Complexation of whey protein with caffeic acid or (−)-epigallocatechin-3-gallate as a strategy to induce oral tolerance to whey allergenic proteins

International Immunopharmacology

Volumn 68, Issue , 2019, Pages 115-123

  Pessato, Tássia B ^a   de Carvalho, Natália C ^a   de Figueiredo, Daniella ^a   Colomeu, Talita C ^a   Fernandes, Luís Gustavo R ^a   Netto, Flavia M ^a   de L Zollner, Ricardo ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Anti allergic capacity; Cow's milk allergy; Hypoallergenic products; Oral immunotherapy; Protein phenolic interactions

Indexed keywords

CAFFEIC ACID; CHOLERA TOXIN; CHYMASE; EPIGALLOCATECHIN GALLATE; FOOD ALLERGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 17; PHENOL DERIVATIVE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; WHEY PROTEIN; WHEY PROTEIN ISOLATE; ALLERGEN; CAFFEIC ACID DERIVATIVE; CATECHIN; CCL2 PROTEIN, MOUSE; IMMUNOGLOBULIN G; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE PROLIFERATION; MILK ALLERGY; MOUSE; NONHUMAN; ORAL IMMUNOTHERAPY; PHENOTYPE; PRIORITY JOURNAL; SENSITIZATION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; TH1 TH2 BALANCE; TH17 CELL; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; C3H MOUSE; CHEMISTRY; DESENSITIZATION; IMMUNOLOGY; ORAL DRUG ADMINISTRATION;

ADMINISTRATION, ORAL; ALLERGENS; ANIMALS; CAFFEIC ACIDS; CATECHIN; CD4-POSITIVE T-LYMPHOCYTES; CHEMOKINE CCL2; DESENSITIZATION, IMMUNOLOGIC; FEMALE; IMMUNE TOLERANCE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; MICE, INBRED C3H; MILK HYPERSENSITIVITY; WHEY PROTEINS;

EID: 85059449587     PISSN: 15675769     EISSN: 18781705     Source Type: Journal    
DOI: 10.1016/j.intimp.2018.12.047     Document Type: Article

References (58)

1. Hochwallner, H., Schulmeister, U., Swoboda, I., Spitzauer, S., Valenta, R., Cow's milk allergy: from allergens to new forms of diagnosis, therapy and prevention. Methods 66:1 (2014), 22–33.
2. Wang, J., Sampson, H.A., Food allergy. J. Clin. Invest. 121:3 (2011), 827–835.
3. Kumar, S., Verma, A.K., Das, M., Dwivedi, P.D., Molecular mechanisms of IgE mediated food allergy. Int. Immunopharmacol. 13:4 (2012), 432–439.
4. Kiewiet, M.B.G., Gros, M., van Neerven, R.J.J., Faas, M.M., de Vos, P., Immunomodulating properties of protein hydrolysates for application in cow's milk allergy. Pediatr. Allergy Immunol. 26:3 (2015), 206–217.
5. Tordesillas, L., Berin, M.C., Mechanisms of Oral Tolerance. 2018.
6. Castro-Junior, A.B., Horta, B.C., Gomes-Santos, A.C., Cunha, A.P., Silva Steinberg, R., Nascimento, D.S., Faria, A.M.C., Vaz, N.M., Oral tolerance correlates with high levels of lymphocyte activity. Cell. Immunol. 280:2 (2012), 171–181.
7. da Cunha, A.P., Wu, H.Y., Rezende, R.M., Vandeventer, T., Weiner, H.L., In vivo anti-LAP mAb enhances IL-17/IFN-γ responses and abrogates anti-CD3-induced oral tolerance. Int. Immunol. 27:2 (2015), 73–82.
8. Krogulska, A., Borowiec, M., Polakowska, E., Dynowski, J., Młynarski, W., Wasowska-Królikowska, K., FOXP3, IL-10, and TGF-β genes expression in children with IgE-dependent food allergy. J. Clin. Immunol. 31:2 (2011), 205–215.
9. Dhuban, K.B., d'Hennezel, E., Ben-Shoshan, M., McCusker, C., Clarke, A., Fiset, P., Mazer, B., Piccirillo, C.A., Altered, T., Helper 17 responses in children with food allergy. Int. Arch. Allergy Immunol. 162:4 (2013), 318–322.
10. Ueno, A., Jeffery, L., Kobayashi, T., Hibi, T., Ghosh, S., Jijon, H., Th17 plasticity and its relevance to inflammatory bowel disease. J. Autoimmun. 87 (2018), 38–49.
11. Rai, G., Das, S., Ansari, M.A., Singh, P.K., Gupta, N., Sharma, S., Akhter, N., Ramachandran, V.G., Haque, S., Dar, S.A., Phenotypic and functional profile of Th17 and Treg cells in allergic fungal sinusitis. Int. Immunopharmacol. 57 (2018), 55–61.
12. Gagliani, N., Amezcua Vesely, M.C., Iseppon, A., Brockmann, L., Xu, H., Palm, N.W., de Zoete, M.R., Licona-Limon, P., Paiva, R.S., Ching, T., Weaver, C., Zi, X., Pan, X., Fan, R., Garmire, L.X., Cotton, M.J., Drier, Y., Bernstein, B., Geginat, J., Stockinger, B., Esplugues, E., Huber, S., Flavell, R.A., Th17 cells transdifferentiate into regulatory T cells during resolution of inflammation. Nature 523:7559 (2015), 221–225.
13. Hyung, K.E., Moon, B.S., Kim, B., Park, E.S., Park, S.-Y., Hwang, K.W., Lactobacillus plantarum isolated from kimchi suppress food allergy by modulating cytokine production and mast cells activation. J. Funct. Foods 29 (2017), 60–68.
14. Hwang, K.-A., Hwang, Y.-J., Song, J., Anti-allergic effect of Aster yomena on ovalbumin-sensitized mouse and RHL-2H3 cells via Th1/Th2 cytokine balance. J. Funct. Foods 44 (2018), 1–8.
15. van Esch, B.C., Knipping, K., Jeurink, P., van der Heide, S., Dubois, A.E., Willemsen, L.E., Garssen, J., Knippels, L.M., In vivo and in vitro evaluation of the residual allergenicity of partially hydrolysed infant formulas. Toxicol. Lett. 201:3 (2011), 264–269.
16. El Mecherfi, K.E., Saidi, D., Kheroua, O., Boudraa, G., Touhami, M., Rouaud, O., Curet, S., Choiset, Y., Rabesona, H., Chobert, J.-M., Haertlé, T., Combined microwave and enzymatic treatments for β‑lactoglobulin and bovine whey proteins and their effect on the IgE immunoreactivity. Eur. Food Res. Technol., 233(5), 2011, 859.
17. Zheng, H., Shen, X., Bu, G., Luo, Y., Effects of pH, temperature and enzyme-to-substrate ratio on the antigenicity of whey protein hydrolysates prepared by Alcalase. Int. Dairy J. 18:10 (2008), 1028–1033.
18. Singh, A., Holvoet, S., Mercenier, A., Dietary polyphenols in the prevention and treatment of allergic diseases. Clin. Exp. Allergy 41:10 (2011), 1346–1359.
19. Muraro, A., Hoekstra, M.O., Meijer, Y., Lifschitz, C., Wampler, J.L., Harris, C., Scalabrin, D.M., Extensively hydrolysed casein formula supplemented with Lactobacillus rhamnosus GG maintains hypoallergenic status: randomised double-blind, placebo-controlled crossover trial. BMJ Open, 2(2), 2012, e000637.
20. van den Elsen, L.W., van Esch, B.C., Hofman, G.A., Kant, J., van de Heijning, B.J., Garssen, J., Willemsen, L.E., Dietary long chain n-3 polyunsaturated fatty acids prevent allergic sensitization to cow's milk protein in mice. Clin. Exp. Allergy 43:7 (2013), 798–810.
21. Maeda-Yamamoto, M., Inagaki, N., Kitaura, J., Chikumoto, T., Kawahara, H., Kawakami, Y., Sano, M., Miyase, T., Tachibana, H., Nagai, H., Kawakami, T., O-methylated catechins from tea leaves inhibit multiple protein kinases in mast cells. J. Immunol. 172:7 (2004), 4486–4492 (Baltimore, Md.: 1950).
22. Venkatesh, P., Mukherjee, P.K., Kumar, N.S., Bandyopadhyay, A., Fukui, H., Mizuguchi, H., Islam, N., Anti-allergic activity of standardized extract of Albizia lebbeck with reference to catechin as a phytomarker. Immunopharmacol. Immunotoxicol. 32:2 (2010), 272–276.
23. Tamura, S., Yoshihira, K., Fujiwara, K., Murakami, N., New inhibitors for expression of IgE receptor on human mast cell. Bioorg. Med. Chem. Lett. 20:7 (2010), 2299–2302.
24. Akiyama, H., Sato, Y., Watanabe, T., Nagaoka, M.H., Yoshioka, Y., Shoji, T., Kanda, T., Yamada, K., Totsuka, M., Teshima, R., Sawada, J., Goda, Y., Maitani, T., Dietary unripe apple polyphenol inhibits the development of food allergies in murine models. FEBS Lett. 579:20 (2005), 4485–4491.
25. Chung, S.-Y., Champagne, E.T., Reducing the allergenic capacity of peanut extracts and liquid peanut butter by phenolic compounds. Food Chem. 115:4 (2009), 1345–1349.
26. Zuercher, A.W., Holvoet, S., Weiss, M., Mercenier, A., Polyphenol-enriched apple extract attenuates food allergy in mice. Clin. Exp. Allergy 40:6 (2010), 942–950.
27. Ognjenovic, J., Stojadinovic, M., Milcic, M., Apostolovic, D., Vesic, J., Stambolic, I., Atanaskovic-Markovic, M., Simonovic, M., Velickovic, T.C., Interactions of epigallo-catechin 3-gallate and ovalbumin, the major allergen of egg white. Food Chem. 164 (2014), 36–43.
28. Plundrich, N.J., Kulis, M., White, B.L., Grace, M.H., Guo, R., Burks, A.W., Davis, J.P., Lila, M.A., Novel strategy to create hypoallergenic peanut protein–polyphenol edible matrices for oral immunotherapy. J. Agric. Food Chem. 62:29 (2014), 7010–7021.
29. Fujimura, Y., Tachibana, H., Maeda-Yamamoto, M., Miyase, T., Sano, M., Yamada, K., Antiallergic tea catechin, (−)‑epigallocatechin‑3‑O‑(3‑O‑methyl)‑gallate, suppresses FcεRI expression in human basophilic KU812 cells. J. Agric. Food Chem. 50:20 (2002), 5729–5734.
30. A.o.O.A.C. International, Official Methods of Analysis of AOAC International. 2006, AOAC-Association of Official Analytical Chemists International, Gaithersburg (Maryland).
31. Sah, B.N.P., McAinch, A.J., Vasiljevic, T., Modulation of bovine whey protein digestion in gastrointestinal tract: a comprehensive review. Int. Dairy J. 62 (2016), 10–18.
32. Villas-Boas, M.B., Vieira, K.P., Trevizan, G., de Lima Zollner, R., Netto, F.M., The effect of transglutaminase-induced polymerization in the presence of cysteine on β‑lactoglobulin antigenicity. Int. Dairy J. 20:6 (2010), 386–392.
33. Carvalho, N.C.d., Pessato, T.B., Fernandes, L.G.R., Zollner, R.d.L., Netto, F.M., Physicochemical characteristics and antigenicity of whey protein hydrolysates obtained with and without pH control. Int. Dairy J. 71 (2017), 24–34.
34. Thomé, R., Fernandes, L.G.R., Mineiro, M.F., Simioni, P.U., Joazeiro, P.P., Tamashiro, W.M.d.S.C., Oral tolerance and OVA-induced tolerogenic dendritic cells reduce the severity of collagen/ovalbumin-induced arthritis in mice. Cell. Immunol. 280:1 (2012), 113–123.
35. Ando, Y., Yasuoka, C., Mishima, T., Ikematsu, T., Uede, T., Matsunaga, T., Inobe, M., Concanavalin A-mediated T cell proliferation is regulated by herpes virus entry mediator costimulatory molecule. In Vitro Cell. Dev. Biol. Anim. 50:4 (2014), 313–320.
36. Faria, A.M., Weiner, H.L., Oral tolerance and TGF-beta-producing cells. Inflamm. Allergy Drug Targets 5:3 (2006), 179–190.
37. Liu, T., Navarro, S., Lopata, A.L., Current advances of murine models for food allergy. Mol. Immunol. 70 (2016), 104–117.
38. van Esch, B.C.A.M., Kostadinova, A.I., Garssen, J., Willemsen, L.E.M., Knippels, L.M.J., A dietary intervention with non-digestible oligosaccharides and partial hydrolysed whey protein prevents the onset of food allergic symptoms in mice. PharmaNutrition 5:1 (2017), 1–7.
39. Roleira, F.M.F., Tavares-da-Silva, E.J., Varela, C.L., Costa, S.C., Silva, T., Garrido, J., Borges, F., Plant derived and dietary phenolic antioxidants: anticancer properties. Food Chem. 183 (2015), 235–258.
40. Berdowska, I., Zielinski, B., Fecka, I., Kulbacka, J., Saczko, J., Gamian, A., Cytotoxic impact of phenolics from Lamiaceae species on human breast cancer cells. Food Chem. 141:2 (2013), 1313–1321.
41. Pae, M., Ren, Z., Meydani, M., Shang, F., Meydani, S.N., Wu, D., Epigallocatechin‑3‑gallate directly suppresses T cell proliferation through impaired IL-2 utilization and cell cycle progression. J. Nutr. 140:8 (2010), 1509–1515.
42. Wu, D., Guo, Z., Ren, Z., Guo, W., Meydani, S.N., Green tea EGCG suppresses T cell proliferation through impairment of IL-2/IL-2 receptor signaling. Free Radic. Biol. Med. 47:5 (2009), 636–643.
43. Figueiredo, D., Colomeu, T.C., Schumacher, N.S.G., Stivanin-Silva, L.G., Cazarin, C.B.B., Meletti, L.M.M., Fernandes, L.G.R., Prado, M.A., Zollner, R.L., Aqueous leaf extract of Passiflora alata Curtis promotes antioxidant and anti-inflammatory effects and consequently preservation of NOD mice beta cells (non-obese diabetic). Int. Immunopharmacol. 35 (2016), 127–136.
44. Pabst, O., Mowat, A.M., Oral tolerance to food protein. Mucosal Immunol., 5, 2012, 232.
45. Lee, D., Kim, H.S., Shin, E., Do, S.-G., Lee, C.-K., Kim, Y.M., Lee, M.B., Min, K.Y., Koo, J., Kim, S.J., Nam, S.T., Kim, H.W., Park, Y.H., Choi, W.S., Polysaccharide isolated from Aloe vera gel suppresses ovalbumin-induced food allergy through inhibition of Th2 immunity in mice. Biomed. Pharmacother. 101 (2018), 201–210.
46. Hawrylowicz, C.M., O'Garra, A., Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol., 5, 2005, 271.
47. Rindsjö, E., Scheynius, A., Mechanisms of IgE-mediated allergy. Exp. Cell Res. 316:8 (2010), 1384–1389.
48. Openshaw, P., Murphy, E.E., Hosken, N.A., Maino, V., Davis, K., Murphy, K., O'Garra, A., Heterogeneity of intracellular cytokine synthesis at the single-cell level in polarized T helper 1 and T helper 2 populations. J. Exp. Med. 182:5 (1995), 1357–1367.
49. Lee, H.O., Miller, S.D., Hurst, S.D., Tan, L.J., Cooper, C.J., Barrett, T.A., Interferon gamma induction during oral tolerance reduces T-cell migration to sites of inflammation. Gastroenterology 119:1 (2000), 129–138.
50. Perrier, C., Thierry, A.C., Mercenier, A., Corthesy, B., Allergen-specific antibody and cytokine responses, mast cell reactivity and intestinal permeability upon oral challenge of sensitized and tolerized mice. Clin. Exp. Allergy 40:1 (2010), 153–162.
51. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001), 683–765.
52. Palomares, O., Yaman, G., Azkur, A.K., Akkoc, T., Akdis, M., Akdis, C.A., Role of Treg in immune regulation of allergic diseases. Eur. J. Immunol. 40:5 (2010), 1232–1240.
53. Gri, G., Piconese, S., Frossi, B., Manfroi, V., Merluzzi, S., Tripodo, C., Viola, A., Odom, S., Rivera, J., Colombo, M.P., Pucillo, C.E., CD4+CD25+ regulatory T cells suppress mast cell degranulation and allergic responses through OX40-OX40L interaction. Immunity 29:5 (2008), 771–781.
54. Wing, K., Onishi, Y., Prieto-Martin, P., Yamaguchi, T., Miyara, M., Fehervari, Z., Nomura, T., Sakaguchi, S., CTLA-4 control over Foxp3+ regulatory T cell function. Science (New York, N.Y.) 322:5899 (2008), 271–275.
55. Ring, S., Schafer, S.C., Mahnke, K., Lehr, H.A., Enk, A.H., CD4+ CD25+ regulatory T cells suppress contact hypersensitivity reactions by blocking influx of effector T cells into inflamed tissue. Eur. J. Immunol. 36:11 (2006), 2981–2992.
56. Li, M., Cui, J., Ngadi, M.O., Ma, Y., Absorption mechanism of whey-protein-delivered curcumin using Caco-2 cell monolayers. Food Chem. 180 (2015), 48–54.
57. Shpigelman, A., Shoham, Y., Israeli- Lev, G., Livney, Y., β‑Lactoglobulin‑naringenin Complexes: Nano-vehicles for the Delivery of a Hydrophobic Nutraceutical. 2014.
58. Plundrich, N.J., White, B.L., Dean, L.L., Davis, J.P., Foegeding, E.A., Lila, M.A., Stability and immunogenicity of hypoallergenic peanut protein-polyphenol complexes during in vitro pepsin digestion. Food Funct. 6:7 (2015), 2145–2154.