1932

Abstract

The cultural impact of rabies, the fatal neurological disease caused by infection with rabies virus, registers throughout recorded history. Although rabies has been the subject of large-scale public health interventions, chiefly through vaccination efforts, the disease continues to take the lives of about 40,000–70,000 people per year, roughly 40% of whom are children. Most of these deaths occur in resource-poor countries, where lack of infrastructure prevents timely reporting and postexposure prophylaxis and the ubiquity of domestic and wild animal hosts makes eradication unlikely. Moreover, although the disease is rarer than other human infections such as influenza, the prognosis following a bite from a rabid animal is poor: There is currently no effective treatment that will save the life of a symptomatic rabies patient. This review focuses on the major unanswered research questions related to rabies virus pathogenesis, especially those connecting the disease progression of rabies with the complex dysfunction caused by the virus in infected cells. The recent applications of cutting-edge research strategies to this question are described in detail.

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2015-11-09
2024-06-16
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Literature Cited

  1. Nicholson KG. 1.  1994. Human rabies. Handbook of Neurovirology RR McKendall, WG Stroop 463–80 New York: Marcel Dekker [Google Scholar]
  2. Kuzmin IV, Tordo N. 2.  2012. Genus Lyssavirus. Rhabdoviruses: Molecular Taxonomy, Evolution, Genomics, Ecology, Host-Vector Interactions, Cytopathology and Control RG Dietzgen, IV Kuzmin 37–58 Norfolk, UK: Caister Acad. [Google Scholar]
  3. Rosner F. 3.  1974. Rabies in the Talmud. Med. Hist. 18:198–200 [Google Scholar]
  4. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI. 4.  et al. 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull. World Health Organ. 83:360–68 [Google Scholar]
  5. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A. 5.  2010. The cell biology of rabies virus: using stealth to reach the brain. Nat. Rev. Microbiol. 8:51–61 [Google Scholar]
  6. Wildy P. 6.  1971. Classification and Nomenclature of Viruses. First Report of the International Committee on Nomenclature of Viruses. Basel: Karger [Google Scholar]
  7. Dietzgen RG. 7.  2012. Morphology, genome organization, transcription and replication of rhabdoviruses. Rhabdoviruses: Molecular Taxonomy, Evolution, Genomics, Ecology, Host-Vector Interactions, Cytopathology and Control RG Dietzgen, IV Kuzmin 5–12 Norfolk, UK: Caister Acad. [Google Scholar]
  8. Marston DA, McElhinney LM, Banyard AC, Horton DL, Nunez A. 8.  et al. 2013. Interspecies protein substitution to investigate the role of the lyssavirus glycoprotein. J. Gen. Virol. 94:284–92 [Google Scholar]
  9. Pollin R, Granzow H, Kollner B, Conzelmann KK, Finke S. 9.  2013. Membrane and inclusion body targeting of lyssavirus matrix proteins. Cell Microbiol. 15:200–12 [Google Scholar]
  10. Wiltzer L, Larrous F, Oksayan S, Ito N, Marsh GA. 10.  et al. 2012. Conservation of a unique mechanism of immune evasion across the Lyssavirus genus. J. Virol. 86:10194–99 [Google Scholar]
  11. Nolden T, Banyard AC, Finke S, Fooks AR, Hanke D. 11.  et al. 2014. Comparative studies on the genetic, antigenic and pathogenic characteristics of Bokeloh bat lyssavirus. J. Gen. Virol. 95:1647–53 [Google Scholar]
  12. Rahmeh AA, Schenk AD, Danek EI, Kranzusch PJ, Liang B. 12.  et al. 2010. Molecular architecture of the vesicular stomatitis virus RNA polymerase. PNAS 107:20075–80 [Google Scholar]
  13. Hummeler K, Tomassini N, Sokol F, Kuwert E, Koprowski H. 13.  1968. Morphology of the nucleoprotein component of rabies virus. J. Virol. 2:1191–99 [Google Scholar]
  14. Lenard J, Vanderoef R. 14.  1990. Localization of the membrane-associated region of vesicular stomatitis virus M protein at the N terminus, using the hydrophobic, photoreactive probe 125I-TID. J. Virol. 64:3486–91 [Google Scholar]
  15. Mebatsion T, Weiland F, Conzelmann KK. 15.  1999. 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. 73:242–50 [Google Scholar]
  16. Zakowski JJ, Wagner RR. 16.  1980. Localization of membrane-associated proteins in vesicular stomatitis virus by use of hydrophobic membrane probes and cross-linking reagents. J. Virol. 36:93–102 [Google Scholar]
  17. Dietzgen RG, Kuzmin IV. 17.  2012. Taxonomy of rhabdoviruses. Rhabdoviruses: Molecular Taxonomy, Evolution, Genomics, Ecology, Host-Vector Interactions, Cytopathology and Control RG Dietzgen, IV Kuzmin 13–22 Norfolk, UK: Caister Acad. [Google Scholar]
  18. Rieder M, Conzelmann KK. 18.  2011. Interferon in rabies virus infection. Adv. Virus Res. 79:91–114 [Google Scholar]
  19. Etessami R, Conzelmann KK, Fadai-Ghotbi B, Natelson B, Tsiang H, Ceccaldi PE. 19.  2000. Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J. Gen. Virol. 81:2147–53 [Google Scholar]
  20. Le Blanc I, Luyet PP, Pons V, Ferguson C, Emans N. 20.  et al. 2005. Endosome-to-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7:653–64 [Google Scholar]
  21. Ivanov I, Yabukarski F, Ruigrok RW, Jamin M. 21.  2011. Structural insights into the rhabdovirus transcription/replication complex. Virus Res. 162:126–37 [Google Scholar]
  22. Banerjee AK, Barik S. 22.  1992. Gene expression of vesicular stomatitis virus genome RNA. Virology 188:417–28 [Google Scholar]
  23. Finke S, Cox JH, Conzelmann KK. 23.  2000. Differential transcription attenuation of rabies virus genes by intergenic regions: generation of recombinant viruses overexpressing the polymerase gene. J. Virol. 74:7261–69 [Google Scholar]
  24. Liu P, Yang J, Wu X, Fu ZF. 24.  2004. Interactions amongst rabies virus nucleoprotein, phosphoprotein and genomic RNA in virus-infected and transfected cells. J. Gen. Virol. 85:3725–34 [Google Scholar]
  25. Finke S, Mueller-Waldeck R, Conzelmann KK. 25.  2003. Rabies virus matrix protein regulates the balance of virus transcription and replication. J. Gen. Virol. 84:1613–21 [Google Scholar]
  26. Abraham G, Banerjee AK. 26.  1976. Sequential transcription of the genes of vesicular stomatitis virus. PNAS 73:1504–8 [Google Scholar]
  27. Mebatsion T, Konig M, Conzelmann KK. 27.  1996. Budding of rabies virus particles in the absence of the spike glycoprotein. Cell 84:941–51 [Google Scholar]
  28. Okumura A, Harty RN. 28.  2011. Rabies virus assembly and budding. Adv. Virus Res. 79:23–32 [Google Scholar]
  29. Hastie E, Cataldi M, Marriott I, Grdzelishvili VZ. 29.  2013. Understanding and altering cell tropism of vesicular stomatitis virus. Virus Res. 176:16–32 [Google Scholar]
  30. Beier KT, Saunders AB, Oldenburg IA, Sabatini BL, Cepko CL. 30.  2013. Vesicular stomatitis virus with the rabies virus glycoprotein directs retrograde transsynaptic transport among neurons in vivo. Front. Neural Circuits 7:11 [Google Scholar]
  31. Lafon M. 31.  2005. Rabies virus receptors. J. Neurovirol. 11:82–87 [Google Scholar]
  32. Ugolini G. 32.  2011. Rabies virus as a transneuronal tracer of neuronal connections. Adv. Virus Res. 79:165–202 [Google Scholar]
  33. Jackson AC, Ye H, Phelan CC, Ridaura-Sanz C, Zheng Q, Li Z. 33.  et al. 1999. Extraneural organ involvement in human rabies. Lab. Investig. 79:945–51 [Google Scholar]
  34. Jogai S, Radotra BD, Banerjee AK. 34.  2002. Rabies viral antigen in extracranial organs: a post-mortem study. Neuropathol. Appl. Neurobiol. 28:334–38 [Google Scholar]
  35. Macedo CI, Carnieli P Jr, Brandao PE, Travassos da Rosa ES, Oliveira RdN. 35.  et al. 2006. Diagnosis of human rabies cases by polymerase chain reaction of neck-skin samples. Braz. J. Infect. Dis. 10:341–45 [Google Scholar]
  36. Graf W, Gerrits N, Yatim-Dhiba N, Ugolini G. 36.  2002. Mapping the oculomotor system: the power of transneuronal labelling with rabies virus. Eur. J. Neurosci. 15:1557–62 [Google Scholar]
  37. Wilbur LA, Aubert MFA. 37.  1996. The NIH test for potency. Laboratory Techniques in Rabies FX Meslin, MM Kaplan, H Koprowski 360–68 Geneva: World Health Organ. [Google Scholar]
  38. Schnell MJ, Tan GS, Dietzschold B. 38.  2005. The application of reverse genetics technology in the study of rabies virus (RV) pathogenesis and for the development of novel RV vaccines. J. Neurovirol. 11:76–81 [Google Scholar]
  39. Davis AD, Jarvis JA, Pouliott CE, Morgan SM, Rudd RJ. 39.  2013. Susceptibility and pathogenesis of little brown bats (Myotis lucifugus) to heterologous and homologous rabies viruses. J. Virol. 87:9008–15 [Google Scholar]
  40. Morimoto K, Patel M, Corisdeo S, Hooper DC, Fu ZF. 40.  et al. 1996. Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. PNAS 93:5653–58 [Google Scholar]
  41. Schnell MJ, Mebatsion T, Conzelmann KK. 41.  1994. Infectious rabies viruses from cloned cDNA. EMBO J. 13:4195–203 [Google Scholar]
  42. O'Donnell LA, Rall GF. 42.  2010. Blue moon neurovirology: the merits of studying rare CNS diseases of viral origin. J. Neuroimmune Pharmacol. 5:443–55 [Google Scholar]
  43. Bearer EL, Breakefield XO, Schuback D, Reese TS, LaVail JH. 43.  2000. Retrograde axonal transport of herpes simplex virus: evidence for a single mechanism and a role for tegument. PNAS 97:8146–50 [Google Scholar]
  44. Kramer T, Enquist LW. 44.  2013. Directional spread of alphaherpesviruses in the nervous system. Viruses 5:678–707 [Google Scholar]
  45. Fredericksen BL. 45.  2014. The neuroimmune response to West Nile virus. J. Neurovirol. 20:113–21 [Google Scholar]
  46. Johnson RT. 46.  1998. Viral Infections of the Nervous System Philadelphia: Lippincott-Raven [Google Scholar]
  47. Preuss MA, Faber ML, Tan GS, Bette M, Dietzschold B. 47.  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:e1000485 [Google Scholar]
  48. Lentz TL, Burrage TG, Smith AL, Crick J, Tignor GH. 48.  1982. Is the acetylcholine receptor a rabies virus receptor?. Science 215:182–84 [Google Scholar]
  49. Burrage TG, Tignor GH, Smith AL. 49.  1985. Rabies virus binding at neuromuscular junctions. Virus Res. 2:273–89 [Google Scholar]
  50. Bracci L, Antoni G, Cusi MG, Lozzi L, Niccolai N. 50.  et al. 1988. Antipeptide monoclonal antibodies inhibit the binding of rabies virus glycoprotein and α-bungarotoxin to the nicotinic acetylcholine receptor. Mol. Immunol. 25:881–88 [Google Scholar]
  51. Watson HD, Tignor GH, Smith AL. 51.  1981. Entry of rabies virus into the peripheral nerves of mice. J. Gen. Virol. 56:372–82 [Google Scholar]
  52. Charlton KM, Casey GA. 52.  1981. Experimental rabies in skunks: persistence of virus in denervated muscle at the inoculation site. Can. J. Comp. Med. 45:357–62 [Google Scholar]
  53. Charlton KM, Nadin-Davis S, Casey GA, Wandeler AI. 53.  1997. The long incubation period in rabies: delayed progression of infection in muscle at the site of exposure. Acta Neuropathol. 94:73–77 [Google Scholar]
  54. Coulon P, Derbin C, Kucera P, Lafay F, Prehaud C, Flamand A. 54.  1989. Invasion of the peripheral nervous systems of adult mice by the CVS strain of rabies virus and its avirulent derivative AvO1. J. Virol. 63:3550–54 [Google Scholar]
  55. Shankar V, Dietzschold B, Koprowski H. 55.  1991. Direct entry of rabies virus into the central nervous system without prior local replication. J. Virol. 65:2736–38 [Google Scholar]
  56. Morcuende S, Delgado-Garcia JM, Ugolini G. 56.  2002. Neuronal premotor networks involved in eyelid responses: retrograde transneuronal tracing with rabies virus from the orbicularis oculi muscle in the rat. J. Neurosci. 22:8808–18 [Google Scholar]
  57. Tang Y, Rampin O, Giuliano F, Ugolini G. 57.  1999. Spinal and brain circuits to motoneurons of the bulbospongiosus muscle: retrograde transneuronal tracing with rabies virus. J. Comp. Neurol. 414:167–92 [Google Scholar]
  58. Rathelot JA, Strick PL. 58.  2006. Muscle representation in the macaque motor cortex: an anatomical perspective. PNAS 103:8257–62 [Google Scholar]
  59. Velandia-Romero ML, Castellanos JE, Martinez-Gutierrez M. 59.  2013. In vivo differential susceptibility of sensory neurons to rabies virus infection. J. Neurovirol. 19:367–75 [Google Scholar]
  60. Tsiang H. 60.  1979. Evidence for an intraaxonal transport of fixed and street rabies virus. J. Neuropathol. Exp. Neurol. 38:286–99 [Google Scholar]
  61. Bulenga G, Heaney T. 61.  1978. Post-exposure local treatment of mice infected with rabies with two axonal flow inhibitors, colchicine and vinblastine. J. Gen. Virol. 39:381–85 [Google Scholar]
  62. Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ. 62.  et al. 2001. Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum. Mol. Genet. 10:2109–21 [Google Scholar]
  63. Jacob Y, Badrane H, Ceccaldi PE, Tordo N. 63.  2000. Cytoplasmic dynein LC8 interacts with lyssavirus phosphoprotein. J. Virol. 74:10217–22 [Google Scholar]
  64. Raux H, Flamand A, Blondel D. 64.  2000. Interaction of the rabies virus P protein with the LC8 dynein light chain. J. Virol. 74:10212–16 [Google Scholar]
  65. Rasalingam P, Rossiter JP, Mebatsion T, Jackson AC. 65.  2005. Comparative pathogenesis of the SAD-L16 strain of rabies virus and a mutant modifying the dynein light chain binding site of the rabies virus phosphoprotein in young mice. Virus Res. 111:55–60 [Google Scholar]
  66. Tan GS, Preuss MA, Williams JC, Schnell MJ. 66.  2007. The dynein light chain 8 binding motif of rabies virus phosphoprotein promotes efficient viral transcription. PNAS 104:7229–34 [Google Scholar]
  67. Klingen Y, Conzelmann KK, Finke S. 67.  2008. Double-labeled rabies virus: live tracking of enveloped virus transport. J. Virol. 82:237–45 [Google Scholar]
  68. Bauer A, Nolden T, Schroter J, Romer-Oberdorfer A, Gluska S. 68.  et al. 2014. Anterograde glycoprotein-dependent transport of newly generated rabies virus in dorsal root ganglion neurons. J. Virol. 88:14172–83 [Google Scholar]
  69. Thoulouze MI, Lafage M, Schachner M, Hartmann U, Cremer H, Lafon M. 69.  1998. The neural cell adhesion molecule is a receptor for rabies virus. J. Virol. 72:7181–90 [Google Scholar]
  70. Tuffereau C, Benejean J, Blondel D, Kieffer B, Flamand A. 70.  1998. Low-affinity nerve-growth factor receptor (P75NTR) can serve as a receptor for rabies virus. EMBO J. 17:7250–59 [Google Scholar]
  71. Tuffereau C, Schmidt K, Langevin C, Lafay F, Dechant G, Koltzenburg M. 71.  2007. The rabies virus glycoprotein receptor p75NTR is not essential for rabies virus infection. J. Virol. 81:13622–30 [Google Scholar]
  72. Cox JH, Dietzschold B, Schneider LG. 72.  1977. Rabies virus glycoprotein. II. Biological and serological characterization. Infect. Immun. 16:754–59 [Google Scholar]
  73. Coulon P, Rollin P, Aubert M, Flamand A. 73.  1982. Molecular basis of rabies virus virulence. I. Selection of avirulent mutants of the CVS strain with anti-G monoclonal antibodies. J. Gen. Virol. 61:97–100 [Google Scholar]
  74. Coulon P, Rollin PE, Flamand A. 74.  1983. Molecular basis of rabies virus virulence. II. Identification of a site on the CVS glycoprotein associated with virulence. J. Gen. Virol. 64:693–96 [Google Scholar]
  75. Dietzschold B, Wiktor TJ, Trojanowski JQ, Macfarlan RI, Wunner WH. 75.  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 [Google Scholar]
  76. Seif I, Coulon P, Rollin PE, Flamand A. 76.  1985. Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J. Virol. 53:926–34 [Google Scholar]
  77. Morimoto K, Foley HD, McGettigan JP, Schnell MJ, Dietzschold B. 77.  2000. Reinvestigation of the role of the rabies virus glycoprotein in viral pathogenesis using a reverse genetics approach. J. Neurovirol. 6:373–81 [Google Scholar]
  78. Faber M, Pulmanausahakul R, Nagao K, Prosniak M, Rice AB. 78.  et al. 2004. Identification of viral genomic elements responsible for rabies virus neuroinvasiveness. PNAS 101:16328–32 [Google Scholar]
  79. Pulmanausahakul R, Li J, Schnell MJ, Dietzschold B. 79.  2008. The glycoprotein and the matrix protein of rabies virus affect pathogenicity by regulating viral replication and facilitating cell-to-cell spread. J. Virol. 82:2330–38 [Google Scholar]
  80. Lafon M. 80.  2011. Evasive strategies in rabies virus infection. Adv. Virus Res. 79:33–53 [Google Scholar]
  81. Thoulouze MI, Lafage M, Yuste VJ, Kroemer G, Susin SA. 81.  et al. 2003. Apoptosis inversely correlates with rabies virus neurotropism. Ann. N.Y. Acad. Sci. 1010:598–603 [Google Scholar]
  82. Morimoto K, Hooper DC, Spitsin S, Koprowski H, Dietzschold B. 82.  1999. Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J. Virol. 73:510–18 [Google Scholar]
  83. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A. 83.  et al. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994–97 [Google Scholar]
  84. Diamond MS, Farzan M. 84.  2013. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 13:46–57 [Google Scholar]
  85. Der SD, Zhou A, Williams BR, Silverman RH. 85.  1998. Identification of genes differentially regulated by interferon α, β, or γ using oligonucleotide arrays. PNAS 95:15623–28 [Google Scholar]
  86. Chopy D, Detje CN, Lafage M, Kalinke U, Lafon M. 86.  2011. The type I interferon response bridles rabies virus infection and reduces pathogenicity. J. Neurovirol. 17:353–67 [Google Scholar]
  87. Marcovistz R, Galabru J, Tsiang H, Hovanessian AG. 87.  1986. Neutralization of interferon produced early during rabies virus infection in mice. J. Gen. Virol. 67:387–90 [Google Scholar]
  88. Marschalek A, Finke S, Schwemmle M, Mayer D, Heimrich B. 88.  et al. 2009. Attenuation of rabies virus replication and virulence by picornavirus internal ribosome entry site elements. J. Virol. 83:1911–19 [Google Scholar]
  89. Chenik M, Chebli K, Blondel D. 89.  1995. Translation initiation at alternate in-frame AUG codons in the rabies virus phosphoprotein mRNA is mediated by a ribosomal leaky scanning mechanism. J. Virol. 69:707–12 [Google Scholar]
  90. Brzozka K, Finke S, Conzelmann KK. 90.  2005. Identification of the rabies virus alpha/beta interferon antagonist: Phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673–81 [Google Scholar]
  91. Finke S, Brzozka K, Conzelmann KK. 91.  2004. Tracking fluorescence-labeled rabies virus: Enhanced green fluorescent protein-tagged phosphoprotein P supports virus gene expression and formation of infectious particles. J. Virol. 78:12333–43 [Google Scholar]
  92. Rieder M, Brzozka K, Pfaller CK, Cox JH, Stitz L, Conzelmann KK. 92.  2011. Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: Inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J. Virol. 85:842–52 [Google Scholar]
  93. Vidy A, Chelbi-Alix M, Blondel D. 93.  2005. Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J. Virol. 79:14411–20 [Google Scholar]
  94. Vidy A, El Bougrini J, Chelbi-Alix MK, Blondel D. 94.  2007. The nucleocytoplasmic rabies virus P protein counteracts interferon signaling by inhibiting both nuclear accumulation and DNA binding of STAT1. J. Virol. 81:4255–63 [Google Scholar]
  95. Ito N, Moseley GW, Blondel D, Shimizu K, Rowe CL. 95.  et al. 2010. Role of interferon antagonist activity of rabies virus phosphoprotein in viral pathogenicity. J. Virol. 84:6699–710 [Google Scholar]
  96. Yamaoka S, Ito N, Ohka S, Kaneda S, Nakamura H. 96.  et al. 2013. Involvement of the rabies virus phosphoprotein gene in neuroinvasiveness. J. Virol. 87:12327–38 [Google Scholar]
  97. Galelli A, Baloul L, Lafon M. 97.  2000. Abortive rabies virus central nervous infection is controlled by T lymphocyte local recruitment and induction of apoptosis. J. Neurovirol. 6:359–72 [Google Scholar]
  98. Camelo S, Lafage M, Galelli A, Lafon M. 98.  2001. Selective role for the p55 Kd TNF-α receptor in immune unresponsiveness induced by an acute viral encephalitis. J. Neuroimmunol. 113:95–108 [Google Scholar]
  99. Roy A, Phares TW, Koprowski H, Hooper DC. 99.  2007. Failure to open the blood-brain barrier and deliver immune effectors to central nervous system tissues leads to the lethal outcome of silver-haired bat rabies virus infection. J. Virol. 81:1110–18 [Google Scholar]
  100. Hooper DC, Roy A, Barkhouse DA, Li J, Kean RB. 100.  2011. Rabies virus clearance from the central nervous system. Adv. Virus Res. 79:55–71 [Google Scholar]
  101. Roy A, Hooper DC. 101.  2008. Immune evasion by rabies viruses through the maintenance of blood-brain barrier integrity. J. Neurovirol. 14:401–11 [Google Scholar]
  102. Roy A, Hooper DC. 102.  2007. Lethal silver-haired bat rabies virus infection can be prevented by opening the blood-brain barrier. J. Virol. 81:7993–98 [Google Scholar]
  103. Baloul L, Camelo S, Lafon M. 103.  2004. Up-regulation of Fas ligand (FasL) in the central nervous system: a mechanism of immune evasion by rabies virus. J. Neurovirol. 10:372–82 [Google Scholar]
  104. Lafon M, Megret F, Meuth SG, Simon O, Velandia Romero ML. 104.  et al. 2008. Detrimental contribution of the immuno-inhibitor B7-H1 to rabies virus encephalitis. J. Immunol. 180:7506–15 [Google Scholar]
  105. Jackson AC, Randle E, Lawrance G, Rossiter JP. 105.  2008. Neuronal apoptosis does not play an important role in human rabies encephalitis. J. Neurovirol. 14:368–75 [Google Scholar]
  106. Faber M, Pulmanausahakul R, Hodawadekar SS, Spitsin S, McGettigan JP. 106.  et al. 2002. Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response. J. Virol. 76:3374–81 [Google Scholar]
  107. Lahaye X, Vidy A, Pomier C, Obiang L, Harper F. 107.  et al. 2009. Functional characterization of Negri bodies (NBs) in rabies virus-infected cells: evidence that NBs are sites of viral transcription and replication. J. Virol. 83:7948–58 [Google Scholar]
  108. Lahaye X, Vidy A, Fouquet B, Blondel D. 108.  2012. Hsp70 protein positively regulates rabies virus infection. J. Virol. 86:4743–51 [Google Scholar]
  109. Li XQ, Sarmento L, Fu ZF. 109.  2005. Degeneration of neuronal processes after infection with pathogenic, but not attenuated, rabies viruses. J. Virol. 79:10063–68 [Google Scholar]
  110. Scott CA, Rossiter JP, Andrew RD, Jackson AC. 110.  2008. Structural abnormalities in neurons are sufficient to explain the clinical disease and fatal outcome of experimental rabies in yellow fluorescent protein-expressing transgenic mice. J. Virol. 82:513–21 [Google Scholar]
  111. Jackson AC, Kammouni W, Zherebitskaya E, Fernyhough P. 111.  2010. Role of oxidative stress in rabies virus infection of adult mouse dorsal root ganglion neurons. J. Virol. 84:4697–705 [Google Scholar]
  112. Zherebitskaya E, Akude E, Smith DR, Fernyhough P. 112.  2009. Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucose-induced oxidative stress. Diabetes 58:1356–64 [Google Scholar]
  113. Alandijany T, Kammouni W, Roy Chowdhury SK, Fernyhough P, Jackson AC. 113.  2013. Mitochondrial dysfunction in rabies virus infection of neurons. J. Neurovirol. 19:537–49 [Google Scholar]
  114. Gomme EA, Wirblich C, Addya S, Rall GF, Schnell MJ. 114.  2012. Immune clearance of attenuated rabies virus results in neuronal survival with altered gene expression. PLOS Pathog. 8:e1002971 [Google Scholar]
  115. Hemachudha T, Wacharapluesadee S, Laothamatas J, Wilde H. 115.  2006. Rabies. Curr. Neurol. Neurosci. Rep. 6:460–68 [Google Scholar]
  116. Balachandran A, Charlton K. 116.  1994. Experimental rabies infection of non-nervous tissues in skunks (Mephitis mephitis) and foxes (Vulpes vulpes). Vet. Pathol. 31:93–102 [Google Scholar]
  117. Lackay SN, Kuang Y, Fu ZF. 117.  2008. Rabies in small animals. Vet. Clin. N. Am. Small Anim. Pract. 38:851–61 [Google Scholar]
  118. Davis AD, Gordy PA, Bowen RA. 118.  2013. Unique characteristics of bat rabies viruses in big brown bats (Eptesicus fuscus). Arch. Virol. 158:809–20 [Google Scholar]
  119. Turmelle AS, Jackson FR, Green D, McCracken GF, Rupprecht CE. 119.  2010. Host immunity to repeated rabies virus infection in big brown bats. J. Gen. Virol. 91:2360–66 [Google Scholar]
  120. Jackson AC. 120.  2013. Current and future approaches to the therapy of human rabies. Antivir. Res. 99:61–67 [Google Scholar]
  121. Gilbert AT, Petersen BW, Recuenco S, Niezgoda M, Gomez J. 121.  et al. 2012. Evidence of rabies virus exposure among humans in the Peruvian Amazon. Am. J. Trop. Med. Hyg. 87:206–15 [Google Scholar]
  122. Davis AD, Jarvis JA, Pouliott C, Rudd RJ. 122.  2013. Rabies virus infection in Eptesicus fuscus bats born in captivity (naive bats). PLOS ONE 8:e64808 [Google Scholar]
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