Skip to main content

Advertisement

Log in

Delayed progression of rabies transmitted by a vampire bat

  • Brief Report
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Here, we compared the growth kinetics, cell-to-cell spread, and virus internalization kinetics in N2a cells of RABV variants isolated from vampire bats (V-3), domestic dogs (V-2) and marmosets (V-M) as well as the clinical symptoms and mortality caused by these variants. The replication rate of V-3 was significantly higher than those of V-2 and V-M. However, the uptake and spread of these RABV variants into N2a cells were inversely proportional. Nevertheless, V-3 had longer incubation and evolution periods. Our results provide evidence that the clinical manifestations of infection with bat RABV variant occur at a later time when compared to what was observed with canine and marmoset rabies virus variants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

References

  1. Rupprecht CE, Hanlon CA, Hemachudha T (2002) Rabies re-examined. Lancet Infect Dis 2(6):327–343. doi:10.1016/S1473-3099(02)00287-6

    Article  PubMed  Google Scholar 

  2. Messenger SL, Smith JS, Rupprecht CE (2002) Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States. Clin Infect Dis 35:738–747. doi:10.1086/342387

    Article  PubMed  Google Scholar 

  3. Favoretto SR, de Mattos CC, de Mattos CA et al (2013) The emergence of wildlife species as a source of human rabies infection in Brazil. Epidemiol Infect 141(7):1552–1561. doi:10.1017/S0950268813000198

    Article  CAS  PubMed  Google Scholar 

  4. Diaz AM, Papo S, Rodriguez A et al (1994) Antigenic analysis of rabies-virus isolates from Latin America and the Caribbean. Zentralbl Veterinarmed B 41(3):153–160. doi:10.1111/j.1439-0450.1994.tb00219.x

    CAS  PubMed  Google Scholar 

  5. Favoretto SR, Mattos CC, Morais NB et al (2001) Rabies in marmosets (Callithrix jacchus) from the State of Ceará, Brazil. Emerg Infect Dis 7:1062–1065. http://wwwnc.cdc.gov/eid/article/7/6/pdfs/01-0630.pdf

  6. De Mattos CC, de Mattos CA, Loza-Rubio E et al (1999) Molecular characterization of rabies virus isolates from Mexico: implications for transmission dynamics and human risk. Am J Trop Med Hyg 61(4):587–597. doi:10.1017/S0950268813000198

    PubMed  Google Scholar 

  7. Castilho JC, Iamamoto K, Lima JYO et al (2007) Padronização e aplicação da técnica de isolamento do vírus da raiva em células de neuroblastoma de camundongo (N2a). Bol Epidemiol Paulista 4(47):12–18. ISSN 1806-423-X. http://periodicos.ses.sp.bvs.br/pdf/bepa/v4n47/v4n47a02.pdf

  8. Faber M, Pulmanausahakul R, Nagao K et al (2004) Identification of viral genomic elements responsible for rabies virus neuroinvasiveness. Proc Natl Acad Sci 101:16328–16332. doi:10.1073/pnas.0407289101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Pulmanausahakul R, Li J, Schnell MJ et al (2008) The glycoprotein and the matrix protein of rabies virus affect pathogenicity by regulating viral replication and facilitating cell-to-cell spread. J Virol 82(5):2330–2338. doi:10.1128/JVI.02327-07

    Article  CAS  PubMed  Google Scholar 

  10. Faber M, Faber ML, Li J et al (2007) Dominance of a nonpathogenic glycoprotein gene over a pathogenic glycoprotein gene in rabies virus. J Virol 81(13):7041–7047. doi:10.1128/JVI.00357-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Charlton KM, Casey GA (1979) Experimental rabies in skunks: immunofluorescence light and electron microscopic studies. Lab Invest 41:36–44

    CAS  PubMed  Google Scholar 

  12. Murphy FA, Bauer SP (1974) Early street rabies virus infection in striated muscle and later progression to the central nervous system. Intervirology 3:256–268

    Article  CAS  PubMed  Google Scholar 

  13. Shankar V, Dietzschold B, Koprowski H (1991) Direct entry of rabies virus into the central nervous system without prior local replication. J Virol 65:2736–2738

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Dietzschold B, Li J, Faber M et al (2008) Concepts in the pathogenesis of rabies. Future Virol 3(5):481–490. doi:10.2217/17460794.3.5.481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kgaladi J, Nel LH, Markotter W (2013) Comparison of pathogenic domains of rabies and African rabies-related lyssaviruses and pathogenicity observed in mice. Onderstepoort J Vet Res 80(1):511. doi:10.4102/ojvr.v80i1.511

    Article  PubMed  Google Scholar 

  16. Morimoto K, Patel M, Corisedo S et al (1996) Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. Proc Natl Acad Sci USA 93:5653–5658. doi:10.1073/pnas.93.11.5653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Jackson AC (2014) Recovery from rabies: a call to arms. J Neurol Sci 339(1–2):5–7. doi:10.1016/j.jns.2014.02.012

    Article  PubMed  Google Scholar 

  18. Orciari LA, Niezgoda M, Hanlon CA et al (2001) Rapid clearance of SAG-2 rabies virus from dogs after oral vaccination. Vaccine 19:4511–4518. doi:10.1016/S0264-410X(01)00186-4

    Article  CAS  PubMed  Google Scholar 

  19. Hierholzer JC, Killington RA (1996) Suspension assay method. Virology Methods Manual. Academic, San Diego, pp 39–40

    Google Scholar 

  20. Cunha EM, Nassar AF, Lara do C M et al (2010) Pathogenicity of different rabies virus isolates and protection test in vaccinated mice. Rev Inst Med Trop Sao Paulo 52(5):231–236. doi:10.1590/S0036-46652010000500002

    Article  PubMed  Google Scholar 

  21. Preuss MA, Faber ML, Tan GS et al (2009) Intravenous inoculation of a bat-associated rabies virus causes lethal encephalopathy in mice through invasion of the brain via neurosecretory hypothalamic fibers. PLoS Pathog 5(6):e1000485. doi:10.1371/journal.ppat.1000485

    Article  PubMed Central  Google Scholar 

  22. Faber M, Faber ML, Papaneri A et al (2005) A Single amino acid change in rabies virus glycoprotein increases virus spread and enhances virus pathogenicity. J Virol 79(22):14141–14148. doi:10.1128/JVI.79.22.14141-14148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dietzschold B, Wiktor TJ, Trojanowski JQ et al (1985) Differences in cell- to-cell spread of pathogenic and apathogenic rabies virus in vivo and in vitro. J Virol 56:12–18

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Jackson AC (2003) Rabies virus infection: an update. J Neurovirol 9(2):253–258. doi:10.1080/13550280390193975

    Article  PubMed  Google Scholar 

  25. Hemachudha T, Laothamatas J, Rupprecht CE (2002) Human rabies: a disease of complex neuropathogenic mechanism and diagnostic challenges. Lancet Neurol 1:101–109. doi:10.1016/S1474-4422(02)00041-8

    Article  PubMed  Google Scholar 

  26. Warrell MJ, Warrell DA (2004) Rabies and other lyssaviruses disease. Lancet 363:959–969. doi:10.1016/S0140-6736(04)15792-9

    Article  CAS  PubMed  Google Scholar 

  27. Zhang G, Wang H, Mahmood F et al (2013) Rabies virus glycoprotein is an important determinant for the induction of innate immune responses and the pathogenic mechanisms. Vet Microbiol 162(2–4):601–613. doi:10.1016/j.vetmic.2012.11.031

    Article  CAS  PubMed  Google Scholar 

  28. Appolinário C, Allendorf SD, Vicente AF et al (2015) Fluorescent antibody test, quantitative PCR pattern and clinical aspects of rabies virus strains isolated from main reservoirs in Brazil. Braz J Infect Dis 19(5):479–485. doi:10.1016/j.bjid.2015.06.012

    Article  PubMed  Google Scholar 

  29. Badrane H, Bahloul C, Perrin P et al (2001) Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75(7):268–3276. doi:10.1128/JVI.75.7.3268-3276.2001

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Keila Iamamoto Nogi and Willian de Oliveira Fahl for testing the RABV virus samples. We would like to thank Leo Iwai and Liron Kufert for refining the use of English in the manuscript.

This work was supported by Instituto Pasteur/Brazil.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Iana Suly Santos Katz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Katz, I.S.S., Fuoco, N.L., Chaves, L.B. et al. Delayed progression of rabies transmitted by a vampire bat. Arch Virol 161, 2561–2566 (2016). https://doi.org/10.1007/s00705-016-2927-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-016-2927-3

Keywords

Navigation