 2003. The small envelope protein E is not essential for murine coronavirus replication. J. Virol. 77:4597-4608.
19. Lamirande EW, DeDiego ML, Roberts A, Jackson JP, Alvarez E, Sheahan T, Shieh WJ, Zaki SR, Baric R, Enjuanes L, Subbarao K. 2008. A live attenuated severe acute respiratory syndrome coronavirus is immunogenic and efficacious in golden Syrian hamsters. J. Virol. 82:7721-7724.
20. Netland J, DeDiego ML, Zhao J, Fett C, Alvarez E, Nieto-Torres JL, Enjuanes L, Perlman S. 2010. Immunization with an attenuated severe acute respiratory syndrome coronavirus deleted in E protein protects against lethal respiratory disease. Virology 399:120 -128.
21. McCray PB, Jr, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD, Meyerholz DK, Kirby P, Look DC, Perlman S. 2007. Lethal infection in K18-hACE2 mice infected with SARS-CoV. J. Virol. 81:813-821.
22. Roberts A, Paddock C, Vogel L, Butler E, Zaki S, Subbarao K. 2005. Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J. Virol. 79:5833-5838.
23. Subbarao K, Roberts A. 2006. Is there an ideal animal model for SARS? Trends Microbiol. 14:299 -303.
24. Roberts A, Deming D, Paddock CD, Cheng A, Yount B, Vogel L, Herman BD, Sheahan T, Heise M, Genrich GL, Zaki SR, Baric R, Subbarao K. 2007. A mouse-adapted SARS-coronavirus causes disease and mortality in BALB/c mice. PLoS Pathog. 3:e5. doi:10.1371/journal .ppat.0030005.
25. Sheahan T, Whitmore A, Long K, Ferris M, Rockx B, Funkhouser W, Donaldson E, Gralinski L, Collier M, Heise M, Davis N, Johnston R, Baric RS. 2011. Successful vaccination strategies that protect aged mice from lethal challenge from influenza virus and heterologous severe acute respiratory syndrome coronavirus. J. Virol. 85:217-230.
26. Zhao J, Zhao J, Legge K, Perlman S. 2011. Age-related increases in PGD(2) expression impair respiratory DC migration, resulting in diminished T cell responses upon respiratory virus infection in mice. J. Clin. Invest. 121:4921-4930.
27. Almazan F, Dediego ML, Galan C, Escors D, Alvarez E, Ortego J, Sola I, Zuniga S, Alonso S, Moreno JL, Nogales A, Capiscol C, Enjuanes L. 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.
28. 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. doi:10.1371/journal.ppat.1000636.
29. Wu GF, Dandekar AA, Pewe L, Perlman S. 2000. CD4 and CD8 T cells have redundant but not identical roles in virus-induced demyelination. J. Immunol. 165:2278 -2286.
30. Houtman JJ, Fleming JO. 1996. Dissociation of demyelination and viral clearance in congenitally immunodeficient mice infected with murine coronavirus JHM. J. Neurovirol. 2:101-110.
31. + T cells. J. Virol. 64:4589-4592.
32. Ramakrishna C, Stohlman SA, Atkinson RD, Shlomchik MJ, Bergmann CC. 2002. Mechanisms of central nervous system viral persistence: the critical role of antibody and B cells. J. Immunol. 168:1204 -1211.
33. Kamitani W, Narayanan K, Huang C, Lokugamage K, Ikegami T, Ito N, Kubo H, Makino S. 2006. Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc. Natl. Acad. Sci. U. S. A. 103:12885-12890.
34. Narayanan K, Huang C, Lokugamage K, Kamitani W, Ikegami T, Tseng CT, Makino S. 2008. Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J. Virol. 82:4471-4479.
35. Zust R, Cervantes-Barragan L, Kuri T, Blakqori G, Weber F, Ludewig B, Thiel V. 2007. Coronavirus non-structural protein 1 is a major pathogenicity factor: implications for the rational design of coronavirus vaccines. PLoS Pathog. 3:e109. doi:10.1371/journal.ppat.0030109.
36. Graham RL, Becker MM, Eckerle LD, Bolles M, Denison MR, Baric RS. 2012. A live, impaired-fidelity coronavirus vaccine protects in an aged, immunocompromised mouse model of lethal disease. Nat. Med. 18: 1820-1826.
37. Yu X, Bi W, Weiss SR, Leibowitz JL. 1994. Mouse hepatitis virus gene 5b protein is a new virion envelope protein. Virology 202:1018 -1023.
38. Ortego J, Ceriani JE, Patino C, Plana J, Enjuanes L. 2007. Absence of E protein arrests transmissible gastroenteritis coronavirus maturation in the secretory pathway. Virology 368:296-308.
39. Nieto-Torres JL, Dediego ML, Alvarez E, Jimenez-Guardeno JM, Regla-Nava JA, Llorente M, Kremer L, Shuo S, Enjuanes L. 2011. Subcellular location and topology of severe acute respiratory syndrome coronavirus envelope protein. Virology 415:69-82.
40. Pervushin K, Tan E, Parthasarathy K, Lin X, Jiang FL, Yu D, Vararattanavech A, Soong TW, Liu DX, Torres J. 2009. Structure and inhibition of the SARS coronavirus envelope protein ion channel. PLoS Pathog. 5:e1000511. doi:10.1371/journal.ppat.1000511.
41. Verdia-Baguena C, Nieto-Torres JL, Alcaraz A, DeDiego ML, Torres J, Aguilella VM, Enjuanes L. 2012. Coronavirus E protein forms ion channels with functionally and structurally-involved membrane lipids. Virology 432:485-494.
42. DeDiego ML, Nieto-Torres JL, Jimenez-Guardeno JM, Regla-Nava JA, Alvarez E, Oliveros JC, Zhao J, Fett C, Perlman S, Enjuanes L. 2011.Severe acute respiratory syndrome coronavirus envelope protein regulates cell stress response and apoptosis. PLoS Pathog. 7:e1002315. doi:10.1371 /journal.ppat.1002315.