Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated

Virology

Volumn 347, Issue 2, 2006, Pages 410-421

  Butler, Noah ^a   Pewe, Lecia ^b   Trandem, Kathryn ^b   Perlman, Stanley ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Coronavirus; Encephalitis; Rodent model

Indexed keywords

GLYCOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN; CELL GROWTH; CONTROLLED STUDY; CORONAVIRUS; CORRELATION ANALYSIS; ENCEPHALITIS; HUMAN; HUMAN CELL; IMMUNE MEDIATED INJURY; MALE; MAMMAL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT GROWTH; PLASTICITY; PRIORITY JOURNAL; SARS CORONAVIRUS; SPECIES DIFFERENCE; TISSUE CULTURE CELL; VIRUS INFECTION; VIRUS ISOLATION; VIRUS VIRULENCE;

ANIMALS; CELL LINE; CORONAVIRUS INFECTIONS; CORONAVIRUS OC43, HUMAN; ENCEPHALITIS, VIRAL; HUMANS; MICE; MICE, INBRED C57BL; SPECIES SPECIFICITY; SPINAL CORD;

ANIMALIA; AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS; MAMMALIA; MURINAE; RODENTIA; SARS CORONAVIRUS;

EID: 33646028491     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2005.11.044     Document Type: Article

References (58)

1. Akashi H., Inaba Y., Miura Y., Sato K., Tokuhisa S., Asagi M., and Hayashi Y. Propagation of the Kakegawa strain of bovine coronavirus in suckling mice, rats and hamsters. Arch. Virol. 67 4 (1981) 367-370
2. Barthold S.W., de Souza M.S., and Smith A.L. Susceptibility of laboratory mice to intranasal and contact infection with coronaviruses of other species. Lab. Anim. Sci. 40 5 (1990) 481-485
3. Bergmann C.C., Altman J.D., Hinton D., and Stohlman S.A. Inverted immunodominance and impaired cytolytic function of CD8+T cells during viral persistence in the central nervous system. J. Immunol. 163 (1999) 3379-3387
4. Binder G.K., and Griffin D.E. Interferon-gamma-mediated site-specific clearance of alphavirus from CNS neurons. Science 293 5528 (2001) 303-306
5. Byrnes A.P., and Griffin D.E. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72 9 (1998) 7349-7356
6. Chinese SARS Molecular Epidemiology Consortium. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303 5664 (2004) 1666-1669
7. Collins A.R. HLA class I antigen serves as a receptor for human coronavirus OC43. Immunol. Invest. 22 (1993) 95-105
8. Drosten C., Gunther S., Preiser W., van der Werf S., Brodt H.R., Becker S., Rabenau H., Panning M., Kolesnikova L., Fouchier R.A., Berger A., Burguiere A.M., Cinatl J., Eickmann M., Escriou N., Grywna K., Kramme S., Manuguerra J.C., Muller S., Rickerts V., Sturmer M., Vieth S., Klenk H.D., Osterhaus A.D., Schmitz H., and Doerr H.W. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348 (2003) 1967-1976
9. Fouchier R.A., Kuiken T., Schutten M., van Amerongen G., van Doornum G.J., van den Hoogen B.G., Peiris M., Lim W., Stohr K., and Osterhaus A.D. Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423 (2003) 240
10. Gallagher T.M., and Buchmeier M.J. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279 2 (2001) 371-374
11. Gu J., Gong E., Zhang B., Zheng J., Gao Z., Zhong Y., Zou W., Zhan J., Wang S., Xie Z., Zhuang H., Wu B., Zhong H., Shao H., Fang W., Gao D., Pei F., Li X., He Z., Xu D., Shi X., Anderson V.M., and Leong A.S. Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 202 (2005) 415-424
12. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., Luo S.W., Li P.H., Zhang L.J., Guan Y.J., Butt K.M., Wong K.L., Chan K.W., Lim W., Shortridge K.F., Yuen K.Y., Peiris J.S., and Poon L.L. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 302 (2003) 276-278
13. Haring J.S., Pewe L.L., and Perlman S. High-magnitude, virus-specific CD4 T-cell response in the central nervous system of coronavirus-infected mice. J. Virol. 75 6 (2001) 3043-3047
14. Jacomy H., and Talbot P.J. Susceptibility of murine CNS to OC43 infection. Adv. Exp. Med. Biol. 494 (2001) 101-107
15. Jacomy H., and Talbot P.J. Vacuolating encephalitis in mice infected by human coronavirus OC43. Virology 315 1 (2003) 20-33
16. Jeffers S.A., Tusell S.M., Gillim-Ross L., Hemmila E.M., Achenbach J.E., Babcock G.J., Thomas Jr. W.D., Thackray L.B., Young M.D., Mason R.J., Ambrosino D.M., Wentworth D.E., Demartini J.C., and Holmes K.V. CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. U.S.A. 101 44 (2004) 15748-15753
17. Joly E., and Oldstone M.B. Neuronal cells are deficient in loading peptides onto MHC class I molecules. Neuron 8 6 (1992) 1185-1190
18. Kan B., Wang M., Jing H., Xu H., Jiang X., Yan M., Liang W., Zheng H., Wan K., Liu Q., Cui B., Xu Y., Zhang E., Wang H., Ye J., Li G., Li M., Cui Z., Qi X., Chen K., Du L., Gao K., Zhao Y.T., Zou X.Z., Feng Y.J., Gao Y.F., Hai R., Yu D., Guan Y., and Xu J. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J. Virol. 79 18 (2005) 11892-11900
19. Klimstra W.B., Ryman K.D., and Johnston R.E. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72 9 (1998) 7357-7366
20. Kunkel F., and Herrler G. Bovine coronavirus hemagglutinin protein. Virus Res. 2 (1993) 53-61
21. Kunkel F., and Herrler G. Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 195 1 (1993) 195-202
22. Kunkel F., and Herrler G. Structural and functional analysis of the S proteins of two human coronavirus OC43 strains adapted to growth in different cells. Arch. Virol. 141 6 (1996) 1123-1131
23. Lassnig C., Sanchez C.M., Egerbacher M., Walter I., Majer S., Kolbe T., Pallares P., Enjuanes L., and Muller M. Development of a transgenic mouse model susceptible to human coronavirus 229E. Proc. Natl. Acad. Sci. U.S.A. (2005)
24. Li W., Moore M.J., Vasilieva N., Sui J., Wong S.K., Berne M.A., Somasundaran M., Sullivan J.L., Luzuriaga K., Greenough T.C., Choe H., and Farzan M. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426 6965 (2003) 450-454
25. Li W., Zhang C., Sui J., Kuhn J.H., Moore M.J., Luo S., Wong S.K., Huang I.C., Xu K., Vasilieva N., Murakami A., He Y., Marasco W.A., Guan Y., Choe H., and Farzan M. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J. 24 8 (2005) 1634-1643
26. Marzi A., Gramberg T., Simmons G., Moller P., Rennekamp A.J., Krumbiegel M., Geier M., Eisemann J., Turza N., Saunier B., Steinkasserer A., Becker S., Bates P., Hofmann H., and Pohlmann S. DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J. Virol. 78 21 (2004) 12090-12095
27. McIntosh K., Becker W.B., and Chanock R.M. Growth in suckling-mouse brain of "IBV-like" viruses from patients with upper respiratory tract disease. Proc. Natl. Acad. Sci. U.S.A. 58 (1967) 2268-2273
28. Medana I.M., Gallimore A., Oxenius A., Martinic M.M., Wekerle H., and Neumann H. MHC class I-restricted killing of neurons by virus-specific CD8+T lymphocytes is effected through the Fas/FasL, but not the perforin pathway. Eur. J. Immunol. 30 12 (2000) 3623-3633
29. Mounir S., and Talbot P.J. Molecular characterization of the S protein gene of human coronavirus OC43. J. Gen. Virol. 74 (1993) 1981-1987
30. Neumann H., Cavalie A., Jenne D., and Wekerle H. Induction of MHC class I genes in neurons. Science 269 (1995) 549-552
31. Neumann H., Schmidt H., Cavalie A., Jenne D., and Wekerle H. Major histocompatibility complex (MHC) class I gene expression in single neurons of the central nervous system: differential regulation by interferon (IFN)-gamma and tumor necrosis factor (TNF)-alpha. J. Exp. Med. 185 (1997) 305-316
32. Peiris J.S., Guan Y., and Yuen K.Y. Severe acute respiratory syndrome. Nat. Med. 10 12 Suppl. (2004) S88-S97
33. Perlman S., Jacobsen G., and Afifi A. Spread of a neurotropic murine coronavirus into the CNS via the trigeminal and olfactory nerves. Virology 170 (1989) 556-560
34. Perlman S., Evans G., and Afifi A. Effect of olfactory bulb ablation on spread of a neurotropic coronavirus into the mouse brain. J. Exp. Med. 172 (1990) 1127-1132
35. Pewe L., Haring J., and Perlman S. CD4 T-cell-mediated demyelination is increased in the absence of gamma interferon in mice infected with mouse hepatitis virus. J. Virol. 76 (2002) 7329-7333
36. Pewe L., Zhou H., Netland J., Tangadu C., Olivares H., Shi L., Look D., Gallagher T.M., and Perlman S. A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J. Virol. 79 (2005) 11335-11342
37. Phillips J.J., Chua M.M., Lavi E., and Weiss S.R. Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J. Virol. 73 (1999) 7752-7760
38. Reddi H.V., and Lipton H.L. Heparan sulfate mediates infection of high-neurovirulence Theiler's viruses. J. Virol. 76 16 (2002) 8400-8407
39. Saeki K., Ohtsuka N., and Taguchi F. Identification of spike protein residues of murine coronavirus responsible for receptor-binding activity by use of soluble receptor-resistant mutants. J. Virol. 71 12 (1997) 9024-9031
40. Schultze B., and Herrler G. Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J. Gen. Virol. 73 (1992) 901-906
41. Song H.D., Tu C.C., Zhang G.W., Wang S.Y., Zheng K., Lei L.C., Chen Q.X., Gao Y.W., Zhou H.Q., Xiang H., Zheng H.J., Chern S.W., Cheng F., Pan C.M., Xuan H., Chen S.J., Luo H.M., Zhou D.H., Liu Y.F., He J.F., Qin P.Z., Li L.H., Ren Y.Q., Liang W.J., Yu Y.D., Anderson L., Wang M., Xu R.H., Wu X.W., Zheng H.Y., Chen J.D., Liang G., Gao Y., Liao M., Fang L., Jiang L.Y., Li H., Chen F., Di B., He L.J., Lin J.Y., Tong S., Kong X., Du L., Hao P., Tang H., Bernini A., Yu X.J., Spiga O., Guo Z.M., Pan H.Y., He W.Z., Manuguerra J.C., Fontanet A., Danchin A., Niccolai N., Li Y.X., Wu C.I., and Zhao G.P. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc. Natl. Acad. Sci. U.S.A. 102 7 (2005) 2430-2435
42. Stauber R., Pfleidera M., and Siddell S. Proteolytic cleavage of the murine coronavirus surface glycoprotein is not required for fusion activity. J. Gen. Virol. 74 (1993) 183-191
43. St-Jean J.R., Jacomy H., Desforges M., Vabret A., Freymuth F., and Talbot P.J. Human respiratory coronavirus OC43: genetic stability and neuroinvasion. J. Virol. 78 16 (2004) 8824-8834
44. Stohlman S.A., Bergmann C.C., Lin M.T., Cua D.J., and Hinton D.R. CTL effector function within the central nervous system requires CD4+T Cells. J. Immunol. 160 (1998) 2896-2904
45. Taguchi F. Fusion formation by the uncleaved spike protein of murine coronavirus JHMV variant cl-2. J. Virol. 67 (1993) 1195-1202
46. Taguchi F., Siddell S., Wege H., and ter Meulen V. Characterization of a variant virus selected in rat brains after infection by coronavirus MHV JHM. J. Virol. 54 (1985) 429-435
47. Thorp E.B., and Gallagher T.M. Diversity of coronavirus spikes: relationship to pathogen entry and dissemination. In: Fischer W. (Ed). Viral membrane Proteins: Structure, function and Drug Design (2004), Kluwer Academic/Plenum Publishers, New York
48. Tsai J.C., de Groot L., Pinon J.D., Iacono K.T., Phillips J.J., Seo S.H., Lavi E., and Weiss S.R. Amino acid substitutions within the heptad repeat domain 1 of murine coronavirus spike protein restrict viral antigen spread in the central nervous system. Virology 312 2 (2003) 369-380
49. Vabret A., Mourez T., Gouarin S., Petitjean J., and Freymuth F. An outbreak of coronavirus OC43 respiratory infection in Normandy, France. Clin. Infect. Dis. 36 (2003) 985-989
50. van der Hoek L., Pyrc K., Jebbink M.F., Vermeulen-Oost W., Berkhout R.J., Wolthers K.C., Wertheim-van Dillen P.M., Kaandorp J., Spaargaren J., and Berkhout B. Identification of a new human coronavirus. Nat. Med. 10 4 (2004) 368-373
51. Vijgen L., Keyaerts E., Lemey P., Moes E., Li S., Vandamme A.M., and Van Ranst M. Circulation of genetically distinct contemporary human coronavirus OC43 strains. Virology 337 1 (2005) 85-92
52. Vijgen L., Keyaerts E., Moes E., Thoelen I., Wollants E., Lemey P., Vandamme A.M., and Van Ranst M. Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event. J. Virol. 79 3 (2005) 1595-1604
53. Vlasak R., Luytjes W., Spaan W., and Palese P. Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 4526-4529
54. Wentworth D.E., Tresnan D.B., Turner B.C., Lerman I.R., Bullis B., Hemmila E.M., Levis R., Shapiro L.H., and Holmes K.V. Cells of human aminopeptidase N (CD13) transgenic mice are infected by human coronavirus-229E in vitro, but not in vivo. Virology 335 2 (2005) 185-197
55. Woo P.C., Lau S.K., Chu C.M., Chan K.H., Tsoi H.W., Huang Y., Wong B.H., Poon R.W., Cai J.J., Luk W.K., Poon L.L., Wong S.S., Guan Y., Peiris J.S., and Yuen K.Y. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79 2 (2005) 884-895
56. Wu G.F., Dandekar A.A., Pewe L., and Perlman S. CD4 and CD8 T cells have redundant but not identical roles in virus-induced demyelination. J. Immunol. 165 (2000) 2278-2286
57. Xiao X., Chakraborti S., Dimitrov A.S., Gramatikoff K., and Dimitrov D.S. The SARS-CoV S glycoprotein: expression and functional characterization. Biochem. Biophys. Res. Commun. 312 4 (2003) 1159-1164
58. Zhang X.M., Kousoulas K.G., and Storz J. Comparison of the nucleotide and deduced amino acid sequences of the S genes specified by virulent and avirulent strains of bovine coronaviruses. Virology 183 1 (1991) 397-404