A single dose of an avian H3N8 influenza virus vaccine is highly immunogenic and efficacious against a recently emerged seal influenza virus in mice and ferrets

Journal of Virology

Volumn 89, Issue 13, 2015, Pages 6907-6917

  Baz, Mariana ^a   Paskel, Myeisha ^a   Matsuoka, Yumiko ^a   Zengel, James R ^b   Cheng, Xing ^b   Treanor, John J ^c   Jin, Hong ^b   Subbarao, Kanta ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b MEDIMMUNE   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; CROSS REACTION; DRUG EFFICACY; DRUG SAFETY; FEMALE; FERRET; HEMAGGLUTININ GENE; HUMAN; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N8; MALE; MOUSE; NEURAMINIDASE GENE; NONHUMAN; PINNIPEDIA; PRIORITY JOURNAL; SEROLOGY; SINGLE DRUG DOSE; VACCINE PRODUCTION; VIRUS GENE; VIRUS STRAIN; VIRUS TRANSMISSION; ADOLESCENT; ANIMAL; BAGG ALBINO MOUSE; BLOOD; DOG; GENETIC RECOMBINATION; GENETICS; IMMUNOLOGY; INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H3N8); ISOLATION AND PURIFICATION; MIDDLE AGED; ORTHOMYXOVIRIDAE INFECTIONS; PROCEDURES; REVERSE GENETICS; VACCINATION; VERY ELDERLY; YOUNG ADULT;

AVES; AVIAN INFLUENZA VIRUS; CANIS FAMILIARIS; INFLUENZA A VIRUS; MAMMALIA; MUS; MUSTELA; ORTHOMYXOVIRIDAE; SUIDAE;

ADOLESCENT; AGED; AGED, 80 AND OVER; ANIMALS; ANTIBODIES, VIRAL; DOGS; FEMALE; FERRETS; HUMANS; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA A VIRUS, H3N8 SUBTYPE; INFLUENZA VACCINES; MALE; MICE, INBRED BALB C; MIDDLE AGED; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINATION, GENETIC; REVERSE GENETICS; VACCINATION; YOUNG ADULT;

EID: 84930885285     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00280-15     Document Type: Article

References (44)

1. Palese P. 2004. Influenza: old and new threats. Nat Med 10:S82-S87. http://dx.doi.org/10.1038/nm1141.
2. CDC. 2009. Update: novel influenza A (H1N1) virus infections-worldwide. MMWR 58(17):453-458.
3. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD. 2005. Characterization of a novel influenzaAvirus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814-2822. http://dx.doi.org/10.1128/JVI.79.5.2814-2822.2005.
4. Yoon SW, Webby RJ, Webster RG. 2014. Evolution and ecology of influenzaAviruses. Curr Top Microbiol Immunol 385:359-375. http://dx .doi.org/10.1007/82_2014_396.
5. Wu Y, Wu Y, Tefsen B, Shi Y, Gao GF. 2014. Bat-derived influenza-like viruses H17N10 and H18N11. Trends Microbiol 22:183-191. http://dx .doi.org/10.1016/j.tim.2014.01.010.
6. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, Smith C, Hill RC, Ferro P, Pompey J, Bright RA, Medina MJ, Johnson CM, Olsen CW, Cox NJ, Klimov AI, Katz JM, Donis RO. 2005. Transmission of equine influenza virus to dogs. Science 310:482-485. http://dx.doi.org/10.1126/science.1117950.
7. Waddell GH, Teigland MB, Sigel MM. 1963. A new influenza virus associated with equine respiratory disease. J Am Vet Med Assoc 143:587-590.
8. Tu J, Zhou H, Jiang T, Li C, Zhang A, Guo X, Zou W, Chen H, Jin M. 2009. Isolation and molecular characterization of equine H3N8 influenza viruses from pigs in China. Arch Virol 154:887-890. http://dx.doi.org/10.1007/s00705-009-0381-1.
9. Qi T, Guo W, Huang W, Dai L, Zhao L, Li H, Li X, Zhang X, Wang Y, Yan Y, He N, Xiang W. 2010. Isolation and genetic characterization of H3N8 equine influenza virus from donkeys in China. Vet Microbiol 144:455-460. http://dx.doi.org/10.1016/j.vetmic.2010.01.006.
10. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, Navarrete-Macias I, Sanchez-Leon M, Saliki JT, Pedersen J, Karesh W, Daszak P, Rabadan R, Rowles T, Lipkin WI. 2012. Emergence of fatal avian influenza in New England harbor seals. mBio 3(4):e00166-12. http://dx.doi.org/10.1128/mBio.00166-12.
11. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, Sorrell EM, Bestebroer TM, Burke DF, Smith DJ, Rimmelzwaan GF, Osterhaus AD, Fouchier RA. 2012. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534-1541. http://dx.doi.org/10.1126/science.1213362.
12. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, Zhong G, Hanson A, Katsura H, Watanabe S, Li C, Kawakami E, Yamada S, Kiso M, Suzuki Y, Maher EA, Neumann G, Kawaoka Y. 2012. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420-428. http://dx.doi.org/10.1038/nature10831.
13. Karlsson EA, Ip HS, Hall JS, Yoon SW, Johnson J, Beck MA, Webby RJ, Schultz-Cherry S. 2014. Respiratory transmission of an avian H3N8 influenza virus isolated from a harbour seal. Nat Commun 5:4791. http://dx .doi.org/10.1038/ncomms5791.
14. Baz M, Paskel M, Matsuoka Y, Zengel J, Cheng X, Jin H, Subbarao K. 2013. Replication and immunogenicity of swine, equine, and avian H3 subtype influenza viruses in mice and ferrets. J Virol 87:6901-6910. http://dx.doi.org/10.1128/JVI.03520-12.
15. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am J Hyg (Lond) 27:493-497.
16. Hoffmann E, Neumann G, Kawaoka Y, Hobom G, Webster RG. 2000. A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97:6108-6113. http://dx.doi.org/10.1073/pnas.100133697.
17. Chen GL, Lamirande EW, Yang CF, Jin H, Kemble G, Subbarao K. 2010. Evaluation of replication and cross-reactive antibody responses of H2 subtype influenza viruses in mice and ferrets. J Virol 84:7695-7702. http://dx.doi.org/10.1128/JVI.00511-10.
18. Joseph T, McAuliffe J, Lu B, Jin H, Kemble G, Subbarao K. 2007. Evaluation of replication and pathogenicity of avian influenza a H7 subtype viruses in a mouse model. J Virol 81:10558-10566. http://dx.doi.org/10.1128/JVI.00970-07.
19. WHO. 2002. WHO manual on animal influenza diagnosis and surveillance. WHO, Geneva, Switzerland. http://www.who.int/vaccine_research/diseases/influenza/WHO_manual_on_animal-diagnosis_and_surveillance:2002_5.pdf.
20. Sangster MY, Baer J, Santiago FW, Fitzgerald T, Ilyushina NA, Sundararajan A, Henn AD, Krammer F, Yang H, Luke CJ, Zand MS, Wright PF, Treanor JJ, Topham DJ, Subbarao K. 2013. B cell response and hemagglutinin stalk-reactive antibody production in different age cohorts following 2009 H1N1 influenza virus vaccination. Clin Vaccine Immunol 20:867-876. http://dx.doi.org/10.1128/CVI.00735-12.
21. Gallagher M, Bucher DJ, Dourmashkin R, Davis JF, Rosenn G, Kilbourne ED. 1984. Isolation of immunogenic neuraminidases of human influenza viruses by a combination of genetic and biochemical procedures. J Clin Microbiol 20:89-93.
22. O'Donnell CD, Wright A, Vogel LN, Wei CJ, Nabel GJ, Subbarao K. 2012. Effect of priming with H1N1 influenza viruses of variable antigenic distances on challenge with 2009 pandemic H1N1 virus. J Virol 86:8625-8633. http://dx.doi.org/10.1128/JVI.00147-12.
23. Baz M, Paskel M, Matsuoka Y, Zengel J, Cheng X, Treanor JJ, Jin H, Subbarao K. 2014. A live attenuated equine H3N8 influenza vaccine is highly immunogenic and efficacious in mice and ferrets. J Virol 89:1652-1659. http://dx.doi.org/10.1128/JVI.02449-14.
24. Richard M, de Graaf M, Herfst S. 2014. Avian influenza A viruses: from zoonosis to pandemic. Future Virol 9:513-524. http://dx.doi.org/10.2217/fvl.14.30.
25. Clements ML, Murphy BR. 1986. Development and persistence of local and systemic antibody responses in adults given live attenuated or inactivated influenza A virus vaccine. J Clin Microbiol 23:66-72.
26. Gorse GJ, Campbell MJ, Otto EE, Powers DC, Chambers GW, Newman FK. 1995. Increased anti-influenza A virus cytotoxic T cell activity following vaccination of the chronically ill elderly with live attenuated or inactivated influenza virus vaccine. J Infect Dis 172:1-10. http://dx.doi.org/10.1093/infdis/172.1.1.
27. Chen GL, Lamirande EW, Cheng X, Torres-Velez F, Orandle M, Jin H, Kemble G, Subbarao K. 2014. Evaluation of three live attenuated H2 pandemic influenza vaccine candidates in mice and ferrets. J Virol 88:2867-2876. http://dx.doi.org/10.1128/JVI.01829-13.
28. Chen Z, Santos C, Aspelund A, Gillim-Ross L, Jin H, Kemble G, Subbarao K. 2009. Evaluation of live attenuated influenza a virus H6 vaccines in mice and ferrets. J Virol 83:65-72. http://dx.doi.org/10.1128/JVI.01775-08.
29. Min JY, Vogel L, Matsuoka Y, Lu B, Swayne D, Jin H, Kemble G, Subbarao K. 2010. A live attenuated H7N7 candidate vaccine virus induces neutralizing antibody that confers protection from challenge in mice, ferrets, and monkeys. J Virol 84:11950-11960. http://dx.doi.org/10.1128/JVI.01305-10.
30. Suguitan AL, Jr, McAuliffe J, Mills KL, Jin H, Duke G, Lu B, Luke CJ, Murphy B, Swayne DE, Kemble G, Subbarao K. 2006. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 3:e360. http://dx.doi.org/10.1371/journal .pmed.0030360.
31. Chen H, Subbarao K, Swayne D, Chen Q, Lu X, Katz J, Cox N, Matsuoka Y. 2003. Generation and evaluation of a high-growth reassortant H9N2 influenza A virus as a pandemic vaccine candidate. Vaccine 21:1974-1979. http://dx.doi.org/10.1016/S0264-410X(02)00809-5.
32. Karron RA, Callahan K, Luke C, Thumar B, McAuliffe J, Schappell E, Joseph T, Coelingh K, Jin H, Kemble G, Murphy BR, Subbarao K. 2009. A live attenuated H9N2 influenza vaccine is well tolerated and immunogenic in healthy adults. J Infect Dis 199:711-716. http://dx.doi.org/10.1086/596558.
33. Karron RA, Talaat K, Luke C, Callahan K, Thumar B, Dilorenzo S, McAuliffe J, Schappell E, Suguitan A, Mills K, Chen G, Lamirande E, Coelingh K, Jin H, Murphy BR, Kemble G, Subbarao K. 2009. Evaluation of two live attenuated cold-adapted H5N1 influenza virus vaccines in healthy adults. Vaccine 27:4953-4960. http://dx.doi.org/10.1016/j.vaccine.2009.05.099.
34. Talaat KR, Karron RA, Callahan KA, Luke CJ, DiLorenzo SC, Chen GL, Lamirande EW, Jin H, Coelingh KL, Murphy BR, Kemble G, Subbarao K. 2009. A live attenuated H7N3 influenza virus vaccine is well tolerated and immunogenic in a phase I trial in healthy adults. Vaccine 27:3744-3753. http://dx.doi.org/10.1016/j.vaccine.2009.03.082.
35. Talaat KR, Karron RA, Liang PH, McMahon BA, Luke CJ, Thumar B, Chen GL, Min JY, Lamirande EW, Jin H, Coelingh KL, Kemble GW, Subbarao K. 2013. An open-label phase I trial of a live attenuated H2N2 influenza virus vaccine in healthy adults. Influenza Other Respir Viruses 7:66-73. http://dx.doi.org/10.1111/j.1750-2659.2012.00350.x.
36. Talaat KR, Karron RA, Luke CJ, Thumar B, McMahon BA, Chen GL, Lamirande EW, Jin H, Coelingh KL, Kemble G, Subbarao K. 2011. An open label phase I trial of a live attenuated H6N1 influenza virus vaccine in healthy adults. Vaccine 29:3144-3148. http://dx.doi.org/10.1016/j.vaccine.2011.02.043.
37. Babu TM, Levine M, Fitzgerald T, Luke C, Sangster MY, Jin H, Topham D, Katz J, Treanor J, Subbarao K. 2014. Live attenuated H7N7 influenza vaccine primes for a vigorous antibody response to inactivated H7N7 influenza vaccine. Vaccine 32:6798-6804. http://dx.doi.org/10.1016/j .vaccine.2014.09.070.
38. Talaat KR, Luke CJ, Khurana S, Manischewitz J, King LR, McMahon BA, Karron RA, Lewis KD, Qin J, Follmann DA, Golding H, Neuzil KM, Subbarao K. 2014. A live attenuated influenza A(H5N1) vaccine induces long-term immunity in the absence of a primary antibody response. J Infect Dis 209:1860-1869. http://dx.doi.org/10.1093/infdis/jiu123.
39. Yewdell JW, Bennink JR, Smith GL, Moss B. 1985. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 82:1785-1789. http://dx.doi.org/10.1073/pnas.82.6.1785.
40. Doherty PC, Kelso A. 2008. Toward a broadly protective influenza vaccine. J Clin Invest 118:3273-3275. http://dx.doi.org/10.1172/JCI37232.
41. Kreijtz JH, Bodewes R, van Amerongen G, Kuiken T, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. 2007. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25:612-620. http://dx.doi.org/10.1016/j.vaccine.2006.08.036.
42. Epstein SL, Lo CY, Misplon JA, Bennink JR. 1998. Mechanism of protective immunity against influenza virus infection in mice without antibodies. J Immunol 160:322-327.
43. Cheng X, Zengel JR, Suguitan AL, Jr, Xu Q, Wang W, Lin J, Jin H. 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. http://dx.doi.org/10.1093/infdis/jit207.
44. Plennevaux E, Sheldon E, Blatter M, Reeves-Hoche MK, Denis M. 2010. Immuneresponse after a single vaccination against 2009 influenzaAH1N1in USA: a preliminary report of two randomised controlled phase 2 trials. Lancet 375:41-48. http://dx.doi.org/10.1016/S0140-6736(09)62026-2.