Development and pre-clinical evaluation of two LAIV strains against potentially pandemic H2N2 influenza virus

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Isakova Sivak, Irina ^a   De Jonge, Jørgen ^b   Smolonogina, Tatiana ^a   Rekstin, Andrey ^a   Van Amerongen, Geert ^c   Van Dijken, Harry ^b   Mouthaan, Justin ^b   Roholl, Paul ^d   Kuznetsova, Victoria ^a   Doroshenko, Elena ^a   Tsvetnitsky, Vadim ^e   Rudenko, Larisa ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Russian Federation)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c Animal Research Center InTraVacc   (Netherlands)

^d Microscope Consultancy   (Netherlands)

^e PATH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; SIALIDASE; LIVE VACCINE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY; VIRUS HEMAGGLUTININ;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; CROSS REACTION; DOMESTIC FERRET; DRUG EFFECT; ENZYME INHIBITION; FEMALE; GENETIC REASSORTMENT; HEMAGGLUTINATION; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA A (H2N2); INFLUENZA VACCINATION; INFLUENZA VIRUS A H2N2; MOUSE; NONHUMAN; PHENOTYPE; TEMPERATURE SENSITIVITY; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS STRAIN; WEIGHT REDUCTION; WILD TYPE; ANIMAL; BLOOD; CBA MOUSE; DRUG EFFECTS; DRUG SCREENING; FERRET; GENE EXPRESSION; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; LUNG; NOSE; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS; VIROLOGY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DRUG EVALUATION, PRECLINICAL; FEMALE; FERRETS; GENE EXPRESSION; HEMAGGLUTININS, VIRAL; HUMANS; IMMUNIZATION; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA VACCINES; LUNG; MICE; MICE, INBRED CBA; NEURAMINIDASE; NOSE; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS; REASSORTANT VIRUSES; VACCINES, ATTENUATED; VIRUS REPLICATION;

EID: 84904802066     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102339     Document Type: Article

References (53)

1. WHO (2009) Influenza (Seasonal). Fact sheet No211, April 2009. http://www.who.int/mediacentre/factsheets/fs211/en/index.html.
2. Anonymous (2003) Development of a Clinical Trial Plan for Pandemic Influenza Vaccines. Department of Health and Human Services. National Institute of Allergy and Infection Diseases. September 22-23, 2003, Bethesda, Maryland. Meeting Summary. http://www.niaid.nih.gov/about/organization/dmid/Documents/ pansummary.pdf.
3. Nabel GJ, Wei CJ, Ledgerwood JE (2011) Vaccinate for the next H2N2 pandemic now. Nature 471: 157-158.
4. Pyhala R (1985) Antibody status to influenza A/Singapore/1/57(H2N2) in Finland during a period of outbreaks caused by H3N2 and H1N1 subtype viruses. J Hyg (Lond) 95: 437-445.
5. Mulder J, Masurel N (1958) Pre-epidemic antibody against 1957 strain of Asiatic influenza in serum of older people living in the Netherlands. Lancet 1: 810-814.
6. Simonsen L, Clarke MJ, Schonberger LB, Arden NH, Cox NJ, et al. (1998) Pandemic versus epidemic influenza mortality: a pattern of changing age distribution. J Infect Dis 178: 53-60. (Pubitemid 28328076)
7. Glaser L, Zamarin D, Acland HM, Spackman E, Palese P, et al. (2006) Sequence analysis and receptor specificity of the hemagglutinin of a recent influenza H2N2 virus isolated from chicken in North America. Glycoconj J 23:93-99.
8. Makarova NV, Kaverin NV, Krauss S, Senne D, Webster RG (1999) Transmission of Eurasian avian H2 influenza virus to shorebirds in North America. J Gen Virol 80 (Pt 12): 3167-3171.
9. Schafer JR, Kawaoka Y, Bean WJ, Suss J, Senne D, et al. (1993) Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 194: 781-788.
10. Stohr K (2010) Vaccinate before the next pandemic? Nature 465: 161.
11. Ma W, Vincent AL, Gramer MR, Brockwell CB, Lager KM, et al. (2007) Identification of H2N3 influenza A viruses from swine in the United States. Proc Natl Acad Sci U S A 104: 20949-20954.
12. Aleksandrova GI, Mikutskaia BA, Pleshanova RA, Panova NG, Smorodintsev AA (1965) [The reactive and immunogenic properties and epidemiological effectiveness of further attenuated influenza virus vaccinal strains (observed in preschool children)]. Vopr Virusol 10: 67-73.
13. Lindstrom SE, Cox NJ, Klimov A (2004) Genetic analysis of human H2N2 and early H3N2 influenza viruses, 1957-1972: evidence for genetic divergence and multiple reassortment events. Virology 328: 101-119. (Pubitemid 39221916)
14. Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. The American Journal of Hygiene 27: 493-497.
15. Aleksandrova GI (1977) [Use of the genetic recombination method for obtaining vaccinal strains of the influenza virus]. Vopr Virusol: 387-395.
16. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Archives of Virology 146: 2275-2289. (Pubitemid 34682391)
17. WHO (2002) WHO Manual on Animal Influenza Diagnosis and Surveillance; WHO/CDS/CSR/NCS/2002.5 Rev. 1.
18. Lambre CR, Terzidis H, Greffard A, Webster RG (1990) Measurement of anti-influenza neuraminidase antibody using a peroxidase-linked lectin and microtitre plates coated with natural substrates. J Immunol Methods 135: 49-57.
19. Connor RJ, Kawaoka Y, Webster RG, Paulson JC (1994) Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205: 17-23. (Pubitemid 24360586)
20. Wareing MD, Watson JM, Brooks MJ, Tannock GA (2001) Immunogenic and isotype-specific responses to Russian and US cold-adapted influenza a vaccine donor strains A/Leningrad/134/17/57, A/Leningrad/134/47/57, and A/Ann Arbor/6/60 (H2N2) in mice. J Med Virol 65: 171-177.
21. Desheva JA, Lu XH, Rekstin AR, Rudenko LG, Swayne DE, et al. (2006) Characterization of an influenza A H5N2 reassortant as a candidate for liveattenuated and inactivated vaccines against highly pathogenic H5N1 viruses with pandemic potential. Vaccine 24: 6859-6866. (Pubitemid 46107188)
22. Jonassen CM, Handeland K (2007) Avian influenza virus screening in wild waterfowl in Norway, 2005. Avian Dis 51: 425-428. (Pubitemid 46671324)
23. Kishida N, Sakoda Y, Shiromoto M, Bai GR, Isoda N, et al. (2008) H2N5 influenza virus isolates from terns in Australia: genetic reassortants between those of the Eurasian and American lineages. Virus Genes 37: 16-21.
24. Krauss S, Obert CA, Franks J, Walker D, Jones K, et al. (2007) Influenza in migratory birds and evidence of limited intercontinental virus exchange. PLoS Pathog 3: e167.
25. Suss J, Schafer J, Sinnecker H, Webster RG (1994) Influenza virus subtypes in aquatic birds of eastern Germany. Arch Virol 135: 101-114. (Pubitemid 2059506)
26. Tumova B, Eisengarten HJ, Siebelist-Konstantinow I, Stumpa A, Webster RG (1975) A duck influenza virus with haemagglutinin related to that of A/ Singapore/57 (H2N2) virus. Acta Virol 19: 261.
27. Shortridge KF (1979) H2N2 influenza viruses in domestic ducks. Lancet 1: 439.
28. Kawaoka Y, Krauss S, Webster RG (1989) Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 63: 4603-4608. (Pubitemid 19257834)
29. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56: 152-179.
30. Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, et al. (2000) Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74: 8502-8512. (Pubitemid 30666701)
31. Xu R, McBride R, Paulson JC, Basler CF, Wilson IA (2010) Structure, receptor binding, and antigenicity of influenza virus hemagglutinins from the 1957 H2N2 pandemic. J Virol 84: 1715-1721.
32. WHO (2005) WHO global influenza preparedness plan. WHO/CDS/CSR/GIP/2005.5 http://www.who.int/csr/resources/publications/influenza/en/WHO-CDS-CSR-GIP- 2005-5.pdf.
33. Rudenko LG, Slepushkin AN, Monto AS, Kendal AP, Grigorieva EP, et al. (1993) Efficacy of live attenuated and inactivated influenza vaccines in schoolchildren and their unvaccinated contacts in Novgorod, Russia. J Infect Dis 168: 881-887. (Pubitemid 23282559)
34. Rudenko LG, Lonskaya NI, Klimov AI, Vasilieva RI, Ramirez A (1996) Clinical and epidemiological evaluation of a live, cold-adapted influenza vaccine for 3-14-year-olds. Bull World Health Organ 74: 77-84.
35. Slepushkin AN, Obrosova-Serova NP, Burtseva EI, Rudenko LG, Govorkova EA, et al. (1993) Comparison of live attenuated and inactivated influenza vaccines in schoolchildren in Russia: I. Safety and efficacy in two Moscow schools, 1987/88. Vaccine 11: 323-328. (Pubitemid 23061175)
36. Rudenko LG, Arden NH, Grigorieva E, Naychin A, Rekstin A, et al. (2000) Immunogenicity and efficacy of Russian live attenuated and US inactivated influenza vaccines used alone and in combination in nursing home residents. Vaccine 19: 308-318. (Pubitemid 30621525)
37. Lu X, Edwards LE, Desheva JA, Nguyen DC, Rekstin A, et al. (2006) Cross-protective immunity in mice induced by live-attenuated or inactivated vaccines against highly pathogenic influenza A (H5N1) viruses. Vaccine 24: 6588-6593. (Pubitemid 46107146)
38. Gustin KM, Maines TR, Belser JA, van Hoeven N, Lu X, et al. (2011) Comparative immunogenicity and cross-clade protective efficacy of mammalian cell-grown inactivated and live attenuated H5N1 reassortant vaccines in ferrets. J Infect Dis 204: 1491-1499.
39. Jang YH, Byun YH, Lee YJ, Lee YH, Lee KH, et al. (2012) Cold-adapted pandemic 2009 H1N1 influenza virus live vaccine elicits cross-reactive immune responses against seasonal and H5 influenza A viruses. J Virol 86: 5953-5958.
40. Tamura S, Tanimoto T, Kurata T (2005) Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis 58: 195-207. (Pubitemid 41460922)
41. Jang YH, Seong BL (2013) Cross-protective immune responses elicited by live attenuated influenza vaccines. Yonsei Med J 54: 271-282.
42. Petukhova G, Korenkov D, Chirkova T, Donina S, Rudenko L, et al. (2012) B- and T-cell memory elicited by a seasonal live attenuated reassortant influenza vaccine: assessment of local antibody avidity and virus-specific memory T-cells using trogocytosis-based method. Influenza Other Respi Viruses 6: 119-126.
43. Petukhova G, Naikhin A, Chirkova T, Donina S, Korenkov D, et al. (2009) Comparative studies of local antibody and cellular immune responses to influenza infection and vaccination with live attenuated reassortant influenza vaccine (LAIV) utilizing a mouse nasal-associated lymphoid tissue (NALT) separation method. Vaccine 27: 2580-2587.
44. Naykhin A, Petukhova G, Chirkova T, Korenkov D, Donina S, et al. (2011) Virus-specific CD4+ and CD8+ memory T-cells in young volunteers after immunization with pandemic live attenuated reassortant influenza vaccines A(H5N2) and A(H1N1). Influenza and other respiratory viruses 5 (Suppl. 1): 195-201.
45. Cheng X, Zengel JR, Suguitan AL Jr, Xu Q, Wang W, et al. (2013) Evaluation of the humoral and cellular immune responses elicited by the live attenuated and inactivated influenza vaccines and their roles in heterologous protection in ferrets. J Infect Dis 208: 594-602.
46. Alexandrova GI, Smorodintsev AA (1965) Obtaining of an additionally attenuated vaccinating cryophilic influenza strain. Rev Roum Inframicrobiol 2: 179-189.
47. Chen GL, Lamirande EW, Yang CF, Jin H, Kemble G, et al. (2010) Evaluation of replication and cross-reactive antibody responses of H2 subtype influenza viruses in mice and ferrets. J Virol 84: 7695-7702.
48. Chen GL, Lamirande EW, Jin H, Kemble G, Subbarao K (2010) Safety, immunogencity, and efficacy of a cold-adapted A/Ann Arbor/6/60 (H2N2) vaccine in mice and ferrets. Virology 398: 109-114.
49. Talaat KR, Karron RA, Liang PH, McMahon BA, Luke CJ, et al. (2013) An open-label phase I trial of a live attenuated H2N2 influenza virus vaccine in healthy adults. Influenza Other Respi Viruses 7: 66-73.
50. Baz M, Luke CJ, Cheng X, Jin H, Subbarao K (2013) H5N1 vaccines in humans. Virus Res 178: 78-98.
51. Rockman S, Brown LE, Barr IG, Gilbertson B, Lowther S, et al. (2013) Neuraminidase-inhibiting antibody is a correlate of cross-protection against lethal H5N1 influenza virus in ferrets immunized with seasonal influenza vaccine. J Virol 87: 3053-3061.
52. Belser JA, Katz JM, Tumpey TM (2011) The ferret as a model organism to study influenza A virus infection. Dis Model Mech 4: 575-579.
53. Bodewes R, Rimmelzwaan GF, Osterhaus AD (2010) Animal models for the preclinical evaluation of candidate influenza vaccines. Expert Rev Vaccines 9: 59-72.