Abstract
Allergic rhinitis (AR) is one of the most common chronic diseases. Although current medications are highly effective in controlling its symptoms, they do not reverse the allergen-specific hypersensitivities that underlie the disease. Immunoglobulin E is a key mediator of AR, and preventing its production is clinically important. In this study, we developed an efficient needleless intranasal protein delivery system using the hemagglutinating virus of Japan envelope vector (HVJ-E). Intranasal delivery of ovalbumin (OVA) once a week for 3 weeks using this system enhanced OVA-induced interferon-γ production by murine splenocytes. This treatment also attenuated the OVA-induced release interleukin-4 (IL-4) and IL-5 from splenocytes and the production of plasma OVA-specific immunoglobulin E in OVA-sensitive AR model mice. Thus, allergen-containing HVJ-E may be useful for noninvasive treatment of AR.
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Abbreviations
- AR:
-
allergic rhinitis
- HVJ-E:
-
hemagglutinating virus of Japan envelope vector
- OVA:
-
ovalbumin
References
Naclerio RM (1991) Allergic rhinitis. N Engl J Med 325:860–869
Savage J, Roy D (2005) Allergic rhinitis: an update. J R Soc Health 125:172–175
Platts-Mills TA (2001) The role of immunoglobulin E in allergy and asthma. Am J Respir Crit Care Med 164:S1–S5
Kitaura J, Song J, Tsai M, Asai K, Maeda-Yamamoto M, Mocsai A, Kawakami Y, Liu FT, Lowell CA, Barisas BG, Galli SJ, Kawakami T (2003) Evidence that IgE molecules mediate a spectrum of effects on mast cell survival and activation via aggregation of the Fc∈RI. Proc Natl Acad Sci U S A 100:12911–12916
Pandey V, Mihara S, Fensome-Green A, Bolsover S, Cockcroft S (2004) Monomeric IgE stimulates NFAT translocation into the nucleus, a rise in cytosol Ca2+, degranulation, and membrane ruffling in the cultured rat basophilic leukemia-2H3 mast cell line. J Immunol 172:4048–4058
Bacharier LB, Geha RS (2000) Molecular mechanisms of IgE regulation. J Allergy Clin Immunol 105:S547–S558
Umetsu DT, DeKruyff RH (1997) Th1 and Th2 CD4+ cells in the pathogenesis of allergic diseases. Proc Soc Exp Biol Med 215:11–20
Grogan JL, Locksley RM (2002) T helper cell differentiation: on again, off again. Curr Opin Immunol 14:366–372
Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100:655–669
O’Garra A (1998) Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8:275–283
Paludan SR (1998) Interleukin-4 and interferon-gamma: the quintessence of a mutual antagonistic relationship. Scand J Immunol 48:459–468
Chretien I, Pene J, Briere F, De Waal Malefijt R, Rousset F, De Vries JE (1990) Regulation of human IgE synthesis. I. Human IgE synthesis in vitro is determined by the reciprocal antagonistic effects of interleukin 4 and interferon-gamma. Eur J Immunol 20:243–251
Purkerson J, Isakson P (1992) A two-signal model for regulation of immunoglobulin isotype switching. FASEB J 6:3245–3252
Romagnani S (1990) Regulation and deregulation of human IgE synthesis. Immunol Today 11:316–321
Snapper CM, Paul WE (1987) Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236:944–947
Paul WE (1989) Pleiotropy and redundancy: T cell-derived lymphokines in the immune response. Cell 57:521–524
Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, Mosmann TR, Vitetta ES (1988) Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334:255–258
Finkelman FD, Katona IM, Urban JF, Jr., Holmes J, Ohara J, Tung AS, Sample JV, Paul WE (1988) IL-4 is required to generate and sustain in vivo IgE responses. J Immunol 141:2335–2341
Finkelman FD, Katona IM, Urban JF, Jr., Snapper CM, Ohara J, Paul WE (1986) Suppression of in vivo polyclonal IgE responses by monoclonal antibody to the lymphokine B-cell stimulatory factor 1. Proc Natl Acad Sci U S A 83:9675–9678
Kilmon MA, Ghirlando R, Strub MP, Beavil RL, Gould HJ, Conrad DH (2001) Regulation of IgE production requires oligomerization of CD23. J Immunol 167:3139–3145
von Garnier C, Astori M, Kettner A, Dufour N, Heusser C, Corradin G, Spertini F (2000) Allergen-derived long peptide immunotherapy down-regulates specific IgE response and protects from anaphylaxis. Eur J Immunol 30:1638–1645
Kaneda Y, Nakajima T, Nishikawa T, Yamamoto S, Ikegami H, Suzuki N, Nakamura H, Morishita R, Kotani H (2002) Hemagglutinating virus of Japan (HVJ) envelope vector as a versatile gene delivery system. Molec Ther 6:219–226
Okada Y (1993) Sendai virus-induced cell fusion. Methods Enzymol 221:18–41
Ito M, Yamamoto S, Nimura K, Hiraoka K, Tamai K, Kaneda Y (2005) Rad51 siRNA delivered by HVJ envelope vector enhances the anti-cancer effect of cisplatin. J Gene Med 7:1044–1052
Ikeda Y, Kaneko A, Yamamoto M, Ishige A, Sasaki H (2002) Possible involvement of suppression of Th2 differentiation in the anti-allergic effect of Sho-seiryu-to in mice. Jpn J Pharmacol 90:328–336
Sakaguchi M, Ikeda Y, Kido T, Yuzurihara M, Kase Y, Yamamoto M, Ishige A, Sasaki H (2002) Pharmacological characteristics of Ryokan-kyomi-shinge-nin-to, an antiallergic Kampo medicine. Biol Pharm Bull 25:1562–1565
Greenfeder S, Umland SP, Cuss FM, Chapman RW, Egan RW (2001) Th2 cytokines and asthma. The role of interleukin-5 in allergic eosinophilic disease. Respir Res 2:71–79
Kidd P (2003) Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev 8:223–246
Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL (1986) Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 136:2348–2357
Romagnani S (1991) Human TH1 and TH2 subsets: doubt no more. Immunol Today 12:256–257
Gauchat JF, Aubry JP, Mazzei G, Life P, Jomotte T, Elson G, Bonnefoy JY (1993) Human CD40-ligand: molecular cloning, cellular distribution and regulation of expression by factors controlling IgE production. FEBS Lett 315:259–266
Worm M, Henz BM (1997) Molecular regulation of human IgE synthesis. J Mol Med 75:440–447
Gavett SH, O’Hearn DJ, Li X, Huang SK, Finkelman FD, Wills-Karp M (1995) Interleukin 12 inhibits antigen-induced airway hyperresponsiveness, inflammation, and Th2 cytokine expression in mice. J Exp Med 182:1527–1536
Kung TT, Stelts DM, Zurcher JA, Jones H, Umland SP, Egan RW, Kreutner W, Chapman RW (1995) Interferon-gamma and antibodies to interleukin-5 and interleukin-4 inhibit the pulmonary eosinophilia in allergic mice. Inflamm Res 44 Suppl 2:S185–S186
Wynn TA, Eltoum I, Oswald IP, Cheever AW, Sher A (1994) Endogenous interleukin 12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylactically immunizes against egg pathology. J Exp Med 179:1551–1561
McCusker C, Chicoine M, Hamid Q, Mazer B (2002) Site-specific sensitization in a murine model of allergic rhinitis: role of the upper airway in lower airways disease. J Allergy Clin Immunol 110:891–898
Schramm CM, Puddington L, Wu C, Guernsey L, Gharaee-Kermani M, Phan SH, Thrall RS (2004) Chronic inhaled ovalbumin exposure induces antigen-dependent but not antigen-specific inhalational tolerance in a murine model of allergic airway disease. Am J Pathol 164:295–304
Lopez CB, Garcia-Sastre A, Williams BR, Moran TM (2003) Type I interferon induction pathway, but not released interferon, participates in the maturation of dendritic cells induced by negative-strand RNA viruses. J Infect Dis 187:1126–1136
Lopez CB, Moltedo B, Alexopoulou L, Bonifaz L, Flavell RA, Moran TM (2004) TLR-independent induction of dendritic cell maturation and adaptive immunity by negative-strand RNA viruses. J Immunol 173:6882–6889
Ito T, Amakawa R, Inaba M, Hori T, Ota M, Nakamura K, Takebayashi M, Miyaji M, Yoshimura T, Inaba K, Fukuhara S (2004) Plasmacytoid dendritic cells regulate Th cell responses through OX40 ligand and type I IFNs. J Immunol 172:4253–4259
Brinkmann V, Geiger T, Alkan S, Heusser CH (1993) Interferon alpha increases the frequency of interferon gamma-producing human CD4+ T cells. J Exp Med 178:1655–1663
Van Weyenbergh J, MP PSilva, Bafica A, Cardoso S, Wietzerbin J, Barral-Netto M (2001) IFN-beta and TGF-beta differentially regulate IL-12 activity in human peripheral blood mononuclear cells. Immunol Lett 75:117–122
Hoglund CO, Axen J, Kemi C, Jernelov S, Grunewald J, Muller-Suur C, Smith Y, Gronneberg R, Eklund A, Stierna P, Lekander M (2006) Changes in immune regulation in response to examination stress in atopic and healthy individuals. Clin Exp Allergy 36:982–992
Bungener L, Huckriede A, de Mare A, de Vries-Idema J, Wilschut J, Daemen T (2005) Virosome-mediated delivery of protein antigens in vivo: efficient induction of class I MHC-restricted cytotoxic T lymphocyte activity. Vaccine 23:1232–1241
Nakanishi T, Hayashi A, Kunisawa J, Tsutsumi Y, Tanaka K, Yashiro-Ohtani Y, Nakanishi M, Fujiwara H, Hamaoka T, Mayumi T (2000) Fusogenic liposomes efficiently deliver exogenous antigen through the cytoplasm into the MHC class I processing pathway. Eur J Immunol 30:1740–1747
Kaneda Y, Yamamoto S, Nakajima T (2005) Development of HVJ envelope vector and its application to gene therapy. Adv Genet 53PA:307–332
Acknowledgment
This work was supported by a grant from the Ministry of Health, Labor, and Welfare of Japan.
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Yasuoka, E., Oshima, K., Tamai, K. et al. Needleless intranasal administration of HVJ-E containing allergen attenuates experimental allergic rhinitis. J Mol Med 85, 283–292 (2007). https://doi.org/10.1007/s00109-006-0120-y
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DOI: https://doi.org/10.1007/s00109-006-0120-y