Abstract
The primary organ for absorbing dietary fat is the gut. High dietary lipid intake negatively affects health and absorption by causing fat deposition in the intestine. This research explores the effect of a high-fat diet (HFD) on intestinal microbiota and its connections with endoplasmic reticulum stress and inflammation. 60 fish (average weight: 45.84 ± 0.07 g) were randomly fed a control diet (6% fat) and a high-fat diet (12 % fat) in four replicates for 12 weeks. From the result, hepatosomatic index (HSI), Visceralsomatic index (VSI), abdominal fat (ADF), Intestosomatic index (ISI), mesenteric fat (MFI), Triglycerides (TG), total cholesterol (TC), non-esterified fatty acid (NEFA) content were substantially greater on HFD compared to the control diet. Moreover, fish provided the HFD significantly obtained lower superoxide dismutase (SOD) and glutathione peroxidase (GPX) activities. In contrast, an opposite result was seen in malondialdehyde (MDA) content in comparison to the control. HFD significantly altered intestinal microbiota in blunt snout bream, characterized by an increased abundance of Aeromonas, Plesiomonas proteobacteria, and firmicutes with a reduced abundance of Cetobacterium and ZOR0006. The transcriptional levels of glucose-regulated protein 78 (grp78), inositol requiring enzyme 1 (ire1), spliced X box-binding protein 1 (xbp1), DnaJ heat shock protein family (Hsp40) member B9 (dnajb9), tumor necrosis factor alpha (tnf-α), nuclear factor-kappa B (nf-κb), monocyte chemoattractant protein-1 (mcp-1), and interleukin-6 (il-6) in the intestine were markedly upregulated in fish fed HFD than the control group. Also, the outcome was similar in bax, caspases-3, and caspases-9, ZO-1, Occludin-1, and Occludin-2 expressions. In conclusion, HFD could alter microbiota and facilitate chronic inflammatory signals via activating endoplasmic reticulum stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data generated or used during the study appear in the submitted article.
References
Abasubong K, Li XF, Zhang DD, Jia ET, Xiang-Yang Y, Xu C, Liu WB (2018) Dietary supplementation of xylooligosaccharides benefits the growth performance and lipid metabolism of common carp (Cyprinus carpio) fed high-fat diets. Aquac Nutr 24:1416–1424. https://doi.org/10.1111/anu.12678
Abasubong KP, Li XF, Adjoumani JJY, Jiang GZ, Desouky HE, Liu, W.b. (2022) Effects of dietary xylooligosaccharide prebiotic supplementation on growth, antioxidant and intestinal immune-related genes expression in common carp Cyprinus carpio fed a high-fat diet. J Anim Physiol Anim Nutr 106:403–418. https://doi.org/10.1111/jpn.13669
Altieri C, Bevilacqua A, Cardillo D, Sinigaglia M (2009) Effectiveness of fatty acids and their monoglycerides against gram-negative pathogens. International. J Food Sci Technol 44:359–366. https://doi.org/10.1111/vde.12712
Arii K, Suehiro T, Yamamoto M, Ito H, Hashimoto K (1997) Suppression of plasma cholesteryl ester transfer protein activity in acute hyperinsulinemia and effect of plasma nonesterified fatty acid. Metabolism 46:1166–1170. https://doi.org/10.1016/s0026-0495(97)90211-0
Balasubramaniyan N, Ananthanarayanan M, Suchy FJ (2016) Nuclear factor-κB regulates the expression of multiple genes encoding liver transport proteins. American Journal of Physiology-Gastrointestinal and Liver. Physiology 310:G618–G628. https://doi.org/10.1152/ajpgi.00363.2015
Barnabei L, Laplantine E, Mbongo W, Rieux-Laucat F, Weil R (2021) NF-κB: at the borders of autoimmunity and inflammation. Front Immunol 12:716469. https://doi.org/10.3389/fimmu.2021.716469
Beard RS, Reynolds JJ, Bearden SE (2011) Hyperhomocysteinemia increases permeability of the blood-brain barrier by NMDA receptor-dependent regulation of adherens and tight junctions. Blood 118(7):2007–2014. https://doi.org/10.1182/blood-2011-02-338269
Bergmann KR, Liu SXL, Tian R, Kushnir A, Turner JR, Li H-L, Chou PM, Weber CR, De Plaen IG (2013) Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis. Am J Pathol 182(5):1595–1606. https://doi.org/10.1016/j.ajpath.2013.01.013
Bhatt D, Ghosh S (2014) Regulation of the NF-κB-mediated transcription of inflammatory genes. Front Immunol 5:71. https://doi.org/10.3389/fimmu.2014.00071
Brugman S, Nieuwenhuis EE (2010) Mucosal control of the intestinal microbial community. J Mol Med 88:881–888. https://doi.org/10.1007/s00109-010-0639-9
Brunvold L, Sandaa R-A, Mikkelsen H, Welde E, Bleie H, Bergh Ø (2007) Characterisation of bacterial communities associated with early stages of intensively reared cod (Gadus morhua) using Denaturing Gradient Gel Electrophoresis (DGGE). Aquaculture 272(1-4):319–327. https://doi.org/10.1016/j.aquaculture.2007.08.053
Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet–induced obesity and diabetes in mice. Diabetes 57(6):1470–1481. https://doi.org/10.2337/db07-1403
Cantas L, Sørby JRT, Aleström P, Sørum, H (2012) Culturable gut microbiota diversity in zebrafish. Zebrafish 9(1):26–37. https://doi.org/10.1089/zeb.2011.0712
Capaldo CT, Nusrat A (2009) Cytokine regulation of tight junctions. Biochimica et Biophysica Acta (BBA). Biomembranes 1788:864–871. https://doi.org/10.1016/j.bbamem.2008.08.027
Carracedo A, Lorente M, Egia A (2006) The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 9:301–312
Cerf-Bensussan N, Gaboriau-Routhiau V (2010) The immune system and the gut microbiota: friends or foes? Nat Rev Immunol 10:735–744. https://doi.org/10.1038/nri2850
Cebra JJ (1999) Influences of microbiota on intestinal immune system development. Am J Clin Nutr 69(5):1046s–1051s. https://doi.org/10.1093/ajcn/69.5.1046s
Chasiotis H, Kolosov D, Bui P, Kelly SP (2012) Tight junctions, tight junction proteins and paracellular permeability across the gill epithelium of fishes: a review. Respir Physiol Neurobiol 184:269–281. https://doi.org/10.1016/j.resp.2012.05.020
Chelakkot C, Ghim J, Ryu SH (2018) Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp Mol Med 50:1–9. https://doi.org/10.1038/s12276-018-0126-x
Chen Q-Q, Liu W-B, Zhou M, Dai Y-J, Xu C, Tian H-Y, Xu W-N (2016) Effects of berberine on the growth and immune performance in response to ammonia stress and high-fat dietary in blunt snout bream Megalobrama amblycephala. Fish Shellfish Immunol 55:165–172. https://doi.org/10.1016/j.fsi.2016.05.023
Chen X, Yang S, Pan Y, Li X, Ma S (2018) Mitochondrial pathway-mediated apoptosis is associated with erlotinib-induced cytotoxicity in hepatic cells. Oncol Lett 15:783–788. https://doi.org/10.3892/ol.2017.7359
Choi Y, Abdelmegeed MA, Akbar M, Song B-J (2016) Dietary walnut reduces hepatic triglyceride content in high-fat-fed mice via modulation of hepatic fatty acid metabolism and adipose tissue inflammation. J Nutr Biochem 30:116–125. https://doi.org/10.1016/j.jnutbio.2015.12.005
Dai Y-J, Cao X-F, Zhang D-D, Li X-F, Liu W-B, Jiang G-Z (2019) Chronic inflammation is a key to inducing liver injury in blunt snout bream (Megalobrama amblycephala) fed with high-fat diet. Dev Comp Immunol 97:28–37. https://doi.org/10.1016/j.dci.2019.03.009
Dai Y-J, Jiang G-Z, Yuan X-Y, Liu W-B (2018) High-fat-diet-induced inflammation depresses the appetite of blunt snout bream (Megalobrama amblycephala) through the transcriptional regulation of leptin/mammalian target of rapamycin. Br J Nutr 120:1422–1431. https://doi.org/10.1017/S000711451800288X
Dawood MA, Koshio S, El-Sabagh M, Billah MM, Zaineldin AI, Zayed MM, Omar AAE-D (2017) Changes in the growth, humoral and mucosal immune responses following β-glucan and vitamin C administration in red sea bream, Pagrus major. Aquaculture 470:214–222. https://doi.org/10.1016/j.aquaculture.2016.12.036
De RB, Youmans BP, Danzeisen JL, Tran H, Johnson TJ (2018) Microbiome profiling of commercial pigs from farrow to finish. J Anim Sci 96:1778–1794. https://doi.org/10.1093/jas/sky109
Deng Y-P, Jiang W-D, Liu Y, Jiang J, Kuang S-Y, Tang L, Wu P, Zhang Y-A, Feng L, Zhou X-Q (2014) Differential growth performance, intestinal antioxidant status and relative expression of Nrf2 and its target genes in young grass carp (Ctenopharyngodon idella) fed with graded levels of leucine. Aquaculture 434:66–73. https://doi.org/10.1016/j.aquaculture.2014.07.026
Desouky HE, Jiang GZ, Zhang DD, Abasubong KP, Yuan X, Li XF, Liu WB (2020) Influences of glycyrrhetinic acid (GA) dietary supplementation on growth, feed utilization, and expression of lipid metabolism genes in channel catfish (Ictalurus punctatus) fed a high-fat diet. Fish Physiol Biochem 46:653–663. https://doi.org/10.1007/s10695-019-00740-4
Du Z-Y, Clouet P, Zheng W-H, Degrace P, Tian L-X, Liu Y-J (2006) Biochemical hepatic alterations and body lipid composition in the herbivorous grass carp (Ctenopharyngodon idella) fed high-fat diets. Br J Nutr 95:905–915. https://doi.org/10.1079/bjn20061733
Du Z, Clouet P, Huang L, Degrace P, Zheng W, He J, Tian L, Liu Y (2008) Utilization of different dietary lipid sources at a high level in herbivorous grass carp (Ctenopharyngodon idella): mechanism related to hepatic fatty acid oxidation. Aquac Nutr 14:77–92. https://doi.org/10.1111/j.1365-2095.2007.00507.x
Eddy SD, Jones SH (2002) Microbiology of summer flounder Paralichthys dentatus fingerling production at a marine fish hatchery. Aquaculture 211(1-4):9–28. https://doi.org/10.1016/S0044-8486(01)00882-1
Frayn KN (1998) Non-esterified fatty acid metabolism and postprandial lipaemia. Atherosclerosis 141:S41–S46. https://doi.org/10.1016/s0021-9150(98)00216-0
Habte-Tsion H-M, Ren M, Liu B, Ge, X, Xie J, Chen R (2016) Threonine modulates immune response, antioxidant status, and gene expressions of antioxidant enzymes and antioxidantimmune-cytokine-related signaling molecules in juvenile blunt snout bream (Megalobrama amblycephala). Fish Shellfish Immuno 51:189–199. https://doi.org/10.1016/j.fsi.2015.11.033
Haywood J, Yammani RR (2016) Free fatty acid palmitate activates unfolded protein response pathway and promotes apoptosis in meniscus cells. Osteoarthr Cartil 24:942–945
Galindo-Villegas J, García-Moreno D, De Oliveira S, Meseguer J, Mulero V (2012) Regulation of immunity and disease resistance by commensal microbes and chromatin modifications during zebrafish development. Proc Natl Acad Sci 109:E2605–E2614. https://doi.org/10.1073/pnas.1209920109
Guo G, Shi F, Zhu J, Shao Y, Gong W, Zhou G, Wu H, She J, Shi W (2020) Piperine, a functional food alkaloid, exhibits inhibitory potential against TNBS-induced colitis via the inhibition of IκB-α/NF-κB and induces tight junction protein (claudin-1, occludin, and ZO-1) signaling pathway in experimental mice. Hum Exp Toxicol 39:477–491. https://doi.org/10.1177/0960327119892042
Hagi T, Tanaka D, Iwamura Y, Hoshino T (2004) Diversity and seasonal changes in lactic acid bacteria in the intestinal tract of cultured freshwater fish. Aquaculture 234:335–346. https://doi.org/10.1016/j.aquaculture.2004.01.018
Han J, Kaufman RJ (2016) The role of ER stress in lipid metabolism and lipotoxicity. J Lipid Res 57:1329–1338. https://doi.org/10.1194/jlr.R067595
Hansen JØ, Berge GM, Hillestad M, Krogdahl Å, Galloway TF, Holm H, Holm J, Ruyter B (2008) Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels. Aquaculture 284:159–166. https://doi.org/10.1016/j.aquaculture.2008.07.043
He C, Cheng D, Peng C, Li Y, Zhu Y, Lu N (2018) High-fat diet induces dysbiosis of gastric microbiota prior to gut microbiota in association with metabolic disorders in mice. Front Microbiol 9:639. https://doi.org/10.3389/fmicb.2018.00639
Hu C, Xu Y, Xia M, Xiong L, Xu Z (2007) Effects of Cu2+-exchanged montmorillonite on growth performance, microbial ecology and intestinal morphology of Nile tilapia (Oreochromis niloticus). Aquaculture 270:200–206. https://doi.org/10.1016/j.aquaculture.2007.01.027
Ismail M, Al-Naqeep G, Chan KW (2010) Nigella sativa thymoquinone-rich fraction greatly improves plasma antioxidant capacity and expression of antioxidant genes in hypercholesterolemic rats. Free Radic Biol Med 48:664–672. https://doi.org/10.1016/j.freeradbiomed.2009.12.002
Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T, Ferré P, Foufelle F (2009) GRP78 expression inhibits insulin and ER stress–induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 119:1201–1215. https://doi.org/10.1172/JCI37007
Kikuchi K, Furuta T, Iwata N, Onuki K, Noguchi T (2009) Effect of dietary lipid levels on the growth, feed utilization, body composition and blood characteristics of tiger puffer Takifugu rubripes. Aquaculture 298:111–117. https://doi.org/10.1016/j.aquaculture.2009.10.026
Kim S, Joe Y, Kim HJ, Kim Y-S, Jeong SO, Pae H-O, Ryter SW, Surh Y-J, Chung HT (2015) Endoplasmic reticulum stress–induced IRE1α activation mediates cross-talk of GSK-3β and XBP-1 To regulate inflammatory cytokine production. J Immunol 194:4498–4506. https://doi.org/10.4049/jimmunol.1401399
Kühlwein H, Emery M, Rawling M, Harper G, Merrifield D, Davies S (2013) Effects of a dietary β-(1, 3)(1, 6)-D-glucan supplementation on intestinal microbial communities and intestinal ultrastructure of mirror carp (Cyprinus carpio L.). J Appl Microbiol 115:1091–1106. https://doi.org/10.1111/jam.12313
Kuwana T, Olson NH, Kiosses WB, Peters B, Newmeyer DD (2016) Pro-apoptotic Bax molecules densely populate the edges of membrane pores. Sci Rep 6:27299. https://doi.org/10.1038/srep27299
Lagrost L, Florentin E, Guyard-Dangremont V, Athias A, Gandjini H, Lallemant C, Gambert P (1995) Evidence for nonesterified fatty acids as modulators of neutral lipid transfers in normolipidemic human plasma. Arterioscler Thromb Vasc Biol 15:1388–1396. https://doi.org/10.1161/01.atv.15.9.1388
Lam YY, Ha CW, Hoffmann JM, Oscarsson J, Dinudom A, Mather TJ, Cook DI, Hunt NH, Caterson ID, Holmes AJ (2015) Effects of dietary fat profile on gut permeability and microbiota and their relationships with metabolic changes in mice. Obesity 23:1429–1439. https://doi.org/10.1002/oby.21122
Lappi J, Salojärvi J, Kolehmainen M, Mykkänen H, Poutanen K, de Vos WM (2013) Intake of whole-grain and fiber-rich rye bread versus refined wheat bread does not differentiate intestinal microbiota composition in Finnish adults with metabolic syndrome. J Nutr 143:648–655. https://doi.org/10.3945/jn.112.172668
Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23:7448–7459
Lee J-S, Mendez R, Heng HH, Yang ZQ, Zhang K (2012) Pharmacological ER stress promotes hepatic lipogenesis and lipid droplet formation. Am J Transl Res 4:102–113
Li A, Yuan X, Liang X-F, Liu L, Li J, Li B, Fang J, Li J, He S, Xue M (2016a) Adaptations of lipid metabolism and food intake in response to low and high fat diets in juvenile grass carp (Ctenopharyngodon idellus). Aquaculture 457:43–49. https://doi.org/10.1016/j.aquaculture.2016.01.014
Li H, Jiang W, Liu Y, Jiang J, Zhang Y, Wu P, Zhao J, Duan X, Zhou X, Feng L (2016b) The metabolites of glutamine prevent hydroxyl radical-induced apoptosis through inhibiting mitochondria and calcium ion involved pathways in fish erythrocytes. Free Radic Biol Med 92:126–140. https://doi.org/10.1016/j.freeradbiomed.2016.01.007
Liang XP, Li Y, Hou YM, Qiu H, Zhou QC (2017) Effect of dietary vitamin C on the growth performance, antioxidant ability and innate immunity of juvenile yellow catfish (P elteobagrus fulvidraco Richardson). Aquac Res 48(1):149–160. https://doi.org/10.1016/j.fsi.2012.01.024
Ling S-C, Wu K, Zhang D-G, Luo Z (2019) Endoplasmic reticulum stress-mediated autophagy and apoptosis alleviate dietary fat-induced triglyceride accumulation in the intestine and in isolated intestinal epithelial cells of yellow catfish. J Nutr 149(10):1732–1741. https://doi.org/10.1093/jn/nxz135
Liu T, Zhang L, Joo D, Sun S-C (2017) NF-κB signaling in inflammation. Signal Transduct Target Ther 2:1–9. https://doi.org/10.1038/sigtrans.2017.23
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Llewellyn MS, McGinnity P, Dionne M, Letourneau J, Thonier F, Carvalho GR, Creer S, Derome N (2016) The biogeography of the Atlantic salmon (Salmo salar) gut microbiome. The ISME J 10:1280–1284. https://doi.org/10.1038/ismej.2015.189
Lu K-L, Xu W-N, Liu W-B, Wang L-N, Zhang C-N, Li X-F (2013) Association of mitochondrial dysfunction with oxidative stress and immune suppression in blunt snout bream Megalobrama amblycephala fed a high-fat diet. J Aquat Anim Health 26(2):100–112. https://doi.org/10.1080/08997659.2014.893460
Martin-Antonio B, Manchado M, Infante C, Zerolo R, Labella A, Alonso C, Borrego JJ (2007) Intestinal microbiota variation in Senegalese sole (Solea senegalensis) under different feeding regimes. Aquac Res 38:1213–1222. https://doi.org/10.1111/j.1365-2109.2007.01790.x
Martínez-Llorens S, Baeza-Ariño R, Nogales-Mérida S, Jover-Cerdá M, Tomás-Vidal A (2012) Carob seed germ meal as a partial substitute in gilthead sea bream (Sparus aurata) diets: amino acid retention, digestibility, gut and liver histology. Aquaculture 338:124–133. https://doi.org/10.1016/j.aquaculture.2012.01.029
Merrifield D, Dimitroglou A, Bradley G, Baker R, Davies S (2009) Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises the intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32(9):755–766. https://doi.org/10.1111/j.1365-2761.2009.01052.x
Morales P, Brignardello J, Gotteland M (2010) The association of intestinal microbiota with obesity. Rev Med Chil 138:1020–1027
Mu H, Shen H, Liu J, Xie F, Zhang W, Mai K (2018) High level of dietary soybean oil depresses the growth and anti-oxidative capacity and induces inflammatory response in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol 77:465–473. https://doi.org/10.1016/j.fsi.2018.04.017
Nazli SA, Loeser RF, Chubinskaya S, Willey JS, Yammani RR (2017) High fat-diet and saturated fatty acid palmitate inhibits IGF-1 function in chondrocytes. Osteoarthr Cartil 25:1516–1521
Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, Nie D, Myers MG, Ozcan U (2009) Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab 9:35–51. https://doi.org/10.1111/obr.12673
Regost C, Arzel J, Cardinal M, Robin J, Laroche M, Kaushik S (2001) Dietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 193(3-4):291–309. https://doi.org/10.1016/S0044-8486(00)00493-2
Ringø E, Zhou Z, Vecino JG, Wadsworth S, Romero J, Krogdahl Å, Olsen RE, Dimitroglou A, Foey A, Davies S (2015) Effect of dietary components on the gut microbiota ofaquatic animals. A never‐ending story? Aquac Nutr 22(2):219–282. https://doi.org/10.1111/anu.12346
Reinecker H-C, Loh EY, Ringler DJ, Mehta A, Rombeau JL, MacDermott RP (1995) Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology 108:40–50. https://doi.org/10.1002/jlb.59.6.804
Rizzatti G, Lopetuso L, Gibiino G, Binda C, Gasbarrini A (2017) Proteobacteria: a common factor in human diseases. Biomed Res Int 2017:9351507. https://doi.org/10.1155/2017/9351507
Rochfort KD, Cummins PM (2015) Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium. Microvasc Res 100:48–53. https://doi.org/10.1016/j.mvr.2015.04.010
Rohr MW, Narasimhulu CA, Rudeski-Rohr TA, Parthasarathy S (2020) Negative effects of a high-fat diet on intestinal permeability: a review. Adv Nutr 11(1):77–91. https://doi.org/10.1093/advances/nmz061
Rueda-Jasso R et al (2004) Effect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 231:417–433
Rutkowski DT, Wu J, Back S-H, Callaghan MU, Ferris SP, Iqbal J, Clark R, Miao H, Hassler JR, Fornek J (2008) UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 15:829–840. https://doi.org/10.1016/j.devcel.2008.10.015
Safari Z, Monnoye M, Abuja PM, Mariadassou M, Kashofer K, Gerard P, Zatloukal K (2019) Steatosis and gut microbiota dysbiosis induced by high-fat diet are reversed by 1-week chow diet administration. Nutr Res 71:72–88. https://doi.org/10.1016/j.nutres.2019.09.004
Simoes CD, Maukonen J, Kaprio J, Rissanen A, Pietiläinen KH, Saarela M (2013) Habitual dietary intake is associated with stool microbiota composition in monozygotic twins. J Nutr 143:417–423. https://doi.org/10.3945/jn.112.166322
Song B, Li H, Wu Y, Zhen W, Wang Z, Xia Z, Guo Y (2017) Effect of microencapsulated sodium butyrate dietary supplementation on growth performance and intestinal barrier function of broiler chickens infected with necrotic enteritis. Anim Feed Sci Technol 232:6–15. https://doi.org/10.1016/j.anifeedsci.2017.07.009
Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV (2003) Potential role of MCP-1 in endothelial cell tight junction opening': signaling via Rho and Rho kinase. J Cell Sci 116:4615–4628. https://doi.org/10.1242/jcs.00755
Tam AB, Mercado EL, Hoffmann A, Niwa M (2012) ER stress activates NF-κB by integrating functions of basal IKK activity, IRE1 and PERK. PLoS One 7(10):e45078. https://doi.org/10.1371/journal.pone.0045078
Tang W, Pan L, Cheng J, Wang X, Zheng L, Wang S, Zhou Y, Wang H (2022) High-fat-diet-induced gut microbiome changes in mice. Stress and Brain 2:17–30. https://doi.org/10.26599/SAB.2022.9060012
Tarnecki AM, Burgos FA, Ray CL, Arias CR (2017) Fish intestinal microbiome: diversity and symbiosis unraveled by metagenomics. J Appl Microbiol 123:2–17. https://doi.org/10.1111/jam.13415
Trust T, Sparrow R (1974) The bacterial flora in the alimentary tract of freshwater salmonid fishes. Can J Microbiol 20:1219–1228. https://doi.org/10.1139/m74-188
Todd DJ, Lee AH, Glimcher LH (2008) The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 8:663–674
Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science. 334:1081–1086
Wang A, Zhang Z, Ding Q, Yang Y, Bindelle J, Ran C, Zhou Z (2021) Intestinal Cetobacterium and acetate modify glucose homeostasis via parasympathetic activation in zebrafish. Gut Microbes 13:1–15. https://doi.org/10.1080/19490976.2021.1900996
Wang J-T, Liu Y-J, Tian L-X, Mai K-S, Du Z-Y, Wang Y, Yang H-J (2005) Effect of dietary lipid level on growth performance, lipid deposition, hepatic lipogenesis in juvenile cobia (Rachycentron canadum). Aquaculture 249:439–447. https://doi.org/10.1016/j.aquaculture.2005.04.038
Xie M, Zhou W, Xie Y, Li Y, Zhang Z, Yang Y, Olsen RE, Ran C, Zhou Z (2021) Effects of Cetobacterium somerae fermentation product on gut and liver health of common carp (Cyprinus carpio) fed diet supplemented with ultra-micro ground mixed plant proteins. Aquaculture 543:736943. https://doi.org/10.1016/j.aquaculture.2021.736943
Xu X, Huang E, Tai Y (2017) Nupr1 modulates methamphetamine-induced dopaminergic neuronal apoptosis and autophagy through CHOP-Trib3-mediated endoplasmic reticulum stress signaling pathway. Front Mol Neurosci 10:203
Yan J, Liao K, Wang T, Mai K, Xu W, Ai Q (2015) Dietary lipid levels influence lipid deposition in the liver of large yellow croaker (Larimichthys crocea) by regulating lipoprotein receptors, fatty acid uptake and triacylglycerol synthesis and catabolism at the transcriptional level. PLoS One 10:e0129937. https://doi.org/10.1371/journal.pone.0129937
Yu H, Huang X, Ma Y, Gao M, Wang O, Gao T, Shen Y, Liu X (2013) Interleukin-8 regulates endothelial permeability by down-regulation of tight junctions but not dependent on integrins induced focal adhesions. Int J Biol Sci 9:966–979. https://doi.org/10.7150/ijbs.6996
Zhang K, Shen X, Wu J, Sakaki K, Saunders T, Rutkowski DT, Back SH, Kaufman RJ (2006) Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell 124:587–599. https://doi.org/10.1016/j.cell.2005.11.040
Zhu S, Stavrovskaya IG, Drozda M, Kim BYS, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu DC, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74–78. https://doi.org/10.1038/417074a
Funding
This research was funded by the Jiangsu Natural Science Foundation for Basic Research (BK 20201325), National Technology System, and Conventional Freshwater Fish Industries of China (grant number CARS-45-14)
Author information
Authors and Affiliations
Contributions
All authors participated in the study’s design, interpretation of the findings and analysis of the data, and review of the manuscript. Kenneth Prudence Abasubong, Guang-zhen Jiang, and Wen-bin Liu provided ideas and schemes for this experiment; Kenneth Prudence Abasubong Hui-Xing Guo and Xi Wang completed the feeding trial; Hui-Xing Guo, and Xi Wang assisted sampling. Kenneth Prudence Abasubong finished data analysis and manuscript writing; Xiang-Fei Li, Dong Yan-zou, Wen-bin Liu, and Hesham Eed. Desouky polished the manuscript
Corresponding author
Ethics declarations
Ethical approval
Animals were managed, and the experimental manipulations were performed following the guidelines of the Animal Care and Use Committee in China. The Animal Research Ethics Committee has approved the current study at Nanjing Agricultural University, China (permit number: SYXK (Su) 2011-0036). Furthermore, the animals were handled and used based on the international laboratory animal care and use guidelines.
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Abasubong, K.P., Jiang, GZ., Guo, Hx. et al. High-fat diet alters intestinal microbiota and induces endoplasmic reticulum stress via the activation of apoptosis and inflammation in blunt snout bream. Fish Physiol Biochem 49, 1079–1095 (2023). https://doi.org/10.1007/s10695-023-01240-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01240-2