Continuous intake of resistant maltodextrin enhanced intestinal immune response through changes in the intestinal environment in mice

Shoko Miyazato, Yuka Kishimoto, Kyoko Takahashi, Shuichi Kaminogawa, Akira Hosono, Shoko Miyazato, Yuka Kishimoto, Kyoko Takahashi, Shuichi Kaminogawa, Akira Hosono

Abstract

We investigated the effect of resistant maltodextrin (RMD), a non-viscous soluble dietary fiber, on intestinal immune response and its mechanism in mice. Intestinal and fecal immunoglobulin A (IgA) were determined as indicators of intestinal immune response, and changes in the intestinal environment were focused to study the mechanism. BALB/c mice were fed one of three experimental diets, a control diet or a diet containing either 5% or 7.5% RMD, for two weeks. Continuous intake of RMD dose-dependently increased total IgA levels in the intestinal tract. Total IgA production from the cecal mucosa was significantly increased by RMD intake, while there were no significant differences in mucosal IgA production between the control group and experimental groups in the small intestine and colon. Continuous intake of RMD changed the composition of the cecal contents; that is, the composition of the cecal microbiota was changed, and short-chain fatty acids (SCFAs) were increased. There was an increased trend in Bacteroidales in the cecal microbiota, and butyrate, an SCFA, was significantly increased. Our study demonstrated that continuous intake of RMD enhanced the intestinal immune response by increasing the production of IgA in the intestinal tract. It suggested that the increase in total SCFAs and changes in the intestinal microbiota resulting from the fermentation of RMD orally ingested were associated with the induction of IgA production in intestinal immune cells, with the IgA production of the cecal mucosa in particular being significantly increased.

Keywords: IgA; cecal fermentation; cecal microbiota; resistant maltodextrin; short-chain fatty acid.

Figures

Fig. 1.
Fig. 1.
Effect of dietary RMD on total IgA amount in the intestinal tracts and feces of mice. (a) Total IgA amount in the intestinal tract including intestinal content (n=12). (b) Total IgA amount in feces excreted for 24 hours (n=3). BALB/c mice were fed diets containing 5% or 7.5% RMD and the IgA levels in the intestinal tract and feces were determined. Data are presented as the mean ± SD. *Significant difference from the control group (p

Fig. 2.

Effect of dietary RMD on…

Fig. 2.

Effect of dietary RMD on total IgA production from the intestinal mucosa in…

Fig. 2.
Effect of dietary RMD on total IgA production from the intestinal mucosa in mice. (a) Small intestine, (b) Cecum, (c) Colon BALB/c mice were fed diets containing 5% or 7.5% RMD. Intestines were divided into 3 segments, the small intestine, cecum and colon, and IgA levels in mucosal extracts were determined. Each circle represents an individual mouse (n=11). *Significant difference from the control group (p

Fig. 3.

Effect of dietary RMD on…

Fig. 3.

Effect of dietary RMD on the composition of the cecal microbiota analyzed by…

Fig. 3.
Effect of dietary RMD on the composition of the cecal microbiota analyzed by the T-RFLP method. BALB/c mice were fed diets conctaining 5% or 7.5% RMD for 2 weeks. Data are presented as the mean and are expressed in percentage. *Significant difference from the control group (p

Fig. 4.

Effect of RMD on SCFAs…

Fig. 4.

Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed…

Fig. 4.
Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed diets containing 5% or 7.5% RMD for 2 weeks. Data are presented as the mean ± SD (n=6). *Significant difference from the control group (p
Similar articles
Cited by
References
    1. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N, Iwase T, Moro I. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin Exp Immunol 137: 52–58. - PMC - PubMed
    1. Sato T, Nakamura Y, Ozawa O. 2008. Effect of galactooligosaccharides on immune system in mice. J Jpn Soc Nutr Food Sci 61: 79–88.
    1. Hino K, Kurose M, Sakurai T, Inoue S, Oku K, Chaen H, Fukuda S. 2007. Effect of dietary lactosucrose (4G-β-D-galactosylsucrose) on the intestinal immune functions in mice. J Appl Glycosci 54: 169–172.
    1. Fastinger ND, Karr-Lilienthal LK, Spears JK, Swanson KS, Zinn KE, Nava GM, Ohkuma K, Kanahori S, Gordon DT, Fahey GC., Jr 2008. A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27: 356–366. - PubMed
    1. Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H. 2010. Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49: 165–171. - PMC - PubMed
Show all 19 references
Related information
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig. 2.
Fig. 2.
Effect of dietary RMD on total IgA production from the intestinal mucosa in mice. (a) Small intestine, (b) Cecum, (c) Colon BALB/c mice were fed diets containing 5% or 7.5% RMD. Intestines were divided into 3 segments, the small intestine, cecum and colon, and IgA levels in mucosal extracts were determined. Each circle represents an individual mouse (n=11). *Significant difference from the control group (p

Fig. 3.

Effect of dietary RMD on…

Fig. 3.

Effect of dietary RMD on the composition of the cecal microbiota analyzed by…

Fig. 3.
Effect of dietary RMD on the composition of the cecal microbiota analyzed by the T-RFLP method. BALB/c mice were fed diets conctaining 5% or 7.5% RMD for 2 weeks. Data are presented as the mean and are expressed in percentage. *Significant difference from the control group (p

Fig. 4.

Effect of RMD on SCFAs…

Fig. 4.

Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed…

Fig. 4.
Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed diets containing 5% or 7.5% RMD for 2 weeks. Data are presented as the mean ± SD (n=6). *Significant difference from the control group (p
Similar articles
Cited by
References
    1. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N, Iwase T, Moro I. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin Exp Immunol 137: 52–58. - PMC - PubMed
    1. Sato T, Nakamura Y, Ozawa O. 2008. Effect of galactooligosaccharides on immune system in mice. J Jpn Soc Nutr Food Sci 61: 79–88.
    1. Hino K, Kurose M, Sakurai T, Inoue S, Oku K, Chaen H, Fukuda S. 2007. Effect of dietary lactosucrose (4G-β-D-galactosylsucrose) on the intestinal immune functions in mice. J Appl Glycosci 54: 169–172.
    1. Fastinger ND, Karr-Lilienthal LK, Spears JK, Swanson KS, Zinn KE, Nava GM, Ohkuma K, Kanahori S, Gordon DT, Fahey GC., Jr 2008. A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27: 356–366. - PubMed
    1. Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H. 2010. Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49: 165–171. - PMC - PubMed
Show all 19 references
Related information
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig. 3.
Fig. 3.
Effect of dietary RMD on the composition of the cecal microbiota analyzed by the T-RFLP method. BALB/c mice were fed diets conctaining 5% or 7.5% RMD for 2 weeks. Data are presented as the mean and are expressed in percentage. *Significant difference from the control group (p

Fig. 4.

Effect of RMD on SCFAs…

Fig. 4.

Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed…

Fig. 4.
Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed diets containing 5% or 7.5% RMD for 2 weeks. Data are presented as the mean ± SD (n=6). *Significant difference from the control group (p
Similar articles
Cited by
References
    1. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N, Iwase T, Moro I. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin Exp Immunol 137: 52–58. - PMC - PubMed
    1. Sato T, Nakamura Y, Ozawa O. 2008. Effect of galactooligosaccharides on immune system in mice. J Jpn Soc Nutr Food Sci 61: 79–88.
    1. Hino K, Kurose M, Sakurai T, Inoue S, Oku K, Chaen H, Fukuda S. 2007. Effect of dietary lactosucrose (4G-β-D-galactosylsucrose) on the intestinal immune functions in mice. J Appl Glycosci 54: 169–172.
    1. Fastinger ND, Karr-Lilienthal LK, Spears JK, Swanson KS, Zinn KE, Nava GM, Ohkuma K, Kanahori S, Gordon DT, Fahey GC., Jr 2008. A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27: 356–366. - PubMed
    1. Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H. 2010. Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49: 165–171. - PMC - PubMed
Show all 19 references
Related information
Full text links [x]
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig. 4.
Fig. 4.
Effect of RMD on SCFAs in the cecal contents. BALB/c mice were fed diets containing 5% or 7.5% RMD for 2 weeks. Data are presented as the mean ± SD (n=6). *Significant difference from the control group (p

References

    1. Nakamura Y, Nosaka S, Suzuki M, Nagafuchi S, Takahashi T, Yajima T, Takenouchi-Ohkubo N, Iwase T, Moro I. 2004. Dietary fructooligosaccharides up-regulate immunoglobulin A response and polymeric immunoglobulin receptor expression in intestines of infant mice. Clin Exp Immunol 137: 52–58.
    1. Sato T, Nakamura Y, Ozawa O. 2008. Effect of galactooligosaccharides on immune system in mice. J Jpn Soc Nutr Food Sci 61: 79–88.
    1. Hino K, Kurose M, Sakurai T, Inoue S, Oku K, Chaen H, Fukuda S. 2007. Effect of dietary lactosucrose (4G-β-D-galactosylsucrose) on the intestinal immune functions in mice. J Appl Glycosci 54: 169–172.
    1. Fastinger ND, Karr-Lilienthal LK, Spears JK, Swanson KS, Zinn KE, Nava GM, Ohkuma K, Kanahori S, Gordon DT, Fahey GC., Jr 2008. A novel resistant maltodextrin alters gastrointestinal tolerance factors, fecal characteristics, and fecal microbiota in healthy adult humans. J Am Coll Nutr 27: 356–366.
    1. Miyazato S, Nakagawa C, Kishimoto Y, Tagami H, Hara H. 2010. Promotive effects of resistant maltodextrin on apparent absorption of calcium, magnesium, iron and zinc in rats. Eur J Nutr 49: 165–171.
    1. Ohta A, Ohtsuki M, Baba S, Adachi T, Sakata T, Sakaguchi E. 1995. Calcium and magnesium absorption from the colon and rectum are increased in rats fed fructooligosaccharides. J Nutr 125: 2417–2424.
    1. Nakamura T, Nagura T, Sato K, Ohnishi M. 2012. Evaluation of the effects of dietary organic germanium, ge-132, and raffinose supplementation on caecal flora in rats. Biosci Microbiota Food Health 31: 37–45.
    1. Tanioka A, Tanabe K, Hosono A, Kawakami H, Kaminogawa S, Tsubaki K, Hachimura S. 2013. Enhancement of intestinal immune function in mice by β-D-glucan from aureobasidium pullulans ADK-34. Scand J Immunol 78: 61–68.
    1. Kimura Y, Sumiyoshi M, Suzuki T, Sakanaka M. 2006. Antitumor and antimetastatic activity of a novel water-soluble low molecular weight beta-1, 3-D-glucan (branch beta-1,6) isolated from Aureobasidium pullulans 1A1 strain black yeast. Anticancer Res 266B: 4131–4141.
    1. Nakanishi Y, Murashima K, Ohara H, Suzuki T, Hayashi H, Sakamoto M, Fukasawa T, Kubota H, Hosono A, Kono T, Kaminogawa S, Benno Y. 2006. Increase in terminal restriction fragments of Bacteroidetes-derived 16S rRNA genes after administration of short-chain fructooligosaccharides. Appl Environ Microbiol 72: 6271–6276.
    1. Hosono A, Ozawa A, Kato R, Ohnishi Y, Nakanishi Y, Kimura T, Nakamura R. 2003. Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer’s patch cells. Biosci Biotechnol Biochem 67: 758–764.
    1. Yanagibashi T, Hosono A, Oyama A, Tsuda M, Hachimura S, Takahashi Y, Itoh K, Hirayama K, Takahashi K, Kaminogawa S. 2009. Bacteroides induce higher IgA production than Lactobacillus by increasing activation-induced cytidine deaminase expression in B cells in murine Peyer’s patches. Biosci Biotechnol Biochem 73: 372–377.
    1. Yanagibashi T, Hosono A, Oyama A, Tsuda M, Suzuki A, Hachimura S, Takahashi Y, Momose Y, Itoh K, Hirayama K, Takahashi K, Kaminogawa S. 2013. IgA production in the large intestine is modulated by a different mechanism than in the small intestine: Bacteroides acidifaciens promotes IgA production in the large intestine by inducing germinal center formation and increasing the number of IgA+ B cells. Immunobiology 218: 645–651.
    1. Baer DJ, Stote KS, Henderson T, Paul DR, Okuma K, Tagami H, Kanahori S, Gordon DT, Rumpler WV, Ukhanova M, Culpepper T, Wang X, Mai V. 2014. The metabolizable energy of dietary resistant maltodextrin is variable and alters fecal microbiota composition in adult men. J Nutr 144: 1023–1029.
    1. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, Rinttilä T, Paulin L, Corander J, Malinen E, Apajalahti J, Palva A. 2007. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology 133: 24–33.
    1. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, Tsutsui Y, Qin H, Honda K, Okada T, Hattori M, Fagarasan S. 2014. Foxp3+ T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity 41: 152–165.
    1. Sakata T, von Engelhardt W. 1983. Stimulatory effect of short chain fatty acids on the epithelial cell proliferation in rat large intestine. Comp Biochem Physiol A 74: 459–462.
    1. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, Nakanishi Y, Uetake C, Kato K, Kato T, Takahashi M, Fukuda NN, Murakami S, Miyauchi E, Hino S, Atarashi K, Onawa S, Fujimura Y, Lockett T, Clarke JM, Topping DL, Tomita M, Hori S, Ohara O, Morita T, Koseki H, Kikuchi J, Honda K, Hase K, Ohno H. 2013. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504: 446–450.
    1. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T, Taylor TD, Itoh K, Kikuchi J, Morita H, Hattori M, Ohno H. 2011. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469: 543–547.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다