Abstract
Rabies is a global problem, but its impact and prevalence vary across different regions. In some areas, such as parts of Africa and Asia, the virus is prevalent in the domestic dog population, leading to epidemic waves and large numbers of human fatalities. In other regions, such as the Americas, the virus predominates in wildlife and bat populations, with sporadic spillover into domestic animals. In this work, we attempted to investigate whether these distinct environments led to selective pressures that result in measurable changes within the genome at the amino acid level. To this end, we collected and sequenced the full genome of two isolates from divergent environments. The first isolate (DRV-AH08) was from China, where the virus is present in the dog population and the country is experiencing a serious epidemic. The second isolate (DRV-Mexico) was taken from Mexico, where the virus is present in both wildlife and domestic dog populations, but at low levels as a consequence of an effective vaccination program. We then combined and compared these with other full genome sequences to identify distinct amino acid changes that might be associated with environment. Phylogenetic analysis identified strain DRV-AH08 as belonging to the China-I lineage, which has emerged to become the dominant lineage in the current epidemic. The Mexico strain was placed in the D11 Mexico lineage, associated with the West USA-Mexico border clade. Amino acid sequence analysis identified only 17 amino acid differences in the N, G and L proteins. These differences may be associated with virus replication and virulence–for example, the short incubation period observed in the current epidemic in China.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anilionis A, Wunner WH, Curtis PJ (1981) Structure of the glycoprotein gene in rabies virus. Nature 294:275–278
Badrane H, Bahloul C, Perrin P, Tordo N (2001) Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75:3268–3276
Badrane H, Tordo N (2001) Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders. J Virol 75:8096–8104
Bourhy H, Kissi B, Audry L, Smreczak M, Sadkowska-Todys M, Kulonen K, Tordo N, Zmudzinski JF, Holmes EC (1999) Ecology and evolution of rabies virus in Europe. J Gen Virol 80(Pt 10):2545–2557
Bourhy H, Reynes JM, Dunham EJ, Dacheux L, Larrous F, Huong VT, Xu G, Yan J, Miranda ME, Holmes EC (2008) The origin and phylogeography of dog rabies virus. J Gen Virol 89:2673–2681
Bourhy H, Dautry-Varsat A, Hotez PJ, Salomon J (2010) Rabies, still neglected after 125 years of vaccination. PLoS Negl Trop Dis 4:e839
Davis PL, Bourhy H, Holmes EC (2006) The evolutionary history and dynamics of bat rabies virus. Infect Genet Evol 6:464–473
Dietzschold B, Morimoto K, Hooper DC, Smith JS, Rupprecht CE, Koprowski H (2000) Genotypic and phenotypic diversity of rabies virus variants involved in human rabies: implications for postexposure prophylaxis. J Hum Virol 3:50–57
Fu ZF (1997) Rabies and rabies research: past, present and future. Vaccine 15(Suppl):S20–S24
Henderson JC, Biek R, Hanlon CA, O’Dee S, Real LA (2008) Rabies virus in raccoons, Ohio, 2004. Emerg Infect Dis 14:650–652
Hirano S, Itou T, Shibuya H, Kashiwazaki Y, Sakai T (2005) Molecular epidemiology of rabies virus isolates in Uganda. Virus Res 147:135–138
Holmes EC, Woelk CH, Kassis R, Bourhy H (2002) Genetic constraints and the adaptive evolution of rabies virus in nature. Virology 292:247–257
Hughes GJ, Orciari LA, Rupprecht CE (2005) Evolutionary timescale of rabies virus adaptation to North American bats inferred from the substitution rate of the nucleoprotein gene. J Gen Virol 86:1467–1474
Ito N, Takayama M, Yamada K, Sugiyama M, Minamoto N (2001) 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
Ito N, Takayama-Ito M, Yamada K, Hosokawa J, Sugiyama M, Minamoto N (2003) Improved recovery of rabies virus from cloned cDNA using a vaccinia virus-free reverse genetics system. Microbiol Immunol 47:613–617
Kakkar M, Venkataramanan V, Krishnan S, Chauhan RS, Abbas SS (2012) Moving from rabies research to rabies control: lessons from India. PLoS Negl Trop Dis 6:e1748
Kissi B, Tordo N, Bourhy H (1995) Genetic polymorphism in the rabies virus nucleoprotein gene. Virology 209:526–537
Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, Miranda ME, Shaw A, Zinsstag J, Meslin FX (2005) Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83:360–368
Kuzmin IV, Orciari LA, Arai YT, Smith JS, Hanlon CA, Kameoka Y, Rupprecht CE (2003) Bat lyssaviruses (Aravan and Khujand) from Central Asia: phylogenetic relationships according to N, P and G gene sequences. Virus Res 97:65–79
Kuzmin IV, Shi M, Orciari LA, Yager PA, Velasco-Villa A, Kuzmina NA, Streicker DG, Bergman DL, Rupprecht CE (2012) Molecular inferences suggest multiple host shifts of rabies viruses from bats to mesocarnivores in Arizona during 2001–2009. PLoS Pathog 8:e1002786
Meng SL, Yan JX, Xu GL, Nadin-Davis SA, Ming PG, Liu SY, Wu J, Ming HT, Zhu FC, Zhou DJ, Xiao QY, Dong GM, Yang XM (2007) A molecular epidemiological study targeting the glycoprotein gene of rabies virus isolates from China. Virus Res 124:125–138
Morimoto K, Foley HD, McGettigan JP, Schnell MJ, Dietzschold B (2000) Reinvestigation of the role of the rabies virus glycoprotein in viral pathogenesis using a reverse genetics approach. J Neurovirol 6:373–381
Nadin-Davis SA, Sampath MI, Casey GA, Tinline RR, Wandeler AI (1999) Phylogeographic patterns exhibited by Ontario rabies virus variants. Epidemiol Infect 123:325–336
Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics Chapter 6: Unit 6 5
Takayama-Ito M, Ito N, Yamada K, Sugiyama M, Minamoto N (2006) Multiple amino acids in the glycoprotein of rabies virus are responsible for pathogenicity in adult mice. Virus Res 115:169–175
Tao X, Han N, Guo Z, Tang Q, Rayner S, Liang G (2013) Molecular characterization of China human rabies vaccine strains. Virol Sin 28(2):116–123
Velasco-Villa A, Orciari LA, Souza V, Juarez-Islas V, Gomez-Sierra M, Castillo A, Flisser A, Rupprecht CE (2005) Molecular epizootiology of rabies associated with terrestrial carnivores in Mexico. Virus Res 111:13–27
Velasco-Villa A, Orciari LA, Juarez-Islas V, Gomez-Sierra M, Padilla-Medina I, Flisser A, Souza V, Castillo A, Franka R, Escalante-Mane M, Sauri-Gonzalez I, Rupprecht CE (2006) Molecular diversity of rabies viruses associated with bats in Mexico and other countries of the Americas. J Clin Microbiol 44:1697–1710
Velasco-Villa A, Reeder SA, Orciari LA, Yager PA, Franka R, Blanton JD, Zuckero L, Hunt P, Oertli EH, Robinson LE, Rupprecht CE (2008) Enzootic rabies elimination from dogs and reemergence in wild terrestrial carnivores, United States. Emerg Infect Dis 14:1849–1854
Wunner WH, Larson JK, Dietzschold B, Smith CL (1988) The molecular biology of rabies viruses. Rev Infect Dis 10(Suppl 4):S771–S784
Xue X, Zheng X, Gai W, Liang H, Ma J, Li L, Wang T, Feng N, Huang G, Zhao Y, Yang S, Xia X (2010) Sequencing the complete genome of rabies virus CVS-11 strain and constructing its full-length infectious cDNA clone. Wei Sheng Wu Xue Bao 53:409–415
Yin CP, Zhou H, Wu H, Tao XY, Rayner S, Wang SM, Tang Q, Liang GD (2012) Analysis on factors related to rabies epidemic in China from 2007–2011. Virol Sin 27:132–143
Yu F, Zhang G, Xiao S, Fang L, Xu G, Yan J, Chen H, Fu ZF (2012) Complete genome sequence of a street rabies virus isolated from a rabid dog in China. J Virol 86:10890–10891
Yu J, Li H, Tang Q, Rayner S, Han N, Guo Z, Liu H, Adams J, Fang W, Tao X, Wang S, Liang G (2012) The spatial and temporal dynamics of rabies in China. PLoS Negl Trop Dis 6:e1640
Zhang G, Fu ZF (2012) Complete genome sequence of a street rabies virus from Mexico. J Virol 86:10892–10893
Zhang YZ, Xiong CL, Xiao DL, Jiang RJ, Wang ZX, Zhang LZ, Fu ZF (2005) Human rabies in China. Emerg Infect Dis 11:1983–1984
Zhang YZ, Xiong CL, Zou Y, Wang DM, Jiang RJ, Xiao QY, Hao ZY, Zhang LZ, Yu YX, Fu ZF (2006) Molecular characterization of rabies virus isolates in China during 2004. Virus Res 121:179–188
Acknowledgements
This work was supported partially by Public Health Service grant AI-051560 from the National Institute of Allergy and Infectious Diseases, USA, and a grant from the Natural Science Foundation of China (30928020).
Author information
Authors and Affiliations
Corresponding authors
Additional information
F. Yu and G. Zhang contributed equally to this paper.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yu, F., Zhang, G., Zhong, X. et al. Comparison of complete genome sequences of dog rabies viruses isolated from China and Mexico reveals key amino acid changes that may be associated with virus replication and virulence. Arch Virol 159, 1593–1601 (2014). https://doi.org/10.1007/s00705-013-1966-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-013-1966-2