Assessing the hepatoprotective effects of hesperidin on liver-associated disorders in albino rats with experimentally induced obesity and type II diabetes: A histological and biochemical study

Heliyon - Tập 9 - Trang e16031 - 2023
Ihab Shafek Atta1,2, Mohamed R. Elnady3, Ali G. Alghamdi4, Ahmed Hassan Alghamdi5, Alaa A. Aboulata6,7, Ibrahim M. Shatla3,8
1Pathology Department, Faculty of Medicine, Al-Azhar University, Assuit, Egypt
2Pathology Department, Faculty of Medicine, Al Baha University, Saudi Arabia
3Physiology Department, Damietta Faculty of Medicine, Al-Azhar University, Egypt
4Surgery Department, Faculty of Medicine, Al Baha University, Saudi Arabia
5Paediatric Department, Faculty of Medicine, Al Baha University, Saudi Arabia
6Microbiology and Immunology Department, Faculty of Medicine, Al-Azhar University, Egypt
7Biomedical and Dental Sciences, Faculty of Dentistry, Al Baha University, Saudi Arabia
8Physiology Department, Faculty of Medicine, Al Baha University, Saudi Arabia

Tài liệu tham khảo

Galicia-Garcia, 2020, Pathophysiology of type 2 diabetes mellitus, Int. J. Mol. Sci., 21, 6275, 10.3390/ijms21176275 Saeedi, 2019, Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 157 Williams, 2020, Global and regional estimates, and projections of diabetes-related health expenditure: results from the international diabetes federation diabetes atlas Hamed, 2019, Diabetes association with liver diseases: an overview for clinicians, Endocr., Metab. Immune Disord.: Drug Targets, 19, 274, 10.2174/1871530318666181116111945 Loria, 2013, Liver, and diabetes. A vicious circle, Hepatol. Res., 43, 51, 10.1111/j.1872-034X.2012.01031.x Machado, 2015, Hepatic steatosis: a role for mitochondria in the pathogenesis of nonalcoholic fatty liver disease, J. Lipid Res., 56, 2233 Younossi, 2019, Global epidemiology of nonalcoholic fatty liver disease—meta‐analytic assessment of prevalence, incidence, and outcomes, Hepatology, 71, 1913 Rizza, 2018, Evaluation of the safety and efficacy of Hesperidin supplementation in human: a systematic review of clinical trials, Phytother Res., 32, 219 Morand, 2011 Pandey, 2019, Hesperidin induces ROS-mediated apoptosis along with cell cycle arrest at G2/M phase in human gall bladder carcinoma, Nutr. Cancer, 71, 676, 10.1080/01635581.2018.1508732 Jo, 2019, Hesperetin inhibits neuroinflammation on microglia by suppressing inflammatory cytokines and MAPK pathways, Arch Pharm. Res. (Seoul), 42, 695, 10.1007/s12272-019-01174-5 Ciftci, 2015, Hesperidin, a Citrus flavonoid, has the ameliorative effects against experimental autoimmune encephalomyelitis (EAE) in a C57BL/J6 mouse model, Neurochem. Res., 40, 1111, 10.1007/s11064-015-1571-8 El-Shahawy, 2021, A novel layered double hydroxide-hesperidin nanoparticles exert antidiabetic, antioxidant and anti-infammatory efects in rats with diabetes, Mol. Biol. Rep., 48, 5217, 10.1007/s11033-021-06527-2 Zanwar, 2014, Chapter 76 - cardiovascular effects of hesperidin: a Flavanone glycoside, 989 Li, 2019, Acute and sub-chronic oral toxicity studies of hesperidin isolated from orange peel extract in Sprague Dawley rats, Regul. Toxicol. Pharmacol., 105, 77, 10.1016/j.yrtph.2019.04.001 Xue, 2016, Improved glycemic control and vascular function in overweight and obese subjects by glyoxalase 1 inducer formulation, Diabetes, 65, 2282, 10.2337/db16-0153 Xue, 2012, Transcriptional control of glyoxalase 1 by Nrf2 provides a stress-responsive defence against dicarbonyl glycation, Biochem. J., 443, 213, 10.1042/BJ20111648 Liu, 2017, Mangiferin upregulates glyoxalase 1 through activation of Nrf2/ARE signaling in central neurons cultured with high glucose, Mol. Neurobiol., 54, 4060, 10.1007/s12035-016-9978-z Chen, 2019, Hesperetin ameliorates diabetic nephropathy in rats by activating Nrf2/ARE/glyoxalase 1 pathway, Biomed. Pharmacother., 111, 1166, 10.1016/j.biopha.2019.01.030 Chen, 2010, Hesperidin upregulates heme oxygenase-1 to attenuate hydrogen peroxide-induced cell damage in hepatic L02 cells, J. Agric. Food Chem., 58, 3330, 10.1021/jf904549s Ren, 2016, Hesperetin suppresses inflammatory responses in lipopolysaccharide-induced RAW 264.7 cells via the inhibition of NF-kappaB and activation of Nrf2/HO-1 pathways, Inflammation, 39, 964 Lee, 2021, Phytochemicals in cancer immune checkpoint inhibitor therapy, Biomolecules, 11, 1107, 10.3390/biom11081107 Rizzo, 2022, Which role for predictors of response to immune checkpoint inhibitors in hepatocellular carcinoma?, Expet Rev. Gastroenterol. Hepatol., 16, 333, 10.1080/17474124.2022.2064273 Rizzo, 2022, Biomarkers for breast cancer immunotherapy: PD-L1, TILs, and beyond, Expet Opin. Invest. Drugs, 31, 549, 10.1080/13543784.2022.2008354 Esmail, 2021, Effect of Nigella sativa, atorvastatin, or L-Carnitine on high fat diet-induced obesity in adult male Albino rats, Biomed. Pharmacother., 141, 10.1016/j.biopha.2021.111818 2011 Tietz, 1995, 268 Carlsson, 2010, Concomitant enzyme-linked immunosorbent assay measurements of rat insulin, rat C-peptide, and rat proinsulin from rat pancreatic islets: effects of prolonged exposure to different glucose concentrations, Endocrinology, 151, 5048, 10.1210/en.2010-0433 Matthews, 1985, Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man, Diabetologia, 28, 412, 10.1007/BF00280883 Friedewald, 1972, Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge, Clin. Chem., 18, 499, 10.1093/clinchem/18.6.499 Krishnaveni, 2015, Assessing the validity of friedewald's formula and anandraja's formula for serum LDL-cholesterol calculation, J. Clin. Diagn. Res., 9, BC01 Nishikimi, 1972, The occurrence of superoxide anion in the reaction ofreduced phenazinemethosulfate and molecular oxygen, Biochem. Biophys. Res. Commun., 46, 849, 10.1016/S0006-291X(72)80218-3 Aebi, 1983, Catalase, 273 Prins, 1969, 127 Drury, 1983, Theory and practice of histological techniques, J. Clin. Pathol., 36, 609, 10.1136/jcp.36.5.609-d Torbenson, 2014 Albersen, 2011, Functional, metabolic, and morphologic characteristics of a novel rat model of type 2 diabetes-associated erectile dysfunction, Urology, 78, e471 Sahin, 2007, Effect of chromium on carbohydrate and lipid metabolism in a rat model of type 2 diabetes mellitus: the fat-fed, streptozotocin-treated rat, Metab., Clin. Exp., 56, 1233, 10.1016/j.metabol.2007.04.021 Srinivasan, 2005, Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening, Pharmacol. Res., 52, 313, 10.1016/j.phrs.2005.05.004 El-Bassossy, 2015, Xanthine oxidase inhibition alleviates the cardiac complications of insulin resistance: effect on low grade inflammation and the angiotensin system, J. Transl. Med., 13, 82, 10.1186/s12967-015-0445-9 Lee, 2015, Histologic and metabolic derangement in high-fat, high-fructose, and combination diet animal models, TheScientificWorldJOURNAL, 10.1155/2015/306326 Pyo, 2014, Preventive effect of Monascus-fermented products enriched with ubiquinones on type 2 diabetic rats induced by a high-fructose plus high-fat diet, J. Med. Food, 17, 826, 10.1089/jmf.2013.3001 Reed, 2000, A new rat model of type 2 diabetes: the fat-fed, streptozotocin-treated rat, Metab., Clin. Exp., 49, 1390, 10.1053/meta.2000.17721 Zhang, 2008, The characterization of high-fat diet and multiple low-dose streptozotocin induced type 2 diabetes rat model, Exp. Diabetes Res., 10.1155/2008/704045 Sharma, 2008, Hypoglycemic and hypolipidemic effects of flavonoid rich extract from Eugenia jambolana seeds on streptozotocin induced diabetic rats, Food Chem. Toxicol., 46, 2376, 10.1016/j.fct.2008.03.020 Cao, 2007, Green tea polyphenol extract regulates the expression of genes involved in glucose uptake and insulin signaling in rats fed a high fructose diet, J. Agric. Food Chem., 55, 6372, 10.1021/jf070695o Miyake, 1998, Protective effects of lemon flavonoids on oxidative stress in diabetic rats, Lipids, 33, 689, 10.1007/s11745-998-0258-y Jung, 2006, Effect of citrus flavonoids on lipid metabolism and glucose-regulating enzyme mRNA levels in type-2 diabetic mice, Int. J. Biochem. Cell Biol., 38, 1134, 10.1016/j.biocel.2005.12.002 Abdel-Moneim, 2011, Insulin sensitizing effects of hesperidin and naringin in experimental model of induced type 2 diabetes in rats: focus on tumor necrosis factor-alpha and resistin, Nat. Sci., 7, 134 Hu, 2013, Pioglitazone ameliorates intracerebral insulin resistance and tau‐protein hyperphosphorylation in rats with type 2 diabetes, Exp. Clin. Endocrinol. Diabetes, 121, 220, 10.1055/s-0032-1333277 Abo-elmatty, 2013, Antioxidant and anti‐inflammatory effects of Urtica pilulifera extracts in type 2 diabetic rats, J. Ethnopharmacol., 145, 269, 10.1016/j.jep.2012.11.002 Khan, 2013, Anti‐inflammatory and anti‐hyperlipidemic effect of Semecarpus anacardium in a high fat diet: STZ‐induced type 2 diabetic rat model, Inflammopharmacology, 21, 37, 10.1007/s10787-011-0109-1 Gandhi, 2013, Insulin sensitization via partial agonism of PPAR gamma and glucose uptake through translocation and activation of GLUT4 in PI3K/p‐Akt signaling pathway by embelin in type 2 diabetic rats, Biochim. Biophys. Acta, 1830, 2243, 10.1016/j.bbagen.2012.10.016 Horcajada, 2008, Hesperidin inhibits ovariectomized-induced osteopenia and shows differential effects on bone mass and strength in young and adult intact rats, J. Appl. Physiol., 104, 648, 10.1152/japplphysiol.00441.2007 Akiyama, 2010, Dietary hesperidin exerts hypoglycemic and hypolipidemic effects in streptozotocin-induced marginal type 1 diabetic rats, J. Clin. Biochem. Nutr., 46, 87, 10.3164/jcbn.09-82 Bok, 1999, Plasma and hepatic cholesterol and hepatic activities of 3-hydroxy-3-methyl-glutaryl-CoA reductase and acyl CoA: cholesterol transferase are lower in rats fed citrus peel extract or a mixture of citrus bioflavonoids, J. Nutr., 129, 1182, 10.1093/jn/129.6.1182 Wilcox, 2001, Secretion of hepatocyte apoB is inhibited by the flavonoids, naringenin and hesperetin, via reduced activity and expression of ACAT2 and MTP, J. Lipid Res., 42, 725, 10.1016/S0022-2275(20)31634-5 Azuma, 2007, Lowering effects of onion intake on oxidative stress biomarkers in streptozotocin-induced diabetic rats, J. Clin. Biochem. Nutr., 40, 131, 10.3164/jcbn.40.131 Jalal, 2007, Hypoglycemic effect of aqueous shallot and garlic extracts in rats with fructose-induced insulin resistance, J. Clin. Biochem. Nutr., 41, 218, 10.3164/jcbn.2007031 Stanley Mainzen Prince, 2006, Rutin improves glucose homeostasis in streptozotocin diabetic tissues by altering glycolytic and gluconeogenic enzymes, J. Biochem. Mol. Toxicol., 20, 96, 10.1002/jbt.20117 Chen, 2016, Elevated Interleukin-17 levels in patients with newly diagnosed type 2 diabetes mellitus, Biochem Physiol, 5, 206, 10.4172/2168-9652.1000206 Ohshima, 2012, Roles of interleukin 17 in angiotensin II type 1 receptor-mediated insulin resistance, Hypertension, 59, 493, 10.1161/HYPERTENSIONAHA.111.183178 Marx, 2003, Antidiabetic PPAR gamma-activator rosiglitazone reduces MMP-9 serum levels in type 2 diabetic patients with coronary artery disease, Arterioscler. Thromb. Vasc. Biol., 23, 283, 10.1161/01.ATV.0000054195.35121.5E Wang, 2006, Tumor necrosis factor-induced toxic liver injury results from JNK2-dependent activation of caspase-8 and the mitochondrial death pathway, J. Biol. Chem., 281, 15258, 10.1074/jbc.M512953200 Kohl, 2013, Diabetic liver injury from streptozotocin is regulated through the caspase-8 homolog cFLIP involving activation of JNK2 and intrahepatic immunocompetent cells, Cell Death Dis., 4, 10.1038/cddis.2013.228 Barrière, 2018, Combination of high-fat/high-fructose diet and low-dose streptozotocin to model long-term type-2 diabetes complications, Sci. Rep., 8, 424, 10.1038/s41598-017-18896-5 Mo'men, 2019, Involvement of PI3K/Akt pathway in the protective effect of hesperidin against a chemically induced liver cancer in rats, J. Biochem. Mol. Toxicol., 33 Qi, 2019, Hesperidin inhibits synovial cell inflammation and macrophage polarization through suppression of the PI3K/AKT pathway in complete Freund's adjuvant-induced arthritis in mice, Chem. Biol. Interact., 306, 19, 10.1016/j.cbi.2019.04.002 Justin-Thenmozhi, 2018, Attenuation of aluminum chloride-induced neuroinflammation and caspase activation through the AKT/GSK-3β pathway by hesperidin in wistar rats, Neurotox. Res., 34, 463, 10.1007/s12640-018-9904-4 Li, 2016, Short-term hesperidin pretreatment attenuates rat myocardial ischemia/reperfusion injury by inhibiting high mobility group box 1 protein expression via the PI3K/Akt pathway, Cell. Physiol. Biochem., 39, 1850, 10.1159/000447884 Li, 2020, Hesperidin ameliorates liver ischemia/reperfusion injury via activation of the Akt pathway, Mol. Med. Rep., 22, 4519, 10.3892/mmr.2020.11561 Park, 2019, Hesperidin ameliorates hepatic ischemia-reperfusion injury in Sprague-Dawley rats, Transplant. Proc., 51, 2828, 10.1016/j.transproceed.2019.02.059 Cassiman, 2001, Human and rat hepatic stellate cells express neurotrophins and neurotrophin receptors, Hepatology, 33, 148, 10.1053/jhep.2001.20793 Michalopoulos, 2005, Liver regeneration, growth factors, and amphiregulin, Gastroenterology, 128, 503, 10.1053/j.gastro.2004.12.039 Gebhardt, 2007, Hepatocellular expression of glutamine synthetase: an indicator of morphogen actions as master regulators of zonation in adult liver, Prog. Histochem. Cytochem., 41, 201, 10.1016/j.proghi.2006.12.001