Prevention of allergic asthma by vaccination with transgenic rice seed expressing mite allergen: Induction of allergen-specific oral tolerance without bystander suppression

Plant Biotechnology Journal

Volumn 9, Issue 9, 2011, Pages 982-990

  Suzuki, Kazuya ^a,b   Kaminuma, Osamu ^b   Yang, Lijun ^a   Takai, Toshiro ^c   Mori, Akio ^d   Umezu Goto, Makiko ^d   Ohtomo, Takayuki ^d   Ohmachi, Yasushi ^e   Noda, Yuko ^e   Hirose, Sakiko ^a   Okumura, Ko ^c   Ogawa, Hideoki ^c   Takada, Kazuko ^f   Hirasawa, Masatomo ^f   Hiroi, Takachika ^b   Takaiwa, Fumio ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d SAGAMIHARA NATIONAL HOSPITAL   (Japan)

^e NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^f NIHON UNIVERSITY   (Japan)

Author keywords

Bronchial asthma; Bystander suppression; Edible vaccine; House dust mite; Immunotherapy; Transgenic plant

Indexed keywords

ARTHROPOD PROTEIN; CYSTEINE PROTEINASE; DERMATOPHAGOIDES PTERONYSSINUS ANTIGEN P 1; EDIBLE VACCINE; EPITOPE; HOUSE DUST ALLERGEN; IMMUNOGLOBULIN E; SUBUNIT VACCINE;

ANIMAL; ANTIBODY PRODUCTION; ARTICLE; ASTHMA; BAGG ALBINO MOUSE; BYSTANDER EFFECT; CELL PROLIFERATION; CELLULAR IMMUNITY; DESENSITIZATION; FEMALE; GENETICS; HUMAN; IMMUNOLOGY; LUNG; METABOLISM; MOUSE; PATHOLOGY; PLANT SEED; PLASMID; PYROGLYPHIDAE; RICE; TRANSGENIC PLANT; VACCINATION;

ANIMALS; ANTIBODY FORMATION; ANTIGENS, DERMATOPHAGOIDES; ARTHROPOD PROTEINS; ASTHMA; BYSTANDER EFFECT; CELL PROLIFERATION; CYSTEINE ENDOPEPTIDASES; DESENSITIZATION, IMMUNOLOGIC; EPITOPES, T-LYMPHOCYTE; FEMALE; HUMANS; IMMUNITY, CELLULAR; IMMUNOGLOBULIN E; LUNG; MICE; MICE, INBRED BALB C; ORYZA SATIVA; PLANTS, GENETICALLY MODIFIED; PLASMIDS; PYROGLYPHIDAE; SEEDS; VACCINATION; VACCINES, EDIBLE; VACCINES, SUBUNIT;

ACARI; DERMATOPHAGOIDES; MUS; PYROGLYPHIDAE;

EID: 79953730113     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/j.1467-7652.2011.00613.x     Document Type: Article

References (43)

1. Carvalho, C.R., Verdolin, B.A. and Vaz, N.M. (1997) Indirect effects of oral tolerance cannot be ascribed to bystander suppression. Scand. J. Immunol. 45, 276-281.
2. Chen, Y., Kuchroo, V.K., Inobe, J., Hafler, D.A. and Weiner, H.L. (1994) Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science, 265, 1237-1240.
3. Chen, Y., Inobe, J., Marks, R., Gonnella, P., Kuchroo, V.K. and Weiner, H.L. (1995) Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature, 376, 177-180.
4. Chua, K.Y., Stewart, G.A., Thomas, W.R., Simpson, R.J., Dilworth, R.J., Plozza, T.M. and Turner, K.J. (1988) Sequence analysis of cDNA coding for a major house dust mite allergen, Der p 1. Homology with cysteine proteases. J. Exp. Med. 167, 175-182.
5. Faria, A.M. and Weiner, H.L. (2006) Oral tolerance and TGF-beta-producing cells. Inflamm. Allergy Drug Targets, 5, 179-190.
6. Friedman, A. and Weiner, H.L. (1994) Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc. Natl Acad. Sci. USA, 91, 6688-6692.
7. Geha, R.S., Jabara, H.H. and Brodeur, S.R. (2003) The regulation of immunoglobulin E class-switch recombination. Nat. Rev. Immunol. 3, 721-732.
8. Goto, F., Yoshihara, T., Shigemoto, N., Toki, S. and Takaiwa, F. (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat. Biotechnol. 17, 282-286.
9. Gough, L., Schulz, O., Sewell, H.F. and Shakib, F. (1999) The cysteine protease activity of the major dust mite allergen Der p 1 selectively enhances the immunoglobulin E antibody response. J. Exp. Med.190, 1897-1902.
10. Hiroi, T. and Takaiwa, F. (2006) Peptide immunotherapy for allergic diseases using a rice-based edible vaccine. Curr. Opin. Allergy Clin. Immunol. 6, 455-460.
11. Jacquet, A., Magi, M., Petry, H. and Bollen, A. (2002) High-level expression of recombinant house dust mite allergen Der p 1 in Pichia pastoris. Clin. Exp. Allergy, 32, 1048-1053.
12. Kikuchi, Y., Takai, T., Kuhara, T., Ota, M., Kato, T., Hatanaka, H., Ichikawa, S., Tokura, T., Akiba, H., Mitsuishi, K., Ikeda, S., Okumura, K. and Ogawa, H. (2006a) Crucial commitment of proteolytic activity of a purified recombinant major house dust mite allergen Der p1 to sensitization toward IgE and IgG responses. J. Immunol. 177, 1609-1617.
13. Kikuchi, Y., Takai, T., Ota, M., Kato, T., Takeda, K., Mitsuishi, K., Ikeda, S., Okumura, K. and Ogawa, H. (2006b) Application of immunoreaction enhancer solutions to an enzyme-linked immunosorbent assay for antigen-specific IgE in mice immunized with recombinant major mite allergens or ovalbumin. Int. Arch. Allergy Immunol. 141, 322-330.
14. Mayer, L. and Shao, L. (2004) Therapeutic potential of oral tolerance. Nat. Rev. Immunol. 4, 407-419.
15. Michell, E.M.C., Daniela, W., Kim, H.T.P., Erin, L., Robert, W., Engelman, C.T.L., Diana, S., Katja, K. and William, G.K. (2009) SHIP limits immunoregulatory capacity in the T-cell compartment. Blood, 113, 2934-2944.
16. Miller, A., Lider, O. and Weiner, H.L. (1991) Antigen-driven bystander suppression after oral administration of antigens. J. Exp. Med. 174, 791-798.
17. Mowat, A.M. (1987) The regulation of immune responses to dietary protein antigens. Immunol. Today, 8, 93-98.
18. Nagatani, K., Sagawa, K., Komagata, Y. and Yamamoto, K. (2004) Peyer's patch dendritic cells capturing oral antigen interact with antigen-specific T cells and induce gut-homing CD4(+)CD25(+) regulatory T cells in Peyer's patches. Ann. N Y Acad. Sci. 1029, 366-370.
19. Nakata, A., Kaminuma, O., Ogawa, K., Fujimura, H., Fushimi, K., Kikkawa, H., Naito, K., Ikezawa, K., Egan, R.W. and Mori, A. (2001) Correlation between eosinophilia induced by CD4(+) T cells and bronchial hyper-responsiveness. Int. Immunol. 13, 329-339.
20. Nelson, H.S. (2007) Allergen immunotherapy: where is it now? J. Allergy Clin. Immunol. 119, 769-779.
21. Nochi, T., Takagi, H., Yuki, Y., Yang, L., Masumura, T., Mejima, M., Nakanishi, U., Matsumura, A., Uozumi, A., Hiroi, T., Morita, S., Tanaka, K., Takaiwa, F. and Kiyono, H. (2007) Rice-based mucosal vaccine as a global strategy for cold-chain- and needle-free vaccination. Proc. Natl Acad. Sci. USA, 104, 10986-10991.
22. O'Brien, R.M., Thomas, W.R. and Tait, B.D. (1994) An immunogenetic analysis of T-cell reactive regions on the major allergen from the house dust mite, Der p I, with recombinant truncated fragments. J. Allergy Clin. Immunol. 93, 623-634.
23. Qu, L.Q. and Takaiwa, F. (2004) Evaluation of tissue specificity and expression strength of rice seed component gene promoters in transgenic rice. Plant Biotechnol. J. 2, 113-125.
24. Richman, L.K., Chiller, J.M., Brown, W.R., Hanson, D.G. and Vaz, N.M. (1978) Enterically induced immunologic tolerance. I. Induction of suppressor T lymphoyctes by intragastric administration of soluble proteins. J. Immunol. 121, 2429-2434.
25. Shakib, F., Ghaemmaghami, A.M. and Sewell, H.F. (2008) The molecular basis of allergenicity. Trends Immunol. 29, 633-642.
26. Streatfield, S.J. (2006) Mucosal immunization using recombinant plant-based oral vaccines. Methods, 38, 150-157.
27. Takagi, H., Hiroi, T., Yang, L., Tada, Y., Yuki, Y., Takamura, K., Ishimitsu, R., Kawauchi, H., Kiyono, H. and Takaiwa, F. (2005a) A rice-based edible vaccine expressing multiple T cell epitopes induces oral tolerance for inhibition of Th2-mediated IgE responses. Proc. Natl Acad. Sci. USA, 102, 17525-17530.
28. Takagi, H., Saito, S., Yang, L., Nagasaka, S., Nishizawa, N. and Takaiwa, F. (2005b) Oral immunotherapy against a pollen allergy using a seed-based peptide vaccine. Plant Biotechnol. J. 3, 521-533.
29. Takagi, H., Hiroi, T., Hirose, S., Yang, L. and Takaiwa, F. (2010) Rice seed ER-derived protein body as an efficient delivery vehicle for oral tolerogenic peptides. Peptides, 31, 1421-1425.
30. Takai, T., Kato, T., Yasueda, H., Okumura, K. and Ogawa, H. (2005) Analysis of the structure and allergenicity of recombinant pro- and mature Der p 1 and Der f 1: major conformational IgE epitopes blocked by prodomains. J. Allergy Clin. Immunol. 115, 555-563.
31. Takai, T., Mizuuchi, E., Kikuchi, Y., Nagamune, T., Okumura, K. and Ogawa, H. (2006) Glycosylation of recombinant proforms of major house dust mite allergens Der p 1 and Der f 1 decelerates the speed of maturation. Int. Arch. Allergy Immunol. 139, 181-187.
32. Takai, T., Ochiai, Y., Ichikawa, S., Sato, E., Ogawa, T., Tokura, T., Kuhara, T., Kawai, H., Hatanaka, H., Takahashi, S., Ogawa, H. and Okumura, K. (2009) Enzyme-linked immunosorbent assays with high sensitivity for antigen-specific and total murine IgE: a useful tool for the study of allergies in mouse models. Allergol. Int. 58, 225-235.
33. Takaiwa, F. (2007a) A rice-based edible vaccine expressing multiple T-cell epitopes to induce oral tolerance and inhibit allergy. Immunol. Allergy Clin. North Am. 27, 129-139.
34. Takaiwa, F. (2007b) Transgenic rice seed as a nutriceutical delivery system, CAB reviews: perspectives in agriculture, veterinary science. Nutr. Nat. Resour. 2, No. 041.
35. Takaiwa, F., Ogawa, M. and Okita, T.W. (1999) Rice glutelins. In Seed Proteins (Shewry, P.R. and Casey, R., eds), pp. 401-425, Dordrecht: Kluwer Academic Publishers.
36. Takaiwa, F., Hirose, S., Takagi, H., Yang, L. and Wakasa, Y. (2009) Deposition of a recombinant peptide in ER-derived protein bodies by retention with cysteine-rich prolamins in transgenic rice seed. Planta, 229, 1147-1158.
37. Tanaka, K., Sugimoto, T., Ogawa, M. and Kasai, Z. (1980) Isolation and characterization of two types of protein bodies in the rice endosperm. Agric. Biol. Chem. 44, 1633-1639.
38. Tang, Q. and Bluestone, J.A. (2008) The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat. Immunol. 9, 239-244.
39. Thomas, W.R., Smith, W.A., Hales, B.J., Mills, K.L. and O'Brien, R.M. (2002) Characterization and immunobiology of house dust mite allergens. Int. Arch. Allergy Immunol. 129, 1-18.
40. Tovey, E.R., Chapman, M.D. and Platts-Mills, T.A. (1981) Mite faeces are a major source of house dust allergens. Nature, 289, 592-593.
41. Weiner, H.L. (2001) Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol. Rev. 182, 207-214.
42. Yang, L., Kajiura, H., Suzuki, K., Hirose, S., Fujiyama, K. and Takaiwa, F. (2008) Generation of a transgenic rice seed-based edible vaccine against house dust mite allergy. Biochem. Biophys. Res. Commun. 365, 334-339.
43. Yssel, H., Johnson, K.E., Schneider, P.V., Wideman, J., Terr, A., Kastelein, R. and De Vries, J.E. (1992) T cell activation-inducing epitopes of the house dust mite allergen Der p I. Proliferation and lymphokine production patterns by Der p I- specific CD4+ T cell clones. J. Immunol. 148, 738-745.