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Enzymatically modified starch up-regulates expression of incretins and sodium-coupled monocarboxylate transporter in jejunum of growing pigs

Published online by Cambridge University Press:  08 December 2016

B. U. Metzler-Zebeli ,
R. Ertl ,
D. Grüll ,
T. Molnar  and
Q. Zebeli
B. U. Metzler-Zebeli*
Affiliation:
University Clinic for Swine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria Research Cluster ‘Animal Gut Health’, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
R. Ertl
Affiliation:
VetCore Facility for Research, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
D. Grüll
Affiliation:
Agrana Research & Innovation Center GmbH, 3430 Tulln, Austria
T. Molnar
Affiliation:
Agrana Research & Innovation Center GmbH, 3430 Tulln, Austria
Q. Zebeli
Affiliation:
Research Cluster ‘Animal Gut Health’, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria Institute of Animal Nutrition and Functional Plant Compounds, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, 1210 Vienna, Austria
*
†E-mail: barbara.metzler@vetmeduni.ac.at
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Abstract

Dietary effects on the host are mediated via modulation of the intestinal mucosal responses. The present study investigated the effect of an enzymatically modified starch (EMS) product on the mucosal expression of genes related to starch digestion, sugar and short-chain fatty acid (SCFA) absorption and incretins in the jejunum and cecum in growing pigs. Moreover, the impact of the EMS on hepatic expression of genes related to glucose and lipid metabolism, and postprandial serum metabolites were assessed. Barrows (n=12/diet; initial BW 29 kg) were individually fed three times daily with free access to a diet containing either EMS or waxy corn starch as control (CON) for 10 days. The enzymatic modification led to twice as many α-1,6-glycosidic bonds (~8%) in the amylopectin fraction in the EMS in comparison with the non-modified native waxy corn starch (4% α-1,6-glycosidic bonds). Linear discriminant analysis revealed distinct clustering of mucosal gene expression for EMS and CON diets in jejunum. Compared with the CON diet, the EMS intake up-regulated jejunal expression of sodium-coupled monocarboxylate transporter (SMCT), glucagon-like peptide-1 (GLP1) and gastric inhibitory polypeptide (GIP) (P<0.05) and intestinal alkaline phosphatase (ALPI) (P=0.08), which may be related to greater luminal SCFA availability, whereas cecal gene expression was unaffected by diet. Hepatic peroxisome proliferator-activated receptor γ (PPARγ) expression tended (P=0.07) to be down-regulated in pigs fed the EMS diet compared with pigs fed the CON diet, which may explain the trend (P=0.08) of 30% decrease in serum triglycerides in pigs fed the EMS diet. Furthermore, pigs fed the EMS diet had a 50% higher (P=0.03) serum urea concentration than pigs fed the CON diet potentially indicating an increased use of glucogenic amino acids for energy acquisition in these pigs. Present findings suggested the jejunum as the target site to influence the intestinal epithelium and altered lipid and carbohydrate metabolism by EMS feeding.

Keywords

enzymatically modified starchgene expressionjejunumliverpig
Type
Research Article
Information
animal , Volume 11 , Issue 7 , July 2017 , pp. 1180 - 1188
Copyright
© The Animal Consortium 2016 

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References

Baggio, LL and Drucker, DJ 2007. Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131–2157.CrossRefGoogle ScholarPubMed
Birt, DF, Boylston, T, Hendrich, S, Jane, JL, Hollis, J, Li, L, McClelland, J, Moore, S, Phillips, GJ, Rowling, M, Schalinske, K, Scott, MP and Whitley, EM 2013. Resistant starch: promise for improving human health. Advances in Nutrition 4, 587–601.Google Scholar
Cuff, MA and Shirazi-Beechey, SP 2004. The importance of butyrate transport to the regulation of gene expression in the colonic epithelium. Biochemical Society Transactions 32, 1100–1102.CrossRefGoogle Scholar
Den Besten, G, Bleeker, A, Gerding, A, van Eunen, K, Havinga, R, van Dijk, TH, Oosterveer, MH, Jonker, JW, Groen, AK, Reijngoud, DJ and Bakker, BM 2015a. Short-chain fatty acids protect against high-fat diet-induced obesity via a PPARγ-dependent switch from lipogenesis to fat oxidation. Diabetes 64, 2398–2408.Google Scholar
Den Besten, G, Gerding, A, van Dijk, TH, Ciapaite, J, Bleeker, A, van Eunen, K, Havinga, R, Groen, AK, Reijngoud, DJ and Bakker, BM 2015b. Protection against the metabolic syndrome by guar gum-derived short-chain fatty acids depends on peroxisome proliferator-activated receptor γ and glucagon-like peptide-1. PLoS ONE 10, e0136364.Google Scholar
Haenen, D, Zhang, J, Souza da Silva, C, Bosch, G, van der Meer, IM, van Arkel, J, van den Borne, JJ, Pérez Gutiérrez, O, Smidt, H, Kemp, B, Müller, M and Hooiveld, GJ 2013. A diet high in resistant starch modulates microbiota composition, SCFA concentrations, and gene expression in pig intestine. Journal of Nutrition 143, 274–283.Google Scholar
Halestrap, AP and Meredith, D 2004. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflügers Archiv 447, 619–628.Google Scholar
Heo, JM, Agyekum, AK, Yin, YL, Rideout, TC and Nyachoti, CM 2014. Feeding a diet containing resistant potato starch influences gastrointestinal tract traits and growth performance of weaned pigs. Journal of Animal Science 92, 3906–3913.Google Scholar
Iwanaga, T, Takebe, K, Kato, I, Karaki, S and Kuwahara, A 2006. Cellular expression of monocarboxylate transporters (MCT) in the digestive tract of the mouse, rat, and humans, with special reference to slc5a8. Biomedical Research 27, 243–254.Google Scholar
Lallès, JP 2014. Luminal ATP: the missing link between intestinal alkaline phosphatase, the gut microbiota, and inflammation? American Journal of Physiology, Gastrointestinal and Liver Physiology 306, G824–G825.Google Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the ddCT method. Methods 25, 402–408.Google Scholar
Metzler-Zebeli, BU, Eberspächer, E, Grüll, D, Kowalczyk, L, Molnar, T and Zebeli, Q 2015a. Enzymatically modified starch ameliorates postprandial serum triglycerides and lipid metabolome in growing pigs. PLoS ONE 10, e0130553.CrossRefGoogle ScholarPubMed
Metzler-Zebeli, BU, Hollmann, M, Sabitzer, S, Podstatzky-Lichtenstein, L, Klein, D and Zebeli, Q 2013. Epithelial response to high-grain diets involves alteration in nutrient transporters and Na+/K+-ATPase mRNA expression in rumen and colon of goats. Journal of Animal Science 91, 4256–4266.CrossRefGoogle ScholarPubMed
Metzler-Zebeli, BU, Mann, E, Ertl, R, Schmitz-Esser, S, Wagner, M, Klein, D, Ritzmann, M and Zebeli, Q 2015b. Dietary calcium concentration and cereals differentially affect mineral balance and tight junction proteins expression in jejunum of weaned pigs. British Journal of Nutrition 113, 1019–1031.Google Scholar
Metzler-Zebeli, BU, Schmitz-Esser, S, Mann, E, Grüll, D, Molnar, T and Zebeli, Q 2015c. Adaptation of the cecal bacterial microbiome of growing pigs in response to resistant starch type 4. Applied and Environmental Microbiology 15, 8489–8499.Google Scholar
Naumann, C and Bassler, R 2012. Die chemische Untersuchung von Futtermitteln. VDLUFA Verlag, Darmstadt, Germany.Google Scholar
Nøhr, MK, Pedersen, MH, Gille, A, Egerod, KL, Engelstoft, MS, Husted, AS, Sichlau, RM, Grunddal, KV, Poulsen, SS, Han, S, Jones, RM, Offermanns, S and Schwartz, TW 2013. GPR41/FFAR3 and GPR43/FFAR2 as cosensors for short-chain fatty acids in enteroendocrine cells vs FFAR3 in enteric neurons and FFAR2 in enteric leukocytes. Endocrinology 154, 3552–3564.Google Scholar
Nutrient Research Council 2012. Nutrient requirements of swine, 10th edition. National Academic Press, Washington, DC, USA.Google Scholar
Pluske, JR 2013. Feed- and feed additives-related aspects of gut health and development in weanling pigs. Journal of Animal Science and Biotechnology 4, 1. doi:10.1186/2049-1891-4-1.Google Scholar
Sepponen, K, Ruusunen, M, Pakkanen, JA and Pösö, AR 2007. Expression of CD147 and monocarboxylate transporters MCT1, MCT2 and MCT4 in porcine small intestine and colon. Veterinary Journal 174, 122–128.Google Scholar
Shirazi-Beechey, SP, Moran, AW, Bravo, D and Al-Rammahi, M 2011. Nonruminant Nutrition Symposium: intestinal glucose sensing and regulation of glucose absorption: implications for swine nutrition. Journal of Animal Science 89, 1854–1862.CrossRefGoogle ScholarPubMed
Sim, L, Willemsma, C, Mohan, S, Naim, HY, Pinto, BM and Rose, DR 2010. Structural basis for substrate selectivity in human maltase-glucoamylase and sucrase-isomaltase N-terminal domains. Journal of Biological Chemistry 285, 17763–17770.Google Scholar
Singh, J, Dartois, A and Kaur, L 2010. Starch digestibility in food matrix: a review. Trends in Food Science and Technology 21, 168–180.Google Scholar
Soares, MJ, Murhadi, LL, Kurpad, AV, Chan She Ping-Delfos, WL and Piers, LS 2012. Mechanistic roles for calcium and vitamin D in the regulation of body weight. Obesity Reviews 13, 592–605.Google Scholar
Souza da Silva, C, Bosch, G, Bolhuis, JE, Stappers, LJ, van Hees, HM, Gerrits, WJ and Kemp, B 2014. Effects of alginate and resistant starch on feeding patterns, behaviour and performance in ad libitum-fed growing pigs. Animal 8, 1917–1927.Google Scholar
Vandesompele, J, De Preter, K, Pattyn, F, Poppe, B, Van Roy, N, De Paepe, A and Speleman, F 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, RESEARCH0034.CrossRefGoogle ScholarPubMed
Woodward, AD, Regmi, PR, Gänzle, MG, van Kempen, TA and Zijlstra, RT 2012. Slowly digestible starch influences mRNA abundance of glucose and short-chain fatty acid transporters in the porcine distal intestinal tract. Journal of Animal Science 90, 80–82.Google Scholar
Zhou, J, Hegsted, M, McCutcheon, KL, Keenan, MJ, Xi, X, Raggio, AM and Martin, RJ 2006. Peptide YY and proglucagon mRNA expression patterns and regulation in the gut. Obesity 14, 683–689.CrossRefGoogle ScholarPubMed