Resveratrol inclusion alleviated high-dietary-carbohydrate-induced glycogen deposition and immune response of largemouth bass, Micropterus salmoides

Abstract Excessive hepatic glycogen accumulation commonly impairs hepatocytes function and further produces negative effects on growth and health status of carnivorous fish. A 9-week feeding trial was conducted to explore the potential regulation of resveratrol (RSV) on high-carbohydrate-induced glycogen deposition and immune response of largemouth bass. Results showed that high dietary carbohydrate (10 % inclusion of starch) led to hepatic glycogen accumulation and post-prandial hyperglycemia compared with the diet with 5 % starch, which was both alleviated with the inclusion of RSV. The use of RSV promoted the expression of sirtuin 1, which was down-regulated by high dietary carbohydrate. Meanwhile, RSV inclusion promoted the expression of genes involved in insulin pathway and glycolysis and inhibited the expression of gluconeogenesis-related genes. Additionally, high dietary carbohydrate significantly reduced lysozyme content but increased complement C4 content, which were both reversed with RSV supplementation. Meanwhile, RSV inclusion inhibited the expression of pro-inflammatory cytokines but promoted anti-inflammatory cytokines expression, compared with the high carbohydrate treatment. In conclusion, RSV inclusion was beneficial in alleviating high-dietary-carbohydrate-induced glycogen accumulation and immune response in largemouth bass.

[1]  张伟涛,et al.  Megalobrama amblycephala , 2022, CABI Compendium.

[2]  Songlin Li,et al.  Starch in aquafeeds: The benefits of a high amylose to amylopectin ratio and resistant starch content in diets for the carnivorous fish, largemouth bass (Micropterus salmoides). , 2020, The British journal of nutrition.

[3]  Songlin Li,et al.  Antioxidant defenses and non-specific immunity at enzymatic and transcriptional levels in response to dietary carbohydrate in a typical carnivorous fish, hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂). , 2020, Fish & shellfish immunology.

[4]  Songlin Li,et al.  Effects of dietary carbohydrate sources on growth performance, glycogen accumulation, insulin signaling pathway and hepatic glucose metabolism in largemouth bass, Micropterus salmoides , 2019, Aquaculture.

[5]  X. Ge,et al.  Effects of dietary fenugreek seed extracts on growth performance, plasma biochemical parameters, lipid metabolism, Nrf2 antioxidant capacity and immune response of juvenile blunt snout bream (Megalobrama amblycephala). , 2019, Fish & shellfish immunology.

[6]  Songlin Li,et al.  The impacts of dietary carbohydrate levels on growth performance, feed utilization, glycogen accumulation and hepatic glucose metabolism in hybrid grouper (Epinephelus fuscoguttatus ♀ × E. lanceolatus ♂) , 2019, Aquaculture.

[7]  Wen‐bin Liu,et al.  Combined effects of dietary quercetin and resveratrol on growth performance, antioxidant capability and innate immunity of blunt snout bream (Megalobrama amblycephala) , 2019, Animal Feed Science and Technology.

[8]  Xiaoyan Xu,et al.  Complement component 3 (C3): An important role in grass carp (Ctenopharyngodon idella) experimentally exposed to Aeromonas hydrophila , 2019, Fish & shellfish immunology.

[9]  Shi‐Mei Lin,et al.  Effect of dietary starch level on growth, metabolism enzyme and oxidative status of juvenile largemouth bass, Micropterus salmoides , 2019, Aquaculture.

[10]  Wen‐bin Liu,et al.  Resveratrol Improves the Energy Sensing and Glycolipid Metabolism of Blunt Snout Bream Megalobrama amblycephala Fed High-Carbohydrate Diets by Activating the AMPK–SIRT1–PGC-1α Network , 2018, Front. Physiol..

[11]  Ming-Ming Mu,et al.  Effect of high dietary starch levels on growth, hepatic glucose metabolism, oxidative status and immune response of juvenile largemouth bass, Micropterus salmoides , 2018, Fish & shellfish immunology.

[12]  Mingzhu Pan,et al.  Chronic stress of high dietary carbohydrate level causes inflammation and influences glucose transport through SOCS3 in Japanese flounder Paralichthys olivaceus , 2018, Scientific Reports.

[13]  S. Xia,et al.  High fish oil diet promotes liver inflammation and activates the complement system. , 2018, Molecular medicine reports.

[14]  S. Dar,et al.  Alterations in non-specific immune responses, antioxidant capacities and expression levels of immunity genes in Labeo rohita fed with graded level of carbohydrates , 2018 .

[15]  Pei Li,et al.  Resveratrol attenuates high glucose-induced nucleus pulposus cell apoptosis and senescence through activating the ROS-mediated PI3K/Akt pathway , 2017, Bioscience reports.

[16]  Wen‐bin Liu,et al.  Resveratrol supplementation improves lipid and glucose metabolism in high-fat diet-fed blunt snout bream , 2017, Fish Physiology and Biochemistry.

[17]  Hongmei Wu,et al.  Resveratrol ameliorates diet-induced dysregulation of lipid metabolism in zebrafish (Danio rerio) , 2017, PloS one.

[18]  M. L. Michalani,et al.  Resveratrol Improves Glycemic Control in Type 2 Diabetic Obese Mice by Regulating Glucose Transporter Expression in Skeletal Muscle and Liver , 2017, Molecules.

[19]  M. Birnbaum,et al.  Unraveling the Regulation of Hepatic Metabolism by Insulin , 2017, Trends in Endocrinology & Metabolism.

[20]  M. L. Michalani,et al.  Resveratrol improves glycemic control in insulin-treated diabetic rats: participation of the hepatic territory , 2016, Nutrition & Metabolism.

[21]  S. Harpaz,et al.  Effects of different dietary carbohydrate levels on growth, feed utilization and body composition of juvenile grouper Epinephelus akaara , 2016 .

[22]  Jinyun Ye,et al.  The effects of dietary carbohydrate on the growth, antioxidant capacities, innate immune responses and pathogen resistance of juvenile Black carp Mylopharyngodon piceus. , 2016, Fish & shellfish immunology.

[23]  G. Nava,et al.  Resveratrol increases glycolytic flux in Saccharomyces cerevisiae via a SNF1-dependet mechanism , 2015, Journal of Bioenergetics and Biomembranes.

[24]  S. Kinsey,et al.  Effects of resveratrol on growth and skeletal muscle physiology of juvenile southern flounder. , 2015, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[25]  H. Ahmadieh,et al.  Anti‐inflammatory properties of resveratrol in the retinas of type 2 diabetic rats , 2015, Clinical and experimental pharmacology & physiology.

[26]  X. Ge,et al.  Effect of dietary carbohydrate on non-specific immune response, hepatic antioxidative abilities and disease resistance of juvenile golden pompano (Trachinotus ovatus). , 2014, Fish & shellfish immunology.

[27]  L. Tang,et al.  Dietary tryptophan modulates intestinal immune response, barrier function, antioxidant status and gene expression of TOR and Nrf2 in young grass carp (Ctenopharyngodon idella). , 2014, Fish & shellfish immunology.

[28]  P. Schrauwen,et al.  Therapeutic potential of resveratrol in obesity and type 2 diabetes: new avenues for health benefits? , 2013, Annals of the New York Academy of Sciences.

[29]  A. Gómez-Tato,et al.  Modulation by resveratrol of inflammatory and immune gene expression in turbot leucocytes , 2013 .

[30]  Zhong Zhong,et al.  SIRT1 Activators Suppress Inflammatory Responses through Promotion of p65 Deacetylation and Inhibition of NF-κB Activity , 2012, PloS one.

[31]  S. Panserat,et al.  Glucose metabolism in fish: a review , 2012, Journal of Comparative Physiology B.

[32]  Bo Liu,et al.  Effect of high dietary carbohydrate on growth, serum physiological response, and hepatic heat shock cognate protein 70 expression of the top-mouth culter Erythroculter ilishaeformis Bleeker , 2012, Fisheries Science.

[33]  R. DePinho,et al.  Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice. , 2012, Endocrinology.

[34]  Thomas A. Burgess,et al.  Improving glucose metabolism with resveratrol in a swine model of metabolic syndrome through alteration of signaling pathways in the liver and skeletal muscle. , 2011, Archives of surgery.

[35]  T. Szkudelski,et al.  Anti‐diabetic effects of resveratrol , 2011, Annals of the New York Academy of Sciences.

[36]  Y. Ahn,et al.  Role of resveratrol in FOXO1-mediated gluconeogenic gene expression in the liver. , 2010, Biochemical and biophysical research communications.

[37]  S. Subramanian,et al.  Resveratrol attenuates hyperglycemia-mediated oxidative stress, proinflammatory cytokines and protects hepatocytes ultrastructure in streptozotocin-nicotinamide-induced experimental diabetic rats. , 2010, Chemico-biological interactions.

[38]  M. Øverland,et al.  Starch source, screw configuration and injection of steam into the barrel affect the physical quality of extruded fish feed , 2010 .

[39]  T. Unterman,et al.  FoxO1 and HNF-4 Are Involved in Regulation of Hepatic Glucokinase Gene Expression by Resveratrol* , 2009, The Journal of Biological Chemistry.

[40]  S. Panserat,et al.  Nutritional regulation of hepatic glucose metabolism in fish , 2009, Fish Physiology and Biochemistry.

[41]  Raj Kishore,et al.  IL-10 Inhibits Inflammation and Attenuates Left Ventricular Remodeling After Myocardial Infarction via Activation of STAT3 and Suppression of HuR , 2009, Circulation research.

[42]  J. Olefsky,et al.  SIRT1 Exerts Anti-Inflammatory Effects and Improves Insulin Sensitivity in Adipocytes , 2008, Molecular and Cellular Biology.

[43]  R. Durborow,et al.  Effects of Graded Levels of Carbohydrate on Growth and Survival of Largemouth Bass, Micropterus salmoides , 2008 .

[44]  P. Sahoo,et al.  Lysozyme: an important defence molecule of fish innate immune system , 2008 .

[45]  Amy V. Lynch,et al.  Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes , 2007, Nature.

[46]  Q. Zhai,et al.  SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. , 2007, Cell metabolism.

[47]  R. DePinho,et al.  Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor Foxo1 in liver. , 2007, Cell metabolism.

[48]  Juei-Tang Cheng,et al.  Phosphatidylinositol-3-kinase is involved in the antihyperglycemic effect induced by resveratrol in streptozotocin-induced diabetic rats. , 2007, Life sciences.

[49]  A. Brunet,et al.  FOXO transcription factors , 2007, Current Biology.

[50]  P. Puigserver,et al.  Resveratrol Improves Mitochondrial Function and Protects against Metabolic Disease by Activating SIRT1 and PGC-1α , 2006, Cell.

[51]  P. Puigserver,et al.  Resveratrol improves health and survival of mice on a high-calorie diet , 2006, Nature.

[52]  Jiahuai Han,et al.  Limiting inflammatory responses during activation of innate immunity , 2005, Nature Immunology.

[53]  M. Permutt,et al.  Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. , 2005, Cell metabolism.

[54]  M. Mayo,et al.  Modulation of NF‐κB‐dependent transcription and cell survival by the SIRT1 deacetylase , 2004, The EMBO journal.

[55]  D. A. Stone,et al.  Dietary Carbohydrate Utilization by Fish , 2003 .

[56]  R. Lochmann,et al.  Massive Hepatic Necrosis and Nodular Regeneration in Largemouth Bass Fed Diets High in Available Carbohydrate , 2002 .

[57]  B. McCleary,et al.  Measurement of resistant starch by enzymatic digestion in starch and selected plant materials: collaborative study. , 2002, Journal of AOAC International.

[58]  John D Lambris,et al.  The complement system in teleosts. , 2002, Fish & shellfish immunology.

[59]  Takao Yokota,et al.  Plant foods and herbal sources of resveratrol. , 2002, Journal of agricultural and food chemistry.

[60]  C. Kahn,et al.  Insulin signalling and the regulation of glucose and lipid metabolism , 2001, Nature.

[61]  S. Panserat,et al.  Nutritional regulation and tissue specificity of gene expression for proteins involved in hepatic glucose metabolism in rainbow trout (Oncorhynchus mykiss). , 2001, The Journal of experimental biology.

[62]  S. Panserat,et al.  Hepatic phosphoenolpyruvate carboxykinase gene expression is not repressed by dietary carbohydrates in rainbow trout (Oncorhynchus mykiss). , 2001, The Journal of experimental biology.

[63]  H. Pahl.  Activators and target genes of Rel/NF-κB transcription factors , 1999, Oncogene.

[64]  L. Gold,et al.  Increased expression of transforming growth factor beta isoforms (beta 1, beta 2, beta 3) in bleomycin-induced pulmonary fibrosis. , 1995, American journal of respiratory cell and molecular biology.

[65]  A. Soivio,et al.  Changes in plasma lysozyme and blood leucocyte levels of hatchery-reared Atlantic salmon (Salmo salar L.) and sea trout (Salmo trutta L.) during parr-smolt transformation , 1992 .

[66]  P. Trinder,et al.  Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen , 1969, Journal of clinical pathology.

[67]  K. Pallauf,et al.  Dietary resveratrol impairs body weight gain due to reduction of feed intake without affecting fatty acid composition in Atlantic salmon. , 2019, Animal : an international journal of animal bioscience.

[68]  Y. Ding,et al.  Artesunate protects pancreatic beta cells against cytokine-induced damage via SIRT1 inhibiting NF-κB activation , 2015, Journal of Endocrinological Investigation.

[69]  S. Panserat,et al.  Lack of significant long-term effect of dietary carbohydrates on hepatic glucose-6-phosphatase expression in rainbow trout (Oncorhynchus mykiss). , 2000, The Journal of nutritional biochemistry.

[70]  S. Seifter,et al.  The estimation of glycogen with the anthrone reagent. , 1950, Archives of biochemistry.