Co-administration of cholera toxin and apple polyphenol extract as a novel and safe mucosal adjuvant strategy

Vaccine

Volumn 27, Issue 35, 2009, Pages 4808-4817

  Yoshino, Naoto ^a   Fujihashi, Kohtaro ^b   Hagiwara, Yukari ^c   Kanno, Hiroyuki ^a   Takahashi, Kiyomi ^a   Kobayashi, Ryoki ^b   Inaba, Noriyuki ^d   Noda, Masatoshi ^e   Sato, Shigehiro ^a  

^a IWATE MEDICAL UNIVERSITY   (Japan)

^b Departments of Pediatric Dentistry and Microbiology   (United States)

^c KITASATO INSTITUTE   (Japan)

^d DOKKYO MEDICAL UNIVERSITY   (Japan)

^e CHIBA UNIVERSITY   (Japan)

Author keywords

Apple polyphenol extract; Cholera toxin; Mucosal adjuvant

Indexed keywords

CHOLERA TOXIN; CYCLIC AMP; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 1BETA; INTERLEUKIN 6; OVALBUMIN; POLYPHENOL DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; APPLE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG ACCUMULATION; DRUG MEGADOSE; HISTOPATHOLOGY; IMMUNOGENICITY; LOW DRUG DOSE; MOUSE; NONHUMAN; NOSE MUCOSA; OLFACTORY EPITHELIUM; OLFACTORY NERVE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VACCINE PRODUCTION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODY FORMATION; CHLOROGENIC ACID; CHOLERA TOXIN; FLAVONOIDS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN E; MICE; MICE, INBRED C57BL; OVALBUMIN; TANNINS;

EID: 67650266243     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.05.081     Document Type: Article

References (63)

1. Elson C.O., and Ealding W. Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J Immunol 132 6 (1984) 2736-2741
2. Clements J.D., Hartzog N.M., and Lyon F.L. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 6 3 (1988) 269-277
3. Yamamoto S., Kiyono H., Yamamoto M., Imaoka K., Fujihashi K., van Ginkel F.W., et al. A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc Natl Acad Sci USA 94 10 (1997) 5267-5272
4. Rowe B., Taylor J., and Bettelheim K.A. An investigation of traveller's diarrhoea. Lancet 1 7636 (1970) 1-5
5. Sack R.B., Gorbach S.L., Banwell J.G., Jacobs B., Chatterjee B.D., and Mitra R.C. Enterotoxigenic Escherichia coli isolated from patients with severe cholera-like disease. J Infect Dis 123 4 (1971) 378-385
6. Gorbach S.L., and Khurana C.M. Escherichia coli: a cause of infantile diarrhea in Chicago. N Engl J Med 287 16 (1972) 791-795
7. Spangler B.D. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 56 4 (1992) 622-647
8. Dickinson B.L., and Clements J.D. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect Immun 63 5 (1995) 1617-1623
9. Glück R., Mischler R., Durrer P., Fürer E., Lang A.B., Herzog C., et al. Safety and immunogenicity of intranasally administered inactivated trivalent virosome-formulated influenza vaccine containing Escherichia coli heat-labile toxin as a mucosal adjuvant. J Infect Dis 181 3 (2000) 1129-1132
10. Glück U., Gebbers J.O., and Glück R. Phase 1 evaluation of intranasal virosomal influenza vaccine with and without Escherichia coli heat-labile toxin in adult volunteers. J Virol 73 9 (1999) 7780-7786
11. Glueck R. Pre-clinical and clinical investigation of the safety of a novel adjuvant for intranasal immunization. Vaccine 20 Suppl 1 (2001) S42-S44
12. Mutsch M., Zhou W., Rhodes P., Bopp M., Chen R.T., Linder T., et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. N Engl J Med 350 9 (2004) 896-903
13. Lee A., and Chen M. Successful immunization against gastric infection with helicobacter species: use of a cholera toxin B-subunit-whole-cell vaccine. Infect Immun 62 8 (1994) 3594-3597
14. Tamura S., Samegai Y., Kurata H., Nagamine T., Aizawa C., and Kurata T. Protection against influenza virus infection by vaccine inoculated intranasally with cholera toxin B subunit. Vaccine 6 5 (1998) 409-413
15. Yamamoto S., Takeda Y., Yamamoto M., Kurazono H., Imaoka K., Yamamoto M., et al. Mutants in the ADP-ribosyltransferase cleft of cholera toxin lack diarrheagenicity but retain adjuvanticity. J Exp Med 185 7 (1997) 1203-1210
16. Hagiwara Y., Kawamura Y.I., Kataoka K., Rahima B., Jackson R.J., Komase K., et al. A second generation of double mutant cholera toxin adjuvants: enhanced immunity without intracellular trafficking. J Immunol 177 5 (2006) 3045-3054
17. Yoshino N., Lü F.X., Fujihashi K., Hagiwara Y., Kataoka K., Lu D., et al. A novel adjuvant for mucosal immunity to HIV-1 gp120 in nonhuman primates. J Immunol 173 11 (2004) 6850-6857
18. Agren L.C., Ekman L., Lowenadler B., Nedrud J.G., and Lycke N.Y. Adjuvanticity of the cholera toxin A1-based gene fusion protein, CTA1-DD, is critically dependent on the ADP-ribosyltransferase and Ig-binding activity. J Immunol 162 4 (1999) 2432-2440
19. Lycke N., and Schon K. The B cell targeted adjuvant, CTA1-DD, exhibits potent mucosal immunoenhancing activity despite pre-existing anti-toxin immunity. Vaccine 19 17-19 (2001) 2542-2548
20. Eriksson A.M., Schön K.M., and Lycke N.Y. The cholera toxin-derived CTA1-DD vaccine adjuvant administered intranasally does not cause inflammation or accumulate in the nervous tissues. J Immunol 173 5 (2004) 3310-3319
21. Bowman C.C., and Clements J.D. Differential biological and adjuvant activities of cholera toxin and Escherichia coli heat-labile enterotoxin hybrids. Infect Immun 69 3 (2001) 1528-1535
22. Boyaka P.N., Ohmura M., Fujihashi K., Koga T., Yamamoto M., Kweon M.N., et al. Chimeras of labile toxin one and cholera toxin retain mucosal adjuvanticity and direct Th cell subsets via their B subunit. J Immunol 170 1 (2003) 454-462
23. Kweon M.N., Yamamoto M., Watanabe F., Tamura S., van Ginkel F.W., Miyauchi A., et al. A nontoxic chimeric enterotoxin adjuvant induces protective immunity in both mucosal and systemic compartments with reduced IgE antibodies. J Infect Dis 186 9 (2002) 1261-1269
24. Saito T., Miyake M., Toba M., Okamatsu H., Shimizu S., and Noda M. Inhibition by apple polyphenols of ADP-ribosyltransferase activity of cholera toxin and toxin-induced fluid accumulation in mice. Microbiol Immunol 46 4 (2002) 249-255
25. Morinaga N., Iwamaru Y., Yahiro K., Tagashira M., Moss J., and Noda M. Differential activities of plant polyphenols on the binding and internalization of cholera toxin in vero cells. J Biol Chem 280 24 (2005) 23303-23309
26. Shoji T., Akazome Y., Kanda T., and Ikeda M. The toxicology and safety of apple polyphenol extract. Food Chem Toxicol 42 6 (2004) 959-967
27. Kojima T., Akiyama H., Sasai M., Taniuchi S., Goda Y., Toyoda M., et al. Anti-allergic effect of apple polyphenol on patients with atopic dermatitis: a pilot study. Allergol Int 49 1 (2000) 69-73
28. Kanda T., Akiyama H., Yanagida A., Tanabe M., Goda Y., Toyoda M., et al. Inhibitory effects of apple polyphenol on induced histamine release from RBL-2H3 cells and rat mast cells. Biosci Biotechnol Biochem 62 7 (1998) 1284-1289
29. Donta S.T., Moon H.W., and Whipp S.C. Detection of heat-labile Escherichia coli enterotoxin with the use of adrenal cells in tissue culture. Science 183 122 (1974) 334-336
30. + T cells in nasopharyngeal-associated lymphoreticular tissue. J Immunol 170 4 (2003) 1754-1762
31. Yamamoto M., Briles D.E., Yamamoto S., Ohmura M., Kiyono H., and McGhee J.R. A nontoxic adjuvant for mucosal immunity to pneumococcal surface protein A. J Immunol 161 8 (1998) 4115-4121
32. Tamura S., Miyata K., Matsuo K., Asanuma H., Takahashi H., Nakajima K., et al. Acceleration of influenza virus clearance by Th1 cells in the nasal site of mice immunized intranasally with adjuvant-combined recombinant nucleoprotein. J Immunol 156 10 (1996) 3892-3900
33. van Ginkel F.W., Jackson R.J., Yuki Y., and McGhee J.R. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 165 9 (2000) 4778-4782
34. Takahashi K., Funata N., Ikuta F., and Sato S. Neuronal apoptosis and inflammatory responses in the central nervous system of a rabbit treated with Shiga toxin-2. J Neuroinflamm 5 (2008) 11
35. Miller S.A., Morton M.S., and Turkes A. Chemiluminescence immunoassay for progesterone in plasma incorporating acridinium ester labelled antigen. Ann Clin Biochem 25 1 (1988) 27-34
36. Wu H.Y., and Russell M.W. Induction of mucosal immunity by intranasal application of a streptococcal surface protein antigen with the cholera toxin B subunit. Infect Immun 61 1 (1993) 314-322
37. Moldoveanu Z., and Fujihashi K. Collection and processing of external secretions and tissues of mouse origin. In: Mestecky J., Lamm M.E., McGhee J.R., Bienenstock J., Mayer L., and Strober W. (Eds). Mucosal immunology. 3rd ed. (2005), Academic Press, San Diego 1841-1852
38. Guerrant R.L., Brunton L.L., Schnaitman T.C., Rebhun L.I., and Gilman A.G. Cyclic adenosine monophosphate and alteration of Chinese hamster ovary cell morphology: a rapid, sensitive in vitro assay for the enterotoxins of Vibrio cholerae and Escherichia coli. Infect Immun 10 2 (1974) 320-327
39. van Ginkel F.W., Jackson R.J., Yoshino N., Hagiwara Y., Metzger D.J., Connell T.D., et al. Enterotoxin-based mucosal adjuvants alter antigen trafficking and induce inflammatory responses in the nasal tract. Infect Immun 73 10 (2005) 6892-6902
40. Ohnishi-Kameyama M., Yanagida A., Kanda T., and Nagata T. Identification of catechin oligomers from apple (Malus pumila cv. Fuji) in matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and fast-atom bombardment mass spectrometry. Rapid Commun Mass Spectrom 11 1 (1997) 31-36
41. Kawamura Y.I., Kawashima R., Shirai Y., Kato R., Hamabata T., Yamamoto M., et al. Cholera toxin activates dendritic cells through dependence on GM1-ganglioside which is mediated by NF-κB translocation. Eur J Immunol 33 11 (2003) 3205-3212
42. Krakauer T. Evidence for protein kinase C pathway in the response of human peripheral blood mononuclear cells to cholera toxin. Cell Immunol 172 2 (1996) 224-228
43. Schmidt H.W.H., and Neukom H. Identification of the main oligomeric proanthocyanidin occurring in apples. J Agric Food Chem 17 2 (1969) 344-346
44. Wilson E.L. High-pressure liquid chromatography of apple juice phenolic compounds. J Sci Food Agric 32 3 (1981) 257-264
45. Bohuon G., Baron A., and Drilleau J.F. High-performance liquid chromatography of the phenolic compounds in the juice of some French cider apple varieties. J Chromatogr 555 1-2 (1991) 125-136
46. Suárez Vallés B., Santamaría Victorero J., Mangas Alonso J.J., and Blanco Gomis D. High-performance liquid chromatography of the neutral phenolic compounds of low molecular weight in apple juice. J Agric Food Chem 42 12 (1994) 2732-2736
47. Enomoto T., Nagasako-Akazome Y., Kanda T., Ikeda M., and Dake Y. Clinical effects of apple polyphenols on persistent allergic rhinitis: a randomized double-blind placebo-controlled parallel arm study. J Invest Allergol Clin Immunol 16 5 (2006) 283-289
48. Yoon H., and Liu R.H. Effect of selected phytochemicals and apple extracts on NF-κB activation in human breast cancer MCF-7 cells. J Agric Food Chem 55 8 (2007) 3167-3173
49. Davis P.A., Polagruto J.A., Valacchi G., Phung A., Soucek K., Keen C.L., et al. Effect of apple extracts on NF-κB activation in human umbilical vein endothelial cells. Exp Biol Med 231 5 (2006) 594-598
50. Hutchinson A., Taper C.D., and Towers G.H. Studies of phloridzin in Malus. Can J Biochem Physiol 37 3 (1959) 901-910
51. Shoji T., Kobori M., Shinmoto H., Tanabe M., and Tsushida T. Progressive effects of phloridzin on melanogenesis in B16 mouse melanoma cells. Biosci Biotechnol Biochem 61 12 (1997) 1963-1967
52. Kern M., Pahlke G., Balavenkatraman K.K., Böhmer F.D., and Marko D. Apple polyphenols affect protein kinase C activity and the onset of apoptosis in human colon carcinoma cells. J Agric Food Chem 55 13 (2007) 4999-5006
53. Polya G.M., Wang B.H., and Foo L.Y. Inhibition of signal-regulated protein kinases by plant-derived hydrolysable tannins. Phytochemistry 38 2 (1995) 307-314
54. Wang B.H., Foo L.Y., and Polya G.M. Differential inhibition of eukaryote protein kinases by condensed tannins. Phytochemistry 43 2 (1996) 359-365
55. Zhu M., Phillipson J.D., Greengrass P.M., Bowery N.E., and Cai Y. Plant polyphenols: biologically active compounds or non-selective binders to protein?. Phytochemistry 44 3 (1997) 441-447
56. Kelso J.M., Jones R.T., and Yunginger J.W. Anaphylaxis to measles, mumps, and rubella vaccine mediated by IgE to gelatin. J Allergy Clin Immunol 91 4 (1993) 867-872
57. Sakaguchi M., Ogura H., and Inouye S. IgE antibody to gelatin in children with immediate-type reactions to measles and mumps vaccines. J Allergy Clin Immunol 96 4 (1995) 563-565
58. Kumagai T., Yamanaka T., Wataya Y., Umetsu A., Kawamura N., Ikeda K., et al. Gelatin-specific humoral and cellular immune responses in children with immediate- and nonimmediate-type reactions to live measles, mumps, rubella, and varicella vaccines. J Allergy Clin Immunol 100 1 (1997) 130-134
59. Simecka J.W., Jackson R.J., Kiyono H., and McGhee J.R. Mucosally induced immunoglobulin E-associated inflammation in the respiratory tract. Infect Immun 68 2 (2000) 672-679
60. Tokura T., Nakano N., Ito T., Matsuda H., Nagasako-Akazome Y., Kanda T., et al. Inhibitory effect of polyphenol-enriched apple extracts on mast cell degranulation in vitro targeting the binding between IgE and FcεRI. Biosci Biotechnol Biochem 69 10 (2005) 1974-1977
61. Akiyama H., Sakushima J., Taniuchi S., Kanda T., Yanagida A., Kojima T., et al. Antiallergic effect of apple polyphenols on the allergic model mouse. Biol Pharm Bull 23 11 (2000) 1370-1373
62. Gizurarson S., Tamura S., Aizawa C., and Kurata T. Stimulation of the transepithelial flux of influenza HA vaccine by cholera toxin B subunit. Vaccine 10 2 (1992) 101-106
63. Hagiwara Y., Tsuji T., Iwasaki T., Kadowaki S., Asanuma H., Chen Z., et al. Effectiveness and safety of mutant Escherichia coli heat-labile enterotoxin (LT H44A) as an adjuvant for nasal influenza vaccine. Vaccine 19 15-16 (2001) 2071-2079