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Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

General Research Article

Effects of Quercetin and Coenzyme Q10 on Biochemical, Molecular, and Morphological Parameters of Skeletal Muscle in Trained Diabetic Rats

Author(s): Amal M. Youssef , Dalia A. Mohamed, Samia Hussein*, Doaa M. Abdullah and Shaimaa A. Abdelrahman

Volume 15, Issue 1, 2022

Published on: 21 May, 2021

Article ID: e210521193500 Pages: 13

DOI: 10.2174/1874467214666210521170339

Price: $65

Abstract

Background: Diabetes mellitus (DM) affects the musculoskeletal system through its metabolic perturbations. Exercise modulates blood sugar levels and increases the body’s sensitivity to insulin in patients with DM.

Objective: This study aimed to investigate the potential effects of combined quercetin and coenzyme Q10 (CoQ10) supplements with or without exercise on the histological, biochemical and molecular structures of diabetic rat’s skeletal muscle

Methods: A total of 64 adult male albino rats were divided into six groups: control, trained nondiabetic, non-trained diabetic, diabetic rats treated with combined CoQ10 and quercetin, diabetic rats with treadmill training, and diabetic rats treated with treadmill training and CoQ10 and quercetin. Blood and skeletal muscle samples were obtained from all groups for routine histological examination and biochemical determination of cytokine levels and protein activities. Quantitative real-time polymerase chain reaction (qRT-PCR) and morphometric analysis of PAS and Bax expressions were also performed.

Results: Biochemical analysis revealed improvement in all studied parameters with combined Co- Q10 and quercetin than exercise training alone. Combined treatment and exercise showed significant improvement in all parameters especially interleukin 6 and malondialdehyde. Fibronectin type III domain-containing protein 5 (FNDC5) expression and irisin levels increased in all trained groups but combined treatment with exercise significantly increased their levels than exercise alone. Histological analysis revealed improvement after exercise or combined treatment; however, when exercise was combined with CoQ10 and quercetin, marked improvement was observed.

Conclusion: the combination of CoQ10 and quercetin could be promising in preserving musculoskeletal function in patients with DM concomitantly with physical exercise.

Keywords: Diabetes mellitus, skeletal muscle, quercetin, coenzyme Q10, exercise, irisin.

Graphical Abstract

[1]
Hameed, I.; Masoodi, S.R.; Mir, S.A.; Nabi, M.; Ghazanfar, K.; Ganai, B.A. Type 2 diabetes mellitus: From a metabolic disorder to an inflammatory condition. World J. Diabetes, 2015, 6(4), 598-612.
[http://dx.doi.org/10.4239/wjd.v6.i4.598] [PMID: 25987957]
[2]
Davis, M.J.; D’Alessio, D.A.; Fradkin, J.; Kernan, W.N.; Mathieu, C.; Mingrone, G.; Rossing, P.; Tsapas, A.; Wexler, D.J.; Buse, J.B. Management of hyperglycemia in type 2 diabetes,2018.Aconsensus report by the American Diabetes Association (ADA) and the European Association for the study of Diabetes (EASD). Diabetologica, 2018, 61, 2461-2498.
[http://dx.doi.org/10.1007/s00125-018-4729-5]
[3]
Aydeniz, A.; Gursoy, S.; Guney, E. Which musculoskeletal complications are most frequently seen in type 2 diabetes mellitus? J. Int. Med. Res., 2008, 36(3), 505-511.
[http://dx.doi.org/10.1177/147323000803600315] [PMID: 18534132]
[4]
Mueller, M.J. Musculoskeletal Impairments Are Often Unrecognized and Underappreciated Complications From Diabetes. Phys. Ther., 2016, 96(12), 1861-1864.
[http://dx.doi.org/10.2522/ptj.20160326] [PMID: 27909254]
[5]
Majjad, A; Errahali, Y; Toufik, H; Djossou, JH; Ghassem, MA; Kasouati, J; ElMaghraoui, A Musculoskeletal disorders in patients with diabetes mellitus: Across-sectional study Int. J. of Rheumatology, 2018, 2018, 1-6.DOI.org/
[http://dx.doi.org/10.1155/2018/3839872]
[6]
Wali, J.A.; Thomas, H.E.; Sutherland, A.P. Linking obesity with type 2 diabetes: the role of T-bet. Diabetes Metab. Syndr. Obes., 2014, 7(7), 331-340.
[http://dx.doi.org/10.2147/DMSO.S51432] [PMID: 25092994]
[7]
Collins, K.H.; Herzog, W.; MacDonald, G.Z.; Reimer, R.A.; Rios, J.L.; Smith, I.C.; Zernicke, R.F.; Hart, D.A. Obesity, Metabolic Syndrome, and Musculoskeletal Disease: Common Inflammatory Pathways Suggest a Central Role for Loss of Muscle Integrity. Front. Physiol., 2018, 9(112), 112.
[http://dx.doi.org/10.3389/fphys.2018.00112] [PMID: 29527173]
[8]
Touyz, R.M.; Schiffrin, E.L. Reactive oxygen species in vascular biology: implications in hypertension. Histochem. Cell Biol., 2004, 122(4), 339-352.
[http://dx.doi.org/10.1007/s00418-004-0696-7] [PMID: 15338229]
[9]
Savini, I.; Catani, M.V.; Evangelista, D.; Gasperi, V.; Avigliano, L. Obesity-associated oxidative stress: strategies finalized to improve redox state. Int. J. Mol. Sci., 2013, 14(5), 10497-10538.
[http://dx.doi.org/10.3390/ijms140510497] [PMID: 23698776]
[10]
Corpeleijn, E.; Saris, W.H.; Blaak, E.E. Metabolic flexibility in the development of insulin resistance and type 2 diabetes: effects of lifestyle. Obes. Rev., 2009, 10(2), 178-193.
[http://dx.doi.org/10.1111/j.1467-789X.2008.00544.x] [PMID: 19207879]
[11]
Ferraro, E.; Giammarioli, A.M.; Chiandotto, S.; Spoletini, I.; Rosano, G. Exercise-induced skeletal muscle remodeling and metabolic adaptation: redox signaling and role of autophagy. Antioxid. Redox Signal., 2014, 21(1), 154-176.
[http://dx.doi.org/10.1089/ars.2013.5773] [PMID: 24450966]
[12]
Kheiripour, N.; Karimi, J.; Khodadadi, I.; Tavilani, H.; Taghi Goodarzi, M.; Hashemnia, M. Hepatoprotective Effects of Silymarin on Liver Injury via Irisin Upregulation and Oxidative Stress Reduction in Rats with Type 2 Diabetes. Iran. J. Med. Sci., 2019, 44(2), 108-117.
[PMID: 30936597]
[13]
Mahajan, R.D.; Patra, S.K. Irisin, a novel myokine responsible for exercise induced browning of white adipose tissue. Indian J. Clin. Biochem., 2013, 28(1), 102-103.
[http://dx.doi.org/10.1007/s12291-012-0255-2] [PMID: 24381432]
[14]
Roca-Rivada, A.; Castelao, C.; Senin, L.L.; Landrove, M.O.; Baltar, J.; Belén Crujeiras, A.; Seoane, L.M.; Casanueva, F.F.; Pardo, M. FNDC5/irisin is not only a myokine but also an adipokine. PLoS One, 2013, 8(4), e60563.
[http://dx.doi.org/10.1371/journal.pone.0060563] [PMID: 23593248]
[15]
Petrovic, N.; Walden, T.B.; Shabalina, I.G.; Timmons, J.A.; Cannon, B.; Nedergaard, J. Chronic peroxisome proliferator-activated receptor gamma (PPARgamma) activation of epididymally derived white adipocyte cultures reveals a population of thermogenically competent, UCP1-containing adipocytes molecularly distinct from classic brown adipocytes. J. Biol. Chem., 2010, 285(10), 7153-7164.
[http://dx.doi.org/10.1074/jbc.M109.053942] [PMID: 20028987]
[16]
Moreno-Navarrete, J.M.; Ortega, F.; Serrano, M.; Guerra, E.; Pardo, G.; Tinahones, F.; Ricart, W.; Fernández-Real, J.M. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J. Clin. Endocrinol. Metab., 2013, 98(4), E769-E778.
[http://dx.doi.org/10.1210/jc.2012-2749] [PMID: 23436919]
[17]
Tang, L.; Tong, Y.; Zhang, F.; Chen, G.; Zhang, Y.C.; Jobin, J.; Tong, N. The association of circulating irisin with metabolic risk factors in Chinese adults: a cross-sectional community-based study. BMC Endocr. Disord., 2019, 19(1), 147.
[http://dx.doi.org/10.1186/s12902-019-0479-8] [PMID: 31881940]
[18]
Skrovankova, S.; Sumczynski, D.; Mlcek, J.; Jurikova, T.; Sochor, J. Bioactive compound and antioxidant activity in different types of berries. Int. J. Mol. Sci., 2015, 16(10), 24673-24706.
[http://dx.doi.org/10.3390/ijms161024673] [PMID: 26501271]
[19]
Coskun, O.; Kanter, M.; Korkmaz, A.; Oter, S. Quercetin, a flavonoid antioxidant, prevents and protects streptozotocin-induced oxidative stress and beta-cell damage in rat pancreas. Pharmacol. Res., 2005, 51(2), 117-123.
[http://dx.doi.org/10.1016/j.phrs.2004.06.002] [PMID: 15629256]
[20]
Shi, G.J.; Li, Y.; Cao, Q.H.; Wu, H.X.; Tang, X.Y.; Gao, X.H.; Yu, J.Q.; Chen, Z.; Yang, Y. in vitro and in vivo evidence that quercetin protects against diabetes and its complications: A systematic review of the literature. Biomed. Pharmacother., 2019, 109, 1085-1099.
[http://dx.doi.org/10.1016/j.biopha.2018.10.130] [PMID: 30551359]
[21]
Hershey, A.D.; Powers, S.W.; Vockell, A.L.; Lecates, S.L.; Ellinor, P.L.; Segers, A.; Burdine, D.; Manning, P.; Kabbouche, M.A. Coenzyme Q10 deficiency and response to supplementation in pediatric and adolescent migraine. Headache, 2007, 47(1), 73-80.
[http://dx.doi.org/10.1111/j.1526-4610.2007.00652.x] [PMID: 17355497]
[22]
Mancuso, M.; Orsucci, D.; Calsolaro, V.; Choub, A.; Siciliano, G. Coenzyme Q10 and neurological diseases. Pharmaceuticals (Basel), 2009, 2(3), 134-149.
[http://dx.doi.org/10.3390/ph203134] [PMID: 27713230]
[23]
Mizuno, K.; Tanaka, M.; Nozaki, S.; Mizuma, H.; Ataka, S.; Tahara, T.; Sugino, T.; Shirai, T.; Kajimoto, Y.; Kuratsune, H.; Kajimoto, O.; Watanabe, Y. Antifatigue effects of coenzyme Q10 during physical fatigue. Nutrition, 2008, 24(4), 293-299.
[http://dx.doi.org/10.1016/j.nut.2007.12.007] [PMID: 18272335]
[24]
Peng, J.; Li, Q.; Li, K.; Zhu, L.; Lin, X.; Lin, X.; Shen, Q.; Li, G.; Xie, X. Quercetin improves glucose and lipid metabolism of diabetic rats: involvement of Akt signaling and SIRT1. J. Diabetes Res., 2017, 2017, 3417306.
[http://dx.doi.org/10.1155/2017/3417306] [PMID: 29379801]
[25]
Motawi, T.K.; Darwish, H.A.; Hamed, M.A.; El-Rigal, N.S.; Aboul Naser, A.F. Coenzyme Q10 and niacin mitigate streptozotocin- induced diabetic encephalopathy in a rat model. Metab. Brain Dis., 2017, 32(5), 1519-1527.
[http://dx.doi.org/10.1007/s11011-017-0037-x] [PMID: 28560538]
[26]
Yang, D.K.; Kang, H.S. Anti-diabetic effect of cotreatment with quercetin and resveratrol in streptozotocin-induced diabetic rats. Biomol. Ther. (Seoul), 2018, 26(2), 130-138.
[http://dx.doi.org/10.4062/biomolther.2017.254] [PMID: 29462848]
[27]
Annadurai, T.; Muralidharan, A.R.; Joseph, T.; Hsu, M.J.; Thomas, P.A.; Geraldine, P. Antihyperglycemic and antioxidant effects of a flavanone, naringenin, in streptozotocin-nicotinamide-induced experimental diabetic rats. J. Physiol. Biochem., 2012, 68(3), 307-318.
[http://dx.doi.org/10.1007/s13105-011-0142-y] [PMID: 22234849]
[28]
Cho, D.K.; Choi, D.H.; Cho, J.Y. Effect of treadmill exercise on skeletal muscle autophagy in rats with obesity induced by a high- fat diet. J. Exerc. Nutrition Biochem., 2017, 21(3), 26-34.
[http://dx.doi.org/10.20463/jenb.2017.0013] [PMID: 29036763]
[29]
Choi, D.H.; Kwon, I.S.; Koo, J.H.; Jang, Y.C.; Kang, E.B.; Byun, J.E.; Um, H.S.; Park, H.S.; Yeom, D.C.; Cho, I.H.; Cho, J.Y. The effect of treadmill exercise on inflammatory responses in rat model of streptozotocin-induced experimental dementia of Alzheimer’s type. J. Exerc. Nutrition Biochem., 2014, 18(2), 225-233.
[http://dx.doi.org/10.5717/jenb.2014.18.2.225] [PMID: 25566459]
[30]
Kara, A.; Unal, D.; Simsek, N.; Yucel, A.; Yucel, N.; Selli, J. Ultra-structural changes and apoptotic activity in cerebellum of post- menopausal-diabetic rats: a histochemical and ultra-structural study. Gynecol. Endocrinol., 2014, 30(3), 226-231.
[http://dx.doi.org/10.3109/09513590.2013.864270] [PMID: 24397360]
[31]
Suvarna, K.; Layton, C.; Bancroft, J. Bancroft;s Theory and Practice of Histological Techniques, 8th ed.; Churchill Livingstone of El Sevier, Philadelphia, Ch. 10 (the hematoxylin and eosin)., 2018, p. 672.
[32]
Ramos-Vara, J.A.; Kiupel, M.; Baszler, T.; Bliven, L.; Brodersen, B.; Chelack, B.; Czub, S.; Del Piero, F.; Dial, S.; Ehrhart, E.J.; Graham, T.; Manning, L.; Paulsen, D.; Valli, V.E.; West, K. Suggested guidelines for immunohistochemical techniques in veterinary diagnostic laboratories. J. Vet. Diagn. Invest., 2008, 20(4), 393-413.
[http://dx.doi.org/10.1177/104063870802000401] [PMID: 18599844]
[33]
Ran, X.; Wang, C.; Wang, H.; Zhao, T.; Tong, N.; Song, B.; Bu, H.; Luo, Y.; Tian, H.; Li, X. Muscle infarction involving muscles of abdominal and thoracic walls in diabetes. Diabet. Med., 2005, 22(12), 1757-1760. [PMID 16401324].
[http://dx.doi.org/10.1111/j.1464-5491.2005.01728.x] [PMID: 16401324]
[34]
Torres, S.H.; De Sanctis, J.B.; de L Briceño, M.; Hernández, N.; Finol, H.J. Inflammation and nitric oxide production in skeletal muscle of type 2 diabetic patients. J. Endocrinol., 2004, 181(3), 419-427. [PMID 15171690].
[http://dx.doi.org/10.1677/joe.0.1810419] [PMID: 15171690]
[35]
Elsy, B.; Khan, A.A.; Maheshwari, V. Effect of d-α-tocopherol on skeletal muscle regeneration in crushed injury of diabetic rats. Eur. J. Anat., 2017, 21(4), 293-304.
[36]
Zima, T.; Fialová, L.; Mestek, O.; Janebová, M.; Crkovská, J.; Malbohan, I.; Stípek, S.; Mikulíková, L.; Popov, P. Oxidative stress, metabolism of ethanol and alcohol-related diseases. J. Biomed. Sci., 2001, 8(1), 59-70.
[http://dx.doi.org/10.1007/BF02255972] [PMID: 11173977]
[37]
Yang, F.; Yu, X.; Li, T.; Wu, J.; Zhao, Y.; Liu, J.; Sun, A.; Dong, S.; Wu, J.; Zhong, X.; Xu, C.; Lu, F.; Zhang, W. Exogenous H2S regulates endoplasmic reticulum-mitochondria cross-talk to inhibit apoptotic pathways in STZ-induced type I diabetes. Am. J. Physiol. Endocrinol. Metab., 2017, 312(3), E190-E203.
[http://dx.doi.org/10.1152/ajpendo.00196.2016] [PMID: 27998959]
[38]
Jiang, P.; Zhang, D.; Qiu, H.; Yi, X.; Zhang, Y.; Cao, Y.; Zhao, B.; Xia, Z.; Wang, C. Tiron ameliorates high glucose-induced cardiac myocyte apoptosis by PKCδ-dependent inhibition of osteopontin. Clin. Exp. Pharmacol. Physiol., 2017, 44(7), 760-770.
[http://dx.doi.org/10.1111/1440-1681.12762] [PMID: 28394420]
[39]
Ghiasi, R.; Ghadiri Soufi, F.; Mohaddes, G.; Alihemmati, A.; Somi, M.H.; Ebrahimi, H.; Mirzaie Bavil, F.; Alipour, M.R. Influance of regular swimming on serum levels of CRP, IL-6, TNF-α in high-fat diet-induced type 2 diabetic rats Gen Physiol Biophys, 2016, 34(4), 469-476.
[40]
Kim, J.S.; Lee, Y.H.; Kim, J.C.; Ko, Y.H.; Yoon, C.S.; Yi, H.K. Effect of exercise training of different intensities on anti-inflammatory reaction in streptozotocin-induced diabetic rats. Biol. Sport, 2014, 31(1), 73-79.
[http://dx.doi.org/10.5604/20831862.1093775] [PMID: 25187675]
[41]
Talebi-Garakani, E.; Safarzade, A. Resistance training decreases serum inflammatory markers in diabetic rats. Endocrine, 2013, 43(3), 564-570.
[http://dx.doi.org/10.1007/s12020-012-9786-9] [PMID: 22948775]
[42]
Belotto, M.F.; Magdalon, J.; Rodrigues, H.G.; Vinolo, M.A.; Curi, R.; Pithon-Curi, T.C.; Hatanaka, E. Moderate exercise improves leucocyte function and decreases inflammation in diabetes. Clin. Exp. Immunol., 2010, 162(2), 237-243.
[http://dx.doi.org/10.1111/j.1365-2249.2010.04240.x] [PMID: 20846161]
[43]
Frati, G.; Schirone, L.; Chimenti, I.; Yee, D.; Biondi-Zoccai, G.; Volpe, M.; Sciarretta, S. An overview of the inflammatory signalling mechanisms in the myocardium underlying the development of diabetic cardiomyopathy. Cardiovasc. Res., 2017, 113(4), 378-388.
[http://dx.doi.org/10.1093/cvr/cvx011] [PMID: 28395009]
[44]
Barbieri, E.; Sestili, P. Reactive oxygen species in skeletal muscle signaling. J. Signal Transduct., 2012, 2012, 982794.
[http://dx.doi.org/10.1155/2012/982794] [PMID: 22175016]
[45]
Della Gatta, P.A.; Garnham, A.P.; Peake, J.M.; Cameron-Smith, D. Effect of exercise training on skeletal muscle cytokine expression in the elderly. Brain Behav. Immun., 2014, 39, 80-86.
[http://dx.doi.org/10.1016/j.bbi.2014.01.006] [PMID: 24434040]
[46]
Campi-Azevedo, A.C.; Cleto, L.S.; Silva, R.S.; Sousa-Franco, Jd.; Magalhães, J.C.; Penaforte, C.L.; Castro Pinto, K.M.; Rocha-Vieira, E. Divergent cytokine response following maximum progressive swimming in hot water. Cell Biochem. Funct., 2011, 29(7), 610-616.
[http://dx.doi.org/10.1002/cbf.1795] [PMID: 21887695]
[47]
Rauscher, F.M.; Sanders, R.A.; Watkins, J.B., III Effects of coenzyme Q10 treatment on antioxidant pathways in normal and streptozotocin-induced diabetic rats. J. Biochem. Mol. Toxicol., 2001, 15(1), 41-46.
[http://dx.doi.org/10.1002/1099-0461(2001)15:1<41::AID-JBT5>3.0.CO;2-Z] [PMID: 11170314]
[48]
Sena, C.M.; Nunes, E.; Gomes, A.; Santos, M.S.; Proença, T.; Martins, M.I.; Seiça, R.M. Supplementation of coenzyme Q10 and alpha-tocopherol lowers glycated hemoglobin level and lipid peroxidation in pancreas of diabetic rats. Nutr. Res., 2008, 28(2), 113-121.
[http://dx.doi.org/10.1016/j.nutres.2007.12.005] [PMID: 19083397]
[49]
Sourris, K.C.; Harcourt, B.E.; Tang, P.H.; Morley, A.L.; Huynh, K.; Penfold, S.A.; Coughlan, M.T.; Cooper, M.E.; Nguyen, T.V.; Ritchie, R.H.; Forbes, J.M. Ubiquinone (coenzyme Q10) prevents renal mitochondrial dysfunction in an experimental model of type 2 diabetes. Free Radic. Biol. Med., 2012, 52(3), 716-723.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.11.017] [PMID: 22172526]
[50]
Sarian, M.N.; Ahmed, Q.U.; Mat So'ad, S.Z.; Alhassan, A.M.; Murugesu, S.; Perumal, V.; Syed Mohamad, S.N.A.; Khatib, A.; Latip, J. Antioxidant and Antidiabetic Effects of Flavonoids: A Structure-Activity Relationship Based Study. Biomed Res Int. , 2017, 2017
[http://dx.doi.org/10.1155/2017/8386065] [PMID: 29318154]
[51]
Mahmoud, M.F.; Hassan, N.A.; El Bassossy, H.M.; Fahmy, A. Quercetin protects against diabetes-induced exaggerated vasoconstriction in rats: effect on low grade inflammation. PloS one, 2013, 8(5), e63784.
[52]
Caponi, P.W.; Lehnen, A.M.; Pinto, G.H.; Borges, J.; Markoski, M.; Machado, U.F.; Schaan, B.D. Aerobic exercise training induces metabolic benefits in rats with metabolic syndrome independent of dietary changes. Clinics (São Paulo), 2013, 68(7), 1010-1017.
[http://dx.doi.org/10.6061/clinics/2013(07)20] [PMID: 23917668]
[53]
Xiao, J.; Li, J.; Xu, T.; Lv, D.; Shen, B.; Song, Y.; Xu, J. Pregnancy-induced physiological hypertrophy protects against cardiac ischemia-reperfusion injury. Int. J. Clin. Exp. Pathol., 2013, 7(1), 229-235. a
[PMID: 24427343]
[54]
Xiao, J.; Xu, T.; Li, J.; Lv, D.; Chen, P.; Zhou, Q.; Xu, J. Exercise-induced physiological hypertrophy initiates activation of cardiac progenitor cells. Int. J. Clin. Exp. Pathol., 2014, 7(2), 663-669. b
[PMID: 24551287]
[55]
Gordon, L.A.; Morrison, E.Y.; McGrowder, D.A.; Young, R.; Fraser, Y.T.; Zamora, E.M.; Alexander-Lindo, R.L.; Irving, R.R. Effect of exercise therapy on lipid profile and oxidative stress indicators in patients with type 2 diabetes. BMC Complement. Altern. Med., 2008, 8, 21.
[http://dx.doi.org/10.1186/1472-6882-8-21] [PMID: 18477407]
[56]
Stewart, L.K.; Soileau, J.L.; Ribnicky, D.; Wang, Z.Q.; Raskin, I.; Poulev, A.; Majewski, M.; Cefalu, W.T.; Gettys, T.W. Quercetin transiently increases energy expenditure but persistently decreases circulating markers of inflammation in C57BL/6J mice fed a high- fat diet. Metabolism, 2008, 57(7)(Suppl. 1), S39-S46.
[http://dx.doi.org/10.1016/j.metabol.2008.03.003] [PMID: 18555853]
[57]
Krskova, K.; Eckertova, M.; Kukan, M.; Kuba, D.; Kebis, A.; Olszanecki, R.; Suski, M.; Gajdosechova, L.; Zorad, S. Aerobic training lasting for 10 weeks elevates the adipose tissue FABP4, Giα, and adiponectin expression associated by a reduced protein oxidation. Endocr. Regul., 2012, 46(3), 137-146.
[http://dx.doi.org/10.4149/endo_2012_03_137] [PMID: 22808905]
[58]
Madeddu, C.; Maccio, A.; Mantovani, G. Multitargeted treatment of cancer cachexia. Crit. Rev. Oncog., 2012, 17(3), 305-314.
[http://dx.doi.org/10.1615/CritRevOncog.v17.i3.80] [PMID: 22831161]
[59]
Ramadan, B.K.; Schaalan, M.F.; Tolba, A.M. Hypoglycemic and pancreatic protective effects of Portulaca oleracea extract in alloxan induced diabetic rats. BMC Complement. Altern. Med., 2017, 17(1), 37.
[http://dx.doi.org/10.1186/s12906-016-1530-1] [PMID: 28077129]
[60]
Bonnard, C.; Durand, A.; Peyrol, S.; Chanseaume, E.; Chauvin, M.A.; Morio, B.; Vidal, H.; Rieusset, J. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest., 2008, 118(2), 789-800.
[http://dx.doi.org/10.1172/JCI32601] [PMID: 18188455]
[61]
Andersen, H.; Schmitz, O.; Nielsen, S. Decreased isometric muscle strength after acute hyperglycaemia in Type 1 diabetic patients. Diabet. Med., 2005, 22(10), 1401-1407.
[http://dx.doi.org/10.1111/j.1464-5491.2005.01649.x] [PMID: 16176203]
[62]
Krause, M.P.; Riddell, M.C.; Hawke, T.J. Effects of type 1 diabetes mellitus on skeletal muscle: clinical observations and physiological mechanisms. Pediatr. Diabetes, 2011, 12(4 Pt 1), 345-364.
[http://dx.doi.org/10.1111/j.1399-5448.2010.00699.x] [PMID: 20860561]
[63]
van Loon, L.J. Use of intramuscular triacylglycerol as a substrate source during exercise in humans. J. Appl. Physiol. (1985), 2004, 97(4), 1170-1187.
[http://dx.doi.org/10.1152/japplphysiol.00368.2004] [PMID: 15358749]
[64]
Ergen, N.; Kurdak, H.; Erdogan, S.; Mete, U.O.; Kaya, M.; Dikmen, N.; Doğan, A.; Kurdak, S.S. The effects of aerobic exercise on skeletal muscle metabolism, morphology and in situ endurance in diabetic rats. J. Sports Sci. Med., 2005, 4(4), 472-481.
[PMID: 24501562]
[65]
Egan, B.; Zierath, J.R. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab., 2013, 17(2), 162-184.
[http://dx.doi.org/10.1016/j.cmet.2012.12.012] [PMID: 23395166]
[66]
Ranjbari, A.; Azarbayjani, M.A.; Yusof, A.; Mokhtar, A.; Akbarzadeh, S.; Ibrahim, M.Y.; Tarverdizadeh, B.; Farzadinia, P.; Hajiaghaee, R.; Dehghan, F. In vivo and in vitro evaluation of the effects of Urtica dioica and swimming activity on diabetic factors and pancreatic beta cells. BMC Complement. Altern. Med., 2016, 16:101.
[http://dx.doi.org/10.1186/s12906-016-1064-6]
[67]
Lee, M.; Son, M.; Ryu, E.; Shin, Y.S.; Kim, J.G.; Kang, B.W.; Cho, H.; Kang, H. Quercetin-induced apoptosis prevents EBV infection. Oncotarget, 2015, 2; 6(14), 12603-24.
[68]
Delavar, R.; Heidarianpour, A. The Effect of Aerobic Exercise Training on Plasma Apelin Levels and Pain Threshold in T1DM Rats. Iran. Red Crescent Med. J., 2016, 18(9), e31737.
[http://dx.doi.org/10.5812/ircmj.31737] [PMID: 28144460]
[69]
Delbin, M.A.; Davel, A.P.; Couto, G.K.; de Araújo, G.G.; Rossoni, L.V.; Antunes, E.; Zanesco, A. Interaction between advanced glycation end products formation and vascular responses in femoral and coronary arteries from exercised diabetic rats. PLoS One, 2012, 7(12), e53318.
[http://dx.doi.org/10.1371/journal.pone.0053318] [PMID: 23285277]
[70]
Morales, A.I.; Vicente-Sánchez, C.; Jerkic, M.; Santiago, J.M.; Sánchez-González, P.D.; Pérez-Barriocanal, F.; López-Novoa, J.M. Effect of quercetin on metallothionein, nitric oxide synthases and cyclooxygenase-2 expression on experimental chronic cadmium nephrotoxicity in rats. Toxicol. Appl. Pharmacol., 2006, 210(1-2), 128-135.
[http://dx.doi.org/10.1016/j.taap.2005.09.006] [PMID: 16226777]
[71]
Gülçin, I.; Elmastas, M.; Aboul-Enein, H.Y. Determination of antioxidant and radical scavenging activity of basil (Ocimum basilicum) assayed by different methodologies. Phytother. Res., 2007, 21, 354-361.
[http://dx.doi.org/10.1002/ptr.2069] [PMID: 17221941]
[72]
Bardy, G.; Virsolvy, A.; Quignard, J.F.; Ravier, M.A.; Bertrand, G.; Dalle, S.; Cros, G.; Magous, R.; Richard, S.; Oiry, C. Quercetin induces insulin secretion by direct activation of L-type calcium channels in pancreatic beta cells. Br. J. Pharmacol., 2013, 169(5), 1102-1113.
[http://dx.doi.org/10.1111/bph.12194] [PMID: 23530660]
[73]
Hussein, J. Therapeutic role of Coenzyme Q10 in brain injury during experimental Diabetes. J. Appl. Pharm. Sci., 2013, 3(6), 213-217.
[74]
De Matteis, R.; Lucertini, F.; Guescini, M.; Polidori, E.; Zeppa, S.; Stocchi, V.; Cinti, S.; Cuppini, R. Exercise as a new physiological stimulus for brown adipose tissue activity. Nutr. Metab. Cardiovasc. Dis., 2013, 23(6), 582-590.
[http://dx.doi.org/10.1016/j.numecd.2012.01.013] [PMID: 22633794]
[75]
Boström, P.; Wu, J.; Jedrychowski, M.P.; Korde, A.; Ye, L.; Lo, J.C.; Rasbach, K.A.; Boström, E.A.; Choi, J.H.; Long, J.Z.; Kajimura, S.; Zingaretti, M.C.; Vind, B.F.; Tu, H.; Cinti, S.; Højlund, K.; Gygi, S.P.; Spiegelman, B.M. A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature, 2012, 481(7382), 463-468.
[http://dx.doi.org/10.1038/nature10777] [PMID: 22237023]
[76]
Huh, J.Y.; Mougios, V.; Kabasakalis, A.; Fatouros, I.; Siopi, A.; Douroudos, I.I.; Filippaios, A.; Panagiotou, G.; Park, K.H.; Mantzoros, C.S. Exercise-induced irisin secretion is independent of age or fitness level and increased irisin may directly modulate muscle metabolism through AMPK activation. J. Clin. Endocrinol. Metab., 2014, 99(11), E2154-E2161.
[http://dx.doi.org/10.1210/jc.2014-1437] [PMID: 25119310]
[77]
Pedersen, B.K.; Febbraio, M.A. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol., 2012, 8(8), 457-465.
[http://dx.doi.org/10.1038/nrendo.2012.49] [PMID: 22473333]
[78]
Kim, H.J.; Song, W. Resistance training increases fibroblast growth factor-21 and irisin levels in the skeletal muscle of Zucker diabetic fatty rats. J. Exerc. Nutrition Biochem., 2017, 21(3), 50-54.
[http://dx.doi.org/10.20463/jenb.2017.0008] [PMID: 29036766]
[79]
Pekkala, S.; Wiklund, P.K.; Hulmi, J.J.; Ahtiainen, J.P.; Horttanainen, M.; Pöllänen, E.; Mäkelä, K.A.; Kainulainen, H.; Häkkinen, K.; Nyman, K.; Alén, M.; Herzig, K.H.; Cheng, S. Are skeletal muscle FNDC5 gene expression and irisin release regulated by exercise and related to health? J. Physiol., 2013, 591(21), 5393-5400.
[http://dx.doi.org/10.1113/jphysiol.2013.263707] [PMID: 24000180]

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