High definition viral vaccine strain identity and stability testing using full-genome population data - The next generation of vaccine quality control

Vaccine

Volumn 33, Issue 43, 2015, Pages 5829-5837

  Höper, Dirk ^a   Freuling, Conrad M ^a   Müller, Thomas ^a   Hanke, Dennis ^a   von Messling, Veronika ^b   Duchow, Karin ^b   Beer, Martin ^a   Mettenleiter, Thomas C ^a  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Deep sequencing; Live attenuated vaccines; Population distance; Vaccine quality control; Viral population analysis

Indexed keywords

RABIES VACCINE; LIVE VACCINE; VIRUS RNA;

ARTICLE; BIOINFORMATICS; CONSENSUS SEQUENCE; CONTROLLED STUDY; DRUG STABILITY; GENETIC VARIABILITY; MOLECULAR PHYLOGENY; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; QUALITY CONTROL; SEQUENCE ANALYSIS; STRAIN IDENTIFICATION; VIRUS GENOME; VIRUS STRAIN; DNA SEQUENCE; GENETIC VARIATION; GENETICS; GENOMIC INSTABILITY; HUMAN; PHARMACEUTICS; POPULATION GENETICS; PROCEDURES; RABIES VIRUS; STANDARDS;

GENETIC VARIATION; GENETICS, POPULATION; GENOMIC INSTABILITY; HUMANS; QUALITY CONTROL; RABIES VACCINES; RABIES VIRUS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; TECHNOLOGY, PHARMACEUTICAL; VACCINES, ATTENUATED;

EID: 84944089007     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2015.08.091     Document Type: Article

References (56)

1. Hampson K., Coudeville L., Lembo T., Sambo M., Kieffer A., Attlan M., et al. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis 2015, 9:e0003709. 10.1371/journal.pntd.0003709.
2. Freuling C.M., Hampson K., Selhorst T., Schröder R., Meslin F.X., Mettenleiter T.C., et al. The elimination of fox rabies from Europe: determinants of success and lessons for the future. Philos Trans R Soc Lond Ser B Biol Sci 2013, 368:20120142. 10.1098/rstb.2012.0142.
3. MacInnes C.D., Smith S.M., Tinline R.R., Ayers N.R., Bachmann P., Ball D.G., et al. Elimination of rabies from red foxes in eastern Ontario. J Wildl Dis 2001, 37:119-132. 10.7589/0090-3558-37.1.119.
4. Rosatte R.C., Power M.J., Donovan D., Davies J.C., Allan M., Bachmann P., et al. Elimination of arctic variant rabies in red foxes, metropolitan Toronto. Emerg Infect Dis 2007, 13:25-27. 10.3201/eid1301.060622.
5. Sacramento D., Badrane H., Bourhy H., Tordo N. Molecular epidemiology of rabies virus in France: comparison with vaccine strains. J Gen Virol 1992, 73:1149-1158. 10.1099/0022-1317-73-5-1149.
6. Švrček Š., Ďurove A., Ondrejka R., Závadová J., Süliová J., Beníšek Z., et al. Immunogenic and antigenic activity of an experimental oral rabies vaccine prepared from the strain Vnukovo-32/107. Vet Med (Praha) 1995, 40:87-96.
7. Abelseth M.K. An attenuated rabies vaccine for domestic animals produced in tissue culture. Can Vet J 1964, 5:279-286.
8. Abelseth M.K. Propagation of rabies virus in pig kidney cell culture. Can Vet J 1964, 5:84-87.
9. Fenje P. Propagation of rabies virus in cultures of hamster kidney cells. Can J Microbiol 1960, 6:479-484.
10. Baer G.M., Abelseth M.K., Debbie J.G. Oral vaccination of foxes against rabies. Am J Epidemiol 1971, 93:487-490.
11. Häfliger U., Bichsel P., Wandeler A., Steck F. Zur oralen Immunisierung von Füchsen gegen Tollwut: Stabilisierung und Köderapplikation des Impfvirus. Zen Vet R B 1982, 29:604-618. 10.1111/j. 1439-0450.1982.tb01261.x.
12. Matouch O. The rabies situation in Eastern Europe. Dev Biol 2008, 131:27-35.
13. Schneider L.G., Cox J.H. Ein Feldversuch zur oralen Immunisierung von Füchsen gegen die Tollwut in der Bundesrepublik Deutschland: Unschädlichkeit, Wirksamkeit und Stabilität der Vakzine SAD B 19. Tierärztl Umsch 1983, 38:315-324.
14. Sinnecker H., Apitzsch L., Berndt D., Schrader C., Gogolin J., Egert J. Die Entwicklung des Tollwutlebendimpfvirus SAD/Potsdam 5/88 zur oralen Fuchsimpfung sowie seine Charakterisierung am Mausmodell. Mon Vet 1990, 45:77-78.
15. Schneider L.G. Tollwut-Lebendimpfstoff. European Patent 1993, Office 0 210 552 B1.
16. Bern. Vaccine 1994, 12:317-320. 10.1016/0264-410x(94)90095-7.
17. Mähl P., Cliquet F., Guiot A.L., Niin E., Fournials E., Saint-Jean N., et al. Twenty year experience of the oral rabies vaccine SAG2 in wildlife: a global review. Vet Res 2014, 45:77. 10.1186/s13567-014-0077-8.
18. Geue L., Schares S., Schnick C., Kliemt J., Beckert A., Freuling C., et al. Genetic characterisation of attenuated SAD rabies virus strains used for oral vaccination of wildlife. Vaccine 2008, 26:3227-3235. 10.1016/j.vaccine.2008.04.007.
19. Tuplin A. Diverse roles and interactions of RNA structures during the replication of positive-stranded RNA viruses of humans and animals. J Gen Virol 2015, 96:1497-1503. 10.1099/vir.0.000066.
20. European Medicines Agency Veterinary medicines and inspections. VICH topic GL41 - guideline on target animal safety: examination of live veterinary vaccines in target animals for absence of reversion to virulence 2007, European Medicines Agency, London.
21. Beckert A., Geue L., Vos A., Neubert A., Freuling C., Müller T. Genetic stability (in vivo) of the attenuated oral rabies virus vaccine SAD B19. Microbiol Immunol 2009, 53:16-21. 10.1111/j. 1348-0421.2008.00085.x.
22. Drake J.W. Rates of spontaneous mutation among RNA viruses. Proc Nat Acad Sci USA 1993, 90:4171-4175. 10.1073/pnas.90.9.4171.
23. Drake J.W., Holland J.J. Mutation rates among RNA viruses. Proc Nat Acad Sci USA 1999, 96:13910-13913. 10.1073/pnas.96.24.13910.
24. Lauring A.S., Andino R. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 2010, 6:e1001005. 10.1371/journal.ppat.1001005.
25. Domingo E., Sheldon J., Perales C. Viral quasispecies evolution. Microbiol Mol Biol Rev 2012, 76:159-216. 10.1128/MMBR. 05023-11.
26. Wright S. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Sixth International Congress on Genetics 1932, 356-366.
27. Kissi B., Badrane H., Audry L., Lavenu A., Tordo N., Brahimi M., et al. Dynamics of rabies virus quasispecies during serial passages in heterologous hosts. J Gen Virol 1999, 80(Pt 8):2041-2050. 10.1099/0022-1317-80-8-2041.
28. Benmansour A., Brahimi M., Tuffereau C., Coulon P., Lafay F., Flamand A. Rapid sequence evolution of street rabies glycoprotein is related to the highly heterogeneous nature of the viral population. Virology 1992, 187:33-45. 10.1016/0042-6822(92)90292-w.
29. Marston D.A., McElhinney L.M., Ellis R.J., Horton D.L., Wise E.L., Leech S.L., et al. Next generation sequencing of viral RNA genomes. BMC Gen 2013, 14:444. 10.1186/1471-2164-14-444.
30. Höper D., Finke S., Freuling C.M., Hoffmann B., Beer M. What can we learn about lyssavirus genomes using 454 sequencing. Berl Munch Tierarztl Wochenschr 2012, 125:242-248.
31. Flaherty P., Natsoulis G., Muralidharan O., Winters M., Buenrostro J., Bell J., et al. Ultrasensitive detection of rare mutations using next-generation targeted resequencing. Nucleic Acids Res 2012, 40:e2. 10.1093/nar/gkr861.
32. Acevedo A., Brodsky L., Andino R. Mutational and fitness landscapes of an RNA virus revealed through population sequencing. Nature 2014, 505:686-690. 10.1038/nature12861.
33. Schmitt M.W., Fox E.J., Prindle M.J., Reid-Bayliss K.S., True L.D., Radich J.P., et al. Sequencing small genomic targets with high efficiency and extreme accuracy. Nat Meth 2015, 12:423-425. 10.1038/nmeth.3351.
34. Cliquet F., Robardet E., Picard Meyer E. Genetic strain modification of a live rabies virus vaccine widely used in Europe for wildlife oral vaccination. Antivir Res 2013, 100:84-89. 10.1016/j.antiviral.2013.07.012.
35. Rupprecht C.E., Plotkin S.A. Rabies vaccines. Vaccines 2013, 646-668. Elsevier. 6th ed. S.A. Plotkin, W. Orenstein, P. Offit (Eds.).
36. Steck F., Wandeler A., Bichsel P., Capt S., Häfliger U., Schneider L. Oral immunization of foxes against rabies. Laboratory and field studies. Comp Immunol Microbiol Infect Dis 1982, 5:165-171. 10.1016/0147-9571(82)90031-5.
37. Vrzal V. Safety study of the Bio-10-SAD Bern strain of the rabies virus on the rhesus macaque monkey species. Acta Vet Brun 2013, 82:13-17. 10.2754/avb201382010013.
38. Höper D., Hoffmann B., Beer M. A comprehensive deep sequencing strategy for full-length genomes of influenza A. PLoS One 2011, 6:e19075. 10.1371/journal.pone.0019075.
39. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797. 10.1093/nar/gkh340.
40. R Development Core Team R: a language and environment for statistical computing. 3.1.0 ed. 2014, R Foundation for Statistical Computing, Vienna, Austria.
41. Wang C., Mitsuya Y., Gharizadeh B., Ronaghi M., Shafer R.W. Characterization of mutation spectra with ultra-deep pyrosequencing: application to HIV-1 drug resistance. Genome Res 2007, 17:1195-1201. 10.1101/gr.6468307.
42. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410. 10.1016/S0022-2836(05)80360-2.
43. Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015, 32:268-274. 10.1093/molbev/msu300.
44. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389.
45. Van De Peer Y. Phylogenetic inference based on distance methods. The phylogenetic handbook: a practical approach to phylogenetic analysis and hypothesis testing 2009, 142-180. Cambridge University Press, Cambridge. 2nd ed. P. Lemey, M. Salemi, A.-M. Vandamme (Eds.).
46. Eigen M. Viral quasispecies. Sci Am 1993, 269:42-49.
47. Eigen M., Schuster P. The hypercyde - a principle of natural self-organization. Part A: emergence of the hypercycle. Naturwissenschaften 1977, 64:541-565.
48. Burch C.L., Chao L. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 2000, 406:625-628. 10.1038/35020564.
49. Domingo E., Escarmís C., Sevilla N., Moya A., Elena S.F., Quer J., et al. Basic concepts in RNA virus evolution. FASEB J 1996, 10:859-864.
50. Steinhauer D.A., Holland J.J. Rapid evolution of RNA viruses. Annu Rev Microbiol 1987, 41:409-433. 10.1146/annurev.mi.41.100187.002205.
51. Lauring A.S., Frydman J., Andino R. The role of mutational robustness in RNA virus evolution. Nat Rev Microbiol 2013, 11:327-336. 10.1038/nrmicro3003.
52. Vignuzzi M., Stone J.K., Arnold J.J., Cameron C.E., Andino R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 2006, 439:344-348.
53. OIE Principles of veterinary vaccine production. Manual of diagnostic tests and vaccines for terrestrial animals 2015, International Office of Epizootics, Paris.
54. Center for Biologics Evaluation and Research Guidance for Industry. Characterization and qualification of cell substrates and other biological materials used in the production of viral vaccines for infectious disease indications. Food and drug administration, editor 2010, Department of Health and Human Services, Rockville, USA.
55. Committee for Medicinal Products for Human Use Guideline on influenza vaccines - quality module 2014, 34. European Medicines Agency, London, United Kingdom.
56. WHO Expert Committee on Biological Standardization WHO Expert Committee on Biological Standardization - Sixty-third report 2012, World Health Organization, Geneva, Switzerland.