1887

Abstract

Nearly 1.7 million cases of dog bites are reported every year in India and many cases of animal rabies are left unattended and undiagnosed. Therefore, a mere diagnosis of rabies is not sufficient to understand the epidemiology and the spread of the rabies virus (RV) in animals. There is a paucity of information about the evolutionary dynamics of RV in dogs and its biodiversity patterns in India. In total, 50 dog-brain samples suspected of rabies were screened by the nucleoprotein- (N) and glycoprotein- (G) gene PCR. The N and G genes were subsequently sequenced to understand the molecular evolution in these genes. The phylogenetic analysis of the N gene revealed that six isolates in the Mumbai region belonged to a single Arctic lineage. Time-scaled phylogeny by Bayesian coalescent analysis of the partial N gene revealed that the time to the most recent common ancestor (TMRCA) for the sequences belonged to the cluster from 2006.68 with a highest posterior density of 95 % betweeen 2005–2008, which is assigned to Indian lineage I. Migration pattern revealed a strong Bayes factor between Mumbai to Delhi, Panji to Hyderabad, Delhi to Chennai, and Chennai to Chandigarh. Phylogenetic analysis of the G gene revealed that the RVs circulating in the Mumbai region are divided into three lineages. Time-scaled phylogeny by the Bayesian coalescent analysis method estimated that the TMRCA for sequences under study was from 1993 and Indian clusters was from 1962. In conclusion, the phylogenetic analysis of the N gene revealed that six isolates belonged to single Arctic lineages along with other Indian isolates and they were clustered into a single lineage but divided into three clades based on the G-gene sequences. The present study highlights and enhances the current molecular epidemiology and evolution of RV and revealed strong location bias and geographical clustering within Indian isolates on the basis of N and G genes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001521
2021-02-05
2021-02-26
Loading full text...

Full text loading...

References

  1. Fooks AR, Cliquet F, Finke S, Freuling C. Nature Revi. Dis Primers 2017; 3: 1 19
    [Google Scholar]
  2. Sumitra D. Dog bite cases up 20% in Mumbai, rabies death worries BMC, Mumbai, The Times of India- City News –Mumbai. 2019 1 6
  3. Tordo N, Poch O, Ermine A, Keith G, Rougeon F. Walking along the rabies genome: is the large GL intergenic region a remnant gene?. Proc Natl Acad Sci U S A 1986; 83: 3914 3918 [CrossRef]
    [Google Scholar]
  4. Badrane H, Bahloul C, Perrin P, Tordo N. Evidence of two lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 2001; 75: 3268 3276 [CrossRef] [PubMed]
    [Google Scholar]
  5. Nadin-Davis SA, Turner G, Paul JPV, Madhusudana SN, Wandeler AI. Emergence of Arctic-like rabies lineage in India. Emerg Infect Dis 2007; 13: 111 116 [CrossRef] [PubMed]
    [Google Scholar]
  6. Nagarajan T, Mohanasubramanian B, Seshagiri EV, Nagendrakumar SB, Saseendranath MR et al. Molecular epidemiology of rabies virus isolates in India. J Clin Microbiol 2006; 44: 3218 3224 [CrossRef] [PubMed]
    [Google Scholar]
  7. Reddy GM, Singh R, Singh RP, Singh KP, Gupta PK et al. Molecular characterization of Indian rabies virus isolates by partial sequencing of nucleoprotein (N) and phosphoprotein (P) genes. Virus Genes 2011; 43: 13 17 [CrossRef] [PubMed]
    [Google Scholar]
  8. Arai YT, Yamada K, Kameoka Y, Horimoto T, Yamamoto K et al. Nucleoprotein gene analysis of fixed and street rabies virus variants using RT-PCR. Arch Virol 1997; 142: 1787 1796 [CrossRef] [PubMed]
    [Google Scholar]
  9. Kamolvarin N, Tirawatnpong T, Rattanasiwamoke R, Tirawatnpong S, Panpanich T et al. Diagnosis of rabies by polymerase chain reaction with nested primers. J Infect Dis 1993; 167: 207 210 [CrossRef] [PubMed]
    [Google Scholar]
  10. Sacramento D, Bourhy H, Tordo N. PCR technique as an alternative method for diagnosis and molecular epidemiology of rabies virus. Mol Cell Probes 1991; 5: 229 240 [CrossRef] [PubMed]
    [Google Scholar]
  11. Johnson N, Vos A, Freuling C, Tordo N, Fooks AR et al. Human rabies due to lyssavirus infection of bat origin. Vet Microbiol 2010; 142: 151 159 [CrossRef] [PubMed]
    [Google Scholar]
  12. Cherian S, Singh R, Singh KP, Manjunatha Reddy GB et al. Phylogenetic analysis of Indian rabies virus isolates targeting the complete glycoprotein gene. Infect Genet Evol 2015; 36: 333 338 [CrossRef] [PubMed]
    [Google Scholar]
  13. Mahadevan A, Suja MS, Mani RS, Shankar SK. Perspectives in diagnosis and treatment of rabies viral encephalitis: insights from pathogenesis. Neurotherapeutics 2016; 13: 477 492 [CrossRef] [PubMed]
    [Google Scholar]
  14. Rabies WH WHO. General Aspect & Laboratory Diagnosis Techniques New Delhi: WHO Collaborating Centre for Rabies; 2007
    [Google Scholar]
  15. Meslin FX, Kaplan MM, Koprowisk H. Laboratory techniques in rabies. Geneva: World Health Organization; 1996. & FERNANDES, MEB-Virological and serological diagnosis of rabies in bats from an urban area in the Brazilian Amazon. Rev Inst Med Trop Sao Paulo 2015; 57: 497 503
    [Google Scholar]
  16. Nagaraj T, Vasanth JP, Desai A, Kamat A, Madhusudana SN et al. Ante mortem diagnosis of human rabies using saliva samples: comparison of real time and conventional RT-PCR techniques. J Clin Virol 2006; 36: 17 23 [CrossRef] [PubMed]
    [Google Scholar]
  17. Nadin-Davis SA. Polymerase chain reaction protocols for rabies virus discrimination. J Virol Methods 1998; 75: 1 8 [CrossRef] [PubMed]
    [Google Scholar]
  18. Gupta PK, Chaturvedi VK, Verma PC, Pandey KD. Differentiation of rabies fixed and street viruses using RT-PCR coupled with restriction endonuclease analysis. Indian J. of Biotech 2005; 4: 284 286
    [Google Scholar]
  19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215: 403 410 [CrossRef] [PubMed]
    [Google Scholar]
  20. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32: 1792 1797 [CrossRef] [PubMed]
    [Google Scholar]
  21. Tamura K, Peterson D, Peterson N, Stecher G, Nei M et al. mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731 2739 [CrossRef] [PubMed]
    [Google Scholar]
  22. Nagarajan T, Nagendrakumar SB, Mohanasubramanian B, Rajalakshmi S, Hanumantha NR et al. Phylogenetic analysis of nucleoprotein gene of dog rabies virus isolates from southern India. Infect Genet Evol 2009; 9: 976 982 [CrossRef] [PubMed]
    [Google Scholar]
  23. Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 2006; 23: 254 267 [CrossRef] [PubMed]
    [Google Scholar]
  24. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. InNucleic acids symposium series 1999; 41: 95 98
    [Google Scholar]
  25. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM et al. UCSF Chimera--a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605 1612 [CrossRef] [PubMed]
    [Google Scholar]
  26. Drummond AJ, Rambaut A. Beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7: 214 [CrossRef] [PubMed]
    [Google Scholar]
  27. Rambaut A. FigTree V1. 4.2, a graphical viewer of phylogenetic trees. 2014
  28. Sharp PM, Tuohy TM, Mosurski KR. Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 1986; 14: 5125 5143 [CrossRef] [PubMed]
    [Google Scholar]
  29. Nagaraja T, Madhusudana S, Desai A. Molecular characterization of the full-length genome of a rabies virus isolate from India. Virus Genes 2008; 36: 449 459 [CrossRef] [PubMed]
    [Google Scholar]
  30. Reddy GBM, Sumana K, Shankar BP, Patil SS, Rahman H. Diagnosis and molecular phylogeny of rabies virus obtained from an Indian wolf. Indian J Vet Pathol 2015; 39: 290 292 [CrossRef]
    [Google Scholar]
  31. Sagar KS. Molecular Charcterization of the Nuckeoprotein (N) Gene of Rabies Virus. M.v.sc Thesis Submitted To Nagpur, Maharashtra: Maharashtra Animal and Fishery Sciences University; 2013
    [Google Scholar]
  32. Mehta S, Samant L, Chowdhary A. Computational modeling and in silico characterization of rabies virus glycoprotein and nucleoprotein. Int J Pharm Res 2014; 6: 39
    [Google Scholar]
  33. Albagi SOA, Ahmed OH, Gumaa MA, Abd elrahman KA, Abu Haraz AH et al. Immunoinformatics-Peptide driven vaccine and In silico modeling for Duvenhage rabies virus glycoprotein G. J Clin Cell Immunol 2017; 08: 517 [CrossRef]
    [Google Scholar]
  34. He C-Q, Meng S-L, Yan H-Y, Ding N-Z, He H-B et al. Isolation and identification of a novel rabies virus lineage in China with natural recombinant nucleoprotein gene. PLoS One 2012; 7: e49992 [CrossRef] [PubMed]
    [Google Scholar]
  35. Denduangboripant J, Wacharapluesadee S, Lumlertdacha B, Ruankaew N, Hoonsuwan W et al. Transmission dynamics of rabies virus in Thailand: implications for disease control. BMC Infect Dis 2005; 5: 52 [CrossRef] [PubMed]
    [Google Scholar]
  36. Zhang JM, Zhang ZS, Deng YQ, Wu S-L, Wang W et al. Incidence of human rabies and characterization of rabies virus nucleoprotein gene in dogs in Fujian Province, Southeast China, 2002-2012. BMC Infect Dis 2017; 17: 599 [CrossRef] [PubMed]
    [Google Scholar]
  37. Smith J, McElhinney L, Parsons G, Brink N, Doherty T et al. Case report: rapid ante-mortem diagnosis of a human case of rabies imported into the UK from the Philippines. J Med Virol 2003; 69: 150 155 [CrossRef] [PubMed]
    [Google Scholar]
  38. Tao L, Ge J, Wang X, Zhai H, Hua T et al. Molecular basis of neurovirulence of flury rabies virus vaccine strains: importance of the polymerase and the glycoprotein R333Q mutation. J Virol 2010; 84: 8926 8936 [CrossRef] [PubMed]
    [Google Scholar]
  39. Singh CK, Ahmad A. Molecular approach for ante-mortem diagnosis of rabies in dogs. Indian J Med Res 2018; 147: 513 [CrossRef] [PubMed]
    [Google Scholar]
  40. Bourhy H, Kissi B, Audry L, Smreczak M, Sadkowska-Todys M et al. Ecology and evolution of rabies virus in Europe. J Gen Virol 1999; 80 (Pt 10: 2545 2557 [CrossRef] [PubMed]
    [Google Scholar]
  41. Sato G, Kobayashi Y, Shoji Y, Sato T, Itou T et al. Molecular epidemiology of rabies from Maranhão and surrounding states in the northeastern region of Brazil. Arch Virol 2006; 151: 2243 2251 [CrossRef] [PubMed]
    [Google Scholar]
  42. Jayakumar R, Tirumurugaan KG, Ganga G, Kumanan K, Mahalinga Nainar A. Characterization of nucleoprotein gene sequence of an Indian isolate of rabies virus. Acta Virol 2004; 48: 47 50 [PubMed]
    [Google Scholar]
  43. Johnson N, McElhinney LM, Smith J, Lowings P, Fooks AR. Phylogenetic comparison of the genus lyssavirus using distal coding sequences of the glycoprotein and nucleoprotein genes. Arch Virol 2002; 147: 2111 2123 [CrossRef] [PubMed]
    [Google Scholar]
  44. Reddy MGB. Molecular Epidemiology and Pathogenesis of Rabies. PhD thesis submitted to Indian Veterinary Research Institute Izatnagar; Uttar Pradesh: 2010
    [Google Scholar]
  45. Sanjuán R, Domingo-Calap P. Mechanisms of viral mutation. Cell Mol Life Sci 2016; 73: 4433 4448 [CrossRef] [PubMed]
    [Google Scholar]
  46. Kouznetzoff A, Buckle M, Tordo N. Identification of a region of the rabies virus N protein involved in direct binding to the viral RNA. J Gen Virol 1998; 79 (Pt 5: 1005 1013 [CrossRef] [PubMed]
    [Google Scholar]
  47. Yu F, Zhang G, Zhong X, Han N, Song Y 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 2014; 159: 1593 1601 [CrossRef] [PubMed]
    [Google Scholar]
  48. Reddy RVC, Mohana Subramanian B, Surendra KSNL, Babu RPA, Rana SK et al. Rabies virus isolates of India – simultaneous existence of two distinct evolutionary lineages. Infect Gen Evol 2014; 27: 163 172 [CrossRef]
    [Google Scholar]
  49. Yu J, Li H, Tang Q, Rayner S, Han N et al. The spatial and temporal dynamics of rabies in China. PLoS Negl Trop Dis 2012; 6: e1640 [CrossRef] [PubMed]
    [Google Scholar]
  50. Zhang X, Cai Y, Zhai X, Liu J, Zhao W et al. Comprehensive analysis of codon usage on rabies virus and other lyssaviruses. Int J Mol Sci 2018; 19: 2397 [CrossRef] [PubMed]
    [Google Scholar]
  51. Chapat L, Hilaire F, Bouvet J, Pialot D, Philippe-Reversat C et al. Multivariate analysis of the immune response to a vaccine as an alternative to the repetition of animal challenge studies for vaccines with demonstrated efficacy. Vet Immunol Immunopathol 2017; 189: 58 65 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001521
Loading
/content/journal/jgv/10.1099/jgv.0.001521
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error