Flow cytometry reveals that H5N1 vaccination elicits cross-reactive stem-directed antibodies from multiple ig heavy-chain lineages

Journal of Virology

Volumn 88, Issue 8, 2014, Pages 4047-4057

  Whittle, James R R ^a   Wheatley, Adam K ^a   Wu, Lan ^a,b   Lingwood, Daniel ^a   Kanekiyo, Masaru ^a   Ma, Steven S ^a   Narpala, Sandeep R ^a   Yassine, Hadi M ^a   Frank, Gregory M ^a   Yewdell, Jonathan W ^a   Ledgerwood, Julie E ^a   Wei, Chih Jen ^a,b   McDermott, Adrian B ^a   Graham, Barney S ^a   Koup, Richard A ^a   Nabel, Gary J ^a,b  

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

^b SANOFI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD19 ANTIGEN; CD27 ANTIGEN; HEMAGGLUTININ STEM ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INFLUENZA VIRUS HEMAGGLUTININ H1; INFLUENZA VIRUS HEMAGGLUTININ H5; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG CROSS REACTIVITY; DRUG DESIGN; DRUG PROTEIN BINDING; DRUG SELECTIVITY; FLOW CYTOMETRY; HEMAGGLUTINATION INHIBITION; HEMAGGLUTINATION TEST; HUMAN; HUMAN CELL; IC 50; INFLUENZA VACCINATION; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR PROBE; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL (TOPIC); POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ALIGNMENT; STRUCTURE ACTIVITY RELATION; VACCINE PRODUCTION;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CROSS REACTIONS; FLOW CYTOMETRY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN HEAVY CHAINS; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA;

EID: 84896917279     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03422-13     Document Type: Article

References (36)

1. 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.
2. 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.
3. 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.
4. Ekiert DC, Friesen RH, Bhabha G, Kwaks T, Jongeneelen M, Yu W, Ophorst C, Cox F, Korse HJ, Brandenburg B, Vogels R, BrakenhoffJP, 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.
5. Whittle JR, Zhang R, Khurana S, King LR, Manischewitz J, Golding H, Dormitzer PR, Haynes BF, Walter EB, Moody MA, Kepler TB, Liao HX, Harrison SC. 2011. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 108:14216-14221. http://dx.doi.org/10.1073/pnas.1111497108.
6. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, Lee JH, Metlagel Z, Bujny MV, Jongeneelen M, van der Vlugt R, Lamrani M, Korse HJ, Geelen E, Sahin O, Sieuwerts M, BrakenhoffJP, Vogels R, Li OT, Poon LL, Peiris M, Koudstaal W, Ward AB, Wilson IA, Goudsmit J, Friesen RH. 2012. Highly conserved protective epitopes on influenza B viruses. Science 337:1343-1348. http://dx.doi.org/10.1126/science.1222908.
7. Throsby M, van den Brink E, Jongeneelen M, Poon LL, Alard P, Cornelissen L, Bakker A, Cox F, van Deventer E, Guan Y, Cinatl J, ter Meulen J, Lasters I, Carsetti R, Peiris M, de Kruif J, Goudsmit J. 2008. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 3:e3942. http://dx.doi.org/10.1371/journal.pone.0003942.
8. Friesen RH, Koudstaal W, Koldijk MH, Weverling GJ, BrakenhoffJP, 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.
9. Corti D, Suguitan AL, Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, Santos C, Luke CJ, Torres-Velez FJ, Temperton NJ, Weiss RA, Sallusto F, Subbarao K, Lanzavecchia A. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120:1663-1673. http://dx.doi.org/10.1172/JCI41902.
10. 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.
11. 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.
12. 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 cross-protective antibodies that target the hemagglutinin stem. Front. Immunol. 3:87. http://dx.doi.org/10.3389/fimmu.2012.00087.
13. Doucett VP, Gerhard W, Owler K, Curry D, Brown L, Baumgarth N. 2005. Enumeration and characterization of virus-specific B cells by multicolor flow cytometry. J. Immunol. Methods 303:40-52. http://dx.doi.org/10.1016/j.jim.2005.05.014.
14. 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.
15. Alberts B, Bray D, Lewis J, RaffM, Roberts K, Watson J. 1994. Molecular biology of the cell, 3rd ed. Garland Science, New York, NY.
16. Ledgerwood J, Zephir K, Hu Z, Wei C-J, Chang L, Enama M, Hendel C, Sitar S, Bailer R, Koup R, Mascola J, Nabel G, Graham B, VRC 310 Study Team. 2013. Prime-boost interval matters: A randomized phase I study to identify the minimum interval necessary to observe the h5 DNA influenza vaccine priming effect. J. Infect. Dis. 208:418-422. http://dx.doi.org/10.1093/infdis/jit180.
17. Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, Boyington JC, Wei CJ, Nabel GJ. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489: 566-570. http://dx.doi.org/10.1038/nature11371.
18. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, Wardemann H. 2008. Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J. Immunol. Methods 329:112-124. http://dx.doi.org/10.1016/j.jim.2007.09.017.
19. Brochet X, Lefranc MP, Giudicelli V. 2008. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res. 36:W503-W508. http://dx.doi.org/10.1093/nar/gkn316.
20. Giudicelli V, Brochet X, Lefranc MP. 2011. IMGT/V-QUEST: IMGT standardized analysis of the immunoglobulin (IG) and T cell receptor (TR) nucleotide sequences. Cold Spring Harb. Protoc. 2011:695-715. http://dx.doi.org/10.1101/pdb.prot5633.
21. Wei CJ, Boyington JC, Dai K, Houser KV, Pearce MB, Kong WP, Yang ZY, Tumpey TM, Nabel GJ. 2010. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci. Transl. Med. 2:24ra21. http://dx.doi.org/10.1126/scitranslmed.3000799.
22. Kanekiyo M, Wei C-J, Yassine HM, McTamney PM, Boyington JC, Whittle JRR, Rao SS, Kong W-P, Wang L, Nabel GJ. 2013. Selfassembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499:102-106. http://dx.doi.org/10.1038/nature12202.
23. Joyce MG, Kanekiyo M, Xu L, Biertumpfel C, Boyington JC, Moquin S, Shi W, Wu X, Yang Y, Yang ZY, Zhang B, Zheng A, Zhou T, Zhu J, Mascola JR, Kwong PD, Nabel GJ. 2013. Outer domain of HIV-1 gp120: Antigenic optimization, structural malleability, and crystal structure with antibody VRC-PG04. J. Virol. 87:2294-2306. http://dx.doi.org/10.1128/JVI.02717-12.
24. Martin J, Wharton SA, Lin YP, Takemoto DK, Skehel JJ, Wiley DC, Steinhauer DA. 1998. Studies of the binding properties of influenza hemagglutinin receptor-site mutants. Virology 241:101-111. http://dx.doi.org/10.1006/viro.1997.8958.
25. Bradley KC, Galloway SE, Lasanajak Y, Song X, Heimburg-Molinaro J, Yu H, Chen X, Talekar GR, Smith DF, Cummings RD, Steinhauer DA. 2011. Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics. J. Virol. 85:12387-12398. http://dx.doi.org/10.1128/JVI.05570-11.
26. Gamblin SJ, Haire LF, Russell RJ, Stevens DJ, Xiao B, Ha Y, Vasisht N, Steinhauer DA, Daniels RS, Elliot A, Wiley DC, Skehel JJ. 2004. The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838-1842. http://dx.doi.org/10.1126/science.1093155.
27. Ekiert DC, Kashyap AK, Steel J, Rubrum A, Bhabha G, Khayat R, Lee JH, Dillon MA, O'Neil RE, Faynboym AM, Horowitz M, Horowitz L, Ward AB, Palese P, Webby R, Lerner RA, Bhatt RR, Wilson IA. 2012. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489:526-532. http://dx.doi.org/10.1038/nature11414.
28. Yang ZY, Wei CJ, Kong WP, Wu L, Xu L, Smith DF, Nabel GJ. 2007. Immunization by avian H5 influenza hemagglutinin mutants with altered receptor binding specificity. Science 317:825-828. http://dx.doi.org/10.1126/science.1135165.
29. Ledgerwood JE, Wei CJ, Hu Z, Gordon IJ, Enama ME, Hendel CS, McTamney PM, Pearce MB, Yassine HM, Boyington JC, Bailer R, Tumpey TM, Koup RA, Mascola JR, Nabel GJ, Graham BS. 2011. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect. Dis. 11:916-924. http://dx.doi.org/10.1016/S1473-3099(11)70240-7.
30. Reading SA, Dimmock NJ. 2007. Neutralization of animal virus infectivity by antibody. Arch. Virol. 152:1047-1059. http://dx.doi.org/10.1007/s00705-006-0923-8.
31. 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.
32. 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.
33. 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. Sci. U. S. A. 109:2573-2578. http://dx.doi.org/10.1073/pnas.1200039109.
34. Sui J, Sheehan J, Hwang WC, Bankston LA, Burchett SK, Huang CY, Liddington RC, Beigel JH, Marasco WA. 2011. Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies. Clin. Infect. Dis. 52:1003-1009. http://dx.doi.org/10.1093/cid/cir121.
35. Miller MS, Tsibane T, Krammer F, Hai R, Rahmat S, Basler CF, Palese P. 2013. 1976 and 2009 H1N1 influenza virus vaccines boost antihemagglutinin stalk antibodies in humans. J. Infect. Dis. 207:98-105. http://dx.doi.org/10.1093/infdis/jis652.
36. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE, Jr, Wilson IA. 2010. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328:357-360. http://dx.doi.org/10.1126/science.1186430.