Productivity, apoptosis, and infection dynamics of influenza A/PR/8 strains and A/PR/8-based reassortants

Vaccine

Volumn 30, Issue 35, 2012, Pages 5253-5261

  Isken, B ^a   Genzel, Y ^a   Reichl, U ^a,b  

^a MAX PLANCK INSTITUTE FOR DYNAMICS OF COMPLEX TECHNICAL SYSTEMS   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Flow cytometry; Infection dynamics; Influenza vaccine; Multiplicity of infection; TCID50

Indexed keywords

INFLUENZA VACCINE;

APOPTOSIS; ARTICLE; CELL POPULATION; FLOW CYTOMETRY; GENETIC REASSORTMENT; INFLUENZA VIRUS A; PRIORITY JOURNAL; STIRRED REACTOR; VACCINE PRODUCTION; VIRION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS STRAIN;

ANIMALS; APOPTOSIS; BIOREACTORS; CELL CULTURE TECHNIQUES; DOGS; FLOW CYTOMETRY; INFLUENZA A VIRUS; INFLUENZA VACCINES; MADIN DARBY CANINE KIDNEY CELLS; REASSORTANT VIRUSES; VIRUS CULTIVATION; VIRUS REPLICATION;

EID: 84863830949     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.05.065     Document Type: Article

References (45)

1. Tree J.A., Richardson C., Fooks A.R., Clegg J.C., Looby D. Comparison of large-scale mammalian cell culture systems with egg culture for the production of influenza virus A vaccine strains. Vaccine 2001, 19(May (25-26)):3444-3450.
2. Audsley J.M., Tannock G.A. Cell-based influenza vaccines: progress to date. Drugs 2008, 68(11):1483-1491.
3. Wood J.M., Oxford J.S., Dunleavy U., Newman R.W., Major D., Robertson J.S. Influenza A (H1N1) vaccine efficacy in animal models is influenced by two amino acid substitutions in the hemagglutinin molecule. Virology 1989, 171(July (1)):214-221.
4. Katz J.M., Webster R.G. Efficacy of inactivated influenza A virus (H3N2) vaccines grown in mammalian cells or embryonated eggs. J Infect Dis 1989, 160(August (2)):191-198.
5. Barrett P.N., Berezuk G., Fritsch S., Aichinger G., Hart M.K., El-Amin W., et al. Efficacy, safety, and immunogenicity of a Vero-cell-culture-derived trivalent influenza vaccine: a multicentre, double-blind, randomised, placebo-controlled trial. Lancet 2011, 377(February (9767)):751-759.
6. Genzel Y., Reichl U. Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines 2009, 8(December (12)):1681-1692.
7. Feng S.Z., Jiao P.R., Qi W.B., Fan H.Y., Liao M. Development and strategies of cell-culture technology for influenza vaccine. Appl Microbiol Biotechnol 2011, 89(February (4)):893-902.
8. Gregersen J.P., Schmitt H.J., Trusheim H., Broker M. Safety of MDCK cell culture-based influenza vaccines. Future Microbiol 2011, 6(February (2)):143-152.
9. Genzel Y., Dietzsch C., Rapp E., Schwarzer J., Reichl U. M.D.C.K. Vero cells for influenza virus vaccine production: a one-to-one comparison up to lab-scale bioreactor cultivation. Appl Microbiol Biotechnol 2010, 88(September (2)):461-475.
10. WHO guidance on development of influenza vaccine reference viruses by reverse genetics July 2005, Department of Communicable Disease Surveillance and Response.
11. Price G.E., Smith H., Sweet C. Differential induction of cytotoxicity and apoptosis by influenza virus strains of differing virulence. J Gen Virol 1997, 78(November (Pt 11)):2821-2829.
12. Voeten J.T., Brands R., Palache A.M., van Scharrenburg G.J., Rimmelzwaan G.F., Osterhaus A.D., et al. Characterization of high-growth reassortant influenza A viruses generated in MDCK cells cultured in serum-free medium. Vaccine 1999, 17(April (15-16)):1942-1950.
13. Hornickova Z. Different progress of MDCK cell death after infection by two different influenza virus isolates. Cell Biochem Funct 1997, 15(June (2)):87-93.
14. Mersich S.E., Baumeister E.G., Riva D., Lewis A.P., Cadario M.E., Pontoriero A.V., et al. Influenza circulating strains in Argentina exhibit differential induction of cytotoxicity and caspase-3 in vitro. J Clin Virol 2004, 31(October (2)):134-139.
15. Morris S.J., Nightingale K., Smith H., Sweet C. Influenza A virus-induced apoptosis is a multifactorial process: exploiting reverse genetics to elucidate the role of influenza A virus proteins in virus-induced apoptosis. Virology 2005, 335(2):198-211.
16. Jaberhossain M., Mori I., Liu B., Kimura Y. Influenza A virus derived from persistently virus-infected cells shows attenuated cytotoxicity in cultured cells but virulent pathogenicity in mice. Microb Pathog 2008, 44(5):417-425.
17. McLean J.E., Datan E., Matassov D., Zakeri Z.F. Lack of bax prevents influenza A virus-induced apoptosis and causes diminished viral replication. J Virol 2009, 83(16):8233-8246.
18. Stray S.J., Air G.M. Apoptosis by influenza viruses correlates with efficiency of viral mRNA synthesis. Virus Res 2001, 77(September (1)):3-17.
19. Lonsdale R., Pau M.G., Oerlemans M., Ophorst C., Vooys A., Havenga M., et al. A rapid method for immunotitration of influenza viruses using flow cytometry. J Virol Methods 2003, 110(June (1)):67-71.
20. Schulze-Horsel J., Schulze M., Agalaridis G., Genzel Y., Reichl U. Infection dynamics and virus-induced apoptosis in cell culture-based influenza vaccine production-flow cytometry and mathematical modeling. Vaccine 2009, 27(May (20)):2712-2722.
21. Kalbfuss B., Knochlein A., Krober T., Reichl U. Monitoring influenza virus content in vaccine production: precise assays for the quantitation of hemagglutination and neuraminidase activity. Biologicals 2008, 36(May (3)):145-161.
22. Genzel Y., Reichl U. Vaccine production-state of the art and future needs in upstream processing. Animal cell biotechnology: methods and protocols 2007, 457-473. Humana Press Inc. R. Poertner (Ed.).
23. Budowsky E.I., Zalesskaya M.A. Principles of selective inactivation of viral genome. V. Rational selection of conditions for inactivation of the viral suspension infectivity to a given extent by the action of beta-propiolactone. Vaccine 1991, 9(May (5)):319-325.
24. Budowsky E.I., Friedman E.A., Zheleznova N.V., Noskov F.S. Principles of selective inactivation of viral genome. VI. Inactivation of the infectivity of the influenza virus by the action of beta-propiolactone. Vaccine 1991, 9(June (6)):398-402.
25. Virology methods manual 1996, Academic Press, London. B. Mahy, H. Kangro (Eds.).
26. Schulze-Horsel J., Genzel Y., Reichl U. Flow cytometric monitoring of influenza A virus infection in MDCK cells during vaccine production. BMC Biotechnol 2008, 8:45.
27. Isken B., Schulze-Horsel J., Bock A., Genzel Y., Reichl U. Monitoring of host-cell infection and virus-induced apoptosis in influenza vaccine production. 21st annual meeting of the European society for animal cell technology 2009, Springer, Dublin. N. Jenkins (Ed.).
28. Sidorenko Y., Schulze-Horsel J., Voigt A., Reichl U., Kienle A. Stochastic population balance modeling of influenza virus replication in vaccine production processes. Chem Eng Sci 2008, 63:157-169.
29. Müller T., Dürr R., Isken B., Schulze-Horsel J., Reichl U., Kienle A. Population balance modelling of influenza virus replication during vaccine production-influence of apoptosis. 21st European symposium on computer aided process engineering 2011, Elsevier, Chalkidiki. E.N. Pistikopoulos, M.C. Georgiadis, A.C. Kokossis (Eds.).
30. Aggarwal K., Jing F., Maranga L., Liu J. Bioprocess optimization for cell culture based influenza vaccine production. Vaccine 2011, 29(April (17)):3320-3328.
31. Mohler L., Flockerzi D., Sann H., Reichl U. Mathematical model of influenza A virus production in large-scale microcarrier culture. Biotechnol Bioeng 2005, 90(April (1)):46-58.
32. Genzel Y., Olmer R.M., Schafer B., Reichl U. Wave microcarrier cultivation of MDCK cells for influenza virus production in serum containing and serum-free media. Vaccine 2006, 24(August (35-36)):6074-6087.
33. Rimmelzwaan G.F., Baars M., Claas E.C., Osterhaus A.D. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J Virol Methods 1998, 74(September (1)):57-66.
34. Maranga L., Brazao T.F., Carrondo M.J. Virus-like particle production at low multiplicities of infection with the baculovirus insect cell system. Biotechnol Bioeng 2003, 84(October (2)):245-253.
35. Carinhas N., Bernal V., Yokomizo A.Y., Carrondo M.J., Oliveira R., Alves P.M. Baculovirus production for gene therapy: the role of cell density, multiplicity of infection and medium exchange. Appl Microbiol Biotechnol 2009, 81(January (6)):1041-1049.
36. Nayak D.P., Chambers T.M., Akkina R.K. Defective-interfering (DI) RNAs of influenza viruses: origin, structure, expression, and interference. Curr Top Microbiol Immunol 1985, 114:103-151.
37. Marcus P.I. Interferon induction by viruses. IX. Antagonistic activities of virus particles modulated interferon production. J Interferon Res 1982, 2(4):511-518.
38. Marcus P.I., Rojek J.M., Sekellick M.J. Interferon induction and/or production and its suppression by influenza A viruses. J Virol 2005, 79(March (5)):2880-2890.
39. Ngunjiri J.M., Sekellick M.J., Marcus P.I. Clonogenic assay of type A influenza viruses reveals noninfectious cell-killing (apoptosis-inducing) particles. J Virol 2008, 82(6):2673-2680.
40. Marcus P.I., Ngunjiri J.M., Sekellick M.J. Dynamics of biologically active subpopulations of influenza virus: plaque-forming, noninfectious cell-killing, and defective interfering particles. J Virol 2009, 83(16):8122-8130.
41. Kurokawa M., Koyama A.H., Yasuoka S., Adachi A. Influenza virus overcomes apoptosis by rapid multiplication. Int J Mol Med 1999, 3(May (5)):527-530.
42. Wurzer W.J., Planz O., Ehrhardt C., Giner M., Silberzahn T., Pleschka S., et al. Caspase 3 activation is essential for efficient influenza virus propagation. EMBO J 2003, 22(June (11)):2717-2728.
43. Heynisch B., Frensing T., Heinze K., Seitz C., Genzel Y., Reichl U. Differential activation of host cell signalling pathways through infection with two variants of influenza A/Puerto Rico/8/34 (H1N1) in MDCK cells. Vaccine 2010, 28(November (51)):8210-8218.
44. Seitz C., Frensing T., Höper D., Kochs G., Reichl U. High yields of influenza A virus in Madin-Darby canine kidney cells are promoted by an insufficient interferon-induced antiviral state. J Gen Virol 2010, 91(July (Pt 7)):1754-1763.
45. Marcus P.I., Ngunjiri J.M., Sekellick M.J., Wang L., Lee C.W. In vitro analysis of virus particle subpopulations in candidate live-attenuated influenza vaccines distinguishes effective from ineffective vaccines. J Virol 2010, 84(November (21)):10974-10981.