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Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention

BACKGROUND: It has become clear that the intestinal microbiota plays a role in food allergies. The objective of this study was to assess the food allergy-preventive effects of combined intake of a short fructan (1-kestose [Kes]) and a long fructan (inulin ([Inu]) in an ovalbumin (OVA)-induced food a...

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Autores principales: Takahashi, Hideaki, Fujii, Tadashi, Yamakawa, Saki, Yamada, Chikako, Fujiki, Kotoyo, Kondo, Nobuhiro, Funasaka, Kohei, Hirooka, Yoshiki, Tochio, Takumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515425/
https://www.ncbi.nlm.nih.gov/pubmed/37737162
http://dx.doi.org/10.1186/s12866-023-03021-6
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author Takahashi, Hideaki
Fujii, Tadashi
Yamakawa, Saki
Yamada, Chikako
Fujiki, Kotoyo
Kondo, Nobuhiro
Funasaka, Kohei
Hirooka, Yoshiki
Tochio, Takumi
author_facet Takahashi, Hideaki
Fujii, Tadashi
Yamakawa, Saki
Yamada, Chikako
Fujiki, Kotoyo
Kondo, Nobuhiro
Funasaka, Kohei
Hirooka, Yoshiki
Tochio, Takumi
author_sort Takahashi, Hideaki
collection PubMed
description BACKGROUND: It has become clear that the intestinal microbiota plays a role in food allergies. The objective of this study was to assess the food allergy-preventive effects of combined intake of a short fructan (1-kestose [Kes]) and a long fructan (inulin ([Inu]) in an ovalbumin (OVA)-induced food allergy mouse model. RESULTS: Oral administration of fructans lowered the allergenic symptom score and alleviated the decreases in rectal temperature and total IgA levels and increases in OVA-specific IgE and IgA levels induced by high-dose OVA challenge, and in particular, combined intake of Kes and Inu significantly suppressed the changes in all these parameters. The expression of the pro-inflammatory cytokine IL-4, which was increased in the allergy model group, was significantly suppressed by fructan administration, and the expression of the anti-inflammatory cytokine IL-10 was significantly increased upon Kes administration. 16 S rRNA amplicon sequencing of the gut microbiota and beta diversity analysis revealed that fructan administration may induce gut microbiota resistance to food allergy sensitization, rather than returning the gut microbiota to a non-sensitized state. The relative abundances of the genera Parabacteroides B 862,066 and Alloprevotella, which were significantly reduced by food allergy sensitization, were restored by fructan administration. In Parabacteroides, the relative abundances of Parabacteroides distasonis, Parabacteroides goldsteinii, and their fructan-degrading glycoside hydrolase family 32 gene copy numbers were increased upon Kes or Inu administration. The concentrations of short-chain fatty acids (acetate and propionate) and lactate were increased by fructan administration, especially significantly in the Kes + Inu, Kes, and Inu-fed (Inu, Kes + Inu) groups. CONCLUSION: Combined intake of Kes and Inu suppressed allergy scores more effectively than single intake, suggesting that Kes and Inu have different allergy-preventive mechanisms. This indicates that the combined intake of these short and long fructans may have an allergy-preventive benefit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-03021-6.
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spelling pubmed-105154252023-09-23 Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention Takahashi, Hideaki Fujii, Tadashi Yamakawa, Saki Yamada, Chikako Fujiki, Kotoyo Kondo, Nobuhiro Funasaka, Kohei Hirooka, Yoshiki Tochio, Takumi BMC Microbiol Research BACKGROUND: It has become clear that the intestinal microbiota plays a role in food allergies. The objective of this study was to assess the food allergy-preventive effects of combined intake of a short fructan (1-kestose [Kes]) and a long fructan (inulin ([Inu]) in an ovalbumin (OVA)-induced food allergy mouse model. RESULTS: Oral administration of fructans lowered the allergenic symptom score and alleviated the decreases in rectal temperature and total IgA levels and increases in OVA-specific IgE and IgA levels induced by high-dose OVA challenge, and in particular, combined intake of Kes and Inu significantly suppressed the changes in all these parameters. The expression of the pro-inflammatory cytokine IL-4, which was increased in the allergy model group, was significantly suppressed by fructan administration, and the expression of the anti-inflammatory cytokine IL-10 was significantly increased upon Kes administration. 16 S rRNA amplicon sequencing of the gut microbiota and beta diversity analysis revealed that fructan administration may induce gut microbiota resistance to food allergy sensitization, rather than returning the gut microbiota to a non-sensitized state. The relative abundances of the genera Parabacteroides B 862,066 and Alloprevotella, which were significantly reduced by food allergy sensitization, were restored by fructan administration. In Parabacteroides, the relative abundances of Parabacteroides distasonis, Parabacteroides goldsteinii, and their fructan-degrading glycoside hydrolase family 32 gene copy numbers were increased upon Kes or Inu administration. The concentrations of short-chain fatty acids (acetate and propionate) and lactate were increased by fructan administration, especially significantly in the Kes + Inu, Kes, and Inu-fed (Inu, Kes + Inu) groups. CONCLUSION: Combined intake of Kes and Inu suppressed allergy scores more effectively than single intake, suggesting that Kes and Inu have different allergy-preventive mechanisms. This indicates that the combined intake of these short and long fructans may have an allergy-preventive benefit. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-023-03021-6. BioMed Central 2023-09-22 /pmc/articles/PMC10515425/ /pubmed/37737162 http://dx.doi.org/10.1186/s12866-023-03021-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Takahashi, Hideaki
Fujii, Tadashi
Yamakawa, Saki
Yamada, Chikako
Fujiki, Kotoyo
Kondo, Nobuhiro
Funasaka, Kohei
Hirooka, Yoshiki
Tochio, Takumi
Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title_full Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title_fullStr Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title_full_unstemmed Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title_short Combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
title_sort combined oral intake of short and long fructans alters the gut microbiota in food allergy model mice and contributes to food allergy prevention
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10515425/
https://www.ncbi.nlm.nih.gov/pubmed/37737162
http://dx.doi.org/10.1186/s12866-023-03021-6
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