From brain passage to cell adaptation: the road of human rabies vaccine development

References

• Pasteur L, Chamberland CE, Roux E. Methode pour prevenir la rage après morsue (in French). C. R. Acad. Sci.101, 765–774 (1885).
   Google Scholar
• M. Pasteur on the virus of rabies, medical progress: medicine. JAMA3, 40–41 (1884).
   Google Scholar
• Constantine DG. Geographic translocaton of bats: known and potential problems. Emerg. Infect. Dis.9, 17–21 (2003).
   PubMed Web of Science ®Google Scholar
• Marano N, Arguin PM, Pappaioanou M. Impact of globalization and animal trade on infectious disease ecology. Emerg. Infect. Dis.13, 1807–1809 (2007).
   PubMedGoogle Scholar
• Castrodale L, Walker V, Baldwin J, Hofmann J, Hanlon C. Rabies in a puppy imported from India to the USA. March 2007. Zoonoses Public Health55, 427–430 (2008).
   PubMed Web of Science ®Google Scholar
• Meng S, Sun Y, Wu X et al. Evolutionary dynamics of rabies viruses highlights the importance of China rabies transmission in Asia. Virology410, 403–409 (2011).
   PubMedGoogle Scholar
• Malerczyk C, Nel LH, Gniel D, Blumberg L. Rabies in South Afica and the FIFA Soccer World Cup: travelers’ awareness for an endemic but neglected disease. Hum. Vaccine6, 385–389 (2010).
   PubMed Web of Science ®Google Scholar
• Yamamoto S, Iwasaki C, Oono H, Ninomiya K, Matsumura T. The first imported case of rabies into Japan in 36 years: a forgotton life-threatening disease. J. Travel Med.15, 372–374 (2008).
   PubMedGoogle Scholar
• Smith J, McElhinney L, Parsons G et al. Case report: rapid ante-mortem diagnosis of a human case of rabies imported into the UK from the Philippines. J. Med. Virol.69, 150–155 (2003).
   PubMedGoogle Scholar
• Watson EM. The negri bodies in rabies. J. Exp. Med.17(1), 29–42 (1913).
   PubMedGoogle Scholar
• The Pasteur treatment of hydrophobia. JAMA17, 376–378 (1891).
   Google Scholar
• Théodoridés J. Pasteur and rabies: the British connection. J. Royal Soc. Med.82, 488–490 (1989).
   PubMed Web of Science ®Google Scholar
• Burke DS. Joseph-Alexandre Auzias-Turenne, Louis Pasteur, and early concepts of virulence, attenuation, and vaccination. Perspective Biol. Med.39, 171–186 (1996).
   PubMedGoogle Scholar
• Gelfand T. 11 January 1887, the day medicine changed: Joseph Grancher’s defense of Pasteur’s treatment for rabies. Bull. Hist. Med.76, 698–718 (2002).
   PubMedGoogle Scholar
• Fermi C. Über die Immunisierung gegen Wutkrankheit (in German). Z. Hyg. Infectionskrankh.58, 233–276 (1908).
   Google Scholar
• Semple D. The preparation of a safe and efficient antirabic vaccine. Sci. Mem. Med. Sanit. Dept. India.44 (1911).
   Google Scholar
• Sudarshan MK, Bhardwaj S, Mahendra BJ et al. An immunogenicity, safety and post-marketing surveillance of a novel adsorbed human diploid cell rabies vaccine (Rabivax) in Indian subjects. Hum. Vaccines4, 275–279 (2009).
   Google Scholar
• Svet-Moldavskij G, Andjaparidze O, Unanov S et al. An allergen-free antirabies vaccine. Bull. World Health Organ.32, 47–58 (1965).
   PubMedGoogle Scholar
• Fuenzalida E, Palacios R, Borgono JM. Anti-rabies antibody responses in man to vaccine made from infected suckling-mouse brains. Bull. World Health Organ.30, 431–436 (1964).
   PubMedGoogle Scholar
• McKendrick AG. A ninth analytical review of reports from Pasteur Institute on the results of anti-rabies treatment. Bull. Hlth Org.9, 31–78 (1940).
   Google Scholar
• Greenwood M. Tenth report on data of antirabies treatment supplied by Pasteur Institute. Bull. Hlth Org.12, 301–364 (1945).
   Google Scholar
• Sellers TF. Rabies, the physician’s dilemma. Am. J. Trop. Med. Hyg.28, 453–456 (1948).
   PubMedGoogle Scholar
• Bonito RF, de Oliveira NM, Nishioka Sde A. Adverse reactions associated with a Fuenzalida-Palacios rabies vaccine: a quasiexperimental study. Rev. Soc. Bras. Med. Trop.37, 7–9 (2004).
   PubMedGoogle Scholar
• Goodpasture EW, Woodruff AM, Buddingh GJ. The cultivation of vaccine and other viruses in the chorioallantoic membrane of chick embryos. Science74, 371–372 (1931).
   PubMedGoogle Scholar
• Koprowski L, Cox HR. Studies on chick embryo adapted rabies virus: I. Culture characteristics and pathogenicity. J. Immunol.60, 533–554 (1948).
   PubMed Web of Science ®Google Scholar
• Koprowski L, Black J. Studies on chick embryo adapted rabies virus: II. Pathogenicity for dogs and use of egg-adapted strains for vaccination purpose. J. Immunol.64, 185–196 (1950).
   PubMedGoogle Scholar
• Koprowski L, Black J. Studies on chick embryo adapted rabies virus: IV. Immunization of guinea-pigs and description of a potency control test. J. Immunol.72, 79–84 (1954).
   PubMedGoogle Scholar
• Koprowski L, Black J. Studies on chick embryo adapted rabies virus: V. Protection of animals with antiserum and living attenuated virus after exposure to street strain of rabies virus. J. Immunol.72, 85–93 (1954).
   PubMedGoogle Scholar
• Koprowski L, Black J, Nelsen DJ. Studies on chick embryo adapted rabies virus: VI. Further changes in pathogenic properties following prolonged cultivation in the developing chick embryo. J. Immunol.72, 94–106 (1954).
   PubMedGoogle Scholar
• Koprowski L, Black J. Studies on chick embryo adapted rabies virus: VII. Immunological responses of animals to vaccination with high egg passage Flury strain. J. Immunol.72, 503–510 (1954).
   PubMedGoogle Scholar
• Leach CN, Johnson HN. Human rabies, with special reference to virus distribution and titer. Am. J. Trop. Med. Hyg.20, 335–340 (1940).
   Google Scholar
• Fox JP, Koprowski H, Conwell DP, Black J, Gelfand HM. Study of antirabies immunization of man. Observations with HEP Flury and other vaccines, with and without hyperimmune serum, in primary and recall immunizations. Bull. Org. Mond. Sante. Bull. Wld Hlth Org.17, 869–904 (1957).
   PubMedGoogle Scholar
• Peck FB, Powell HM, Culbertson CG. A new antirabies vaccine for human use. Appl. Microbiol.679–683 (1955).
   Google Scholar
• Vodopija I, Clarke HF. Human vaccination against rabies. In: The Natural History of Rabies (2nd Edition). Baer GM (Ed.). CRC Press, FL, USA, 571–595 (1991).
   Google Scholar
• Sabin AB. Experiments on the purification and concentration of the virus of poliomyelitis. J. Exp. Med.56, 307–317 (1932).
   PubMedGoogle Scholar
• Enders JF, Robbins FC, Weller TH. Classics in infectious diseases: the cultivation of the poliomyelitis virus in tissue culture. Nobel lecture, delivered at the Karolinska Institute, Stockholm, Sweden, on Dec 11, 1954. Rev. Infect. Dis.2, 493–504 (1980).
   PubMedGoogle Scholar
• Enders JF, Weller TH, Robbins FC. Cultivation of Lansing strain of poliomyelitis virus in culture of various human embryonic tissues. Science109, 85–87 (1949).
   PubMed Web of Science ®Google Scholar
• Norrby E. Nobel prize and the emerging virus concept. Arch. Virol.153, 1109–1123 (2008).
   PubMedGoogle Scholar
• Atanasiu P, Laurent C. Multiplication of the virus of rabies of dogs on a glial cell (mouse ependymoma) in tissue culture: histological aspect (in French). C. R. Hebd. Seances Acad. Sci.245, 2562–2564 (1957).
   PubMedGoogle Scholar
• Kissling RE. Growth of rabies virus in non-nervous tissue culture. Proc. Soc. Exp. Biol. Med.98, 223–225 (1958).
   PubMed Web of Science ®Google Scholar
• Kissling RE, Reese DR. Anti-rabies vaccine of tissue culture origin. J. Immun.91, 362–368 (1963).
   PubMed Web of Science ®Google Scholar
• Fenje P. A rabies vaccine from hamster kidney tissue cultures: preparation and evaluation in animals. Can. J. Microbiol.6, 605–609 (1960).
   PubMed Web of Science ®Google Scholar
• Mitchell JR, Everest RE, Anderson GR. Sensitive procedure for detecting residual viable virus in inactivated rabies vaccine. Appl. Microbiol.22, 600–603 (1971).
   PubMedGoogle Scholar
• Sureau P. Rabies vaccine production in animal cell cultures. Adv. Biochem. Eng. Biotechnol.34, 111–128 (1987).
   PubMedGoogle Scholar
• Lin F, Zeng F, Lu L et al. The primary hamster kidney cell rabies vaccine: adaptation of viral strain, production of vaccine, and pre- and postexposure treatment. J. Infect. Dis.147, 467–473 (1983).
   PubMed Web of Science ®Google Scholar
• Lin F. The protective effects of the large-scale use of PHKC rabies vaccine in humans in China. Bull. Wld. Hlth. Org.68, 449–454 (1990).
   PubMedGoogle Scholar
• Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp. Cell Res.25, 585–621 (1961).
   PubMed Web of Science ®Google Scholar
• Hayflick L. The coming of age of WI-38. Adv. Cell Culture3, 303–316 (1984).
   Google Scholar
• Hayflick L, Plotkin SA, Norton TW, Koprowski H. Preparation of poliovirus vaccines in a human fetal diploid cell strain. Am. J. Hyg.75, 240–258 (1962).
   PubMedGoogle Scholar
• Fernandes MV, Wiktor TJ, Koprowski H. Mechanism of the cytopathic effect of rabies virus in tissue culture. Virology21, 128–131 (1963).
   PubMedGoogle Scholar
• Wiktor TJ, Fernandes MV, Koprowski H. Cultivation of rabies virus in human diploid cell strain WI-38. J. Immunol.93, 353–366 (1964).
   PubMed Web of Science ®Google Scholar
• Petricciani J, Sheets R. An overview of animal cell substrates for biological products. Biologicals36, 359–362 (2008).
   PubMed Web of Science ®Google Scholar
• Jacob JP, Jones CM, Baille JP. Characterization of a human diploid cell designated MRC-5. Nature277, 168 (1970).
   Google Scholar
• Bernard KW, Smith PW, Kader FJ, Moran MJ. Neuroparalytic illness and human diploid cell rabies vaccine. JAMA248, 3136–3138 (1982).
   PubMedGoogle Scholar
• Boe E, Nyland H. Guillain-Barré syndrome after vaccination with human diploid cell rabies vaccine. Scand. J. Infect. Dis.12, 231–232 (1980).
   PubMed Web of Science ®Google Scholar
• Burgoyne GH, Kajiya KD, Brown WE, Mitchell JR. Rhesus diploid rabies vaccine (adsorbed): a new rabies vaccine using FRhL-2 cells. J. Infect. Dis.152, 204–210 (1985).
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention. Current trends rabies vaccine, adsorbed: a new rabies vaccine for use in humans. MMWR Morb. Mortal. Wkly Rep.37, 217–218, 223 (1988).
   PubMedGoogle Scholar
• Lavender JF, Frank RM. Zonal-centrifuged purified duck embryo cell culture rabies vaccine for human vaccination. Appl. Microbiol.22, 358–365 (1971).
   PubMedGoogle Scholar
• Ashwathnarayana DH, Madhusudana SN, Sampath G et al. A comparative study on the safety and immunogenicity of purified duck embryo cell vaccine (PDEV, Vaxirab) with purified chick embryo cell vaccine (PCEC, Rabipur) and purified Vero cell rabies vaccine (PVRV, Verorab). Vaccine28, 148–151 (2010).
   Google Scholar
• Torlone V, Titoli F. Development and diffusion of the rabies virus (Flury HEP strain) in embryonated egg and its multiplication on trypsinized cells of infected chick embryo (In Italian). Nuovi. Ann. Ig. Microbio.15, 263–264 (1964).
   PubMedGoogle Scholar
• Kondo A. Growth characteristics of rabies virus in primary chicken embryo cells. Virology27, 199–204 (1965).
   PubMed Web of Science ®Google Scholar
• Barth R, Gruschkau H, Bijok U et al. A new inactivated tissue culture rabies vaccine for use in human evaluation of PCEC-vaccine by laboratory tests. J. Biological Stand.12, 29–46 (1984).
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention. Notice to readers availability of new rabies vaccine for human use. MMWR Morb. Mortal. Wkly Rep.47, 12, 19 (1998).
   PubMedGoogle Scholar
• Sedwick WD, Wiktor TJ. Reproducible plaguing system for rabies, lymphocytic choriomeningitis and other ribonucleic acid viruses in BHK-21/13S agarose suspensions. J. Virol.1, 1224–1226 (1967).
   PubMedGoogle Scholar
• Yasumura Y, Kawakita Y. Study of SV40 in tissue culture (in Japanese). Nippon Rinsho21, 1201–1205 (1963).
   Google Scholar
• Debbie JG, Andrulonis JA, Abelseth MK. Rabies antibody determination by immunofluorescence in tissue culture. Infect. Immun.5, 902–904 (1972).
   PubMedGoogle Scholar
• Buckley SM, Tignor GH. Plaque assay for rabies serogroup viruses in Vero cells. J. Clin. Microbiol.1, 241–242 (1975).
   PubMedGoogle Scholar
• Pullen K, Johnston MD, Philips AW, Ball GD, Finter WB. Very large scale suspension cultures of mammalian cells. Dev. Biol. Standard60, 175–177 (1984).
   Google Scholar
• Roumiantzeff M, Ajjan N, Branche R et al. Rabies vaccine produced in cell culture: production and control and clinical results. In: Applied Virology. Kurstak (Ed.). Academic Press, FL, USA, 241–296 (1984).
   Google Scholar
• Fournier P, Montagnon B, Vincent-Falquet JC, Ajjan N, Drucker J, Roumiantzeff M. A new vaccine produced from rabies virus cultivated on Vero cells. In: Improvements in Rabies Post-Exposure Treatment. Vodopija I, Nicholson KG, Smerdel S, Bijok U (Eds). Institute of Public Health, Zagreb, Croatia (1985).
   Google Scholar
• Suntharasamai P, Chanthavanich P, Warrell MJ et al. Purified Vero cell rabies vaccine and human diploid cell strain vaccine: comparison of neutralizing antibody responses to post-exposure regimens. J. Hyg.96, 483–489 (1986).
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention. Rabies in a laboratory worker – New York. MMWR Morb. Mortal. Wkly Rep.26, 183–184 (1977).
   Google Scholar
• Sacramento D, Badrane H, Bourhy H, Tordo N. Molecular epidemiology of rabies virus in France: comparison with vaccine strains. J. Gen. Virol.73, 1149–1158 (1992).
   PubMedGoogle Scholar
• Pará M. An outbreak of post-vaccinal rabies (Rage de Laboratoire) in Fortaleza, Brazil, in 1960: residual fixed virus as the etiological agent. Bull. Org. mond. Santé/Bull. World Health Organ.33, 177–182 (1965).
   PubMed Web of Science ®Google Scholar
• Abelseth MK. Further studies on the use of ERA rabies vaccine in domestic animals. Can. Vet. J.8, 221–227 (1967).
   PubMedGoogle Scholar
• Fehlner-Gardiner C, Nadin-Davis S, Armstrong J, Muldoon F, Bachmann P, Wandeler A. ERA vaccine-derived cases of rabies in wildlife and domestic animals in Ontario, Canada, 1989–2004. J. Wildl. Dis.44, 71–85 (2008).
   PubMedGoogle Scholar
• Follmann EH, Ritter DG, Baer GM. Evaluation of the safety of two attenuated oral rabies vaccines, SAG1 and SAG2, in six Arctic mammals. Vaccine14, 270–273 (1996).
   PubMedGoogle Scholar
• Wang C, Zhang X, Song Q, Tang K. Promising rabies vaccine for postexposure prophylaxis in developing countries, a purified Vero cell vaccine produced in China. Clin. Vaccine Immunol.17, 688–690 (2010).
   PubMedGoogle Scholar
• Schnell MJ, Mebatsion T, Conzelmann KK. Infectious rabies viruses from cloned cDNA. EMBO J.13, 4195–4203 (1994).
   PubMed Web of Science ®Google Scholar
• Inoue K, Shoji Y, Kurane I, lijima T, Sakai T, Morimoto K. An improved method for recovering rabies virus from cloned cDNA. J. Virol. Methods107, 229–236 (2003).
   PubMed Web of Science ®Google Scholar
• Wu X, Franka R, Velasco-Villa A, Rupprecht CE. Are all lyssavirus genes equal for phylogenetic analyses? Virus Res.129, 91–103 (2007).
   PubMedGoogle Scholar
• Wu X, Rupprecht CE. Glycoprotein gene relocation in rabies virus. Virus Res.131, 95–99 (2008).
   PubMedGoogle Scholar
• Shantavasinkul P, Tantawichien T, Wilde H et al. Postexposure rabies prophylaxis completed in 1 week: preliminary study. Clin Infect Dis.50, 56–60 (2010).
   PubMed Web of Science ®Google Scholar
• Sudarshan MK, Madhusudana SN, Mahendra BJ. Post-exposure prophylaxis with purified Vero cell vaccine during pregnancy-safety and immunogenicity. J. Commun. Dis.31, 229–236 (1999).
   PubMedGoogle Scholar
• Ajjan N, Pilet C. Comparative study of the safety and protective value, in pre-exposure use, of rabies vaccine cultivated on human diploid cells (HDCV) and of the new vaccine grown on Vero cells. Vaccine7, 125–128 (1989).
   PubMedGoogle Scholar
• Arai YT, Montalban CS. Comparative studies on chick embryo cell rabies vaccine and human diploid cell vaccine: pre-exposure use and purity of the vaccines. Southeast Asian J. Trop. Med. Public Health24, 747–750 (1993).
   PubMedGoogle Scholar
• Dietzschold B, Hooper DC. Human diploid cell culture rabies vaccine (HDCV) and purified chick embryo cell culture rabies vaccine (PCECV) both confer protective immunity against infection with the silver-haired bat rabies virus strain (SHBRV). Vaccine16, 1656–1659 (1998).
   PubMed Web of Science ®Google Scholar
• Sabchareon A, Lang J, Attanath P et al. A new Vero cell rabies vaccine: results of a comparative trial with human diploid cell rabies vaccine in children. Clin. Infect. Dis.29, 141–149 (1999).
   PubMedGoogle Scholar
• Jones RL, Froeschle JE, Atmar RL et al. Immunogenicity, safety and lot consistency in adults of a chromatographically purified Vero-cell rabies vaccine: a randomized, double-blind trial with human diploid cell rabies vaccine. Vaccine19, 4635–4643 (2001).
   PubMed Web of Science ®Google Scholar
• Madhusudana SN, Sanjay TV, Mahendra BJ et al. Comparison of safety and immunogenicity of purified chick embryo cell rabies vaccine (PCECV) and purified Vero cell rabies vaccine (PVRV) using the Thai Red Cross intradermal regimen at a dose of 0.1 ML. Hum. Vaccine2, 200–204 (2006).
   PubMed Web of Science ®Google Scholar
• WHO. The immunological basis for immunization series. Rabies17, 1–23 (2011).
   Google Scholar
• Cox JH, Schneider LG. Prophylactic immunization of humans against rabies by intradermal inoculation of human diploid cell culture vaccine. J. Clin Microbiol.3, 96–101 (1976).
   PubMed Web of Science ®Google Scholar
• Harverson G. Post-exposure intradermal antirabies vaccine: a cheaper alternative for developing countries. Trop. Doct.14, 67–70 (1984).
   PubMedGoogle Scholar
• Centers for Disease Control and Prevention. Recommendation of the Immunization Practices Advisory Committee (ACIP). Supplementary statement on pre-exposure rabies prophylaxis by the intradermal route. MMWR Morb. Mortal. Wkly Rep.31, 285, 279–280 (1982).
   PubMedGoogle Scholar
• WHO Expert Committee on rabies. World Health Organ. Tech. Rep. Ser.824, 1–84 (1992).
   PubMedGoogle Scholar
• Osinubi MO, Wu X, Franka R et al. Enhancing comparative rabies DNA vaccine effectiveness through glycoprotein gene modification. Vaccine27, 7214–7218 (2009).
   PubMed Web of Science ®Google Scholar
• Gupta PK, Dahiya SS, Kumar P et al. Sindbis virus replicon-based DNA vaccine encoding rabies virus glycoprotein elicits specific humoral and cellular immune responses in dogs. Acta Virol.53, 83–88 (2009).
   PubMedGoogle Scholar
• Kaur M, Rai A, Bhatnagar R. Rabies DNA vaccine: no impact of MHC class I and class II targeting sequences on immune response and protection against lethal challenge. Vaccine27, 2128–2137 (2009).
   PubMed Web of Science ®Google Scholar
• Chen H, Xiang ZQ, Li Y et al. Adenovirus-based vaccines: comparison of vectors from three species of adenoviridae. J. Virol.84, 10522–10532 (2010).
   PubMed Web of Science ®Google Scholar
• Bouet-Cararo C, Contreras V, Fournier A et al. Canine adenoviruses elicit both humoral and cell-mediated immune responses against rabies following immunization of sheep. Vaccine29, 1304–1310 (2011).
   PubMedGoogle Scholar
• Wayer J, Rupprecht CE, Nel LH. Poxvirus-vectored vaccines for rabies – a review. Vaccine27, 7198–7201 (2009).
   PubMedGoogle Scholar
• Smith TG, Wu X, Franka R, Rupprecht CE. Design of future rabies biologics and antiviral drugs. Adv. Virus Res.79, 345–363 (2011).
   PubMed Web of Science ®Google Scholar
• Faber M, Li J, Kean RB, Hooper DC, Alugupalli KR, Dietzschold B. Effective preexposure and postexposure of rabies with a highly attenuated recombinant rabies virus. Proc. Natl Acad. Sci. USA106, 11300–11305 (2009).
   PubMed Web of Science ®Google Scholar
• Gomme EA, Faul EJ, Flomenberg P, McGettigan JP, Schnell MJ. Characterization of a single-cycle rabies virus-based vaccine vector. J. Virol.84, 2820–2831 (2010).
   PubMedGoogle Scholar
• Wu X, Franka R, Henderson H, Rupprecht CE. Live attenuated rabies virus co-infected with street rabies virus protects animals against rabies. Vaccine29, 4195–4201 (2011).
   PubMedGoogle Scholar
• Lang J, Feroldi E, Vien NC. Pre-exposure purified Vero cell rabies vaccine and concomitant routine childhood vaccinations: 5-year post-vaccination follow-up study of an infant cohort in Vietnam. J. Trop. Pediatr.55, 26–31 (2009).
   PubMedGoogle Scholar