Table of Contents
Pathology Research International
Volume 2011, Article ID 374286, 13 pages
http://dx.doi.org/10.4061/2011/374286
Research Article

Role of Apoptosis in Rabies Viral Encephalitis: A Comparative Study in Mice, Canine, and Human Brain with a Review of Literature

1Department of Neuropathology, National Institute of Mental Health and Neurosciences (NIMHANS), Bangalore 560 029, India
2Department Neurovirology, National Institute of Mental Health and Neurosciences (NIMHANS), Bangalore 560 029, India

Received 16 October 2010; Accepted 9 June 2011

Academic Editor: C. Sundaram

Copyright © 2011 M. S. Suja et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. WHO, Expert Consultation on Rabies, Technical Report Series 931, WHO, Geneva, Switzerland, 2005.
  2. M. K. Sudarshan, S. N. Madhusudana, B. J. Mahendra et al., “Assessing the burden of human rabies in India: results of a national multi-center epidemiological survey,” International Journal of Infectious Diseases, vol. 11, no. 1, pp. 29–35, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. B. Dietschold, C. E. Rupprecht, Z. F. Fu, and H. Koprowski, “Rhabdo virus,” in Fields Virology, B. Fields, D. Knipe, P. M. Howley et al., Eds., pp. 1137–1159, Lippincott-Raven, Philadelphia, Pa, USA, 3rd edition, 1996. View at Google Scholar
  4. D. G. Constantine, “Rabies transmission by nonbite route,” Public Health Reports, vol. 77, pp. 287–289, 1962. View at Google Scholar · View at Scopus
  5. T. Hemachudha, “Human rabies: clinical aspects, pathogenesis, and potential therapy,” Current Topics in Microbiology and Immunology, vol. 187, pp. 122–143, 1993. View at Google Scholar
  6. Z. F. Fu and A. C. Jackson, “Neuronal dysfunction and death in rabies virus infection,” Journal of NeuroVirology, vol. 11, no. 1, pp. 101–106, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. D. E. Bredesen, “Neural apoptosis,” Annals of Neurology, vol. 38, no. 6, pp. 839–851, 1995. View at Publisher · View at Google Scholar · View at Scopus
  8. E. S. Razvi and R. M. Welsh, “Apoptosis in viral infections,” Advances in Virus Research, vol. 45, pp. 1–60, 1995. View at Google Scholar · View at Scopus
  9. C. B. Thompson, “Apoptosis in the pathogenesis and treatment of disease,” Science, vol. 267, pp. 1456–1462, 1995. View at Google Scholar · View at Scopus
  10. J. M. Hardwick and D. E. Griffin, “Viral effects on cellular functions,” in Viral Pathogenesis, N. Nathanson, R. Ahmed, F. G. Searano et al., Eds., pp. 55–83, Lippincott-Raven, Philadelphia , Pa, USA, 1997. View at Google Scholar
  11. S. C. Weli, C. A. Scott, C. A. Ward, and A. C. Jackson, “Rabies virus infection of primary neuronal cultures and adult mice: failure to demonstrate evidence of excitotoxicity,” Journal of Virology, vol. 80, no. 20, pp. 10270–10273, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. A. C. Jackson and J. P. Rossiter, “Apoptosis plays an important role in experimental rabies virus infection,” Journal of Virology, vol. 71, no. 7, pp. 5603–5607, 1997. View at Google Scholar · View at Scopus
  13. J. E. Reid and A. C. Jackson, “Experimental rabies virus infection in Artibeus jamaicensis bats with CVS-24 variants,” Journal of NeuroVirology, vol. 7, no. 6, pp. 511–517, 2001. View at Publisher · View at Google Scholar · View at Scopus
  14. X. Yan, M. Prosniak, M. T. Curtis et al., “Silver-haired bat rabies virus variant does not induce apoptosis in the brain of experimentally infected mice,” Journal of NeuroVirology, vol. 7, no. 6, pp. 518–527, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Adle-Biassette, H. Bourhy, M. Gisselbrecht et al., “Rabies encephalitis in a patient with AIDS: a clinicopathological study,” Acta Neuropathologica, vol. 92, no. 4, pp. 415–420, 1996. View at Publisher · View at Google Scholar
  16. A. C. Jackson, E. Randle, G. Lawrance, and J. P. Rossiter, “Neuronal apoptosis does not play an important role in human rabies encephalitis,” Journal of NeuroVirology, vol. 14, no. 5, pp. 368–375, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. S. Suja, A. Mahadevan, S. N. Madhusudhana, S. K. Vijayasarathi, and S. K. Shankar, “Neuroanatomical mapping of rabies nucleocapsid viral antigen distribution and apoptosis in pathogenesis in street dograbies—an immunohistochemical study,” Clinical Neuropathology, vol. 28, no. 2, pp. 113–124, 2009. View at Google Scholar · View at Scopus
  18. K. Morimoto, D. C. Hooper, H. Carbaugh, Z. F. Fu, H. Koprowski, and B. Dietzschold, “Rabies virus quasispecies: implications for pathogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 6, pp. 3152–3156, 1998. View at Publisher · View at Google Scholar · View at Scopus
  19. E. White, “Life, death, and the pursuit of apoptosis,” Genes and Development, vol. 10, no. 1, pp. 1–15, 1996. View at Google Scholar · View at Scopus
  20. D. L. Vaux and A. Strasser, “The molecular biology of apoptosis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 6, pp. 2239–2244, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. L. M. Esolen, S. W. Park, J. M. Hardwick, and D. E. Griffin, “Apoptosis as a cause of death in measles virus-infected cells,” Journal of Virology, vol. 69, no. 6, pp. 3955–3958, 1995. View at Google Scholar · View at Scopus
  22. V. S. Hinshaw, C. W. Olsen, N. Dybdahl-Sissoko, and D. Evans, “Apoptosis: a mechanism of cell killing by influenza A and B viruses,” Journal of Virology, vol. 68, no. 6, pp. 3667–3673, 1994. View at Google Scholar · View at Scopus
  23. T. Takizawa, S. Matsukawa, Y. Higuchi, S. Nakamura, Y. Nakanishi, and R. Fukuda, “Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells,” Journal of General Virology, vol. 74, no. 11, pp. 2347–2355, 1993. View at Google Scholar · View at Scopus
  24. S. H. Jeurissen, F. Wagenaar, J. M. Pol, A. J. van der Eb, and M. H. M. Noteborn, “Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection,” Journal of Virology, vol. 66, no. 12, pp. 7383–7388, 1992. View at Google Scholar · View at Scopus
  25. E. A. Tolskaya, L. I. Romanova, M. S. Kolesnikova et al., “Apoptosis-inducing and apoptosis-preventing functions of poliovirus,” Journal of Virology, vol. 69, no. 2, pp. 1181–1189, 1995. View at Google Scholar · View at Scopus
  26. S. M. Oberhaus, T. S. Dermody, and K. L. Tyler, “Apoptosis and the cytopathic effects of reovirus,” Current Topics in Microbiology and Immunology, vol. 233, pp. 23–49, 1998. View at Google Scholar · View at Scopus
  27. J. G. Teodoro and P. E. Branton, “Regulation of apoptosis by viral gene products,” Journal of Virology, vol. 71, no. 3, pp. 1739–1746, 1997. View at Google Scholar · View at Scopus
  28. A. H. Koyama, “Induction of apoptotic DNA fragmentation by the infection of vesicular stomatitis virus,” Virus Research, vol. 37, no. 3, pp. 285–290, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Kurokawa, A. H. Koyama, S. Yasuoka, and A. Adachi, “Influenza virus overcomes apoptosis by rapid multiplication,” International Journal of Molecular Medicine, vol. 3, no. 5, pp. 527–530, 1999. View at Google Scholar · View at Scopus
  30. J. Lewis, S. L. Wesselingh, D. E. Griffin, and J. M. Hardwick, “Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence,” Journal of Virology, vol. 70, no. 3, pp. 1828–1835, 1996. View at Google Scholar · View at Scopus
  31. X. H. Liang, L. K. Kleeman, H. H. Jiang et al., “Protection against fatal sindbis virus encephalitis by Beclin, a novel Bcl-2-interacting protein,” Journal of Virology, vol. 72, no. 11, pp. 8586–8596, 1998. View at Google Scholar · View at Scopus
  32. A. Pekosz, J. Phillips, D. Pleasure, D. Merry, and F. Gonzalez-Scarano, “Induction of apoptosis by La Crosse virus infection and role of neuronal differentiation and human bcl-2 expression in its prevention,” Journal of Virology, vol. 70, no. 8, pp. 5329–5335, 1996. View at Google Scholar · View at Scopus
  33. M. I. Thoulouze, J. P. Rossiter, J. A. Montano-Hirose, and M. Lafon, “Rabies virus infects mouse and human lymphocytes and induces apoptosis,” Journal of Virology, vol. 71, pp. 5603–5607, 1997. View at Google Scholar
  34. S. Ubol, C. Sukwattanapan, and P. Utaisincharoen, “Rabies virus replication induces Bax-related, caspase dependent apoptosis in mouse neuroblastoma cells,” Virus Research, vol. 56, no. 2, pp. 207–215, 1998. View at Publisher · View at Google Scholar · View at Scopus
  35. A. C. Jackson and H. Park, “Apoptotic cell death in experimental rabies in suckling mice,” Acta Neuropathologica, vol. 95, no. 2, pp. 159–164, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Theerasurakarn and S. Ubol, “Apoptosis induction in brain during the fixed strain of rabies virus infection correlates with onset and severity of illness,” Journal of NeuroVirology, vol. 4, no. 4, pp. 407–414, 1998. View at Google Scholar · View at Scopus
  37. S. Ubol and J. Kasisith, “Reactivation of Nedd-2, a developmentally down-regulated apoptotic gene, in apoptosis induced by a street strain of rabies virus,” Journal of Medical Microbiology, vol. 49, no. 11, pp. 1043–1046, 2000. View at Google Scholar · View at Scopus
  38. S. Ubol, J. Kasisith, D. Pitidhammabhorn, and V. Tepsumethanol, “Screening of pro-apoptotic genes upregulated in an experimental street rabies virus-infected neonatal mouse brain,” Microbiology and Immunology, vol. 49, no. 5, pp. 423–431, 2005. View at Google Scholar · View at Scopus
  39. A. C. Jackson, “Apoptosis in experimental rabies in bax-deficient mice,” Acta Neuropathologica, vol. 98, no. 3, pp. 288–294, 1999. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Rutherford and A. C. Jackson, “Neuronal apoptosis in immunodeficient mice infected with the challenge virus standard strain of rabies virus by intracerebral inoculation,” Journal of NeuroVirology, vol. 10, no. 6, pp. 409–413, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. A. C. Jackson and H. Park, “Experimental rabies virus infection of p75 neurotrophin receptor-deficient mice,” Acta Neuropathologica, vol. 98, no. 6, pp. 641–644, 1999. View at Publisher · View at Google Scholar · View at Scopus
  42. C. A. Scott, J. P. Rossiter, R. D. Andrew, and A. C. Jackson, “Structural abnormalities in neurons are sufficient to explain the clinical disease and fatal outcome of experimental rabies in yellow fluorescent protein-expressing transgenic mice,” Journal of Virology, vol. 82, no. 1, pp. 513–521, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. I. Thoulouze, M. Lafage, V. J. Yuste et al., “Apoptosis inversely correlates with rabies virus neurotropism,” Annals of the New York Academy of Sciences, vol. 1010, pp. 598–603, 2003. View at Publisher · View at Google Scholar · View at Scopus
  44. L. I. Baloul and M. Lafon, “Apoptosis and rabies virus neuroinvasion,” Biochimie, vol. 85, no. 8, pp. 777–788, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. L. Sarmento, X. Q. Li, E. Howerth, A. C. Jackson, and Z. F. Fu, “Glycoprotein-mediated induction of apoptosis limits the spread of attenuated rabies viruses in the central nervous system of mice,” Journal of NeuroVirology, vol. 11, no. 6, pp. 571–581, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Morimoto, D. C. Hooper, S. Spitsin, H. Koprowski, and B. Dietzschold, “Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures,” Journal of Virology, vol. 73, no. 1, pp. 510–518, 1999. View at Google Scholar · View at Scopus
  47. S. Lay, C. Préhaud, B. Dietzschold, and M. Lafon, “Glycoprotein of nonpathogenic rabies viruses is a major inducer of apoptosis in human jurkat T cells,” Annals of the New York Academy of Sciences, vol. 1010, pp. 577–581, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. A. C. Jackson, P. Rasalingam, and S. C. Weli, “Comparative pathogenesis of recombinant rabies vaccine strain SAD-L16 and SAD-D29 with replacement of Arg333 in the glycoprotein after peripheral inoculation of neonatal mice: less neurovirulent strain is a stronger inducer of neuronal apoptosis,” Acta Neuropathologica, vol. 111, no. 4, pp. 372–378, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Juntrakul, P. Ruangvejvorachai, S. Shuangshoti, S. Wacharapluesadee, and T. Hemachudha, “Mechanisms of escape phenomenon of spinal cord and brainstem in human rabies,” BMC Infectious Diseases, vol. 16, no. 5, article 104, 2005. View at Publisher · View at Google Scholar · View at Scopus