Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 20, Number 5—May 2014
Research

Molecular Characterization of Cryptically Circulating Rabies Virus from Ferret Badgers, Taiwan

Hue-Ying Chiou, Chia-Hung Hsieh, Chian-Ren Jeng, Fang-Tse Chan, Hurng-Yi Wang, and Victor Fei PangComments to Author 
Author affiliations: National Taiwan University, Taipei, Taiwan, Republic of China (H.-Y. Chiou, C.-H. Hsieh, C.-R. Jeng, H.-Y. Wang, V.F. Pang); Council of Agriculture, Executive Yuan, Nantou County, Taiwan, Republic of China (F.-T. Chan)

Main Article

Figure 5

Maximum-likelihood trees of rabies virus based on (A) nucleoprotein and (B) glycoprotein gene sequences. Numbers on the branches are estimated divergences (above) and their 95% highest posterior density (below). The divergence time between different viral lineages and time to the most recent common ancestor of virus isolates were estimated by using an established Bayesian Markov chain Monte Carlo approach implemented in BEAST version 1.7 (21). The substitution rate was assumed to be 4.3 × 10–4 (

Figure 5. Maximum-likelihood trees of rabies virus based on (A) nucleoprotein and (B) glycoprotein gene sequencesNumbers on the branches are estimated divergences (above) and their 95% highest posterior density (below)The divergence time between different viral lineages and time to the most recent common ancestor of virus isolates were estimated by using an established Bayesian Markov chain Monte Carlo approach implemented in BEAST version 1.7 (21)The substitution rate was assumed to be 4.3 × 10–4 (range 3.1–6.6 × 10–4) or 2.3 × 10–4 (range 1.1–3.6 × 10–4)/sites/year (hatched numbers) for nucleoprotein (N) and 3.9 × 10–4 (1.2–6.5 × 10–4)/sites/year for glycoprotein (G) genes (17,23)The analysis was performed by using the general time-reversible model of nucleotide substitution, assuming an uncorrelated lognormal molecular clock (22)TW1955 is the only isolate from a shrew that is very close to TW1614 collected from the same area, suggesting that TW1955 was a spillover from a ferret badger (see also Figure 1)Scale bar indicates nucleotide substitutions per site.

Main Article

References
  1. Jackson  AC. Pathogenesis. In: Jackson AC, Wunner WH, editors. Rabies. London: Elsevier Academic Press; 2007.
  2. World Health Organization. WHO Expert Consultation on Rabies: second report. Geneva. Organization. 2013;•••:1139.
  3. Wandeler  A. Virus infections of non-domestic carnivores: rabies virus. In: Appel MJ, editor. Virus infections of carnivores. Amsterdam: Elsevier Science Publishers; 1987. p. 449–61.
  4. Barnard  BJH. The role played by wildlife in the epizootiology of rabies in South Africa and South-West Africa. Onderstepoort J Vet Res. 1979;46:15563 .PubMedGoogle Scholar
  5. Smith  GC, Wilkinson  D. Modelling disease spread in a novel host: rabies in the European badger Meles meles. J Appl Ecol. 2002;39:86574. DOIGoogle Scholar
  6. Wandeler  A, Wachendorfer  G, Forster  U, Krekel  H, Muller  J, Steck  F. Rabies in wild carnivores in central Europe. II. Virological and serological examinations. Zentralbl Veterinarmed B. 1974;21:75764 . DOIPubMedGoogle Scholar
  7. Liu  Y, Zhang  SF, Wu  XF, Zhao  JH, Hou  YL, Zhang  F, Ferret badger rabies origin and its revisited importance as potential source of rabies transmission in southeast China. BMC Infect Dis. 2010;10:234. DOIPubMedGoogle Scholar
  8. Zhenyu  G, Zhen  W, Enfu  C, Fan  H, Junfen  L, Yixin  L, Human rabies cluster following badger bites, People’s Republic of China. Emerg Infect Dis. 2007;13:19567. DOIPubMedGoogle Scholar
  9. Zhang  S, Tang  Q, Wu  XF, Liu  Y, Zhang  F, Rupprecht  CE, Rabies in ferret badgers, southeastern China. Emerg Infect Dis. 2009;15:9469 . DOIPubMedGoogle Scholar
  10. Lei  YL, Wang  XG, Liu  FM, Chen  XY, Ye  BF, Mei  JH, Complete genome sequencing and analyses of rabies viruses isolated from wild animals (Chinese ferret-badger) in Zhejiang Province [in Chinese]. Zhonghua Liu Xing Bing Xue Za Zhi. 2009;30:8248 .PubMedGoogle Scholar
  11. Thompson  JD, Higgins  DG, Gibson  TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:467380. DOIPubMedGoogle Scholar
  12. Tamura  K, Peterson  D, Peterson  N, Stecher  G, Nei  M, Kumar  S. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:27319. DOIPubMedGoogle Scholar
  13. Librado  P, Rozas  J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:14512. DOIPubMedGoogle Scholar
  14. Tajima  F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123:58595 .PubMedGoogle Scholar
  15. Fu  YX, Li  WH. Statistical tests of neutrality of mutations. Genetics. 1993;133:693709 .PubMedGoogle Scholar
  16. He  CQ, Meng  SL, Yan  HY, Ding  NZ, He  HB, Yan  JX, Isolation and identification of a novel rabies virus lineage in China with natural recombinant nucleoprotein gene. PLoS ONE. 2012;7:e49992. DOIPubMedGoogle Scholar
  17. Bourhy  H, Reynes  JM, Dunham  EJ, Dacheux  L, Larrous  F, Huong  VT, The origin and phylogeography of dog rabies virus. J Gen Virol. 2008;89:267381. DOIPubMedGoogle Scholar
  18. Guindon  S, Gascuel  O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696704. DOIPubMedGoogle Scholar
  19. Posada  D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25:12536. DOIPubMedGoogle Scholar
  20. Ronquist  F, Huelsenbeck  JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:15724. DOIPubMedGoogle Scholar
  21. Drummond  AJ, Suchard  MA, Xie  D, Rambaut  A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:196973. DOIPubMedGoogle Scholar
  22. Drummond  AJ, Ho  SY, Phillips  MJ, Rambaut  A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006;4:e88. DOIPubMedGoogle Scholar
  23. Meng  S, Sun  Y, Wu  X, Tang  J, Xu  G, Lei  Y, Evolutionary dynamics of rabies viruses highlights the importance of China rabies transmission in Asia. Virology. 2011;410:4039. DOIPubMedGoogle Scholar
  24. Kissi  B, Tordo  N, Bourhy  H. Genetic polymorphism in the rabies virus nucleoprotein gene. Virology. 1995;209:52637. DOIPubMedGoogle Scholar
  25. Mebatsion  T, Weiland  F, Conzelmann  KK. Matrix protein of rabies virus is responsible for the assembly and budding of bullet-shaped particles and interacts with the transmembrane spike glycoprotein G. J Virol. 1999;73:24250 .PubMedGoogle Scholar
  26. Finke  S, Mueller-Waldeck  R, Conzelmann  KK. Rabies virus matrix protein regulates the balance of virus transcription and replication. J Gen Virol. 2003;84:161321. DOIPubMedGoogle Scholar
  27. Kassis  R, Larrous  F, Estaquier  J, Bourhy  H. Lyssavirus matrix protein induces apoptosis by a TRAIL-dependent mechanism involving caspase-8 activation. J Virol. 2004;78:654355. DOIPubMedGoogle Scholar
  28. Lentz  TL, Wilson  PT, Hawrot  E, Speicher  DW. Amino acid sequence similarity between rabies virus glycoprotein and snake venom curaremimetic neurotoxins. Science. 1984;226:8478. DOIPubMedGoogle Scholar
  29. Poch  O, Blumberg  BM, Bougueleret  L, Tordo  N. Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. J Gen Virol. 1990;71:115362. DOIPubMedGoogle Scholar
  30. Kuzmin  IV, Wu  X, Tordo  N, Rupprecht  CE. Complete genomes of Aravan, Khujand, Irkut and West Caucasian bat viruses, with special attention to the polymerase gene and non-coding regions. Virus Res. 2008;136:8190. DOIPubMedGoogle Scholar
  31. Zhang  S, Zhao  J, Liu  Y, Fooks  AR, Zhang  F, Hu  R. Characterization of a rabies virus isolate from a ferret badger (Melogale moschata) with unique molecular differences in glycoprotein antigenic site III. Virus Res. 2010;149:14351. DOIPubMedGoogle Scholar
  32. Gong  W, Jiang  Y, Za  Y, Zeng  Z, Shao  M, Fan  J, Temporal and spatial dynamics of rabies viruses in China and Southeast Asia. Virus Res. 2010;150:1118. DOIPubMedGoogle Scholar
  33. Saito  M, Oshitani  H, Orbina  JR, Tohma  K, de Guzman  AS, Kamigaki  T, Genetic diversity and geographic distribution of genetically distinct rabies viruses in the Philippines. PLoS Negl Trop Dis. 2013;7:e2144. DOIPubMedGoogle Scholar
  34. Streicker  DG, Lemey  P, Velasco-Villa  A, Rupprecht  CE. Rates of viral evolution are linked to host geography in bat rabies. PLoS Pathog. 2012;8:e1002720. DOIPubMedGoogle Scholar
  35. Biek  R, Henderson  JC, Waller  LA, Rupprecht  CE, Real  LA. A high-resolution genetic signature of demographic and spatial expansion in epizootic rabies virus. Proc Natl Acad Sci U S A. 2007;104:79938. DOIPubMedGoogle Scholar
  36. Faber  M, Faber  ML, Papaneri  A, Bette  M, Weihe  E, Dietzschold  B, A single amino acid change in rabies virus glycoprotein increases virus spread and enhances virus pathogenicity. J Virol. 2005;79:141418. DOIPubMedGoogle Scholar
  37. Faber  M, Li  J, Kean  RB, Hooper  DC, Alugupalli  KR, Dietzschold  B. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc Natl Acad Sci U S A. 2009;106:113005. DOIPubMedGoogle Scholar
  38. Lafon  M. Rabies virus receptors. J Neurovirol. 2005;11:827. DOIPubMedGoogle Scholar
  39. Tuffereau  C, Schmidt  K, Langevin  C, Lafay  F, Dechant  G, Koltzenburg  M. The rabies virus glycoprotein receptor p75NTR is not essential for rabies virus infection. J Virol. 2007;81:1362230. DOIPubMedGoogle Scholar
  40. Kuzmin  IV, Shi  M, Orciari  LA, Yager  PA, Velasco-Villa  A, Kuzmina  NA, Molecular inferences suggest multiple host shifts of rabies viruses from bats to mesocarnivores in Arizona during 2001–2009. PLoS Pathog. 2012;8:e1002786 . DOIPubMedGoogle Scholar

Main Article

1Joint senior authors who contributed equally to this article.

Page created: April 16, 2014
Page updated: April 16, 2014
Page reviewed: April 16, 2014
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external