Skip to main content
Top
Published in: European Journal of Nutrition 7/2020

01-10-2020 | Cytokines | Original Contribution

Egg yolk augments type 2 immunity by activating innate cells

Authors: Leticia Pérez-Rodríguez, Mónica Martínez-Blanco, Daniel Lozano-Ojalvo, Elena Molina, Rosina López-Fandiño

Published in: European Journal of Nutrition | Issue 7/2020

Login to get access

Abstract

Purpose

Egg yolk (EY) may play a role during the sensitizing phase of egg allergy by exerting intestinal type 2-biasing effects. We aimed to identify the mechanism and role of EY in the induction of allergy to egg white (EW).

Methods

BALB/c mice were exposed intragastrically to EW, EY, or the mixture of EW:EY. In addition in vitro experiments were conducted with intestinal epithelial cells (IECs), dendritic cells (DCs), and T cells from naïve mice. Inflammatory and type 2 responses were evaluated.

Results

Administration of EW upregulated duodenal expression of factors that influence epithelial barrier integrity and function, such as Muc2 and Cldn2, type 2-promoting epithelial cytokines Il33 and Il25, DC genes Irf4 and Tnfsf4, and Th2-cytokines Il14 and Il13. EW:EY further increased the expression of Il25 and Tslp in the duodenum, Il33 and Tslp in the jejunum, and the proportion of lamina propria group 2 innate immune cells (ILC2s) over EW alone. Moreover, it distinctively enhanced the expression of Irf4 and Cd1d1 in the Peyer’s patches (PPs), and of Il6, Il33, Gata3, and Il13, both in PPs and mesenteric lymph nodes. In co-cultures of DCs and T cells, EW:EY induced a higher expression of Gata3, Il4, and Il13, secretion of IL-13 and expansion of CD4+ T cells expressing ST2, the IL-33 receptor, than EW or EY added individually.

Conclusion

Co-administration of EY may promote sensitization to EW through activation of innate immune cells, such as IECs, DCs and ILC2s, that are central to the progress of allergies.
Appendix
Available only for authorised users
Literature
1.
go back to reference Cayrol C, Duval A, Schmitt P, Roga S, Camus M, Stella A, Burlet-Schiltz O, Gonzalez-de-Peredo A, Girard JP (2018) Environmental allergens induce allergic inflammation through proteolytic maturation of IL-33. Nat Immunol 19(4):375–385PubMedCrossRef Cayrol C, Duval A, Schmitt P, Roga S, Camus M, Stella A, Burlet-Schiltz O, Gonzalez-de-Peredo A, Girard JP (2018) Environmental allergens induce allergic inflammation through proteolytic maturation of IL-33. Nat Immunol 19(4):375–385PubMedCrossRef
2.
go back to reference Benedé S, López-Expósito I, Molina E, López-Fandiño R (2015) Egg proteins as allergens and the effects of the food matrix and processing. Food Funct 6(3):694–713PubMedCrossRef Benedé S, López-Expósito I, Molina E, López-Fandiño R (2015) Egg proteins as allergens and the effects of the food matrix and processing. Food Funct 6(3):694–713PubMedCrossRef
4.
go back to reference Hammad H, Lambrecht BN (2015) Barrier epithelial cells and the control of type 2 immunity. Immunity 43(1):29–40PubMedCrossRef Hammad H, Lambrecht BN (2015) Barrier epithelial cells and the control of type 2 immunity. Immunity 43(1):29–40PubMedCrossRef
5.
go back to reference Chu DK, Llop-Guevara A, Walker TD, Flader K, Goncharova S, Boudreau JE, Moore CL, Seunghyun In T, Waserman S, Coyle AJ, Kolbeck R, Humbles AA, Jordana M (2013) IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 131(1):187–200.e18PubMedCrossRef Chu DK, Llop-Guevara A, Walker TD, Flader K, Goncharova S, Boudreau JE, Moore CL, Seunghyun In T, Waserman S, Coyle AJ, Kolbeck R, Humbles AA, Jordana M (2013) IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 131(1):187–200.e18PubMedCrossRef
6.
go back to reference Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, Hippe A, Corrigan CJ, Dong C, Homey B, Yao Z, Ying S, Huston DP, Liu YJ (2007) IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med 204(8):1837–1847PubMedPubMedCentralCrossRef Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, Hippe A, Corrigan CJ, Dong C, Homey B, Yao Z, Ying S, Huston DP, Liu YJ (2007) IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med 204(8):1837–1847PubMedPubMedCentralCrossRef
7.
go back to reference Halim TYF, Rana BMJ, Walker JA, Kerscher B, Knolle MD, Jolin HE, Serrao EM, Haim-Vilmovsky L, Teichmann SA, Rodewald HR, Botto M, Vyse TJ, Fallon PG, Li Z, Withers DR, McKenzie ANJ (2018) Tissue-restricted adaptive type 2 immunity is orchestrated by expression of the costimulatory molecule OX40L on group 2 innate lymphoid cells. Immunity 48(6):1195–1207.e6PubMedPubMedCentralCrossRef Halim TYF, Rana BMJ, Walker JA, Kerscher B, Knolle MD, Jolin HE, Serrao EM, Haim-Vilmovsky L, Teichmann SA, Rodewald HR, Botto M, Vyse TJ, Fallon PG, Li Z, Withers DR, McKenzie ANJ (2018) Tissue-restricted adaptive type 2 immunity is orchestrated by expression of the costimulatory molecule OX40L on group 2 innate lymphoid cells. Immunity 48(6):1195–1207.e6PubMedPubMedCentralCrossRef
8.
go back to reference Girardi E, Zajonc DM (2012) Molecular basis of lipid antigen presentation by CD1d and recognition by natural killer T cells. Immunol Rev 250(1):167–179PubMedPubMedCentralCrossRef Girardi E, Zajonc DM (2012) Molecular basis of lipid antigen presentation by CD1d and recognition by natural killer T cells. Immunol Rev 250(1):167–179PubMedPubMedCentralCrossRef
9.
go back to reference Pablos-Tanarro A, Lozano-Ojalvo D, Martínez-Blanco M, Molina M, López-Fandiño R (2018) Egg yolk provides Th2 adjuvant stimuli and promotes sensitization to egg white allergens in BALB/c mice. Mol Nutr Food Res 62(13):e1800057PubMedCrossRef Pablos-Tanarro A, Lozano-Ojalvo D, Martínez-Blanco M, Molina M, López-Fandiño R (2018) Egg yolk provides Th2 adjuvant stimuli and promotes sensitization to egg white allergens in BALB/c mice. Mol Nutr Food Res 62(13):e1800057PubMedCrossRef
10.
go back to reference Anton M (2007) Composition and structure of hen egg yolk. In: Houpalahti R, López-Fandiño R, Anton M, Schade R (eds) Bioactive egg compounds. Springer, Berlin, Heidelberg, New York, pp 1–6 Anton M (2007) Composition and structure of hen egg yolk. In: Houpalahti R, López-Fandiño R, Anton M, Schade R (eds) Bioactive egg compounds. Springer, Berlin, Heidelberg, New York, pp 1–6
11.
go back to reference Graves CL, Harden SW, LaPato M, Nelson M, Amador B, Sorenson H, Frazier CJ, Wallet SM (2014) A method for high purity intestinal epithelial cell culture from adult human and murine tissues for the investigation of innate immune function. J Immunol Methods 414:20–31PubMedPubMedCentralCrossRef Graves CL, Harden SW, LaPato M, Nelson M, Amador B, Sorenson H, Frazier CJ, Wallet SM (2014) A method for high purity intestinal epithelial cell culture from adult human and murine tissues for the investigation of innate immune function. J Immunol Methods 414:20–31PubMedPubMedCentralCrossRef
12.
go back to reference Lozano-Ojalvo D, Pérez-Rodríguez L, Pablos-Tanarro A, Molina E, López-Fandiño R (2017) Hydrolysed ovalbumin offers more effective preventive and therapeutic protection against egg allergy than the intact protein. Clin Exp Allergy 47(10):1342–1354PubMedCrossRef Lozano-Ojalvo D, Pérez-Rodríguez L, Pablos-Tanarro A, Molina E, López-Fandiño R (2017) Hydrolysed ovalbumin offers more effective preventive and therapeutic protection against egg allergy than the intact protein. Clin Exp Allergy 47(10):1342–1354PubMedCrossRef
13.
go back to reference Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408CrossRefPubMed Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408CrossRefPubMed
14.
go back to reference Blázquez AB, Berin MC (2008) Gastrointestinal dendritic cells promote Th2 skewing via OX40L. J Immunol 180(7):4441–4450PubMedCrossRef Blázquez AB, Berin MC (2008) Gastrointestinal dendritic cells promote Th2 skewing via OX40L. J Immunol 180(7):4441–4450PubMedCrossRef
15.
go back to reference Doherty TA (2015) At the bench: understanding group 2 innate lymphoid cells in disease. J Leukoc Biol 97(3):455–467PubMedCrossRef Doherty TA (2015) At the bench: understanding group 2 innate lymphoid cells in disease. J Leukoc Biol 97(3):455–467PubMedCrossRef
16.
go back to reference Williams JW, Tjota MY, Clay BS, Vander Lugt B, Bandukwala HS, Hrusch CL, Decker DC, Blaine KM, Fixsen BR, Singh H, Sciammas R, Sperling AI (2013) Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat Commun 4:2990PubMedPubMedCentralCrossRef Williams JW, Tjota MY, Clay BS, Vander Lugt B, Bandukwala HS, Hrusch CL, Decker DC, Blaine KM, Fixsen BR, Singh H, Sciammas R, Sperling AI (2013) Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat Commun 4:2990PubMedPubMedCentralCrossRef
17.
go back to reference Amsen D, Blander JM, Lee GR, Tanigaki K, Honjo T, Flavell RA (2004) Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117(4):515–526PubMedCrossRef Amsen D, Blander JM, Lee GR, Tanigaki K, Honjo T, Flavell RA (2004) Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117(4):515–526PubMedCrossRef
18.
go back to reference Tordesillas L, Cubells-Baeza N, Gómez-Casado C, Berin C, Esteban V, Barcik W, O'Mahony L, Ramirez C, Pacios LF, Garrido-Arandia M, Díaz-Perales A (2017) Mechanisms underlying induction of allergic sensitization by Pru p 3. Clin Exp Allergy 47(11):1398–1408PubMedPubMedCentralCrossRef Tordesillas L, Cubells-Baeza N, Gómez-Casado C, Berin C, Esteban V, Barcik W, O'Mahony L, Ramirez C, Pacios LF, Garrido-Arandia M, Díaz-Perales A (2017) Mechanisms underlying induction of allergic sensitization by Pru p 3. Clin Exp Allergy 47(11):1398–1408PubMedPubMedCentralCrossRef
19.
go back to reference Jyonouchi S, Abraham V, Orange JS, Spergel JM, Gober L, Dudek E, Saltzman R, Nichols KE, Cianferoni A (2011) Invariant natural killer T cells from children with versus without food allergy exhibit differential responsiveness to milk-derived sphingomyelin. J Allergy Clin Immunol 128(1):102–109.e13PubMedPubMedCentralCrossRef Jyonouchi S, Abraham V, Orange JS, Spergel JM, Gober L, Dudek E, Saltzman R, Nichols KE, Cianferoni A (2011) Invariant natural killer T cells from children with versus without food allergy exhibit differential responsiveness to milk-derived sphingomyelin. J Allergy Clin Immunol 128(1):102–109.e13PubMedPubMedCentralCrossRef
20.
go back to reference Rodriguez MJ, Aranda A, Fernandez TD, Cubells-Baeza N, Torres MJ, Gomez F, Palomares F, Perkins JR, Rojo J, Diaz-Perales MC (2017) LPS promotes Th2 dependent sensitisation leading to anaphylaxis in a Pru p 3 mouse model. Sci Rep 7:40449PubMedPubMedCentralCrossRef Rodriguez MJ, Aranda A, Fernandez TD, Cubells-Baeza N, Torres MJ, Gomez F, Palomares F, Perkins JR, Rojo J, Diaz-Perales MC (2017) LPS promotes Th2 dependent sensitisation leading to anaphylaxis in a Pru p 3 mouse model. Sci Rep 7:40449PubMedPubMedCentralCrossRef
21.
go back to reference Luda KM, Joeris T, Persson EK, Rivollier A, Demiri M, Sitnik KM, Pool L, Holm JB, Melo-Gonzalez F, Richter L, Lambrecht BN, Kristiansen K, Travis MA, Svensson-Frej M, Kotarsky K, Agace WW (2016) IRF8 transcription-factor-dependent classical dendritic cells are essential for intestinal T cell homeostasis. Immunity 44(4):860–874PubMedCrossRef Luda KM, Joeris T, Persson EK, Rivollier A, Demiri M, Sitnik KM, Pool L, Holm JB, Melo-Gonzalez F, Richter L, Lambrecht BN, Kristiansen K, Travis MA, Svensson-Frej M, Kotarsky K, Agace WW (2016) IRF8 transcription-factor-dependent classical dendritic cells are essential for intestinal T cell homeostasis. Immunity 44(4):860–874PubMedCrossRef
22.
go back to reference Ito T, Wang YH, Duramad O, Hori T, Delespesse GJ, Watanabe N, Qin FX, Yao Z, Cao W, Liu YJ (2005) TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med 202(9):1213–1223PubMedPubMedCentralCrossRef Ito T, Wang YH, Duramad O, Hori T, Delespesse GJ, Watanabe N, Qin FX, Yao Z, Cao W, Liu YJ (2005) TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med 202(9):1213–1223PubMedPubMedCentralCrossRef
23.
go back to reference Lozano-Ojalvo D, Martínez-Blanco M, Pérez-Rodríguez L, Molina E, Peláez M, Requena T, López-Fandiño R (2019) Egg white peptide-based immunotherapy enhances vitamin A metabolism and induces RORγt+ regulatory T cells. J Funct Foods 52(1):204–211CrossRef Lozano-Ojalvo D, Martínez-Blanco M, Pérez-Rodríguez L, Molina E, Peláez M, Requena T, López-Fandiño R (2019) Egg white peptide-based immunotherapy enhances vitamin A metabolism and induces RORγt+ regulatory T cells. J Funct Foods 52(1):204–211CrossRef
24.
25.
go back to reference Turner JE, Stockinger B, Helmby H (2013) IL-22 mediates goblet cell hyperplasia and worm expulsion in intestinal helminth infection. PLoS Pathog 9:e1003698PubMedPubMedCentralCrossRef Turner JE, Stockinger B, Helmby H (2013) IL-22 mediates goblet cell hyperplasia and worm expulsion in intestinal helminth infection. PLoS Pathog 9:e1003698PubMedPubMedCentralCrossRef
26.
go back to reference Wang Y, Mumm JB, Herbst R, Kolbeck R, Wang Y (2017) IL-22 increases permeability of intestinal epithelial tight junctions by enhancing claudin-2 expression. J Immunol 199(9):3316–3325PubMedCrossRef Wang Y, Mumm JB, Herbst R, Kolbeck R, Wang Y (2017) IL-22 increases permeability of intestinal epithelial tight junctions by enhancing claudin-2 expression. J Immunol 199(9):3316–3325PubMedCrossRef
27.
go back to reference Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23(5):479–490CrossRefPubMed Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, Zurawski G, Moshrefi M, Qin J, Li X, Gorman DM, Bazan JF, Kastelein RA (2005) IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity 23(5):479–490CrossRefPubMed
28.
go back to reference Kurowska-Stolarska M, Kewin P, Murphy G, Russo RC, Stolarski B, Garcia CC, Komai-Koma M, Pitman N, Li Y, Niedbala W, McKenzie AN, Teixeira MM, Liew FY, Xu D (2008) IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol 181(7):4780–4790PubMedCrossRef Kurowska-Stolarska M, Kewin P, Murphy G, Russo RC, Stolarski B, Garcia CC, Komai-Koma M, Pitman N, Li Y, Niedbala W, McKenzie AN, Teixeira MM, Liew FY, Xu D (2008) IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol 181(7):4780–4790PubMedCrossRef
29.
go back to reference Suzuki T, Yoshinaga N, Tanabe S (2011) Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 286(36):31263–31271PubMedPubMedCentralCrossRef Suzuki T, Yoshinaga N, Tanabe S (2011) Interleukin-6 (IL-6) regulates claudin-2 expression and tight junction permeability in intestinal epithelium. J Biol Chem 286(36):31263–31271PubMedPubMedCentralCrossRef
30.
go back to reference Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70(4):631–659PubMedCrossRef Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70(4):631–659PubMedCrossRef
31.
go back to reference Willemsen LE, Koetsier MA, Balvers M, Beermann C, Stahl B, van Tol EA (2008) Polyunsaturated fatty acids support epithelial barrier integrity and reduce IL-4 mediated permeability in vitro. Eur J Nutr 47(4):183–191PubMedCrossRef Willemsen LE, Koetsier MA, Balvers M, Beermann C, Stahl B, van Tol EA (2008) Polyunsaturated fatty acids support epithelial barrier integrity and reduce IL-4 mediated permeability in vitro. Eur J Nutr 47(4):183–191PubMedCrossRef
32.
go back to reference Noval-Rivas M, Burton OT, Oettgen HC, Chatila T (2016) IL-4 production by group 2 innate lymphoid cells promotes food allergy by blocking regulatory T-cell function. J Allergy Clin Immunol 138(3):801–811.e9PubMedCrossRef Noval-Rivas M, Burton OT, Oettgen HC, Chatila T (2016) IL-4 production by group 2 innate lymphoid cells promotes food allergy by blocking regulatory T-cell function. J Allergy Clin Immunol 138(3):801–811.e9PubMedCrossRef
33.
go back to reference Doherty TA, Broide DH (2018) Lipid regulation of group 2 innate lymphoid cell function: moving beyond epithelial cytokines. J Allergy Clin Immunol 141(5):1587–1589PubMedPubMedCentralCrossRef Doherty TA, Broide DH (2018) Lipid regulation of group 2 innate lymphoid cell function: moving beyond epithelial cytokines. J Allergy Clin Immunol 141(5):1587–1589PubMedPubMedCentralCrossRef
34.
go back to reference Li J, Wang Y, Tang L, de Villiers WJ, Cohen D, Woodward J, Finkelman FD, Eckhardt ER (2013) Dietary medium-chain triglycerides promote oral allergic sensitization and orally induced anaphylaxis to peanut protein in mice. J Allergy Clin Immunol 131(2):442–450PubMedCrossRef Li J, Wang Y, Tang L, de Villiers WJ, Cohen D, Woodward J, Finkelman FD, Eckhardt ER (2013) Dietary medium-chain triglycerides promote oral allergic sensitization and orally induced anaphylaxis to peanut protein in mice. J Allergy Clin Immunol 131(2):442–450PubMedCrossRef
35.
go back to reference Khodoun MV, Tomar S, Tocker JE, Wang YH, Finkelman FD (2018) Prevention of food allergy development and suppression of established food allergy by neutralization of thymic stromal lymphopoietin, IL-25, and IL-33. J Allergy Clin Immunol 141(1):171–179.e1PubMedCrossRef Khodoun MV, Tomar S, Tocker JE, Wang YH, Finkelman FD (2018) Prevention of food allergy development and suppression of established food allergy by neutralization of thymic stromal lymphopoietin, IL-25, and IL-33. J Allergy Clin Immunol 141(1):171–179.e1PubMedCrossRef
36.
go back to reference Chu DK, Mohammed-Ali Z, Jiménez-Saiz R, Walker TD, Goncharova S, Llop-Guevara A, Kong J, Gordon ME, Barra NG, Gillgrass AE, Van Seggelen H, Khan WI, Ashkar AA, Bramson JL, Humbles AA, Kolbeck R, Waserman S, Jordana M (2014) T helper cell IL-4 drives intestinal Th2 priming to oral peanut antigen, under the control of OX40L and independent of innate-like lymphocytes. Mucosal Immunol 7(6):1395–1404PubMedCrossRef Chu DK, Mohammed-Ali Z, Jiménez-Saiz R, Walker TD, Goncharova S, Llop-Guevara A, Kong J, Gordon ME, Barra NG, Gillgrass AE, Van Seggelen H, Khan WI, Ashkar AA, Bramson JL, Humbles AA, Kolbeck R, Waserman S, Jordana M (2014) T helper cell IL-4 drives intestinal Th2 priming to oral peanut antigen, under the control of OX40L and independent of innate-like lymphocytes. Mucosal Immunol 7(6):1395–1404PubMedCrossRef
37.
go back to reference Lee JB, Chen CY, Liu B, Mugge L, Angkasekwinai P, Facchinetti V, Dong C, Liu YJ, Rothenberg ME, Hogan SP, Finkelman FD, Wang YH (2016) IL-25 and CD4+ TH2 cells enhance type 2 innate lymphoid cell-derived IL-13 production, which promotes IgE-mediated experimental food allergy. J Allergy Clin Immunol 137(4):1216–1225 (e1–5)PubMedCrossRef Lee JB, Chen CY, Liu B, Mugge L, Angkasekwinai P, Facchinetti V, Dong C, Liu YJ, Rothenberg ME, Hogan SP, Finkelman FD, Wang YH (2016) IL-25 and CD4+ TH2 cells enhance type 2 innate lymphoid cell-derived IL-13 production, which promotes IgE-mediated experimental food allergy. J Allergy Clin Immunol 137(4):1216–1225 (e1–5)PubMedCrossRef
38.
go back to reference Anjuère F, Luci C, Lebens M, Rousseau D, Hervouet C, Milon G, Holmgren J, Ardavin C, Czerkinsky C (2004) In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J Immunol 173(8):5103–5111PubMedCrossRef Anjuère F, Luci C, Lebens M, Rousseau D, Hervouet C, Milon G, Holmgren J, Ardavin C, Czerkinsky C (2004) In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J Immunol 173(8):5103–5111PubMedCrossRef
39.
go back to reference Roth-Walter F, Berin MC, Arnaboldi P, Escalante CR, Dahan S, Rauch J, Jensen-Jarolim E, Mayer L (2008) Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer's patches. Allergy 63(7):882–890PubMedCrossRef Roth-Walter F, Berin MC, Arnaboldi P, Escalante CR, Dahan S, Rauch J, Jensen-Jarolim E, Mayer L (2008) Pasteurization of milk proteins promotes allergic sensitization by enhancing uptake through Peyer's patches. Allergy 63(7):882–890PubMedCrossRef
40.
go back to reference Besnard AG, Togbe D, Guillou N, Erard F, Quesniaux V, Ryffel B (2011) IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur J Immunol 41(6):1675–1686PubMedCrossRef Besnard AG, Togbe D, Guillou N, Erard F, Quesniaux V, Ryffel B (2011) IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur J Immunol 41(6):1675–1686PubMedCrossRef
41.
go back to reference Su Z, Lin J, Lu F, Zhang X, Zhang L, Gandhi NB, de Paiva CS, Pflugfelder SC, Li DQ (2013) Potential autocrine regulation of interleukin-33/ST2 signaling of dendritic cells in allergic inflammation. Mucosal Immunol 6(5):921–930PubMedPubMedCentralCrossRef Su Z, Lin J, Lu F, Zhang X, Zhang L, Gandhi NB, de Paiva CS, Pflugfelder SC, Li DQ (2013) Potential autocrine regulation of interleukin-33/ST2 signaling of dendritic cells in allergic inflammation. Mucosal Immunol 6(5):921–930PubMedPubMedCentralCrossRef
42.
go back to reference Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H (2009) IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 123(5):1047–1054PubMedPubMedCentralCrossRef Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H (2009) IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 123(5):1047–1054PubMedPubMedCentralCrossRef
43.
go back to reference Yanagawa Y, Suzuki M, Matsumoto M, Togashi H (2011) Prostaglandin E2 enhances IL-33 production by dendritic cells. Immunol Lett 141(1):55–60PubMedCrossRef Yanagawa Y, Suzuki M, Matsumoto M, Togashi H (2011) Prostaglandin E2 enhances IL-33 production by dendritic cells. Immunol Lett 141(1):55–60PubMedCrossRef
45.
go back to reference Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, Hoshino T, Fujimoto J, Nakanishi K (2008) Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 20(6):791–800PubMedCrossRef Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, Hoshino T, Fujimoto J, Nakanishi K (2008) Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 20(6):791–800PubMedCrossRef
46.
go back to reference Komai-Koma M, Brombacher F, Pushparaj PN, Arendse B, McSharry C, Alexander J, Chaudhuri R, Thomson NC, McKenzie AN, McInnes I, Liew FY, Xu D (2012) Interleukin-33 amplifies IgE synthesis and triggers mast cell degranulation via interleukin-4 in naïve mice. Allergy 67(9):1118–1126PubMedPubMedCentralCrossRef Komai-Koma M, Brombacher F, Pushparaj PN, Arendse B, McSharry C, Alexander J, Chaudhuri R, Thomson NC, McKenzie AN, McInnes I, Liew FY, Xu D (2012) Interleukin-33 amplifies IgE synthesis and triggers mast cell degranulation via interleukin-4 in naïve mice. Allergy 67(9):1118–1126PubMedPubMedCentralCrossRef
47.
go back to reference Bourgeois E, Van LP, Samson M, Diem S, Barra A, Roga S, Gombert JM, Schneider E, Dy M, Gourdy P, Girard JP, Herbelin A (2009) The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39(4):1046–1055PubMedCrossRef Bourgeois E, Van LP, Samson M, Diem S, Barra A, Roga S, Gombert JM, Schneider E, Dy M, Gourdy P, Girard JP, Herbelin A (2009) The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur J Immunol 39(4):1046–1055PubMedCrossRef
48.
go back to reference O'Brien TF, Bao K, Dell'Aringa M, Ang WX, Abraham S, Reinhardt RL (2016) Cytokine expression by invariant natural killer T cells is tightly regulated throughout development and settings of type-2 inflammation. Mucosal Immunol 9(3):597–609PubMedCrossRef O'Brien TF, Bao K, Dell'Aringa M, Ang WX, Abraham S, Reinhardt RL (2016) Cytokine expression by invariant natural killer T cells is tightly regulated throughout development and settings of type-2 inflammation. Mucosal Immunol 9(3):597–609PubMedCrossRef
49.
go back to reference Lee YJ, Wang H, Starrett GJ, Phuong V, Jameson SC, Hogquist KA (2015) Tissue-specific distribution of iNKT cells impacts their cytokine response. Immunity 43(3):566–578PubMedPubMedCentralCrossRef Lee YJ, Wang H, Starrett GJ, Phuong V, Jameson SC, Hogquist KA (2015) Tissue-specific distribution of iNKT cells impacts their cytokine response. Immunity 43(3):566–578PubMedPubMedCentralCrossRef
50.
go back to reference Abós-Gracia B, del Moral MG, López-Relaño J, Viana-Huete V, Castro L, Villalba M, Martínez-Naves E (2013) Olea europaea pollen lipids activate invariant natural killer T cells by upregulating CD1d expression on dendritic cells. J Allergy Clin Immunol 131(5):1393–1399.e5PubMedCrossRef Abós-Gracia B, del Moral MG, López-Relaño J, Viana-Huete V, Castro L, Villalba M, Martínez-Naves E (2013) Olea europaea pollen lipids activate invariant natural killer T cells by upregulating CD1d expression on dendritic cells. J Allergy Clin Immunol 131(5):1393–1399.e5PubMedCrossRef
Metadata
Title
Egg yolk augments type 2 immunity by activating innate cells
Authors
Leticia Pérez-Rodríguez
Mónica Martínez-Blanco
Daniel Lozano-Ojalvo
Elena Molina
Rosina López-Fandiño
Publication date
01-10-2020
Publisher
Springer Berlin Heidelberg
Keyword
Cytokines
Published in
European Journal of Nutrition / Issue 7/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-019-02163-6

Other articles of this Issue 7/2020

European Journal of Nutrition 7/2020 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.