Trying to treat the untreatable: experimental approaches to clear rabies virus infection from the CNS

References

1. Fooks AR, Cliquet F, Finke S, Freuling C, Hemachudha T et al. Rabies. Nat Rev Dis Primers 2017; 3:17091 [View Article]
   [Google Scholar]
2. Nandi S, Kumar M. Development in immunoprophylaxis against rabies for animals and humans. Avicenna Research Institute 20103–21
   [Google Scholar]
3. Conzelmann KK, Cox JH, Schneider LG, Thiel HJ. Molecular cloning and complete nucleotide sequence of the attenuated rabies virus sad B19. Virology 1990; 175:485–499 [View Article]
   [Google Scholar]
4. Kessels JA, Recuenco S, Navarro-Vela AM, Deray R, Vigilato M et al. Pre-exposure rabies prophylaxis: a systematic review. Bull World Health Organ 2017; 95:210–219C [View Article]
   [Google Scholar]
5. Blaise A, Gautret P. Current perspectives on rabies postexposure prophylaxis. Infect Disord Drug Targets 2015; 15:13–19 [View Article]
   [Google Scholar]
6. Beckert A, Geue L, Vos A, Neubert A, Freuling C et al. Genetic stability (in vivo) of the attenuated oral rabies virus vaccine sad B19. Microbiol Immunol 2009; 53:16–21 [View Article]
   [Google Scholar]
7. Takayama-Ito M, Inoue K, Shoji Y, Inoue S, Iijima T et al. A highly attenuated rabies virus HEP-Flury strain reverts to virulent by single amino acid substitution to arginine at position 333 in glycoprotein. Virus Res 2006; 119:208–215 [View Article]
   [Google Scholar]
8. Geue L, Schares S, Schnick C, Kliemt J, Beckert A et al. Genetic characterisation of attenuated sad rabies virus strains used for oral vaccination of wildlife. Vaccine 2008; 26:3227–3235 [View Article]
   [Google Scholar]
9. Fooks AR, Johnson N, Brookes SM, Parsons G, McElhinney LM. Risk factors associated with travel to rabies endemic countries. J Appl Microbiol 2003; 94:31S–36S [View Article]
   [Google Scholar]
10. Fooks AR, Koraka P, de Swart RL, Rupprecht CE, Osterhaus AD. Development of a multivalent paediatric human vaccine for rabies virus in combination with Measles–Mumps–Rubella (MMR). Vaccine 2014; 32:2020–2021 [View Article]
    [Google Scholar]
11. Warrell MJ. Current rabies vaccines and prophylaxis schedules: preventing rabies before and after exposure. Travel Med Infect Dis 2012; 10:1–15 [View Article]
    [Google Scholar]
12. World Health Organization Who expert consultation on rabies. Second report; 2013 Report No: 931
13. Both L, Banyard AC, van Dolleweerd C, Horton DL, Ma JK et al. Passive immunity in the prevention of rabies. Lancet Infect Dis 2012; 12:397–407 [View Article]
    [Google Scholar]
14. Fooks AR, Banyard AC, Horton DL, Johnson N, McElhinney LM et al. Current status of rabies and prospects for elimination. Lancet 2014; 384:1389–1399 [View Article]
    [Google Scholar]
15. Shim E, Hampson K, Cleaveland S, Galvani AP. Evaluating the cost-effectiveness of rabies post-exposure prophylaxis: a case study in Tanzania. Vaccine 2009; 27:7167–7172 [View Article]
    [Google Scholar]
16. Hampson K, Cleaveland S, Briggs D. Evaluation of cost-effective strategies for rabies post-exposure vaccination in low-income countries. PLoS Negl Trop Dis 2011; 5:e982 [View Article]
    [Google Scholar]
17. WHO. World Health Organization Who Consultation on a Rabies Monoclonal Antibody Cocktail for Rabies Post Exposure Treatment WHO, Geneva: WHO; 2002 pp 23–24
    [Google Scholar]
18. Müller T, Dietzschold B, Ertl H, Fooks AR, Freuling C et al. Development of a mouse monoclonal antibody cocktail for post-exposure rabies prophylaxis in humans. PLoS Negl Trop Dis 2009; 3:e542 [View Article]
    [Google Scholar]
19. Goudsmit J, Marissen WE, Weldon WC, Niezgoda M, Hanlon CA et al. Comparison of an anti-rabies human monoclonal antibody combination with human polyclonal anti-rabies immune globulin. J Infect Dis 2006; 193:796–801 [View Article]
    [Google Scholar]
20. Both L, van Dolleweerd C, Wright E, Banyard AC, Bulmer-Thomas B et al. Production, characterization, and antigen specificity of recombinant 62-71-3, a candidate monoclonal antibody for rabies prophylaxis in humans. FASEB J 2013; 27:2055–2065 [View Article]
    [Google Scholar]
21. van Dolleweerd CJ, Teh AY, Banyard AC, Both L, Lotter-Stark HC et al. Engineering, expression in transgenic plants and characterisation of E559, a rabies virus-neutralising monoclonal antibody. J Infect Dis 2014; 210:200–208 [View Article]
    [Google Scholar]
22. 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 [View Article]
    [Google Scholar]
23. Willoughby RE Jr, Tieves KS, Hoffman GM, Ghanayem NS, Amlie-Lefond CM et al. Survival after treatment of rabies with induction of coma. N Engl J Med 2005; 352:2508–2514 [View Article]
    [Google Scholar]
24. Rubin J, David D, Willoughby RE Jr, Rupprecht CE, Garcia C et al. Applying the Milwaukee protocol to treat canine rabies in equatorial guinea. Scand J Infect Dis 2009; 41:372–375 [View Article]
    [Google Scholar]
25. Madhusudana SN, Nagaraj D, Uday M, Ratnavalli E, Kumar MV. Partial recovery from rabies in a six-year-old girl. Int J Infect Dis 2002; 6:85–86 [View Article]
    [Google Scholar]
26. M N, V U, Rs M, V G, M A A et al. Unique clinical and imaging findings in a first ever documented PCR positive rabies survival patient: a case report. J Clin Virol 2015; 70:83–88 [View Article]
    [Google Scholar]
27. Kumar KV, Ahmad FM, Dutta V. Pituitary cachexia after rabies encephalitis. Neurol India 2015; 63:255–256 [View Article]
    [Google Scholar]
28. Karande S, Muranjan M, Mani RS, Anand AM, Amoghimath R et al. Atypical rabies encephalitis in a six-year-old boy: clinical, radiological, and laboratory findings. Int J Infect Dis 2015; 36:1–3 [View Article]
    [Google Scholar]
29. Hunter M, Johnson N, Hedderwick S, McCaughey C, Lowry K et al. Immunovirological correlates in human rabies treated with therapeutic coma. J Med Virol 2010; 82:1255–1265 [View Article]
    [Google Scholar]
30. Centers for Disease Control and Prevention (CDC) Recovery of a patient from clinical rabies-California, 2011. MMWR Morb Mortal Wkly Rep 2012; 61:61–65
    [Google Scholar]
31. Centers for Disease Control and Prevention (CDC) Recovery of a patient from clinical rabies-Wisconsin, 2004. MMWR Morb Mortal Wkly Rep 2004; 53:1171–1173
    [Google Scholar]
32. Caicedo Y, Paez A, Kuzmin I, Niezgoda M, Orciari LA et al. Virology, immunology and pathology of human rabies during treatment. Pediatr Infect Dis J 2015; 34:520–528 [View Article]
    [Google Scholar]
33. Wilde H, Lumlertdacha B, Meslin FX, Ghai S, Hemachudha T. Worldwide rabies deaths prevention-A focus on the current inadequacies in postexposure prophylaxis of animal bite victims. Vaccine 2016; 34:187–189 [View Article]
    [Google Scholar]
34. Zeiler FA, Jackson AC. Critical appraisal of the Milwaukee protocol for rabies: this failed approach should be abandoned. Can J Neurol Sci 2016; 43:44–51 [View Article]
    [Google Scholar]
35. Jackson AC. Current and future approaches to the therapy of human rabies. Antiviral Res 2013; 99:61–67 [View Article]
    [Google Scholar]
36. Dufkova L, Sirmarova J, Salat J, Honig V, Palus M et al. Mannitol treatment is not effective in therapy of rabies virus infection in mice. Vaccine 201720 Dec 2017 [View Article]
    [Google Scholar]
37. Marosi A, Dufkova L, Forró B, Felde O, Erdélyi K et al. Combination therapy of rabies-infected mice with inhibitors of pro-inflammatory host response, antiviral compounds and human rabies immunoglobulin. Vaccine 2018 [View Article]
    [Google Scholar]
38. Smreczak M, Marzec A, Orłowska A, Trębas P, Reichert M et al. The effect of selected molecules influencing the detrimental host immune response on a course of rabies virus infection in a murine model. Vaccine 201715 Nov 2017 [View Article]
    [Google Scholar]
39. Scott T, Nel L. Subversion of the immune response by rabies virus. Viruses 2016; 8:231 [View Article]
    [Google Scholar]
40. Finke S, Conzelmann KK. Replication strategies of rabies virus. Virus Res 2005; 111:120–131 [View Article]
    [Google Scholar]
41. Gilbert AT, Petersen BW, Recuenco S, Niezgoda M, Gómez J et al. Evidence of rabies virus exposure among humans in the Peruvian Amazon. Am J Trop Med Hyg 2012; 87:206–215 [View Article]
    [Google Scholar]
42. Johnson N, Cunningham AF, Fooks AR. The immune response to rabies virus infection and vaccination. Vaccine 2010; 28:3896–3901 [View Article]
    [Google Scholar]
43. Dimaano EM, Scholand SJ, Alera MTP, Belandres DB. Clinical and epidemiological features of human rabies cases in the Philippines: a review from 1987 to 2006. Int J Infect Dis 2011; 15:e495–e499 [View Article]
    [Google Scholar]
44. Lafon M. Rabies virus receptors. J Neurovirol 2005; 11:82–87 [View Article]
    [Google Scholar]
45. Piccinotti S, Whelan SPJ. Rabies internalizes into primary peripheral neurons via clathrin coated pits and requires fusion at the cell body. PLoS Pathog 2016; 12:e1005753 [View Article]
    [Google Scholar]
46. Xu H, Hao X, Wang S, Wang Z, Cai M et al. Real-time imaging of rabies virus entry into living Vero cells. Sci Rep 2015; 5:11753 [View Article]
    [Google Scholar]
47. Ugolini G. Advances in viral transneuronal tracing. J Neurosci Methods 2010; 194:2–20 [View Article]
    [Google Scholar]
48. Yousaf MZ, Qasim M, Zia S, Khan Mu, Ashfaq UA et al. Rabies molecular virology, diagnosis, prevention and treatment. Virol J 2012; 9:50 [View Article]
    [Google Scholar]
49. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 2010; 37:13–25 [View Article]
    [Google Scholar]
50. Hooper DC, Phares TW, Fabis MJ, Roy A. The production of antibody by invading B cells is required for the clearance of rabies virus from the central nervous system. PLoS Negl Trop Dis 2009; 3:e535 [View Article]
    [Google Scholar]
51. Roy A, Hooper DC. Lethal silver-haired bat rabies virus infection can be prevented by opening the blood-brain barrier. J Virol 2007; 81:7993–7998 [View Article]
    [Google Scholar]
52. Roy A, Phares TW, Koprowski H, Hooper DC. 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 2007; 81:1110–1118 [View Article]
    [Google Scholar]
53. Zhang G, Wang H, Mahmood F, Fu ZF. Rabies virus glycoprotein is an important determinant for the induction of innate immune responses and the pathogenic mechanisms. Vet Microbiol 2013; 162:601–613 [View Article]
    [Google Scholar]
54. Phares TW, Kean RB, Mikheeva T, Hooper DC. Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system. J Immunol 2006; 176:7666–7675 [View Article]
    [Google Scholar]
55. Roy A, Hooper DC. Immune evasion by rabies viruses through the maintenance of blood-brain barrier integrity. J Neurovirol 2008; 14:401–411 [View Article]
    [Google Scholar]
56. Chai Q, He WQ, Zhou M, Lu H, Fu ZF. Enhancement of blood-brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol 2014; 88:4698–4710 [View Article]
    [Google Scholar]
57. Li C, Zhang H, Ji L, Wang X, Wen Y et al. Deficient incorporation of rabies virus glycoprotein into virions enhances virus-induced immune evasion and viral pathogenicity. Viruses 2019; 11:218 [View Article]
    [Google Scholar]
58. Pulmanausahakul R, Li J, Schnell MJ, Dietzschold B. The glycoprotein and the matrix protein of rabies virus affect pathogenicity by regulating viral replication and facilitating cell-to-cell spread. J Virol 2008; 82:2330–2338 [View Article]
    [Google Scholar]
59. Sarmento L, Tseggai T, Dhingra V, Fu ZF. Rabies virus-induced apoptosis involves caspase-dependent and caspase-independent pathways. Virus Res 2006; 121:144–151 [View Article]
    [Google Scholar]
60. Weihe E, Bette M, Preuss MA, Faber M, Schafer MK et al. Role of virus-induced neuropeptides in the brain in the pathogenesis of rabies. Dev Biol 2008; 131:73–81
    [Google Scholar]
61. Appolinário CM, Allendorf SD, Peres MG, Ribeiro BD, Fonseca CR et al. Profile of cytokines and chemokines triggered by wild-type strains of rabies virus in mice. Am J Trop Med Hyg 2016; 94:378–383 [View Article]
    [Google Scholar]
62. Koraka P, Martina B. Antivirals for human use against rabies and prospects for their future application. Rev Sci Tech 2018; 37:673–680 [View Article]
    [Google Scholar]
63. Bussereau F, Chermann JC, De Clercq D, Hannoun C. Search for compounds which have an inhibitory effect on rhabdovirus multiplication in vitro . Annales de l'Institut Pasteur / Virologie 1983; 134:127–134 [View Article]
    [Google Scholar]
64. Bussereau F, Ermine A. Effects of heteropolyanions and nucleoside analogues on rabies virus: in vitro study of syntheses and viral production. Annales de l'Institut Pasteur / Virologie 1983; 134:487–506 [View Article]
    [Google Scholar]
65. Tsiang H, Atanasiu P, Chermann JC, Jasmin C. Inhibition of rabies virus in vitro by the ammonium-5-tungsto-2-antimoniate. J Gen Virol 1978; 40:665–668 [View Article]
    [Google Scholar]
66. De Clercq E, Bergstrom DE, Holy A, Montgomery JA. Broad-spectrum antiviral activity of adenosine analogues. Antiviral Res 1984; 4:119–133 [View Article]
    [Google Scholar]
67. Streissle G, Paessens A, Oediger H. New antiviral compounds. Adv Virus Res 1985; 30:83–138
    [Google Scholar]
68. Sodja I, Holý A. Effect of 9-(S)-(2,3-dihydroxypropyl)adenine on experimental rabies infection in laboratory mice. Acta Virol 1980; 24:317–324
    [Google Scholar]
69. Bussereau F, Picard M, Blancou J, Sureau P. Treatment of rabies in mice and Foxes with antiviral compounds. Acta Virol 1988; 32:33–49
    [Google Scholar]
70. Appolinario CM, Jackson AC. Antiviral therapy for human rabies. Antivir Ther 2015; 20:1–10 [View Article]
    [Google Scholar]
71. Yamada K, Noguchi K, Komeno T, Furuta Y, Nishizono A. Efficacy of Favipiravir (T-705) in rabies postexposure prophylaxis. J Infect Dis 2016; 213:1253–1261 [View Article]
    [Google Scholar]
72. Brandão PE, Castilho JG, Fahl W, Carnieli P Jr, Oliveira Rde N et al. Short-interfering RNAs as antivirals against rabies. Braz J Infect Dis 2007; 11:224–225 [View Article]
    [Google Scholar]
73. Gupta PK, Sonwane AA, Singh NK, Meshram CD, Dahiya SS et al. Intracerebral delivery of small interfering RNAs (siRNAs) using adenoviral vector protects mice against lethal peripheral rabies challenge. Virus Res 2012; 163:11–18 [View Article]
    [Google Scholar]
74. Sonwane AA, Dahiya SS, Saini M, Chaturvedi VK, Singh RP et al. Inhibition of rabies virus multiplication by siRNA delivered through adenoviral vector in vitro in BHK-21 cells and in vivo in mice. Res Vet Sci 2012; 93:498–503 [View Article]
    [Google Scholar]
75. Durymanova Ono EA, Iamamoto K, Castilho JG, Carnieli P Jr, de Novaes Oliveira R et al. In vitro and in vivo inhibition of rabies virus replication by RNA interference. Braz J Microbiol 2013; 44:879–882 [View Article]
    [Google Scholar]
76. Meshram CD, Singh NK, Sonwane AA, Pawar SS, Mishra BP et al. Evaluation of single and dual siRNAs targeting rabies virus glycoprotein and nucleoprotein genes for inhibition of virus multiplication in vitro . Arch Virol 2013; 158:2323–2332 [View Article]
    [Google Scholar]
77. Kumar P, Wu H, McBride JL, Jung KE, Kim MH et al. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007; 448:39–43 [View Article]
    [Google Scholar]
78. Zheng M, Tao W, Zou Y, Farokhzad OC, Shi B. Nanotechnology-based strategies for siRNA brain delivery for disease therapy. Trends Biotechnol 2018; 36:562–575 [View Article]
    [Google Scholar]
79. World Health Organization Who expert consultation on rabies. Second report. World Health Organ Tech Rep Ser 20131–139
    [Google Scholar]
80. Strady A, Lang J, Lienard M, Blondeau C, Jaussaud R et al. Antibody persistence following preexposure regimens of cell-culture rabies vaccines: 10-year follow-up and proposal for a new booster policy. J Infect Dis 1998; 177:1290–1295 [View Article]
    [Google Scholar]
81. Diseases WDoCoNT Rabies Vaccines: Who Position Paper - 2018 WHO: WHO; 2018 pp 201–220
    [Google Scholar]
82. Nandi S, Kumar M. Development in immunoprophylaxis against rabies for animals and humans. Avicenna J Med Biotechnol 2010; 2:3–21
    [Google Scholar]
83. Wu X, Franka R, Henderson H, Rupprecht CE. Live attenuated rabies virus co-infected with street rabies virus protects animals against rabies. Vaccine 2011; 29:4195–4201 [View Article]
    [Google Scholar]
84. Franka R, Wu X, Jackson FR, Velasco-Villa A, Palmer DP et al. Rabies virus pathogenesis in relationship to intervention with inactivated and attenuated rabies vaccines. Vaccine 2009; 27:7149–7155 [View Article]
    [Google Scholar]
85. Zhu S, Guo C. Rabies control and treatment: from prophylaxis to strategies with curative potential. Viruses 2016; 8:279 [View Article]
    [Google Scholar]
86. Nakagawa K, Ito N, Masatani T, Abe M, Yamaoka S et al. Generation of a live rabies vaccine strain attenuated by multiple mutations and evaluation of its safety and efficacy. Vaccine 2012; 30:3610–3617 [View Article]
    [Google Scholar]
87. Barkhouse DA, Faber M, Hooper DC. Pre- and post-exposure safety and efficacy of attenuated rabies virus vaccines are enhanced by their expression of IFNγ. Virology 2015; 474:174–180 [View Article]
    [Google Scholar]
88. Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012; 32:1959–1972 [View Article]
    [Google Scholar]
89. Varatharaj A, Galea I. The blood-brain barrier in systemic inflammation. Brain Behav Immun 2017; 60:1–12 [View Article]
    [Google Scholar]
90. Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006; 147:S232–S240 [View Article]
    [Google Scholar]
91. Minor PD. Live attenuated vaccines: historical successes and current challenges. Virology 2015; 479-480:379–392 [View Article]
    [Google Scholar]
92. Yang DK, Kim HH, Lee KW, Song JY. The present and future of rabies vaccine in animals. Clin Exp Vaccine Res 2013; 2:19–25 [View Article]
    [Google Scholar]
93. Blutt SE, Conner ME. The gastrointestinal frontier: IgA and viruses. Front Immunol 2013; 4:402 [View Article]
    [Google Scholar]
94. Wandeler AI, Capt S, Kappeler A, Hauser R. Oral immunization of wildlife against rabies: concept and first field experiments. Rev Infect Dis 1988; 10:S649–S653 [View Article]
    [Google Scholar]
95. Müller TF, Schröder R, Wysocki P, Mettenleiter TC, Freuling CM. Spatio-temporal use of oral rabies vaccines in Fox rabies elimination programmes in Europe. PLoS Negl Trop Dis 2015; 9:e0003953 [View Article]
    [Google Scholar]
96. Cliquet F, Picard-Meyer E, Mojzis M, Dirbakova Z, Muizniece Z et al. In-depth characterization of live vaccines used in Europe for oral rabies vaccination of wildlife. PLoS One 2015; 10:e0141537 [View Article]
    [Google Scholar]
97. Ogino M, Ito N, Sugiyama M, Ogino T. The rabies virus L protein catalyzes mRNA capping with GDP Polyribonucleotidyltransferase activity. Viruses 2016; 8:144 [View Article]
    [Google Scholar]
98. Szanto AG, Nadin-Davis SA, White BN. Complete genome sequence of a raccoon rabies virus isolate. Virus Res 2008; 136:130–139 [View Article]
    [Google Scholar]
99. Velasco-Villa A, Escobar LE, Sanchez A, Shi M, Streicker DG et al. Successful strategies implemented towards the elimination of canine rabies in the Western Hemisphere. Antiviral Res 2017; 143:1–12 [View Article]
    [Google Scholar]
100. Müller T, Bätza HJ, Beckert A, Bunzenthal C, Cox JH et al. Analysis of vaccine-virus-associated rabies cases in red foxes (Vulpes vulpes) after oral rabies vaccination campaigns in Germany and Austria. Arch Virol 2009; 154:1081–1091 [View Article]
     [Google Scholar]
101. Hostnik P, Picard-Meyer E, Rihtarič D, Toplak I, Cliquet F. Vaccine-induced rabies in a red fox (Vulpes vulpes): isolation of vaccine virus in brain tissue and salivary glands. J Wildl Dis 2014; 50:397–401 [View Article]
     [Google Scholar]
102. Fehlner-Gardiner C, Nadin-Davis S, Armstrong J, Muldoon F, Bachmann P et al. Era vaccine-derived cases of rabies in wildlife and domestic animals in Ontario, Canada, 1989–2004. J Wildl Dis 2008; 44:71–85 [View Article]
     [Google Scholar]
103. Brown LJ, Rosatte RC, Fehlner-Gardiner C, Ellison JA, Jackson FR et al. Oral vaccination and protection of striped skunks (mephitis mephitis) against rabies using ONRAB®. Vaccine 2014; 32:3675–3679 [View Article]
     [Google Scholar]
104. Faber M, Li J, Kean RB, Hooper DC, Alugupalli KR et al. Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc Natl Acad Sci USA 2009; 106:11300–11305 [View Article]
     [Google Scholar]
105. Li J, Ertel A, Portocarrero C, Barkhouse DA, Dietzschold B et al. Postexposure treatment with the live-attenuated rabies virus (RV) vaccine TriGAS triggers the clearance of wild-type RV from the central nervous system (CNS) through the rapid induction of genes relevant to adaptive immunity in CNS tissues. J Virol 2012; 86:3200–3210 [View Article]
     [Google Scholar]
106. Huang F, Ahmad W, Duan M, Liu Z, Guan Z et al. Efficiency of live attenuated and inactivated rabies viruses in prophylactic and post exposure vaccination against the street virus strain. Acta Virol 2015; 59:117–124 [View Article]
     [Google Scholar]
107. Vos A, Freuling C, Ortmann S, Kretzschmar A, Mayer D et al. An assessment of shedding with the oral rabies virus vaccine strain SPBN GASGAS in target and non-target species. Vaccine 2018; 36:811–817 [View Article]
     [Google Scholar]
108. Cliquet F, Gurbuxani JP, Pradhan HK, Pattnaik B, Patil SS et al. The safety and efficacy of the oral rabies vaccine SAG2 in Indian stray dogs. Vaccine 2007; 25:3409–3418 [View Article]
     [Google Scholar]
109. Hsu AP, Tseng CH, Barrat J, Lee SH, Shih YH et al. Safety, efficacy and immunogenicity evaluation of the SAG2 oral rabies vaccine in Formosan ferret badgers. PLoS One 2017; 12:e0184831 [View Article]
     [Google Scholar]
110. Masson E, Cliquet F, Aubert M, Barrat J, Aubert A et al. Safety study of the SAG2 rabies virus mutant in several non-target species with a view to its future use for the immunization of foxes in Europe. Vaccine 1996; 14:1506–1510 [View Article]
     [Google Scholar]
111. Orłowska A, Żmudziński JF. Genetic characterisation of the rabies virus vaccine strains used for oral immunization of foxes in Poland to estimate the effectiveness of vaccination. Arch Virol 2015; 160:509–515 [View Article]
     [Google Scholar]
112. Seif I, Coulon P, Rollin PE, Flamand A. Rabies virulence: effect on pathogenicity and sequence characterization of rabies virus mutations affecting antigenic site III of the glycoprotein. J Virol 1985; 53:926–934
     [Google Scholar]
113. Dietzschold B, Wunner WH, Wiktor TJ, Lopes AD, Lafon M et al. Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc Natl Acad Sci USA 1983; 80:70–74 [View Article]
     [Google Scholar]
114. Faber M, Faber ML, Papaneri A, Bette M, Weihe E et al. A single amino acid change in rabies virus glycoprotein increases virus spread and enhances virus pathogenicity. J Virol 2005; 79:14141–14148 [View Article]
     [Google Scholar]
115. Faber M, Faber ML, Li J, Preuss MA, Schnell MJ et al. Dominance of a nonpathogenic glycoprotein gene over a pathogenic glycoprotein gene in rabies virus. J Virol 2007; 81:7041–7047 [View Article]
     [Google Scholar]
116. Faber M, Pulmanausahakul R, Hodawadekar SS, Spitsin S, McGettigan JP et al. Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response. J Virol 2002; 76:3374–3381 [View Article]
     [Google Scholar]
117. Faber M, Pulmanausahakul R, Nagao K, Prosniak M, Rice AB et al. Identification of viral genomic elements responsible for rabies virus neuroinvasiveness. Proc Natl Acad Sci USA 2004; 101:16328–16332 [View Article]
     [Google Scholar]
118. Sarmento L, Li XQ, Howerth E, Jackson AC, Fu ZF. Glycoprotein-mediated induction of apoptosis limits the spread of attenuated rabies viruses in the central nervous system of mice. J Neurovirol 2005; 11:571–581 [View Article]
     [Google Scholar]
119. Nakagawa K, Nakagawa K, Omatsu T, Katayama Y, Oba M et al. Generation of a novel live rabies vaccine strain with a high level of safety by introducing attenuating mutations in the nucleoprotein and glycoprotein. Vaccine 2017; 35:5622–5628 [View Article]
     [Google Scholar]
120. Shimizu K, Ito N, Mita T, Yamada K, Hosokawa-Muto J et al. Involvement of nucleoprotein, phosphoprotein, and matrix protein genes of rabies virus in virulence for adult mice. Virus Res 2007; 123:154–160 [View Article]
     [Google Scholar]
121. Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V et al. Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol 2005; 79:12554–12565 [View Article]
     [Google Scholar]
122. Griffin DE. Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol 2003; 3:493–502 [View Article]
     [Google Scholar]
123. Stamatovic SM, Keep RF, Andjelkovic AV. Brain endothelial cell-cell junctions: how to "open" the blood brain barrier. Curr Neuropharmacol 2008; 6:179–192 [View Article]
     [Google Scholar]
124. He S, Wang L, Wu Y, Li D, Zhang Y. CCL3 and CCL20-recruited dendritic cells modified by melanoma antigen gene-1 induce anti-tumor immunity against gastric cancer ex vivo and in vivo . J Exp Clin Cancer Res 2010; 29:37 [View Article]
     [Google Scholar]
125. Baba T, Mukaida N. Role of macrophage inflammatory protein (MIP)-1α/CCL3 in leukemogenesis. Mol Cell Oncol 2014; 1:e29899 [View Article]
     [Google Scholar]
126. Zhang Y, Yoneyama H, Wang Y, Ishikawa S, Hashimoto S et al. Mobilization of dendritic cell precursors into the circulation by administration of MIP-1alpha in mice. J Natl Cancer Inst 2004; 96:201–209 [View Article]
     [Google Scholar]
127. Wen Y, Wang H, Wu H, Yang F, Tripp RA et al. Rabies virus expressing dendritic cell-activating molecules enhances the innate and adaptive immune response to vaccination. J Virol 2011; 85:1634–1644 [View Article]
     [Google Scholar]
128. Ushach I, Zlotnik A. Biological role of granulocyte macrophage colony-stimulating factor (GM-CSF) and macrophage colony-stimulating factor (M-CSF) on cells of the myeloid lineage. J Leukoc Biol 2016; 100:481–489 [View Article]
     [Google Scholar]
129. Wertel I, Surówka J, Polak G, Barczyński B, Bednarek W et al. Macrophage-derived chemokine CCL22 and regulatory T cells in ovarian cancer patients. Tumor Biol 2015; 36:4811–4817 [View Article]
     [Google Scholar]
130. Ramos HC, Rumbo M, Sirard JC. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 2004; 12:509–517 [View Article]
     [Google Scholar]
131. Zhou M, Zhang G, Ren G, Gnanadurai CW, Li Z et al. Recombinant rabies viruses expressing GM-CSF or flagellin are effective vaccines for both intramuscular and oral immunizations. PLoS One 2013; 8:e63384 [View Article]
     [Google Scholar]
132. Vempati UD, Diaz F, Barrientos A, Narisawa S, Mian AM et al. Role of cytochrome c in apoptosis: increased sensitivity to tumor necrosis factor alpha is associated with respiratory defects but not with lack of cytochrome c release. Mol Cell Biol 2007; 27:1771–1783 [View Article]
     [Google Scholar]
133. Pulmanausahakul R, Faber M, Morimoto K, Spitsin S, Weihe E et al. Overexpression of cytochrome c by a recombinant rabies virus attenuates pathogenicity and enhances antiviral immunity. J Virol 2001; 75:10800–10807 [View Article]
     [Google Scholar]
134. Irani DN. Regulated production of CXCL13 within the central nervous system. J Clin Cell Immunol 2016; 7:05 10 2016 [View Article]
     [Google Scholar]
135. Jogdand GM, Mohanty S, Devadas S. Regulators of Tfh cell differentiation. Front Immunol 2016; 7:520 [View Article]
     [Google Scholar]
136. Kerfoot SM, Yaari G, Patel JR, Johnson KL, Gonzalez DG et al. Germinal center B cell and T follicular helper cell development initiates in the interfollicular zone. Immunity 2011; 34:947–960 [View Article]
     [Google Scholar]
137. Wang Z, Li M, Zhou M, Zhang Y, Yang J et al. A novel rabies vaccine expressing CXCL13 enhances humoral immunity by recruiting both T follicular helper and germinal center B cells. J Virol 2017; 91: [View Article]
     [Google Scholar]
138. Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS et al. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005; 175:7867–7879 [View Article]
     [Google Scholar]
139. Zotos D, Coquet JM, Zhang Y, Light A, D'Costa K et al. IL-21 regulates germinal center B cell differentiation and proliferation through a B cell–intrinsic mechanism. J Exp Med 2010; 207:365–378 [View Article]
     [Google Scholar]
140. Ettinger R, Kuchen S, Lipsky PE. The role of IL-21 in regulating B-cell function in health and disease. Immunol Rev 2008; 223:60–86 [View Article]
     [Google Scholar]
141. Zhang Y, Zhou M, Wang Z, Yang J, Li M et al. Recombinant rabies virus expressing IL-21 enhances immunogenicity through activation of T follicular helper cells and germinal centre B cells. J Gen Virol 2016; 97:3154–3160 [View Article]
     [Google Scholar]
142. Steel JC, Waldmann TA, Morris JC. Interleukin-15 biology and its therapeutic implications in cancer. Trends Pharmacol Sci 2012; 33:35–41 [View Article]
     [Google Scholar]
143. Burton JD, Bamford RN, Peters C, Grant AJ, Kurys G et al. A lymphokine, provisionally designated interleukin T and produced by a human adult T-cell leukemia line, stimulates T-cell proliferation and the induction of lymphokine-activated killer cells. Proc Natl Acad Sci USA 1994; 91:4935–4939 [View Article]
     [Google Scholar]
144. Gordy LE, Bezbradica JS, Flyak AI, Spencer CT, Dunkle A et al. IL-15 regulates homeostasis and terminal maturation of NKT cells. J Immunol 2011; 187:6335–6345 [View Article]
     [Google Scholar]
145. Waldmann TA, Dubois S, Tagaya Y. Contrasting roles of IL-2 and IL-15 in the life and death of lymphocytes: implications for immunotherapy. Immunity 2001; 14:105–110 [View Article]
     [Google Scholar]
146. Chen T, Zhang Y, Wang Z, Yang J, Li M et al. Recombinant rabies virus expressing IL-15 enhances immunogenicity through promoting the activation of dendritic cells in mice. Virol Sin 2017; 32:317–327 [View Article]
     [Google Scholar]
147. Li Y, Zhou M, Luo Z, Zhang Y, Cui M et al. Overexpression of interleukin-7 extends the humoral immune response induced by rabies vaccination. J Virol 2017; 91: [View Article]
     [Google Scholar]
148. Kaplanski G. Interleukin-18: biological properties and role in disease pathogenesis. Immunol Rev 2018; 281:138–153 [View Article]
     [Google Scholar]
149. Gai W, Zheng W, Wang C, Wong G, Song Y et al. Immunization with recombinant rabies virus expressing interleukin-18 exhibits enhanced immunogenicity and protection in mice. Oncotarget 2017; 8:91505–91515 [View Article]
     [Google Scholar]
150. Luo J, Zhang B, Wu Y, Tian Q, Zhao J et al. Expression of interleukin-6 by a recombinant rabies virus enhances its immunogenicity as a potential vaccine. Vaccine 2017; 35:938–944 [View Article]
     [Google Scholar]
151. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003; 10:45–65 [View Article]
     [Google Scholar]
152. Apostolaki M, Armaka M, Victoratos P, Kollias G. Cellular mechanisms of TNF function in models of inflammation and autoimmunity. Curr Dir Autoimmun 2010; 11:1–26 [View Article]
     [Google Scholar]
153. Naudé PJ, den Boer JA, Luiten PG, Eisel UL. Tumor necrosis factor receptor cross-talk. FEBS J 2011; 278:888–898 [View Article]
     [Google Scholar]
154. Kollias G, Douni E, Kassiotis G, Kontoyiannis D. The function of tumour necrosis factor and receptors in models of multi-organ inflammation, rheumatoid arthritis, multiple sclerosis and inflammatory bowel disease. Ann Rheum Dis 1999; 58:i32–i39 [View Article]
     [Google Scholar]
155. Faber M, Bette M, Preuss MA, Pulmanausahakul R, Rehnelt J et al. Overexpression of tumor necrosis factor alpha by a recombinant rabies virus attenuates replication in neurons and prevents lethal infection in mice. J Virol 2005; 79:15405–15416 [View Article]
     [Google Scholar]
156. Lee EY, Schultz KL, Griffin DE. Mice deficient in interferon-gamma or interferon-gamma receptor 1 have distinct inflammatory responses to acute viral encephalomyelitis. PLoS One 2013; 8:e76412 [View Article]
     [Google Scholar]
157. Zaidi MR, Merlino G. The two faces of interferon-γ in cancer. Clin Cancer Res 2011; 17:6118–6124 [View Article]
     [Google Scholar]
158. Barkhouse DA, Garcia SA, Bongiorno EK, Lebrun A, Faber M et al. Expression of interferon gamma by a recombinant rabies virus strongly attenuates the pathogenicity of the virus via induction of type I interferon. J Virol 2015; 89:312–322 [View Article]
     [Google Scholar]
159. Ivashkiv LB, Donlin LT. Regulation of type I interferon responses. Nat Rev Immunol 2014; 14:36–49 [View Article]
     [Google Scholar]
160. Wang Y, Tian Q, Xu X, Yang X, Luo J et al. Recombinant rabies virus expressing IFNα1 enhanced immune responses resulting in its attenuation and stronger immunogenicity. Virology 2014; 468-470:621–630 [View Article]
     [Google Scholar]
161. Wang Z, Liang Q, Zhang Y, Yang J, Li M et al. An optimized HMGB1 expressed by recombinant rabies virus enhances immunogenicity through activation of dendritic cells in mice. Oncotarget 2017; 8:83539–83554 [View Article]
     [Google Scholar]
162. Zhang Y, Zhou M, Li Y, Luo Z, Chen H et al. Recombinant rabies virus with the glycoprotein fused with a DC-binding peptide is an efficacious rabies vaccine. Oncotarget 2018; 9:831–841 [View Article]
     [Google Scholar]
163. Curiel TJ, Morris C, Brumlik M, Landry SJ, Finstad K et al. Peptides identified through phage display direct immunogenic antigen to dendritic cells. J Immunol 2004; 172:7425–7431 [View Article]
     [Google Scholar]
164. Li L. The Analysis of the Growth Characteristics and the Animal Infection Characteristics of Different Host-Derived Street Rabies Virus [Masters Thesis] Changchun, China: Jilin University; 2014
     [Google Scholar]
165. Kang H, Qi Y, Wang H, Zheng X, Gao Y et al. Chimeric rabies virus-like particles containing membrane-anchored GM-CSF enhances the immune response against rabies virus. Viruses 2015; 7:1134–1152 [View Article]
     [Google Scholar]
166. Rasalingam P, Rossiter JP, Mebatsion T, Jackson AC. 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 2005; 111:55–60 [View Article]
     [Google Scholar]
167. Savina A, Amigorena S. Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 2007; 219:143–156 [View Article]
     [Google Scholar]
168. Zhao L, Toriumi H, Kuang Y, Chen H, Fu ZF. The roles of chemokines in rabies virus infection: overexpression may not always be beneficial. J Virol 2009; 83:11808–11818 [View Article]
     [Google Scholar]
169. Elena-Real CA, Díaz-Quintana A, González-Arzola K, Velázquez-Campoy A, Orzáez M et al. Cytochrome c speeds up caspase cascade activation by blocking 14-3-3ε-dependent Apaf-1 inhibition. Cell Death Dis 2018; 9:365 [View Article]
     [Google Scholar]
170. Martin SJ, Henry CM, Cullen SP. A perspective on mammalian caspases as positive and negative regulators of inflammation. Mol Cell 2012; 46:387–397 [View Article]
     [Google Scholar]
171. Eivazi S, Bagheri S, Hashemzadeh MS, Ghalavand M, Qamsari ES et al. Development of T follicular helper cells and their role in disease and immune system. Biomed Pharmacother 2016; 84:1668–1678 [View Article]
     [Google Scholar]
172. Manz RA, Radbruch A. Plasma cells for a lifetime?. Eur J Immunol 2002; 32:923–927 [View Article]
     [Google Scholar]
173. Saikh KU, Khan AS, Kissner T, Ulrich RG. IL-15-induced conversion of monocytes to mature dendritic cells. Clin Exp Immunol 2001; 126:447–455 [View Article]
     [Google Scholar]
174. Saikh KU, Kissner TL, Nystrom S, Ruthel G, Ulrich RG. Interleukin-15 increases vaccine efficacy through a mechanism linked to dendritic cell maturation and enhanced antibody titers. Clin Vaccine Immunol 2008; 15:131–137 [View Article]
     [Google Scholar]
175. Seo YB, Im SJ, Namkoong H, Kim SW, Choi YW et al. Crucial roles of interleukin-7 in the development of T follicular helper cells and in the induction of humoral immunity. J Virol 2014; 88:8998–9009 [View Article]
     [Google Scholar]
176. Stevceva L, Moniuszko M, Ferrari MG. Utilizing IL-12, IL-15 and IL-7 as mucosal vaccine adjuvants. Lett Drug Des Discov 2006; 3:586–592 [View Article]
     [Google Scholar]
177. Parrish YK, Baez I, Milford TA, Benitez A, Galloway N et al. IL-7 dependence in human B lymphopoiesis increases during progression of ontogeny from cord blood to bone marrow. J Immunol 2009; 182:4255–4266 [View Article]
     [Google Scholar]
178. Aliyari Z, Alami F, Mostafavi T, Taiefi Nasrabadi H, Soleimanirad J et al. The roles of IL-2, IL-7, and IL15 ligands in B cells development from cord blood mononuclear cells. Iran J Ped Hematol Oncol 2015; 5:155–160
     [Google Scholar]
179. Chen G, Ward MF, Sama AE, Wang H. Extracellular HMGB1 as a proinflammatory cytokine. J Interferon Cytokine Res 2004; 24:329–333 [View Article]
     [Google Scholar]
180. Mähl P, Cliquet F, Guiot AL, Niin E, Fournials E et al. Twenty year experience of the oral rabies vaccine SAG2 in wildlife: a global review. Vet Res 2014; 45:77 [View Article]
     [Google Scholar]
181. MacInnes CD, Smith SM, Tinline RR, Ayers NR, Bachmann P et al. Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis 2001; 37:119–132 [View Article]
     [Google Scholar]
182. Anindita PD, Sasaki M, Okada K, Ito N, Sugiyama M et al. Ribavirin-related compounds exert in vitro inhibitory effects toward rabies virus. Antiviral Res 2018; 154:1–9 [View Article]
     [Google Scholar]
183. Superti F, Seganti L, Panà A, Orsi N. Effect of amantadine on rhabdovirus infection. Drugs Exp Clin Res 1985; 11:69–74
     [Google Scholar]
184. Banyard AC, Mansfield KL, Wu G, Selden D, Thorne L et al. Re-evaluating the effect of Favipiravir treatment on rabies virus infection. Vaccine 201710 Nov 2017 [View Article]
     [Google Scholar]
185. Appolinario CM, Prehaud C, Allendorf SD, Antunes JM, Peres MG et al. Ribavirin has an in vitro antiviral effect in rabies virus infected neuronal cells but fails to provide benefit in experimental rabies in mice. J Virol Antivir Res 2013; 2:
     [Google Scholar]