Sequential infection in ferrets with antigenically distinct seasonal H1N1 influenza viruses boosts hemagglutinin stalk-specific antibodies

Journal of Virology

Volumn 90, Issue 2, 2016, Pages 1116-1128

  Kirchenbaum, Greg A ^a,b   Carter, Donald M ^a,b   Ross, Ted M ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b Vaccine and Gene Therapy Institute of Florida   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC ANTIBODY; HEMAGGLUTININ; H1N1 VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY COMBINING SITE; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGENICITY; ARTICLE; COMPETITIVE BINDING ASSAY; CROSS REACTION; FERRET; IMMUNOMODULATION; INFLUENZA A (H1N1); NONHUMAN; PRIORITY JOURNAL; REINFECTION; SEASONAL INFLUENZA; SEQUENTIAL INFECTION; VIRUS IMMUNITY; VIRUS ISOLATION; VIRUS STRAIN; ANIMAL; BLOOD; BODY WEIGHT; CROSS PROTECTION; DISEASE MODEL; FEMALE; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); NOSE CAVITY; ORTHOMYXOVIRIDAE INFECTIONS; VIROLOGY; VIRUS LOAD;

ANIMALS; ANTIBODIES, VIRAL; BODY WEIGHT; CROSS PROTECTION; DISEASE MODELS, ANIMAL; FEMALE; FERRETS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; NASAL CAVITY; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL LOAD;

EID: 84954130115     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02372-15     Document Type: Article

References (62)

1. Houser K, Subbarao K. 2015. Influenza vaccines: challenges and solutions. Cell Host Microbe 17:295-300. http://dx.doi.org/10.1016/j.chom.2015.02.012.
2. Bouvier NM, Palese P. 2008. The biology of influenza viruses. Vaccine 26(Suppl 4):D49-D53. http://dx.doi.org/10.1016/j.vaccine.2008.07.039.
3. Skehel JJ, Wiley DC. 2000. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531-569. http://dx.doi.org/10.1146/annurev.biochem.69.1.531.
4. Gerhard W. 2001. The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 260:171-190.
5. Ohmit SE, Petrie JG, Cross RT, Johnson E, Monto AS. 2011. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccineinduced protection. J Infect Dis 204:1879-1885. http://dx.doi.org/10.1093/infdis/jir661.
6. Knossow M, Skehel JJ. 2006. Variation and infectivity neutralization in influenza. Immunology 119:1-7. http://dx.doi.org/10.1111/j.1365-2567.2006.02421.x.
7. Webster RG, Laver WG, Air GM, Schild GC. 1982. Molecular mechanisms of variation in influenza viruses. Nature 296:115-121. http://dx.doi.org/10.1038/296115a0.
8. Ellebedy AH, Ahmed R. 2012. Re-engaging cross-reactive memory B cells: the influenza puzzle. Front Immunol 3:53. http://dx.doi.org/10.3389/fimmu.2012.00053.
9. 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.
10. Clementi N, De Marco D, Mancini N, Solforosi L, Moreno GJ, Gubareva LV, Mishin V, Di Pietro A, Vicenzi E, Siccardi AG, Clementi M, Burioni R. 2011. A human monoclonal antibody with neutralizing activity against highly divergent influenza subtypes. PLoS One 6:e28001. http://dx.doi.org/10.1371/journal.pone.0028001.
11. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, Silacci C, Fernandez-Rodriguez BM, Agatic G, Bianchi S, Giacchetto-Sasselli I, Calder L, Sallusto F, Collins P, Haire LF, Temperton N, Langedijk JP, Skehel JJ, Lanzavecchia A. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333:850-856. http://dx.doi.org/10.1126/science.1205669.
12. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, Brakenhoff JP, Kompier R, Koldijk MH, Cornelissen LA, Poon LL, Peiris M, Koudstaal W, Wilson IA, Goudsmit J. 2011. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333:843-850. http://dx.doi.org/10.1126/science.1204839.
13. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LM, Santelli E, Stec B, Cadwell G, Ali M, Wan H, Murakami A, Yammanuru A, Han T, Cox NJ, Bankston LA, Donis RO, Liddington RC, Marasco WA. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16:265-273. http://dx.doi.org/10.1038/nsmb.1566.
14. Tan GS, Krammer F, Eggink D, Kongchanagul A, Moran TM, Palese P. 2012. A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J Virol 86:6179-6188. http://dx.doi.org/10.1128/JVI.00469-12.
15. Tan GS, Lee PS, Hoffman RM, Mazel-Sanchez B, Krammer F, Leon PE, Ward AB, Wilson IA, Palese P. 2014. Characterization of a broadly neutralizing monoclonal antibody that targets the fusion domain of group 2 influenza A virus hemagglutinin. J Virol 88:13580-13592. http://dx.doi.org/10.1128/JVI.02289-14.
16. + memory B cells. PLoS One 3:e3942. http://dx.doi.org/10.1371/journal.pone.0003942.
17. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O'Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208:181-193. http://dx.doi.org/10.1084/jem.20101352.
18. Ellebedy AH, Krammer F, Li GM, Miller MS, Chiu C, Wrammert J, Chang CY, Davis CW, McCausland M, Elbein R, Edupuganti S, Spearman P, Andrews SF, Wilson PC, Garcia-Sastre A, Mulligan MJ, Mehta AK, Palese P, Ahmed R. 2014. Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc Natl Acad Sci U S A 111:13133-13138. http://dx.doi.org/10.1073/pnas.1414070111.
19. Nachbagauer R, Wohlbold TJ, Hirsh A, Hai R, Sjursen H, Palese P, Cox RJ, Krammer F. 2014. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans. J Virol 88:13260-13268. http://dx.doi.org/10.1128/JVI.02133-14.
20. Pica N, Hai R, Krammer F, Wang TT, Maamary J, Eggink D, Tan GS, Krause JC, Moran T, Stein CR, Banach D, Wrammert J, Belshe RB, Garcia-Sastre A, Palese P. 2012. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc Natl Acad SciUSA109:2573-2578. http://dx.doi.org/10.1073/pnas.1200039109.
21. Whittle JR, Wheatley AK, Wu L, Lingwood D, Kanekiyo M, Ma SS, Narpala SR, Yassine HM, Frank GM, Yewdell JW, Ledgerwood JE, Wei CJ, McDermott AB, Graham BS, Koup RA, Nabel GJ. 2014. Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stemdirected antibodies from multiple Ig heavy-chain lineages. J Virol 88: 4047-4057. http://dx.doi.org/10.1128/JVI.03422-13.
22. Carter DM, Bloom CE, Nascimento EJ, Marques ET, Craigo JK, Cherry JL, Lipman DJ, Ross TM. 2013. Sequential seasonal H1N1 influenza virus infections protect ferrets against novel 2009 H1N1 influenza virus. J Virol 87:1400-1410. http://dx.doi.org/10.1128/JVI.02257-12.
23. Maines TR, Chen LM, Matsuoka Y, Chen H, Rowe T, Ortin J, Falcon A, Nguyen TH, Mai le Q, Sedyaningsih ER, Harun S, Tumpey TM, Donis RO, Cox NJ, Subbarao K, Katz JM. 2006. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103:12121-12126. http://dx.doi.org/10.1073/pnas.0605134103.
24. He W, Mullarkey CE, Duty JA, Moran TM, Palese P, Miller MS. 2015. Broadly neutralizing anti-influenza virus antibodies: enhancement of neutralizing potency in polyclonal mixtures and IgA backbones. J Virol 89:3610-3618. http://dx.doi.org/10.1128/JVI.03099-14.
25. 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.
26. Dreyfus C, Ekiert DC, Wilson IA. 2013. Structure of a classical broadly neutralizing stem antibody in complex with a pandemic H2 influenza virus hemagglutinin. J Virol 87:7149-7154. http://dx.doi.org/10.1128/JVI.02975-12.
27. Okuno Y, Isegawa Y, Sasao F, Ueda S. 1993. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J Virol 67:2552-2558.
28. Chiu C, Ellebedy AH, Wrammert J, Ahmed R. 2015. B cell responses to influenza infection and vaccination. Curr Top Microbiol Immunol 386: 381-398. http://dx.doi.org/10.1007/82_2014_425.
29. Margine I, Hai R, Albrecht RA, Obermoser G, Harrod AC, Banchereau J, Palucka K, Garcia-Sastre A, Palese P, Treanor JJ, Krammer F. 2013. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J Virol 87:4728-4737. http://dx.doi.org/10.1128/JVI.03509-12.
30. Li GM, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng NY, Lee JH, Huang M, Qu X, Edupuganti S, Mulligan M, Das SR, Yewdell JW, Mehta AK, Wilson PC, Ahmed R. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly crossreactive memory B cells. Proc Natl Acad Sci U S A 109:9047-9052. http://dx.doi.org/10.1073/pnas.1118979109.
31. Thomson CA, Wang Y, Jackson LM, Olson M, Wang W, Liavonchanka A, Keleta L, Silva V, Diederich S, Jones RB, Gubbay J, Pasick J, Petric M, Jean F, Allen VG, Brown EG, Rini JM, Schrader JW. 2012. Pandemic H1N1 influenza infection and vaccination in humans induces crossprotective antibodies that target the hemagglutinin stem. Front Immunol 3:87. http://dx.doi.org/10.3389/fimmu.2012.00087.
32. Cox RJ, Pedersen G, Madhun AS, Svindland S, Saevik M, Breakwell L, Hoschler K, Willemsen M, Campitelli L, Nostbakken JK, Weverling GJ, Klap J, McCullough KC, Zambon M, Kompier R, Sjursen H. 2011. Evaluation of a virosomal H5N1 vaccine formulated with matrixMadjuvant in a phase I clinical trial. Vaccine 29:8049-8059. http://dx.doi.org/10.1016/j.vaccine.2011.08.042.
33. Miller MS, Gardner TJ, Krammer F, Aguado LC, Tortorella D, Basler CF, Palese P. 2013. Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Sci Transl Med 5:198ra107. http://dx.doi.org/10.1126/scitranslmed.3006637.
34. Radbruch A, Muehlinghaus G, Luger EO, Inamine A, Smith KG, Dorner T, Hiepe F. 2006. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat Rev Immunol 6:741-750. http://dx.doi.org/10.1038/nri1886.
35. Marcelin G, DuBois R, Rubrum A, Russell CJ, McElhaney JE, Webby RJ. 2011. A contributing role for anti-neuraminidase antibodies on immunity to pandemic H1N1 2009 influenza A virus. PLoS One 6:e26335. http://dx.doi.org/10.1371/journal.pone.0026335.
36. Palese P, Wang TT. 2011. Why do influenza virus subtypes die out? A hypothesis. mBio 2(5):e00150-11. http://dx.doi.org/10.1128/mBio.00150-11.
37. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251. http://dx.doi.org/10.1126/science.1171491.
38. Sakabe S, Iwatsuki-Horimoto K, Horimoto T, Nidom CA, Le M, Takano R, Kubota-Koketsu R, Okuno Y, Ozawa M, Kawaoka Y. 2010. A cross-reactive neutralizing monoclonal antibody protects mice from H5N1 and pandemic (H1N1) 2009 virus infection. Antiviral Res 88:249-255. http://dx.doi.org/10.1016/j.antiviral.2010.09.007.
39. Friesen RH, Koudstaal W, Koldijk MH, Weverling GJ, Brakenhoff JP, Lenting PJ, Stittelaar KJ, Osterhaus AD, Kompier R, Goudsmit J. 2010. New class of monoclonal antibodies against severe influenza: prophylactic and therapeutic efficacy in ferrets. PLoS One 5:e9106. http://dx.doi.org/10.1371/journal.pone.0009106.
40. 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.
41. Terajima M, Cruz J, Co MD, Lee JH, Kaur K, Wrammert J, Wilson PC, Ennis FA. 2011. Complement-dependent lysis of influenza a virusinfected cells by broadly cross-reactive human monoclonal antibodies. J Virol 85:13463-13467. http://dx.doi.org/10.1128/JVI.05193-11.
42. 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.
43. 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.
44. Renegar KB, Small PA, Jr, Boykins LG, Wright PF. 2004. Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J Immunol 173:1978-1986. http://dx.doi.org/10.4049/jimmunol.173.3.1978.
45. 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.
46. He W, Mullarkey CE, Miller MS. 6 May 2015. Measuring the neutralization potency of influenza A virus hemagglutinin stalk/stem-binding antibodies in polyclonal preparations by microneutralization assay. Methods http://dx.doi.org/10.1016/j.ymeth.2015.04.037.
47. Krammer F, Palese P. 2015. Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14:167-182. http://dx.doi.org/10.1038/nrd4529.
48. Schneemann A, Speir JA, Tan GS, Khayat R, Ekiert DC, Matsuoka Y, Wilson IA. 2012. A virus-like particle that elicits cross-reactive antibodies to the conserved stem of influenza virus hemagglutinin. J Virol 86:11686-11697. http://dx.doi.org/10.1128/JVI.01694-12.
49. Wang TT, Tan GS, Hai R, Pica N, Ngai L, Ekiert DC, Wilson IA, Garcia-Sastre A, Moran TM, Palese P. 2010. Vaccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes. Proc Natl Acad SciUSA 107:18979-18984. http://dx.doi.org/10.1073/pnas.1013387107.
50. 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.
51. Wohlbold TJ, Nachbagauer R, Margine I, Tan GS, Hirsh A, Krammer F. 2015. Vaccination with soluble headless hemagglutinin protects mice from challenge with divergent influenza viruses. Vaccine 33:3314-3321. http://dx.doi.org/10.1016/j.vaccine.2015.05.038.
52. Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K, Garcia-Sastre A, Palese P. 2010. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1(1):e00018-10. http://dx.doi.org/10.1128/mBio.00018-10.
53. Margine I, Krammer F, Hai R, Heaton NS, Tan GS, Andrews SA, Runstadler JA, Wilson PC, Albrecht RA, Garcia-Sastre A, Palese P. 2013. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 87:10435-10446. http://dx.doi.org/10.1128/JVI.01715-13.
54. 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.
55. 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.
56. Krammer F, Margine I, Hai R, Flood A, Hirsh A, Tsvetnitsky V, Chen D, Palese P. 2014. H3 stalk-based chimeric hemagglutinin influenza virus constructs protect mice from H7N9 challenge. J Virol 88:2340-2343. http://dx.doi.org/10.1128/JVI.03183-13.
57. Eggink D, Goff PH, Palese P. 2014. Guiding the immune response against influenza virus hemagglutinin toward the conserved stalk domain by hyperglycosylation of the globular head domain. J Virol 88:699-704. http://dx.doi.org/10.1128/JVI.02608-13.
58. Bommakanti G, Lu X, Citron MP, Najar TA, Heidecker GJ, ter Meulen J, Varadarajan R, Liang X. 2012. Design of Escherichia coli-expressed stalk domain immunogens of H1N1 hemagglutinin that protect mice from lethal challenge. J Virol 86:13434-13444. http://dx.doi.org/10.1128/JVI.01429-12.
59. Bommakanti G, Citron MP, Hepler RW, Callahan C, Heidecker GJ, Najar TA, Lu X, Joyce JG, Shiver JW, Casimiro DR, ter Meulen J, Liang X, Varadarajan R. 2010. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc Natl Acad Sci U S A 107:13701-13706. http://dx.doi.org/10.1073/pnas.1007465107.
60. Impagliazzo A, Milder F, Kuipers H, Wagner M, Zhu X, Hoffman RM, van Meersbergen R, Huizingh J, Wanningen P, Verspuij J, de Man M, Ding Z, Apetri A, Kukrer 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, Radosevic 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.
61. Hai R, Krammer F, Tan GS, Pica N, Eggink D, Maamary J, Margine I, Albrecht RA, Palese P. 2012. Influenza viruses expressing chimeric hemagglutinins: globular head and stalk domains derived from different subtypes. J Virol 86:5774-5781. http://dx.doi.org/10.1128/JVI.00137-12.
62. Krammer F, Palese P. 2014. Universal influenza virus vaccines: need for clinical trials. Nat Immunol 15:3-5. http://dx.doi.org/10.1038/nri3797.