Effects of dietary supplementation with apple peel powder on the growth, blood and liver parameters, and transcriptome of genetically improved farmed tilapia (GIFT, Oreochromis niloticus)
Autoři:
Jun Qiang aff001; Omyia Ahmed Mohamed Khamis aff001; Huo Jin Jiang aff002; Zhe Ming Cao aff001; Jie He aff001; Yi Fan Tao aff001; Pao Xu aff001; Jin Wen Bao aff001
Působiště autorů:
Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, Jiangsu, China
aff001; Beijing Yujing Biotechnology Co., Ltd., Beijing, China
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224995
Souhrn
High-density aquaculture and nutritional imbalances may promote fatty liver in genetically improved farmed tilapia (GIFT, Oreochromis niloticus), thus reducing the gains achieved by breeding. In this study, apple peel powder (APP) was used as a feed additive for GIFT. A control group (fed on a diet without APP) and five groups fed on diets supplemented with APP (at 0.05%, 0.1%, 0.2%, 0.4%, or 0.8% of the diet, by weight) were established to investigate the effects of APP on GIFT growth performance and physiological parameters, and on gene expression as determined by transcriptomic analysis. Dietary supplementation with APP at 0.2% promoted GIFT growth, reduced total cholesterol and triacylglycerol levels in the serum and liver, and decreased alanine aminotransferase and aspartate aminotransferase activities in the serum. Gene expression profiles in the liver were compared among the control, 0.2% APP, and 0.8% APP groups, and differentially expressed genes among these groups were identified. Annotation analyses using tools at the Gene Ontology and Kyoto Encyclopedia of Genes and Genomes databases showed that the differentially expressed genes were mainly involved in the regulation of immunity and fat metabolism. The results showed that excessive supplementation with APP in the diet significantly inhibited the expression of insulin-like growth factor 2 and liver-type fatty acid-binding protein, and stimulated the expression of fatty acid desaturase 2, heat shock protein 90 beta family member 1, and nuclear factor kappa B. This resulted in disordered lipid metabolism and increased pro-inflammatory reactions, which in turn caused liver damage. Therefore, APP has good potential as an environmentally friendly feed additive for GIFT at levels of 0.1%–0.2% in the diet, but excessive amounts can have adverse effects.
Klíčová slova:
Diet – Fats – Fatty liver – Gene expression – Inflammation – Lipid metabolism – Transcriptome analysis – Gamete intra-fallopian transfer
Zdroje
1. Sakai M. Current research status of fish immunostimulants. Aquaculture 1999; 172: 63–92.
2. Gabriel NN, Qiang J, He J, Ma XY, Kpundeh MD, Xu P. Dietary Aloe vera supplementation on growth performance, some haemato-biochemical parameters and disease resistance against Streptococcus iniae in tilapia (GIFT). Fish Shellfish Immunol. 2015; 44: 504–514. doi: 10.1016/j.fsi.2015.03.002 25758848
3. Yin GJ, Ardo L, Thompson KD, Adams A, Jeney Z, Jeney G. Chinese herbs (Astragalus radix and Ganoderma lucidum) enhance immune response of carp, Cyprinus carpio, and protection against Aeromonas hydrophila. Fish. Shellfish Immunol. 2009; 26: 140–145. doi: 10.1016/j.fsi.2008.08.015 18817878
4. Denis MC, Furtos A, Dudonné S, Montoudis A, Garofalo C, Desjardins Y, et al. Apple peel polyphenols and their beneficial actions on oxidative stress and inflammation. PLoS ONE 2013; 8: e53725. doi: 10.1371/journal.pone.0053725 23372666
5. O'Shea N, Arendt EK, Gallagher E. Dietary fiber and phytochemical characteristics of fruit and vegetable by-products and their recent applications as novel ingredients in food products, Innov. Food Sci. Emerg. 2012; 16:1–10.
6. Galanakis C. Recovery of high added-value components from food wastes: conventional, emerging technologies and commercialized applications, Trends in Food Sci. Tech. 2012; 26: 68–87.
7. Wolfe KL, Liu RH. Apple peels as a value-added food ingredient. J. Agr. Food Chem. 2003; 51: 1676–1683.
8. Djilas S, Čanadanovič-Brunet J. Četkovič G. By-products of fruit processing as a source of phytochemicals. Chem. Ind. Chem. Eng. Q. 2009; 15:191–202.
9. Qin YX, Liu HQ. Study on the effect of apple peel extracts to type 2 diabetes. Journal of Community Medicine 2011; 9: 11–13(In Chinese).
10. Li HC, Wang JX, Meng J, Liu SW, Li J. Effect of different doses of apple dietary fiber on blood glucose in diabetic mice and blood lipid in hyperlipidic mice. Food Science 2011; 32: 281–283(In Chinese).
11. Mock TS, Francis DS, Jago MK, Glencross BD, Smullen RP, Keast RSJ, et al. The impact of dietary protein: lipid ratio on growth performance, fatty acid metabolism, product quality and waste output in Atlantic salmon (Salmo salar). Aquaculture 2019; 501: 191–201.
12. Qiang J, Wasipe A, He J, Tao YF, Xu P, Bao JW, et al. Dietary vitamin E deficiency inhibits fat metabolism, antioxidant capacity, and immune regulation of inflammatory response in genetically improved farmed tilapia (GIFT, Oreochromis niloticus) fingerlings following Streptococcus iniae infection. Fish Shellfish Immunol. 2019; 92, 395–404. doi: 10.1016/j.fsi.2019.06.026 31226419
13. Ni PJ, Jiang WD, Wu P, Liu Y, Kuang SY, Tang L, et al. Dietary low or excess levels of lipids reduced growth performance, and impaired immune function and structure of head kidney, spleen and skin in young grass carp (Ctenopharyngodon idella) under the infection of Aeromonas hydrophila. Fish Shellfish Immunol. 2016; 55: 28–47. doi: 10.1016/j.fsi.2016.03.163 27157598
14. Jia R, Gu ZY, He Q, Du JL, Cao LP, Jeney G, et al. Anti-oxidative, anti-inflammatory and hepatoprotective effects of Radix Bupleuri extract against oxidative damage in tilapia (Oreochromis niloticus) via Nrf2 and TLRs signaling pathway. Fish Shellfish Immunol. 2019; 93: 395–405. doi: 10.1016/j.fsi.2019.07.080 31374313
15. He X, Liu RH. Phytochemicals of apple peels: isolation, structure elucidation, and their antiproliferative and antioxidant activities. J. Agr. Food Chem. 2008; 56: 9905–9910.
16. Leccese A, Bartolini S, Viti R. Antioxidant properties of peel and flesh in ‘GoldRush’ and ‘Fiorina’ scab-resistant apple (Malus domestica) cultivars. New Zeal. J. Crop Hort. 2009; 37: 71–78.
17. Mueller D, Triebel S, Rudakovski O, Richling E. Influence of triterpenoids present in apple peel on inflammatory gene expression associated with inflammatory bowel disease (IBD). Food Chem. 2013; 139: 339–346. doi: 10.1016/j.foodchem.2013.01.101 23561115
18. Wang XQ, Deng XY, Yu XB, Wang H. Green tea polyphenols ameliorates Type 2 diabetes mellitus through lipid-lowering, anti-oxidation, anti-inflammation and regulating TGF-β/Smad signal pathway. Pharmacology and Clinics of Chinese Materia Medica 2018; 3: 46–50(In Chinese).
19. Qiang J, He J, Yang H, Sun YL, Tao YF, Xu P, et al. Dietary lipid requirements of larval genetically improved farmed tilapia, Oreochromis niloticus (L.), and effects on growth performance, expression of digestive enzyme genes, and immune response. Aquac Res. 2017; 48: 2827–2840.
20. Qiang J, Tao YF, Bao JW, Chen DJ, Li HX, He J, et al. High fat diet-induced miR-122 regulates lipid metabolism and fat deposition in genetically improved farmed tilapia (GIFT, Oreochromis niloticus) liver. Front Physiol; 2018. 9:1422. doi: 10.3389/fphys.2018.01422 30344495
21. Gou GW, Jiang M, Wen H, Wu F, Liu W, Juan T, et al. Effects of dietary silymarin on growth performance, enzymes of hepatic lipid metabolism and antioxidant ability in GIFT Oreochromis niloticus. Journal of Fisheries of China 2016; 40: 1309–1320(In Chinese).
22. Qiang J, Sun YL, Huang Y, Yang H, Xu P, Yuan QH, et al. Effects of chitosan supplementation on growth performance, immunomodulatory and against Streptococcus iniae infection of juvenile GIFT tilapia (Oreochromis niloticus). Chinese Journal of Animal Nutrition 2015; 27: 1769–1778(In Chinese).
23. Qiang J, Bao JW, Li HX, Chen DJ, He J, Tao YF, et al. miR-1338-5p modulates growth hormone secretion and glucose utilization by regulating ghitm in genetically improved farmed tilapia (GIFT, Oreochromis niloticus). Front. Physiol; 2017. 8: 998. doi: 10.3389/fphys.2017.00998 29270127
24. Xu QY, Xu ZC, Wang CA, Zhao ZG, Luo L. Effect of dietary lipid levels on liver free fatty acids, serum biochemical parameters and liver histological structure in mirror common carp at different temperatures. Journal of Northeast Agricultural University 2012; 43: 118–126(In Chinese).
25. Zhang GS, Yin SW, Mao JQ, Liang FF, Zhao C, Li P, et al. Integrated analysis of mRNA-seq and miRNA-seq in the liver of Pelteobagrus vachelli in response to hypoxia. Sci. Rep. 2016; 6: 22907. doi: 10.1038/srep22907 26961594
26. Huang HY, Liu RR, Zhao GP, Li QH, Zheng MQ, Zhang JJ, et al. Integrated analysis of microRNA and mRNA expression profiles in abdominal adipose tissues in chickens. Sci. Rep. 2015; 5: 16132. doi: 10.1038/srep16132 26531148
27. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14: R36. doi: 10.1186/gb-2013-14-4-r36 23618408
28. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 2010; 28: 511–515. doi: 10.1038/nbt.1621 20436464
29. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7: 562–578. doi: 10.1038/nprot.2012.016 22383036
30. Henriquez C, Speisky H, Chiffelle I, Valenzuela T, Araya M, Simpson R, et al. Development of an ingredient containing apple peel, as a source of polyphenols and dietary fiber. J. Food Sci. 2010; 75: 172–181.
31. Gorinstein S, Zachwieja Z, Folta M, Barton HK, Piotrowicz J, Zemser M, et al. Comparative contents of dietary fiber, total phenolics, and minerals in persimmons and apples. J. Agric. Food Chem. 2001; 49: 952–957. doi: 10.1021/jf000947k 11262055
32. Zhao MG, Yang HM, Jiang CH, Zhang J, Yin ZQ. Intervention effects of the triterpenoids from Cyclocarya paliurus on free fatty acids-induced steatosis in Hep G2 cells. J. China Pharm. Univ. 2018; 49: 333–340(In Chinese).
33. Nouri MK, Reazpour AK. Effect of apple (Malus domestica) supplementation on serum lipids and lipoproteins level in cholesterol-fed male rat. Middle-East J Sci Res. 2011; 9: 744–748.
34. Feldstein AE, Werneburg NW, Li ZZ, Bronk SF, Gores GJ. Bax inhibition protects against free fatty acid-induced lysosomal permeabilization. Am. J. Physiol. Gastrointest Liver Physiol. 2006; 6: 1339–1346.
35. Feldstein AE. Novel insights into the pathophysiology of nonalcoholic fatty liver disease. Semin. Liver Dis. 2010; 30: 391–401. doi: 10.1055/s-0030-1267539 20960378
36. Cao LX, Zhou YX, Dun BS, Zhao X. Effect of total flavonoids of Ligustrum lucidum on lipid metabolism in rats with high fat model. J. Fourth Mil. Med. Univ. 2009; 30: 2129–2132.
37. Li S, Aygul A, Entizar A, Sun P, Feng YL, Wang XY. Effect of total organic acids from Armeniaca sibirica L. on antihyperlipidemia in hyperlipidemia rats. Science and Technology of Food Industry 2018; 39: 301–305(In Chinese).
38. Petit V, Arnould L, Martin P, Monnot M, Pineau T, Besnard P, et al. Chronic high-fat diet affects intestinal fat absorption and postprandial triglyceride levels in the mouse. J. Lipid Res. 2007; 48: 278–287. doi: 10.1194/jlr.M600283-JLR200 17114807
39. Martin GG, Atshaves BP, Mcintosh AL, Payne RH, Mackie JT, Kier AB. Liver fatty acid binding protein gene ablation potentiates hepatic cholesterol accumulation in cholesterol-fed female mice. Am. J. Physiol Gastrointest Liver Physoil. 2006; 290: G36.
40. Newberry EP, Xie Y, Kennedy S, Han X, Buhman KK, Luo J, et al. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J. Biol. Chem. 2003; 278: 51664. doi: 10.1074/jbc.M309377200 14534295
41. Zhu JL, Zhang H, Zhang SH, Yao HT, Zhang JB, Zhu LL. Dynamic expression of L-FABP and PPAR-α mRNAs in nonalcoholic fatty liver disease in rats. World Chinese Journal of Digestology 2010; 18: 1525–1530(In Chinese).
42. Newberry EP, Xie Y, Kennedy S, Luo JY, Davidson NO. Protection against western diet-induced obesity and hepatic steatosis in liver fatty acid-binding protein knockout mice. Hepatology 2006; 44: 1191–1205. doi: 10.1002/hep.21369 17058218
43. Wang SQ, Monroig Ó, Tang GX, Zhang L, You CH, Douglas R, et al. Investigating long-chain polyunsaturated fatty acid biosynthesis in teleost fish: functional characterization of fatty acyl desaturase (fads2) and elovl5 elongase in the catadromous species, japanese eel Anguilla japonica. Aquaculture 2014; 434: 57–65.
44. Reardon HT, Hsieh AT, Park WJ, Kothapalli KSD, Anthony JC, Nathanielsz PW. Dietary long-chain polyunsaturated fatty acids upregulate expression of FADS3 transcripts. Prostag. Leukotr. Ess. 2013; 88: 15–19.
45. Gimeno RE, Klaman LD. Adipose tissue as an active endocrine organ: recent advances. Curr. Opin. Pharmacol. 2005; 5: 122–128. doi: 10.1016/j.coph.2005.01.006 15780819
46. Hill DJ, Strutt B, Arany E, Zaina S, Coukell S, Graham CF, et al. Increased and persistent circulating insulin-like growth factor-II in neonatal transgenic mice suppresses developmental apoptosis in the pancreatic islets. Endocrinology 2000; 141: 1151–1157. doi: 10.1210/endo.141.3.7354 10698192
47. Lamberson WR, Sterle JA, Matteri RL. Relationship of serum insulin like growth factor II concentrations to growth, compositional and reproductive traits of swine. J. Amin. Sci. 1996; 74: 1753–1756.
48. Spencer GSG, Decuypere E, Buyse J, Zeman M. Effect of recombinant human insulin-like growth factor II on weight gain and body composition of broiler chickens. Poult. Sci. 1996; 75: 388–392. doi: 10.3382/ps.0750388 8778734
49. Han ZK. Studies of isoflavonic phytoestrogen-daidzein affecting growth and related endocrine secretion in male animals. Animal Husbandry and Veterinary Medicine 1999; 31: 1–2(In Chinese).
50. Lin M, Li L, Li LP, Gaurab P, Qi GS, Rong RM, et al. The protective effect of baicalin against renal ischemia-reperfusion injury through inhibition of inflammation and apoptosis. BMC Complem. Altern. M. 2014; 14: 19.
51. Li X, Liu HC, Yao QY, Xu BL, Zhang SC, Tu CT. Quercetin protects mice from ConA-induced hepatitis by inhibiting HMGB1-TLR expression and down-regulating the nuclear factor kappa B pathway. Inflammation 2016; 39: 96–106. doi: 10.1007/s10753-015-0227-9 26267064
52. Zhang HQ, Wang R, Zhang L, Song B. TLR2 knockout downregulates inflammatory factors expression and apoptosis in adipose tissue of high-fat-diet obesity mice. Immunological Journal 2017; 2: 164–168(In Chinese).
53. Li QT, Verma IM. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2002; 2: 725–734. doi: 10.1038/nri910 12360211
54. Xie XW. Liquiritigenin attenuates cardiac injury induced by high fructose-feeding through fibrosis and inflammation suppression. Biomed. Pharmacother. 2017; 86: 694–704. doi: 10.1016/j.biopha.2016.12.066 28039849
55. Ferguson LR, Denny WA. Genotoxicity of non-covalent interaction: DNA intercalators. Mutat. Res. 2007; 623: 14–23. doi: 10.1016/j.mrfmmm.2007.03.014 17498749
56. Noritaka S, Hideki W, Kelichiron M, Wei M, Nishikawa T, Hirata K, et al. Enhancement of flung carcinogenesis by nonylpheol and genistein in a F344 rat multiorgan carcinogenesis mode. Cancer Lett. 2003; 192: 25–36. doi: 10.1016/s0304-3835(02)00684-5 12637150
57. Qin S, Ni M, Wang X, Maurier-Mahé F, Shurland DL, Rodrigues GA. Inhibition of RPE cell sterile inflammatory responses and endotoxin -induced uveitis by a cell-impermeable HSP90 inhibitor. Exp. Eye Res. 2011; 93: 889–897. doi: 10.1016/j.exer.2011.10.002 22019372
58. Rose N, Lambert M, Christian D, Ron K, Tony M. Basal and infection -induced levels of heat shock proteins in human aging. Biogerontology 2007; 8: 353–364. doi: 10.1007/s10522-006-9078-y 17211576
59. Bao LG, Zhou L, Hao DC, Zhu XC, Luo HL, Li PF. Effect of taurochenodeoxycholic acid on GR-mediated HSP90 gene expression in FLS cells. Animal Husbandry and Feed Science 2018; 39: 1–3(In Chinese).
60. Dai Z, Wang H, Jin X, Wang H, He J, Liu M, et al. Depletion of suppressor of cytokine signaling-1a causes hepatic steatosis and insulin resistance in zebrafish. Am J Physiol Endocrinol Metab. 2015; 308: 849–859.
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