Neutralizing antibodies against previously encountered influenza virus strains increase over time: A longitudinal analysis

Science Translational Medicine

Volumn 5, Issue 198, 2013, Pages

  Miller, Matthew S ^a   Gardner, Thomas J ^a   Krammer, Florian ^a   Aguado, Lauren C ^a   Tortorella, Domenico ^a   Basler, Christopher F ^a   Palese, Peter ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; NEUTRALIZING ANTIBODY;

ADULT; AGED; ANTIBODY SPECIFICITY; ANTIBODY TITER; ANTIGEN SHIFT; CLINICAL ARTICLE; CROSS REACTION; FEMALE; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMORAL IMMUNITY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N2; LONGITUDINAL STUDY; MALE; NONHUMAN; PANDEMIC INFLUENZA; PRIORITY JOURNAL; REVIEW; SEASONAL INFLUENZA; VIRUS MUTATION; VIRUS STRAIN;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODIES, NEUTRALIZING; FEMALE; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA, HUMAN; LONGITUDINAL STUDIES; MALE; MIDDLE AGED; PANDEMICS; YOUNG ADULT;

EID: 84883856356     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006637     Document Type: Review

References (38)

1. J. A. McCullers, L. A. Van De Velde, K. J. Allison, K. C. Branum, R. J. Webby, P. M. Flynn, Recipients of vaccine against the 1976 "swine flu" have enhanced neutralization responses to the 2009 novel H1N1 influenza virus. Clin. Infect. Dis. 50, 1487-1492 (2010).
2. B. Manicassamy, R. A. Medina, R. Hai, T. Tsibane, S. Stertz, E. Nistal-Villán, P. Palese, C. F. Basler, A. García-Sastre, Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog. 6, e1000745 (2010).
3. M. S. Miller, T. Tsibane, F. Krammer, R. Hai, S. Rahmat, C. F. Basler, P. Palese, 1976 and 2009 H1N1 influenza virus vaccines boost anti-hemagglutinin stalk antibodies in humans. J. Infect. Dis. 207, 98-105 (2013).
4. + T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc. Natl. Acad. Sci. U.S.A. 107, 12599-12604 (2010).
5. P. Palese, T. T. Wang, Why do influenza virus subtypes die out? A hypothesis. MBio 2, e00150-11 (2011).
6. N. Pica, R. Hai, F. Krammer, T. T. Wang, J. Maamary, D. Eggink, G. S. Tan, J. C. Krause, T. Moran, C. R. Stein, D. Banach, J. Wrammert, R. B. Belshe, A. García-Sastre, P. Palese, 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 (2012).
7. R. G. Webster, Original antigenic sin in ferrets: The response to sequential infections with influenza viruses. J. Immunol. 97, 177-183 (1966).
8. T. Francis, F. M. Davenport, A. V. Hennessy, A serological recapitulation of human infection with different strains of influenza virus. Trans. Assoc. Am. Physicians 66, 231-239 (1953).
9. T. W. Hoskins, J. R. Davies, A. J. Smith, C. L. Miller, A. Allchin, Assessment of inactivated influenza-A vaccine after three outbreaks of influenza A at Christ's Hospital. Lancet 1, 33-35 (1979).
10. I. J. Amanna, N. E. Carlson, M. K. Slifka, Duration of humoral immunity to common viral and vaccine antigens. N. Engl. J. Med. 357, 1903-1915 (2007).
11. Original antigenic sin. N. Engl. J. Med. 258, 1016-1017 (1958).
12. F. de St Groth, R. G. Webster, Disquisitions of original antigenic sin. I. Evidence in man. J. Exp. Med. 124, 331-345 (1966).
13. F. de St Groth, R. G. Webster, Disquisitions on original antigenic sin. II. Proof in lower creatures. J. Exp. Med. 124, 347-361 (1966).
14. F. M. Davenport, A. V. Hennessy, T. Francis, Epidemiologic and immunologic significance of age distribution of antibody to antigenic variants of influenza virus. J. Exp. Med. 98, 641-656 (1953).
15. J. Lessler, S. Riley, J. M. Read, S. Wang, H. Zhu, G. J. D. Smith, Y. Guan, C. Q. Jiang, D. A. T. Cummings, Evidence for antigenic seniority in influenza A (H3N2) antibody responses in southern China. PLoS Pathog. 8, e1002802 (2012).
16. G. M. Li, C. Chiu, J. Wrammert, M. McCausland, S. F. Andrews, N. Y. Zheng, J. H. Lee, M. Huang, X. Qu, S. Edupuganti, M. Mulligan, S. R. Das, J. W. Yewdell, A. K. Mehta, P. C. Wilson, R. Ahmed, Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc. Natl. Acad. Sci. U.S.A. 109, 9047-9052 (2012).
17. J. Sui, J. Sheehan, W. C. Hwang, L. A. Bankston, S. K. Burchett, C. Y. Huang, R. C. Liddington, J. H. Beigel, W. A. Marasco, Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies. Clin. Infect. Dis. 52, 1003-1009 (2011).
18. J. Wrammert, D. Koutsonanos, G. M. Li, S. Edupuganti, J. Sui, M. Morrissey, M. McCausland, I. Skountzou, M. Hornig, W. I. Lipkin, A. Mehta, B. Razavi, C. Del Rio, N. Y. Zheng, J. H. Lee, M. Huang, Z. Ali, K. Kaur, S. Andrews, R. R. Amara, Y. Wang, S. R. Das, C. D. O'Donnell, J. W. Yewdell, K. Subbarao, W. A. Marasco, M. J. Mulligan, R. Compans, R. Ahmed, P. C. Wilson, Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208, 181-193 (2011).
19. D. Corti, A. L. Suguitan, D. Pinna, C. Silacci, B. M. Fernandez-Rodriguez, F. Vanzetta, C. Santos, C. J. Luke, F. J. Torres-Velez, N. J. Temperton, R. A. Weiss, F. Sallusto, K. Subbarao, A. Lanzavecchia, Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120, 1663-1673 (2010).
20. D. Corti, J. Voss, S. J. Gamblin, G. Codoni, A. Macagno, D. Jarrossay, S. G. Vachieri, D. Pinna, A. Minola, F. Vanzetta, C. Silacci, B. M. Fernandez-Rodriguez, G. Agatic, S. Bianchi, I. Giacchetto-Sasselli, L. Calder, F. Sallusto, P. Collins, L. F. Haire, N. Temperton, J. P. M. Langedijk, J. J. Skehel, A. Lanzavecchia, A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011).
21. I. Margine, R. Hai, R. A. Albrecht, G. Obermoser, A. C. Harrod, J. Banchereau, K. Palucka, A. García-Sastre, P. Palese, J. J. Treanor, F. Krammer, H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J. Virol. 87, 4728-4737 (2013).
22. D. C. Ekiert, R. H. E. Friesen, G. Bhabha, T. Kwaks, M. Jongeneelen, W. Yu, C. Ophorst, F. Cox, H. J. W. M. Korse, B. Brandenburg, R. Vogels, J. P. J. Brakenhoff, R. Kompier, M. H. Koldijk, L. A. H. M. Cornelissen, L. L. M. Poon, M. Peiris, W. Koudstaal, I. A. Wilson, J. Goudsmit, A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850 (2011).
23. N. Jiang, J. He, J. A. Weinstein, L. Penland, S. Sasaki, X. S. He, C. L. Dekker, N. Y. Zheng, M. Huang, M. Sullivan, P. C. Wilson, H. B. Greenberg, M. M. Davis, D. S. Fisher, S. R. Quake, Lineage structure of the human antibody repertoire in response to influenza vaccination. Sci. Transl. Med. 5, 171ra19 (2013).
24. F. Krammer, N. Pica, R. Hai, G. S. Tan, P. Palese, Hemagglutinin stalk-reactive antibodies are boosted following sequential infection with seasonal and pandemic H1N1 influenza virus in mice. J. Virol. 86, 10302-10307 (2012).
25. C. A. Thomson, Y. Wang, L. M. Jackson, M. Olson, W. Wang, A. Liavonchanka, L. Keleta, V. Silva, S. Diederich, R. B. Jones, J. Gubbay, J. Pasick, M. Petric, F. Jean, V. G. Allen, E. G. Brown, J. M. Rini, J. W. Schrader, Pandemic H1N1 influenza infection and vaccination in humans induces cross-protective antibodies that target the hemagglutinin stem. Front. Immunol. 3, 87 (2012).
26. D. J. Smith, A. S. Lapedes, J. C. de Jong, T. M. Bestebroer, G. F. Rimmelzwaan, A. D.M. E. Osterhaus, R. A. M. Fouchier, Mapping the antigenic and genetic evolution of influenza virus. Science 305, 371-376 (2004).
27. J. C. Krause, T. Tsibane, T. M. Tumpey, C. J. Huffman, R. Albrecht, D. L. Blum, I. Ramos, A. Fernandez-Sesma, K. M. Edwards, A. García-Sastre, C. F. Basler, J. E. Crowe, Human monoclonal antibodies to pandemic 1957 H2N2 and pandemic 1968 H3N2 influenza viruses. J. Virol. 86, 6334-6340 (2012).
28. N. L. Bernasconi, E. Traggiai, A. Lanzavecchia, Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298, 2199-2202 (2002).
29. D. Corti, A. Lanzavecchia, Broadly neutralizing antiviral antibodies. Annu. Rev. Immunol. 31, 705-742 (2013).
30. S. Varani, M. P. Landini, Cytomegalovirus-induced immunopathology and its clinical consequences. Herpesviridae 2, 6 (2011).
31. M. Reeves, J. Sinclair, Aspects of human cytomegalovirus latency and reactivation. Curr. Top. Microbiol. Immunol. 325, 297-313 (2008).
32. R. Alonso Arias, M. A. Moro-García, A. Echeverría, J. J. Solano-Jaurrieta, F. M. Suárez-García, C. López-Larrea, Intensity of the humoral response to cytomegalovirus is associated with the phenotypic and functional status of the immune system. J. Virol. 87, 4486-4495 (2013).
33. R. P. Stowe, E. V. Kozlova, D. L. Yetman, D. M. Walling, J. S. Goodwin, R. Glaser, Chronic herpesvirus reactivation occurs in aging. Exp. Gerontol. 42, 563-570 (2007).
34. F. Krammer, I. Margine, G. S. Tan, N. Pica, J. C. Krause, P. Palese, A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7, e43603 (2012).
35. R. Hai, F. Krammer, G. S. Tan, N. Pica, D. Eggink, J. Maamary, I. Margine, R. A. Albrecht, P. Palese, Influenza viruses expressing chimeric hemagglutinins: Globular head and stalk domains derived from different subtypes. J. Virol. 86, 5774-5781 (2012).
36. T. J. Gardner, C. Bolovan-Fritts, M. W. Teng, V. Redmann, T. A. Kraus, R. Sperling, T. Moran, W. Britt, L. S. Weinberger, D. Tortorella, Development of a high-throughput assay to measure the neutralization capability of anti-cytomegalovirus antibodies. Clin. Vaccine Immunol. 20, 540-550 (2013).
37. M. W. Teng, C. Bolovan-Fritts, R. D. Dar, A. Womack, M. L. Simpson, T. Shenk, L. S. Weinberger, An endogenous accelerator for viral gene expression confers a fitness advantage. Cell 151, 1569-1580 (2012).
38. M. S. Miller, T. J. Gardner, F. Krammer, L. C. Aguado, D. Tortorella, C. F. Basler, P. Palese, Neutralizing antibodies against previously encountered influenza virus strains increase over time: A longitudinal analysis. Sci. Transl. Med. 5, 198ra107 (2013).