Expression of hemagglutinin esterase protein from recombinant mouse hepatitis virus enhances neurovirulence

Journal of Virology

Volumn 79, Issue 24, 2005, Pages 15064-15073

  Kazi, Lubna ^a   Lissenberg, Arjen ^b   Watson, Richard ^a   De Groot, Raoul J ^b   Weiss, Susan R ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; ESTERASE; HEMAGGLUTININ; HEMAGGLUTININ ESTERASE; RECEPTOR; RECEPTOR BINDING PROTEIN; S RECEPTOR; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS SPIKE PROTEIN;

ADOLESCENT; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DEMYELINATING DISEASE; ENZYME ACTIVITY; HEPATITIS; MALE; MEMBRANE FUSION; MOUSE; MURINE HEPATITIS CORONAVIRUS; MURINE HEPATITIS CORONAVIRUS A59; MURINE HEPATITIS CORONAVIRUS JHM; NEUROTROPISM; NEUROVIRULENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; VIRUS ENCEPHALITIS; VIRUS GENE; VIRUS INFECTION; VIRUS PATHOGENESIS; VIRUS RECOMBINANT; VIRUS S GENE; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; CELL LINE; HEMAGGLUTININS, VIRAL; MICE; MURINE HEPATITIS VIRUS; RECEPTORS, VIRUS; RECOMBINANT PROTEINS; VIRAL FUSION PROTEINS; VIRAL PROTEINS; VIRULENCE;

ANIMALIA; MURINE HEPATITIS VIRUS;

EID: 29744436856     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.24.15064-15073.2005     Document Type: Article

References (63)

1. Bond, C. W., J. L. Leibowitz, and J. A. Robb. 1979. Pathogenic murine coronaviruses. II. Characterization of virus-specific proteins of murine coronaviruses JHMV and A59V. Virology 94:371-384.
2. Bosch, B. J., R. van der Zee, C. A. de Haan, and P. J. Rottier. 2003. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J. Virol. 77:8801-8811.
3. Brian, D. A., B. G. Hogue, and T. E. Kienzle. 1995. The coronavirus hemagglutinin esterase glycoprotein, p. 165-179. In S. C. Siddell (ed.), The coronaviridae. Plenum Press, New York, N.Y.
4. Bridger, J. C., E. O. Caul, and S. I. Egglestone. 1978. Replication of an enteric bovine coronavirus in intestinal organ cultures. Arch. Virol. 57:43-51.
5. Cavanagh, D. 1995. The coronavirus surface glycoprotein, p. 73-113. In S. G. Siddell (ed.), The coronaviridae. Plenum Press, New York, N.Y.
6. Cornelissen, L. A., C. M. Wierda, F. J. van der Meer, A. A. Herrewegh, M. C. Horzinek, H. F. Egberink, and R. J. de Groot. 1997. Hemaggiutinin-esterase, a novel structural protein of torovirus. J. Virol. 71:5277-5286.
7. Das Sarma, J., L. Fu, S. T. Hingley, M. M. Lai, and E. Lavi. 2001. Sequence analysis of the S gene of recombinant MHV-2/A59 coronaviruses reveals three candidate mutations associated with demyelination and hepatitis. J. Neurovirol. 7:432-436.
8. Duckmanton, L. M., R. Tellier, P. Liu, and M. Petric. 1998. Bovine torovirus: sequencing of the structural genes and expression of the nucleocapsid protein of Breda virus. Virus Res. 58:83-96.
9. Dveksler, G. S., C. W. Dieffenbach, C. B. Cardellichio, K. McCuaig, M. N. Pensiero, G. S. Jiang, N. Beauchemin, and K. V. Holmes. 1993. Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. J. Virol. 67:1-8.
10. Fouchier, R. A., N. G. Hartwig, T. M. Bestebroer, B. Niemeyer, J. C. de Jong, J. H. Simon, and A. D. Osterhaus. 2004. A previously undescribed coronavirus associated with respiratory disease in humans. Proc. Natl. Acad. Sci. USA 101:6212-6216.
11. Gagneten, S., O. Gout, M. Dubois-Dalcq, P. Rottier, J. Rossen, and K. V. Holmes. 1995. Interaction of mouse hepatitis virus (MHV) spike glycoprotein with receptor glycoprotein MHVR is required for infection with an MHV strain that expresses the hemagglutinin-esterase glycoprotein. J. Virol. 69:889-895.
12. Gallagher, T. M., and M. J. Buchmeier. 2001. Coronavirus spike proteins in viral entry and pathogenesis. Virology 279:371-374.
13. Gombold, J. L., S. T. Hingley, and S. R. Weiss. 1993. Fusion-defective mutants of mouse hepatitis virus A59 contain a mutation in the spike protein cleavage signal. J. Virol. 67:4504-4512.
14. Herrler, G., and H. D. Klenk. 1991. Structure and function of the HEF glycoprotein of influenza C virus. Adv. Virus Res. 40:213-234.
15. Hingley, S. T., J. L. Gombold, E. Lavi, and S. R. Weiss. 1994. MHV-A59 fusion mutants are attenuated and display altered hepatotropism. Virology 200:1-10.
16. Ksiazek, T. G., D. Erdman, C. S. Goldsmith, S. R. Zaki, T. Peret, S. Emery, S. Tong, C. Urbani, J. A. Comer, W. Lim, P. E. Rollin, S. F. Dowell, A. E. Ling, C. D. Humphrey, W. J. Shieh, J. Guarner, C. D. Paddock, P. Rota, B. Fields, J. DeRisi, J. Y. Yang, N. Cox, J. M. Hughes, J. W. LeDuc, W. J. Bellini, and L. J. Anderson. 2003. A novel coronavirus associated with severe acute respiratory syndrome. N. Engl. J. Med. 348:1953-1966.
17. Künkel, F., and G. Herrler. 1993. Structural and functional analysis of the surface protein of human coronavirus OC43. Virology 195:195-202.
18. Kuo, L., G. J. Godeke, M. J. Raamsman, P. S. Masters, and P. J. Rottier. 2000. Retargeting of coronavirus by substitution of the spike glycoprotein ectodomain: crossing the host cell species barrier. J. Virol. 74:1393-1406.
19. LaMonica, N., L. R. Banner, V. L. Morris, and M. M. C. Lai. 1991. Localization of extensive deletions in the structural genes of two neurotropic variants of murine coronavirus JHM. Virology 182:883-888.
20. Lavi, E., D. H. Gilden, M. K. Highkin, and S. R. Weiss. 1984. MHV-A59 pathogenesis in mice. Adv. Exp. Med. Biol. 173:237-245.
21. Lavi, E., D. H. Gilden, M. K. Highkin, and S. R. Weiss. 1986. The organ tropism of mouse hepatitis virus A59 in mice is dependent on dose and route of inoculation. Lab. Anim. Sci. 36:130-135.
22. Lavi, E., D. H. Gilden, Z. Wroblewska, L. B. Rorke, and S. R. Weiss. 1984. Experimental demyelination produced by the A59 strain of mouse hepatitis virus. Neurology 34:597-603.
23. Leparc-Goffart, I., S. T. Hingley, M. M. Chua, X. Jiang, E. Lavi, and S. R. Weiss. 1997. Altered pathogenesis of a mutant of the murine coronavirus MHV-A59 is associated with a Q159L amino acid substitution in the spike protein. Virology 239:1-10.
24. 23a. Lissenberg, A., M. M. Vrolijk, A. L. W. van Vliet, M. A. Langereis, J. D. F. de Groot-Mijnes, P. J. M. Rottier, and R. J. de Groot. 2005. Luxury at a cost? Recombinant mouse hepatitis viruses expressing the accessory hemagglutinin esterase protein display reduced fitness in vitro. J. Virol. 79:15054-15063.
25. Luytjes, W., P. J. Bredenbeek, A. F. Noten, M. C. Horzinek, and W. J. Spaan. 1988. Sequence of mouse hepatitis virus A59 mRNA 2: indications for RNA recombination between coronaviruses and influenza C virus. Virology 166:415-422.
26. + T cells prevent murine coronavirus spread to the spinal cord and subsequent demyelination. J. Virol. 79:3370-3381.
27. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
28. Masters, P. S., and P. J. Rottier. 2005. Coronavirus reverse genetics by targeted RNA recombination. Curr. Top. Microbiol. Immunol. 287:133-159.
29. Navas, S., S. H. Seo, M. M. Chua, J. Das Sarma, S. T. Hingley, E. Lavi, and S. R. Weiss. 2001. Role of the spike protein in murine coronavirus induced hepatitis: an in vivo study using targeted RNA recombination. Adv. Exp. Med. Biol. 494:139-144.
30. Navas, S., S. H. Seo, M. M. Chua, J. D. Sarma, E. Lavi, S. T. Hingley, and S. R. Weiss. 2001. Murine coronavirus spike protein determines the ability of the virus to replicate in the liver and cause hepatitis. J. Virol. 75:2452-2457.
31. Navas, S., and S. R. Weiss. 2003. Murine coronavirus-induced hepatitis: JHM genetic background eliminates A59 spike-determined hepatotropism. J. Virol. 77:4972-4978.
32. Pfleiderer, M., E. Routledge, G. Herrler, and S. G. Siddell. 1991. High level transient expression of the murine coronavirus haemagglutinin-esterase. J. Gen. Virol. 72:1309-1315.
33. Phillips, J. J., M. M. Chua, E. Lavi, and S. R. Weiss. 1999. Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J. Virol. 73:7752-7760.
34. Phillips, J. J., M. M. Chua, G. F. Rall, and S. R. Weiss. 2002. Murine coronavirus spike glycoprotein mediates degree of viral spread, inflammation, and virus-induced immunopathology in the central nervous system. Virology 301:109-120.
35. Phillips, J. J., and S. R. Weiss. 2001. MHV neuropathogenesis: the study of chimeric S genes and mutations in the hypervariable region. Adv. Exp. Med. Biol. 494:115-119.
36. Popova, R., and X. Zhang. 2002. The spike but not the hemagglutinin/esterase protein of bovine coronavirus is necessary and sufficient for viral infection. Virology 294:222-236.
37. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent points. Am. J. Hyg. 27:493-497.
38. Regl, G., A. Kaser, M. Iwersen, H. Schmid, G. Kohla, B. Strobl, U. Vilas, R. Schauer, and R. Vlasak. 1999. The hemagglutinin-esterase of mouse hepatitis virus strain S is a sialate-4-O-acetylesterase. J. Virol. 73:4721-4727.
39. Rempel, J. D., and M. J. Buchmeier. 2001. Analysis of CNS inflammatory responses to MHV. Role of spike determinants in initiating chemokine and cytokine responses. Adv. Exp. Med. Biol. 494:77-82.
40. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M. H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Gunther, A. D. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
41. Rottier, P. J. M., M. C. Horzinek, and B. A. M. van der Zeijst. 1981. Viral protein synthesis in mouse hepatitis virus strain A59-infected cells. J. Virol. 40:350-357.
42. Schultze, B., H. J. Gross, R. Brossmer, and G. Herrler. 1991. The S protein of bovine coronavirus is a hemagglutinin recognizing 9-O-acetylated sialic acid as a receptor determinant. J. Virol. 65:6232-6237.
43. Schultze, B., K. Wahn, H. D. Klenk, and G. Herrler. 1991. Isolated HE-protein from hemagglutinating encephalomyelitis virus and bovine coronavirus has receptor-destroying and receptor-binding activity. Virology 180:221-228.
44. Shieh, C. K., H. J. Lee, K. Yokomori, N. La Monica, S. Makino, and M. M. Lai. 1989. Identification of a new transcriptional initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome. J. Virol. 63:3729-3736.
45. Smits, S. L., G. J. Gerwig, A. L. van Vliet, A. Lissenberg, P. Briza, J. P. Kamerling, R. Vlasak, and R. J. de Groot. 2005. Nidovirus sialate-O-acetyl-esterases: evolution and substrate specificity of corona- and toroviral receptor-destroying enzymes. J. Biol. Chem. 280:6933-6941.
46. Smits, S. L., A. Lavazza, K. Matiz, M. C. Horzinek, M. P. Koopmans, and R. J. de Groot. 2003. Phylogenetic and evolutionary relationships among torovirus field variants: evidence for multiple intertypic recombination events. J. Virol. 77:9567-9577.
47. Snijder, E. J., J. A. den Boon, M. C. Horzinek, and W. J. Spaan. 1991. Comparison of the genome organization of toro- and coronaviruses: evidence for two nonhomologous RNA recombination events during Berne virus evolution. Virology 180:448-452.
48. Sugiyama, K., M. Kasai, S. Kato, H. Kasai, and K. Hatakeyama. 1998. Haemagglutinin-esterase protein (HE) of murine corona virus: DVIM (diarrhea virus of infant mice). Arch. Virol. 143:1523-1534.
49. Taguchi, F., M. Aiuchi, and K. Fujiwara. 1977. Age-dependent response of mice to a mouse hepatitis virus, MHV-S. Jpn. J. Exp. Med. 47:109-115.
50. Taguchi, F., P. T. Massa, and V. ter Meulen. 1986. Characterization of a variant virus isolated from neural cell culture after infection of mouse coronavirus JHMV. Virology 155:267-270.
51. Tsai, J. C., L. de Groot, J. D. Pinon, K. T. Iacono, J. J. Phillips, S. H. Seo, E. Lavi, and S. R. Weiss. 2003. Amino acid substitutions within the heptad repeat domain 1 of murine coronavirus spike protein restrict viral antigen spread in the central nervous system. Virology 312:369-380.
52. van der Hoek, L., K. Pyre, M. F. Jebbink, W. Vermeulen-Oost, R. J. M. Berkhout, K. C. Wolthers, P. M. E. Wertheim-van Dillen, J. Kaandorp, J. Spaargaren, and B. Berkhout. 2004. Identification of a new human coronavirus. Nat. Med. 10:368-373.
53. Vlasak, R., W. Luytjes, J. Leider, W. Spaan, and P. Palese. 1988. The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activity. J. Virol. 62:4686-4690.
54. Vlasak, R., W. Luytjes, W. Spaan, and P. Palese. 1988. Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc. Natl. Acad. Sci. USA 85:4526-4529.
55. Vlasak, R., T. Muster, A. M. Lauro, and P. Palese. 1989. Influenza C virus esterase: analysis of catalytic site, inhibition, and possible function. J. Virol. 63:2056-2062.
56. Wagaman, P. C., H. A. Spence, and R. J. O'Callaghan. 1989. Detection of influenza C virus by using an in situ esterase assay. J. Clin. Microbiol. 27:832-836.
57. Woo, P. C., S. K. Lau, C. M. Chu, K. H. Chan, H. W. Tsoi, Y. Huang, B. H. Wong, R. W. Poon, J. J. Cai, W. K. Luk, L. L. Poon, S. S. Wong, Y. Guan, J. S. Peiris, and K. Y. Yuen. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J. Virol. 79:884-895.
58. Wurzer, W. J., K. Obojes, and R. Vlasak. 2002. The sialate-4-O- acetylesterases of coronaviruses related to mouse hepatitis virus: a proposal to reorganize group 2 Coronaviridae. J. Gen. Virol. 83:395-402.
59. Yokomori, K., M. Asanaka, S. A. Stohlman, S. Makino, R. A. Shubin, W. Gilmore, L. P. Weiner, F. I. Wang, and M. M. Lai. 1995. Neuropathogenicity of mouse hepatitis virus JHM isolates differing in hemagglutinin-esterase protein expression. J. Neurovirol. 1:330-339.
60. Yokomori, K., L. R. Banner, and M. M. Lai. 1991. Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses. Virology 183:647-657.
61. Yokomori, K., S. A. Stohlman, and M. M. Lai. 1993. The detection and characterization of multiple hemagglutinin-esterase (HE)-defective viruses in the mouse brain during subacute demyelination induced by mouse hepatitis virus. Virology 192:170-178.
62. Yoo, D., F. L. Graham, L. Prevec, M. D. Parker, M. Benko, T. Zamb, and L. A. Babiuk. 1992. Synthesis and processing of the haemagglutinin-esterase glycoprotein of bovine coronavirus encoded in the E3 region of adenovirus. J. Gen. Virol. 73:2591-2600.
63. Zhang, X., D. R. Hinton, S. Park, B. Parra, C. L. Liao, M. M. Lai, and S. A. Stohlman. 1998. Expression of hemagglutinin/esterase by a mouse hepatitis virus coronavirus defective-interfering RNA alters viral pathogenesis. Virology 242:170-183.