Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Dietary corn resistant starch regulates intestinal morphology and barrier functions by activating the Notch signaling pathway of broilers

  • Zhang, Yingying (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University) ;
  • Liu, Yingsen (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University) ;
  • Li, Jiaolong (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University) ;
  • Xing, Tong (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University) ;
  • Jiang, Yun (School of Food Science and Pharmaceutical Engineering, Nanjing Normal University) ;
  • Zhang, Lin (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University) ;
  • Gao, Feng (College of Animal Science and Technology, Key Laboratory of Animal Origin Food Production and Safety Guarantee of Jiangsu Province, Jiangsu Collaborative Innovation Center of Meat Production and Processing, Quality and Safety Control, Joint International Research Laboratory of Animal Health and Food Safety, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University)
  • Received : 2019.12.20
  • Accepted : 2020.02.21
  • Published : 2020.12.01
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Abstract

Objective: This study was conducted to investigate the effects of dietary corn resistant starch (RS) on the intestinal morphology and barrier functions of broilers. Methods: A total of 320 one-day-old broilers were randomly allocated to 5 dietary treatments: one normal corn-soybean (NC) diet, one corn-soybean-based diet supplementation with 20% corn starch (CS), and 3 corn-soybean-based diets supplementation with 4%, 8%, and 12% corn resistant starch (RS) (identified as 4% RS, 8% RS, and 12% RS, respectively). Each group had eight replicates with eight broilers per replicate. After 21 days feeding, one bird with a body weight (BW) close to the average BW of their replicate was selected and slaughtered. The samples of duodenum, jejunum, ileum, caecum digesta, and blood were collected. Results: Birds fed 4% RS, 8% RS and 12% RS diets showed lower feed intake, BW gain, jejunal villus height (VH), duodenal crypt depth (CD), jejunal VH/CD ratio, duodenal goblet cell density as well as mucin1 mRNA expressions compared to the NC group, but showed higher concentrations of cecal acetic acid and butyric acid, percentage of jejunal proliferating cell nuclear antigen-positive cells and delta like canonical Notch ligand 4 (Dll4), and hes family bHLH transcription factor 1 mRNA expressions. However, there were no differences on the plasma diamine oxidase activity and D-lactic acid concentration among all groups. Conclusion: These findings suggested that RS could suppress intestinal morphology and barrier functions by activating Notch pathway and inhibiting the development of goblet cells, resulting in decreased mucins and tight junction mRNA expression.

Keywords

References

  1. Montagne L, Pluske JR, Hampson DJ. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Anim Feed Sci Technol 2003;108:95-117. https://doi.org/10.1016/S0377-8401(03)00163-9
  2. Fre S, Huyghe M, Mourikis P, et al. Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005;435:964-8. https://doi.org/10.1038/nature03589
  3. Turner JR. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009;9:799-809. https://doi.org/10.1038/nri2653
  4. Englyst HN, Kingman SM, Cummings JH. Classification and measurement of nutritionally important starch fractions. Eur J Clin Nutr 1992;46(Suppl 2):S33-50.
  5. Nugent AP. Health properties of resistant starch. Nutr Bull 2005;30:27-54. https://doi.org/10.1111/j.1467-3010.2005. 00481.x
  6. Bird A, Conlon M, Christophersen C, et al. Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Benef Microbes 2010;1:423-31. https://doi.org/10.3920/BM2010.0041
  7. Alfa MJ, Strang D, Tappia PS, et al. A randomized trial to determine the impact of a digestion resistant starch composition on the gut microbiome in older and mid-age adults. Clin Nutr 2018;37:797-807. https://doi.org/10.1016/j.clnu.2017.03.025
  8. Hedemann MS, Knudsen KEB. Resistant starch for weaning pigs-Effect on concentration of short chain fatty acids in digesta and intestinal morphology. Livest Sci 2007;108:175-7. https://doi.org/10.1016/j.livsci.2007.01.045
  9. Ribeiro RS, Pinho M, Falcao-Cunha L, et al. The use of chestnuts (Castanea sativa Mill.) as a source of resistant starch in the diet of the weaned piglet. Anim Feed Sci Technol 2013; 182:111-20. https://doi.org/10.1016/j.anifeedsci.2013.04.009
  10. Simon TC, Gordon JI. Intestinal epithelial cell differentiation: new insights from mice, flies and nematodes. Curr Opin Genet Dev 1995;5:577-86. https://doi.org/10.1016/0959-437X(95)80026-3
  11. Stanger BZ, Datar R, Murtaugh LC, et al. Direct regulation of intestinal fate by Notch. Proc Natl Acad Sci USA 2005;102: 12443-8. https://doi.org/10.1073/pnas.0505690102
  12. Vandussen KL, Carulli AJ, Keeley TM, et al. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 2011;139:488-97. https://doi.org/10.1242/dev.070763
  13. Mumm JS, Kopan R. Notch signaling: from the outside in. Dev Biol 2000;228:151-65. https://doi.org/10.1006/dbio.2000. 9960
  14. Artavanis-Tsakonas S. Notch signaling: cell fate control and signal integration in development. Science 1999;284:770-6. https://doi.org/10.1126/science.284.5415.770
  15. Van Der Flier LG, Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009;71:241-60. https://doi.org/10.1146/annurev.physiol.010908.163145
  16. Smirnov A, Tako E, Ferket PR, et al. Mucin gene expression and mucin content in the chicken intestinal goblet cells are affected by in ovo feeding of carbohydrates. Poult Sci 2006;85:669-73. https://doi.org/10.1093/ps/85.4.669
  17. Kim YS, Ho SB. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 2010;12:319-30. https://doi.org/10.1007/s11894-010-0131-2
  18. Kurokowa M, Lynch K, Podolsky DK. Effects of growth factors on an intestinal epithelial cell line: transforming growth factor $\beta$ inhibits proliferation and stimulates differentiation. Biochem Biophys Res Commun 1987;142:775-82. https://doi.org/10.1016/0006-291X(87)91481-1
  19. Uni Z, Geyra A, Ben-Hur H, et al. Small intestinal development in the young chick: crypt formation and enterocyte proliferation and migration. Br Poult Sci 2000;41:544-51. https://doi.org/10.1080/00071660020009054
  20. Gabriel I, Lessire M, Mallet S, Guillot JF. Microflora of the digestive tract: critical factors and consequences for poultry. World Poult Sci J 2006;62:499-511. https://doi.org/10.1017/S0043933906001115
  21. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-{\Delta}{\Delta}CT}$ method. Methods 2001;25:402-8. https://doi.org/10.1006/meth.2001
  22. Cowieson AJ. Factors that affect the nutritional value of maize for broilers. Anim Feed Sci Technol 2005;119:293-305. https://doi.org/10.1016/j.anifeedsci.2004.12.017
  23. Bird A R, Vuaran M, Brown I, et al. Two high-amylose maize starches with different amounts of resistant starch vary in their effects on fermentation, tissue and digesta mass accretion, and bacterial populations in the large bowel of pigs. Br J Nutr 2007;97(01):134-144. https://doi.org/10.1017/S0007114507250433
  24. Bergh MO, Razdan A, Aman P. Nutritional influence of broiler chicken diets based on covered normal, waxy and high amylose barleys with or without enzyme supplementation. Anim Feed Sci Technol 1999;78:215-26. https://doi.org/10.1016/S0377-8401(98)00281-8
  25. Zhou J, Martin RJ, Tulley RT, et al. Dietary resistant starch upregulates total GLP-1 and PYY in a sustained day-long manner through fermentation in rodents. Am J Physiol Endocrinol Metab 2008;295:E1160-6. https://doi.org/10.1152/ajpendo.90637.2008
  26. Maki KC, Pelkman CL, Finocchiaro ET, et al. Resistant starch from high-amylose maize increases insulin sensitivity in overweight and obese men. J Nutr 2012;142:717-23. https://doi.org/10.3945/jn.111.152975
  27. De Silva A, Bloom SR. Gut hormones and appetite control: a focus on PYY and GLP-1 as therapeutic targets in obesity. Gut Liver 2012;6:10-20. https://doi.org/10.5009/gnl.2012.6.1.10
  28. Liu YS, Zhang YY, Li JL, et al. Growth performance, carcass traits and digestive function of broiler chickens fed diets with graded levels of corn resistant starch. Br Poult Sci 2020;61: 146-55. https://doi.org/10.1080/00071668.2019.1694137
  29. Wijtten PJA, Langhout DJ, Verstegen MWA. Small intestine development in chicks after hatch and in pigs around the time of weaning and its relation with nutrition: a review. Acta Agric Scand A Anim Sci 2012;62:1-12. https://doi.org/10.10 80/09064702.2012.676061
  30. Qin S, Zhang K, Applegate TJ, et al. Dietary administration of resistant starch improved caecal barrier function by enhancing intestinal morphology and modulating microbiota composition in meat duck. Br J Nutr 2020;123:172-81. https://doi.org/10.1017/S0007114519002319
  31. Jozefiak D, Rutkowski A, Martin SA. Carbohydrate fermentation in the avian ceca: a review. Anim Feed Sci Technol 2004;113:1-15. https://doi.org/10.1016/j.anifeedsci.2003.09.007
  32. Khan S, Jena GB. Protective role of sodium butyrate, a HDAC inhibitor on beta-cell proliferation, function and glucose homeostasis through modulation of p38/ERK MAPK and apoptotic pathways: study in juvenile diabetic rat. Chem Biol Interact 2014;213:1-12. https://doi.org/10.1016/j.cbi.2014.02.001
  33. Moldovan GL, Pfander B, Jentsch S. PCNA, the maestro of the replication fork. Cell 2007;129:665-79. https://doi.org/10.1016/j.cell.2007.05.003
  34. Kelman Z. PCNA: structure, functions and interactions. Oncogene 1997;14:629-40. https://doi.org/10.1038/sj.onc.1200886
  35. Mcauley JL, Linden SK, Png CW, et al. MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007;117:2313-24. https://doi.org/10.1172/JCI26705
  36. Sanchez de Medina F, Romero-Calvo I, Mascaraque C, et al. Intestinal inflammation and mucosal barrier function. Inflamm Bowel Dis 2014;20(12):2394-404. https://doi.org/10.1097/MIB.0000000000000204
  37. Peterson LW, Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014;14:141-53. https://doi.org/10.1038/nri3608
  38. Suzuki T. Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 2013;70:631-59. https://doi.org/10.1007/s00018-012-1070-x
  39. Kamei H, Hachisuka T, Nakao M, et al. Quick recovery of serum diamine oxidase activity in patients undergoing total gastrectomy by oral enteral nutrition. Am J Surg 2005;189: 38-43. https://doi.org/10.1016/j.amjsurg.2004.03.015

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