Serological memory and long-term protection to novel H1N1 influenza virus after skin vaccination

Journal of Infectious Diseases

Volumn 204, Issue 4, 2011, Pages 582-591

  Koutsonanos, Dimitrios G ^a   Del Pilar Martin, Maria ^a   Zarnitsyn, Vladimir G ^b   Jacob, Joshy ^a   Prausnitz, Mark R ^a   Compans, Richard W ^a   Skountzou, Ioanna ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Georgia Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HEMAGGLUTININ; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; INFLUENZA VACCINE; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA;

2009 H1N1 INFLUENZA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; BONE MARROW CELL; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG ADMINISTRATION ROUTE; DRUG EFFICACY; FEMALE; HEMAGGLUTINATION INHIBITION TEST; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; INFLUENZA VACCINATION; INFLUENZA VIRUS A H1N1; LETHAL DOSE; LONG TERM CARE; LONGEVITY; MATERIAL COATING; MICRONEEDLE; MOUSE; NEEDLE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; SPLEEN CELL; VIRAL CLEARANCE; VIRUS INHIBITION; VIRUS PNEUMONIA; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, VIRAL; BONE MARROW CELLS; CELL LINE; DOGS; FEMALE; IMMUNITY, HUMORAL; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INJECTIONS, INTRADERMAL; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; SPLEEN; VIRUS REPLICATION;

EID: 79960860961     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir094     Document Type: Article

References (50)

1. Subbarao K, Murphy BR, Fauci AS. Development of effective vaccines against pandemic influenza. Immunity 2006; 24:5-9. (Pubitemid 43077193)
2. Subbramanian RA, Basha S, Brady RC, Hazenfeld S, Shata MT, Bernstein DI. Age-related changes in magnitude and diversity of cross-reactive CD4(+) T-cell responses to the novel pandemic H1N1 influenza hemagglutinin. Hum Immunol 2010; 71:957-63.
3. Castellino F, Galli G, Del Giudice G, Rappuoli R. Generating memory with vaccination. Eur J Immunol 2009; 39:2100-5.
4. Charest AF, McDougall J, Goldstein MB. A randomized comparison of intradermal and intramuscular vaccination against hepatitis B virus in incident chronic hemodialysis patients. Am J Kidney Dis 2000; 36:976-82.
5. Egemen A, Aksit S, Kurugol Z, Erensoy S, Bilgic A, Akilli M. Low-dose intradermal versus intramuscular administration of recombinant hepatitis B vaccine: a comparison of immunogenicity in infants and preschool children. Vaccine 1998; 16:1511-5. (Pubitemid 28370049)
6. Raz E, Carson DA, Parker SE, et al. Intradermal gene immunization: the possible role of DNA uptake in the induction of cellular immunity to viruses. Proc Natl Acad Sci U S A 1994; 91:9519-23. (Pubitemid 24297946)
7. Berzofsky JA, Ahlers JD, Belyakov IM. Strategies for designing and optimizing new generation vaccines. Nat Rev Immunol 2001; 1:209-19. (Pubitemid 33741959)
8. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392:245-52. (Pubitemid 28155090)
9. Kupper TS, Fuhlbrigge RC. Immune surveillance in the skin: mechanisms and clinical consequences. Nat Rev Immunol 2004; 4:211-22. (Pubitemid 38339087)
10. Abadie V, Bonduelle O, Duffy D, Parizot C, Verrier B, Combadiere B. Original encounter with antigen determines antigen-presenting cell imprinting of the quality of the immune response in mice. PLoS One 2009; 4:e8159.
11. Bos JD, Kapsenberg ML. The skin immune system: progress in cutaneous biology. Immunol Today 1993; 14:75-8. (Pubitemid 23046167)
12. Glenn GM, Kenney RT. Mass vaccination: solutions in the skin. Curr Top Microbiol Immunol 2006; 304:247-68. (Pubitemid 47413300)
13. Angel CE, George E, Ostrovsky LL, Dunbar PR. Comprehensive analysis of MHC-II expression in healthy human skin. Immunol Cell Biol 2007; 85:363-9. (Pubitemid 47035608)
14. Koutsonanos DG, del Pilar Martin M, Zarnitsyn VG, et al. Transdermal influenza immunization with vaccine-coated microneedle arrays. PLoS One 2009; 4:e4773.
15. Zhu Q, Zarnitsyn VG, Ye L, et al. Immunization by vaccine-coated microneedle arrays protects against lethal influenza virus challenge. Proc Natl Acad Sci U S A 2009; 106:7968-73.
16. Sullivan SP, Koutsonanos DG, Del Pilar Martin M, et al. Dissolving polymer microneedle patches for influenza vaccination. Nat Med 2010; 16:915-20.
17. Kim YC, Quan FS, Yoo DG, Compans RW, Kang SM, Prausnitz MR. Improved influenza vaccination in the skin using vaccine coated microneedles. Vaccine 2009; 27:6932-8.
18. Cohen J, Enserink M. Swine flu. After delays, WHO agrees: the 2009 pandemic has begun. Science 2009; 324:1496-7.
19. Garten RJ, Davis CT, Russell CA, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009; 325:197-201.
20. Glezen WP. Containing the novel influenza A (H1N1) virus. Clin Infect Dis 2010; 50:869-70.
21. Kim YC, Quan FS, Compans RW, Kang SM, Prausnitz MR. Formulation and coating of microneedles with inactivated influenza virus to improve vaccine stability and immunogenicity. J Control Release 2010; 142:187-95.
22. Skountzou I, Quan FS, Jacob J, Compans RW, Kang SM. Transcutaneous immunization with inactivated influenza virus induces protective immune responses. Vaccine 2006; 24:6110-9. (Pubitemid 44175614)
23. Compans RW. Hemagglutination-inhibition: rapid assay for neuraminic acid-containing viruses. J Virol 1974; 14:1307-9.
24. Czerkinsky CC, Nilsson LA, Nygren H, Ouchterlony O, Tarkowski A. A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J Immunol Methods 1983; 65:109-21. (Pubitemid 14203438)
25. Slifka MK, Ahmed R. Long-lived plasma cells: a mechanism for maintaining persistent antibody production. Curr Opin Immunol 1998; 10:252-8. (Pubitemid 28286950)
26. Crotty S, Aubert RD, Glidewell J, Ahmed R. Tracking human antigenspecific memory B cells: a sensitive and generalized ELISPOT system. J Immunol Methods 2004; 286:111-22. (Pubitemid 38490401)
27. Itoh Y, Shinya K, Kiso M, et al. In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature 2009; 460:1021-5.
28. Combadiere B, Siberil S, Duffy D. Keeping the memory of influenza viruses. Pathol Biol (Paris) 2010; 58:e79-86.
29. Agace WW. Tissue-tropic effector T cells: generation and targeting opportunities. Nat Rev Immunol 2006; 6:682-92. (Pubitemid 44298217)
30. Fitzner N, Clauberg S, Essmann F, Liebmann J, Kolb-Bachofen V. Human skin endothelial cells can express all 10 TLR genes and respond to respective ligands. Clin Vaccine Immunol 2008; 15:138-46. (Pubitemid 351966534)
31. Elgueta R, de Vries VC, Noelle RJ. The immortality of humoral immunity. Immunol Rev 2010; 236:139-50.
32. Kaech SM, Wherry EJ, Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002; 2:251-62. (Pubitemid 37323225)
33. Graham CM, Christensen JR, Thomas DB. Differential induction of CD94 and NKG2 in CD4 helper T cells. A consequence of influenza virus infection and interferon-gamma? Immunology 2007; 121:238-47. (Pubitemid 46663092)
34. McKinstry KK, Strutt TM, Swain SL. The potential of CD4 T-cell memory. Immunology 2010; 130:1-9.
35. Doherty PC, Kelso A. Toward a broadly protective influenza vaccine. J Clin Invest 2008; 118:3273-5.
36. Weiss ID, Wald O, Wald H, et al. IFN-gamma treatment at early stages of influenza virus infection protects mice from death in a NK cell-dependent manner. J Interferon Cytokine Res 2010; 30:439-49.
37. Vogt A, Mahe B, Costagliola D, et al. Transcutaneous anti-influenza vaccination promotes both CD4 and CD8 T cell immune responses in humans. J Immunol 2008; 180:1482-9.
38. Abadie V, Badell E, Douillard P, et al. Neutrophils rapidly migrate via lymphatics afterMycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 2005; 106:1843-50. (Pubitemid 41208603)
39. Wrammert J, Ahmed R. Maintenance of serological memory. Biol Chem 2008; 389:537-9. (Pubitemid 351874200)
40. Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science 1996; 272:54-60. (Pubitemid 26110754)
41. Traggiai E, Puzone R, Lanzavecchia A. Antigen dependent and independent mechanisms that sustain serum antibody levels. Vaccine 2003; 21(Suppl 2):S35-7. (Pubitemid 36588647)
42. Slifka MK, Antia R, Whitmire JK, Ahmed R. Humoral immunity due to long-lived plasma cells. Immunity 1998; 8:363-72. (Pubitemid 28188896)
43. Ahuja A, Anderson SM, Khalil A, Shlomchik MJ. Maintenance of the plasma cell pool is independent of memory B cells. Proc Natl Acad Sci U S A 2008; 105:4802-7. (Pubitemid 351753827)
44. DiLillo DJ, Hamaguchi Y, Ueda Y, et al. Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J Immunol 2008; 180:361-71.
45. Edwards KM. The burden of influenza in children: time for prevention. Clin Infect Dis 2009; 49:1022-4.
46. Zimmerman RK, Lauderdale DS, Tan SM, Wagener DK. Prevalence of high-risk indications for influenza vaccine varies by age, race, and income. Vaccine 2010; 28:6470-7.
47. Pinna D, Corti D, Jarrossay D, Sallusto F, Lanzavecchia A. Clonal dissection of the human memory B-cell repertoire following infection and vaccination. Eur J Immunol 2009; 39:1260-70.
48. Bernasconi NL, Traggiai E, Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 2002; 298:2199-202. (Pubitemid 35471246)
49. Lambert PH, Laurent PE. Intradermal vaccine delivery: will new delivery systems transform vaccine administration? Vaccine 2008; 26:3197-208.
50. Prausnitz MR, Mikszta JA, Cormier M, Andrianov AK. Microneedle-based vaccines. Curr Top Microbiol Immunol 2009; 333:369-93.