Modulation of gut immune response by probiotic fermented milk consumption to control IgE in a respiratory allergy model
äºBeneficial MicrobesInstituto de Medicina Molecular y Celular Aplicada (IMMCA), Dorrego 1080, 4000, Tucumán, Argentina.
Search for other papers by E. Velez in
Current site
Google Scholar
Search for other papers by I. Novotny-Nuñez in
Current site
Google Scholar
Search for other papers by S. Correa in
Current site
Google Scholar
Search for other papers by G. Perdigón in
Current site
Google Scholar
Centro de referencia para Lactobacilos (CERELA-CONICET), Chacabuco 145, 4000 Tucumán, Argentina.
Search for other papers by C. Maldonado-Galdeano in
Current site
Google Scholar
Allergies are a world increasing health issue and most treatments are oriented to alleviate symptoms. Probiotics have several health benefits including the improvement of the immune system. In previous work we found that consumption of commercial probiotic fermented milk (PFM) significantly reduced specific-immunoglobulin (Ig) E in serum and lungs by increasing specific-IgG and controlled allergic response to ovalbumin (OVA) in an adult mouse respiratory allergy model. Here we continued our study determining the mechanism triggered in the gut by the PFM ingestion that influenced the results previously reported. Five groups of BALB/c mice were assessed: normal-control, basal (drinks PFM five days without OVA sensitisation), sensitisation-control (no PFM intake), previous and continuous-PFM administration. Allergen administration: 3 OVA injections (1% in PBS) followed by aerosols exposure for 7 days. We determined total secretory-IgA and cytokines in small intestine (SI) fluid; CD11b+, CD103+, IgA+ cells and cytokine producing cells in SI tissue. In lungs we analysed co-expression of CD4/interferon (IFN)-γ or CD4/interleukin (IL)-10, IgE+ cells and IL-12 production. Results: continuous intake of PFM increased the expression of CD103 marker and decreased CD11b and pro-inflammatory cytokines. Coexpression of CD4/IFN-γ was confirmed in lungs of animals that consumed PFM continuously. This group had a lower count of IgE+ cells and a higher concentration of IL-12. The consumption of PFM reinforces the mucosal barrier by increasing IgA+ cells and induces signalling from the intestine to the lungs by increasing the expression of CD103+ dendritic cells related to regulatory mechanisms. The results found in this work together with those previously reported demonstrated that the intake of PFM induces a clear balance towards the Th1 response, preventing the Th2 allergic response by controlling the previously reported IgE level. According to our model, the intake of PFM could be a good strategy to alleviate the development of allergies.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
-
Abbas, A.K., Lichtman, A.H.H. and Pillai, S., 2011. Cellular and Molecular Immunology. Elsevier, Amsterdam, the Netherlands.
'Cellular and Molecular Immunology', ().
-
Bäckhed, F., Roswall, J., Peng, Y., Feng, Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., Khan, M.T., Zhang, J., Li, J., Xiao, L., Al-Aama, J., Zhang, D., Lee, Y.S., Kotowska, D., Colding, C., Tremaroli, V., Yin, Y., Bergman, S., Xu, X., Madsen, L., Kristiansen, K., Dahlgren, J. and Wang, J., 2015. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17: 690-703. https://doi.org/10.1016/j.chom.2015.04.004
-
Bernardo, D., 2013. Human intestinal dendritic cells as controllers of mucosal immunity. Revista Española de Enfermedades Digestivas 105: 279-290. https://doi.org/10.4321/s1130-01082013000500006
-
Blumenthal, K.G., Peter, J.G., Trubiano, J.A. and Phillips, E.J., 2019. Antibiotic allergy. The Lancet 393: 183-198. https://doi.org/10.1016/10.1016/s0140-6736(18)32218-9
-
Brown, E.M., Arrieta, M.C. and Finlay, B.B., 2013. A fresh look at the hygiene hypothesis: how intestinal microbial exposure drives immune effector responses in atopic disease. Seminars in Immunology 25: 378-387. https://doi.org/10.1016/10.1016/j.smim.2013.09.003
-
Cai, S., Batra, S., Langohr, I., Iwakura, Y. and Jeyaseelan, S., 2016. IFN-γ induction by neutrophil-derived IL-17A homodimer augments pulmonary antibacterial defense. Mucosal Immunology 9: 718-729. https://doi.org/10.1016/10.1038/mi.2015.95
-
Cosenza, L., Nocerino, R., Di Scala, C., Di Costanzo, M., Amoroso, A., Leone, L., Paparo, L., Pezzella, C., Aitoro, R. and Berni Canani, R., 2015. Bugs for atopy: the Lactobacillus rhamnosus GG strategy for food allergy prevention and treatment in children. Beneficial Microbes 6: 225-232. https://doi.org/10.1016/10.3920/bm2014.0158
-
Cuvelier, C., Barbatis, C., Mielants, H., De Vos, M., Roels, H. and Veys, E., 1987. Histopathology of intestinal inflammation related to reactive arthritis. Gut 28: 394-401. https://doi.org/10.1136/gut.28.4.394
-
De Martinis, M., Sirufo, M.M., Suppa, M. and Ginaldi, L., 2020. New perspectives in food allergy. International Journal of Molecular Science 21. https://doi.org/10.1016/10.3390/ijms21041474
-
De Moreno de LeBlanc, A., Dogi, C.A., Galdeano, C.M., Carmuega, E., Weill, R. and Perdigon, G., 2008. Effect of the administration of a fermented milk containing Lactobacillus casei DN-114001 on intestinal microbiota and gut associated immune cells of nursing mice and after weaning until immune maturity. BMC Immunology 9: 27. https://doi.org/10.1016/10.1186/1471-2172-9-27
-
De Moreno de LeBlanc, A., Galdeano, C.M., Chaves, S. and Perdigón, G., 2005. Oral Administration of L. casei CRL 431 increases immunity in bronchus and mammary glands. European Journal of Inflammation 3: 23-28. https://doi.org/10.1016/10.1177/1721727X0500300105
-
Forsythe, P., Wang, B., Khambati, I. and Kunze, W.A., 2012. Systemic effects of ingested Lactobacillus rhamnosus: inhibition of mast cell membrane potassium (IKCa) current and degranulation. PLoS ONE 7: e41234. https://doi.org/10.1016/10.1371/journal.pone.0041234
-
Gauvreau, G.M., El-Gammal, A.I. and OâByrne, P.M., 2015. Allergen-induced airway responses. European Respiratory Journal 46: 819-831. https://doi.org/10.1016/10.1183/13993003.00536-2015
-
Good, M., Kolls, J.K. and McGarr Empey, K., 2017. Neonatal pulmonary host defense. In: Polin, R.A., Abman, S.H., Rowitch, D.H., Benitz, W.E. and Fox, W.W. (eds.) Fetal and neonatal physiology (5th ed.). Elsevier, Amsterdam, the Netherlands, pp. 1262-1293.e1212.
'Neonatal pulmonary host defense ', () 1262 -1293.e1212.
-
Guo, C. and Zhang, L., 2010. [Cholesterol-lowering effects of probiotics â a review]. Wei Sheng Wu Xue Bao 50: 1590-1599.
'Cholesterol-lowering effects of probiotics â a review ' () 50 Wei Sheng Wu Xue Bao : 1590 -1599.
-
Hattori, K., Nishikawa, M., Watcharanurak, K., Ikoma, A., Kabashima, K., Toyota, H., Takahashi, Y., Takahashi, R., Watanabe, Y. and Takakura, Y., 2010. Sustained exogenous expression of therapeutic levels of IFN-gamma ameliorates atopic dermatitis in NC/Nga mice via Th1 polarization. Journal of Immunology 184: 2729-2735. https://doi.org/10.1016/10.4049/jimmunol.0900215
-
He, F., Morita, H., Hashimoto, H., Hosoda, M., Kurisaki, J., Ouwehand, A.C., Isolauri, E., Benno, Y. and Salminen, S., 2002. Intestinal Bifidobacterium species induce varying cytokine production. Journal of Allergy and Clinical Immunology 109: 1035-1036. https://doi.org/10.1016/10.1067/mai.2002.124894
-
Johnson, C.C. and Ownby, D.R., 2016. Allergies and asthma: do atopic disorders result from inadequate immune homeostasis arising from infant gut dysbiosis? Expert Review of Clinical Immunology 12: 379-388. https://doi.org/10.1016/10.1586/1744666x.2016.1139452
-
Johnson, C.C. and Ownby, D.R., 2017. The infant gut bacterial microbiota and risk of pediatric asthma and allergic diseases. Translational Research 179: 60-70. https://doi.org/10.1016/10.1016/j.trsl.2016.06.010
-
Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P. and Isolauri, E., 2001. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. The Lancet 357: 1076-1079. https://doi.org/10.1016/10.1016/s0140-6736(00)04259-8
-
Lam, Y.F., Tong, K.K., Kwan, K.M., Tsuneyama, K., Shu, S.A., Leung, P.S. and Chu, K.H., 2015. Gastrointestinal immune response to the shrimp allergen tropomyosin: histological and immunological analysis in an animal model of shrimp tropomyosin hypersensitivity. International Archives of Allergy and Immunology 167: 29-40. https://doi.org/10.1016/10.1159/000431228
-
Larenas-Linnemann, D., Sánchez-Borges, M., Del RÃo-Navarro, B.E., Alonzo-Romero Pareyón Mde, L., Maldonado-GarcÃa, C.A., Mendoza-López, E., Ortega-Martell, J.A., Sienra-Monge, J.J., Medina-Ãvalos, M.A., Rojo-Gutiérrez, M.I., Beirana-Palencia, A.M., Vargas-Correa, J.B., Báez-Loyola, C., RamÃrez-Segura, R.I. and Guzmán-Perea, M.G., 2015. [Antihistamines for the treatment of urticaria in Mexico]. Revista Alergia Mexico 62: 157-174.
'Antihistamines for the treatment of urticaria in Mexico ' () 62 Revista Alergia Mexico : 157 -174.
-
Leung, A.S.Y., Wong, G.W.K. and Tang, M.L.K., 2018. Food allergy in the developing world. Journal of Allergy and Clinical Immunology 141: 76-78 e71. https://doi.org/10.1016/10.1016/j.jaci.2017.11.008
-
Maldonado Galdeano, C., Cazorla, S.I., Perdigon, G. and Lemme Dumit, J.M., 2018. Evidencias cientÃficas de los mecanismos inducidos por probióticos en la modulación del sistema inmune. In: Weill, R., De Paula, J.A. and Vinderola, G. (eds.) Probióticos: Su impacto en la nutrición y la salud. Una visión desde el cono sur. Asociación Civil Danone para la Nutrición, la Salud y la Calidad de Vida, Buenos Aires, Argentina, pp. 157-178.
'Evidencias cientÃficas de los mecanismos inducidos por probióticos en la modulación del sistema inmune ', () 157 -178.
-
Maldonado Galdeano, C., Lemme Dumit, J.M., Velez, E.M. and Perdigón, G., 2016. Sistema inmune de las mucosas. Influencia bacteriana en la activación y homeostasis intestinal. In: Ãlvarez Calatayud, G., Marcos, A. and Margolles, A. (eds.) Probióticos, prebióticos y salud: Evidencia cientÃfica. Sociedad Española de Probióticos y Prebiótico, Madrid, Spain, pp. 133-138.
'Sistema inmune de las mucosas ', () 133 -138.
-
Maldonado Galdeano, C., Novotny Nuñez, I., Carmuega, E., de Moreno de LeBlanc, A. and Perdigón, G., 2015. Role of probiotics and functional foods in health: gut immune stimulation by two probiotic strains and a potential probiotic yoghurt. Endocrine, Metabolic and Immune Disorders â Drug Targets 15: 37-45. https://doi.org/10.1016/10.2174/1871530314666141216121349
-
Maldonado Galdeano, C., Novotny Nunez, I., De Moreno de LeBlanc, A., Carmuega, E., Weill, R. and Perdigon, G., 2011. Impact of a probiotic fermented milk in the gut ecosystem and in the systemic immunity using a non-severe protein-energy-malnutrition model in mice. BMC Gastroenterology 11: 64. https://doi.org/10.1016/10.1186/1471-230x-11-64
-
Mora, J.R. and Von Andrian, U.H., 2009. Role of retinoic acid in the imprinting of gut-homing IgA-secreting cells. Seminars in Immunology 21: 28-35. https://doi.org/10.1016/10.1016/j.smim.2008.08.002
-
Motta, J.M. and Rumjanek, V.M., 2016. Sensitivity of dendritic cells to microenvironment signals. Journal of Immunology Research 2016: 4753607. https://doi.org/10.1016/10.1155/2016/4753607
-
Muzaki, A.R., Tetlak, P., Sheng, J., Loh, S.C., Setiagani, Y.A., Poidinger, M., Zolezzi, F., Karjalainen, K. and Ruedl, C., 2016. Intestinal CD103(+)CD11b(-) dendritic cells restrain colitis via IFN-γ-induced anti-inflammatory response in epithelial cells. Mucosal Immunology 9: 336-351. https://doi.org/10.1016/10.1038/mi.2015.64
-
Ouwehand, A.C., 2007. Antiallergic effects of probiotics. Journal of Nutrition 137: 794S-797S. https://doi.org/10.1016/10.1093/jn/137.3.794S
-
Park, J.H., Um, J.I., Lee, B.J., Goh, J.S., Park, S.Y., Kim, W.S. and Kim, P.H., 2002. Encapsulated Bifidobacterium bifidum potentiates intestinal IgA production. Cell Immunology 219: 22-27. https://doi.org/10.1016/10.1016/s0008-8749(02)00579-8
-
Prepageran, N., Wang, D.Y., Nair, G. and Maurer, M., 2014. The status quo and unmet needs in the management of allergic rhinitis and chronic rhinosinusitis: a Malaysian perspective. Asia Pacific Allergy 4: 142-148. https://doi.org/10.1016/10.5415/apallergy.2014.4.3.142
-
Randazzo, C.L., Pino, A., Ricciardi, L., Romano, C., Comito, D., Arena, E., Saitta, S. and Caggia, C., 2015. Probiotic supplementation in systemic nickel allergy syndrome patients: study of its effects on lactic acid bacteria population and on clinical symptoms. Journal of Applied Microbiology 118: 202-211. https://doi.org/10.1016/10.1111/jam.12685
-
Ren, C., Dokter-Fokkens, J., Figueroa Lozano, S., Zhang, Q., De Haan, B.J., Zhang, H., Faas, M.M. and De Vos, P., 2018. Lactic acid bacteria may impact intestinal barrier function by modulating goblet cells. Molecular Nutrition and Food Research 62: e1700572. https://doi.org/10.1016/10.1002/mnfr.201700572
-
Sainte-Marie, G., 1962. A paraffin embedding technique for studies employing immunofluorescence. Journal of Histochemistry and Cytochemistry 10: 250-256. https://doi.org/10.1016/10.1177/10.3.250
-
Salameh, M., Burney, Z., Mhaimeed, N., Laswi, I., Yousri, N.A., Bendriss, G. and Zakaria, D., 2020. The role of gut microbiota in atopic asthma and allergy, implications in the understanding of disease pathogenesis. Scandinavian Journal of Immunology 91: e12855. 10.1111/sji.12855
'The role of gut microbiota in atopic asthma and allergy, implications in the understanding of disease pathogenesis ' () 91 Scandinavian Journal of Immunology : e12855.
-
Schwarzer, M., Srutkova, D., Schabussova, I., Hudcovic, T., Akgün, J., Wiedermann, U. and Kozakova, H., 2013. Neonatal colonization of germ-free mice with Bifidobacterium longum prevents allergic sensitization to major birch pollen allergen Bet v 1. Vaccine 31: 5405-5412. https://doi.org/10.1016/10.1016/j.vaccine.2013.09.014
-
Segura, E. and Amigorena, S., 2013. Inflammatory dendritic cells in mice and humans. Trends in Immunology 34: 440-445. https://doi.org/10.1016/10.1016/j.it.2013.06.001
-
Sigmundsdottir, H. and Butcher, E.C., 2008. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nature Immunology 9: 981-987. https://doi.org/10.1016/10.1038/ni.f.208
-
Solovjov, D.A., Pluskota, E. and Plow, E.F., 2005. Distinct roles for the alpha and beta subunits in the functions of integrin alphaMbeta2. Journal of Biological Chemistry 280: 1336-1345. https://doi.org/10.1016/10.1074/jbc.M406968200
-
Suzuki, K., Maruya, M., Kawamoto, S., Sitnik, K., Kitamura, H., Agace, W.W. and Fagarasan, S., 2010. The sensing of environmental stimuli by follicular dendritic cells promotes immunoglobulin A generation in the gut. Immunity 33: 71-83. https://doi.org/10.1016/10.1016/j.immuni.2010.07.003
-
Tan-Lim, C.S.C. and Esteban-Ipac, N.A.R., 2018. Probiotics as treatment for food allergies among pediatric patients: a meta-analysis. World Allergy Organization Journal 11: 25. https://doi.org/10.1016/10.1186/s40413-018-0204-5
-
Tang, M.L., Ponsonby, A.L., Orsini, F., Tey, D., Robinson, M., Su, E.L., Licciardi, P., Burks, W. and Donath, S., 2015. Administration of a probiotic with peanut oral immunotherapy: a randomized trial. Journal of Allergy and Clinical Immunology 135: 737-744 e738. https://doi.org/10.1016/10.1016/j.jaci.2014.11.034
-
Untersmayr, E., Bax, H.J., Bergmann, C., Bianchini, R., Cozen, W., Gould, H.J., Hartmann, K., Josephs, D.H., Levi-Schaffer, F., Penichet, M.L., OâMahony, L., Poli, A., Redegeld, F.A., Roth-Walter, F., Turner, M.C., Vangelista, L., Karagiannis, S.N. and Jensen-Jarolim, E., 2019. AllergoOncology: microbiota in allergy and cancer â a European Academy for Allergy and Clinical Immunology position paper. Allergy 74: 1037-1051. https://doi.org/10.1016/10.1111/all.13718
-
Valenta, R., Karaulov, A., Niederberger, V., Gattinger, P., van Hage, M., Flicker, S., Linhart, B., Campana, R., Focke-Tejkl, M., Curin, M., Eckl-Dorna, J., Lupinek, C., Resch-Marat, Y., Vrtala, S., Mittermann, I., Garib, V., Khaitov, M., Valent, P. and Pickl, W.F., 2018. Molecular aspects of allergens and allergy. Advances in Immunology 138: 195-256. https://doi.org/10.1016/10.1016/bs.ai.2018.03.002
-
Van Overtvelt, L., Moussu, H., Horiot, S., Samson, S., Lombardi, V., Mascarell, L., van de Moer, A., Bourdet-Sicard, R. and Moingeon, P., 2010. Lactic acid bacteria as adjuvants for sublingual allergy vaccines. Vaccine 28: 2986-2992. https://doi.org/10.1016/10.1016/j.vaccine.2010.02.009
-
Van Vliet, M.J., Harmsen, H.J., de Bont, E.S. and Tissing, W.J., 2010. The role of intestinal microbiota in the development and severity of chemotherapy-induced mucositis. PLoS Pathogens 6: e1000879. https://doi.org/10.1016/10.1371/journal.ppat.1000879
-
Velez, E.M., Maldonado Galdeano, C., Carmuega, E., Weill, R., Bibas Bonet, M.E. and Perdigon, G., 2015. Probiotic fermented milk consumption modulates the allergic process induced by ovoalbumin in mice. British Journal of Nutrition 114: 566-576. https://doi.org/10.1016/10.1017/s0007114515001981
-
Viggiano, D., Ianiro, G., Vanella, G., Bibbò, S., Bruno, G., Simeone, G. and Mele, G., 2015. Gut barrier in health and disease: focus on childhood. European Review for Medical and Pharmacological Sciences 19: 1077-1085.
'Gut barrier in health and disease: focus on childhood ' () 19 European Review for Medical and Pharmacological Sciences : 1077 -1085.
Supplementary Materials
| å ¨é¨æé´ | è¿å»ä¸å¹´ | è¿å»30天 | |
|---|---|---|---|
| æè¦æµè§æ¬¡æ° | 480 | 157 | 9 |
| å ¨ææµè§æ¬¡æ° | 15 | 3 | 1 |
| PDFä¸è½½æ¬¡æ° | 18 | 3 | 3 |
Modulation of gut immune response by probiotic fermented milk consumption to control IgE in a respiratory allergy model
äºBeneficial MicrobesInstituto de Medicina Molecular y Celular Aplicada (IMMCA), Dorrego 1080, 4000, Tucumán, Argentina.
Search for other papers by E. Velez in
Current site
Google Scholar
PubMed
Search for other papers by I. Novotny-Nuñez in
Current site
Google Scholar
PubMed
Search for other papers by S. Correa in
Current site
Google Scholar
PubMed
Search for other papers by G. Perdigón in
Current site
Google Scholar
PubMed
Centro de referencia para Lactobacilos (CERELA-CONICET), Chacabuco 145, 4000 Tucumán, Argentina.
Search for other papers by C. Maldonado-Galdeano in
Current site
Google Scholar
PubMed
Allergies are a world increasing health issue and most treatments are oriented to alleviate symptoms. Probiotics have several health benefits including the improvement of the immune system. In previous work we found that consumption of commercial probiotic fermented milk (PFM) significantly reduced specific-immunoglobulin (Ig) E in serum and lungs by increasing specific-IgG and controlled allergic response to ovalbumin (OVA) in an adult mouse respiratory allergy model. Here we continued our study determining the mechanism triggered in the gut by the PFM ingestion that influenced the results previously reported. Five groups of BALB/c mice were assessed: normal-control, basal (drinks PFM five days without OVA sensitisation), sensitisation-control (no PFM intake), previous and continuous-PFM administration. Allergen administration: 3 OVA injections (1% in PBS) followed by aerosols exposure for 7 days. We determined total secretory-IgA and cytokines in small intestine (SI) fluid; CD11b+, CD103+, IgA+ cells and cytokine producing cells in SI tissue. In lungs we analysed co-expression of CD4/interferon (IFN)-γ or CD4/interleukin (IL)-10, IgE+ cells and IL-12 production. Results: continuous intake of PFM increased the expression of CD103 marker and decreased CD11b and pro-inflammatory cytokines. Coexpression of CD4/IFN-γ was confirmed in lungs of animals that consumed PFM continuously. This group had a lower count of IgE+ cells and a higher concentration of IL-12. The consumption of PFM reinforces the mucosal barrier by increasing IgA+ cells and induces signalling from the intestine to the lungs by increasing the expression of CD103+ dendritic cells related to regulatory mechanisms. The results found in this work together with those previously reported demonstrated that the intake of PFM induces a clear balance towards the Th1 response, preventing the Th2 allergic response by controlling the previously reported IgE level. According to our model, the intake of PFM could be a good strategy to alleviate the development of allergies.
| å ¨é¨æé´ | è¿å»ä¸å¹´ | è¿å»30天 | |
|---|---|---|---|
| æè¦æµè§æ¬¡æ° | 480 | 157 | 9 |
| å ¨ææµè§æ¬¡æ° | 15 | 3 | 1 |
| PDFä¸è½½æ¬¡æ° | 18 | 3 | 3 |
