Abstract
The availability of effective vaccines has had the most profound positive effect on improving the quality of public health by preventing infectious diseases. Despite many successful vaccines, there are still old and new emerging pathogens against which there is no vaccine available. A better understanding of how vaccines work for providing protection will help to improve current vaccines as well as to develop effective vaccines against pathogens for which we do not have a proper means to control. Recent studies have focused on innate immunity as the first line of host defense and its role in inducing adaptive immunity; such studies have been an intense area of research, which will reveal the immunological mechanisms how vaccines work for protection. Toll-like receptors (TLRs), a family of receptors for pathogen-associated molecular patterns on cells of the innate immune system, play a critical role in detecting and responding to microbial infections. Importantly, the innate immune system modulates the quantity and quality of longterm T and B cell memory and protective immune responses to pathogens. Limited studies suggest that vaccines which mimic natural infection and/or the structure of pathogens seem to be effective in inducing long-term protective immunity. A better understanding of the similarities and differences of the molecular and cellular events in host responses to vaccination and pathogen infection would enable the rationale for design of novel preventive measures against many challenging pathogens.
Keywords: adaptive, immune responses, innate, memory B cells, pathogen, plasma cells, signaling, TLRs, vaccine, VLPs
References
- Akira S. TLR signaling. Curr. Top Microbiol. Immunol. 2006;311:1–16. doi: 10.1007/3-540-32636-7_1. [DOI] [PubMed] [Google Scholar]
- Akira S., Yamamoto M., Takeda K. Role of adapters in Toll-like receptor signalling. Biochem. Soc. Trans. 2003;31:637–642. doi: 10.1042/BST0310637. [DOI] [PubMed] [Google Scholar]
- Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006;124:783–801. doi: 10.1016/j.cell.2006.02.015. [DOI] [PubMed] [Google Scholar]
- Alarcon J.B., Hartley A.W., Harvey N.G., Mikszta J.A. Preclinical evaluation of microneedle technology for intradermal delivery of influenza vaccines. Clin. Vaccine Immunol. 2007;14:375–381. doi: 10.1128/CVI.00387-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Auewarakul P., Kositanont U., Sornsathapornkul P., Tothong P., Kanyok R., Thongcharoen P. Antibody responses after dose-sparing intradermal influenza vaccination. Vaccine. 2007;25:659–663. doi: 10.1016/j.vaccine.2006.08.026. [DOI] [PubMed] [Google Scholar]
- Bachmann M.F., Zinkernagel R.M., Oxenius A. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 1998;161:5791–5794. [PubMed] [Google Scholar]
- Barton G.M., Medzhitov R. Toll-like receptor signaling pathways. Science. 2003;300:1524–1525. doi: 10.1126/science.1085536. [DOI] [PubMed] [Google Scholar]
- Bernasconi N.L., Traggiai E., Lanzavecchia A. Maintenance of serological memory by polyclonal activation of human memory B cells. Science. 2002;298:2199–2202. doi: 10.1126/science.1076071. [DOI] [PubMed] [Google Scholar]
- Bertolotti-Ciarlet A., Ciarlet M., Crawford S.E., Conner M.E., Estes M.K. Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine. 2003;21:3885–3900. doi: 10.1016/S0264-410X(03)00308-6. [DOI] [PubMed] [Google Scholar]
- Beutler B., Hoebe K., Georgel P., Tabeta K., Du X. Genetic analysis of innate immunity: TIR adapter proteins in innate and adaptive immune responses. Microbes Infect. 2004;6:1374–1381. doi: 10.1016/j.micinf.2004.08.017. [DOI] [PubMed] [Google Scholar]
- Blazevic V., Trubey C.M., Shearer G.M. Comparison of in vitro immunostimulatory potential of live and inactivated influenza viruses. Hum. Immunol. 2000;61:845–849. doi: 10.1016/S0198-8859(00)00170-1. [DOI] [PubMed] [Google Scholar]
- Blink E.J., Light A., Kallies A., Nutt S.L., Hodgkin P.D., Tarlinton D.M. Early appearance of germinal center-derived memory B cells and plasma cells in blood after primary immunization. J. Exp. Med. 2005;201:545–554. doi: 10.1084/jem.20042060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowie A., O’Neill L.A. The interleukin-1 receptor/Tolllike receptor superfamily: signal generators for pro-inflammatory interleukins and microbial products. J. Leukoc. Biol. 2000;67:508–514. doi: 10.1002/jlb.67.4.508. [DOI] [PubMed] [Google Scholar]
- Bright R.A., Carter D.M., Crevar C.J., Toapanta F.R., Steckbeck J.D., Cole K.S., Kumar N.M., Pushko P., Smith G., Tumpey T.M., et al. Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle. PLoS ONE. 2008;3:e1501. doi: 10.1371/journal.pone.0001501. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buonaguro L., Tornesello M.L., Tagliamonte M., Gallo R.C., Wang L.X., Kamin-Lewis R., Abdelwahab S., Lewis G.K., Buonaguro F.M. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol. 2006;80:9134–9143. doi: 10.1128/JVI.00050-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buonaguro L., Monaco A., Arico E., Wang E., Tornesello M.L., Lewis G.K., Marincola F.M., Buonaguro F.M. Gene expression profile of peripheral blood mononuclear cells in response to HIV-VLPs stimulation. BMC Bioinformatics. 2008;9:S5. doi: 10.1186/1471-2105-9-S2-S5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Burrows P.D., Cooper M.D. B cell development and differentiation. Curr. Opin. Immunol. 1997;9:239–244. doi: 10.1016/S0952-7915(97)80142-2. [DOI] [PubMed] [Google Scholar]
- Cairns B., Maile R., Barnes C.M., Frelinger J.A., Meyer A.A. Increased Toll-like receptor 4 expression on T cells may be a mechanism for enhanced T cell response late after burn injury. J. Trauma. 2006;61:293–298. doi: 10.1097/01.ta.0000228969.46633.bb. [DOI] [PubMed] [Google Scholar]
- Carter R.H., Fearon D.T. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science. 1992;256:105–107. doi: 10.1126/science.1373518. [DOI] [PubMed] [Google Scholar]
- Carter R.H., Spycher M.O., Ng Y.C., Hoffman R., Fearon D.T. Synergistic interaction between complement receptor type 2 and membrane IgM on B lymphocytes. J. Immunol. 1988;141:457–463. [PubMed] [Google Scholar]
- Chen, W., and Gluud, C. (2005). Vaccines for preventing hepatitis B in health-care workers. Cochrane Database Syst. Rev. (4), CD000100. [DOI] [PubMed]
- Chilosi M., Adami F., Lestani M., Montagna L., Cimarosto L., Semenzato G., Pizzolo G., Menestrina F. CD138/syndecan-1: a useful immunohistochemical marker of normal and neoplastic plasma cells on routine trephine bone marrow biopsies. Mod. Pathol. 1999;12:1101–1106. [PubMed] [Google Scholar]
- Coutelier J.P., van der Logt J.T., Heessen F.W., Warnier G., Van Snick J. IgG2a restriction of murine antibodies elicited by viral infections. J. Exp. Med. 1987;165:64–69. doi: 10.1084/jem.165.1.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crotty S., Felgner P., Davies H., Glidewell J., Villarreal L., Ahmed R. Cutting edge: long-term B cell memory in humans after smallpox vaccination. J. Immunol. 2003;171:4969–4973. doi: 10.4049/jimmunol.171.10.4969. [DOI] [PubMed] [Google Scholar]
- Crotty S., Aubert R.D., Glidewell J., Ahmed R. Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods. 2004;286:111–122. doi: 10.1016/j.jim.2003.12.015. [DOI] [PubMed] [Google Scholar]
- de Lalla F., Rinaldi E., Santoro D., Pravettoni G. Immune response to hepatitis B vaccine given at different injection sites and by different routes: a controlled randomized study. Eur. J. Epidemiol. 1988;4:256–258. doi: 10.1007/BF00144763. [DOI] [PubMed] [Google Scholar]
- Deml L., Schirmbeck R., Reimann J., Wolf H., Wagner R. Recombinant human immunodeficiency Pr55gag viruslike particles presenting chimeric envelope glycoproteins induce cytotoxic T-cells and neutralizing antibodies. Virology. 1997;235:26–39. doi: 10.1006/viro.1997.8668. [DOI] [PubMed] [Google Scholar]
- Deml L., Speth C., Dierich M. P., Wolf H., Wagner R. Recombinant HIV-1 Pr55gag virus-like particles: potent stimulators of innate and acquired immune responses. Mol. Immunol. 2005;42:259–277. doi: 10.1016/j.molimm.2004.06.028. [DOI] [PubMed] [Google Scholar]
- den Dunnen, J., Gringhuis, S.I., and Geijtenbeek, T.B. (2008). Innate signaling by the C-type lectin DC-SIGN dictates immune responses. Cancer Immunol. Immunother. DOI 10.1007/s00262-008-0615-1. [DOI] [PMC free article] [PubMed]
- Deng L., Dai P., Parikh T., Cao H., Bhoj V., Sun Q., Chen Z., Merghoub T., Houghton A., Shuman S. Vaccinia virus subverts a mitochondrial antiviral signaling proteindependent innate immune response in keratinocytes through its double-stranded RNA binding protein, E3. J. Virol. 2008;82:10735–10746. doi: 10.1128/JVI.01305-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Diebold S.S. Recognition of viral single-stranded RNA by Toll-like receptors. Adv. Drug Deliv. Rev. 2008;60:813–823. doi: 10.1016/j.addr.2007.11.004. [DOI] [PubMed] [Google Scholar]
- Dubois B., Massacrier C., Caux C. Selective attraction of naive and memory B cells by dendritic cells. J. Leukoc. Biol. 2001;70:633–641. [PubMed] [Google Scholar]
- Fernandez-Sesma A., Marukian S., Ebersole B.J., Kaminski D., Park M.S., Yuen T., Sealfon S.C., Garcia-Sastre A., Moran T.M. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 2006;80:6295–6304. doi: 10.1128/JVI.02381-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Flehmig B., Staedele H., Xueref C., Vidor E., Zuckerman J., Zuckerman A. Early appearance of neutralizing antibodies after vaccination with an inactivated hepatitis A vaccine. J. Infect. 1997;35:37–40. doi: 10.1016/S0163-4453(97)90929-4. [DOI] [PubMed] [Google Scholar]
- Galarza J.M., Latham T., Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 2005;18:244–251. doi: 10.1089/vim.2005.18.244. [DOI] [PubMed] [Google Scholar]
- Gatto D., Pfister T., Jegerlehner A., Martin S.W., Kopf M., Bachmann M.F. Complement receptors regulate differentiation of bone marrow plasma cell precursors expressing transcription factors Blimp-1 and XBP-1. J. Exp. Med. 2005;201:993–1005. doi: 10.1084/jem.20042239. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gavin A.L., Hoebe K., Duong B., Ota T., Martin C., Beutler B., Nemazee D. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science. 2006;314:1936–1938. doi: 10.1126/science.1135299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Germain R.N. An innately interesting decade of research in immunology. Nat. Med. 2004;10:1307–1320. doi: 10.1038/nm1159. [DOI] [PubMed] [Google Scholar]
- Gewirtz A.T., Navas T.A., Lyons S., Godowski P.J., Madara J.L. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 2001;167:1882–1885. doi: 10.4049/jimmunol.167.4.1882. [DOI] [PubMed] [Google Scholar]
- Grgacic E.V., Anderson D.A. Virus-like particles: passport to immune recognition. Methods. 2006;40:60–65. doi: 10.1016/j.ymeth.2006.07.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gururajan M., Jacob J., Pulendran B. Toll-like receptor expression and responsiveness of distinct murine splenic and mucosal B-cell subsets. PLoS ONE. 2007;2:e863. doi: 10.1371/journal.pone.0000863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gustavsson S., Kinoshita T., Heyman B. Antibodies to murine complement receptor 1 and 2 can inhibit the antibody response in vivo without inhibiting T helper cell induction. J. Immunol. 1995;154:6524–6528. [PubMed] [Google Scholar]
- Hai R., Martinez-Sobrido L., Fraser K.A., Ayllon J., Garcia-Sastre A., Palese P. Influenza B virus NS1-truncated mutants: live-attenuated vaccine approach. J. Virol. 2008;82:10580–10590. doi: 10.1128/JVI.01213-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hebell T., Ahearn J.M., Fearon D.T. Suppression of the immune response by a soluble complement receptor of B lymphocytes. Science. 1991;254:102–105. doi: 10.1126/science.1718035. [DOI] [PubMed] [Google Scholar]
- Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740–745. doi: 10.1038/35047123. [DOI] [PubMed] [Google Scholar]
- Hoebe K., Janssen E., Beutler B. The interface between innate and adaptive immunity. Nat. Immunol. 2004;5:971–974. doi: 10.1038/ni1004-971. [DOI] [PubMed] [Google Scholar]
- Honorati M.C., Palareti A., Dolzani P., Busachi C.A., Rizzoli R., Facchini A. A mathematical model predicting antihepatitis B virus surface antigen (HBs) decay after vaccination against hepatitis B. Clin. Exp. Immunol. 1999;116:121–126. doi: 10.1046/j.1365-2249.1999.00866.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jegerlehner A., Maurer P., Bessa J., Hinton H.J., Kopf M., Bachmann M.F. TLR9 signaling in B cells determines class switch recombination to IgG2a. J. Immunol. 2007;178:2415–2420. doi: 10.4049/jimmunol.178.4.2415. [DOI] [PubMed] [Google Scholar]
- Kaech S.M., Wherry E.J., Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2002;2:251–262. doi: 10.1038/nri778. [DOI] [PubMed] [Google Scholar]
- Kalia V., Sarkar S., Gourley T.S., Rouse B.T., Ahmed R. Differentiation of memory B and T cells. Curr. Opin. Immunol. 2006;18:255–264. doi: 10.1016/j.coi.2006.03.020. [DOI] [PubMed] [Google Scholar]
- Kang S.M., Guo L., Yao Q., Skountzou I., Compans R.W. Intranasal immunization with inactivated influenza virus enhances immune responses to coadministered simian-human immunodeficiency virus-like particle antigens. J. Virol. 2004;78:9624–9632. doi: 10.1128/JVI.78.18.9624-9632.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawai T., Akira S. TLR signaling. Semin. Immunol. 2007;19:24–32. doi: 10.1016/j.smim.2006.12.004. [DOI] [PubMed] [Google Scholar]
- Kelsoe G. Studies of the humoral immune response. Immunol. Res. 2000;22:199–210. doi: 10.1385/IR:22:2-3:199. [DOI] [PubMed] [Google Scholar]
- Khanlou H., Sanchez S., Babaie M., Chien C., Hamwi G., Ricaurte J.C., Stein T., Bhatti L., Denouden P., Farthing C. The safety and efficacy of dose-sparing intradermal administration of influenza vaccine in human immunodeficiency virus-positive patients. Arch. Intern. Med. 2006;166:1417. doi: 10.1001/archinte.166.13.1417. [DOI] [PubMed] [Google Scholar]
- Klaus G.G., Pepys M.B., Kitajima K., Askonas B.A. Activation of mouse complement by different classes of mouse antibody. Immunology. 1979;38:687–695. [PMC free article] [PubMed] [Google Scholar]
- Kopf M., Abel B., Gallimore A., Carroll M., Bachmann M.F. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat. Med. 2002;8:373–378. doi: 10.1038/nm0402-373. [DOI] [PubMed] [Google Scholar]
- Koyama S., Ishii K.J., Kumar H., Tanimoto T., Coban C., Uematsu S., Kawai T., Akira S. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J. Immunol. 2007;179:4711–4720. doi: 10.4049/jimmunol.179.7.4711. [DOI] [PubMed] [Google Scholar]
- Kwissa M., Kasturi S.P., Pulendran B. The science of adjuvants. Expert Rev. Vaccines. 2007;6:673–684. doi: 10.1586/14760584.6.5.673. [DOI] [PubMed] [Google Scholar]
- Le Goffic R., Balloy V., Lagranderie M., Alexopoulou L., Escriou N., Flavell R., Chignard M., Si-Tahar M. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus- induced acute pneumonia. PLoS Pathog. 2006;2:e53. doi: 10.1371/journal.ppat.0020053. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee H.K., Dunzendorfer S., Soldau K., Tobias P.S. Double-stranded RNA-mediated TLR3 activation is enhanced by CD14. Immunity. 2006;24:153–163. doi: 10.1016/j.immuni.2005.12.012. [DOI] [PubMed] [Google Scholar]
- Li Z., Jiang Y., Jiao P., Wang A., Zhao F., Tian G., Wang X., Yu K., Bu Z., Chen H. The NS1 gene contributes to the virulence of H5N1 avian influenza viruses. J. Virol. 2006;80:11115–11123. doi: 10.1128/JVI.00993-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin L., Gerth A.J., Peng S.L. CpG DNA redirects class-switching towards “Th1-like” Ig isotype production via TLR9 and MyD88. Eur. J. Immunol. 2004;34:1483–1487. doi: 10.1002/eji.200324736. [DOI] [PubMed] [Google Scholar]
- Liu N., Ohnishi N., Ni L., Akira S., Bacon K.B. CpG directly induces T-bet expression and inhibits IgG1 and IgE switching in B cells. Nat. Immunol. 2003;4:687–693. doi: 10.1038/ni941. [DOI] [PubMed] [Google Scholar]
- Lobue A.D., Lindesmith L., Yount B., Harrington P.R., Thompson J.M., Johnston R.E., Moe C.L., Baric R.S. Multivalent norovirus vaccines induce strong mucosal and systemic blocking antibodies against multiple strains. Vaccine. 2006;24:5220–5234. doi: 10.1016/j.vaccine.2006.03.080. [DOI] [PubMed] [Google Scholar]
- Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., Garcia-Sastre A., Katze M.G., et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 2008;82:335–345. doi: 10.1128/JVI.01080-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mansson A., Adner M., Hockerfelt U., Cardell L.O. A distinct Toll-like receptor repertoire in human tonsillar B cells, directly activated by PamCSK, R-837 and CpG-2006 stimulation. Immunology. 2006;118:539–548. doi: 10.1111/j.1365-2567.2006.02392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Manz R.A., Hauser A.E., Hiepe F., Radbruch A. Maintenance of serum antibody levels. Annu. Rev. Immunol. 2005;23:367–386. doi: 10.1146/annurev.immunol.23.021704.115723. [DOI] [PubMed] [Google Scholar]
- Markine-Goriaynoff D., van der Logt J.T., Truyens C., Nguyen T.D., Heessen F.W., Bigaignon G., Carlier Y., Coutelier J.P. IFN-gamma-independent IgG2a production in mice infected with viruses and parasites. Int. Immunol. 2000;12:223–230. doi: 10.1093/intimm/12.2.223. [DOI] [PubMed] [Google Scholar]
- Martin M., Michalek S.M., Katz J. Role of innate immune factors in the adjuvant activity of monophosphoryl lipid A. Infect. Immun. 2003;71:2498–2507. doi: 10.1128/IAI.71.5.2498-2507.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McHeyzer-Williams L.J., McHeyzer-Williams M.G. Antigen-specific memory B cell development. Annu. Rev. Immunol. 2005;23:487–513. doi: 10.1146/annurev.immunol.23.021704.115732. [DOI] [PubMed] [Google Scholar]
- Meyer-Bahlburg A., Khim S., Rawlings D.J. B cell intrinsic TLR signals amplify but are not required for humoral immunity. J. Exp. Med. 2007;204:3095–3101. doi: 10.1084/jem.20071250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Minges Wols H.A., Underhill G.H., Kansas G.S., Witte P.L. The role of bone marrow-derived stromal cells in the maintenance of plasma cell longevity. J. Immunol. 2002;169:4213–4221. doi: 10.4049/jimmunol.169.8.4213. [DOI] [PubMed] [Google Scholar]
- Mortola E., Roy P. Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett. 2004;576:174–178. doi: 10.1016/j.febslet.2004.09.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nemazee D., Gavin A., Hoebe K., Beutler B. Immunology: Toll-like receptors and antibody responses. Nature. 2006;441:E4. doi: 10.1038/nature04875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nimmerjahn F., Ravetch J.V. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science. 2005;310:1510–1512. doi: 10.1126/science.1118948. [DOI] [PubMed] [Google Scholar]
- Ochsenbein A.F., Pinschewer D.D., Odermatt B., Carroll M.C., Hengartner H., Zinkernagel R.M. Protective T cellindependent antiviral antibody responses are dependent on complement. J. Exp. Med. 1999;190:1165–1174. doi: 10.1084/jem.190.8.1165. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Palese P., Muster T., Zheng H., O’Neill R., Garcia-Sastre A. Learning from our foes: a novel vaccine concept for influenza virus. Arch. Virol. Suppl. 1999;15:131–138. doi: 10.1007/978-3-7091-6425-9_9. [DOI] [PubMed] [Google Scholar]
- Palucka A.K., Laupeze B., Aspord C., Saito H., Jego G., Fay J., Paczesny S., Pascual V., Banchereau J. Immunotherapy via dendritic cells. Adv. Exp. Med. Biol. 2005;560:105–114. doi: 10.1007/0-387-24180-9_14. [DOI] [PubMed] [Google Scholar]
- Pasare C., Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Microbes Infect. 2004;6:1382–1387. doi: 10.1016/j.micinf.2004.08.018. [DOI] [PubMed] [Google Scholar]
- Pasare C., Medzhitov R. Control of B-cell responses by Toll-like receptors. Nature. 2005;438:364–368. doi: 10.1038/nature04267. [DOI] [PubMed] [Google Scholar]
- Pashine A., Valiante N.M., Ulmer J.B. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med. 2005;11:S63–68. doi: 10.1038/nm1210. [DOI] [PubMed] [Google Scholar]
- Persing D.H., Coler R.N., Lacy M.J., Johnson D.A., Baldridge J.R., Hershberg R.M., Reed S.G. Taking toll: lipid A mimetics as adjuvants and immunomodulators. Trends Microbiol. 2002;10:S32–7. doi: 10.1016/S0966-842X(02)02426-5. [DOI] [PubMed] [Google Scholar]
- Pichichero M.E., Voloshen T., Passador S. Kinetics of booster responses to Haemophilus influenzae type B conjugate after combined diphtheria-tetanus-acelluar pertussis-Haemophilus influenzae type b vaccination in infants. Pediatr. Infect. Dis. J. 1999;18:1106–1108. doi: 10.1097/00006454-199912000-00019. [DOI] [PubMed] [Google Scholar]
- Plotkin S.A. Vaccines: past, present and future. Nat. Med. 2005;11:S5–11. doi: 10.1038/nm1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pulendran B. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol. Rev. 2004;199:227–250. doi: 10.1111/j.0105-2896.2004.00144.x. [DOI] [PubMed] [Google Scholar]
- Pulendran B., Ahmed R. Translating innate immunity into immunological memory: implications for vaccine development. Cell. 2006;124:849–863. doi: 10.1016/j.cell.2006.02.019. [DOI] [PubMed] [Google Scholar]
- Pushko P., Tumpey T.M., Bu F., Knell J., Robinson R., Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine. 2005;23:5751–5759. doi: 10.1016/j.vaccine.2005.07.098. [DOI] [PubMed] [Google Scholar]
- Quan F.S., Huang C., Compans R.W., Kang S.M. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol. 2007;81:3514–3524. doi: 10.1128/JVI.02052-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quan F.S., Sailaja G., Skountzou I., Huang C., Vzorov A., Compans R.W., Kang S.M. Immunogenicity of viruslike particles containing modified human immunodeficiency virus envelope proteins. Vaccine. 2007;25:3841–3850. doi: 10.1016/j.vaccine.2007.01.107. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quan F.S., Compans R.W., Nguyen H.H., Kang S.M. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol. 2008;82:1350–1359. doi: 10.1128/JVI.01615-07. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quan F.S., Steinhauer D., Huang C., Ross T.M., Compans R.W., Kang S.M. A bivalent influenza VLP vaccine confers complete inhibition of virus replication in lungs. Vaccine. 2008;26:3352–3361. doi: 10.1016/j.vaccine.2008.03.055. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Querec T., Bennouna S., Alkan S., Laouar Y., Gorden K., Flavell R., Akira S., Ahmed R., Pulendran B. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J. Exp. Med. 2006;203:413–424. doi: 10.1084/jem.20051720. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rappuoli R. From Pasteur to genomics: progress and challenges in infectious diseases. Nat. Med. 2004;10:1177–1185. doi: 10.1038/nm1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rappuoli R. Bridging the knowledge gaps in vaccine design. Nat. Biotechnol. 2007;25:1361–1366. doi: 10.1038/nbt1207-1361. [DOI] [PubMed] [Google Scholar]
- Reif K., Ekland E.H., Ohl L., Nakano H., Lipp M., Forster R., Cyster J.G. Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position. Nature. 2002;416:94–99. doi: 10.1038/416094a. [DOI] [PubMed] [Google Scholar]
- Ridderstad A., Tarlinton D.M. Kinetics of establishing the memory B cell population as revealed by CD38 expression. J. Immunol. 1998;160:4688–4695. [PubMed] [Google Scholar]
- Sailaja G., Skountzou I., Quan F.S., Compans R.W., Kang S.M. Human immunodeficiency virus-like particles activate multiple types of immune cells. Virology. 2007;362:331–341. doi: 10.1016/j.virol.2006.12.014. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sancho D., Gomez M., Sanchez-Madrid F. CD69 is an immunoregulatory molecule induced following activation. Trends Immunol. 2005;26:136–140. doi: 10.1016/j.it.2004.12.006. [DOI] [PubMed] [Google Scholar]
- Schnare M., Barton G.M., Holt A.C., Takeda K., Akira S., Medzhitov R. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2001;2:947–950. doi: 10.1038/ni712. [DOI] [PubMed] [Google Scholar]
- Shapiro-Shelef M., Calame K. Regulation of plasmacell development. Nat. Rev. Immunol. 2005;5:230–242. doi: 10.1038/nri1572. [DOI] [PubMed] [Google Scholar]
- Shin D., Yang C.S., Lee J.Y., Lee S.J., Choi H.H., Lee H.M., Yuk J.M., Harding C.V., Jo E.K. Mycobacterium tuberculosis lipoprotein-induced association of TLR2 with protein kinase C zeta in lipid rafts contributes to reactive oxygen species-dependent inflammatory signalling in macrophages. Cell Microbiol. 2008;10:1893–1905. doi: 10.1111/j.1462-5822.2008.01179.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shinall S.M., Gonzalez-Fernandez M., Noelle R.J., Waldschmidt T.J. Identification of murine germinal center B cell subsets defined by the expression of surface isotypes and differentiation antigens. J. Immunol. 2000;164:5729–5738. doi: 10.4049/jimmunol.164.11.5729. [DOI] [PubMed] [Google Scholar]
- Sun Y., Carrion R., Jr., Ye L., Wen Z., Ro Y.T., Brasky K., Ticer A.E., Schwegler E.E., Patterson J.L., Compans R.W., et al. Protection against lethal challenge by Ebola virus-like particles produced in insect cells. Virology. 2009;538:12–21. doi: 10.1016/j.virol.2008.09.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeda K., Akira S. TLR signaling pathways. Semin. Immunol. 2004;16:3–9. doi: 10.1016/j.smim.2003.10.003. [DOI] [PubMed] [Google Scholar]
- Takeshita F., Kobiyama K., Miyawaki A., Jounai N., Okuda K. The non-canonical role of Atg family members as suppressors of innate antiviral immune signaling. Autophagy. 2008;4:67–69. doi: 10.4161/auto.5055. [DOI] [PubMed] [Google Scholar]
- Talon J., Salvatore M., O’Neill R. E., Nakaya Y., Zheng H., Muster T., Garcia-Sastre A., Palese P. Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach. Proc. Natl. Acad. Sci. USA. 2000;97:4309–4314. doi: 10.1073/pnas.070525997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tiberio L., Fletcher L., Eldridge J.H., Duncan D.D. Host factors impacting the innate response in humans to the candidate adjuvants RC529 and monophosphoryl lipid A. Vaccine. 2004;22:1515–1523. doi: 10.1016/j.vaccine.2003.10.019. [DOI] [PubMed] [Google Scholar]
- Unterholzner L., Bowie A.G. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem. Pharmacol. 2008;75:589–602. doi: 10.1016/j.bcp.2007.07.043. [DOI] [PubMed] [Google Scholar]
- Van Damme P., Oosterhuis-Kafeja F., Van der Wielen M., Almagor Y., Sharon O., Levin Y. Safety and efficacy of a novel microneedle device for dose sparing intradermal influenza vaccination in healthy adults. Vaccine. 2009;27:454–459. doi: 10.1016/j.vaccine.2008.10.077. [DOI] [PubMed] [Google Scholar]
- van der Sluijs K.F., van Elden L., Nijhuis M., Schuurman R., Florquin S., Jansen H.M., Lutter R., van der Poll T. Toll-like receptor 4 is not involved in host defense against respiratory tract infection with Sendai virus. Immunol. Lett. 2003;89:201–206. doi: 10.1016/S0165-2478(03)00138-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van Duin D., Medzhitov R., Shaw A.C. Triggering TLR signaling in vaccination. Trends Immunol. 2006;27:49–55. doi: 10.1016/j.it.2005.11.005. [DOI] [PubMed] [Google Scholar]
- Van Herck K., Beutels P., Van Damme P., Beutels M., Van den Dries J., Briantais P., Vidor E. Mathematical models for assessment of long-term persistence of antibodies after vaccination with two inactivated hepatitis A vaccines. J. Med. Virol. 2000;60:1–7. doi: 10.1002/(SICI)1096-9071(200001)60:1<1::AID-JMV1>3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
- Vinuesa C.G., Tangye S.G., Moser B., Mackay C.R. Follicular B helper T cells in antibody responses and autoimmunity. Nat. Rev. Immunol. 2005;5:853–865. doi: 10.1038/nri1714. [DOI] [PubMed] [Google Scholar]
- Warfield K.L., Swenson D.L., Demmin G., Bavari S. Filovirus-like particles as vaccines and discovery tools. Expert Rev. Vaccines. 2005;4:429–440. doi: 10.1586/14760584.4.3.429. [DOI] [PubMed] [Google Scholar]