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http://dx.doi.org/10.5187/jast.2022.e42

Transcriptome-wide analysis reveals gluten-induced suppression of small intestine development in young chickens  

Darae, Kang (Department of Animal Biotechnology, Jeonbuk National University)
Donghyun, Shin (Department of Agricultural Convergence Technology, Jeonbuk National University)
Hosung, Choe (Department of Animal Biotechnology, Jeonbuk National University)
Doyon, Hwang (Institute for Animal Products Quality Evaluation)
Andrew Wange, Bugenyi (Department of Agricultural Convergence Technology, Jeonbuk National University)
Chong-Sam, Na (Department of Animal Biotechnology, Jeonbuk National University)
Hak-Kyo, Lee (Department of Animal Biotechnology, Jeonbuk National University)
Jaeyoung, Heo (Department of Animal Biotechnology, Jeonbuk National University)
Kwanseob, Shim (Department of Animal Biotechnology, Jeonbuk National University)
Publication Information
Journal of Animal Science and Technology / v.64, no.4, 2022 , pp. 752-769 More about this Journal
Abstract
Wheat gluten is an increasingly common ingredient in poultry diets but its impact on the small intestine in chicken is not fully understood. This study aimed to identify effects of high-gluten diets on chicken small intestines and the variation of their associated transcriptional responses by age. A total of 120 broilers (Ross Strain) were used to perform two animal experiments consisting of two gluten inclusion levels (0% or 25%) by bird's age (1 week or 4 weeks). Transcriptomics and histochemical techniques were employed to study the effect of gluten on their duodenal mucosa using randomly selected 12 broilers (3 chicks per group). A reduction in feed intake and body weight gain was found in the broilers fed a high-gluten containing diet at both ages. Histochemical photomicrographs showed a reduced villus height to crypt depth ratio in the duodenum of gluten-fed broilers at 1 week. We found mainly a significant effect on the gene expression of duodenal mucosa in gluten-fed broilers at 1 week (289 differentially expressed genes [DEGs]). Pathway analyses revealed that the significant DEGs were mainly involved in ribosome, oxidative phosphorylation, and peroxisome proliferator-activated receptor (PPAR) signaling pathways. These pathways are involved in ribosome protein biogenesis, oxidative phosphorylation and fatty acid metabolism, respectively. Our results suggest a pattern of differential gene expression in these pathways that can be linked to chronic inflammation, suppression of cell proliferation, cell cycle arrest and apoptosis. And via such a mode of action, high-gluten inclusion levels in poultry diets could lead to the observed retardation of villi development in the duodenal mucosa of young broiler chicken.
Keywords
Transcriptome; RNA sequencing; Small intestines; Gluten; Chicken;
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1 FAO [Food and Agriculture Organization of the United Nations]. FAOSTAT statistical database [Internet]. 2020 [cited 2021 November 27]. https://www.fao.org/faostat/en/#home
2 Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923-30. https://doi.org/10.1093/bioinformatics/btt656   DOI
3 Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41:e108. https://doi.org/10.1093/nar/gkt214   DOI
4 Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNAseq data with DESeq2. Genome Biol. 2014;15:550. https://doi.org/10.1186/s13059-014-0550-8   DOI
5 Pluske JR, Williams IH, Aherne FX. Maintenance of villous height and crypt depth in piglets by providing continuous nutrition after weaning. Anim Sci. 1996;62:131-44. https://doi.org/10.1017/S1357729800014417   DOI
6 Chu Y, Corey DR. RNA sequencing: platform selection, experimental design, and data interpretation. Nucleic Acid Ther. 2012;22:271-4. https://doi.org/10.1089/nat.2012.0367   DOI
7 Kang DR, Belal SA, Tian W, Park BY, Choe HS, Shim KS. Effect of dietary gluten content on small intestinal inflammatory response of broilers. Eur Poult Sci. 2019;83. https://doi.org/10.1399/eps.2019.285   DOI
8 Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015;12:357-60. https://doi.org/10.1038/nmeth.3317   DOI
9 Ducheix S, Peres C, Hardfeldt J, Frau C, Mocciaro G, Piccinin E, et al. Deletion of stearoyl-CoA desaturase-1 from the intestinal epithelium promotes inflammation and tumorigenesis, reversed by dietary oleate. Gastroenterology. 2018;155:1524-38.e9. https://doi.org/10.1053/j.gastro.2018.07.032   DOI
10 Demoulin JB, Ericsson J, Kallin A, Rorsman C, Ronnstrand L, Heldin CH. Platelet-derived growth factor stimulates membrane lipid synthesis through activation of phosphatidylinositol 3-kinase and sterol regulatory element-binding proteins. J Biol Chem. 2004;279:35392-402. https://doi.org/10.1074/jbc.M405924200   DOI
11 Alpers D. Role of lipoprotein lipase in triglyceride metabolism: potential therapeutic target. Future Lipidol. 2008;3:385-97. https://doi.org/10.2217/17460875.3.4.385   DOI
12 Braun JEA, Severson DL. Regulation of the synthesis, processing and translocation of lipoprotein lipase. Biochem J. 1992;287:337-47. https://doi.org/10.1042/bj2870337   DOI
13 Gautier L, Cope L, Bolstad BM, Irizarry RA. affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20:307-15. https://doi.org/10.1093/bioinformatics/btg405   DOI
14 R Core Team. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. 2020.
15 Rau A, Gallopin M, Celeux G, Jaffrezic F. Data-based filtering for replicated high-throughput transcriptome sequencing experiments. Bioinformatics. 2013;29:2146-52. https://doi.org/10.1093/bioinformatics/btt350   DOI
16 Wickham H. ggplot2: elegant graphics for data analysis. 2nd ed. Cham: Springer; 2016.
17 Wang J, Duncan D, Shi Z, Zhang B. WEB-based gene set analysis toolkit (WebGestalt): update 2013. Nucleic Acids Res. 2013;41:W77-83. https://doi.org/10.1093/nar/gkt439   DOI
18 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 2001;25:402-8. https://doi.org/10.1006/meth.2001.1262   DOI
19 Svihus B, Klovstad KH, Perez V, Zimonja O, Sahlstrom S, Schuller RB, et al. Physical and nutritional effects of pelleting of broiler chicken diets made from wheat ground to different coarsenesses by the use of roller mill and hammer mill. Anim Feed Sci Technol. 2004;117:281-93. https://doi.org/10.1016/j.anifeedsci.2004.08.009   DOI
20 Monaghan JM, Snape JW, Chojecki AJS, Kettlewell PS. The use of grain protein deviation for identifying wheat cultivars with high grain protein concentration and yield. Euphytica. 2001;122:309-17. https://doi.org/10.1023/A:1012961703208   DOI
21 Zickermann V, Angerer H, Ding MG, Nubel E, Brandt U. Small single transmembrane domain (STMD) proteins organize the hydrophobic subunits of large membrane protein complexes. FEBS Lett. 2010;584:2516-25. https://doi.org/10.1016/j.febslet.2010.04.021   DOI
22 Bragde H, Jansson U, Fredrikson M, Grodzinsky E, Soderman J. Celiac disease biomarkers identified by transcriptome analysis of small intestinal biopsies. Cell Mol Life Sci. 2018;75:4385-401. https://doi.org/10.1007/s00018-018-2898-5   DOI
23 Simula MP, Cannizzaro R, Canzonieri V, Pavan A, Maiero S, Toffoli G, et al. PPAR signaling pathway and cancer-related proteins are involved in celiac disease-associated tissue damage. Mol Med. 2010;16:199-209. https://doi.org/10.2119/molmed.2009.00173   DOI
24 Soares FLP, de Oliveira Matoso R, Teixeira LG, Menezes Z, Pereira SS, Alves AC, et al. Gluten-free diet reduces adiposity, inflammation and insulin resistance associated with the induction of PPAR-alpha and PPAR-gamma expression. J Nutr Biochem. 2013;24:1105-11. https://doi.org/10.1016/j.jnutbio.2012.08.009   DOI
25 Drose S, Krack S, Sokolova L, Zwicker K, Barth HD, Morgner N, et al. Functional dissection of the proton pumping modules of mitochondrial complex I. PLOS Biol. 2011;9:e1001128. https://doi.org/10.1371/journal.pbio.1001128   DOI
26 Lambert AJ, Brand MD. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J Biol Chem. 2004;279:39414-20. https://doi.org/10.1074/jbc.M406576200   DOI
27 Akashi H, Han HJ, Iizaka M, Nakajima Y, Furukawa Y, Sugano S, et al. Isolation and characterization of a human cDNA encoding a protein homologous to the 7.2-kDa protein (subunit X) of bovine ubiquinol-cytochrome C reductase. J Hum Genet. 2000;45:43-6. https://doi.org/10.1007/s100380050008   DOI
28 Dupont FM, Altenbach SB. Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J Cereal Sci. 2003;38:133-46. https://doi.org/10.1016/S0733-5210(03)00030-4   DOI
29 Kindred DR, Verhoeven TMO, Weightman RM, Swanston JS, Agu RC, Brosnan JM, et al. Effects of variety and fertiliser nitrogen on alcohol yield, grain yield, starch and protein content, and protein composition of winter wheat. J Cereal Sci. 2008;48:46-57. https://doi.org/10.1016/j.jcs.2007.07.010   DOI
30 Shewry PR, Tatham AS, Barro F, Barcelo P, Lazzeri P. Biotechnology of breadmaking: unraveling and manipulating the multi-protein gluten complex. Bio/Technology. 1995;13:1185-90. https://doi.org/10.1038/nbt1195-1185   DOI
31 Wieser H. Chemistry of gluten proteins. Food Microbiol. 2007;24:115-9. https://doi.org/10.1016/j.fm.2006.07.004   DOI
32 Biesiekierski JR. What is gluten? J Gastroenterol Hepatol. 2017;32:78-81. https://doi.org/10.1111/jgh.13703   DOI
33 Ferguson A, McClure JP, MacDonald TT, Holden RJ. Cell-mediated immunity to gliadin within the small-intestinal mucosa in coeliac disease. Lancent. 1975;305:895-7. https://doi.org/10.1016/S0140-6736(75)91689-X   DOI
34 Czaja-Bulsa G. Non coeliac gluten sensitivity: A new disease with gluten intolerance. Clin Nutr. 2015;34:189-94. https://doi.org/10.1016/j.clnu.2014.08.012   DOI
35 Giannenas I, Bonos E, Anestis V, Filioussis G, Papanastasiou DK, Bartzanas T, et al. Effects of protease addition and replacement of soybean meal by corn gluten meal on the growth of broilers and on the environmental performances of a broiler production system in Greece. PLOS ONE. 2017;12:e0169511. https://doi.org/10.1371/journal.pone.0169511   DOI
36 Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029-33. https://doi.org/10.1126/science.1160809   DOI
37 Glerum DM, Shtanko A, Tzagoloff A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem. 1996;271:14504-9. https://doi.org/10.1074/jbc.271.24.14504   DOI
38 Collinson IR, van RaaiJ MJ, Runswick MJ, Fearnley IM, Skehel JM, Orriss GL, et al. ATP synthase from bovine heart mitochondria: in vitro assembly of a stalk complex in the presence of F1-ATPase and in its absence. J Mol Biol. 1994;242:408-21. https://doi.org/10.1016/S0022-2836(84)71591-9   DOI
39 Fujikawa M, Sugawara K, Tanabe T, Yoshida M. Assembly of human mitochondrial ATP synthase through two separate intermediates, F1-c-ring and b-e-g complex. FEBS Lett. 2015;589:2707-12. https://doi.org/10.1016/j.febslet.2015.08.006   DOI
40 Drummond H, Ancona S. Observational field studies reveal wild birds responding to early-life stresses with resilience, plasticity, and intergenerational effects. Ornithology. 2015;132:563-76. https://doi.org/10.1642/AUK-14-244.1   DOI
41 Morenikeji OB, Ajayi OO, Peters SO, Mujibi FD, De Donato M, Thomas BN, Imumorin IG. RNA-seq profiling of skin in temperate and tropical cattle. J Anim Sci Technol. 2020;62:141-158. https://doi.org/10.5187/jast.2020.62.2.141   DOI
42 Zhou X, Liao WJ, Liao JM, Liao P, Lu H. Ribosomal proteins: functions beyond the ribosome. J Mol Cell Biol. 2015;7:92-104. https://doi.org/10.1093/jmcb/mjv014   DOI
43 Wu YB, Ravindran V, Thomas DG, Birtles MJ, Hendriks WH. Influence of method of whole wheat inclusion and xylanase supplementation on the performance, apparent metabolisable energy, digestive tract measurements and gut morphology of broilers. Br Poult Sci. 2004;45:385-94. https://doi.org/10.1080/00071660410001730888   DOI
44 Caspary WF. Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr. 1992;55:299S-308S. https://doi.org/10.1093/ajcn/55.1.299s   DOI
45 Markovic R, Sefer D, Krstic M, Petrujkic B. Effect of different growth promoters on broiler performance and gut morphology. Arch Med Vet. 2009;41:163-9. https://doi.org/10.4067/S0301-732X2009000200010   DOI
46 Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell. 2009;16:369-77. https://doi.org/10.1016/j.ccr.2009.09.024   DOI
47 Tellez G, Latorre JD, Kuttappan VA, Kogut MH, Wolfenden A, Hernandez-Velasco X, et al. Utilization of rye as energy source affects bacterial translocation, intestinal viscosity, microbiota composition, and bone mineralization in broiler chickens. Front Genet. 2014;5:339. https://doi.org/10.3389/fgene.2014.00339   DOI
48 Dutt S, Narla A, Lin K, Mullally A, Abayasekara N, Megerdichian C, et al. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood. 2011;117:2567-76. https://doi.org/10.1182/blood-2010-07-295238   DOI
49 Daftuar L, Zhu Y, Jacq X, Prives C. Ribosomal proteins RPL37, RPS15 and RPS20 regulate the Mdm2-p53-MdmX network. PLOS ONE. 2013;8:e68667. https://doi.org/10.1371/journal.pone.0068667   DOI
50 Hausch F, Shan L, Santiago NA, Gray GM, Khosla C. Intestinal digestive resistance of immunodominant gliadin peptides. Am J Physiol Gastrointest Liver Physiol. 2002;283:G996-1003. https://doi.org/10.1152/ajpgi.00136.2002   DOI
51 Thomas KE, Sapone A, Fasano A, Vogel SN. Gliadin stimulation of murine macrophage inflammatory gene expression and intestinal permeability are MyD88-dependent: role of the innate immune response in Celiac disease. J Immunol. 2006;176:2512-21. https://doi.org/10.4049/jimmunol.176.4.2512   DOI
52 Arentz-Hansen H, Mcadam SN, Molberg O, Fleckenstein B, Lundin KEA, Jorgensen TJD, et al. Celiac lesion T cells recognize epitopes that cluster in regions of gliadins rich in proline residues. Gastroenterology. 2002;123:803-9. https://doi.org/10.1053/gast.2002.35381   DOI
53 Quarsten H, Molberg O, Fugger L, McAdam SN, Sollid LM. HLA binding and T cell recognition of a tissue transglutaminase-modified gliadin epitope. Eur J Immunol. 1999;29:2506-14. https://doi.org/10.1002/(SICI)1521-4141(199908)29:08<2506::AIDIMMU2506>3.0.CO;2-9   DOI
54 Sollid LM. Coeliac disease: dissecting a complex inflammatory disorder. Nat Rev Immunol. 2002;2:647-55. https://doi.org/10.1038/nri885   DOI
55 Bethune MT, Borda JT, Ribka E, Liu MX, Phillippi-Falkenstein K, Jandacek RJ, et al. A non-human primate model for gluten sensitivity. PLOS ONE. 2008;3:e1614. https://doi.org/10.1371/journal.pone.0001614   DOI
56 Hall EJ, Batt RM. Dietary modulation of gluten sensitivity in a naturally occurring enteropathy of Irish setter dogs. Gut. 1992;33:198-205. https://doi.org/10.1136/gut.33.2.198   DOI
57 van der Kolk JH, van Putten LA, Mulder CJ, Grinwis GCM, Reijm M, Butler CM, et al. Gluten-dependent antibodies in horses with inflammatory small bowel disease (ISBD). Vet Q. 2012;32:3-11. https://doi.org/10.1080/01652176.2012.675636   DOI
58 Michalik L, Auwerx J, Berger JP, Chatterjee VK, Glass CK, Gonzalez FJ, et al. International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol Rev. 2006;58:726-41. https://doi.org/10.1124/pr.58.4.5   DOI
59 Galipeau HJ, Rulli NE, Jury J, Huang X, Araya R, Murray JA, et al. Sensitization to gliadin induces moderate enteropathy and insulitis in nonobese diabetic-DQ8 mice. J Immunol. 2011;187:4338-46. https://doi.org/10.4049/jimmunol.1100854   DOI
60 Chen D, Zhang Z, Li M, Wang W, Li Y, Rayburn ER, et al. Ribosomal protein S7 as a novel modulator of p53-MDM2 interaction: binding to MDM2, stabilization of p53 protein, and activation of p53 function. Oncogene. 2007;26:5029-37. https://doi.org/10.1038/sj.onc.1210327   DOI
61 Praslickova D, Torchia EC, Sugiyama MG, Magrane EJ, Zwicker BL, Kolodzieyski L, et al. The ileal lipid binding protein is required for efficient absorption and transport of bile acids in the distal portion of the murine small intestine. PLOS ONE. 2012;7:e50810. https://doi.org/10.1371/journal.pone.0050810   DOI
62 Powell AA, LaRue JM, Batta AK, Martinez JD. Bile acid hydrophobicity is correlated with induction of apoptosis and/or growth arrest in HCT116 cells. Biochem J. 2001;356:481-6. https://doi.org/10.1042/bj3560481   DOI
63 Alpers DH, Bass NM, Engle MJ, DeSchryver-Kecskemeti K. Intestinal fatty acid binding protein may favor differential apical fatty acid binding in the intestine. Biochim Biophys Acta 2000;1483:352-62. https://doi.org/10.1016/S1388-1981(99)00200-0   DOI
64 Prows DR, Murphy EJ, Moncecchi D, Schroeder F. Intestinal fatty acid-binding protein expression stimulates fibroblast fatty acid esterification. Chem Phys Lipids. 1996;84:47-56. https://doi.org/10.1016/S0009-3084(96)02619-9   DOI
65 Plavnik I, Macovsky B, Sklan D. Effect of feeding whole wheat on performance of broiler chickens. Anim Feed Sci Technol. 2002;96:229-36. https://doi.org/10.1016/S0377-8401(01)00321-2   DOI
66 Scaglia N, Igal RA. Stearoyl-CoA desaturase is involved in the control of proliferation, anchorage-independent growth, and survival in human transformed cells. J Biol Chem. 2005;280:25339-49. https://doi.org/10.1074/jbc.M501159200   DOI
67 Baker PRS, Lin Y, Schopfer FJ, Woodcock SR, Groeger AL, Batthyany C, et al. Fatty acid transduction of nitric oxide signaling: multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferator-activated receptor ligands. J Biol Chem. 2005;280:42464-75. https://doi.org/10.1074/jbc.M504212200   DOI
68 Afshar M, Moslehi H. Investigation in the effect of using wheat gluten meal on broiler performance. In: World Poultry Science Association (WPSA) XII European Poultry Conference; 2006; Verona, Italy.
69 Blasco M, Fondevila M, Guada JA. Inclusion of wheat gluten as a protein source in diets for weaned pigs. Anim Res. 2005;54:297-306. https://doi.org/10.1051/animres:2005026   DOI
70 Branton SL, Reece FN, Hagler WM Jr. Influence of a wheat diet on mortality of broiler chickens associated with necrotic enteritis. Poult Sci. 1987;66:1326-30. https://doi.org/10.3382/ps.0661326   DOI
71 Liao RB, Yan HJ, Liu GH, Zhang S, Chang WH, Liu W, et al. Effect of gut stress induced by oxidized wheat gluten on the growth performance, gut morphology and oxidative states of broilers. J Anim Physiol Anim Nutr. 2018;102:e849-55. https://doi.org/10.1111/jpn.12845   DOI
72 Gabriel I, Mallet S, Leconte M, Travel A, Lalles JP. Effects of whole wheat feeding on the development of the digestive tract of broiler chickens. Anim Feed Sci Technol. 2008;142:144-62. https://doi.org/10.1016/j.anifeedsci.2007.06.036   DOI