Abstract
The authors have previously reported that the glycoprotein of the pathogenic Nishigahara strain of rabies virus is required to lethality for adult mice. A cluster region of amino acid substitutions exists at the positions 164 to 303 on the glycoprotein between avirulent and virulent strains. In this study, the authors generated a chimeric strain having the region at the positions 164 to 303 of the glycoprotein derived from the pathogenic Nishigahara strain in the genetic background of the avirulent RC-HL strain. The chimeric R(G 164–303) strain restores the lethality for adult mice. This result clearly shows that the region at the position 164 to 303 of glycoprotein plays an important role in the lethality for adult mice. Moreover, the authors observed that the lethality for adult mice correlated well with the viral growth in a brain but not with the pH-dependent fusion activity in vitro.
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References
Baer GM, Shaddock JH, Quirion R, Dam TV, Lentz TL (1990). Rabies susceptibility and acetylcholine receptor. Lancet 335: 664–665.
Desmezieres E, Maillard AP, Gaudin Y, Tordo N, Perrin P (2003). Differential stability and fusion activity of Lyssavirus glycoprotein trimers. Virus Res 91: 181–187.
Diallo A (1986). Avirulent mutants of the rabies virus: change in site III of the glycoprotein. Ann Rech Vet 17: 3–6.
Dietzschold B, Wiktor TJ, Trojanowski JQ, Macfarlan RI, Wunner WH, Torres-Anjel MJ, Koprowski H (1985). Differences in cell-to-cell spread of pathogenic and apathogenic rabies virus in vivo and in vitro. J Virol 56: 12–18.
Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M, Smith CL, Koprowski H (1983). Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc Natl Acad Sci U S A 80: 70–74.
Durrer P, Gaudin Y, Ruigrok RW, Graf R, Brunner J (1995). Photolabeling identifies a putative fusion domain in the envelope glycoprotein of rabies and vesicular stomatitis viruses. J Biol Chem 270: 17575–17581.
Galelli A, Baloul L, Lafon M (2000). Abortive rabies virus central nervous infection is controlled by T lymphocyte local recruitment and induction of apoptosis. J Neuro-Virol 6: 359–372.
Gaudin Y, Tuffereau C, Durrer P, Brunner J, Flamand A, Ruigrok R (1999). Rabies virus-induced membrane fusion. Mol Membr Biol 16: 21–31.
Goto H, Minamoto N, Ito H, Sugiyama M, Kinjo T, Mannen K, Mifune K, Kawai A (1994). Nucleotide sequence of the nucleoprotein gene of the RC.HL strain of rabies virus, a seed strain used for animal vaccine production in Japan. Virus Genes 8: 91–97.
Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B (1998). Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol 72: 3711–3719.
Ito H, Minamoto N, Watanabe T, Goto H, Rong LT, Sugiyama M, Kinjo T, Mannen K, Mifune K, Konobe T, et al (1994). A unique mutation of glycoprotein gene of the attenuated RC-HL strain of rabies virus, a seed virus used for production of animal vaccine in Japan. Microbiol Immunol 38: 479–482.
Ito N, Kakemizu M, Ito KA, Yamamoto A, Yoshida Y, Sugiyama M, Minamoto N (2001a). A comparison of complete genome sequences of the attenuated RC-HL strain of rabies virus used for production of animal vaccine in Japan, and the parental Nishigahara strain. Microbiol Immunol 45: 51–58.
Ito N, Takayama M, Yamada K, Sugiyama M, Minamoto N (2001b). Rescue of rabies virus from cloned cDNA and identification of the pathogenicity-related gene: glycoprotein gene is associated with virulence for adult mice. J Virol 75: 9121–9128.
Jackson AC (2002). Pathogenesis. In: Rabies. Wunner WH, Jackson AC (eds). San Diego: Academic Press, pp 245–282.
Lafon M (2002). Immunology. In: Rabies. Wunner WH, Jackson AC (eds). San Diego: Academic Press, pp 351–369.
Lentz TL, Burrage TG, Smith AL, Crick J, Tignor GH (1982). Is the acetylcholine receptor a rabies virus receptor? Science 215: 182–184.
Lewis P, Fu Y, Lentz TL (2000). Rabies virus entry at the neuromuscular junction in nerve-muscle cocultures. Muscle Nerve 23: 720–730.
Marcovistz R, Leal EC, Matos DC, Tsiang H (1994). Interferon production and immune response induction in apathogenic rabies virus-infected mice. Acta Virol 38: 193–197.
Mebatsion T (2001). Extensive attenuation of rabies virus by simultaneously modifying the dynein light chain binding site in the P protein and replacing Arg333 in the G protein. J Virol 75: 11496–11502.
Minamoto N, Tanaka H, Hishida M, Goto H, Ito H, Naruse S, Yamamoto K, Sugiyama M, Kinjo T, Mannen K, et al (1994). Linear and conformation-dependent antigenic sites on the nucleoprotein of rabies virus. Microbiol Immunol 38: 449–455.
Montano-Hirose JA, Lafage M, Weber P, Badrane H, Tordo N, Lafon M (1993). Protective activity of a murine monoclonal antibody against European bat lyssavirus 1 (EBL1) infection in mice. Vaccine 11: 1259–1266.
Morimoto K, Hooper DC, Spitsin S, Koprowski H, Dietzschold B (1999). Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J Virol 73: 510–518.
Morimoto K, McGettigan JP, Foley HD, Hooper DC, Dietzschold B, Schnell MJ (2001). Genetic engineering of live rabies vaccines. Vaccine 19: 3543–3551.
Perry LL, Lodmell DL (1991). Role of CD4+ and CD8+ T cells in murine resistance to street rabies virus. J Virol 65: 3429–3434.
Prehaud C, Coulon P, LaFay F, Thiers C, Flamand A (1988). Antigenic site II of the rabies virus glycoprotein: structure and role in viral virulence. J Virol 62: 1–7.
Reed LJ, Müench H (1938). A simple method of estimating fifty percent end points. Am J Hyg 27: 493–497.
Seif I, Coulon P, Rollin PE, Flamand A (1985). Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J Virol 53: 926–934.
Smith JS (1981). Mouse model for abortive rabies infection of the central nervous system. Infect Immun 31: 297–308.
Smith JS, McCelland CL, Reid FL, Baer GM (1982). Dual role of the immune response in street rabiesvirus infection of mice. Infect Immun 35: 213–221.
Sugamata M, Miyazawa M, Mori S, Spangrude GJ, Ewalt LC, Lodmell DL (1992). Paralysis of street rabies virus-infected mice is dependent on T lymphocytes. J Virol 66: 1252–1260.
Theerasurakarn S, Ubol S (1998). Apoptosis induction in brain during the fixed strain of rabies virus infection correlates with onset and severity of illness. J Neuro Virol 4: 407–414.
Tordo N, Poch O, Ermine A, Keith G, Rougeon F (1986). Walking along the rabies genome: Is the large G-L intergenic region a remnant gene? Proc Natl Acad Sci U S A 83: 3914–3918.
Tuffereau C, Leblois H, Benejean J, Coulon P, Lafay F, Flamand A (1989). Arginine or lysine in position 333 of ERA and CVS glycoprotein is necessary for rabies virulence in adult mice. Virology 172: 206–212.
Ubol S, Sukwattanapan C, Maneerat Y (2001). Inducible nitric oxide synthase inhibition delays death of rabies virus-infected mice. J Med Microbiol 50: 238–242.
Weiland F, Cox JH, Meyer S, Dahme E, Reddehase MJ (1992). Rabies virus neuritic paralysis: immunopatho-genesis of nonfatal paralytic rabies. J Virol 66: 5096–5099.
Yan X, Mohankumar PS, Dietzschold B, Schnell MJ, Fu ZF (2002). The rabies virus glycoprotein determines the distribution of different rabies virus strains in the brain. J NeuroVirol 8: 345–352.
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This study was supported in part by Grants-in-Aid for scientific research from the Ministry of Education, Culture, Sports, Science and Technology, Japan (nos. 13556054 and 14656123).
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Takayama-Ito, M., Ito, N., Yamada, K. et al. Region at amino acids 164 to 303 of the rabies virus glycoprotein plays an important role in pathogenicity for adult mice. Journal of NeuroVirology 10, 131–135 (2004). https://doi.org/10.1080/13550280490279799
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DOI: https://doi.org/10.1080/13550280490279799