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Effect of dietary inclusion of 1% or 3% of native chicory inulin on the large intestinal mucosa proteome of growing pigs

Published online by Cambridge University Press:  13 March 2020

A. Herosimczyk*
Affiliation:
Department of Physiology, Cytobiology and Proteomics, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Janickiego 29 Str., 71-270Szczecin, Poland
A. Lepczyński
Affiliation:
Department of Physiology, Cytobiology and Proteomics, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Janickiego 29 Str., 71-270Szczecin, Poland
M. Ożgo
Affiliation:
Department of Physiology, Cytobiology and Proteomics, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Janickiego 29 Str., 71-270Szczecin, Poland
A. Tuśnio
Affiliation:
Department of Physiology, Cytobiology and Proteomics, Faculty of Biotechnology and Animal Husbandry, West Pomeranian University of Technology, Janickiego 29 Str., 71-270Szczecin, Poland Department of Animal Nutrition, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3 Str., 05-110Jabłonna, Poland
M. Taciak
Affiliation:
Department of Animal Nutrition, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3 Str., 05-110Jabłonna, Poland
M. Barszcz
Affiliation:
Department of Animal Nutrition, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Instytucka 3 Str., 05-110Jabłonna, Poland
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Abstract

Native chicory inulin is one of the promising alternatives to replace antibiotic growth promoters in young animals. Several potential mechanisms of prebiotic action have been proposed, such as modification of the intestinal microbiota composition leading to improved epithelial integrity and gut mucosal immunity of the host. The current study was focused on inulin effect on the large intestinal proteome and its implications for gut barrier functions. Therefore, we used proteomic techniques to determine changes in the large intestinal mucosa proteome of growing pigs after 40-day supplementation with native chicory inulin. The experiment was performed on 24 piglets fed from the 10th day of life an unsupplemented cereal-based diet or inulin-enriched diets (1% or 3%) with an average degree of polymerisation ≥ 10. At the age of 50 days, animals were sacrificed and tissue samples were collected from the cecum, and proximal and distal colon. Feeding diets supplemented with both levels of native inulin increased cecal and colonic expression of molecular chaperones, protein foldases and antioxidant proteins, which are collectively responsible for maintaining mucosal cell integrity as well as protecting against endotoxins and reactive oxygen species. This may confirm the beneficial effect of inulin on the gut health in growing pigs.

Type
Research Article
Copyright
© The Animal Consortium 2020

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References

Association of Official Analytical Chemists 2000. Methods of analysis of AOAC International, volume 2, 17th edition. AOAC, Arlington, VA, USA.Google Scholar
Barszcz, M, Taciak, M and Skomiał, J 2018a. Influence of different inclusion levels and chain length of inulin on microbial ecology and the state of mucosal protective barrier in the large intestine of young pigs. Animal Production Science 58, 11091118.Google Scholar
Barszcz, M, Taciak, M, Tuśnio, A, Święch, E, Bachanek, I, Kowalczyk, P, Borkowski, A and Skomiał, J 2018b. The effect of dietary level of two inulin types differing in chain length on biogenic amine concentration, oxidant-antioxidant balance and DNA repair in the colon of piglets. PLoS ONE 13, e0202799.CrossRefGoogle ScholarPubMed
Böhmer, BM, Branner, GR and Roth-Maier, DA 2005. Precaecal and faecal digestibility of inulin (DP 10-12) or an inulin/Enterococcus faecium mix and effects on nutrient digestibility and microbial gut flora. Journal of Animal Physiology and Animal Nutrition 89, 388396.CrossRefGoogle ScholarPubMed
Burrin, DG, Stoll, B, Guan, X, Cui, L, Chang, X and Hadsell, D 2007. GLP-2 rapidly activates divergent intracellular signaling pathways involved in intestinal cell survival and proliferation in neonatal piglets. American Journal of Physiology Endocrinology and Metabolism 292, 281291.CrossRefGoogle ScholarPubMed
Cani, PD, Possemiers, S, Van de Wiele, T, Guiot, Y, Everard, A, Rottier, O, Geurts, L, Naslain, D, Neyrinck, A, Lambert, DM, Muccioli, GG and Delzenne, NM 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58, 10911103.CrossRefGoogle ScholarPubMed
Chelakkot, C, Ghim, J and Ryu, SH 2018. Mechanisms regulating intestinal barrier integrity and its pathological implications. Experimental and Molecular Medicine 50, 103. doi: 10.1038/s12276-018-0126-x.CrossRefGoogle ScholarPubMed
Danielsen, M, Hornshøj, H, Siggers, RH, Jensen, BB, van Kessel, AG and Bendixen, E 2007. Effects of bacterial colonization on the porcine intestinal proteome. Journal of Proteome Research 6, 25962604.CrossRefGoogle ScholarPubMed
Darcy-Vrillon, B, Cherbuy, C, Morel, MT, Durand, M and Duée, PH 1996. Short chain fatty acid and glucose metabolism in isolated pig colonocytes: modulation by NH4+. Molecular and Cellular Biochemistry 156, 145151.CrossRefGoogle ScholarPubMed
David, JC, Grongnet, JF and Lalles, JP 2002. Weaning affects the expression of heat shock proteins in different regions of the gastrointestinal tract of piglets. Journal of Nutrition 132, 25512561.CrossRefGoogle ScholarPubMed
den Besten, G, van Eunen, K, Groen, AK, Venema, K, Reijngoud, DJ and Bakker, BM 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. Journal of Lipid Research 54, 23252340.CrossRefGoogle ScholarPubMed
Ellgaard, L and Ruddock, LW 2005. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Reports 6, 2832.CrossRefGoogle ScholarPubMed
Herosimczyk, A, Lepczyński, A, Ożgo, M, Barszcz, M, Jaszczuk-Kubiak, E, Pierzchała, M, Tuśnio, A and Skomiał, J 2017. Hepatic proteome changes induced by dietary supplementation with two levels of native chicory inulin in young pigs. Livestock Science 203, 5462.CrossRefGoogle Scholar
Herosimczyk, A, Lepczyński, A, Ożgo, M, Barszcz, M, Marynowska, M, Tuśnio, A, Taciak, M, Markulen, A and Skomiał, J 2018. Proteome changes in ileal mucosa of young pigs resulting from different levels of native chicory inulin in the diet. Journal of Animal and Feed Sciences 27, 229237.CrossRefGoogle Scholar
Herosimczyk, A, Lepczyński, A, Ożgo, M, Skomiał, J, Dratwa-Chałupnik, A, Tuśnio, A, Taciak, M and Barszcz, M 2015. Differentially expressed proteins in the blood serum of piglets in response to a diet supplemented with inulin. Polish Journal of Veterinary Sciences 18, 541548.CrossRefGoogle ScholarPubMed
Hu, SE, Wang, YW, Lichtenstein, L, Tao, Y, Musch, MW, Jabri, B, Antonopoulos, D, Claud, EC and Chang, EB 2010. Regional differences in colonic mucosa-associated microbiota determine the physiological expression of host heat shock proteins. American Journal of Physiology Gastrointestinal and Liver Physiology 299, G1266G1275.CrossRefGoogle ScholarPubMed
Kolachala, VL, Sesikeran, B and Nair, KM 2007. Evidence for a sequential transfer of iron amongst ferritin, transferrin and transferrin receptor during duodenal absorption of iron in rat and human. World Journal of Gastroenterology 13, 10421052.CrossRefGoogle ScholarPubMed
Lepczyński, A, Herosimczyk, A, Ożgo, M, Barszcz, M, Taciak, M and Skomiał, J 2019. Modification of ileal proteome in growing pigs by dietary supplementation with inulin or dried chicory root. Journal of Animal and Feed Sciences 28, 177186.CrossRefGoogle Scholar
Lepczyński, A, Herosimczyk, A, Ożgo, M, Marynowska, M, Pawlikowska, M, Barszcz, M, Taciak, M and Skomiał, J 2017. Dietary chicory root and chicory inulin trigger changes in energetic metabolism, stress prevention and cytoskeletal proteins in the liver of growing pigs – a proteomic study. Journal of Animal Physiology and Animal Nutrition 101, e225e236.CrossRefGoogle ScholarPubMed
Lepczyński, A, Herosimczyk, A, Ożgo, M, Skomiał, J, Taciak, M, Barszcz, M and Bereżecka, N 2015. Dietary supplementation with dried chicory root triggers changes in the blood serum proteins engaged in the clotting process and the innate immune response in growing pigs. Journal of Physiology and Pharmacology 66, 4755.Google ScholarPubMed
Li, C, Zhang, G, Zhao, L, Ma, Z and Chen, H 2016. Metabolic reprogramming in cancer cells: glycolysis, glutaminolysis, and Bcl-2 proteins as novel therapeutic targets for cancer. World Journal of Surgical Oncology 14, 15. doi: 10.1186/s12957-016-0769-9.CrossRefGoogle ScholarPubMed
Liu, HY, Dicksved, J, Lundh, T and Lindberg, JE 2014. Expression of heat shock proteins 27 and 72 correlates with specific commensal microbes in different regions of porcine gastrointestinal tract. American Journal of Physiology Gastrointestinal and Liver Physiology 306, G1033G1041.CrossRefGoogle ScholarPubMed
Liu, Y, Espinosa, CD, Abelilla, JJ, Casas, GA, Lagos, LV, Lee, SA, Kwon, WB, Mathai, JK, Navarro, DMDL, Jaworski, NW and Stein, HH 2018. Non-antibiotic feed additives in diets for pigs: a review. Animal Nutrition 4, 113125.CrossRefGoogle ScholarPubMed
Loh, G, Eberhard, M, Brunner, RM, Hennig, U, Kuhla, S, Kleessen, B and Metges, CC 2006. Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. Journal of Nutrition 136, 11981202.CrossRefGoogle ScholarPubMed
Morgan, EH and Oates, PS 2002. Mechanisms and regulation of intestinal iron absorption. Blood Cells, Molecules and Diseases 29, 384399.CrossRefGoogle ScholarPubMed
Paßlack, N, Al-Samman, M, Vahjen, W, Männer, K and Zentek, J 2012. Chain length of inulin affects its degradation and the microbiota in the gastrointestinal tract of weaned piglets after a short-term dietary application. Livestock Science 149, 128136.CrossRefGoogle Scholar
Sanders, LM, Henderson, CE, Hong, MY, Barhoumi, R, Burghardt, RC, Carroll, RJ, Turner, ND, Chapkin, RS and Lupton, JR 2004. Pro-oxidant environment of the colon compared to the small intestine may contribute to greater cancer susceptibility. Cancer Letters 208, 155161.CrossRefGoogle ScholarPubMed
Tako, E, Glahn, RP, Welch, RM, Lei, X, Yasuda, K and Miller, DD 2008. Dietary inulin affects the expression of intestinal enterocyte iron transporters, receptors and storage protein and alters the microbiota in the pig intestine. British Journal of Nutrition 99, 472480.CrossRefGoogle ScholarPubMed
Teng, PY and Kim, WK 2018. Review: roles of prebiotics in intestinal ecosystem of broilers. Frontiers in Veterinary Science 5, 245. doi: 10.3389/fvets.2018.00245.CrossRefGoogle ScholarPubMed
Theiss, AL, Vijay-Kumar, M, Obertone, TS, Jones, DP, Hansen, JM, Gewirtz, AT, Merlin, D and Sitaraman, SV 2009. Prohibitin is a novel regulator of antioxidant response that attenuates colonic inflammation in mice. Gastroenterology 137, 199208.CrossRefGoogle ScholarPubMed
Volf, J, Polansky, O, Varmuzova, K, Gerzova, L, Sekelova, Z, Faldynova, M, Babak, V, Medvecky, M, Smith, AL, Kaspers, B, Velge, P and Rychlik, I 2016. Transient and prolonged response of chicken cecum mucosa to colonization with different gut microbiota. PLoS ONE 11, e0163932.Google ScholarPubMed
Yasuda, K, Dawson, HD, Wasmuth, EV, Roneker, CA, Chen, C, Urban, JF, Welch, RM, Miller, DD and Lei, XG 2009. Supplemental dietary inulin influences expression of iron and inflammation related genes in young pigs. Journal of Nutrition 139, 20182023.CrossRefGoogle ScholarPubMed
Yu, C, Jia, G, Jiang, Y, Deng, Q, Chen, Z, Xu, Z, Chen, X and Wang, K 2014. Effect of glucagon-like peptide 2 on tight junction in jejunal epithelium of weaned pigs though MAPK signaling pathway. Asian-Australasian Journal of Animal Sciences 27, 733742.CrossRefGoogle ScholarPubMed
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