Hemagglutinin stalk immunity reduces influenza virus replication and transmission in ferrets

Journal of Virology

Volumn 90, Issue 6, 2016, Pages 3268-3273

  Nachbagauer, Raffael ^a,b   Miller, Matthew S ^c   Hai, Rong ^a,e   Ryder, Alex B ^d   Rose, John K ^d   Palese, Peter ^a   García Sastre, Adolfo ^a   Krammer, Florian ^a   Albrecht, Randy A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

^c MCMASTER UNIVERSITY   (Canada)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; H1N1 VIRUS HEMAGGLUTININ; INFLUENZA VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; FERRET; INFLUENZA A (H1N1); INFLUENZA A VIRUS (H1N1); MALE; NONHUMAN; PRIORITY JOURNAL; VIRUS CARRIER; VIRUS NEUTRALIZATION; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS TITRATION; VIRUS TRANSMISSION; ANIMAL; DISEASE MODEL; DISEASE TRANSMISSION; IMMUNOLOGY; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRIDAE INFECTIONS; PHYSIOLOGY; PREVENTION AND CONTROL; TRANSMISSION; VIROLOGY; VIRUS LOAD;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, INFECTIOUS; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; MALE; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL LOAD; VIRUS REPLICATION;

EID: 84961114525     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02481-15     Document Type: Article

References (24)

1. Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086-5096. http://dx.doi.org/10.1016/j.vaccine.2007.03.046.
2. Centers for Disease Control and Prevention (CDC). 2010. Estimates of deaths associated with seasonal influenza-United States, 1976-2007. MMWR Morb Mortal Wkly Rep 59:1057-1062. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5933a1.htm.
3. Wang TT, Palese P. 2011. Biochemistry. Catching a moving target. Science 333:834-835. http://dx.doi.org/10.1126/science.1210724.
4. Centers for Disease Control and Prevention (CDC). 2009. Update on influenza A (H1N1) 2009 monovalent vaccines.MMWRMorb Mortal Wkly Rep 58:1100-1101. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm58 39a3.htm.
5. Centers for Disease Control and Prevention (CDC). 2009. Swine influenza A (H1N1) infection in two children-southern California, March-April 2009.MMWRMorb Mortal Wkly Rep 58:400-402. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5815a5.htm.
6. Yewdell JW. 2013. To dream the impossible dream: universal influenza vaccination. Curr Opin Virol 3:316-321. http://dx.doi.org/10.1016/j.coviro.2013.05.008.
7. Subbarao K, Matsuoka Y. 2013. The prospects and challenges of universal vaccines for influenza. Trends Microbiol 21:350-358. http://dx.doi.org/10.1016/j.tim.2013.04.003.
8. Krammer F, Palese P. 2013. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr Opin Virol 3:521-530. http://dx.doi.org/10.1016/j.coviro.2013.07.007.
9. Krammer F, Hai R, Yondola M, Tan GS, Leyva-Grado VH, Ryder AB, Miller MS, Rose JK, Palese P, Garcia-Sastre A, Albrecht RA. 2014. Assessment of influenza virus hemagglutinin stalk-based immunity in ferrets. J Virol 88:3432-3442. http://dx.doi.org/10.1128/JVI.03004-13.
10. Baker SF, Guo H, Albrecht RA, Garcia-Sastre A, Topham DJ, Martínez-Sobrido L. 2013. Protection against lethal influenza with a viral mimic. J Virol 87:8591-8605. http://dx.doi.org/10.1128/JVI.01081-13.
11. Seibert CW, Rahmat S, Krause JC, Eggink D, Albrecht RA, Goff PH, Krammer F, Duty JA, Bouvier NM, Garcia-Sastre A, Palese P. 2013. Recombinant IgA is sufficient to prevent influenza virus transmission in guinea pigs. J Virol 87:7793-7804. http://dx.doi.org/10.1128/JVI.00979-13.
12. Impagliazzo A, Milder F, Kuipers H, Wagner MV, Zhu X, Hoffman RM, van Meersbergen R, Huizingh J, Wanningen P, Verspuij J, de Man M, Ding Z, Apetri A, Kükrer B, Sneekes-Vriese E, Tomkiewicz D, Laursen NS, Lee PS, Zakrzewska A, Dekking L, Tolboom J, Tettero L, van Meerten S, Yu W, Koudstaal W, Goudsmit J, Ward AB, Meijberg W, Wilson IA, Radošević K. 2015. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science 349:1301-1306. http://dx.doi.org/10.1126/science.aac7263.
13. Yassine HM, Boyington JC, McTamney PM, Wei CJ, Kanekiyo M, Kong WP, Gallagher JR, Wang L, Zhang Y, Joyce MG, Lingwood D, Moin SM, Andersen H, Okuno Y, Rao SS, Harris AK, Kwong PD, Mascola JR, Nabel GJ, Graham BS. 2015. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med 21:1065-1070. http://dx.doi.org/10.1038/nm.3927.
14. DiLillo DJ, Tan GS, Palese P, Ravetch JV. 2014. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat Med 20:143-151. http://dx.doi.org/10.1038/nm.3443.
15. Jegaskanda S, Weinfurter JT, Friedrich TC, Kent SJ. 2013. Antibodydependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques. J Virol 87:5512-5522. http://dx.doi.org/10.1128/JVI.03030-12.
16. Jegaskanda S, Job ER, Kramski M, Laurie K, Isitman G, de Rose R, Winnall WR, Stratov I, Brooks AG, Reading PC, Kent SJ. 2013. Crossreactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J Immunol 190:1837-1848. http://dx.doi.org/10.4049/jimmunol.1201574.
17. Khurana S, Loving CL, Manischewitz J, King LR, Gauger PC, Henningson J, Vincent AL, Golding H. 2013. Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease. Sci Transl Med 5:200ra114. http://dx.doi.org/10.1126/scitranslmed.3006366.
18. Krammer F, Pica N, Hai R, Margine I, Palese P. 2013. Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies. J Virol 87:6542-6550. http://dx.doi.org/10.1128/JVI.00641-13.
19. Krammer F, Pica N, Hai R, Tan GS, Palese P. 2012. Hemagglutinin stalk-reactive antibodies are boosted following sequential infection with seasonal and pandemic H1N1 influenza virus in mice. J Virol 86:10302-10307. http://dx.doi.org/10.1128/JVI.01336-12.
20. Mallajosyula VV, Citron M, Ferrara F, Lu X, Callahan C, Heidecker GJ, Sarma SP, Flynn JA, Temperton NJ, Liang X, Varadarajan R. 2014. Influenza hemagglutinin stem-fragment immunogen elicits broadly neutralizing antibodies and confers heterologous protection. Proc Natl Acad Sci U S A 111:E2514-E2523. http://dx.doi.org/10.1073/pnas.1402766111.
21. Oxford JS. 2013. Towards a universal influenza vaccine: volunteer virus challenge studies in quarantine to speed the development and subsequent licensing. Br J Clin Pharmacol 76:210-216. http://dx.doi.org/10.1111/bcp.12146.
22. Martínez-Romero C, de Vries E, Belicha-Villanueva A, Mena I, Tscherne DM, Gillespie VL, Albrecht RA, de Haan CA, Garcia-Sastre A. 2013. Substitutions T200A and E227A in the hemagglutinin of pandemic 2009 influenza A virus increase lethality but decrease transmission. J Virol 87:6507-6511. http://dx.doi.org/10.1128/JVI.00262-13.
23. Seibert CW, Kaminski M, Philipp J, Rubbenstroth D, Albrecht RA, Schwalm F, Stertz S, Medina RA, Kochs G, Garcia-Sastre A, Staeheli P, Palese P. 2010. Oseltamivir-resistant variants of the 2009 pandemic H1N1 influenza A virus are not attenuated in the guinea pig and ferret transmission models. J Virol 84:11219-11226. http://dx.doi.org/10.1128/JVI.01424-10.
24. Krammer F, Margine I, Tan GS, Pica N, Krause JC, Palese P. 2012. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7:e43603. http://dx.doi.org/10.1371/journal.po ne.0043603.