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Current Pharmaceutical Biotechnology

Editor-in-Chief

ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

Research Article

Salvia officinalis Improves Glycemia and Suppresses Pro-inflammatory Features in Obese Rats with Metabolic Syndrome

Author(s): Diana A. Alsherif, Mohammed A. Hussein* and Suzan S. Abuelkasem

Volume 25, Issue 5, 2024

Published on: 18 August, 2023

Page: [623 - 636] Pages: 14

DOI: 10.2174/1389201024666230811104740

Price: $65

Abstract

Objectives: Obesity is regarded as the main cause of metabolic diseases and a core factor for all-cause mortality in the general population, notably from cardiovascular disease. The majority of people with type 2 diabetes have obesity and insulin resistance. Some evidence indicates that an individual with obesity is approximately 10 times more likely to develop type 2 diabetes than someone with moderate body weight.

One of the most significant therapeutic herbs, Salvia officinalis (Lamiaceae) (SAGE), possesses potent medicinal importance. The aim of this article was to evaluate the anti-diabetic and antiobesity activity of SAGEAE against HFD-induced obesity in rats.

Methods: Thirty adult albino rats were randomly divided into five equal groups: control, High-fat Diet (HFD) administrated rats, HFD + Salvia officinalis Aqueous Extract (SAGEAE) (150 mg/kg.bw.), HFD + SAGEAE (300 mg/kg.bw.) and HFD + metformin (500 mg/kg.bw.). Body weight, plasma biochemical parameters, oxidative stress, inflammatory indicators, hepatic Phosphoenolpyruvate Carboxykinase 1 (PCK1), Glucokinase (GK), brain Leptin Receptor (LepRb), Glucose Transporter-4 (GLUT4), Sirtuin 1 (SIRT1) and mRNA33-5P gene signalling mRNA levels were all assessed after 8 weeks. A histological examination of the liver was also performed to check for lipid accumulation.

Results: The administration of HFD resulted in increased body weight, glucose, insulin, leptin, Total Cholesterol (TC), Triglycerides (TG), Thiobarbaturic Acid Reactive Substances (TBARS), Monocyte Chemoattractant Protein-1 (MCP1), Interleukine-6 (IL-6) and tumor necrosis factor-α (TNF- α) as well as hepatic PCK1, brain LepRb and adipose tissue mRNA33-5P gene expression. However, our findings revealed a significant reduction in adiponectin, High-density Lipoproteincholesterol (HDL-C), reduced glutathione (GSH) and Superoxide Dismutase (SOD) levels as well as the expression of hepatic GK and adipose tissue SIRT1 and GLUT4 genes. Also, administration of SAGEAE significantly normalized body weight, glucose, insulin, leptin, adiponectin, TC, TG, HDL-C, TBARs, SOD, IL-6, MCP-1 and TNF-α in plasma and liver tissue of HFD-treated rats. On the other hand, PCK1, GK, LepRb, SIRT1, GLUT4 and mRNA33-5P gene expression was enhanced in obese rats when administrated with SAGEAE. Histological and US studies support the biochemical, PCR and electrophoretic results.

Conclusion: The findings imply that SAGEAE could be used as a new pharmaceutical formula in the treatment of obesity.

Keywords: SAGE, insulin, leptin, PCK1, GK, LepRb, SIRT1, adiponectin, GLUT4, mRNA33-5P.

Graphical Abstract
[1]
Ren, J.; Wu, N.N.; Wang, S.; Sowers, J.R.; Zhang, Y. Obesity cardiomyopathy: Evidence, mechanisms, and therapeutic implications. Physiol. Rev., 2021, 101(4), 1745-1807.
[http://dx.doi.org/10.1152/physrev.00030.2020] [PMID: 33949876]
[2]
Abdelaal, M.; le Roux, C.W.; Docherty, N.G. Morbidity and mortality associated with obesity. Ann. Transl. Med., 2017, 5(7), 161-175.
[http://dx.doi.org/10.21037/atm.2017.03.107] [PMID: 28480197]
[3]
Abdalla, H.M. Purslane extract effects on obesity-induced diabetic rats fed a high-fat diet. Malays. J. Nutr., 2010, 16(3), 419-429.
[PMID: 22691995]
[4]
M Soliman, S. Mosallam, S.; Mamdouh, M.A.; Hussein, M.A.; M Abd El-Halim, S. Design and optimization of cranberry extract loaded bile salt augmented liposomes for targeting of MCP-1/STAT3/VEGF signaling pathway in DMN-intoxicated liver in rats. Drug Deliv., 2022, 29(1), 427-439.
[http://dx.doi.org/10.1080/10717544.2022.2032875] [PMID: 35098843]
[5]
Mohamad, E.A.; Mohamed, Z.N.; Hussein, M.A.; Elneklawi, M.S. GANE can improve lung fibrosis by reducing inflammation via promoting p38MAPK/TGF-β1/NF-κB signaling pathway downregulation. ACS Omega, 2022, 7(3), 3109-3120.
[http://dx.doi.org/10.1021/acsomega.1c06591] [PMID: 35097306]
[6]
Deshmane, S.L.; Kremlev, S.; Amini, S.; Sawaya, B.E. Monocyte chemoattractant protein-1 (MCP-1): An overview. J. Interferon Cytokine Res., 2009, 29(6), 313-326.
[http://dx.doi.org/10.1089/jir.2008.0027] [PMID: 19441883]
[7]
Murphy, E.A. Novel adipocytokines: Monocyte chemotactic protein-1, plasminogen activator inhibitor-1, chemerin. Energy Balance and Cancer, 2017, 12, 161-186.
[http://dx.doi.org/10.1007/978-3-319-41677-9_8]
[8]
Zhang, Y.; Li, R.; Chen, W.; Li, Y.; Chen, G. Retinoids induced Pck1 expression and attenuated insulin-mediated suppression of its expression via activation of retinoic acid receptor in primary rat hepatocytes. Mol. Cell. Biochem., 2011, 355(1-2), 1-8.
[http://dx.doi.org/10.1007/s11010-011-0831-4] [PMID: 21519922]
[9]
Chen, G.; Zhang, Y.; Lu, D.; Li, N.; Ross, A.C. Retinoids synergize with insulin to induce hepatic Gck expression. Biochem. J., 2009, 419(3), 645-653.
[http://dx.doi.org/10.1042/BJ20082368] [PMID: 19173678]
[10]
Xu, J.; Zhang, M.; Zhang, X.; Yang, H.; Sun, B.; Wang, Z.; Zhou, Y.; Wang, S.; Liu, X.; Liu, L. Contribution of hepatic retinaldehyde dehydrogenase induction to impairment of glucose metabolism by high-fat-diet feeding in C57BL/6J mice. Basic Clin. Pharmacol. Toxicol., 2018, 123(5), 539-548.
[http://dx.doi.org/10.1111/bcpt.13039] [PMID: 29753302]
[11]
Snider, N.T.; Leonard, J.M.; Kwan, R.; Griggs, N.W.; Rui, L.; Omary, M.B. Glucose and SIRT2 reciprocally mediate the regulation of keratin 8 by lysine acetylation. J. Cell Biol., 2013, 200(3), 241-247.
[http://dx.doi.org/10.1083/jcb.201209028] [PMID: 23358244]
[12]
Sun, K.; Wang, X.; Fang, N.; Xu, A. lin, Y.; Zhao, X.; Nazarali, A.J.; Ji, S. SIRT2 suppresses expression of inflammatory factors via Hsp90-glucocorticoid receptor signalling. J. Cell. Mol. Med., 2020, 24(13), 7439-7450.
[http://dx.doi.org/10.1111/jcmm.15365] [PMID: 32515550]
[13]
Min, J.S.; Kim, J.C.; Kim, J.A.; Kang, I.; Ahn, J.K. SIRT2 reduces actin polymerization and cell migration through deacetylation and degradation of HSP90. Biochim. Biophys. Acta Mol. Cell Res., 2018, 1865(9), 1230-1238.
[http://dx.doi.org/10.1016/j.bbamcr.2018.06.005] [PMID: 29908203]
[14]
Barrios, V.; Frago, L.M.; Canelles, S.; Guerra-Cantera, S.; Arilla-Ferreiro, E.; Chowen, J.A.; Argente, J. Leptin modulates the response of brown adipose tissue to negative energy balance: Implication of the GH/IGF-I axis. Int. J. Mol. Sci., 2021, 22(6), 2827.
[http://dx.doi.org/10.3390/ijms22062827] [PMID: 33799501]
[15]
Fang, P.; He, B.; Yu, M.; Shi, M.; Zhu, Y.; Zhang, Z.; Bo, P. Treatment with celastrol protects against obesity through suppression of galanin-induced fat intake and activation of PGC-1α/GLUT4 axis-mediated glucose consumption. Biochim. Biophys. Acta Mol. Basis Dis., 2019, 1865(6), 1341-1350.
[http://dx.doi.org/10.1016/j.bbadis.2019.02.002] [PMID: 30742994]
[16]
Min, W.; Wu, M.; Fang, P.; Yu, M.; Shi, M.; Zhang, Z.; Bo, P. Effect of baicalein on GLUT4 translocation in adipocytes of diet-induced obese mice. Cell. Physiol. Biochem., 2018, 50(2), 426-436.
[http://dx.doi.org/10.1159/000494154] [PMID: 30308480]
[17]
Yang, Y.; Jiang, H.; Xiao, L.; Yang, X. MicroRNA-33b-5p is overexpressed and inhibits GLUT4 by targeting HMGA2 in polycystic ovarian syndrome: An in vivo and in vitro study. Oncol. Rep., 2018, 39(6), 3073-3085.
[http://dx.doi.org/10.3892/or.2018.6375] [PMID: 29693142]
[18]
Ghorbani, A.; Esmaeilizadeh, M. Pharmacological properties of Salvia officinalis and its components. J. Tradit. Complement. Med., 2017, 7(4), 433-440.
[http://dx.doi.org/10.1016/j.jtcme.2016.12.014] [PMID: 29034191]
[19]
Poulios, E.; Giaginis, C.; Vasios, G.K. Current advances on the extraction and identification of bioactive components of sage (Salvia spp.). Curr. Pharm. Biotechnol., 2019, 20(10), 845-857.
[http://dx.doi.org/10.2174/1389201020666190722130440] [PMID: 31333123]
[20]
Poulios, E.; Giaginis, C.; Vasios, G.K. Current state of the art on the antioxidant activity of sage (Salvia spp.) and its bioactive components. Planta Med., 2020, 86(4), 224-238.
[http://dx.doi.org/10.1055/a-1087-8276] [PMID: 31975363]
[21]
Yanagimichi, M.; Nishino, K.; Sakamoto, A.; Kurodai, R.; Kojima, K.; Eto, N.; Isoda, H.; Ksouri, R.; Irie, K.; Kambe, T.; Masuda, S.; Akita, T.; Maejima, K.; Nagao, M. Analyses of putative anti-cancer potential of three STAT3 signaling inhibitory compounds derived from Salvia officinalis. Biochem. Biophys. Rep., 2021, 25, 100882.
[http://dx.doi.org/10.1016/j.bbrep.2020.100882] [PMID: 33392396]
[22]
Hussein, M.A.; Ismail, N.E.M.; Mohamed, A.H.; Borik, R.M.; Ali, A.A.; Mosaad, Y.O. Plasma phospholipids: A promising simple biochemical parameter to evaluate covid-19 infection severity. Bioinform. Biol. Insights, 2021, 15.
[http://dx.doi.org/10.1177/11779322211055891] [PMID: 34840499]
[23]
Boshra, S.A.; Hussein, M.A. Cranberry extract as a supplemented food in treatment of oxidative stress and breast cancer induced by N-Methyl-N-Nitrosourea in female virgin rats. Int. J. Phytomed., 2016, 8(2), 217-227.
[24]
Hussein, M.A.; Borik, R.M. A novel quinazoline-4-one derivatives as a promising cytokine inhibitors: Synthesis, Molecular docking, and structure-activity relationship. Curr. Pharm. Biotechnol., 2022, 23(9), 1179-1203.
[http://dx.doi.org/10.2174/1389201022666210601170650] [PMID: 34077343]
[25]
Gobba, N.A.E.K.; Hussein Ali, A.; El Sharawy, D.E.; Hussein, M.A. The potential hazardous effect of exposure to iron dust in Egyptian smoking and nonsmoking welders. Arch. Environ. Occup. Health, 2018, 73(3), 189-202.
[http://dx.doi.org/10.1080/19338244.2017.1314930] [PMID: 28375782]
[26]
M Fayed, A. A Abdalla, E.; Hassan, S.A.; A Hussein, M.; M Roshdy, T. Downregulation of TLR4-NF-?B-p38 MAPK signalling in cholestatic rats treated with cranberry extract. Pak. J. Biol. Sci., 2022, 25(2), 112-122.
[http://dx.doi.org/10.3923/pjbs.2022.112.122] [PMID: 35233999]
[27]
Lee, A.; Morley, J.E. Metformin decreases food consumption and induces weight loss in subjects with obesity with type II non-insulin-dependent diabetes. Obes. Res., 1998, 6(1), 47-53.
[http://dx.doi.org/10.1002/j.1550-8528.1998.tb00314.x] [PMID: 9526970]
[28]
Assinewe, V.A.; Baum, B.R.; Gagnon, D.; Arnason, J.T. Phytochemistry of wild populations of Panax quinquefolius L. (North American ginseng). J. Agric. Food Chem., 2003, 51(16), 4549-4553.
[http://dx.doi.org/10.1021/jf030042h] [PMID: 14705875]
[29]
Troisi, R.J.; Cowie, C.C.; Harris, M.I. Diurnal variation in fasting plasma glucose: Implications for diagnosis of diabetes in patients examined in the afternoon. JAMA, 2000, 284(24), 3157-3159.
[http://dx.doi.org/10.1001/jama.284.24.3157] [PMID: 11135780]
[30]
Fossati, P.; Prencipe, L. Serum triglycerides determined colorimetrically with an enzyme that produces hydrogen peroxide. Clin. Chem., 1982, 28(10), 2077-2080.
[http://dx.doi.org/10.1093/clinchem/28.10.2077] [PMID: 6812986]
[31]
Allain, C.C.; Poon, L.S.; Chan, C.S.G.; Richmond, W.; Fu, P.C. Enzymatic determination of total serum cholesterol. Clin. Chem., 1974, 20(4), 470-475.
[http://dx.doi.org/10.1093/clinchem/20.4.470] [PMID: 4818200]
[32]
Burstein, M.; Scholnick, H.R.; Morfin, R. Rapid method for the isolation of lipoproteins from human serum by precipitation with polyanions. J. Lipid Res., 1970, 11(6), 583-595.
[http://dx.doi.org/10.1016/S0022-2275(20)42943-8] [PMID: 4100998]
[33]
Tsikas, D. Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Anal. Biochem., 2017, 524, 13-30.
[http://dx.doi.org/10.1016/j.ab.2016.10.021] [PMID: 27789233]
[34]
Owen, J.B.; Butterfield, D.A. Measurement of oxidized/reduced glutathione ratio. Methods Mol. Biol., 2010, 648, 269-277.
[http://dx.doi.org/10.1007/978-1-60761-756-3_18] [PMID: 20700719]
[35]
Kakkar, P.; Das, B.; Visvanathan, P. A modified spectrophotometric assay of SOD. Indian J. Biochem. Biophys., 1984, 21, 130-132.
[PMID: 6490072]
[36]
Bancroft, G.D.; Steven, A. Theory and Practice of Histological Technique, 4th ed; Churchill Livingstone: New York, 1983, pp. 99-112.
[37]
Fan, J.G.; Jia, J.D.; Li, Y.M.; Wang, B.Y.; Lu, L.G.; Shi, J.P.; Chan, L.Y. Guidelines for the diagnosis and management of nonalcoholic fatty liver disease: Update 2010: (published in Chinese on Chinese Journal of Hepatology 2010; 18:163-166). J. Dig. Dis., 2011, 12(1), 38-44.
[http://dx.doi.org/10.1111/j.1751-2980.2010.00476.x] [PMID: 21276207]
[38]
Roa, M.; Blane, K.; Zonneberg, M. One way analysis of variance.Version IA (C); PC-STAT, Program coded by University of Georgia: USA, 1985.
[39]
Wood, I.S.; de Heredia, F.P.; Wang, B.; Trayhurn, P. Cellular hypoxia and adipose tissue dysfunction in obesity. Proc. Nutr. Soc., 2009, 68(4), 370-377.
[http://dx.doi.org/10.1017/S0029665109990206] [PMID: 19698203]
[40]
Zhang, J.; Celli, G.B.; Brooks, M.S. Natural sources of anthocyanins. In: In Anthocyanins from Natural Sources: Exploiting Targeted Delivery for Improved Health,, 1st ed.; Brooks, M.S.L.; Celli, G.B. Eds;.. The Royal Society of Chemistry: Cambridge, UK, 2019; 7, pp. 154-196.
[41]
Lu, Y.; Yeap Foo, L. Antioxidant activities of polyphenols from sage (Salvia officinalis). Food Chem., 2001, 75(2), 197-202.
[http://dx.doi.org/10.1016/S0308-8146(01)00198-4]
[42]
Azevedo, M.F.; Camsari, Ç.; Sá, C.M.; Lima, C.F..; Fernandes- Ferreira, M.; Pereira-Wilson, C. Ursolic acid and luteolin-7- glucoside improve lipid profiles and increase liver glycogen content through glycogen synthase kinase-3. Phytother. Res., 2010, 24(S2), S220-S224.
[http://dx.doi.org/10.1002/ptr.3118] [PMID: 20127879]
[43]
Demori, I.; Voci, A.; Fugassa, E.; Burlando, B. Combined effects of high-fat diet and ethanol induce oxidative stress in rat liver. Alcohol, 2006, 40(3), 185-191.
[http://dx.doi.org/10.1016/j.alcohol.2006.12.006] [PMID: 17418698]
[44]
Sá,C.; Ramos, A.; Azevedo, M.; Lima, C.; Fernandes-Ferreira, M.; Pereira-Wilson, C. Sage tea drinking improves lipid profile and antioxidant defences in humans. Int. J. Mol. Sci., 2009, 10(9), 3937-3950.
[http://dx.doi.org/10.3390/ijms10093937] [PMID: 19865527]
[45]
Rozenberg, O.; Aviram, M. S-Glutathionylation regulates HDL-associated paraoxonase 1 (PON1) activity. Biochem. Biophys. Res. Commun., 2006, 351(2), 492-498.
[http://dx.doi.org/10.1016/j.bbrc.2006.10.059] [PMID: 17070779]
[46]
Uzun, H.; Konukoglu, D.; Gelisgen, R.; Zengin, K.; Taskin, M. Plasma protein carbonyl and thiol stress before and after laparoscopic gastric banding in morbidly obese patients. Obes. Surg., 2007, 17(10), 1367-1373.
[http://dx.doi.org/10.1007/s11695-007-9242-8] [PMID: 18000722]
[47]
Wu, T.; Gao, Y.; Guo, X.; Zhang, M.; Gong, L. Blackberry and blueberry anthocyanin supplementation counteract high-fat-diet-induced obesity by alleviating oxidative stress and inflammation and accelerating energy expenditure. Oxid. Med. Cell. Longev., 2018, 2018, 1-9.
[http://dx.doi.org/10.1155/2018/4051232] [PMID: 30057677]
[48]
Fayed, A.; Ibrahem, M.A.; Hassan, S.A.; Hussein, M.A.; Roshdy, T. Cranberry extract as a promising functional food to regulate srebp1/ppar–α/cpt-1/aco signaling pathways in HFD-induced obesity in rats. Adv. Anim. Vet. Sci., 2022, 10(9), 1933-1944.
[http://dx.doi.org/10.17582/journal.aavs/2022/10.9.1933.1944]
[49]
ESuanarun sawat, T.; Wacharaporn, D.N.A.; Songsak, T.; Rattanamahamphoom, J. Anti-lipidemic actions of essential oil extracted from ociumum Sanctum L. J. Appl. Biomed., 2009, 7, 45-53.
[http://dx.doi.org/10.32725/jab.2009.004]
[50]
El Gizawy, H.A.E.H.; Hussein, M.A.; Abdel-Sattar, E. Biological activities, isolated compounds and HPLC profile of Verbascum nubicum. Pharm. Biol., 2019, 57(1), 485-497.
[http://dx.doi.org/10.1080/13880209.2019.1643378] [PMID: 31401911]
[51]
Siddiqui, J.A.; Partridge, N.C. CCL2/Monocyte chemoattractant protein 1 and parathyroid hormone action on bone. Front. Endocrinol., 2017, 8, 49.
[http://dx.doi.org/10.3389/fendo.2017.00049] [PMID: 28424660]
[52]
Morrison, N.A.; Forwood, M.R. Monocyte chemotactic protein-1 (MCP1) accumulation in human osteoclast precursor cultures. Life, 2022, 12(6), 789.
[http://dx.doi.org/10.3390/life12060789] [PMID: 35743820]
[53]
Mulholland, B.S.; Forwood, M.R.; Morrison, N.A. Monocyte chemoattractant protein-1 (MCP-1/CCL2) drives activation of bone remodelling and skeletal metastasis. Curr. Osteoporos. Rep., 2019, 17(6), 538-547.
[http://dx.doi.org/10.1007/s11914-019-00545-7] [PMID: 31713180]
[54]
Sell, H.; Dietze-Schroeder, D.; Kaiser, U.; Eckel, J. Monocyte chemotactic protein-1 is a potential player in the negative cross-talk between adipose tissue and skeletal muscle. Endocrinology, 2006, 147(5), 2458-2467.
[http://dx.doi.org/10.1210/en.2005-0969] [PMID: 16439461]
[55]
Samuel, V.T.; Petersen, K.F.; Shulman, G.I. Lipid-induced insulin resistance: Unravelling the mechanism. Lancet, 2010, 375(9733), 2267-2277.
[http://dx.doi.org/10.1016/S0140-6736(10)60408-4] [PMID: 20609972]
[56]
Muoio, D.M.; Newgard, C.B. Obesity-related derangements in metabolic regulation. Annu. Rev. Biochem., 2006, 75(1), 367-401.
[http://dx.doi.org/10.1146/annurev.biochem.75.103004.142512] [PMID: 16756496]
[57]
Noakes, T.D. So what comes first: The obesity or the insulin resistance? And which is more important? Clin. Chem., 2018, 64(1), 7-9.
[http://dx.doi.org/10.1373/clinchem.2017.282962] [PMID: 29295832]
[58]
Aragonès, G.; Ardid-Ruiz, A.; Ibars, M. Suárez, M.; Bladé, C. Modulation of leptin resistance by food compounds. Mol. Nutr. Food Res., 2016, 60(8), 1789-1803.
[http://dx.doi.org/10.1002/mnfr.201500964] [PMID: 26842874]
[59]
Ardid-Ruiz, A.; Harazin, A.; Barna, L.; Walter, F.R.; Bladé, C. Suárez, M.; Deli, M.A.; Aragonès, G. The effects of Vitis vinifera L. phenolic compounds on a blood-brain barrier culture model: Expression of leptin receptors and protection against cytokine-induced damage. J. Ethnopharmacol., 2020, 247, 112253.
[http://dx.doi.org/10.1016/j.jep.2019.112253] [PMID: 31562952]
[60]
Polyzos, S.A.; Kountouras, J.; Mantzoros, C.S. Leptin in nonalcoholic fatty liver disease: A narrative review. Metabolism, 2015, 64(1), 60-78.
[http://dx.doi.org/10.1016/j.metabol.2014.10.012] [PMID: 25456097]
[61]
Hussein, M.A. Anti-obesity, antiatherogenic, anti-diabetic and antioxidant activities of J. montana ethanolic formulation in obese diabetic rats fed high-fat diet. Free Radic. Antioxid., 2011, 1(1), 49-60.
[http://dx.doi.org/10.5530/ax.2011.1.9]
[62]
Razny, U.; Kiec-Wilk, B.; Wator, L.; Polus, A.; Dyduch, G.; Solnica, B.; Malecki, M.; Tomaszewska, R.; Cooke, J.P.; Dembinska-Kiec, A. Increased nitric oxide availability attenuates high fat diet metabolic alterations and gene expression associated with insulin resistance. Cardiovasc. Diabetol., 2011, 10(1), 68-72.
[http://dx.doi.org/10.1186/1475-2840-10-68] [PMID: 21781316]
[63]
Salah, A.; Hussein, A.; Hassan, S.; Hussein, M.A.; Bassiouny, K. Green synthesis of RES-CMCS: A promising modulator of the GLUT-4/Leptin Signaling Pathway in HFD-induced insulin resistance. Biomed. Res. Ther., 2022, 9(7), 5166-5178.
[http://dx.doi.org/10.15419/bmrat.v9i7.753]
[64]
Kelly, G. A review of the sirtuin system, its clinical implications, and the potential role of dietary activators like resveratrol: part 1. Altern. Med. Rev., 2010, 15(3), 245-263.
[PMID: 21155626]
[65]
Schenk, S.; McCurdy, C.E.; Philp, A.; Chen, M.Z.; Holliday, M.J.; Bandyopadhyay, G.K.; Osborn, O.; Baar, K.; Olefsky, J.M. Sirt1 enhances skeletal muscle insulin sensitivity in mice during caloric restriction. J. Clin. Invest., 2011, 121(11), 4281-4288.
[http://dx.doi.org/10.1172/JCI58554] [PMID: 21985785]
[66]
Price, N.L.; Gomes, A.P.; Ling, A.J.Y.; Duarte, F.V.; Martin-Montalvo, A.; North, B.J.; Agarwal, B.; Ye, L.; Ramadori, G.; Teodoro, J.S.; Hubbard, B.P.; Varela, A.T.; Davis, J.G.; Varamini, B.; Hafner, A.; Moaddel, R.; Rolo, A.P.; Coppari, R.; Palmeira, C.M.; de Cabo, R.; Baur, J.A.; Sinclair, D.A. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab., 2012, 15(5), 675-690.
[http://dx.doi.org/10.1016/j.cmet.2012.04.003] [PMID: 22560220]
[67]
Cai, S.; Sun, W.; Fan, Y.; Guo, X.; Xu, G.; Xu, T.; Hou, Y.; Zhao, B.; Feng, X.; Liu, T. Effect of mulberry leaf (Folium Mori) on insulin resistance via IRS-1/PI3K/Glut-4 signalling pathway in type 2 diabetes mellitus rats. Pharm. Biol., 2016, 54(11), 2685-2691.
[http://dx.doi.org/10.1080/13880209.2016.1178779] [PMID: 27158744]
[68]
Wilson, R.D.; Islam, M.S. Effects of white mulberry (Morus alba) leaf tea investigated in a type 2 diabetes model of rats. Acta Pol. Pharm., 2015, 72(1), 153-160.
[PMID: 25850211]
[69]
Lee, J.; Padhye, A.; Sharma, A.; Song, G.; Miao, J.; Mo, Y.Y.; Wang, L.; Kemper, J.K. A pathway involving farnesoid X receptor and small heterodimer partner positively regulates hepatic sirtuin 1 levels via microRNA-34a inhibition. J. Biol. Chem., 2010, 285(17), 12604-12611.
[http://dx.doi.org/10.1074/jbc.M109.094524] [PMID: 20185821]
[70]
Kelly, G.S. A review of the sirtuin system, its clinical implications, and the potential role of dietary activators like resveratrol: Part 2. Altern. Med. Rev., 2010, 15(4), 313-328.
[PMID: 21194247]
[71]
Karunakaran, D.; Richards, L.; Geoffrion, M.; Barrette, D.; Gotfrit, R.J.; Harper, M.E.; Rayner, K.J. Therapeutic inhibition of miR-33 promotes fatty acid oxidation but does not ameliorate metabolic dysfunction in diet-induced obesity. Arterioscler. Thromb. Vasc. Biol., 2015, 35(12), 2536-2543.
[http://dx.doi.org/10.1161/ATVBAHA.115.306404] [PMID: 26427794]
[72]
Xie, Q.; Peng, J.; Guo, Y.; Li, F. MicroRNA-33-5p inhibits cholesterol efflux in vascular endothelial cells by regulating citrate synthase and ATP-binding cassette transporter A1. BMC Cardiovasc. Disord., 2021, 21(1), 433.
[http://dx.doi.org/10.1186/s12872-021-02228-7] [PMID: 34517822]
[73]
Shankar, K.; Zhong, Y.; Kang, P.; Lau, F.; Blackburn, M.L.; Chen, J.R.; Borengasser, S.J.; Ronis, M.J.J.; Badger, T.M. Maternal obesity promotes a proinflammatory signature in rat uterus and blastocyst. Endocrinology, 2011, 152(11), 4158-4170.
[http://dx.doi.org/10.1210/EN.2010-1078] [PMID: 21862610]

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