Innate endogenous adjuvants prime to desirable immune responses via mucosal routes
Xiaoguang Wang, Delong Meng
Innate endogenous adjuvants prime to desirable immune responses via mucosal routes
Vaccination is an effective strategy to prevent infectious or immune related diseases, which has made remarkable contribution in human history. Recently increasing attentions have been paid to mucosal vaccination due to its multiple advantages over conventional ways. Subunit or peptide antigens are more reasonable immunogens for mucosal vaccination than live or attenuated pathogens, however adjuvants are required to augment the immune responses. Many mucosal adjuvants have been developed to prime desirable immune responses to different etiologies. Compared with pathogen derived adjuvants, innate endogenous molecules incorporated into mucosal vaccines demonstrate prominent adjuvanticity and safety. Nowadays, cytokines are broadly used as mucosal adjuvants for participation of signal transduction of immune responses, activation of innate immunity and polarization of adaptive immunity. Desired immune responses are promptly and efficaciously primed on basis of specific interactions between cytokines and corresponding receptors. In addition, some other innate molecules are also identified as potent mucosal adjuvants. This review focuses on innate endogenous mucosal adjuvants, hoping to shed light on the development of mucosal vaccines.
mucosal vaccine / adjuvant / innate endogenous molecules
[1] |
Abraham E, Shah S (1992) Intranasal immunization with liposomes containing IL-2 enhances bacterial polysaccharide antigen-speciflc pulmonary secretory antibody-response. J Immunol149: 3719-3726
|
[2] |
Arulanandam BP, Metzger DW (1999) Modulation of mucosal and systemic immunity by intranasal interleukin 12 delivery. Vaccine17: 252-260
CrossRef
Google scholar
|
[3] |
Arulanandam BP, O’Toole M, Metzger DW (1999) Intranasal interleukin-12 is a powerful adjuvant for protective mucosal immunity. J Infect Dis180: 940-949
CrossRef
Google scholar
|
[4] |
Arulanandam BP, Lynch JM, Briles DE, Hollingshead S, Metzger DW (2001) Intranasal vaccination with pneumococcal surface protein A and interleukin-12 augments antibody-mediated opsonization and protective immunity against Streptococcus pneumoniae infection. Infect Immun69: 6718-6724
CrossRef
Google scholar
|
[5] |
Baca-Estrada ME, Foldvari M, Snider M (1999) Induction of mucosal immune responses by administration of liposomeantigen formulations and interleukin-12. J Interferon Cytokine Res19: 455-462
CrossRef
Google scholar
|
[6] |
Baggiolini M, Dahinden CA (1994) CC chemokines in allergic inflammation. Immunol Today15: 127-133
CrossRef
Google scholar
|
[7] |
Baqar S, Pacheco ND, Rollwagen FM (1993) Modulation of mucosal immunity against Campylobacter jejuni by orally-administered cytokines. Antimicrob Agents Chemother37: 2688-2692
CrossRef
Google scholar
|
[8] |
Baron SD, Singh R, Metzger DW (2007) Inactivated Francisella tularensis live vaccine strain protects against respiratory tularemia by intranasal vaccination in an immunoglobulin A-dependent fashion. Infect Immun75: 2152-2162
CrossRef
Google scholar
|
[9] |
Batten M, Groom J, Cachero TG, Qian F, Schneider P, Tschopp J, Browning JL, Mackay F (2000) BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med192: 1453-1465
CrossRef
Google scholar
|
[10] |
Beilharz MW, Cummins MJ, Bennett AL, Cummins JM (2010) Oromucosal administration of interferon to humans. Pharmaceuticals3: 323-344
CrossRef
Google scholar
|
[11] |
Bermudez-Humaran LG, Cortes-Perez NG, Lefevre F, Guimaraes V, Rabot S, Alcocer-Gonzalez JM, Gratadoux JJ, Rodriguez-Padilla C, Tamez-Guerra RS, Corthier G
CrossRef
Google scholar
|
[12] |
Bertley FMN, Kozlowski PA, Wang SW, Chappelle J, Patel J, Sonuyi O, Mazzara G, Monteflori D, Carville A, Mansfleld KG
CrossRef
Google scholar
|
[13] |
Boyaka PN, Marinaro M, Jackson RJ, Menon S, Kiyono H, Jirillo E, McGhee JR (1999) IL-12 is an effective adjuvant for induction of mucosal immunity. J Immunol162: 122-128
|
[14] |
Braat H, Rottiers P, Hommes DW, Huyghebaert N, Remaut E, Remon JP, Van Deventer SJH, Neirynck S, Peppelenbosch MP, Steidler L (2006) A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin Gastroenterol Hepatol4: 754-759
CrossRef
Google scholar
|
[15] |
Bracci L, Canini I, Puzelli S, Sestili P, Venditti M, Spada M, Donatelli I, Belardelli F, Proietti E (2005) Type I IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine23: 2994-3004
CrossRef
Google scholar
|
[16] |
Bracci L, Canini I, Venditti M, Spada M, Puzelli S, Donatelli I, Belardelli F, Proietti E (2006) Type I IFN as a vaccine adjuvant for both systemic and mucosal vaccination against influenza virus. Vaccine24: S56-S57
CrossRef
Google scholar
|
[17] |
Bracci L, La Sorsa V, Belardelli F, Proietti E (2008) Type I interferons as vaccine adjuvants against infectious diseases and cancer. Expert Rev Vaccines7: 373-381
CrossRef
Google scholar
|
[18] |
Braciak TA, Gallichan WS, Graham FL, Richards CD, Ramsay AJ, Rosenthal KL, Gauldie J (2000) Recombinant adenovirus vectors expressing interleukin-5 and-6 speciflcally enhance mucosal immunoglobulin A responses in the lung. Immunology101: 388-396
CrossRef
Google scholar
|
[19] |
Bradney CP, Sempowski GD, Liao HX, Haynes BF, Staats HF (2002) Cytokines as adjuvants for the induction of anti-human immunodeflciency virus peptide immunoglobulin G (IgG) and IgA antibodies in serum and mucosal secretions after nasal immunization. J Virol76: 517-524
CrossRef
Google scholar
|
[20] |
Brogden KA, Heidari M, Sacco RE, Palmquist D, Guthmiller JM, Johnson GK, Jia HP, Tack BF, McCray PB (2003) Defensininduced adaptive immunity in mice and its potential in preventing periodontal disease. Oral Microbiol Immunol18: 95-99
CrossRef
Google scholar
|
[21] |
Bukreyev A, Belyakov IM, Berzofsky JA, Murphy BR, Collins PL (2001) Granulocyte-macrophage colony-stimulating factor expressed by recombinant respiratory syncytial virus attenuates viral replication and increases the level of pulmonary antigenpresenting cells. J Virol75: 12128-12140
CrossRef
Google scholar
|
[22] |
Cao M, Sasaki O, Yamada A, Imanishi J (1992) Enhancement of the protective effect of inactivated influenza virus vaccine by cytokines. Vaccine10: 238-242
CrossRef
Google scholar
|
[23] |
Chodaczek G, Zimecki M, Lukasiewicz J, Lugowski C (2006) A complex of lactoferrin with monophosphoryl lipid A is an efflcient adjuvant of the humoral and cellular immune response in mice. Med Microbiol Immunol195: 207-216
CrossRef
Google scholar
|
[24] |
Chun S, Daheshia M, Lee S, Eo SK, Rouse BT (1999) Distribution fate and mechanism of immune modulation following mucosal delivery of plasmid DNA encoding IL-10. J Immunol163: 2393-2402
|
[25] |
Couch RB, Atmar RL, Cate TR, Quarles JM, Keitel WA, Arden NH, Wells J, Nino D, Wyde PR (2009) Contrasting effects of type I interferon as a mucosal adjuvant for influenza vaccine in mice and humans. Vaccine27: 5344-5348
CrossRef
Google scholar
|
[26] |
Cox E, Verdonck F, Vanrompay D, Goddeeris B (2006) Adjuvants modulating mucosal immune responses or directing systemic responses towards the mucosa. Vet Res37: 511-539
CrossRef
Google scholar
|
[27] |
De Magistnis MT (2006) Mucosal delivery of vaccine antigens and its advantages in pediatrics. Adv Drug Deliv Rev58: 52-67
CrossRef
Google scholar
|
[28] |
Degre M, Bukholm G (1995) Orally administered interferon-gamma but not tumor necrosis factor-alpha suppress infection with Salmonella typhimurium in a mouse model. J Biol Regul Homeost Agents9: 15-20
|
[29] |
Dinarello CA (2000) Proinflammatory cytokines. Chest118: 503-508
CrossRef
Google scholar
|
[30] |
Drexler HG, Quentmeier H (2004) FLT3: receptor and ligand. Growth Factors22: 71-73
CrossRef
Google scholar
|
[31] |
Egan MA, Chong SY, Hagen M, Megati S, Schadeck EB, Piacente P, Ma BJ, Monteflori DC, Haynes BF, Israel ZR
CrossRef
Google scholar
|
[32] |
Eo SK, Lee S, Chun S, Rouse BT (2001a) Modulation of immunity against herpes simplex virus infection via mucosal genetic transfer of plasmid DNA encoding chemokines. J Virol75: 569-578
CrossRef
Google scholar
|
[33] |
Eo SK, Lee S, Kumaraguru U, Rouse BT (2001b) Immunopotentiation of DNA vaccine against herpes simplex virus via co-delivery of plasmid DNA expressing CCR7 ligands. Vaccine19: 4685-4693
CrossRef
Google scholar
|
[34] |
Ferko B, Kittel C, Romanova J, Sereinig S, Katinger H, Egorov A (2006) Live attenuated influenza virus expressing human interleukin-2 reveals increased immunogenic potential in young and aged hosts. J Virol80: 11621-11627
CrossRef
Google scholar
|
[35] |
Fukuiwa T, Sekine S, Kobayashi R, Suzuki H, Kataoka K, Gilbert RS, Kurono Y, Boyaka PN, Krieg AM, McGhee JR
CrossRef
Google scholar
|
[36] |
Giudice EL, Campbell JD (2006) Needle-free vaccine delivery. Adv Drug Deliv Rev58: 68-89
CrossRef
Google scholar
|
[37] |
Griffln KF, Eyles JE, Spiers ID, Alpar HO, Williamson ED (2002) Protection against plague following immunisation with microencapsulated V antigen is reduced by co-encapsulation with IFNgamma or IL-4, but not IL-6. Vaccine20: 3650-3657
CrossRef
Google scholar
|
[38] |
Gwinn WM, Kirwan SM, Wang SH, Ashcraft KA, Sparks NL, Doil CR, Tlusty TG, Casey LS, Hollingshead SK, Briles DE
CrossRef
Google scholar
|
[39] |
Hanazawa T, Antuni JD, Kharitonov SA, Barnes PJ (2000) Intranasal administration of eotaxin increases nasal eosinophils and nitric oxide in patients with allergic rhinitis. J Allergy Clin Immunol105: 58-64
CrossRef
Google scholar
|
[40] |
Hinc K, Stasilojc M, Piatek I, Peszynska-Sularz G, Isticato R, Ricca E, Obuchowski M, Iwanicki A (2014) Mucosal adjuvant activity of IL-2 presenting spores of Bacillus subtilis in a murine model of Helicobacter pylori vaccination. Plos One9: e95187
CrossRef
Google scholar
|
[41] |
Holmgren J, Czerkinsky C (2005) Mucosal immunity and vaccines. Nat Med11: S45-S53
CrossRef
Google scholar
|
[42] |
Holmgren J, Czerkinsky C, Eriksson K, Mharandi A (2003) Mucosal immunisation and adjuvants: a brief overview of recent advances and challenges. Vaccine21: S89-S95
CrossRef
Google scholar
|
[43] |
Hu K, Luo S, Tong L, Huang X, Jin W, Huang W, Du T, Yan Y, He S, Griffln GE
CrossRef
Google scholar
|
[44] |
Huber VC, Arulanandam BP, Arnaboldi PM, Elmore MK, Sheehan CE, Kallakury BV, Metzger DW (2003) Delivery of IL-12 intranasally leads to reduced IL-12-mediated toxicity. Int Immunopharmacol3: 801-809
CrossRef
Google scholar
|
[45] |
Inoue T, Inoue Y, Nakamura T, Yoshida A, Inoue Y, Tano Y, Shimomura Y, Fujisawa Y, Aono A, Hayashi K (2002) The effect of immunization with herpes simplex virus glycoprotein D fused with interleukin-2 against murine herpetic keratitis. Jpn J Ophthalmol46: 370-376
CrossRef
Google scholar
|
[46] |
Jang YS, Kim SH, Lee HY, Lee H, Kim J, Kim DH, Lee KY (2013) The cathelicidin LL-37 exerts its mucosal adjuvant activity via enhancing germinal center formation and dendritic cell maturation. J Immunol190: 124
|
[47] |
Kalled SL (2006) Impact of the BAFF/BR3 axis on B cell survival, germinal center maintenance and antibody production. Semin Immunol18: 290-296
CrossRef
Google scholar
|
[48] |
Kataoka K, McGhee JR, Kobayashi R, Fujihashi K, Shizukuishi S, Fujihashi K (2004) Nasal Flt3 ligand cDNA elicits CD11c(+)CD8 (+) dendritic cells for enhanced mucosal immunity. J Immunol172: 3612-3619
CrossRef
Google scholar
|
[49] |
Kataoka K, Fujihashi K, Oma K, Fukuyama Y, Hollingshead SK, Sekine S, Kawabata S, Ito HO, Briles DE, Oishi K (2011) The nasal dendritic cell-targeting Flt3 ligand as a safe adjuvant elicits effective protection against fatal pneumococcal pneumonia. Infect Immun79: 2819-2828
CrossRef
Google scholar
|
[50] |
Kaul D, Ogra PL (1998) Mucosal responses to parenteral and mucosal vaccines. Dev Biol Stand95: 141-146
|
[51] |
Kayamuro H, Abe Y, Yoshioka Y, Katayama K, Nomura T, Yoshida T, Yamashita K, Yoshikawa T, Kawai Y, Mayumi T
CrossRef
Google scholar
|
[52] |
Kayamuro H, Yoshioka Y, Abe Y, Katayama K, Yoshida T, Yamashita K, Yoshikawa T, Hiroi T, Itoh N, Kawai Y
CrossRef
Google scholar
|
[53] |
Kayamuro H, Abe Y, Yoshioka Y, Katayama K, Yoshida T, Yamashita K, Yoshikawa T, Kawai Y, Mayumi T, Hiroi T
|
[54] |
Kayamuro H, Yoshioka Y, Abe Y, Arita S, Katayama K, Nomura T, Yoshikawa T, Kubota-Koketsu R, Ikuta K, Okamoto S
CrossRef
Google scholar
|
[55] |
Kayamuro H, Yoshioka Y, Abe Y, Katayama K, Arita S, Nomura T, Yoshikawa T, Itoh N, Kamada H, Tsunoda S
CrossRef
Google scholar
|
[56] |
Kim HD, Cao YP, Kong FK, Van Kampen KR, Lewis TL, Ma ZD, Tang DCC, Fukuchi KI (2005) Induction of a Th2 immune response by co-administration of recombinant adenovirus vectors encoding amyloid beta-protein and GM-CSF. Vaccine23: 2977-2986
CrossRef
Google scholar
|
[57] |
Kodama S, Hirano T, Noda K, Abe N, Suzuki M (2010) A single nasal dose of fms-like tyrosine kinase receptor-3 ligand, but not peritoneal application, enhances nontypeable Haemophilus influenzae-speciflc long-term mucosal immune responses in the nasopharynx. Vaccine28: 2510-2516
CrossRef
Google scholar
|
[58] |
Kodama S, Abe N, Hirano T, Suzuki M (2011) A single nasal dose of CCL20 chemokine induces dendritic cell recruitment and enhances nontypable Haemophilus influenzae-speciflc immune responses in the nasal mucosa. Acta Otolaryngol131: 989-996
CrossRef
Google scholar
|
[59] |
Kokuryo S, Inoue H, Fukuizumi T, Tsujisawa T, Tominaga K, Fukuda J (2002) Evaluation of interleukin 1 as a mucosal adjuvant in immunization with Streptococcus sobrinus cells by tonsillar application in rabbits. Oral Microbiol Immunol 17: 163-171
CrossRef
Google scholar
|
[60] |
Kruzel ML, Zimecki M (2002) Lactoferrin and immunologic dissonance: Clinical implications. Arch Immunol Ther Exp50: 399-410
|
[61] |
Lee S, Gierynska M, Eo SK, Kuklin N, Rouse BT (2003) Influence of DNA encoding cytokines on systemic and mucosal immunity following genetic vaccination against herpes simplex virus. Microbes Infect5: 571-578
CrossRef
Google scholar
|
[62] |
Levine MM (2003) Can needle-free administration of vaccines become the norm in global immunization? Nat Med9: 99-103
CrossRef
Google scholar
|
[63] |
Lillard JW, Boyaka PN, Chertov O, Oppenheim JJ, McGhee JR (1999a) Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc Natl Acad Sci USA96: 651-656
CrossRef
Google scholar
|
[64] |
Lillard JW, Boyaka PN, Hedrick JA, Zlotnik A, McGhee JR (1999b) Lymphotactin acts as an innate mucosal adjuvant. J Immunol162: 1959-1965
|
[65] |
Lillard JW, Boyaka PN, Taub DD, McGhee JR (2001) RANTES potentiates antigen-speciflc mucosal immune responses. J Immunol166: 162-169
CrossRef
Google scholar
|
[66] |
Lillard JW Jr, Singh UP, Boyaka PN, Singh S, Taub DD, McGhee JR (2003) MIP-1alpha and MIP-1beta differentially mediate mucosal and systemic adaptive immunity. Blood101: 807-814
CrossRef
Google scholar
|
[67] |
Lu Y, Xin KQ, Hamajima K, Tsuji T, Aoki I, Yang J, Sasaki S, Fukushima J, Yoshimura T, Toda S
CrossRef
Google scholar
|
[68] |
Lynch JM, Briles DE, Metzger DW (2003) Increased protection against pneumococcal disease by mucosal administration of conjugate vaccine plus interleukin-12. Infect Immun71: 4780-4788
CrossRef
Google scholar
|
[69] |
Manrique M, Kozlowski PA, Cobo-Molinos A, Wang SW, Wilson RL, Monteflori DC, Mansfleld KG, Carville A, Aldovini A(2011) Long-term control of simian immunodeflciency virus (mac251) viremia to undetectable levels in half of infected female rhesus macaques nasally vaccinated with simian immunodeflciency virus DNA/ recombinant modifled vaccinia virus ankara. J Immunol186: 3581-3593
CrossRef
Google scholar
|
[70] |
Marinaro M, Boyaka PN, Jackson RJ, Finkelman FD, Kiyono H, Jirillo E, McGhee JR (1999) Use of intranasal IL-12 to target predominantly Th1 responses to nasal and Th2 responses to oral vaccines given with cholera toxin. J Immunol162: 114-121
|
[71] |
McBride S, Hoebe K, Georgel P, Janssen E (2006) Cell-associated double-stranded RNA enhances antitumor activity through the production of type IIFN. J Immunol177: 6122-6128
CrossRef
Google scholar
|
[72] |
Mcghee JR, Mestecky J, Dertzbaugh MT, Eldridge JH, Hirasawa M, Kiyono H (1992) The mucosal immune system from fundamental concepts to vaccine development. Vaccine10: 75-88
CrossRef
Google scholar
|
[73] |
McNeela EA, Mills KHG (2001) Manipulating the immune system: humoral versus cell-mediated immunity. Adv Drug Deliver Rev51: 43-54
CrossRef
Google scholar
|
[74] |
Meritet JF, Maury C, Tovey MG (2001) Effect of oromucosal administration of IFN-alpha on allergic sensitization and the hypersensitive inflammatory response in animals sensitized to ragweed pollen. J Interferon Cytokine Res21: 583-593
CrossRef
Google scholar
|
[75] |
Mutsch M, Zhou WG, Rhodes P, Bopp M, Chen RT, Linder T, Spyr C, Steffen R (2004) Use of the inactivated intranasal influenza vaccine and the risk of Bell’s palsy in Switzerland. New Engl J Med350: 896-903
CrossRef
Google scholar
|
[76] |
Namangala B, Inoue N, Kohara J, Kuboki N, Sakurai T, Hayashida K, Sugimoto C (2006) Evidence for the immunostimulatory effects of low-dose orally delivered human IFN-alpha in cattle. J Interferon Cytokine Res26: 675-681
CrossRef
Google scholar
|
[77] |
Nambiar JK, Ryan AA, Kong CU, Britton WJ, Triccas JA (2010) Modulation of pulmonary DC function by vaccine-encoded GMCSF enhances protective immunity against Mycobacterium tuberculosis infection. Eur J Immunol40: 153-161
CrossRef
Google scholar
|
[78] |
Niethammer AG, Xiang R, Ruehlmann JM, Lode HN, Dolman CS, Gillies SD, Reisfeld RA (2001) Targeted interleukin 2 therapy enhances protective immunity induced by an autologous oral DNA vaccine against murine melanoma. Cancer Res 61: 6178-6184
|
[79] |
Oh YK, Park JS, Yoon H, Kim CK (2003) Enhanced mucosal and systemic immune responses to a vaginal vaccine coadministered with RANTES-expressing plasmid DNA using in situ-gelling mucoadhesive delivery system. Vaccine21: 1980-1988
CrossRef
Google scholar
|
[80] |
O’Hagan DT, Rappuoli R (2004) Novel approaches to vaccine delivery. Pharm Res21: 1519-1530
CrossRef
Google scholar
|
[81] |
Okada E, Sasaki S, Ishii N, Aoki I, Yasuda T, Nishioka K, Fukushima J, Miyazaki J, Wahren B, Okuda K (1997) Intranasal immunization of a DNA vaccine with IL-12- and granulocyte-macrophage colony-stimulating factor (GM-CSF)-expressing plasmids in liposomes induces strong mucosal and cell-mediated immune responses against HIV-1 antigens. J Immunol159: 3638-3647
|
[82] |
Pabst R, Luhrmann A, Steinmetz I, Tschernig T (2003) A single intratracheal dose of the growth factor Fms-like tyrosine kinase receptor-3 ligand induces a rapid differential increase of dendritic cells and lymphocyte subsets in lung tissue and bronchoalveolar lavage, resulting in an increased local antibody production. J Immunol171: 325-330
CrossRef
Google scholar
|
[83] |
Parker JN, Pflster LA, Quenelle D, Gillespie GY, Markert JM, Kern ER, Whitley RJ (2006) Genetically engineered herpes simplex viruses that express IL-12 or GM-CSF as vaccine candidates. Vaccine24: 1644-1652
CrossRef
Google scholar
|
[84] |
Pockley AG, Montgomery PC (1991) In vivo adjuvant effect of interleukins 5 and 6 on rat tear IgA antibody responses. Immunology73: 19-23
|
[85] |
Proietti E, Bracci L, Puzelli S, Di Pucchio T, Sestili P, De Vincenzi E, Venditti M, Capone I, Seif I, De Maeyer E
CrossRef
Google scholar
|
[86] |
Ramsay AJ, Kohonencorish M (1993) Interleukin-5 expressed by a recombinant virus vector enhances speciflc mucosal IgA responses in vivo. Eur J Immunol23: 3141-3145
CrossRef
Google scholar
|
[87] |
Ramsburg E, Publicover J, Buonocore L, Poholek A, Robek M, Palin A, Rose JK (2005) A vesicular stomatitis virus recombinant expressing granulocyte-macrophage colony-stimulating factor induces enhanced T-cell responses and is highly attenuated for replication in animals. J Virol79: 15043-15053
CrossRef
Google scholar
|
[88] |
Sabirov A, Metzger DW (2006) Intranasal vaccination of neonatal mice with polysaccharide conjugate vaccine for protection against pneumococcal otitis media. Vaccine24: 5584-5592
CrossRef
Google scholar
|
[89] |
Scheerlinck JPY (2001) Genetic adjuvants for DNA vaccines. Vaccine19: 2647-2656
CrossRef
Google scholar
|
[90] |
Sekine S, Kataoka K, Fukuyama Y, Adachi Y, Davydova J, Yamamoto M, Kohayashi R, Fujihashi K, Suzuki H, Curiel DT
CrossRef
Google scholar
|
[91] |
Shanmugham LN, Petrarca C, Frydas S, Donelan J, Castellani ML, Boucher W, Madhappan B, Tete S, Falasca K, Conti P
|
[92] |
Staats HF, Ennis FA (1999) IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. J Immunol162: 6141-6147
|
[93] |
Staats HF, Bradney CP, Gwinn WM, Jackson SS, Sempowski GD, Liao HX, Letvin NL, Haynes BF (2001) Cytokine requirements for induction of systemic and mucosal CTL after nasal immunization. J Immunol167: 5386-5394
CrossRef
Google scholar
|
[94] |
Steidler L, Robinson K, Chamberlain L, Schofleld KM, Remaut E, Le Page RW, Wells JM (1998) Mucosal delivery of murine interleukin-2 (IL-2) and IL-6 by recombinant strains of Lactococcus lactis coexpressing antigen and cytokine. Infect Immun66: 3183-3189
|
[95] |
Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W, Fiers W, Remaut E (2000) Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science289: 1352-1355
CrossRef
Google scholar
|
[96] |
Sui Y, Gagnon S, Dzutsev A, Zhu Q, Yu H, Hogg A, Wang Y, Xia Z, Belyakov IM, Venzon D
CrossRef
Google scholar
|
[97] |
Sun K, Salmon SL, Lotz SA, Metzger DW (2007) Interleukin-12 promotes gamma interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect Immun75: 1196-1202
CrossRef
Google scholar
|
[98] |
Tertilt C, Joh J, Krause A, Chou PG, Schneeweiss K, Crystal RG, Worgall S (2009) Expression of B-cell activating factor enhances protective immunity of a vaccine against Pseudomonas aeruginosa. Infect Immun77: 3044-3055
CrossRef
Google scholar
|
[99] |
Thompson AL, Staats HF (2011) Cytokines: the future of intranasal vaccine adjuvants. Clin Dev Immunol2011: 289597
CrossRef
Google scholar
|
[100] |
Thompson AL, Johnson BT, Sempowski GD, Gunn MD, Hou B, DeFranco AL, Staats HF (2012) Maximal adjuvant activity of nasally delivered IL-1 alpha requires adjuvant-responsive CD11c (+) cells and does not correlate with adjuvant-induced in vivo cytokine production. J Immunol188: 2834-2846
CrossRef
Google scholar
|
[101] |
Toka FN, Rouse BT (2005) Mucosal application of plasmid-encoded IL-15 sustains a highly protective anti-Herpes simplex virus immunity. J Leukoc Biol78: 178-186
CrossRef
Google scholar
|
[102] |
Toka FN, Gierynska M, Rouse BT (2003) Codelivery of CCR7 ligands as molecular adjuvants enhances the protective immune response against herpes simplex virus type 1. J Virol77: 12742-12752
CrossRef
Google scholar
|
[103] |
Toka FN, Pack CD, Rouse BT (2004) Molecular adjuvants for mucosal immunity. Immunol Rev199: 100-112
CrossRef
Google scholar
|
[104] |
Tovey MG (2002) Oromucosal cytokine therapy: mechanism(s) of action. Taehan Kan Hakhoe Chi8: 125-131
|
[105] |
Tovey MG, Maury C (1999) Oromucosal interferon therapy: marked antiviral and antitumor activity. J Interferon Cytokine Res19: 145-155
CrossRef
Google scholar
|
[106] |
Tovey MG, Lallemand C, Thyphronitis G (2008) Adjuvant activity of type I interferons. Biol Chem389: 541-545
CrossRef
Google scholar
|
[107] |
Trinchieri G (1995) Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-speciflc adaptive immunity. Annu Rev Immunol13: 251-276
CrossRef
Google scholar
|
[108] |
Van Roey GA, Arias MA, Tregoning JS, Rowe G, Shattock RJ (2012) Thymic stromal lymphopoietin (TSLP) acts as a potent mucosal adjuvant for HIV-1 gp140 vaccination in mice. Eur J Immunol42: 353-363
CrossRef
Google scholar
|
[109] |
Vansnick J (1990) Interleukin-6: an overview. Annu Rev Immunol8: 253-278
CrossRef
Google scholar
|
[110] |
Walker DM (2004) Oral mucosal immunology: an overview. Ann Acad Med Singap33: 27-30
|
[111] |
Wang X, Zhang XY, Kang YM, Jin HL, Du XG, Zhao G, Yu Y, Li JY, Su BW, Huang C
CrossRef
Google scholar
|
[112] |
Watanabe Y, Matsumoto Y, Kikuchi R, Kiriyama M, Nakagawa K, Nomura H, Maruyama K, Matsumoto M (1995) Pharmacokinetics and pharmacodynamics of recombinant human granulocyte colony-stimulating factor (rhG-CSF) following intranasal administration in rabbits. J Drug Targ3: 231-238
CrossRef
Google scholar
|
[113] |
Watford WT, Moriguchi M, Morinobu A, O’Shea JJ (2003) The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev14: 361-368
CrossRef
Google scholar
|
[114] |
Weaver CT, Hatton RD, Mangan PR, Harrington LE (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol25: 821-852
CrossRef
Google scholar
|
[115] |
Wierzbicki A, Kiszka I, Kaneko H, Kmieciak D, Wasik TJ, Gzyl J, Kaneko Y, Kozbor D (2002) Immunization strategies to augment oral vaccination with DNA and viral vectors expressing HIV envelope glycoprotein. Vaccine20: 1295-1307
CrossRef
Google scholar
|
[116] |
Wijesundara DK, Xi Y, Ranasinghe C (2014) Unraveling the convoluted biological roles of type I interferons in infection and immunity: a way forward for therapeutics and vaccine design. Front Immunol5: 412
CrossRef
Google scholar
|
[117] |
Williamson E, Westrich GT, Viney JL (1999) Modulating dendritic cells to optimize mucosal immunization protocols. J Immunol163: 3668-3675
|
[118] |
Wright AKA, Christopoulou I, El Batrawy S, Limer J, Gordon SB (2011) rhIL-12 as adjuvant augments lung cell cytokine responses to pneumococcal whole cell antigen. Immunobiology216: 1143-1147
CrossRef
Google scholar
|
[119] |
Xin KQ, Hamajima K, Sasaki S, Honsho A, Tsuji T, Ishii N, Cao XR, Lu Y, Fukushima J, Shapshak P
CrossRef
Google scholar
|
[120] |
Xin KQ, Hamajima K, Sasaki S, Tsuji T, Watabe S, Okada E, Okuda K (1999a) IL-15 expression plasmid enhances cell-mediated immunity induced by an HIV-1 DNA vaccine. Vaccine17: 858-866
CrossRef
Google scholar
|
[121] |
Xin KQ, Lu Y, Hamajima K, Fukushima J, Yang J, Inamura K, Okuda K (1999b) Immunization of RANTES expression plasmid with a DNA vaccine enhances HIV-1-speciflc immunity. Clin Immunol92: 90-96
CrossRef
Google scholar
|
[122] |
Xu LY, Yang JS, Huang YM, Levi M, Link H, Xiao BG (2000) Combined nasal administration of encephalitogenic myelin basic protein peptide 68-86 and IL-10 suppressed incipient experimental allergic encephalomyelitis in Lewis rats. Clin Immunol96: 205-211
CrossRef
Google scholar
|
[123] |
Zhang X, Yu Q, Zhang X, Yang Q (2009) Co-administration of inactivated avian influenza virus with CpG or rIL-2 strongly enhances the local immune response after intranasal immunization in chicken. Vaccine27: 5628-5632
CrossRef
Google scholar
|
[124] |
Zhang HX, Qiu YY, Zhao YH, Liu XT, Liu M, Yu AL (2014) Immunogenicity of oral vaccination with Lactococcus lactis derived vaccine candidate antigen (UreB) of Helicobacter pylon fused with the human interleukin 2 as adjuvant. Mol Cell Probes28: 25-30
CrossRef
Google scholar
|
[125] |
Zhou M, Zhang G, Ren G, Gnanadurai CW, Li Z, Chai Q, Yang Y, Leyson CM, Wu W, Cui M
CrossRef
Google scholar
|
/
〈 | 〉 |