Infection with 2009 H1N1 influenza virus primes for immunological memory in human nose-associated lymphoid tissue, offering cross-reactive immunity to H1N1 and avian H5N1 viruses

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5331-5339

  Mahallawi, Waleed H ^a   Kasbekar, Anand V ^b   McCormick, Maxwell S ^c   Hoschler, Katja ^d   Temperton, Nigel ^e   Leong, Samuel C ^c   Beer, Helen ^c   Ferrara, Francesca ^e   McNamara, Paul S ^a   Zhang, Qibo ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b ALDER HEY CHILDREN S HOSPITAL   (United Kingdom)

^c ROYAL LIVERPOOL UNIVERSITY HOSPITAL   (United Kingdom)

^d PUBLIC HEALTH ENGLAND   (United Kingdom)

^e UNIVERSITY OF KENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; VIRUS ANTIGEN;

2009 H1N1 INFLUENZA; ADULT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE ACTIVATION; CHILD; CONTROLLED STUDY; CROSS PROTECTION; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOLOGICAL MEMORY; IMMUNOSTIMULATION; INFLUENZA A (H3N2); INFLUENZA A (H5N1); INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; LYMPHOID TISSUE; MEMORY CELL; MUCOSAL IMMUNITY; NONHUMAN; NOSE ASSOCIATED LYMPHOID TISSUE; PRESCHOOL CHILD; PRIORITY JOURNAL; SEASONAL INFLUENZA; VIRUS NEUTRALIZATION;

ADOLESCENT; ADULT; B-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; CROSS REACTIONS; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA, HUMAN; LYMPHOID TISSUE; MALE; NASAL MUCOSA; YOUNG ADULT;

EID: 84877338716     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03547-12     Document Type: Article

References (49)

1. Murphy B, Webster R. 1996. Orthomyxoviruses, p 1397-1445. In Fields BN, Knipe DM, Howley PM (ed), Fields virology, 3rd ed. Lippincott- Raven Publishers, Philadelphia, PA.
2. Brockwell-Staats C, Webster R, Webbyaet R. 2009. Diversity of influenza viruses in swine and the emergence of a novel human pandemic influenza A(H1N1). Influenza Other Respi. Viruses 3:207-213.
3. Dawood F, Finelli J, Shaw M, Lindstrom S, Garten R, Gubareva L, Xu X, Bridges C, Uyeki T. 2009. Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N. Engl. J. Med. 360:2605-2615.
4. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, Liu F, Dong L, DeVos JR, Gargiullo PM, Brammer TL, Cox NJ, Tumpey TM, Katz JM. 2009. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med. 361:1945-1952.
5. Puck JM, Glezen WP, Frank AL, Six HR. 1980. Protection of infants from infection with influenza A virus by transplacentally acquired antibody. J. Infect. Dis. 142:844-849.
6. Simmons CP, Bernasconi NL, Suguitan AL, Jr, Mills K, Ward JM, Chau NVV, Hien TT, Sallusto F, Ha DQ, Farrar J, de Jong MD, Lanzavecchia A, Subbarao K. 2007. Prophylactic and therapeutic efficacy of human monoclonal antibodies against H5N1 influenza. PLoS Med. 4:e178. doi: 10.1371/journal.pmed.0040178.
7. Ikonen N, Strengell M, Kinnunen L, Osterlund P, Pirhonen J, Broman M, Davidkin I, Ziegler T, Julkunen I. 2010. High frequency of crossreacting antibodies against 2009 pandemic influenza A(H1N1) virus among the elderly in Finland. Euro Surveill. 15:19478.
8. Miller E, Hoschler K, Hardelid P, Stanford E, Andrews N, Zambon M. 2010. Incidence of 2009 pandemic influenza A H1N1 infection in England: a cross-sectional serological study. Lancet 375:1100 -1108.
9. 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.
10. Corti D, Suguitan AL, Jr, Pinna D, Silacci C, Fernandez-Rodriguez B, Vanzetta F, Santos C, Luke C, Torres-Velez F, Temperton N, Weiss R, Sallusto F, Subbarao K, Lanzavecchia A. 19 April 2010, posting date. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120:1663-1673. doi:1610.1172/JCI41902.
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 JPM, 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.
12. 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, García-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.
13. 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.
14. Air GM. 1981. Sequence relationships among the hemagglutinin genes of 12 subtypes of influenza A virus. Proc. Natl. Acad. Sci. U. S. A. 78:7639- 7643.
15. Bernstein JM, Gorfien J, Brandtzaeg P. 1999. The immunobiology of the tonsils and adenoids, p 1339-1362. In Ogra PL, Mestecky J, Lamm ME, Strober W, McGhee JR, Bienenstock J (ed), Mucosal immunology. Academic Press, San Diego, CA.
16. Kiyono H, Fukuyama S, Kiyono H, Fukuyama S. 2004. NALT- versus Peyer's-patch-mediated mucosal immunity. Nat. Rev. Immunol. 4:699-710.
17. Wu HY, Nguyen HH, Russell MW. 1997. Nasal lymphoid tissue (NALT) as a mucosal immune inductive site. Scand. J. Immunol. 46:506-513.
18. Boyaka PN, Wright PF, Marinaro M, Kiyono H, Johnson JE, Gonzales RA, Ikizler MR, Werkhaven JA, Jackson RJ, Fujihashi K, Di Fabio S, Staats HF, McGhee JR. 2000. Human nasopharyngealassociated lymphoreticular tissues. Functional analysis of subepithelial and intraepithelial B and T cells from adenoids and tonsils. Am. J. Pathol. 157:2023-2035.
19. Nadal D, Soh N, Schlapfer E, Bernstein JM, Ogra PL. 1992. Distribution characteristics of immunoglobulin-secreting cells in adenoids. Relationship to age and disease. Int. J. Pediatr. Otorhinolaryngol. 24:121-130.
20. Zhang Q, Bagrade L, Clarke E, Paton JC, Nunez DA, Finn A, Zhang Q, Bagrade L, Clarke E, Paton JC, Nunez DA, Finn A. 2010. Bacterial lipoproteins differentially regulate human primary and memory CD4-T and B cell responses to pneumococcal protein antigens through Toll-like receptor 2. J. Infect. Dis. 201:1753-1763.
21. Zhang Q, Choo S, Finn A. 2002. Immune responses to novel pneumococcal proteins pneumolysin, PspA, PsaA, and CbpA in adenoidal B cells from children. Infect. Immun. 70:5363-5369.
22. Guthrie T, Hobbs CGL, Davenport V, Horton RE, Heyderman RS, Williams NA. 2004. Parenteral influenza vaccination influences mucosal and systemic T cell-mediated immunity in healthy adults. J. Infect. Dis. 190:1927-1935.
23. Wiley JA, Hogan RJ, Woodland DL, Harmsen AG. 2001. Antigenspecific CD8- T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167:3293-3299.
24. Zuercher AW, Coffin SE, Thurnheer MC, Fundova P, Cebra JJ. 2002. Nasal-associated lymphoid tissue is a mucosal inductive site for virusspecific humoral and cellular immune responses. J. Immunol. 168:1796-1803.
25. Krause JC, Tumpey TM, Huffman CJ, McGraw PA, Pearce MB, Tsibane T, Hai R, Basler CF, Crowe JE. 2010. Naturally occurring human monoclonal antibodies neutralize both 1918 and 2009 pandemic influenza A (H1N1) viruses. J. Virol. 84:3127-3130.
26. Xu R, Ekiert DC, Krause JC, Hai R, Crowe JE, Wilson IA. 2010. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328:357-360.
27. Yu X, Tsibane T, McGraw PA, House FS, Keefer CJ, Hicar MD, Tumpey TM, Pappas C, Perrone LA, Martinez O, Stevens J, Wilson IA, Aguilar PV, Altschuler EL, Basler CF, Crowe JE, Jr. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455:532-536.
28. Li G-M, Chiu C, Wrammert J, McCausland M, Andrews SF, Zheng N-Y, Lee J-H, 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 cross-reactive memory B cells. Proc. Natl. Acad. Sci. U. S. A. 109:9047-9052.
29. Mahallawi WH, Kasbekar AV, McCormick MS, Hoschler K, Temperton N, Leong SC, Beer H, Ferrara F, McNamara PS, Zhang Q. 2012. Abstr. Eur. Conf. Immunol., 5 to 8 September 2012, Glasgow, United Kingdom, abstr P-0445.
30. Wood JM, Schild GC, Newman RW, Seagroatt V. 1977. An improved single-radial-immunodiffusion technique for the assay of influenza haemagglutinin antigen: application for potency determinations of inactivated whole virus and subunit vaccines. J. Biol. Stand. 5:237-247.
31. Stevens J, Corper AL, Basler CF, Taubenberger JK, Palese P, Wilson IA. 2004. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303:1866-1870.
32. Smith GE, Franklin Volvovitz F, Wilkinson BE, Hackett CS. June 1998. Method for producing influenza hemagglutinin multivalent vaccines using baculovirus. U.S. Patent 5,762,939.
33. Zhang Q, Leong SC, McNamara PS, Mubarak A, Malley R, Finn A. 2011. Characterisation of regulatory T cells in nasal associated lymphoid tissue in children: relationships with pneumococcal colonization. PLoS Pathog. 7:e1002175. doi:10.1371/journal.ppat.1002175.
34. Crotty S, Felgner P, Davies H, Glidewell J, Villarreal L, Ahmed R. 2003. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 171:4969-4973.
35. Zhang Q, Bernatoniene J, Bagrade L, Pollard AJ, Mitchell TJ, Paton JC, Finn A. 2006. Serum and mucosal antibody responses to pneumococcal protein antigens in children: relationships with carriage status. Eur. J. Immunol. 36:46-57.
36. Temperton NJ, Hoschler K, Major D, Nicolson C, Manvell R, Hien VM, Ha DQ, De Jong M, Zambon M, Takeuchi Y, Weiss RA. 2007. A sensitive retroviral pseudotype assay for influenza H5N1-neutralizing antibodies. Influenza Other Respi. Viruses 1:105-112.
37. Kelly H, Peck HA, Laurie KL, Wu P, Nishiura H, Cowling BJ. 2011. The age-specific cumulative incidence of infection with pandemic influenza H1N1 2009 was similar in various countries prior to vaccination. PLoS One 6:e21828. doi:10.1371/journal.pone.0021828.
38. Ekiert DC, Bhabha G, Elsliger M-A, Friesen RHE, Jongeneelen M, Throsby M, Goudsmit J, Wilson IA. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324:246-251.
39. Manicassamy B, Medina RA, Hai R, Tsibane T, Stertz S, Nistal-Villán E, Palese P, Basler CF, García-Sastre A. 2010. 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. doi:10.1371 /journal.ppat.1000745.
40. 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.
41. Ellebedy AH, Ahmed R. 2012. Re-engaging cross-reactive memory B cells: the influenza puzzle. Front. Immunol. 3:53.
42. Miller MS, Tsibane T, Krammer F, Hai R, Rahmat S, Basler CF, Palese P. 2013. 1976 and 2009 H1N1 influenza virus vaccines boost anti-hemagglutinin stalk antibodies in humans. J. Infect. Dis. 207:98- 105.
43. Khurana S, Suguitan AL, Jr, Rivera Y, Simmons CP, Lanzavecchia A, Sallusto F, Manischewitz J, King LR, Subbarao K, Golding H. 2009. Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med. 6:e1000049. doi:10.1371/journal.pmed.1000049.
44. Health Protection Agency. Surveillance of influenza and other respiratory viruses in the UK, 2010-2011. Health Protection Agency, London, United Kingdom. http://www.hpa.org.uk/webc/HPAwebFile/ HPAweb _C/1296687414154.
45. Palese P, Wang TT. 2011. Why do influenza virus subtypes die out? A hypothesis. mBio 2:e00150-11. doi:10.1128/mBio.00150-00111.
46. Health Protection Agency. 2012. HPA weekly national influenza report, 16 August. Summary of UK surveillance of influenza and other seasonal respiratory illnesses. http://www.hpa.org.uk/webc/HPAwebFile/HPAweb _C/1317135659994.
47. Korkeila M, Lehtonen H, Ahman H, Leroy O, Eskola J, Kayhty H. 2000. Salivary anti-capsular antibodies in infants and children immunised with Streptococcus pneumoniae capsular polysaccharides conjugated to diphtheria or tetanus toxoid. Vaccine 18:1218-1226.
48. Nurkka A, MacLennan J, Jantti V, Obaro S, Greenwood B, Kayhty H. 2000. Salivary antibody response to vaccination with meningococcal A/C polysaccharide vaccine in previously vaccinated and unvaccinated Gambian children. Vaccine 19:547-556.
49. Brokstad KA, Cox RJ, Olofsson J, Jonsson R, Haaheim LR. 1995. Parenteral influenza vaccination induces a rapid systemic and local immune response. J. Infect. Dis. 171:198-203.