Is it possible to develop a “universal” influenza virus vaccine?: Immunogenetic considerations underlying b-cell biology in the development of a pan-subtype influenza a vaccine targeting the hemagglutinin stem

Cold Spring Harbor Perspectives in Biology

Volumn 10, Issue 7, 2018, Pages

  Andrews, Sarah F ^a   Graham, Barney S ^a   Mascola, John R ^a   McDermott, Adrian B ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; INFLUENZA VACCINE; VIRUS ANTIBODY;

ANTIBODY SPECIFICITY; B LYMPHOCYTE; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS; METABOLISM; PHYSIOLOGY;

ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; B-LYMPHOCYTES; HEMAGGLUTININS; HUMANS; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN;

EID: 85033980610     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a029413     Document Type: Article

References (48)

1. Andrews SF, Huang Y, Kaur K, Popova LI, Ho IY, Pauli NT, Henry Dunand CJ, Taylor WM, Lim S, Huang M, et al. 2015. Immune history profoundly affects broadly protective B cell responses to influenza. Sci Transl Med 7: 316ra192.
2. Avnir Y, Tallarico AS, Zhu Q, Bennett AS, Connelly G, Sheehan J, Sui J, Fahmy A, Huang CY, Cadwell G, et al. 2014. Molecular signatures of hemagglutinin stem-directed heterosubtypic human neutralizing antibodies against influenza A viruses. PLoS Pathog 10: e1004103.
3. Avnir Y, Watson CT, Glanville J, Peterson EC, Tallarico AS, Bennett AS, Qin K, Fu Y, Huang C-YY, Beigel JH, et al. 2016. IGHV1-69 polymorphism modulates anti-influenza antibody repertoires, correlates with IGHV utilization shifts and varies by ethnicity. Sci Rep 6: 20842.
4. Clementi N, De Marco D, Mancini N, Solforosi L, Moreno GJ, Gubareva LV, Mishin V, Di Pietro A, Vicenzi E, Sic-cardi AG, et al. 2011. A human monoclonal antibody with neutralizing activity against highly divergent influenza subtypes. PloS ONE 6: e28001.
5. Corti D, Suguitan AL, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, Santos C, Luke CJ, Torres-Velez FJ, Temperton NJ, et al. 2010. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest 120: 1663– 1673.
6. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, Vachieri SG, Pinna D, Minola A, Vanzetta F, et al. 2011. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333: 850–856.
7. Dreyfus C, Laursen NS, Kwaks T, Zuijdgeest D, Khayat R, Ekiert DC, Lee JH, Metlagel Z, Bujny MV, Jongeneelen M, et al. 2012. Highly conserved protective epitopes on influenza B viruses. Science 337: 1343–1348.
8. 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.
9. Gorman J, Soto C, Yang MM, Davenport TM, Guttman M, Bailer RT, Chambers M, Chuang G-YY, DeKosky BJ, Do-ria-Rose NA, et al. 2016. Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonali-ties that enable vaccine design. Nat Struct Mol Biol 23: 81–90.
10. 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 Virology 86: 5774–5781.
11. He W, Mullarkey CE, Miller MS. 2015. Measuring the neutralization potency of influenza A virus hemagglutinin stalk/stem-binding antibodies in polyclonal preparations by microneutralization assay. Methods 90: 95–100.
12. Henry Dunand CJ, Wilson PC. 2015. Restricted, canonical, stereotyped and convergent immunoglobulin responses. Philos Trans R Soc Lond B Biol Sci doi: 10.1098/rstb.2014.0238.
13. Hu W, Chen A, Miao Y, Xia S, Ling Z, Xu K, Wang T, Xu Y, Cui J, Wu H, et al. 2013. Fully human broadly neutraliz-ing monoclonal antibodies against influenza A viruses generated from the memory B cells of a 2009 pandemic H1N1 influenza vaccine recipient. Virology 435: 320– 328.
14. Impagliazzo A, Milder F, Kuipers H, Wagner MV, Zhu X, Hoffman RM, van Meersbergen R, Huizingh J, Wannin-gen P, Verspuij J, et al. 2015. A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science 349: 1301–1306.
15. Jackson K, Liu Y, Roskin KM, Glanville J, Hoh RA, Seo K, Marshall EL, Gurley TC, Moody AM, Haynes BF, et al. 2014. Human responses to influenza vaccination show seroconversion signatures and convergent antibody rearrangements. Cell Host Microbe 16: 105–114.
16. Joyce MG, Wheatley AK, Thomas PV, Chuang G-YY, Soto C, Bailer RT, Druz A, Georgiev IS, Gillespie RA, Kanekiyo M, et al. 2016. Vaccine-Induced antibodies that neutralize group 1 and group 2 influenza A viruses. Cell 166: 609– 623.
17. Kallewaard NL, Corti D, Collins PJ, Neu U, McAuliffe JM, Benjamin E, Wachter-Rosati L, Palmer-Hill FJ, Yuan AQ, Walker PA, et al. 2016. Structure and function analysis of an antibody recognizing all influenza A subtypes. Cell 166: 596–608.
18. Kanekiyo M, Bu W, Joyce MG, Meng G, Whittle JR, Baxa U, Yamamoto T, Narpala S, Todd JP, Rao SS, et al. 2015. Rational design of an Epstein–Barr virus vaccine targeting the receptor-binding site. Cell 162: 1090–1100.
19. 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.
20. Kucharski AJ, Lessler J, Read JM, Zhu H, Jiang CQ, Guan Y, Cummings DA, Riley S. 2015. Estimating the life course of influenza A(H3N2) antibody responses from cross-sectional data. PLoS Biol 13: e1002082.
21. Li G-MM, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng N-YY, Lee J-HH, Huang M, Qu X, Edupuganti S, et al. 2012. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci 109: 9047– 9052.
22. 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.
23. Lu Y, Welsh JP, Swartz JR. 2014. Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines. Proc Natl Acad Sci 111: 125–130.
24. Margine I, Krammer F, Hai R, Heaton NS, Tan GS, Andrews SA, Runstadler JA, Wilson PC, Albrecht RA, García-Sastre A, et al. 2013. Hemagglutinin stalk-based universal vaccine constructs protect against group 2 influenza A viruses. J Virol 87: 10435–10446.
25. Martins AJ, Tsang JS. 2014. Random yet deterministic: Convergent immunoglobulin responses to influenza. Trends Microbiol 22: 488–489.
26. McCraw DM, Gallagher JR, Harris AK. 2016. Characterization of influenza vaccine hemagglutinin complexes by cryo-electron microscopy and image analyses reveals structural polymorphisms. Clin Vaccine Immunol 23: 483–495.
27. McLellan JS, Chen M, Joyce MG, Sastry M, Stewart-Jones GB, Yang Y, Zhang B, Chen L, Srivatsan S, Zheng A, et al. 2013. Structure-based design of a fusion glycoprotein vaccine for respiratory syncytial virus. Science 342: 592–598.
28. 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.
29. Nabel GJ, Fauci AS. 2010. Induction of unnatural immunity: Prospects for a broadly protective universal influenza vaccine. Nat Med 16: 1389–1391.
30. Nachbagauer R, Choi A, Izikson R, Cox MM, Palese P, Krammer F. 2016a. Age dependence and isotype specificity of influenza virus hemagglutinin stalk-reactive antibodies in humans. MBio 7: e01996–15.
31. Nachbagauer R, Miller MS, Hai R, Ryder AB, Rose JK, Palese P, Garcia-Sastre A, Krammer F, Albrecht RA. 2016b. Hemagglutinin stalk immunity reduces influenza virus replication and transmission in ferrets. J Virol 90: 3268– 3273.
32. Nakamura G, Chai N, Park S, Chiang N, Lin Z, Chiu H, Fong R, Yan D, Kim J, Zhang J, et al. 2013. An in vivo human-plasmablast enrichment technique allows rapid identification of therapeutic influenza A antibodies. Cell Host Microbe 14: 93–103.
33. Pappas L, Foglierini M, Piccoli L, Kallewaard NL, Turrini F, Silacci C, Fernandez-Rodriguez B, Agatic G, Giacchetto-Sasselli I, Pellicciotta G, et al. 2014. Rapid development of broadly influenza neutralizing antibodies through redundant mutations. Nature 516: 418–422.
34. Parameswaran P, Liu Y, Roskin KM, Jackson K, Dixit VP, Lee J-Y, Artiles KL, Zompi S, Vargas M, Simen BB, et al. 2013. Convergent antibody signatures in human Dengue. Cell Host Microbe 13: 691–700.
35. Skowronski DM, Chambers C, Gilca R, De Serres G. 2016. Repeat influenza vaccination and high-dose efficacy. Clin Infect Dis doi: 10.1093/cid/ciw544.
36. Sui J, Hwang WC, Perez S, Wei G, Aird D, Chen LmM, Santelli E, Stec B, Cadwell G, Ali M, et al. 2009. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat Struct Mol Biol 16: 265–273.
37. 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.
38. Thomson CA, Wang Y, Jackson LM, Olson M, Wang W, Liavonchanka A, Keleta L, Silva V, Diederich S, Jones RB, et al. 2012. Pandemic H1N1 influenza infection and vaccination in humans induces cross-protective antibodies that target the hemagglutinin stem. Front Immunol 3: 87.
39. Valkenburg SA, Mallajosyula VV, Li OT, Chin AW, Carnell G, Temperton N, Varadarajan R, Poon LL. 2016. Stalking influenza by vaccination with pre-fusion headless HA mini-stem. Sci Rep 6: 22666.
40. Watson CT, Steinberg KM, Huddleston J, Warren RL, Malig M, Schein J, Willsey AJ, Joy JB, Scott JK, Graves TA, et al. 2013. Complete haplotype sequence of the human immunoglobulin heavy-chain variable, diversity, and joining genes and characterization of allelic and copy-num-ber variation. Am J Hum Genet 92: 530–546.
41. Weitkamp J-H, Kallewaard NL, Bowen AL, LaFleur BJ, Greenberg HB, Crowe JE. 2005. VH1–46 is the dominant immunoglobulin heavy chain gene segment in rotavirus-specific memory B cells expressing the intestinal homing receptor α4β7. J Immunol 174: 3454–3460.
42. Wheatley AK, Whittle JR, Lingwood D, Kanekiyo M, Yassine HM, Ma SS, Narpala SR, Prabhakaran MS, Matus-Nic-odemos RA, Bailer RT, et al. 2015. H5N1 vaccine-elicited memory B cells are genetically constrained by the IGHV locus in the recognition of a neutralizing epitope in the hemagglutinin stem. J Immunol 195: 602–610.
43. 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.
44. Wrammert J, Koutsonanos D, Li GMM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, et al. 2011. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208: 181–193.
45. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, Wang C, Chen X, Longo NS, Louder M, McKee K, et al. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333: 1593–1602.
46. Wu Y, Cho M, Shore D, Song M, Choi J, Jiang T, Deng YQQ, Bourgeois M, Almli L, Yang H, et al. 2015. A potent broad-spectrum protective human monoclonal antibody crosslinking two haemagglutinin monomers of influenza A virus. Nat Commun 6: 7708.
47. Yassine HM, Boyington JC, McTamney PM, Wei CJ, Kanekiyo M, Kong WP, Gallagher JR, Wang L, Zhang Y, Joyce MG, et al. 2015. Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med 21: 1065–1070.
48. Yen HL, Webster RG. 2009. Pandemic influenza as a current threat. Curr Topics Microbiol Immunol 333: 3–24.