Abstract
Purpose
The protective function of the intestinal mucosa largely depends on carbohydrate moieties that as a part of glycoproteins and glycolipids form the epithelial glycocalyx or are secreted as mucins. Modifications of their expression can be induced by an altered intestinal microenvironment and have been associated with inflammatory disorders and colorectal cancer. Given the influence of dietary factors on the gut ecosystem, here we have investigated whether a long term feeding on a starch-rich diet can modulate the glucidic profile in the colonic mucosa of rats.
Methods
Animals were divided into two groups and maintained for 9 months at different diets: one group was fed a standard diet, the second was fed a starch-enriched diet. Samples of colonic mucosa, divided in proximal and distal portions, were processed for microscopic analysis. Conventional stainings and lectin histochemistry were applied to identify acidic glycoconjugates and specific sugar residues in oligosaccharide chains, respectively. Some lectins were applied on adjacent sections after sialidase/fucosidase digestion, deacetylation, and oxidation to characterize either terminal dimers or sialic acid acetylation.
Results
An increase in sulfomucins was found to be associated with the starch-enriched diet that affected also the expression of several sugar residues as well as fucosylated and sialylated sequences in both proximal and distal colon.
Conclusions
Although the mechanisms leading to such a modulation are at present unknown, either an altered intestinal microbiota or a dysregulation of glycosylation patterns might be responsible for the types and distribution of changes in the glucidic profile here observed.
Similar content being viewed by others
References
Lee YK, Puong KY (2002) Competition for adhesion between probiotics and human gastrointestinal pathogens in the presence of carbohydrate. Br J Nutr 88:S101–S108
Guglielmetti S, Tamagnini I, Minuzzo M, Arioli S, Parini C, Comelli E, Mora D (2009) Study of the adhesion of Bifidobacterium bifidum MIMBb75 to human intestinal cell lines. Curr Microbiol 59:167–172. doi:10.1007/s00284-009-9415
Sharma R, Schumacher U (1995) The influence of diets and gut microflora on lectin binding patterns of intestinal mucins in rats. Lab Invest 73:558–564
Koropatkin NM, Cameron EA, Martens EC (2012) How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10:323–335. doi:10.1038/nrmicro2746
Linden SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA (2008) Mucins in the mucosal barrier to infection. Mucosal Immunol 1:183–197. doi:10.1038/mi.2008.5
Yang Y, Jobin C (2014) Microbial imbalance and intestinal pathologies: connections and contributions. Dis Model Mech 7:1131–1142. doi:10.1242/dmm.016428
Campbell BJ, Hounsell E, Finnie IA, Rhodes JM (1995) Direct demonstration of increased expression of Thomsen–Friedenreich antigen (Galβ1-3GalNAc) by mucus in colon cancer and inflammatory bowel disease. J Clin Invest 95:571–576
de Albuquerque Garcia Redondo P, Nakamura CV, de Souza W, Morgado-Díaz JA (2004) Differential expression of Sialic Acid and N-acetylgalactosamine residues on the cell surface of intestinal epithelial cells according to normal or metastatic potential. J Histochem Cytochem 52:629–640
An G, Wei B, Xia B, McDaniel JM, Ju T, Cummings RD, Braun J, Xia L (2007) Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J Exp Med 204:1417–1429
Saeland E, Belo AI, Mongera S, van Die I, Meijer GA, van Kooyk Y (2012) Differential glycosylation of MUC1 and CEACAM5 between normal mucosa and tumour tissue of colon cancer patients. Int J Cancer 131:117–128. doi:10.1002/ijc.26354
Park JJ, Lee M (2013) Increasing the α2,6 sialylation of glycoproteins may contribute to metastatic spread and therapeutic resistance in colorectal cancer. Gut Liver 7:629–641. doi:10.5009/gnl.2013.7.6.629
Kudo T, Ikehara Y, Togayachi A, Morozumi K, Watanabe M, Nakamura M, Nishihara S, Narimatsu H (1998) Up-regulation of a set of glycosyltransferase genes in human colorectal cancer. Lab Invest 78:797–811
Caderni G, Dolara P, Spagnesi T, Luceri C, Bianchini F, Mastrandrea V, Morozzi G (1993) Rats fed high starch diets have lower colonic proliferation and fecal bile acids than high sucrose-fed controls. J Nutr 123:704–712
Brunsgaard G (1998) Effects of cereal type and feed particle size on morphological characteristics, epithelial cell proliferation, and lectin binding patterns in the large intestine of pigs. J Anim Sci 76:2787–2798
Hedemann MS, Theil PK, Bach Knudsen KE (2009) The thickness of the intestinal mucous layer in the colon of rats fed various sources of non-digestible carbohydrates is positively correlated with the pool of SCFA but negatively correlated with the proportion of butyric acid in digesta. Br J Nutr 102:117–125. doi:10.1017/S0007114508143549
Mao J, Hu X, Xiao Y, Yang C, Ding Y, Hou N, Wang J, Cheng H, Zhang X (2013) Overnutrition stimulates intestinal epithelium proliferation through β-catenin signaling in obese mice. Diabetes 62:3736–3746. doi:10.2337/db13-0035
Zhu QC, Gao RY, Wu W, Guo BM, Peng JY, Qin HL (2014) Effect of a high-fat diet in development of colonic adenoma in an animal model. World J Gastroenterol 20:8119–8129. doi:10.3748/wjg.v20.i25.8119
Key TJ, Spencer EA (2007) Carbohydrates and cancer: an overview of the epidemiological evidence. Eur J Clin Nutr 61/1:S112–S121
Le Leu RK, Hu Y, Brown IL, Young GP (2009) Effect of high amylose maize starches on colonic fermentation and apoptotic response to DNA-damage in the colon of rats. Nutr Metab 6:11. doi:10.1186/1743-7075-6-11
Wang Z, Uchida K, Ohnaka K, Morita M, Toyomura K, Kono S, Ueki T, Tanaka M, Kakeji Y, Maehara Y, Okamura T, Ikejiri K, Futami K, Maekawa T, Yasunami Y, Takenaka K, Ichimiya H, Terasaka R (2014) Sugars, sucrose and colorectal cancer risk: the Fukuoka colorectal cancer study. Scand J Gastroenterol 49:581–588. doi:10.3109/00365521.2013.822091
Roncal-Jimeneza CA, Lanaspaa MA, Rivarda CJ, Nakagawa T, Sanchez-Lozada LG, Jalala D, Andres-Hernando A, Tanabe K, Maderoc M, Lia N, Cicerchia C, Mc Fanna K, Sautin YY, Richard J (2011) Sucrose induces fatty liver and pancreatic inflammation in male breeder rats independent of excess energy intake. Metabolism 60:1259–1270. doi:10.1016/j.metabol.2011.01.008
Hobden MR, Guérin-Deremaux L, Rowland I, Gibson GR, Kennedy OB (2015) Potential anti-obesogenic properties of non-digestible carbohydrates: specific focus on resistant dextrin. Proc Nutr Soc 74:258–267. doi:10.1017/S0029665115000087
Cresci A, Orpianesi C, Silvi S, Mastrandea V, Dolara P (1999) The effect of sucrose or starch-based diet on short-chain fatty acids and faecal microflora in rats. J Appl Microbiol 86:245–250
Schauer R, Srinivasan GV, Wipfler D, Kniep B, Schwartz-Albiez R (2011) O-Acetylated sialic acids and their role in immune defense. Adv Exp Med Biol 705:525–548. doi:10.1007/978-1-4419-7877-6_28
Spicer SS (1965) Diamine methods for differentiating mucosubstances histochemically. J Histochem Cytochem 13:211–234
Accili D, Menghi G, Gabrielli MG (2008) Lectin histochemistry for in situ profiling of rat colon sialoglycoconjugates. Histol Histopathol 23:863–875
Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12:319–330. doi:10.1007/s11894-010-0131-2
Öhman L, Törnblom H, Simrén M (2015) Crosstalk at the mucosal border: importance of the gut microenvironment in IBS. Nat Rev Gastroenterol Hepatol 12:36–49. doi:10.1038/nrgastro.2014.200
Hill RRH, Cowley HM, Andremont A (1990) Influence of colonizing micro-flora on the mucin histochemistry of the neonatal mouse colon. Histochem J 22:102–105
Enss ML, Grosse-Siestrup H, Schmidt-Wittig U, Gärtner K (1992) Changes in colonic mucins of germfree rats in response to the introduction of a”normal” rat microbial flora. Rat colonic mucin. J Exp Anim Sci 35:110–119
Freitas M, Axelsson L, Cayuela C, Midtvedt T, Trugnan G (2002) Microbial–host interactions specifically control the glycosylation pattern in intestinal mouse mucosa. Histochem Cell Biol 118:149–161. doi:10.1007/s00418-002-0432-0
Raouf AH, Tsai HH, Parker N, Hoffman J, Walker RJ, Rhodes JM (1992) Sulphation of colonic and rectal mucin in inflammatory bowel disease: reduced sulphation of rectal mucus in ulcerative colitis. Clin Sci (Lond) 83:623–626
Boltin D, Perets TT, Vilkin A, Niv Y (2013) Mucin function in inflammatory bowel disease: an update. J Clin Gastroenterol 47:106–111. doi:10.1097/MCG.0b013e3182688e73
Tobisawa Y, Imai Y, Fukuda M, Kawashima H (2010) Sulfation of colonic mucins by N-Acetylglucosamine 6-O-sulfotransferase-2 and its protective function in experimental colitis in mice. J Biol Chem 285:6750–6760. doi:10.1074/jbc.M109.067082
Derrien M, Collado MC, Ben-Amor K, Salminen S, de Vos WM (2008) The mucin degrader Akkermansia muciniphila is an abundant resident of human intestinal tract. Appl Environ Microbiol 74:1646–1648
Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, Zomer A et al (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci USA 107:19514–19519. doi:10.1073/pnas.1011100107
Turroni F, Milani C, van Sinderen D, Ventura M (2011) Genetic strategies for mucin metabolism in Bifidobacterium bifidum PRL2010: an example of possible human–microbe co-evolution. Gut Microbes 2:183–189
Xu X, Xu P, Ma C, Tang J, Zhang X (2013) Gut microbiota, host health, and polysaccharides. Biotechnol Adv 31:318–337. doi:10.1016/j.biotechadv.2012.12.009
Dharmani P, Srivastava V, Kissoon-Singh V, Chadee K (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J Innate Immun 1:123–135. doi:10.1159/000163037
Debray H, Montreuil J (1989) Aleuria aurantia agglutinin. A new isolation procedure and further study of its specificity towards various glycopeptides and oligosaccharides. Carbohydr Res 185:15–26
Martin A, Ruggiero-Lopez D, Biol MC, Louisot P (1990) Evidence for the presence of an endogenous cytosolic protein inhibitor of intestinal fucosyltransferase activities. Biochem Biophys Res Commun 166:1024–1031
Biol-N’garagba MC, Louisot P (2003) Regulation of the intestinal glycoprotein glycosylation during postnatal development: role of hormonal and nutritional factors. Biochimie 85:331–352
Pickard JM, Maurice CF, Kinnebrew MA, Abt MC, Schenten D, Golovkina TV, Bogatyrev SR, Ismagilov RF, Pamer EG, Turnbaugh PJ, Chervonsky AV (2014) Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature 514:638–641. doi:10.1038/nature13823
Acknowledgements
Funding was provided by University of Camerino (Grant no: FAR 2014-15).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Gabrielli, M.G., Tomassoni, D. Starch-enriched diet modulates the glucidic profile in the rat colonic mucosa. Eur J Nutr 57, 1109–1121 (2018). https://doi.org/10.1007/s00394-017-1393-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-017-1393-3