Starch microparticles as vaccine adjuvant

Expert Opinion on Drug Delivery

Volumn 2, Issue 5, 2005, Pages 807-828

  Rydell, Niclas ^a   Stertman, Linda ^a   Sjöholm, Ingvar ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Microparticles; Mucosal vaccination; Oral vaccination; Starch; Vaccine adjuvant; Vaccine formulation

Indexed keywords

ADHESIVE AGENT; ADJUVANT; AMYLOPECTIN; AMYLOSE; ANTIGEN; BACTERIAL ANTIGEN; BOVINE SERUM ALBUMIN; CHITOSAN; CHOLERA TOXIN B SUBUNIT; CYCLODEXTRIN; DILUENT; DIPHTHERIA VACCINE; DISINTEGRATING AGENT; DNA; HUMAN SERUM ALBUMIN; INTERLEUKIN 5; INTERLEUKIN 6; LYSOPHOSPHATIDYLCHOLINE; PARASITE ANTIGEN; POLYGLYCOLIDE; POLYLACTIDE; POLYMER; PULLULAN; RECOMBINANT ANTIGEN; SILICONE; STARCH; STARCH MICROSPHERE; SYNTHETIC PEPTIDE; UNINDEXED DRUG; VIRUS ANTIGEN;

ANTIGEN PURIFICATION; BIODEGRADABILITY; DRUG FORMULATION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; INFECTION; MUCOSAL IMMUNITY; NONHUMAN; PARTICLE SIZE; REVIEW;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; EXCIPIENTS; HUMANS; IMMUNITY, MUCOSAL; NANOSTRUCTURES; STARCH; VACCINATION; VACCINES;

EID: 27144473435     PISSN: 17425247     EISSN: None     Source Type: Journal    
DOI: 10.1517/17425247.2.5.807     Document Type: Review

References (157)

1. BRAYDEN DJ: Oral vaccination in man using antigens in particles: current status. Eur. J. Pharm. Sci. (2001) 14(3):183-189.
2. YEH P, ELLENS H, SMITH PL: Physiological considerations in the design of particulate dosage forms for oral vaccine delivery. Adv. Drug Deliv. Rev. (1998) 34(2-3):123-133.
3. CLARK MA, JEPSON MA, HIRST BH: Exploiting M cells for drug and vaccine delivery. Adv. Drug Deliv. Rev. (2001) 50(1-2):81-106.
4. LI WAN PO A: Delivery systems for non-parenteral vaccines. Adv. Drug Deliv. Rev. (1995) 18:101-109.
5. O'HAGAN DT: Microparticles and polymers for the mucosal delivery of vaccines. Adv. Drug Deliv. Rev. (1998) 34:305-320.
6. RYAN EJ, DALY LM, MILLS KH: Immunomodulators and delivery systems for vaccination by mucosal routes. Trends Biotechnol. (2001) 19(8):293-304.
7. SINGH M, LI XM, WANG H et al.: Controlled release microparticles as a single dose diphtheria toxoid vaccine: immunogenicity in small animal models. Vaccine (1998) 16(4):346-352.
8. OGRA PL, FADEN H, WELLIVER RC: Vaccination strategies for mucosal immune responses. Clin. Microbiol. Rev. (2001) 14(2):430-445.
9. ABREU MT: Immunologic regulation of Toll-like receptors in gut epithelium. Curr. Opin. Gastroenterol. (2003) 19(6):559-564.
10. STORNI T, KUNDIG TM, SENTI G, JOHANSEN P: Immunity in response to particulate antigen-delivery systems. Adv. Drug Deliv. Rev. (2005) 57(3):333-355.
11. VAN DER LUBBEN IM, VERHOEF JC, BORCHARD G, JUNGINGER HE: Chitosan for mucosal vaccination. Adv. Drug Deliv. Rev. (2001) 52(2):139-144.
12. GUPTA RK, SINGH M, O'HAGAN DT: Poly(lactide-co-glycolide) microparticles for the development of single-dose controlled-release vaccines. Adv. Drug Deliv. Rev. (1998) 32(3):225-246.
13. TUOVINEN L, PELTONEN S, LIIKOLA M et al.: Drug release from starch-acetate microparticles and films with and without incorporated alpha-amylase. Biomaterials (2004) 25(18):4355-4362.
14. ARTURSSON P, EDMAN P, LAAKSO T, SJÖHOLM I: Characterization of polyacryl starch microparticles as carriers for proteins and drugs. J. Pharm. Sci. (1984) 73(11):1507-1513.
15. HERITAGE PL, LOOMES LM, JIANXIONG J et al.: Novel polymer-grafted starch microparticles for mucosal delivery of vaccines. Immunology (1996) 88(1):162-168.
16. MCDERMOTT MR, HERITAGE PL, BARTZOKA V, BROOK MA. Polymer-grafted starch microparticles for oral and nasal immunization. Immunol. Cell Biol. (1998) 76(3):256-262.
17. Microspheres and Drug Therapy. SS Davis, L Illum, JG McVie, E Tomlinson (Eds), Elsevier, London, UK (1984).
18. O'HAGAN DT, RAPPUOLI R: Novel approaches to vaccine delivery. Pharm. Res. (2004) 21(9):1519-1530.
19. O'HAGAN DT: Oral delivery of vaccines. Formulation and clinical pharmacokinetic considerations. Clin. Pharmacokinet. (1992) 22(1):1-10.
20. ALPAR HO, EYLES JE, WILLIAMSON ED, SOMAVARAPU S: Intranasal vaccination against plague, tetanus and diphtheria. Adv. Drug Deliv. Rev. (2001) 51(1-3):173-201.
21. FLORENCE AT: The oral absorption of micro- and nanoparticulates: neither exceptional nor unusual. Pharm. Res. (1997) 14(3):259-266.
22. ROTHMAN U, ARFORS KE, ARONSEN KF, LINDELL B, NYLANDER G: Enzymatically degradable microspheres for experimental and clinical use. Sixth meeting of the nordic microcirculation group. (1976)
23. LINDBERG M, LOTE K, TEDER H: Biodegradable starch microspheres - a new medical tool. In: Microspheres and Drug Therapy. SS Davis, L Illum, JG McVie, E Tomlinson (Eds), Elsevier, London, UK (1984):153-188.
24. BJÖRK E, EDMAN P: Degradable starch microspheres as a nasal delivery system for insulin. Int. J. Pharm. (1988) 47:233-238.
25. LEPISTÖ M, ARTURSSON P, EDMAN P, LAAKSO T, SJÖHOLM I: Determination of the degree of derivatization of acryloylated polysaccharides by Fourier transform proton NMR spectroscopy. Anal. Biochem. (1983) 133(1):132-135.
26. BETHELL GS, AYERS JS, HANCOCK WS, HEARN MT: A novel method of activation of cross-linked agaroses with 1,1′-carbonyldiimidazole which gives a matrix for affinity chromatography devoid of additional charged groups. J. Biol. Chem. (1979) 254(8):2572-2574.
27. ARTURSSON P, MÅRTENSSON IL, SJÖHOLM I: Biodegradable microspheres. III: some immunological properties of polyacryl starch microparticles. J. Pharm. Sci. (1986) 75(7):697-701.
28. ARTURSSON P, ARRO E, EDMAN P, ERICSSON JLE, SJÖHOLM I: Biodegradable microspheres V: Stimulation of macrophages with microparticles made of various polysaccharides. J. Pharm. Sci. (1987) 76:127-133.
29. DEGLING WIKINGSSON L, SJÖHOLM I: Polyacryl starch microparticles as adjuvant in oral immunisation, inducing mucosal and systemic immune responses in mice. Vaccine (2002) 20:3355-3363.
30. HERITAGE PL, BROOK MA, UNDERDOWN BJ, MCDERMOTT MR: Intranasal immunization with polymer-grafted microparticles activates the nasal-associated lymphoid tissue and draining lymph nodes. Immunology (1998) 93(2):249-256.
31. CONSTANTIN M, FUNDUEANU G, CORTESI R, ESPOSITO E, NASTRUZZI C: Aminated polysaccharide microspheres as DNA delivery systems. Drug Deliv. (2003) 10(3):139-149.
32. ARTURSSON P, EDMAN P, ERICSSON JLE: Macrophage stimulation with some structurally related polysaccharides. Scand J. Immunol. (1987) 25:245-254.
33. ARTURSSON P, ERICSSON JL, SJÖHOLM I: Inflammatory response to polyacryl starch microparticles, role of arachidonic acid metabolites. Int. J. Pharm. (1988) 46:149-157.
34. MYERS RF, SIEGEL MI: Differential effects of anti-inflammatory drugs on lipoxygenase and cyclo-oxygenase activities of neutrophils from a reverse passive Arthus reaction. Biochem. Biophys. Res. Commun. (1983) 112(2):586-594.
35. ARTURSSON P, SJÖHOLM I: Effect on opsonins on the macrophage uptake of polyacryl starch microparticles. Int. J. Pharm. (1986) 32:165-170.
36. ARTURSSON P, JOHANSSON D, SJÖHOLM I: Receptor-mediated uptake of starch and mannan microparticles by macrophages: relative contribution of receptors for complement, immunoglobulines and carbohydrates. Biomaterials (1988) 9:241-246.
37. MONTGOMERY PC, RAFFERTY DE: Induction of secretory and serum antibody responses following oral administration of antigen with bioadhesive degradable starch microparticles. Oral Microbiol. Immunol. (1998) 13(3):139-149.
38. ARTURSSON P, EDMAN P, SJÖHOLM I: Biodegradable microspheres II: Immune response to heterologous and autologous proteins entrapped in polyacryl starch microparticles. J. Pharm. Exp. Ther. (1985) 234:255-260.
39. STJÄRNKVIST P, DEGLING WIKINGSSON L, SJÖHOLM I: Biodegradable microspheres. XIII: Immune response to the DNP hapten conjugated to polyacryl starch microparticles. J. Pharm. Sci. (1991) 80(5):436-440.
40. DEGLING WIKINGSSON L, STJÄRNKVIST P: Biodegradable microspheres. XVIII: The adjuvant effect of polyacryl starch microparticles with conjugated human serum albumin. Vaccine (1995) 13(7):629-636.
41. WORLD HEALTH ORGANIZATION. Report on Leishmaniasis. TDR/SWG (2004)
42. BUTTON LL, REINER NE, MCMASTER WR: Modification of gp63 genes from diverse species of Leishmania for expression of recombinant protein at high levels in Escherichia coli. Mol. Biochem. Parasitol. (1991) 44(2):213-224.
43. RUSSO DM, BURNS JM Jr, CARVALHO EM et al.: Human T cell responses to gp63, a surface antigen of Leishmania. J. Immunol. (1991) 147(10):3575-3580.
44. BRADLEY DJ, KIRKLEY J: Regulation of Leishmania populations within the host. I. The variable course of Leishmania donovani infections in mice. Clin. Exp. Immunol. (1977) 30(1)119-129.
45. IIJIMA H, TAKAHASHI I, KIYONO H: Mucosal immune network in the gut for the control of infectious diseases. Rev. Med. Virol. (2001) 11(2):117-133.
46. DIDIERLAURENT A, SIRARD JC, KRAEHENBUHL JP, NEUTRA MR: How the gut senses its content. Cell Microbiol. (2002) 4(2):61-72.
47. MOWAT AM: Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. (2003) 3(4):331-341.
48. MACDONALD TT: The mucosal immune system. Parasite Immunol. (2003) 25(5):235-246.
49. NAGLER-ANDERSON C: Man the barrier! Strategic defences in the intestinal mucosa. Nat. Rev. Immunol. (2001) 1(1):59-67.
50. MCDERMOTT MR, BIENENSTOCK J: Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J. Immunol. (1979) 122(5):1892-1898.
51. PAPPO J, OWEN RL: Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology (1988) 95(5):1173-1177.
52. SMITH MW: Selective expression of brush border hydrolases by mouse Peyer's patch and jejunal villus enterocytes. J. Cell. Physiol. (1985) 124(2):219-225.
53. OWEN RL: Uptake and transport of intestinal macromolecules and microorganisms by M cells in Peyer's patches - a personal and historical perspective. Semin. Immunol. (1999) 11(3):157-163.
54. NEUTRA MR, MANTIS NJ, KRAEHENBUHL JP: Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. (2001) 2(11):1004-1009.
55. BEIER R, GEBERT A: Kinetics of particle uptake in the domes of Peyer's patches. Am. J. Physiol. (1998) 275(1 Pt 1):G130-G137.
56. SIERRO F, DUBOIS B, COSTE A et al.: Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc. Natl. Acad. Sci. USA (2001) 98(24):13722-13727.
57. RESCIGNO M, URBANO M, VALZASINA B et al.: Dendritic cells express right junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. (2001) 2(4):361-367.
58. SHAO L, SERRANO D, MAYER L: The role of epithelial cells in immune regulation in the gut. Semin. Immunol. (2001) 13(3):163-176.
59. DUCROC R, HEYMAN M, BEAUFRERE B, MORGAT JL, DESJEUX JF: Horseradish peroxidase transport across rabbit jejunum and Peyer's patches in vitro. Am. J. Physiol. (1983) 245(1):G54-58.
60. KAISERLIAN D: Epithelial cells in antigen. Sampling and presentation in mucosal tissues. Curr. Top. Microbiol. Immunol. (1999) 236:55-78.
61. WILLIAMS RC, GIBBONS RJ: Inhibition of bacterial adherence by secretory immunoglobulin A: a mechanism of antigen disposal. Science (1972) 177(50):697-699.
62. BEAGLEY KW, HUSBAND AJ: Intraepithelial lymphocytes: origins, distribution, and function. Crit. Rev. Immunol. (1998) 18(3):237-254.
63. MULLER S, BUHLER-JUNGO M, MUELLER C: Intestinal intraepithelial lymphocytes exert potent protective cytotoxic activity during an acute virus infection. J. Immunol. (2000) 164(4):1986-1994.
64. 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 (1999) 20(6):267-277.
65. KANTELE A, KANTELE JM, SAVILAHTI E et al.: Homing potentials of circulating lymphocytes in humans depend on the site of activation: oral, but not parenteral, typhoid vaccination induces circulating antibody-secreting cells that all bear homing receptors directing them to the gut. J. Immunol. (1997) 158(2):574-579.
66. KANTELE A, HÄKKINEN M, MOLDOVEANU Z et al.: Differences in immune responses induced by oral and rectal immunizations with Salmonella typhi Ty21a: Evidence for compartmentalization within the common mucosal immune system in humans. Infect. Immun. (1998) 66(12):5630-5635.
67. QUIDING-JÄRBRINK M, NORDSTRÖM I, GRANSTRÖM G et al.: Differential expression of tissue-specific adhesion molecules on human circulating antibody-forming cells after systemic, enteric, and nasal immunizations. A molecular basis for the compartmentalization of effector B cell responses. J. Clin. Invest. (1997) 99(6):1281-1286.
68. QUIDING-JÄRBRINK M, LAKEW M, NORDSTRÖM I et al.: Human circulating specific antibody-forming cells after systemic and mucosal immunizations: differential homing commitments and cell surface differentiation markers. Eur. J. Immunol. (1995) 25(2):322-327.
69. SONODA E, MATSUMOTO R, HITOSHI Y et al.: Transforming growth factor beta induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med. (1989) 170(4):1415-1420.
70. LEBMAN DA, NOMURA DY, COFFMAN RL, LEE FD: Molecular characterization of germ-line immunoglobulin A transcripts produced during transforming growth factor type beta-induced isotype switching. Proc. Natl. Acad. Sci. USA (1990) 87(10):3962-3966.
71. WEINSTEIN PD, CEBRA JJ: The preference for switching to IgA expression by Peyer's patch germinal center B cells is likely due to the intrinsic influence of their microenvironment. J. Immunol. (1991) 147(12):4126-4135.
72. WEINSTEIN PD, SCHWEITZER PA, CEBRA-THOMAS JA, CEBRA JJ: Molecular genetic features reflecting the preference for isotype switching to IgA expression by Peyer's patch germinal center B cells. Int. Immunol. (1991) 3(12):1253-1263.
73. HARRIMAN GR, KUNIMOTO DY, ELLIOTT JF, PAETKAU V, STROBER W: The role of IL-5 in IgA B cell differentiation. J. Immunol. (1988) 140(9):3033-3039.
74. BEAGLEY KW, ELDRIDGE JH, KIYONO H et al.: Recombinant murine IL-5 induces high rate IgA synthesis in cycling IgA-positive Peyer's patch B cells. J. Immunol. (1988) 141(6):2035-2042.
75. BEAGLEY KW, ELDRIDGE JH, LEE F et al.: Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committed B cells. J. Exp. Med. (1989) 169(6):2133-2148.
76. DEFRANCE T, VANBERVLIET B, BRIERE F et al.: Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naïve human B cells to secrete immunoglobulin A. J. Exp. Med. (1992) 175(3):671-682.
77. HERSHEY GK: IL-13 receptors and signaling pathways: an evolving web. J. Allergy Clin. Immunol. (2003) 111(4):677-690; quiz 691.
78. H2 cells in murine gut-associated tissues. Frequencies of CD4+ and CD8+ T cells that secrete IFN-gamma and IL-5. J. Immunol. (1990) 145(1):68-77.
79. BAO S, GOLDSTONE S, HUSBAND AJ: Localization of IFN-gamma and IL-6 mRNA in murine intestine by in situ hybridization. Immunology (1993) 80(4):666-670.
80. MACPHERSON G, KUSHNIR N, WYKES M: Dendritic cells, B cells and the regulation of antibody synthesis. Immunol. Rev. (1999) 172:325-334.
81. KUNKEL D, KIRCHHOFF D, NISHIKAWA S, RADBRUCH A, SCHEFFOLD A: Visualization of peptide presentation following oral application of antigen in normal and Peyer's patches-deficient mice. Eur. J. Immunol. (2003) 33(5):1292-1301.
82. ANJUERE F, LUCI C, LEBENS M et al.: In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J Immunol. (2004) 173(8):5103-5111.
83. H3-type TGF-beta-secreting regulatory cells. Microbes Infect. (2001) 3(11):947-954.
84. RONCAROLO MG, BACCHETTA R, BORDIGNON C, NARULA S, LEVINGS MK: Type 1 T regulatory cells. Immunol. Rev. (2001) 182:68-79.
85. IWASAKI A, KELSALL BL: Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper Type 2 cells. J. Exp. Med. (1999) 190(2):229-239.
86. AKBARI O, DEKRUYFF RH, UMETSU DT: Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. (2001) 2(8):725-731.
87. KELSALL BL, STROBER W: Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyer's patch. J. Exp. Med. (1996) 183(1):237-247.
88. IWASAKI A, KELSALL BL: Mucosal immunity and inflammation. I. Mucosal dendritic cells: their specialized role in initiating T cell responses. Am. J. Physiol. (1999) 276(5 Pt 1):G1074-G1078.
89. IWASAKI A, KELSALL BL: Localization of distinct Peyer's patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3alpha, MIP-3beta, and secondary lymphoid organ chemokine. J. Exp. Med. (2000) 191(8):1381-1394.
90. IWASAKI A, KELSALL BL: Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer's patch dendritic cells. J. Immunol. (2001) 166(8):4884-4890.
91. JANEWAY CA, JR, MEDZHITOV R: Innate immune recognition. Ann. Rev. Immunol. (2002) 20:197-216.
92. LAVELLE EC, SHARIF S, THOMAS NW, HOLLAND J, DAVIS SS: The importance of gastrointestinal uptake of particles in the design of oral delivery systems. Adv. Drug Deliv. Rev. (1995) 18:5-22.
93. NORRIS DA, PURI N, SINKO PJ: The effect of physical barriers and properties on the oral absorption of particulates. Adv. Drug Deliv. Rev. (1998) 34(2-3):135-154.
94. CHEN H, LANGER R: Oral particulate delivery: status and future trends. Adv. Drug Deliv. Rev. (1998) 34(2-3):339-350.
95. HUSSAIN N, JAITLEY V, FLORENCE AT: Recent advances in the understanding of uptake of microparticulates across the gastrointestinal lymphatics. Adv. Drug Deliv. Rev. (2001) 50(1-2):107-142.
96. JEPSON MA, CLARK MA, HIRST BH: M cell targeting by lectins: a strategy for mucosal vaccination and drug delivery. Adv. Drug Deliv. Rev. (2004) 56(4):511-525.
97. JANI P, HALBERT GW, LANGRIDGE J, FLORENCE AT: The uptake and translocation of latex nanospheres and microspheres after oral administration to rats. J. Pharm. Pharmacol. (1989) 41(12):809-812.
98. 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(12):821-826.
99. DESAI MP, LABHASETWAR V, AMIDON GL, LEVY RJ: Gastrointestinal uptake of biodegradable microparticles: effect of particle size. Pharm. Res. (1996) 13(12):1838-1845.
100. ERMAK TH, DOUGHERTY EP, BHAGAT HR, KABOK Z, PAPPO J: Uptake and transport of copolymer biodegradable microspheres by rabbit Peyer's patch M cells. Cell Tissue Res. (1995) 279(2):433-436.
101. LEFEVRE ME, HANCOCK DC, JOEL DD: Intestinal barrier to large particulates in mice. J. Toxicol. Environ. Health (1980) 6(4):691-704.
102. EBEL JP: A method for quantifying particle absorption from the small intestine of the mouse. Pharm. Res. (1990) 7(8):848-851.
103. ELDRIGE JH, HAMMOND CJ, MEULBROEK JA et al.: Controlled vaccine release in the gut-associated lymphoid tissue. I. Orally administered biodegradable microspheres target the Peyer's patches. J. Control. Release (1990) 11:205-214.
104. JUNG T, KAMM W, BREITENBACH A et al.: Biodegradable nanoparticles for oral delivery of peptides: Is there a role for polymers to affect mucosal uptake? Eur. J. Pharm. Biopharm. (2000) 50(1):147-160.
105. DELIE F: Evaluation of nano- and microparticle uptake by the gastrointestinal tract. Adv. Drug Deliv. Rev. (1998) 34(2-3):221-233.
106. LARHED A, STERTMAN L, EDVARDSSON E, SJÖHOLM I: Starch microparticles as oral vaccine adjuvant: antigen-dependent uptake in mouse intestinal mucosa. J. Drug Target. (2004) 12(5):289-296.
107. GIANNASCA PJ, GIANNASCA KT, FALK P, GORDON JI, NEUTRA MR: Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccines. Am. J. Physiol. (1994) 267(6 Pt 1):G1108-G1121.
108. FREY A, GIANNASCA KT, WELTZIN R et al.: Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells: implications for microbial attachment and oral vaccine targeting. J. Exp. Med. (1996) 184(3):1045-1059.
109. ÖSTH K, STRINDELIUS L, LARHED A et al.: Uptake of ovalbumin-conjugated starch microparticles by pig respiratory nasal mucosa in vitro. J. Drug Target. (2003) 11(1):75-82.
110. HUSSAIN N, JANI PU, FLORENCE AT: Enhanced oral uptake of tomato lectin-conjugated nanoparticles in the rat. Pharm. Res. (1997) 14(5):613-618.
111. GRDIC D, SMITH R, DONACHIE A et al.: The mucosal adjuvant effects of cholera toxin and immune-stimulating complexes differ in their requirement for IL-12, indicating different pathways of action. Eur. J. Immunol. (1999) 29(6):1774-1784.
112. O'HAGAN DT, RAFFERTY D, WHARTON S, ILLUM L: Intravaginal immunization in sheep using a bioadhesive microsphere antigen delivery system. Vaccine (1993) 11(6):660-664.
113. ILLUM L, FARRAJ NF, CRITCHLEY H, DAVIS SS: Nasal administration of gentamicin using a novel microsphere delivery system. Int. J. Pharm. (1988) 46:261-265.
114. FARRAJ NF, JOHANSEN BR, DAVIS SS, ILLUM L: Nasal administration of insulin using bioadhesive microspheres as a delivery system. J. Control Release (1990) 13:253-261.
115. BJÖRK E, EDMAN P: Characterization of degradable starch microspheres as a nasal delivery system for drugs. Int. J. Pharm. (1990) 62:187-192.
116. BJÖRK E, ISAKSSON U, EDMAN P, ARTURSSON P: Starch microspheres induce pulsatile delivery of drugs and peptides across the epithelial barrier by reversible separation of the tight junctions. J. Drug Target. (1995) 2(6):501-507.
117. HOLMBERG K, BJÖRK E, BAKE B, EDMAN P: Influence of degradable starch microspheres on the human nasal mucosa. Rhinology (1994) 32(2):74-77.
118. AGGERBECK H, GIZURARSON S, WANTZIN J, HERON I: Intranasal booster vaccination against diphtheria and tetanus in man. Vaccine (1997) 15(3):307-316.
119. MILLS KH, COSGROVE C, MCNEELA EA et al.: Protective levels of diphtheria-neutralizing antibody induced in healthy volunteers by unilateral priming-boosting intranasal immunization associated with restricted ipsilateral mucosal secretory immunoglobulin A. Infect. Immun. (2003) 71(2):726-732.
120. H2 responses following nasal delivery. Vaccine (2001) 19(9-10):1188-1198.
121. H2 responses and toxin-neutralizing antibodies by formulation with chitosan. Vaccine (2004) 22(8):909-914.
122. RYDELL N, SJÖHOLM I: Mucosal vaccination against diphtheria using starch microparticles as adjuvant for cross-reacting material (CRM197) of diphtheria toxin. Vaccine (2005) 23:2775-2783.
123. STERTMAN L, STRINDELIUS L, SJÖHOLM I: Starch microparticles as an adjuvant in immunisation: effect of route of administration on the immune response in mice. Vaccine (2004) 22(21-22):2863-2872.
124. H1 clones. J. Immunol. (1987) 138(11):3688-3694.
125. PURKERSON JM, ISAKSON PC: Interleukin 5 (IL-5) provides a signal that is required in addition to IL-4 for isotype switching to immunoglobulin (Ig) G1 and IgE. J. Exp. Med. (1992) 175(4):973-982.
126. LIEW FY: T(H)1 and T(H)2 cells: A historical perspective. Nature Rev. Immunol. (2002) 2(1):55-60.
127. STERTMAN L: Starch microparticles as an oral vaccine adjuvant with emphasis on the differentiation of the immune response (Thesis). Uppsala, Sweden (2004).
128. HERSHBERG RM, CHO DH, YOUAKIM A et al.: Highly polarized HLA class II antigen processing and presentation by human intestinal epithelial cells. J. Clin. Invest. (1998) 102(4):792-803.
129. SANDERSON IR, OUELLETTE AJ, CARTER EA, WALKER WA, HARMATZ PR: Differential regulation of B7 mRNA in enterocytes and lymphoid cells. Immunology (1993) 79(3):434-438.
130. HERSHBERG RM, FRAMSON PE, CHO DH et al.: Intestinal epithelial cells use two distinct pathways for HLA class II antigen processing. J. Clin. Invest. (1997) 100(1):204-215.
131. + T cell down-regulation in human intestinal mucosa: evidence for intestinal tolerance to luminal bacterial antigens. J. Immunol. (1997) 158(8):3626-3634.
132. ANDERSEN P, ASKGAARD D, LJUNGQVIST L, BENTZON MW, HERON I: T-cell proliferative response to antigens secreted by Mycobacterium tuberculosis. Infect. Immun. (1991) 59(4):1558-1563.
133. PAL PG, HORWITZ MA: Immunization with extracellular proteins of Mycobacterium tuberculosis induces cell-mediated immune responses and substantial protective immunity in a guinea pig model of pulmonary tuberculosis. Infect. Immun. (1992) 60(11):4781-4792.
134. STRINDELIUS L, DEGLING WIKINGSSON L, SJÖHOLM I: Extracellular antigens from Salmonella enteritidis induce effective immune response in mice after oral vaccination. Infect. Immun. (2002) 70(3):1434-1442.
135. STRINDELIUS L, FILLER M, SJÖHOLM I: Mucosal immunization with purified flagellin from Salmonella induces systemic and mucosal immune responses in C3H/HeJ mice. Vaccine (2004) 22(27-28):3797-3808.
136. STRINDELIUS L, FOLKESSON A, NORMARK S, SJÖHOLM I: Immunogenic properties of the Salmonella atypical fimbriae in BALB/c mice. Vaccine (2004) 22(11-12):1448-1456.
137. GEWIRTZ AT, NAVAS TA, LYONS S, GODOWSKI PJ, MADARA JL: Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. (2001) 167(4):1882-1885.
138. BUTLER JE, LU EP, NAVARRO P, CHRISTIANSEN B: The absorption of proteins on a polydimethylsiloxane edastomer (PEP) and their antigenic behaviours. In: Immunology of Silicones. M Potler, NR Rose (Eds.), Springer-Verlag, Berlin, Germany: (1996):75-84.
139. HERITAGE PL, UNDERDOWN BJ, BROOK MA, MCDERMOTT MR: Oral administration of polymer-grafted starch microparticles activates gut-associated lymphocytes and primes mice for a subsequent systemic antigen challenge. Vaccine (1998) 16(20):2010-2017.
140. GRIFFITH AH: The role of immunization in the control of diphtheria. Dev. Biol. Stand. (1979) 43:3-13.
141. IPSEN J: Circulating antitoxin at the onset of diphtheria in 425 patients. Dev. Biol. Stand. (1946) 54:325-447.
142. CHRISTENSON B, HELLSTRÖM U, SYLVAN SP, HENRIKSSON L, GRANSTRÖM M: Impact of a vaccination campaign on adult immunity to diphtheria. Vaccine (2000) 19(9-10):1133-1140.
143. CROSSLEY K, IRVINE P, WARREN JB, LEE BK, MEAD K: Tetanus and diphtheria immunity in urban Minnesota adults. JAMA (1979) 242(21):2298-2300.
144. CELLESI C, ZANCHI A, MICHELANGELI C et al.: Immunity to diphtheria in a sample of adult population from central Italy. Vaccine (1989) 7(5):417-420.
145. GALAZKA AM, ROBERTSON SE: Immunization against diphtheria with special emphasis on immunization of adults. Vaccine (1996) 14(9):845-857.
146. MASTERTON RG, TETTMAR RE, PILE RL, JONES J, CROFT KF: Immunity to diphtheria in young British adults. J. Infect. (1987) 15(1):27-32.
147. New generation vaccines. MM Levine, GC Woodrow, JB Kaper, GS Cobon (Eds.), Marcel Dekker, NY, USA (1997).
148. GUPTA RK, RELYVELD EH, LINDBLAD EB et al.: Adjuvants - a balance between toxicity and adjuvanticity. Vaccine (1993) 11(3):293-306.
149. PAPPENHEIMER AM, JR, UCHIDA T, HARPER AA: An immunological study of the diphtheria toxin molecule. Immunochemistry (1972) 9(9):891-906.
150. PETRE J, PIZZA M, NENCIONI L et al.: The reaction of bacterial toxins with formaldehyde and its use for antigen stabilization. Dev. Biol. Stand (1996) 87:125-134.
151. METZ B, KERSTEN GF, HOOGERHOUT P et al.: Identification of formaldehyde-induced modifications in proteins: reactions with model peptides. J. Biol. Chem. (2004) 279(8):6235-6243.
152. RYDELL N, SJÖHOLM I: Oral vaccination against diphtheria using polyacryl starch microparticles as adjuvant. Vaccine (2004) 22(9-10):1265-1274.
153. PORRO M, SALETTI M, NENCIONI L, TAGLIAFERRI L, MARSILI I: Immunogenic correlation between cross-reacting material (CRM197) produced by a mutant of Corynebacterium diphtheriae and diphtheria toxoid. J. Infect. Dis. (1980) 142(5):716-724.
154. MIYAMURA K, SHIGEKO N, ITO A, MURATA R, KONO R: Micro cell culture method for determination of diphtheria toxin and antitoxin titers using VERO cells. J. Biol. Stand. (1974) 2:189-201.
155. VAN KRUININGEN HJ, WEST AB, FREDA BJ, HOLMES KA: Distribution of Peyer's patches in the distal ileum. Inflamm. Bowel Dis. (2002) 8(3):180-185.
156. MICHETTI P, MAHAN MJ, SLAUCH JM, MEKALANOS JJ, NEUTRA MR: Monoclonal secretory immunoglobulin A protects mice against oral challenge with the invasive pathogen Salmonella typhimurium. Infect. Immun. (1992) 60(5):1786-1792.
157. WINNER 3RD L, MACK J, WELTZIN R et al.: New model for analysis of mucosal immunity: intestinal secretion of specific monoclonal immunoglobulin A from hybridoma tumors protects against Vibrio cholerae infection. Infect. Immun. (1991) 59(3):977-982.