Mucosal vaccines: A paradigm shift in the development of mucosal adjuvants and delivery vehicles

APMIS

Volumn 123, Issue 4, 2015, Pages 275-288

  Srivastava, Atul ^a   Gowda, Devegowda Vishakante ^a   Madhunapantula, Subbarao V ^b   Shinde, Chetan G ^a   Iyer, Meenakshi ^c  

^a JSS COLLEGE OF PHARMACY   (India)

^b JSS MEDICAL COLLEGE   (India)

^c JSS DENTAL COLLEGE AND HOSPITAL   (India)

Author keywords

Antigen delivery; Immune response; Mucosal adjuvant; Mucosal vaccines

Indexed keywords

ANTIGEN; CHEMOKINE; CYTOKINE; DNA VACCINE; DRUG VEHICLE; ENTEROTOXIN; IMMUNOLOGICAL ADJUVANT; IMMUNOSTIMULATING AGENT; ISCOM; LIPOSOME; LIVE VACCINE; NANOPARTICLE; POLYMER; TOLL LIKE RECEPTOR AGONIST; VIROSOME; DRUG CARRIER; IMMUNOGLOBULIN A; VACCINE;

DENDRITIC CELL; DRUG DELIVERY SYSTEM; HUMAN; IMMUNITY; MEDICATION COMPLIANCE; MUCOSAL ADMINISTRATION; MUCOSAL IMMUNITY; MUCOSAL VACCINATION; PRIORITY JOURNAL; REVIEW; TH1 CELL; TH2 CELL; TRANSGENIC PLANT; VACCINATION; VACCINE PRODUCTION; IMMUNOLOGY; MUCOSA; PROCEDURES;

ADJUVANTS, IMMUNOLOGIC; CYTOKINES; DRUG CARRIERS; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN A; MUCOUS MEMBRANE; TH1 CELLS; TH2 CELLS; VACCINATION; VACCINES;

EID: 84925299748     PISSN: 09034641     EISSN: 16000463     Source Type: Journal    
DOI: 10.1111/apm.12351     Document Type: Review

References (144)

1. Specht A, Frohlich N, Zoellner Y. The economics of vaccination. J Health Policy Outcome Res 2012;2:2-5.
2. Purchase C, Picard J, McDonald R, Bisschop SP. A comparison of the oral application and injection routes using the onderstepoort biological products fowl typhoid vaccine, its safety, efficacy and duration of protection in commercial laying hens. J S Afr Vet Assoc 2008;79:39-43.
3. Walker RI. New strategies for using mucosal vaccination to achieve more effective immunization. Vaccine 1994;12:387-400.
4. Levine MM, Dougan G. Optimism over vaccines administered via mucosal surfaces. Lancet 1998;351:1375-6.
5. Yuki Y, Kiyono H. Mucosal vaccines: novel advances in technology and delivery. Expert Rev Vaccines 2009;8:1083-97.
6. Neutral MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006;6:148-58.
7. Gallichan WS, Rosenthal KL. Specific secretory immune responses in the female genital tract following intranasal immunization with a recombinant adenovirus expressing glycoprotein B of herpes simplex virus. Vaccine 1995;13:1589-95.
8. Haneberg B, Kendall D, Amerongen HM, Apter FM, Kraehenbuhl JP, Neutra MR. Induction of specific immunoglobulin A in the small intestine, colon-rectum, and vagina measured by a new method for collection of secretions from local mucosal surfaces. Infect Immun 1994;62:15-23.
9. McGhee JR, Lamm ME, Strober W. Mucosal immune responses: an overview. In: Ogra PL, Mestecky J, Lamm ME, Strober W, McGhee JR, Bienenstock J, editors. Mucosal Immunology, 2nd ed. San Diego, CA: Academic Press, 1999: 485-506.
10. Macpherson AJ, McCoy KD, Johansen FE, Brandtzaeg P. The immune geography of IgA induction and function. Mucosal Immunol 2008;1:11-22.
11. Jain S, Khomane K, Jain AK, Dani P. Nanocarriers for transmucosal vaccine delivery. Curr Nanosci 2011;7:160-77.
12. Holmgren J, Svennerholm AM. Vaccines against mucosal infections. Curr Opin Immunol 2012;24:343-53.
13. Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol 2004;82:488-96.
14. Correia-Pinto JF, Csaba N, Alonso MJ. Vaccine delivery carriers: insights and future perspectives. Int J Pharm 2013;440:27-38.
15. Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005;11:S45-53.
16. Chen W, Patel GB, Yan H, Zhang J. Recent advances in the development of novel mucosal adjuvants and antigen delivery systems. Hum Vaccine 2010;6:706-14.
17. Rhee JH, Lee SE, Kim SY. Mucosal vaccine adjuvants update. Clin Exp Vaccine Res 2012;1:50-63.
18. Cogne M, Ballet JJ, Schmitt C, Bizzini B. Total and IgE antibody levels following booster immunization with aluminum absorbed and non-absorbed tetanus toxoid in humans. Ann Allergy 1985;54:148-51.
19. Hajishengallis G, Arce S, Gockel CM, Connell TD, Russel MW. Immunomodulation with enterotoxins for the generation of secretory immunity or tolerance: applications for oral infections. J Dent Res 2005;84:1104-16.
20. Van Heyningen S. Cholera toxin: interaction of subunits with ganglioside GM1. Science 1974;183:656-7.
21. Fukuta S, Magnani JL, Twiddy EM, Holmes RK, Ginsburg V. Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect Immun 1988;56:1748-53.
22. Simmons CP, Ghaem-Magami M, Petrovska L, Lopes L, Chain BM, Williams NA, et al. Immunomodulation using bacterial enterotoxins. Scand J Immunol 2001;53:218-26.
23. Couch RB. Nasal vaccination, Escherichia coli enterotoxin, and Bell's palsy. N Engl J Med 2004;350:860-1.
24. Pizza M, Giuliani MM, Fontana MR, Monaci E, Douce G, Dougan G, et al. Mucosal vaccines: non-toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 2001;19:2534-41.
25. Czerkinsky C, Holmgren J. Topical immunization strategies. Mucosal Immunol 2010;3:545-55.
26. Tochikubo K, Isaka M, Yasuda Y, Kozuka S, Matano K, Miura Y, et al. Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses of mice to mucosally co-administered bovine serum albumin. Vaccine 1998;16:150-5.
27. Haan L, Verweij WR, Holtrop M, Brands R, van Scharrenburg GJ, Palache AM, et al. Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 2001;19:2898-907.
28. 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 2002;85:263-70.
29. Peppoloni S, Ruggiero P, Contorni M, Morandi M, Pizza M, Rappuoli R, et al. Mutants of the Escherichia coli heat-labile enterotoxin as safe and strong adjuvants for intranasal delivery of vaccines. Expert Rev Vaccines 2003;2:285-93.
30. Alejo DM, Moraes MP, Liao X, Dias CC, Tulman ER, Diaz-San Segundo F, et al. An adenovirus vectored mucosal adjuvant augments protection of mice immunized intranasally with an adenovirus-vectored foot-and-mouth disease virus subunit vaccine. Vaccine 2013;31:2302-9.
31. Norton EB, Lawson LB, Freytag LC, Clements JD. Characterization of a mutant Escherichia coli heat-labile toxin, LT (R192G/L211A), as a safe and effective oral adjuvant. Clin Vaccine Immunol 2011;18:546-51.
32. Fang Y, Larsson L, Mattsson J, Lycke N, Xiang Z. Mast cells contribute to the mucosal adjuvant effect of CTA1-DD after IgG-complex formation. J Immunol 2010;185:2935-41.
33. Lycke N. The B-cell targeted CTA1-DD vaccine adjuvant is highly effective at enhancing antibody as well as CTL responses. Curr Opin Mol Ther 2001;3:37-44.
34. Eliasson DG, Helgeby A, Schon K, Nygren C, El-Bakkouri K, Fiers W, et al. A novel non-toxic combined CTA1-DD and ISCOMS adjuvant vector for effective mucosal immunization against influenza virus. Vaccine 2011;29:3951-61.
35. Datta SK, Sabet M, Nguyen KP, Valdez PA, Gonzalez-Navajas JM, Islam S, et al. Mucosal adjuvant activity of cholera toxin requires Th17 cells and protects against inhalation anthrax. Proc Natl Acad Sci U S A 2010;107:10638-43.
36. Lu YJ, Yadav P, Clements JD, Forte S, Srivastava A, Thompson CM, et al. Options for inactivation, adjuvant, and route of topical administration of a killed, unencapsulated pneumococcal whole-cell vaccine. Clin Vaccine Immunol 2010;17:1005-12.
37. Harandi A, Medaglini D. Mucosal adjuvants. Curr HIV Res 2010;8:330-5.
38. Casella CR, Mitchell TC. Putting endotoxin to work for us: monophosphoryl lipid A as a safe and effective vaccine adjuvant. Cell Mol Life Sci 2008;65:3231-40.
39. Baldridge JR, Crane RT. Monophosphoryl lipid A (MPL) formulations for the next generation of vaccines. Methods 1999;19:103-7.
40. Moore A, McCarthy L, Mills KH. The adjuvant combination monophosphoryl lipid A and QS21 switches T cell responses induced with a soluble recombinant HIV protein from Th2 to Th1. Vaccine 1999;17:2517-27.
41. Uhlmann E, Vollmer J. Recent advances in the development of immunostimulatory oligonucleotides. Curr Opin Drug Discov Devel 2003;6:204-17.
42. Shima F, Uto T, Akagi T, Akashi M. Synergistic stimulation of antigen presenting cells via TLR by combining CpG ODN and poly (γ-glutamic acid)-based nanoparticles as vaccine adjuvants. Bioconjug Chem 2013;24:926-33.
43. Moldoveanu Z, Love-Honman L, Hunag WQ, Krieg AM. CpG DNA. A novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine 1998;16:1216-24.
44. Tengvall S, Lundqvist A, Eisenberg RJ, Cohen GH, Harandi AM. Mucosal administration of CpG oligodeoxynucleotide elicits strong CC and CXC chemokine responses in the vagina and serves as a potent Th1-tilting adjuvant for recombinant gD2 protein vaccination against genital herpes. J Virol 2006;80:5283-91.
45. Yang J, Mao M, Zhang S, Li H, Jiang Z, Cao G, et al. Innate defense regulator peptide synergizes with CpG ODN for enhanced innate intestinal immune responses in neonate piglets. Int Immunopharmacol 2012;12:415-24.
46. Asadi Karam MR, Oloomi M, Mahdavi M, Habibi M, Bouzari S. Vaccination with recombinant FimH fused with flagellin enhances cellular and humoral immunity against urinary tract infection in mice. Vaccine 2013;31:1210-6.
47. Lee SE, Kim SY, Jeong BC, Kim YR, Bae SJ, Ahn OS, et al. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect Immun 2006;74:694-702.
48. Nguyen CT, Kim SY, Kim MS, Lee SE, Rhee JH. Intranasal immunization with recombinant PspA fused with a flagellin enhances cross-protective immunity against Streptococcus pneumoniae infection in mice. Vaccine 2011;29:5731-9.
49. Hong SH, Byun YH, Nguyen CT, Kim SY, Seong BL, Park S, et al. Intranasal administration of a flagellin adjuvanted inactivated influenza vaccine enhances immune responses to protect mice against lethal infection. Vaccine 2012;30:466-74.
50. Kayamuro H, Yoshioka Y, Abe Y, Arita S, Katayama K, Nomura T, et al. Interleukin-1 family cytokines as mucosal vaccine adjuvants for induction of protective immunity against influenza virus. J Virol 2010;84:12703-12.
51. Vaidya M, Srivastava I, Polo J, Donnelly J, O'Hagan D, Singh M. Mucosal adjuvants and delivery systems for protein, DNA and RNA based vaccines. Immunol Cell Biol 2004;82:617-27.
52. Bracci L, Canini I, Puzelli S, Sestili P, Venditti M, Spada M, et al. 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. Vaccine 2005;23:2994-3004.
53. Bradney CP, Sempowski GD, Liao HX, Haynes BF, Staats HF. Cytokines as adjuvants for the induction of anti-human immunodeficiency virus peptide immunoglobulin G and IgA antibodies in serum and mucosal secretions after nasal immunization. J Virol 2002;76:517-24.
54. Bermudez LE, Wu M, Young LS. Interleukin-12-stimulated natural killer cells can activate human macrophages to inhibit growth of Mycobacterium avium. Infect Immun 1995;63:4099-104.
55. Trinchieri G. Interleukin-12: a cytokine produced by antigen-presenting cells with immune regulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood 1994;84:4008-27.
56. Jabbal-Gill I. Nasal vaccine innovation. J Drug Target 2010;18:771-86.
57. Huber VC, Arulanandam BP, Arnaboldi PM, Elmore MK, Sheehan CE, Kallakury BV, et al. Delivery of IL-12 intranasally leads to reduced IL-12-mediated toxicity. Int Immunopharmacol 2003;3:801-9.
58. Winstone N, Wilson AJ, morrow G, Boggiano C, Chiuchiolo MJ, Lopez M, et al. Enhanced control of pathogenic simian immunodeficiency virus SIVmac239 replication in Macaques immunized with an interleukin-12 plasmid and a DNA prime-viral vector boost vaccine regimen. J Virol 2011;85:9578-87.
59. Boyaka PN, Marinaro M, Jackson RJ, Menon S, Kiyono H, Jirillo E, et al. IL-12 is an effective adjuvant for induction of mucosal immunity. J Immunol 1999;162:122-8.
60. Gwinn WM, Kirwan SM, Wang SH, Ashcraft KA, Sparks NL, Doil CR, et al. Effective Induction of protective systemic immunity with nasally administered vaccines adjuvanted with IL-1. Vaccine 2010;28:6901-14.
61. Heufler C, Koch F, Schuler G. Granulocyte/macrophage colony-stimulating factor and interleukin 1 mediate the maturation of murine epidermal Langerhans cells into potent immunostimulatory dendritic cells. J Exp Med 1988;167:700-5.
62. Heath AW. Cytokines as immunological adjuvants. Pharm Biotechnol 1995;6:645-58.
63. Staats HF, Bradney CP, Gwinn WM, Jackson SS, Sempowski D, Liao HX, et al. Cytokine requirements for the induction of systemic and mucosal cytotoxic T lymphocytes after nasal immunization. J Immunol 2001;167:5386-94.
64. Lilliard JW Jr, Boyaka PN, Taub DD, McGhee JR. RANTES potentiates antigen-specific mucosal immune responses. J Immunol 2001;166:162-9.
65. Ryan EJ, Daly LM, Mills KH. Immunomodulators and delivery system for vaccination by mucosal routes. Trends Biotechnol 2001;19:293-304.
66. Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 1996;14:275-300.
67. Chung SW, Hil-lal TA, Byun Y. Strategies for non-invasive delivery of biologics. J Drug Target 2012;20:481-501.
68. Delie F, Blanco-Príeto MJ. Polymeric particulates to improve oral bioavailability of peptide drugs. Molecules 2005;10:65-80.
69. Mathew S, Lendlein A, Wischke C. Characterization of protein-adjuvant coencapsulation in microparticles for vaccine delivery. Eur J Pharm Biopharm 2014;87:403-7.
70. O'Hagan DT. Microparticles and polymers for the mucosal delivery of vaccines. Adv Drug Deliv Rev 1998;34:305-20.
71. Eldridge JH, Meulbroek JA, Stass JK, tice TR, Gilley RM. Vaccine-containing biodegradable microspheres specifically enter the gut-associated lymphoid tissue following oral administration and induce a disseminated mucosal immune response. Adv Exp Med Biol 1989;251:191-202.
72. Miller RA, Brady JM, Cutright DE. Degradation rates of oral resorbable implants (polylactates and polyglycolates): rate modification with changes in PLA/PGA copolymer ratios. J Biomed Mater Res 1977;11:711-9.
73. Benoit MA, Baras B, Gillard J. Preparation and characterization of protein-loaded poly (epsilon-caprolactone) microparticles for oral vaccine delivery. Int J Pharm 1999;184:73-84.
74. Estevan M, Gamazo C, Grillo MJ, Barrio GGD, Blasco JM, Irache JM. Experiments on a sub-unit vaccine encapsulated in microparticles and its efficacy against Brucella melitensis in mice. Vaccine 2006;24:4179-87.
75. Carpenter ZK, Williamson ED, Eyles JE. Mucosal delivery of microparticle encapsulated ESAT-6 induces robust cell-mediated responses in the lung milieu. J Control Release 2005;104:67-77.
76. Gunbeyaz M, Faraji A, Ozkul A, Purali N, Şenel S. Chitosan based delivery systems for mucosal immunization against bovine herpesvirus 1 (BHV-1). Eur J Pharm Sci 2010;41:531-45.
77. Howard KA, Li XW, Somavarapu S, Singh J, Green N, Atuah KN, et al. Formulation of a microparticle carrier for oral polyplex-based DNA vaccines. Biochim Biophys Acta 2004;1674:149-57.
78. Hans ML, Lowman AM. Biodegradable nanoparticles for drug delivery and targeting. Curr Opin Solid State Mater Sci 2002;6:319-27.
79. Langer R. Drug delivery and targeting. Nature 1998;392(6679 Suppl):5-10.
80. Lohcharoenkal W, Wang L, Chen YC, Rojanasakul Y. Protein nanoparticles as drug delivery carriers for cancer therapy. Biomed Res Int 2014;2014:180549.
81. des Rieux A, Fievez V, Garinot M, Schneider YJ, Preat V. Nanoparticles as potential oral delivery systems of proteins and vaccines: a mechanistic approach. J Control Release 2006;116:1-27.
82. Illum L. Nanoparticulate systems for nasal delivery of drugs: a real improvement over simple systems? J Pharm Sci 2007;96:473-83.
83. Dionisio M, Cordeiro C, Remuñán-López C, Seijo B, Rosa da Costa AM, Grenha A. Pullulan-based nanoparticles as carriers for transmucosal protein delivery. Eur J Pharm Sci 2013;50:102-13.
84. Irache Garreta JM, Yoncheva KP. 2008. Biodegradable; vinyl methyl ether and maleic anhydride (PVM/MA) copolymer; excellent bioadhesion, size and zeta potential characteristics, US Patent 20080248125A1.
85. Sivasubramanian M, Thambi T, Park JH. Mineralized cyclodextrin nanoparticles for sustained protein delivery. Carbohydr Polym 2013;97:643-9.
86. Sessa G, Weismann G. Phospholipid spherules (liposomes) as a model for biological membranes. J Lipid Res 1968;9:310-8.
87. Alving CR. Liposomes as carriers of antigens and adjuvants. J Immunol Methods 1991;140:1-13.
88. Landesman-Milo D, Peer D. Altering the immune response with lipid-based nanoparticles. J Control Release 2012;161:600-8.
89. Christensen D, Foged C, Rosenkrands I, Lundberg CV, Andersen P, Agger EM, et al. CAF01 liposomes as a mucosal vaccine adjuvant: in vitro and in vivo investigations. Int J Pharm 2010;390:19-24.
90. Tafaghodi M, Jaafari MR, Sajadi Tabassi SA. Nasal immunization studies using liposomes loaded with tetanus toxoid and CpG-ODN. Eur J Pharm Biopharm 2006;64:138-45.
91. Wang HW, Jiang PL, Lin SF, Lin HJ, Ou KL, Deng WP, et al. Application of galactose-modified liposomes as a potent antigen presenting cell targeted carrier for intranasal immunization. Acta Biomater 2013;9:5681-8.
92. Mannino RJ, Canki M, Feketeova E, Scolpino AJ, Wang Z, Zhang F, et al. Targeting immune response induction with cochleate and liposome-based vaccines. Adv Drug Deliv Rev 1998;32:273-87.
93. Gould-Fogerite S, Kheiri MT, Zhang F, Wang Z, Scolpino AJ, Feketeova E, et al. Targeting immune response induction with cochleate and liposome-based vaccines. Adv Drug Deliv Rev 1998;32:273-87.
94. Landge A, Pawar A, Shaikh K. Investigation of cochleates as carriers for topical drug delivery. Int J Pharm Pharm Sci 2013;5:314-20.
95. Rao R, Squillante E 3rd, Kim KH. Lipid-based cochleates: a promising formulation platform for oral and parenteral delivery of therapeutic agents. Crit Rev Ther Drug Carrier Syst 2007;24:41-61.
96. Zarif L, Graybill JR, Perlin D, Mannino RJ. Cochleates: new lipid-based drug delivery system. J Liposome Res 2000;10:523-38.
97. Levi R, Aboud-Pirak E, Leclerc C, Lowell GH, Arnon R. Intranasal immunization of mice against influenza with synthetic peptides anchored to proteosomes. Vaccine 1995;13:1353-9.
98. Orr N, Robin G, Cohen D, Arnon R, Lowell GH. Immunogenicity and efficacy of oral or intranasal Shigella flexneri 2a and Shigella sonnei proteosome-lipopolysaccharide vaccine in animal models. Infect Immun 1993;61:2390-5.
99. Sharma S, Mukkur TK, Benson HA, Chen Y. Pharmaceutical aspects of intranasal delivery of vaccines using particulate system. J Pharm Sci 2009;98:812-43.
100. Treanor J, Nolan C, O'Brien D, Burt D, Lowell G, Linden J, et al. Intranasal administration of a proteosome-influenza vaccine is well-tolerated and induces serum and nasal secretion influenza antibodies in healthy human subjects. Vaccine 2006;24:254-62.
101. Langley JM, Halperin SA, McNeil S, Smith B, Jones T, Burt D, et al. Safety and immunogenicity of a Proteosome TM-trivalent inactivated influenza vaccine given nasally to healthy adult. Vaccine 2006;24:1601-8.
102. Patel GB, Sprott GD. Archaeobacterial ether lipid liposomes (archaeosomes) as novel vaccine and drug delivery systems. Crit Rev Biotechnol 1999;19:317-57.
103. Patel GB, Chen W. Archaeosome immunostimulatory vaccine delivery system. Curr Drug Deliv 2005;2:407-21.
104. Benvegnu T, Lemiègre L, Cammas-Marion S. New generation of liposomes called archaeosomes based on natural or synthetic archaeal lipids as innovative formulations for drug delivery. Recent Pat Drug Deliv Formul 2009;3:206-20.
105. Mangal S, Garg NK, Mounavya A, Sahu T, Tyagi RK. Recent patents on oral vaccine design. Recent Pat Endocr Metab Immune Drug Discov 2009;3:179-93.
106. Krishnan L, Dicaire CJ, Patel GB, Sprott GD. Archaeosome vaccine adjuvants induce strong humoral, cell-mediated, and memory responses: comparison to conventional liposomes and alum. Infect Immun 2000;68:54-63.
107. Gluck R. Adjuvant activity of immunopotentiating reconstituted influenza virosomes (IRIVs). Vaccine 1999;17:1782-7.
108. Durrer P, Gluck U, Spyr C, Lang AB, Zurbriggen R, Herzog C, et al. Mucosal antibody response induced with a nasal virosome-based influenza vaccine. Vaccine 2003;21:4328-34.
109. Gluck R, Metcalfe IC. Novel approaches in the development of immunopotentiating reconstituted influenza virosomes as efficient antigen carrier systems. Vaccine 2003;21:611-5.
110. Bomsel M, Tudor D, Drillet AS, Alfsen A, Ganor Y, et al. Immunization with HIV-1 gp41 subunit virosomes induces mucosal antibodies protecting nonhuman primates against vaginal SHIV challenges. Immunity 2011;34:269-80.
111. Zurbriggen R. Immunostimulating reconstituted influenza virosomes. Vaccine 2003;21:921-4.
112. Cusi MG, Zurbriggen R, Valassina M, Bianchi S, Durrer P, Valensin PE, et al. Intranasal immunization with mumps virus DNA vaccine delivered by influenza virosomes elicits mucosal and systemic immunity. Virology 2000;277:111-8.
113. De Miguel I, Ioualalen K, Bonnefous M, Peyrot M, Nguyen F, Cervilla M, et al. Synthesis and characterization of supramolecular biovector (SMBV) specifically designed for the entrapment of ionic molecules. Biochim Biophys Acta 1995;1237:49-58.
114. Csaba N, Garcia-Fuentes M, Alonso MJ. Nanoparticles for nasal vaccination. Adv Drug Deliv Rev 2009;61:140-57.
115. Debin A, Kravtzoff R, Santiago JV, Cazales L, Sperandio S, Melber K, et al. Intranasal immunization with recombinant antigens associated with new cationic particles induces strong mucosal as well as systemic antibody and ctl responses. Vaccine 2002;20:2752-63.
116. Berton M, Sixou S, Kravtzoff R, Dartigues C, Imbertie L, Allal C, et al. Improved oligonucleotide uptake and stability by a new drug carrier, the SupraMolecular BioVector (SMBV). Biochim Biophys Acta 1997;1355:7-19.
117. Castignolles N, Betbeder D, Loualalen K, Merten O, Leclerc C, Samain D, et al. Stabilization and enhancement of interleukin-2 in vitro bioactivity by new carriers: supramolecular biovectors. Vaccine 1994;12:1413-8.
118. El mir S, Casanova A, Betbeder D, Triebel F. A combination of interleukin-2 and 60 nm cationic supramolecular biovectors for the treatment of established tumours by subcutaneous or intranasal administration. Eur J Cancer 2001;37:1053-60.
119. Lovgren K, Morein B. The requirement of lipids for the formation of immunostimulating complexes (ISCOMs). Biotechnol Appl Biochem 1988;10:161-72.
120. Furrie E, Smith RE, Turner MW, Strobel S, Mowat AM. Induction of local innate immune responses and modulation of antigen uptake as mechanisms underlying the mucosal adjuvant properties of immune stimulating complexes (ISCOMS). Vaccine 2002;20:2254-62.
121. Sanders MT, Deliyannis G, Pearse MJ, McNamara MK, Brown LE. Single dose intranasal immunization with iscomatrix vaccines to elicit antibody-mediated clearance of influenza virus requires delivery to the lower respiratory tract. Vaccine 2009;27:2475-82.
122. Jani P, Halbert GW, Langridge J, Florence AT. Nanoparticle uptake by the rat gastrointestinal mucosa: quantitation and particle size dependency. J Pharm Pharmacol 1990;42:821-6.
123. Eo SK, Gierynska M, Kamar AA, Rouse BT. Prime-boost immunization with DNA vaccine: mucosal route of administration changes the rules. J Immunol 2001;166:5473-9.
124. Ingolotti M, Kawalekar O, Shedlock DJ, Muthumani K, Weiner DB. DNA vaccines for targeting bacterial infections. Expert Rev Vaccines 2010;9:747-63.
125. Noll A, Bucheler N, Schirmbeck R, Reimann J, Autenrieth IB. DNA immunization confers systemic, but not mucosal, protection against enteroinvasive bacteria. Eur J Immunol 1999;29:986-96.
126. Sagodira S, Iochmann S, Mevelec MN, Dimier-Poisson I, Bout D. Nasal immunization of mice with Cryptosporidium parvum DNA induces systemic and intestinal immune responses. Parasite Immunol 1999;21:507-16.
127. Asakura Y, Lundholm P, Kjerrstrom A, Benthin R, Lucht E, Fukushima J, et al. DNA-plasmids of HIV-1 induce systemic and mucosal immune responses. Biol Chem 1999;380:375-9.
128. Hobson P, Barnfield C, Barnes A, Klavinskis LS. Mucosal immunization with DNA vaccines. Methods 2003;31:217-24.
129. Ranasinghe C, Ramshaw IA. Genetic heterologous prime-boost strategies for improved systemic and mucosal immunity. Expert Rev Vaccines 2009;8:1171-81.
130. Streatfield SJ. Mucosal immunization using recombinant plant-based oral vaccines. Methods 2006;38:150-7.
131. Kumar VB, Raja TK, Wani MR, Sheikh SA, Lone MA, Nabi G, et al. Transgenic plants as green factories for vaccine production. Afr J Biotechnol 2013;12:6147.
132. Fischer R, Stoger E, Schillberg S, Christou P, Twyman RM. Plant-based production of biopharmaceuticals. Curr Opin Plant Biol 2004;7:152-8.
133. Haq TA, Mason HS, Clements JD, Arntzen CJ. Oral immunization with a recombinant bacterial antigen produced in transgenic plants. Science 1995;268:714-6.
134. Brennan FR, Bellaby T, Helliwell SM, Jones TD, Kamstrup S, Dalsgaard K, et al. Chimeric plant virus particles administered nasally or orally induce systemic and mucosal immune responses in mice. J Virol 1999;73:930-8.
135. Nochi T, Takagi H, Yuki Y, Yang L, Masumura T, Mejima M, et al. Rice-based mucosal vaccine as a global strategy for cold-chain- and needle-free vaccination. Proc Natl Acad Sci U S A 2007;104:10986-91.
136. Hantman MJ, Hohmann EL, Murphy CG, Knipe DM, Miller SI. Antigen delivery systems: development of recombinant live vaccines using viral or bacterial vectors. In: Ogra PL, Mestecky J, Lamm ME, Strober W, McGhee JR, Bienenstock J, editors. Mucosal Immunology, 2nd ed. San Diego, CA: Academic Press, 1999: 779-91.
137. Abreu MT, Fukata M, Arditi M. TLR signaling in the gut in health and disease. J Immunol 2005;174:4453-60.
138. Chatfield SN, Charles IG, Makoff AJ, Oxer MD, Dougan G, Pickard D, et al. Use of the nirB promoter to direct the stable expression of heterologous antigens in Salmonella oral vaccine strains: development of a single-dose oral tetanus vaccine. Biotechnology 1992;10:888-92.
139. Lagranderie M, Murray A, Gicquel B, Leclerc C, Gheorghiu M. Oral immunization with recombinant BCG induces cellular and humoral immune responses against the foreign antigen. Vaccine 1993;11:1283-90.
140. McFadden G. Poxvirus tropism. Nat Rev Microbiol 2005;3:201-13.
141. Tatsis N, Ertl HC. Adenoviruses as vaccine vectors. Mol Ther 2004;10:616-29.
142. Viret JF, Cryz SJ Jr, Favre D. Expression of Shigella sonnei lipopolysaccharide in Vibrio cholerae. Mol Microbiol 1996;19:949-63.
143. Favre D, Cryz SJ Jr, Viret JF. Development of Shigella sonnei live oral vaccines based on defined rfb Inaba deletion mutants of Vibrio cholerae expressing the Shigella serotype D O polysaccharide. Infect Immun 1996;64:576-84.
144. Walcher P, Mayr UB, Azimpour-Tabrizi C, Eko FO, Jechlinger W, Mayrhofer P, et al. Antigen discovery and delivery of subunit vaccines by nonliving bacterial ghost vectors. Expert Rev Vaccines 2004;3:681-91.