938
Views
68
CrossRef citations to date
0
Altmetric
Reviews

Mucosal immunity and nasal influenza vaccination

, &
Pages 595-607 | Published online: 09 Jan 2014

References

  • Fiore AE, Uyeki TM, Broder K et al.; Centers for Disease Control and Prevention (CDC). Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR. Recomm. Rep. 59(RR-8), 1–62 (2010).
  • Usonis V, Anca I, André F et al. Central European Vaccination Advisory Group guidance statement on recommendations for influenza vaccination in children. BMC Infect. Dis. 10, 168 (2010).
  • Renegar KB, Small PA Jr, Boykins LG, Wright PF. Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J. Immunol. 173(3), 1978–1986 (2004).
  • Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol. 6(2), 148–158 (2006).
  • Asahi-Ozaki Y, Yoshikawa T, Iwakura Y et al. Secretory IgA antibodies provide cross-protection against infection with diff erent strains of influenza B virus. J. Med. Virol. 74, 328–335 (2004).
  • Cerutti A, Rescigno M. The biology of intestinal immunoglobulin A responses. Immunity 28(6), 740–750 (2008).
  • Nimmerjahn F, Ravetch JV. Fcgamma receptors: old friends and new family members. Immunity 24(1), 19–28 (2006).
  • Kunisawa J, Nochi T, Kiyono H. Immunological commonalities and distinctions between airway and digestive immunity. Trends Immunol. 29(11), 505–513 (2008).
  • Brandtzaeg P. Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25(30), 5467–5484 (2007).
  • Shikina T, Hiroi T, Iwatani K et al. IgA class switch occurs in the organized nasopharynx- and gut associated lymphoid tissue, but not in the diffuse lamina propria of airways and gut. J. Immunol. 172, 6259–6264 (2004).
  • Debertin AS, Tschernig T, Tönjes H, Kleemann WJ, Tröger HD, Pabst R. Nasal-associated lymphoid tissue (NALT): frequency and localization in young children. Clin. Exp. Immunol. 134(3), 503–507 (2003).
  • Brandtzaeg P, Farstad IN, Haraldsen G. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol. Today 20, 267–277 (1999).
  • Varol C, Vallon-Eberhard A, Elinav E et al. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 31, 502–512 (2009).
  • Jaensson E, Uronen-Hansson H, Pabst O et al. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 205(9), 2139–2149 (2008).
  • Kiyono H, Fukuyama S. NALT- versus Peyer’s-patch-mediated mucosal immunity. Nat. Rev. Immunol. 4(9), 699–710 (2004).
  • Bumann D, Behre C, Behre K et al. Systemic, nasal and oral live vaccines against Pseudomonas aeruginosa: a clinical trial of immunogenicity in lower airways of human volunteers. Vaccine 28(3), 707–713 (2010).
  • Cunningham-Rundles C. Physiology of IgA and IgA deficiency. J. Clin. Immunol. 21(5), 303–309 (2001).
  • He B, Xu W, Santini PA et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26(6), 812–826 (2007).
  • Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol. 1(1), 11–22 (2008).
  • Mora JR, von Andrian UH. Differentiation and homing of IgA-secreting cells. Mucosal Immunol. 1(2), 96–109 (2008).
  • Sha Z, Kang SM, Compans RW. Mucosal immunization of CD4+ T cell-deficient mice with an inactivated virus induces IgG and IgA responses in serum and mucosal secretions. Virology 331(2), 387–395 (2005).
  • Suzuki K, Meek B, Doi Y et al. Aberrant expansion of segmented filamentous bacteria in IgA deficient gut. Proc. Natl Acad. Sci. USA 101, 1981–1986 (2004).
  • Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413(6856), 639–643 (2001).
  • Mond JJ, Vos Q, Lees A, Snapper CM. T cell independent antigens. Curr. Opin. Immunol. 7(3), 349–354 (1995).
  • Charles N, Hardwick D, Daugas E, Illei GG, Rivera J. Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat. Med. 16(6), 701–707 (2010).
  • Chen K, Cerutti A. New insights into the enigma of immunoglobulin D. Immunol. Rev. 237(1), 160–179 (2010).
  • Brandtzaeg P, Farstad IN, Johansen FE, Morton HC, Norderhaug IN, Yamanaka T. The B-cell system of human mucosae and exocrine glands. Immunol. Rev. 171, 45–87 (1999).
  • Agace WW, Roberts AI, Wu L, Greineder C, Ebert EC, Parker CM. Human intestinal lamina propria and intraepithelial lymphocytes express receptors specific for chemokines induced by inflammation. Eur. J. Immunol. 30(3), 819–826 (2000).
  • Rudraraju R, Surman S, Jones B, Sealy R, Woodland DL, Hurwitz JL. Phenotypes and functions of persistent Sendai virus-induced antibody forming cells and CD8+ T cells in diffuse nasal-associated lymphoid tissue typify lymphocyte responses of the gut. Virology 410(2), 429–436 (2011).
  • Petukhova G, Naikhin A, Chirkova T, Donina S, Korenkov D, Rudenko L. Comparative studies of local antibody and cellular immune responses to influenza infection and vaccination with live attenuated reassortant influenza vaccine (LAIV) utilizing a mouse nasal-associated lymphoid tissue (NALT) separation method. Vaccine 27(19), 2580–2587 (2009).
  • Wiley JA, Tighe MP, Harmsen AG. Upper respiratory tract resistance to influenza infection is not prevented by the absence of either nasal-associated lymphoid tissue or cervical lymph nodes. J. Immunol. 175(5), 3186–3196 (2005).
  • Zhang Y, Pacheco S, Acuna CL et al. Immunoglobulin A-deficient mice exhibit altered T helper 1-type immune responses but retain mucosal immunity to influenza virus. Immunology 105(3), 286–294 (2002).
  • Kaetzel CS, Robinson JK, Chintalacharuvu KR, Vaerman JP, Lamm ME. The polymeric immunoglobulin receptor (secretory component) mediates transport of immune complexes across epithelial cells: a local defense function for IgA. Proc. Natl Acad. Sci. USA. 88(19), 8796–8800 (1991).
  • Peterson DA, McNulty NP, Guruge JL, Gordon JI. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2(5), 328–339 (2007).
  • Ito R, Ozaki YA, Yoshikawa T et al. Roles of anti-hemagglutinin IgA and IgG antibodies in different sites of the respiratory tract of vaccinated mice in preventing lethal influenza pneumonia. Vaccine 21(19–20), 2362–2371 (2003).
  • Baumann U, Gocke K, Gewecke B, Freihorst J, von Specht BU. Assessment of pulmonary antibodies with induced sputum and bronchoalveolar lavage induced by nasal vaccination against Pseudomonas aeruginosa. Respir. Res. 8, 57 (2007).
  • O’Neal CM, Clements JD, Estes MK, Conner ME. Rotavirus 2/6 virus-like particles administered intranasally with cholera toxin, E. coli heat- labile toxin (LT), and LT-R192G induce protection from rotavirus challenge. J. Virol. 72, 3390–3393 (1998).
  • Johansen FE, Pekna M, Norderhaug IN et al. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immunoglobulin receptor/ secretory component-deficient mice. J. Exp. Med. 190, 915–921 (1999).
  • Asahi Y, Yoshikawa T, Watanabe I et al. Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines. J. Immunol. 168(6), 2930–2938 (2002).
  • Shvartsman YS, Agranovskaya EN, Zykov MP. Formation of secretory and circulating antibodies after immunization with live and inactivated influenza virus vaccines. J. Infect. Dis. 135(5), 697–705 (1977).
  • Lim PL, Rowley D. The effect of antibody on the intestinal absorption of macromolecules and on intestinal permeability in adult mice. Int. Arch. Allergy Appl. Immunol. 68(1), 41–46 (1982).
  • Brandtzaeg P, Tolo K. Mucosal penetrability enhanced by serum-derived antibodies. Nature 266(5599), 262–263 (1977).
  • Clements ML, Betts RF, Tierney EL, Murphy BR. Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus. J. Clin. Microbiol. 24(1), 157–160 (1986).
  • Mbawuike IN, Pacheco S, Acuna CL, Switzer KC, Zhang Y, Harriman GR. Mucosal immunity to influenza without IgA: an IgA knockout mouse model. J. Immunol. 162(5), 2530–2537 (1999).
  • Persson CG, Erjefält JS, Greiff L et al. Contribution of plasma- derived molecules to mucosal immune defence, disease and repair in the airways. Scand. J. Immunol. 47, 302–213 (1998).
  • Renegar KB, Johnson CD, Dewitt RC et al. Impairment of mucosal immunity by total parenteral nutrition: requirement for IgA in murine nasotracheal anti-influenza immunity. J. Immunol. 166(2), 819–825 (2001).
  • Arnaboldi PM, Behr MJ, Metzger DW. Mucosal B cell deficiency in IgA-/- mice abrogates the development of allergic lung inflammation. J. Immunol. 175, 1276–1285 (2005).
  • Lamkhioued B, Gounni AS, Gruart V, Pierce A, Capron A, Capron M. Human eosinophils express a receptor for secretory component role in secretory IgA-dependent activation. Eur. J. Immunol. 25, 117–125 (1995).
  • Brokstad KA, Cox RJ, Eriksson JC, Olofsson J, Jonsson R, Davidsson A. High prevalence of influenza specific antibody secreting cells in nasal mucosa. Scand. J. Immunol. 54(1–2), 243–247 (2001).
  • Brokstad KA, Eriksson JC, Cox RJ et al. Parenteral vaccination against influenza does not induce a local antigen-specific immune response in the nasal mucosa. J. Infect. Dis. 185(7), 878–884 (2002).
  • el-Madhun AS, Cox RJ, Søreide A, Olofsson J, Haaheim LR. Systemic and mucosal immune responses in young children and adults after parenteral influenza vaccination. J. Infect. Dis. 178(4), 933–939 (1998).
  • Johansen FE, Baekkevold ES, Carlsen HS, Farstad IN, Soler D, Brandtzaeg P. Regional induction of adhesion molecules and chemokine receptors explains disparate homing of human B cells to systemic and mucosal effector sites: dispersion from tonsils. Blood 106(2), 593–600 (2005).
  • He XS, Holmes TH, Zhang C et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J. Virol. 80(23), 11756–11766 (2006).
  • Rimmelzwaan GF, Fouchier RA, Osterhaus AD. Influenza virus specific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr. Opin. Biotechnol. 18, 529–536 (2007).
  • Treanor J, Wright PF. Immune correlates of protection against influenza in the human challenge model. Dev. Biol. (Basel) 115, 97–104 (2003).
  • Forrest BD, Pride MW, Dunning AJ et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin. Vaccine Immunol. 15(7), 1042–1053 (2008).
  • Hoft DF, Babusis E, Worku S et al. Live and inactivated influenza vaccines induce similar humoral responses, but only live vaccines induce diverse T-cell responses in young children. J. Infect. Dis. 204(6), 845–853 (2011).
  • Forrest BD, Steele AD, Hiemstra L, Rappaport R, Ambrose CS, Gruber WC. A prospective, randomized, open-label trial comparing the safety and efficacy of trivalent live attenuated and inactivated influenza vaccines in adults 60 years of age and older. Vaccine 29(20), 3633–3639 (2011).
  • Sasaki S, He XS, Holmes TH et al. Influence of prior influenza vaccination on antibody and B-cell responses. PLoS ONE 3(8), e2975 (2008).
  • Horvath KM, Herbst M, Zhou H, Zhang H, Noah TL, Jaspers I. Nasal lavage natural killer cell function is suppressed in smokers after live attenuated influenza virus. Respir. Res. 12, 102 (2011).
  • Baumann U. Mucosal vaccination against bacterial respiratory infections. Expert Rev. Vaccines. 7(8), 1257–1276 (2009).
  • Atmar RL, Keitel WA, Cate TR, Munoz FM, Ruben F, Couch RB. A dose-response evaluation of inactivated influenza vaccine given intranasally and intramuscularly to healthy young adults. Vaccine 25(29), 5367–5373 (2007).
  • van Vliet SJ, den Dunnen J, Gringhuis SI, Geijtenbeek TB, van Kooyk Y. Innate signaling and regulation of dendritic cell immunity. Curr. Opin. Immunol. 19(4), 435–440 (2007).
  • Pine S, Barackman J, Ott G, O’Hagan D. Intranasal immunization with influenza vaccine and a detoxified mutant of heat labile enterotoxin from Escherichia coli (LTK63). J. Control. Release 85(1–3), 263–270 (2002).
  • Kenney RT, Frech SA, Muenz LR, Villar CP, Glenn GM. Dose sparing with intradermal injection of influenza vaccine. N. Engl. J. Med. 351(22), 2295–2301 (2004).
  • Mutsch M, Zhou W, Rhodes P et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell’s palsy in Switzerland. N. Engl. J. Med. 350(9), 896–903 (2004).
  • Hinkula J, Devito C, Zuber B et al. A novel DNA adjuvant, N3, enhances mucosal and systemic immune responses induced by HIV-1 DNA and peptide immunizations. Vaccine 24, 4494–4497 (2006).
  • Stephenson I, Zambon MC, Rudin A et al. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J. Virol. 80(10), 4962–4970 (2006).
  • Halperin SA, Smith B, Clarke K, Treanor J, Mabrouk T, Germain M. Phase I, randomized, controlled trial to study the reactogenicity and immunogenicity of a nasal, inactivated trivalent infl uenza virus vaccine in healthy adults. Hum. Vaccin. 1, 37–42 (2005).
  • Illum L, Jabbal-Gill I, Hinchcliffe M, Fisher AN, Davis SS. Chitosan as a novel nasal delivery system for vaccines. Adv. Drug Deliv. Rev. 51(1–3), 81–96 (2001).
  • Read RC, Naylor SC, Potter CW et al. Effective nasal influenza vaccine delivery using chitosan. Vaccine 23(35), 4367–4374 (2005).
  • Ugwoke MI, Agu RU, Verbeke N, Kinget R. Nasal mucoadhesive drug delivery: background, applications, trends, and future perspectives. Adv. Drug. Deliv. Rev. 57, 1640–1665 (2005).
  • Couch RB, Atmar RL, Cate TR et al. Contrasting effects of type I interferon as a mucosal adjuvant for influenza vaccine in mice and humans. Vaccine 27(39), 5344–5348 (2009).
  • Berstad AK, Andersen SR, Dalseg R et al. Inactivated meningococci and pertusis bacteria are immunogenic and act as mucosal adjuvants for a nasal inactivated influenza virus vaccine. Vaccine 18(18), 1910–1919 (2000).
  • Mbow ML, De Gregorio E, Valiante NM, Rappuoli R. New adjuvants for human vaccines. Curr. Opin. Immunol. 22(3), 411–416 (2010).
  • Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313(5790), 1126–1130 (2006).
  • Liu YJ, Soumelis V, Watanabe N et al. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu. Rev. Immunol. 25, 193–219 (2007).
  • Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y. Adjuvants and autoimmunity. Lupus 18(13), 1217–1225 (2009).
  • Huang B, Zhao J, Li H et al. Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res. 65(12), 5009–5014 (2005).
  • Samdal HH, Bakke H, Oftung F et al. A non-living nasal influenza vaccine can induce major humoral and cellular immune responses in humans without the need for adjuvants. Hum. Vaccin. 1(2), 85–90 (2005).
  • Abramson JS. Intranasal, cold-adapted, live, attenuated influenza vaccine. Pediatr. Infect. Dis. J. 18(12), 1103–1104 (1999).
  • Cox RJ, Brokstad KA, Ogra P. Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand. J. Immunol. 59(1), 1–15 (2004).
  • Beyer WE, Palache AM, de Jong JC, Osterhaus AD. Cold-adapted live influenza vaccine versus inactivated vaccine: systemic vaccine reactions, local and systemic antibody response, and vaccine efficacy. A meta-analysis. Vaccine 20(9–10), 1340–1353 (2002).
  • Greenbaum E, Furst A, Kiderman A et al. Mucosal [SIgA] and serum [IgG] immunologic responses in the community after a single intra-nasal immunization with a new inactivated trivalent influenza vaccine. Vaccine 20(7–8), 1232–1239 (2002).
  • Bakke H, Samdal HH, Holst J et al. Oral spray immunization may be an alternative to intranasal vaccine delivery to induce systemic antibodies but not nasal mucosal or cellular immunity. Scand. J. Immunol. 63(3), 223–231 (2006).
  • Soane RJ, Frier M, Perkins AC, Jones NS, Davis SS, Illum L. Evaluation of the clearance characteristics of bioadhesive systems in humans. Int. J. Pharm. 178(1), 55–65 (1999).
  • Tafaghodi M, Abolghasem Sajadi Tabassi S, Jaafari MR, Zakavi SR, Momen-Nejad M. Evaluation of the clearance characteristics of various microspheres in the human nose by gamma-scintigraphy. Int. J. Pharm. 280(1–2), 125–135 (2004).
  • Vidgren MT, Kublik H. Nasal delivery systems and their effect on deposition and absorption. Adv. Drug Deliv. Rev. 29(1–2), 157–177 (1998).
  • Newman SP, Pitcairn GR, Dalby RN. Drug delivery to the nasal cavity: in vitro and in vivo assessment. Crit. Rev. Ther. Drug Carrier Syst. 21(1), 21–66 (2004).
  • Sullivan VJ, Mikszta JA, Laurent P, Huang J, Ford B. Non invasive delivery technologies: respiratory delivery of vaccines. Expert Opin. Drug. Deliv. 3, 87–95 (2006).
  • Glezen WP, Gaglani MJ, Kozinetz CA, Piedra PA. Direct and indirect effectiveness of influenze vaccination delivered to children at school preceding an epidemic caused by 3 new influenza strains. J. Infect. Dis. 202(11), 1626–1633 (2010).
  • Greenbaum E, Engelhard D, Levy R, Schlezinger M, Morag A, Zakay-Rones Z. Mucosal (SIgA) and serum (IgG) immunologic responses in young adults following intranasal administration of one or two doses of inactivated, trivalent anti-influenza vaccine. Vaccine 22(20), 2566–2577 (2004).
  • Tam JS, Capeding MR, Lum LC et al.; Pan-Asian CAIV-T Pediatric Efficacy Trial Network. Efficacy and safety of a live attenuated, cold-adapted influenza vaccine, trivalent against culture-confirmed influenza in young children in Asia. Pediatr. Infect. Dis. J. 26(7), 619–628 (2007).
  • Rhorer J, Ambrose CS, Dickinson S et al. Efficacy of live attenuated influenza vaccine in children: a meta-analysis of nine randomized clinical trials. Vaccine 27(7), 1101–1110 (2009).
  • Belshe RB, Edwards KM, Vesikari T et al. Live attenuated versus inactivated influenza vaccine in infants and young children. N. Engl. J. Med. 356, 685–696 (2007).
  • Ashkenazi S, Vertruyen A, Arístegui J et al. Superior relative efficacy of live atenuated influenza vaccine compared with inactivated influenza vaccine in young children with recurrent respiratory tract infections. Pediatr. Infect. Dis. J. 25, 870–879 (2006).
  • Fleming DM, Crovari P, Wahn U et al.; CAIV-T Asthma Study Group. Comparison of the efficacy and safety of live attenuated cold-adapted influenza vaccine, trivalent, with trivalent inactivated influenza virus vaccine in children and adolescents with asthma. Pediatr. Infect. Dis. J. 25(10), 860–869 (2006).
  • Jefferson T, Rivetti A, Harnden A, Di Pietrantonj C, Demicheli V. Vaccines for preventing influenza in healthy children. Cochrane Database Syst. Rev. 2, CD004879 (2008).
  • Osterholm MT, Kelley NS, Sommer A, Belongia EA. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect. Dis. 12(1), 36–44 (2012).
  • Izurieta HS, Haber P, Wise RP et al. Adverse events reported following live, cold-adapted, intranasal influenza vaccine. JAMA 294(21), 2720–2725 (2005).
  • Belshe RB, Ambrose CS, Yi T. Safety and efficacy of live attenuated influenza vaccine in children 2–7 years of age. Vaccine 26(Suppl. 4), D10–D16 (2008).
  • Haber P, Aarana J, Walton K. Safety of live attenuated influenza vaccine in children aged 24–59 months, vaccine adverse event reporting system (VAERS), 2007–2009. Presented at: 49th Interscience Conference on Antimicrobial Agents and Chemotherapy. CA, USA, 12–15 September 2009.
  • Tennis P, Toback SL, Andrews E, McQuay LJ, Ambrose CS. A postmarketing evaluation of the frequency of use and safety of live attenuated influenza vaccine use in nonrecommended children younger than 5 years. Vaccine 29(31), 4947–4952 (2011).
  • Ambrose CS, Levin MJ, Belshe RB. The relative efficacy of trivalent live attenuated and inactivated influenza vaccines in children and adults. Influenza Other Respi. Viruses 5(2), 67–75 (2011).
  • Reichert TA, Sugaya N, Fedson DS, Glezen WP, Simonsen L, Tashiro M. The Japanese experience with vaccinating schoolchildren against influenza. N. Engl. J. Med. 344(12), 889–896 (2001).
  • Becker PD, Bertot GM, Souss D, Ebensen T, Guzmán CA, Grinstein S. Intranasal vaccination with recombinant outer membrane protein CD and adamantylamide dipeptide as the mucosal adjuvant enhances pulmonary clearance of Moraxella catarrhalis in an experimental murine model. Infect. Immun. 75(4), 1778–1784 (2007).
  • Ebensen T, Link C, Riese P et al. A pegylated derivative of alpha- galactosylceramide exhibits improved biological properties. J. Immunol. 179(4), 2065–2073 (2007).
  • Ebensen T, Schulze K, Riese P, Link C, Morr M, Guzmán CA. The bacterial second messenger cyclic diGMP exhibits potent adjuvant properties. Vaccine 25(8), 1464–1469 (2007).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.