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Diet-Derived Short Chain Fatty Acids Stimulate Intestinal Epithelial Cells to Induce Mucosal Tolerogenic Dendritic Cells

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Diet-Derived Short Chain Fatty Acids Stimulate Intestinal Epithelial Cells to Induce Mucosal Tolerogenic Dendritic Cells Diet-Derived Short Chain Fatty Acids Stimulate Intestinal Epithelial Cells To Induce Mucosal Tolerogenic Dendritic Cells This information is current as Gera Goverse, Rosalie Molenaar, Laurence Macia, Jian Tan, of September 27, 2021. Martje N. Erkelens, Tanja Konijn, Marlene Knippenberg, Emma C. L. Cook, Diana Hanekamp, Marc Veldhoen, Anita Hartog, Guus Roeselers, Charles R. Mackay and Reina E. Mebius J Immunol 2017; 198:2172-2181; Prepublished online 18 Downloaded from January 2017; doi: 10.4049/jimmunol.1600165 http://www.jimmunol.org/content/198/5/2172 http://www.jimmunol.org/ References This article cites 53 articles, 15 of which you can access for free at: http://www.jimmunol.org/content/198/5/2172.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 27, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2017 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Diet-Derived Short Chain Fatty Acids Stimulate Intestinal Epithelial Cells To Induce Mucosal Tolerogenic Dendritic Cells Gera Goverse,* Rosalie Molenaar,* Laurence Macia,† Jian Tan,† Martje N. Erkelens,* Tanja Konijn,* Marlene Knippenberg,* Emma C. L. Cook,* Diana Hanekamp,* Marc Veldhoen,‡ Anita Hartog,x,{ Guus Roeselers,‖ Charles R. Mackay,† and Reina E. Mebius* The gastrointestinal tract is continuously exposed to many environmental factors that influence intestinal epithelial cells and the underlying mucosal immune system. In this article, we demonstrate that dietary fiber and short chain fatty acids (SCFAs) induced Downloaded from the expression of the vitamin A–converting enzyme RALDH1 in intestinal epithelial cells in vivo and in vitro, respectively. Furthermore, our data showed that the expression levels of RALDH1 in small intestinal epithelial cells correlated with the activity of vitamin A–converting enzymes in mesenteric lymph node dendritic cells, along with increased numbers of intestinal regulatory T cells and a higher production of luminal IgA. Moreover, we show that the consumption of dietary fiber can alter the composition of SCFA-producing microbiota and SCFA production in the small intestines. In conclusion, our data illustrate that dietary adjustments affect small intestinal epithelial cells and can be used to modulate the mucosal immune system. The Journal of http://www.jimmunol.org/ Immunology, 2017, 198: 2172–2181. he immune system is influenced by its immediate sur- within the lumen are fundamental to facilitate this process and to roundings, because nutritional intake and dietary changes allow the uptake of all of the necessary nutrients from the diet. They T have large effects on the intestinal and systemic immune are able to process diet-derived products in metabolites that may system. Studies showed that diet-derived products can influence the otherwise not be digestible by the host (10, 11). The highest immune system within the lamina propria of the intestine in a bacterial load in the gastrointestinal tract is found within the co- beneficial manner (1–4). However, dietary intake can also lead to lon. Although the number of bacteria is much lower in the small immune-mediated disorders, such as type 2 diabetes and inflam- intestines (SIs), it was shown that many species of bacteria are by guest on September 27, 2021 matory bowel disease (1, 4–7). Therefore, the diet in Western present in the SIs (12–14). In addition, the distribution of microbiota countries may underlie immunological disorders, such as food within the intestines can be influenced by the available nutrients in allergies, asthma, and certain autoimmune diseases (8, 9). the diet. Many studies, using high-throughput sequencing of gut The intestines provide the body with essential nutrients by di- microbiota, identified specific bacterial taxa that are beneficial for the gestion and absorption of dietary products. Microbiota located host or might be associated with immune disorders (7, 13, 15, 16). Various anaerobic bacteria produce short chain fatty acids *Department of Molecular Cell Biology and Immunology, VU University Medical (SCFAs), predominantly acetate, butyrate, and propionate, upon Center, 1081 HZ Amsterdam, the Netherlands; †Department of Immunology, Monash metabolism of dietary fiber. The production of these SCFAs is University, Clayton, Victoria 3800, Australia; ‡Babraham Institute, Cambridge CB22 x { considered a benefit to the host. Although SCFAs are found at 3AT, United Kingdom; Nutricia Research, 3584 CT Utrecht, the Netherlands; Utrecht Institute for Pharmaceutical Sciences, Utrecht University, 3584 CG Utrecht, the higher concentrations in the colon, they are also present in the ‖ Netherlands; and Microbiology and Systems Biology, TNO, 3704 HE Zeist, the cecum and SI (12, 14). SCFAs, in particular butyrate, form the Netherlands major energy source for intestinal epithelial cells (IECs). In ad- ORCIDs: 0000-0002-9467-8693 (M.N.E.); 0000-0001-9834-7202 (M.K.); 0000- dition, SCFAs are described to promote the barrier function of 0002-1415-4049 (E.C.L.C.); 0000-0002-5902-1127 (D.H.); 0000-0002-1478- 9562 (M.V.); 0000-0002-4725-6105 (G.R.); 0000-0002-6338-7340 (C.R.M.). IECs (10, 17). Recently, multiple studies showed the beneficial Received for publication January 27, 2016. Accepted for publication December 16, effect of SCFAs on intestinal regulatory T cells and during in- 2016. testinal inflammation (18, 19); however, the exact mechanisms of This work was supported by the Dutch Scientific Research program (Netherlands this regulation are not completely understood. Organisation for Scientific Research Grant VICI [918.56.612] and ALW-TOP Grant It is necessary that immunological tolerance toward harmless [854.10.005] to R.E.M.) and by the National Health and Medical Research Council of Australia (Grant 1068890). food Ags and commensal flora is established in the intestines, Address correspondence and reprint requests to Prof. Reina E. Mebius, VU Univer- whereas immunity against pathogens is crucial for host protection. sity Medical Center, OI2 Building, Boelelaan 1108, 1081HZ Amsterdam, the Nether- Tolerogenic dendritic cells (DCs) are well-described immune cells lands. E-mail address: [email protected] that interact with other hematopoietic cells to maintain a balanced Abbreviations used in this article: Ahr, aryl hydrocarbon receptor; ALDH, aldehyde mucosal immune system (20, 21). These tolerogenic DCs express dehydrogenase; 4-CMTB, 4-chloro-a-(1-methylethyl)-N-2-thiazolyl-benzeneacetamide; DC, dendritic cell; DIM, 3,39-diindolymethane; HDAC, histone deacetylase; IEC, intestinal CD103 and are able to sample Ags in the intestinal lamina propria epithelial cell; MLN, mesenteric lymph node; qPCR, quantitative PCR; RA, retinoic acid; and migrate to the draining mesenteric lymph node (MLN) to RALDH, retinaldehyde dehydrogenase; SCFA, short chain fatty acid; SI, small intestine; present Ag and to activate lymphocytes. With the production of TCDD, 2,3,7,8-tetrachlorodibenzo-p-dioxin; TSA, trichostatin A; WT, wild-type. retinoic acid (RA), the active metabolite of vitamin A, these DCs Copyright Ó 2017 by The American Association of Immunologists, Inc. 0022-1767/17/$30.00 are crucial for the differentiation of regulatory T cells and promote www.jimmunol.org/cgi/doi/10.4049/jimmunol.1600165 The Journal of Immunology 2173 IgA class-switching of B cells and induce the expression of gut- 59-CTGCGGACTGTCCCATCAATG-39, reverse: 59-GCAGCTCACCAA- homing molecules on lymphocytes (20–22). We (23) and other CCACAGTTTCT-39) and primers for the housekeeping genes Ubiquitin C 9 9 9 investigators (24–26) showed that these tolerogenic DCs them- (forward: 5 -AGCCCAGTGTTACCACCAAG-3 , reverse: 5 -ACCCAA- GAACAAGCACAAGG-39) and Cyclo (forward: 59-ACCCATCAAAC- selves depend on RA, which is produced by IECs, for their CATTCCTTCTGTA-39,reverse:59-TGAGGAAAATATGGAACCCAAAGA-39) function and phenotype. The critical role of retinol metabolism by (Invitrogen) were used. Quantitative PCR (qPCR) analysis was performed small intestinal epithelium was shown by the absence of tolero- as described earlier (28). genic DCs in CRBPII-deficient mice, because CRBP is predom- Preparation of SI cell and lymph node suspensions inantly expressed in small IECs and is necessary for the uptake of retinol (26). SIs were dissected and opened longitudinally after removal of Peyer’s In this article, we report that fiber-enriched diets promote vitamin patches. SIs were treated with EDTA for the removal of epithelial cells and A metabolism in epithelial cells in the SIs, as well as enhanced digested to obtain a single-cell suspension, as previously described (21, 28). Subsequently, cell suspensions were immunomagnetically purified for tolerogenic activity in MLN DCs, increased percentages of in- CD45+ cells with PE-Cy7–labeled anti-CD45 (clone 30-F11; eBioscience/ testinal regulatory
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