Protective Effect of Tertiary Butylhydroquinone against Obesity-induced Skeletal Muscle Pathology in Post-weaning High Fat Diet Fed Rats


Cite item

Full Text

Abstract

Background:Obesity deleteriously affects skeletal muscle functionality starting from infancy to adulthood, leading to dysfunctional skeletal muscle.

Objectives:This study, therefore, evaluated the protective action of tert-butylhydroquinone (tBHQ) against obesity-induced skeletal muscle pathology in high-fat diet (HFD) fed rats.

Methods:Twenty post-weaning male albino rats were randomized into four groups of five rats each as: Group 1 (control), Group 2 (HFD), Group 3 (orlistat) and Group 4 (tBHQ). Group one received rat pellets for 12 weeks, while groups 2 to 4 received HFD for 12 weeks. At the end of week 8, obesity was confirmed with Lee Obesity Index and body mass index values of ≥ 303 and ≥ 0.68 gcm2, respectively. Group 3 was given oral administration of orlistat (10 mg/kg, once daily), while group 4 was given oral administration of tBHQ (25 mg/kg, once daily). Administration of orlistat and tBHQ commenced from week 9 to the end of the experiment.

Results:Chronic exposure of post-weaning rats to HFD led to their development of the metabolic syndrome phenotypes in adulthood, characterized by obesity, hyperglycemia, dyslipidaemia, hyperinsulinaemia, insulin resistance as well as induction of oxidative stress and alteration of skeletal muscle markers, which were mitigated following supplementation with orlistat and tBHQ.

Conclusion:The study showed the anti-obesity potentials of tBHQ and its protective action against HFD obesity-induced skeletal muscular pathology.

About the authors

Le Zhang

Department of Pediatrics, Hanzhong Central Hospital

Author for correspondence.
Email: info@benthamscience.net

References

  1. Kim, I.; Kim, H.R.; Kim, J.H.; Om, A.S. Beneficial effects of Allium sativum L. stem extract on lipid metabolism and antioxidant status in obese mice fed a high-fat diet. J. Sci. Food Agric., 2013, 93(11), 2749-2757. doi: 10.1002/jsfa.6094 PMID: 23606129
  2. Sour, S.; Belarbi, M.; Sari, N.; Benammar, C.H.; Baghdad, C.H.; Visioli, F. Argan oil reduces, in rats, the high fat diet-induced metabolic effects of obesity. Nutr. Metab. Cardiovasc. Dis., 2015, 25(4), 382-387. doi: 10.1016/j.numecd.2015.01.001 PMID: 25694362
  3. WHO. Obesity 2021. Available from: https://www.who.int/news-room/facts-in-pictures/detail/6-facts-on-obesity
  4. Swinburn, B.A.; Sacks, G.; Hall, K.D.; McPherson, K.; Finegood, D.T.; Moodie, M.L.; Gortmaker, S.L. The global obesity pandemic: Shaped by global drivers and local environments. Lancet, 2011, 378(9793), 804-814. doi: 10.1016/S0140-6736(11)60813-1 PMID: 21872749
  5. Maithilikarpagaselvi, N.; Sridhar, M.G.; Swaminathan, R.P.; Sripradha, R. Preventive effect of curcumin on inflammation, oxidative stress and insulin resistance in high-fat fed obese rats. J. Complement. Integr. Med., 2016, 13(2), 137-143. doi: 10.1515/jcim-2015-0070 PMID: 26845728
  6. Lalanza, J.F.; Caimari, A.; del Bas, J.M.; Torregrosa, D.; Cigarroa, I.; Pallàs, M.; Capdevila, L.; Arola, L.; Escorihuela, R.M. Effects of a post-weaning cafeteria diet in young rats: Metabolic syndrome, reduced activity and low anxiety-like behaviour. PLoS One, 2014, 9(1), e85049. doi: 10.1371/journal.pone.0085049 PMID: 24482678
  7. Bhadoria, A.S.; Sahoo, K.; Sahoo, B.; Choudhury, A.K.; Sofi, N.Y.; Kumar, R. Childhood obesity: Causes and consequences. J. Family Med. Prim. Care, 2015, 4(2), 187-192. doi: 10.4103/2249-4863.154628 PMID: 25949965
  8. Andrich, D.E.; Melbouci, L.; Ou, Y.; Auclair, N.; Mercier, J.; Grenier, J.C.; Lira, F.S.; Barreiro, L.B.; Danialou, G.; Comtois, A.S.; Lavoie, J.C.; St-Pierre, D.H. A short-term high-fat diet alters glutathione levels and IL-6 gene expression in oxidative skeletal muscles of young rats. Front. Physiol., 2019, 10, 372. doi: 10.3389/fphys.2019.00372 PMID: 31024337
  9. Konopelniuk, V.V.; Goloborodko, I.I.; Ishchuk, T.V.; Synelnyk, T.B.; Ostapchenko, L.I.; Spivak, M.Y.; Bubnov, R.V. Efficacy of Fenugreek-based bionanocomposite on renal dysfunction and endogenous intoxication in high-calorie diet-induced obesity rat model—comparative study. EPMA J., 2017, 8(4), 377-390. doi: 10.1007/s13167-017-0098-2 PMID: 29209440
  10. Hu, Z.; Wang, H.; Lee, I.H.; Modi, S.; Wang, X.; Du, J.; Mitch, W.E. PTEN inhibition improves muscle regeneration in mice fed a high-fat diet. Diabetes, 2010, 59(6), 1312-1320. doi: 10.2337/db09-1155 PMID: 20200318
  11. Heo, J.W.; Yoo, S.Z.; No, M.H.; Park, D.H.; Kang, J.H.; Kim, T.W.; Kim, C.J.; Seo, D.Y.; Han, J.; Yoon, J.H.; Jung, S.J.; Kwak, H.B. Exercise training attenuates obesity-induced skeletal muscle remodelling and mitochondria-mediated apoptosis in the skeletal muscle. Int. J. Environ. Res. Public Health, 2018, 15(10), 2301. doi: 10.3390/ijerph15102301 PMID: 30347719
  12. Jimoh, A.; Tanko, Y.; Ahmed, A.; Mohammed, A.; Ayo, J.O. Resveratrol prevents high-fat diet-induced obesity and oxidative stress in rabbits. Pathophysiology, 2018, 25(4), 359-364. doi: 10.1016/j.pathophys.2018.07.003 PMID: 30017743
  13. Nakanishi, T.; Tsujii, M.; Asano, T.; Iino, T.; Sudo, A. Protective effect of edaravone against oxidative stress in C2C12 myoblast and impairment of skeletal muscle regeneration exposed to ischemic injury in Ob/ob mice. Front. Physiol., 2020, 10, 1596. doi: 10.3389/fphys.2019.01596 PMID: 32009986
  14. Timmers, S.; de Vogel-van den Bosch, J.; Towler, M.C.; Schaart, G.; Moonen-Kornips, E.; Mensink, R.P.; Hesselink, M.K.; Hardie, D.G.; Schrauwen, P. Prevention of high-fat diet-induced muscular lipid accumulation in rats by α lipoic acid is not mediated by AMPK activation. J. Lipid Res., 2010, 51(2), 352-359. doi: 10.1194/jlr.M000992 PMID: 19690335
  15. Ramírez, N.M.; Toledo, R.C.L.; Moreira, M.E.C.; Martino, H.S.D.; Benjamin, L.A.; de Queiroz, J.H.; Ribeiro, A.Q.; Ribeiro, S.M.R. Anti-obesity effects of tea from Mangifera indica L. leaves of the Ubá variety in high-fat diet-induced obese rats. Biomed. Pharmacother., 2017, 91, 938-945. doi: 10.1016/j.biopha.2017.05.015 PMID: 28514832
  16. Cho, Y.R.; Lee, J.A.; Kim, Y.Y.; Kang, J.S.; Lee, J.H.; Ahn, E.K. Anti-obesity effects of Clausena excavata in high-fat diet-induced obese mice. Biomed. Pharmacother., 2018, 99, 253-260. doi: 10.1016/j.biopha.2018.01.069 PMID: 29334669
  17. Jang, W.S.; Choung, S.Y. Antiobesity effects of the ethanol extract of laminaria japonica areshoung in high-fat-diet-induced obese rat. Evid. Based Complement. Alternat. Med., 2013, 2013, 492807.
  18. Zhang, Y.; Fang , Liu. F. Bi, X.; Wang, S.; Wu, X.; Jiang, F. The antioxidant compound tert-butylhydroquinone activates Akt in myocardium, suppresses apoptosis and ameliorates pressure overload-induced cardiac dysfunction. Sci. Rep., 2015, 5(1), 13005. doi: 10.1038/srep13005 PMID: 26260024
  19. Nishizono, S.; Hayami, T.; Ikeda, I.; Imaizumi, K. Protection against the diabetogenic effect of feeding tert-butylhydroquinone to rats prior to the administration of streptozotocin. Biosci. Biotechnol. Biochem., 2000, 64(6), 1153-1158. doi: 10.1271/bbb.64.1153 PMID: 10923784
  20. Jin, W.; Ni, H.; Dai, Y.; Wang, H.; Lu, T.; Wu, J.; Jiang, J.; Liang, W. Effects of tert-butylhydroquinone on intestinal inflammatory response and apoptosis following traumatic brain injury in mice. In: Mediators Inflamm; , 2010; 2010, p. 502564. doi: 10.1155/2010/502564
  21. Li, S.; Li, J.; Shen, C.; Zhang, X.; Sun, S.; Cho, M.; Sun, C.; Song, Z. tert-Butylhydroquinone (tBHQ) protects hepatocytes against lipotoxicity via inducing autophagy independently of Nrf2 activation. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2014, 1841(1), 22-33. doi: 10.1016/j.bbalip.2013.09.004 PMID: 24055888
  22. Sargazi, S.; Galavi, H.; Zarei, S. Evaluation of attenuative effect of tert-butylhydroquinone against diazinon-induced oxidative stress on hematological indices in male Wistar rats. Biomed. Rep., 2018, 8(6), 565-570. doi: 10.3892/br.2018.1090 PMID: 29774145
  23. Triwitono, P.; Marsono, Y.; Murdiati, A.; Marseno, D.W. Physiological effects of mung bean starch rs-3 on the obesity index and adipose cell profile of sprague-dawley rats. Pak. J. Nutr., 2016, 15(10), 913-920. doi: 10.3923/pjn.2016.913.920
  24. Zeng, X.P.; Li, X.J.; Zhang, Q.Y.; Liu, Q.W.; Li, L.; Xiong, Y.; He, C.X.; Wang, Y.F.; Ye, Q.F. Tert-Butylhydroquinone protects liver against ischemia/reperfusion injury in rats through Nrf2-activating antioxidative activity. Transplant. Proc., 2017, 49(2), 366-372. doi: 10.1016/j.transproceed.2016.12.008 PMID: 28219600
  25. Zaitone, S.A.; Essawy, S. Addition of a low dose of rimonabant to orlistat therapy decreases weight gain and reduces adiposity in dietary obese rats. Clin. Exp. Pharmacol. Physiol., 2012, 39(6), 551-559. doi: 10.1111/j.1440-1681.2012.05717.x PMID: 22524969
  26. Ji, W.; Zhao, M.; Wang, M.; Yan, W.; Liu, Y.; Ren, S.; Lu, J.; Wang, B.; Chen, L. Effects of canagliflozin on weight loss in high-fat diet-induced obese mice. PLoS One, 2017, 12(6), e0179960. doi: 10.1371/journal.pone.0179960 PMID: 28665967
  27. Amin, K.A.; Nagy, M.A. Effect of Carnitine and herbal mixture extract on obesity induced by high fat diet in rats. Diabetol. Metab. Syndr., 2009, 1(1), 17. doi: 10.1186/1758-5996-1-17 PMID: 19835614
  28. Kim, J.H.; Hahm, D.H.; Yang, D.C.; Kim, J.H.; Lee, H.J.; Shim, I. Effect of crude saponin of Korean red ginseng on high-fat diet-induced obesity in the rat. J. Pharmacol. Sci., 2005, 97(1), 124-131. doi: 10.1254/jphs.FP0040184 PMID: 15655288
  29. Cavalcanti, M.H.; Roseira, J.P.S.; Leandro, E.S.; Arruda, S.F. Effect of a freeze-dried coffee solution in a high-fat diet-induced obesity model in rats: Impact on inflammatory response, lipid profile, and gut microbiota. PLoS One, 2022, 17(1), e0262270. doi: 10.1371/journal.pone.0262270 PMID: 35081143
  30. Friedewald, W.T.; Levy, R.I.; Fredrickson, D.S. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin. Chem., 1972, 18(6), 499-502. doi: 10.1093/clinchem/18.6.499 PMID: 4337382
  31. Castro, M.C.; Francini, F.; Schinella, G.; Caldiz, C.I.; Zubiría, M.G.; Gagliardino, J.J.; Massa, M.L. Apocynin administration prevents the changes induced by a fructose-rich diet on rat liver metabolism and the antioxidant system. Clin. Sci., 2012, 123(12), 681-692. doi: 10.1042/CS20110665 PMID: 22738259
  32. Buege, J.A.; Aust, S.D. Microsomal lipid peroxidation. In: Methods in enzymolgy; Flesicher, S.; Packer, L., Eds.; Academic Press: New York, NY, 1978; pp. 302-310.
  33. Fridovich, I.; Mc-Cord, J.M. Superoxide dismutase an enzymatic function for erythrocuperin. J. Biol. Chem., 1969, 244, 6045-6055.
  34. Doğan, P.; Tanrikulu, G.; Soyuer, Ü.; Köse, K. Oxidative enzymes of polymorphonuclear leucocytes and plasma fibrinogen, ceruloplasmin, and copper levels in Behcet’s disease. Clin. Biochem., 1994, 27(5), 413-418. doi: 10.1016/0009-9120(94)90046-9 PMID: 7867220
  35. Sinha, A.K. Colorimetric assay of catalase. Anal. Biochem., 1972, 47(2), 389-394. doi: 10.1016/0003-2697(72)90132-7 PMID: 4556490
  36. Tietz, N.W. Clinical Guide to Laboratory Tests, 3rd ed; WB Saunders Company: Philadelphia, 1995, pp. 518-519.
  37. Cheng, H.S.; Ton, S.H.; Phang, S.C.W.; Tan, J.B.L.; Abdul Kadir, K. Increased susceptibility of post-weaning rats on high-fat diet to metabolic syndrome. J. Adv. Res., 2017, 8(6), 743-752. doi: 10.1016/j.jare.2017.10.002 PMID: 29062573
  38. Bais, S.; Singh, S.G.; Sharma, R. Anti-obesity and Hypolipidemic Activity of Moringa oleifera Leaves against High Fat Diet-Induced Obesity in Rats. Advances in Biology, 2014.
  39. Saravanan, G.; Ponmurugan, P.; Deepa, M.A.; Senthilkumar, B. Anti-obesity action of gingerol: effect on lipid profile, insulin, leptin, amylase and lipase in male obese rats induced by a high-fat diet. J. Sci. Food Agric., 2014, 94(14), 2972-2977. doi: 10.1002/jsfa.6642 PMID: 24615565
  40. Wu, D.; Gao, B.; Li, M.; Yao, L.; Wang, S.; Chen, M.; Li, H.; Ma, C.; Ji, A.; Li, Y. Hydrogen sulfide mitigates kidney injury in high fat diet induced obese mice. Oxid. Med. Cell. Longev., 2016, 2016, 1-12. doi: 10.1155/2016/2715718 PMID: 27413418
  41. Nadeem, S.; Dhore, P.; Quazi, M.; Pawar, S.; Raj, N. Lagenaria siceraria fruit extract ameliorate fat amassment and serum TNF–in high–fat diet–induced obese rats. Asian Pac. J. Trop. Med., 2012, 5(9), 698-702. doi: 10.1016/S1995-7645(12)60109-6 PMID: 22805720
  42. Boqué, N.; Campión, J.; de la Iglesia, R.; de la Garza, A.L.; Milagro, F.I.; San Román, B.; Bañuelos, Ó.; Martínez, J.A. Screening of polyphenolic plant extracts for anti-obesity properties in Wistar rats. J. Sci. Food Agric., 2013, 93(5), 1226-1232. doi: 10.1002/jsfa.5884 PMID: 23080265
  43. Rufino, A.T.; Costa, V.M.; Carvalho, F.; Fernandes, E. Flavonoids as antiobesity agents: A review. Med. Res. Rev., 2020, 41(1), 556-585. PMID: 33084093
  44. Vasudevan, D.M.; Sreekumari, S.; Vaidyanathan, K. Textbook of Biochemistry for Medical Students, 7th ed; Jaypee Brothers Medical Publishers Ltd, 2013, p. 305.
  45. Lee, H.S.; Jeon, Y.E.; Jung, J.I.; Kim, S.M.; Hong, S.H.; Lee, J.; Hwang, J.S.; Hwang, M.O.; Kwon, K.; Kim, E.J. Anti-obesity effect of Cydonia oblonga Miller extract in high-fat diet-induced obese C57BL/6 mice. J. Funct. Foods, 2022, 89, 104945. doi: 10.1016/j.jff.2022.104945
  46. Amitani, M.; Asakawa, A.; Amitani, H.; Inui, A. The role of leptin in the control of insulin-glucose axis. Front. Neurosci., 2013, 7, 51. doi: 10.3389/fnins.2013.00051 PMID: 23579596
  47. Considine, R.V.; Sinha, M.K.; Heiman, M.L.; Kriauciunas, A.; Stephens, T.W.; Nyce, M.R.; Ohannesian, J.P.; Marco, C.C.; McKee, L.J.; Bauer, T.L.; Caro, J.F. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N. Engl. J. Med., 1996, 334(5), 292-295. doi: 10.1056/NEJM199602013340503 PMID: 8532024
  48. Mopuri, R.; Ganjayi, M.; Banavathy, K.S.; Parim, B.N.; Meriga, B. Evaluation of anti-obesity activities of ethanolic extract of Terminalia paniculata bark on high fat diet-induced obese rats. BMC Complement. Altern. Med., 2015, 15(1), 76. doi: 10.1186/s12906-015-0598-3 PMID: 25887331
  49. Yamauchi, T.; Kamon, J.; Waki, H.; Terauchi, Y.; Kubota, N.; Hara, K.; Mori, Y.; Ide, T.; Murakami, K.; Tsuboyama-Kasaoka, N.; Ezaki, O.; Akanuma, Y.; Gavrilova, O.; Vinson, C.; Reitman, M.L.; Kagechika, H.; Shudo, K.; Yoda, M.; Nakano, Y.; Tobe, K.; Nagai, R.; Kimura, S.; Tomita, M.; Froguel, P.; Kadowaki, T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat. Med., 2001, 7(8), 941-946. doi: 10.1038/90984 PMID: 11479627
  50. Sung, Y.Y.; Yoon, T.; Kim, S.J.; Yang, W.K.; Kim, H.K. Anti-obesity activity of Allium fistulosum L. extract by down-regulation of the expression of lipogenic genes in high-fat diet-induced obese mice. Mol. Med. Rep., 2011, 4(3), 431-435. PMID: 21468588
  51. Lei, F.; Zhang, X.N.; Wang, W.; Xing, D.M.; Xie, W.D.; Su, H.; Du, L.J. Evidence of anti-obesity effects of the pomegranate leaf extract in high-fat diet induced obese mice. Int. J. Obes., 2007, 31(6), 1023-1029. doi: 10.1038/sj.ijo.0803502 PMID: 17299386
  52. de la Garza, A.; Milagro, F.; Boque, N.; Campión, J.; Martínez, J. Natural inhibitors of pancreatic lipase as new players in obesity treatment. Planta Med., 2011, 77(8), 773-785. doi: 10.1055/s-0030-1270924 PMID: 21412692
  53. Skowron, M.; Zalejska-Fiolka, J.; Błaszczyk, U.; Chwalińska, E.; Owczarek, A.; Birkner, E. Antioxidant enzyme activities in rabbits under oxidative stress induced by high fat diet. J. Vet. Res., 2018, 62(2), 199-205. doi: 10.2478/jvetres-2018-0019 PMID: 30364903
  54. Brancaccio, P.; Lippi, G.; Maffulli, N. Biochemical markers of muscular damage. cclm, 2010, 48(6), 757-767. doi: 10.1515/CCLM.2010.179 PMID: 20518645
  55. Akuru, U.B.; Tebekeme, O. Lipidemic properties of sorghum vulgare leaf sheath on oxidative markers and heart function enzymes of dyslipidemic wistar-albino rats. Biochem. Anal. Biochem., 2017, 6, 343.
  56. Huang, W.; Liu, J.; Zhao, J.; Wang, B.; Liu, B.; Xie, M. Yiqi Yangyin and Huatan Quyu granule can improve skeletal muscle energy metabolism in a type 2 diabetic rat model by promoting the AMPK/SIRT/PGC-1α signalling pathway. J. Tradit. Chin. Med. Sci., 2018, 5(2), 128-138. doi: 10.1016/j.jtcms.2018.03.004
  57. Huang, Q.; Ma, S.; Tominaga, T.; Suzuki, K.; Liu, C. An 8-Week, low carbohydrate, high fat, ketogenic diet enhanced exhaustive exercise capacity in mice part 2: Effect on fatigue recovery, post-exercise biomarkers and anti-oxidation capacity. Nutrients, 2018, 10(10), 1339. doi: 10.3390/nu10101339 PMID: 30241310
  58. Chikezie, C.M.; Ojiako, O.A.; Emejulu, A.A.; Chikezie, P.C. Serum lactate dehydrogenase activity and visceral organs and body weights of diabetic rats administered single and combinatorial herbal formulations. Pharmacogn. Commun., 2018, 8(1), 37-42. doi: 10.5530/pc.2018.1.7
  59. Olorunnisola, O.S.; Fadahunsi, O.S.; Adegbola, P.I.; Ajilore, B.S.; Ajayi, F.A.; Olaniyan, L.W.B. Phyllanthus amarus attenuated derangement in renal-cardiac function, redox status, lipid profile and reduced TNF-α, interleukins-2, 6 and 8 in high salt diet fed rats. Heliyon, 2021, 7(10), e08106. doi: 10.1016/j.heliyon.2021.e08106 PMID: 34660924
  60. Shin, K.A.; Park, K.D.; Ahn, J.; Park, Y.; Kim, Y.J. Comparison of changes in biochemical markers for skeletal muscles, hepatic metabolism, and renal function after three types of long-distance running. Medicine, 2016, 95(20), e3657. doi: 10.1097/MD.0000000000003657 PMID: 27196469
  61. Gujjala, S.; Putakala, M.; Nukala, S.; Bangeppagari, M.; Rajendran, R.; Desireddy, S. Modulatory effects of Caralluma fimbriata extract against high-fat diet induced abnormalities in carbohydrate metabolism in Wistar rats. Biomed. Pharmacother., 2017, 92, 1062-1072. doi: 10.1016/j.biopha.2017.06.016 PMID: 28618651
  62. FAO/WHO. Evaluation of certain food additives and contaminants. Forty-ninth report of the Joint FAO/WHO Expert Committee on Food Additives. World Health Organ. Tech. Rep. Ser., 1999, 884, i-viii, 1-96. PMID: 10079756

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers