Heat-induced structural changes affect OVA-antigen processing and reduce allergic response in mouse model of food allergy
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
22629361
PubMed Central
PMC3357411
DOI
10.1371/journal.pone.0037156
PII: PONE-D-11-24744
Knihovny.cz E-zdroje
- MeSH
- cytokiny krev imunologie MeSH
- imunoglobulin E krev imunologie MeSH
- modely nemocí na zvířatech MeSH
- myši MeSH
- ovalbumin chemie imunologie MeSH
- potravinová alergie krev imunologie MeSH
- prezentace antigenu imunologie MeSH
- regulační T-lymfocyty imunologie MeSH
- sekundární struktura proteinů MeSH
- vysoká teplota MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokiny MeSH
- imunoglobulin E MeSH
- ovalbumin MeSH
BACKGROUND AND AIMS: The egg protein ovalbumin (OVA) belongs to six most frequent food allergens. We investigated how thermal processing influences its ability to induce allergic symptoms and immune responses in mouse model of food allergy. METHODOLOGY/PRINCIPAL FINDINGS: Effect of increased temperature (70°C and 95°C) on OVA secondary structure was characterized by circular dichroism and by the kinetics of pepsin digestion with subsequent HPLC. BALB/c mice were sensitized intraperitoneally and challenged with repeated gavages of OVA or OVA heated to 70°C (h-OVA). Levels of allergen-specific serum antibodies were determined by ELISA (IgA and IgGs) or by β-hexosaminidase release test (IgE). Specific activities of digestive enzymes were determined in brush border membrane vesicles of jejunal enterocytes. Cytokine production and changes in regulatory T cells in mesenteric lymph nodes and spleen were assessed by ELISA and FACS. Heating of OVA to 70°C caused mild irreversible changes in secondary structure compared to boiling to 95°C (b-OVA), but both OVA treatments led to markedly different digestion kinetics and Tregs induction ability in vitro, compared to native OVA. Heating of OVA significantly decreased clinical symptoms (allergic diarrhea) and immune allergic response on the level of IgE, IL-4, IL-5, IL-13. Furthermore, h-OVA induced lower activities of serum mast cell protease-1 and enterocyte brush border membrane alkaline phosphatase as compared to native OVA. On the other hand h-OVA stimulated higher IgG2a in sera and IFN-γ secretion by splenocytes. CONCLUSIONS: Minor irreversible changes in OVA secondary structure caused by thermal processing changes both its digestion and antigenic epitopes formation, which leads to activation of different T cell subpopulations, induces shift towards Th1 response and ultimately reduces its allergenicity.
PLoS One. 2012;7(8). doi: 10.1371/annotation/53227638-162d-477c-a487-ad856854d823 PubMed
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Savage JH, Matsui EC, Skripak JM, Wood RA. The natural history of egg allergy. J Allergy Clin Immunol. 2007;120:1413–1417. PubMed
Herouet-Guicheney C, Aldemir H, Bars R, de Barbeyrac D, Kennel P, et al. Inter-laboratory comparisons of assessment of the allergenic potential of proteins in mice. J Appl Toxicol. 2009;29:141–148. PubMed
Sicherer SH, Wood RA, Stablein D, Burks AW, Liu AH, et al. Immunologic features of infants with milk or egg allergy enrolled in an observational study (Consortium of Food Allergy Research) of food allergy. J Allergy Clin Immunol. 2010;125:1077–1083. PubMed PMC
Perrier C, Thierry AC, Mercenier A, Corthésy B. Allergen-specific antibody and cytokine responses, mast cell reactivity and intestinal permeability upon oral challenge of sensitized and tolerized mice. Clin Exp Allergy. 2010;40:153–162. PubMed
Mine Y, Yang M. Epitope characterization of ovalbumin in BALB/c mice using different entry routes. Biochim Biophys Acta. 2007;1774:200–212. PubMed
Repa A, Kozakova H, Hudcovic T, Stepankova R, Hrncir T, et al. Susceptibility to nasal and oral tolerance induction to the major birch pollen allergen Bet v 1 is not dependent on the presence of the microflora. Immunol Lett. 2008;117:50–56. PubMed
Lee SY, Huang CK, Zhang TF, Schofield BH, Burks AW, et al. Oral administration of IL-12 suppresses anaphylactic reactions in a murine model of peanut hypersensitivity. Clin Immunol. 2001;101:220–228. PubMed
Diesner SC, Knittelfelder R, Krishnamurthy D, Pali-Schöll I, Gajdzik L, et al. Dose-dependent food allergy induction against ovalbumin under acid-suppression: A murine food allergy model. Immunol Lett. 2008;121:45–51. PubMed PMC
Brunner R, Wallmann J, Szalai K, Karagiannis P, Altmeppen H, et al. Aluminium per se and in the anti-acid drug sucralfate promotes sensitization via the oral route. Allergy. 2009;64:890–897. PubMed
Pali-Schöll I, Herzog R, Wallmann J, Szalai K, Brunner R, et al. Antacids and dietary supplements with an influence on the gastric pH increase the risk for food sensitization. Clin Exp Allergy. 2010;40:1091–1098. PubMed PMC
Dearman RJ, Kimber I. A mouse model for food allergy using intraperitoneal sensitization. Methods. 2007;41:91–98. PubMed
Brandt EB, Munitz A, Orekov T, Mingler MK, McBride M, et al. Targeting IL-4/IL-13 signaling to alleviate oral allergen-induced diarrhea. J Allergy Clin Immunol. 2009;123:53–58. PubMed PMC
Li X, Schofield BH, Huang CK, Kleiner GI, Sampson HA. A murine model of IgE-mediated cow’s milk hypersensitivity. J Allergy Clin Immunol. 1999;103:206–214. PubMed
Saldanha JCS, Gargiulo DL, Silva SS, Carmo-Pinto FH, Andrade MC, et al. A model of chronic IgE-mediated food allergy in ovalbumin-sensitized mice. Braz J Med Biol Res. 2004;37:809–816. PubMed
van der Ventel ML, Nieuwenhuizen NE, Kirstein F, Hikuam C, Jeebhay MF, et al. Differential responses to natural and recombinant allergens in a murine model of fish allergy. Mol Immunol. 2011;48:637–646. PubMed
Simon PM, Kedinger M, Raul F, Grenier JF, Haffen K. Developmental pattern of rat intestinal brush-border enzymic proteins along the villus-crypt axis. Biochem J. 1979;178:407–413. PubMed PMC
Kozáková H, Reháková Z, Kolínská J. Bifidobacterium bifidum monoassociation of gnotobiotic mice: effect on enterocyte brush-border enzymes. Folia Microbiol. 2001;46:573–576. PubMed
Hudcovic T, Kozáková H, Kolínská J, Stepánková R, Hrncír T, et al. Monocolonization with Bacteroides ovatus protects immunodeficient SCID mice from mortality in chronic intestinal inflammation caused by long-lasting dextran sodium sulfate treatment. Physiol Res. 2009;58:101–110. PubMed
Lallès JP. Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev. 2010;68:323–332. PubMed
Harada T, Koyama I, Kasahara T, Alpers DH, Komoda T. Heat shock induces intestinal-type alkaline phosphatase in rat IEC-18 cells. Am J Physiol Gastrointest Liver Physiol. 2003;284:G255–G262. PubMed
Huntington JA, Stein PE. Structure and properties of ovalbumin. J Chromatogr B Biomed Sci Appl. 2001;756(1–2):189–198. PubMed
Lemon-Mulé H, Sampson HA, Sicherer SH, Shreffler WG, Noone S, et al. Immunologic changes in children with egg allergy ingesting extensively heated egg. J Allergy Clin Immunol. 2008;122:977–983. PubMed
Martos G, Lopez-Exposito I, Bencharitiwong R, Berin MC, Nowak-Węgrzyn A. Mechanisms underlying differential food allergy response to heated egg. J Allergy Clin Immunol. 2011;127:990–997. PubMed PMC
Nowak-Węgrzyn A, Sampson HA. Future therapies for food allergies. J Allergy Clin Immunol. 2011;127:558–573. PubMed PMC
Roth-Walter F, Berin MC, Arnaboldi P, Escalante CR, Dahan S, et al. Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer’s patches. Allergy. 2008;63:882–890. PubMed
Himly M, Nony E, Chabre H, Van Overtvelt L, Neubauer A, et al. Standardization of allergen products: 1. Detailed characterization of GMP-produced recombinant Bet v 1.0101 as biological reference preparation. Allergy. 2009;64:1038–1045. PubMed
Tučková L, Novotná J, Novák P, Flegelová Z, Květoň T, et al. Activation of macrophages by gliadin fragments: isolation and characterization of active peptide. J Leukoc Biol. 2002;71:625–631. PubMed
Wiedermann U, Jahn-Schmid B, Bohle B, Repa A, Renz H, et al. Suppression of antigen-specific T- and B-cell responses by intranasal or oral administration of recombinant bet v 1, the major birch pollen allergen, in a murine model of type I allergy. J Allergy Clin Immunol. 1999;103:1202–1210. PubMed
Lehrer SB, Reish R, Fernandes J, Gaudry P, Dai G, et al. Enhancement of murine IgE antibody detection by IgG removal. J Immunol Methods. 2004;284:1–6. PubMed
Barsumian EL, Isersky C, Petrino MG, Siraganian IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and nonreleasing clones. Eur J Immunol. 1981;11:317–323. PubMed
Kessler M, Acuto O, Storelli C, Murer H, Müller M, et al. A modified procedure for the rapid preparation of efficiently transporting vesicles from small intestinal brush border membranes. Their use in investigating some properties of D-glucose and choline transport systems. Biochim Biophys Acta. 1978;506:136–154. PubMed
Lowry OH, Rosebrough NJ, Farr Al, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265–275. PubMed
Kozakova H, Kolinska J, Lojda Z, Rehakova Z, Sinkora J, et al. Effect of bacterial monoassociation on brush-border enzyme activities in ex-germ-free piglets: comparison of commensal and pathogenic Escherichia coli strains. Microbes Infect. 2006;8:2629–2639. PubMed
Whitacre CC, Gienapp IE, Orosz CG, Bitar DM. Oral tolerance in experimental autoimmune encephalomyelitis. III. Evidence for clonal anergy. J Immunol. 1991;147:2155–2163. PubMed
Vaali K, Puumalainen TJ, Lehto M, Wolff H, Rita H. Murine model of food allergy after epicutaneous sensitization: role of mucosal mast cell protease-1. Scand J Gastroenterol. 2006;41:1405–1413. PubMed
Lynes MD, Widmaier EP. Involvement of CD36 and intestinal alkaline phosphatases in fatty acid transport in enterocytes, and the response to a high-fat diet. Life Sci. 2011;88:384–391. PubMed
Smith MW, Phillips AD. Abnormal expression of dipeptidylpeptidase IV activity in enterocytes brush-border membranes of children suffering from coeliac disease. Exp Physiol. 1990;75:613–616. PubMed
Detel D, Persić M, Varljen J. Serum and intestinal dipeptidyl peptidase IV (DPP IV/CD26) activity in children with celiac disease. J Pediatr Gastroenterol. Nutr. 2007;45:65–70. PubMed
Johansen P, Senti G, Gómez JMM, Wüthrich B, Bot A, et al. Heat denaturation, a simple method to improve the immunotherapeutic potential of allergens. Eur J Immunol. 2005;35:3591–3598. PubMed
Alex P, Zachos NC, Nguyen T, Gonzales L, Chen TE, et al. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm Bowel Dis. 2009;15:341–352. PubMed PMC
Yang M, Yang C, Mine Y. Multiple T cell epitope peptides suppress allergic responses in an egg allergy mouse model by the elicitation of forkhead box transcription factor 3- and transforming growth factor-β-associated mechanisms. Clin Exp Allergy. 2010;40:668–678. PubMed
Viney JL, Mowat AM, O’Malley JM, Williamson E, Fanger NA. Expanding dendritic cells in vivo enhances the induction of oral tolerance. J Immunol. 1998;160:5815–5825. PubMed
Lied GA, Vogelsang P, Berstad A, Appel S. Dendritic cell populations in patients with self-reported food hypersensitivity. Int J Gener Med. 2011;4:389–396. PubMed PMC
McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, et al. Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature. 2012;483:345–349. PubMed PMC