The Role of Reactive Oxygen Species in the Pathogenesis of Adipocyte Dysfunction in Metabolic Syndrome. Prospects of Pharmacological Correction

Cover Page


Cite item

Full Text

Abstract

It is established that oxidative stress induces insulin resistance of adipocytes, increases secretion leptin, IL-6, TNF-α by adipocytes. Adiponectin secretion by adipocytes is reduced after the action of reactive oxygen species. Metabolic syndrome contributes to oxidative stress in adipose tissue, on the one hand due to the activation of production of reactive oxygen species by adipocyte NADPH-oxidase, and on the other hand by reducing the antioxidant defense adipocytes. It is found that obesity itself can induce oxidative stress. Chronic stress, glucocorticoids, mineralocorticoids, angiotensin-II, TNF-α play an important role in the pathogenesis of oxidative stress of adipocytes. Metformin remains the cure for the treatment of insulin resistance. The positive results in the treatment of metabolic syndrome by losartan were obtained. Antioxidants and flavonoids exhibit a positive impact on the course of the experimental metabolic syndrome.

About the authors

E. S. Prokudina

Cardiology Research Institute, Tomsk National Research Medical Centre, Russian Academy of Sciences

Email: goddess27@mail.ru
ORCID iD: 0000-0002-1991-6516

Младший научный сотрудник лаборатории экспериментальной кардиологии.

Адрес: 634012, Томск, ул. Киевская, д. 111

SPIN-код: 3819-7464

Russian Federation

L. N. Maslov

Cardiology Research Institute, Tomsk National Research Medical Centre, Russian Academy of Sciences

Author for correspondence.
Email: maslov@cardio-tomsk.ru
ORCID iD: 0000-0002-6020-1598

Доктор медицинских наук, профессор, руководитель лаборатории экспериментальной кардиологии. 

Адрес: 634012, Томск, ул. Киевская, д. 111

SPIN-код: 5843-2490


V. V. Ivanov

Siberian State Medical University

Email: ivanovvv1953@gmail.com
ORCID iD: 0000-0001-9348-4945

Кандидат биологических наук, руководитель лаборатории биомоделей.

Адрес: 634050, Томск, Московский тракт, д. 2

SPIN-код: 4961-9959

I. D. Bespalova

Siberian State Medical University

Email: innadave@mail2000.ru
ORCID iD: 0000-0002-1053-4781

Кандидат медицинских наук, заведующая кафедрой социальной работы, социальной и клинической психологии.

Адрес: 634050, Томск, Московский тракт, д. 2.

SPIN-код: 6852-6200

D. S. Pismennyi

Cardiology Research Institute, Tomsk National Research Medical Centre, Russian Academy of Sciences

Email: Cross_117@mail.ru
ORCID iD: 0000-0002-4751-8953

Лаборант-исследователь лаборатории экспериментальной кардиологии.

Адрес: 634012, Томск, ул. Киевская, д. 111.

SPIN-код: 7441-0790

N. S. Voronkov

Cardiology Research Institute, Tomsk National Research Medical Centre, Russian Academy of Sciences

Email: maslov@cardio-tomsk.ru
ORCID iD: 0000-0002-9447-4236

Лаборант-исследователь лаборатории экспериментальной кардиологии.

Адрес: 634012, Томск, ул. Киевская, д. 111. 

SPIN-код: 7862-7013

References

  1. who.int [Internet]. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Geneva: World Health Organization; 1999. 59 p. [cited 2017 Jan 21]. Available from: http://apps.who.int/iris/handle/10665/66040.
  2. Isomaa B, Almgren P, Tuomi T, et al. Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care. 2001;24(4):683−689. doi: 10.2337/diacare.24.4.683.
  3. Aguilar M, Bhuket T, Torres S, et al. Prevalence of the metabolic syndrome in the United States, 2003–2012. JAMA. 2015;313(19):1973−1974. doi: 10.1001/jama.2015.4260.
  4. Block A, Schipf S, Van der Auwera S, et al. Sex- and age-specific associations between major depressive disorder and metabolic syndrome in two general population samples in Germany. Nord J Psychiatry. 2016;70(8):611−620. doi: 10.1080/08039488.2016.1191535.
  5. de Carvalho Vidigal F, Bressan J, Babio N, Salas-Salvadó J. Prevalence of metabolic syndrome in Brazilian adults: a systematic review. BMC Public Health. 2013;13:1198. doi: 10.1186/1471-2458-13-1198.
  6. Deepa M, Farooq S, Datta M, et al. Prevalence of metabolic syndrome using WHO, ATPIII and IDF definitions in Asian Indians: the Chennai Urban Rural Epidemiology Study (CURES-34). Diabetes Metab Res Rev. 2007;23 (2):127−134. doi: 10.1002/dmrr.658.
  7. Metelskaya VA, Shkolnikova MA, Shalnova SA, et al. Prevalence, components, and correlates of metabolic syndrome (MetS) among elderly Muscovites. Arch Gerontol Geriatr. 2012;55(2):231−237. doi: 10.1016/j.archger.2011.09.005.
  8. Reaven GM. Banting Lecture 1988. Role of insulin resistance in human disease. Diabetes. 1988;37(12):1595−1607. doi: 10.2337/diab.37.12.1595.
  9. Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC-δ activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab. 2003;285(2):E295−E302. doi: 10.1152/ajpendo.00044.2003.
  10. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114(12):1752−1761. doi: 10.1172/JCI21625.
  11. Kurata A, Nishizawa H, Kihara S, et al. Blockade of Angiotensin II type-1 receptor reduces oxidative stress in adipose tissue and ameliorates adipocytokine dysregulation. Kidney Int. 2006;70(10):1717−1724. doi: 10.1038/sj.ki.5001810.
  12. Hirata A, Maeda N, Hiuge A, et al. Blockade of mineralocorticoid receptor reverses adipocyte dysfunction and insulin resistance in obese mice. Cardiovasc Res. 2009;84(1):164−172. doi: 10.1093/cvr/cvp191.
  13. Marcus Y, Shefer G, Sasson K, et al. Angiotensin 1−7 as means to prevent the metabolic syndrome: lessons from the fructose-fed rat model. Diabetes. 2013;62(4):1121−1130. doi: 10.2337/db12-0792.
  14. Farina JP, García ME, Alzamendi A, et al. Antioxidant treatment prevents the development of fructose-induced abdominal adipose tissue dysfunction. Clin Sci (Lond). 2013;125(2):87−97. doi: 10.1042/CS20120470.
  15. Wang CH, Wang CC, Huang HC, Wei YH. Mitochondrial dysfunction leads to impairment of insulin sensitivity and adiponectin secretion in adipocytes. FEBS J. 2013;280(4):1039−1050. doi: 10.1111/febs.12096.
  16. Guerra RC, Zuñiga-Muñoz A, Guarner Lans V, et al. Modulation of the activities of catalase, Cu-Zn, Mn superoxide dismutase, and glutathione peroxidase in adipocyte from ovariectomised female rats with metabolic syndrome. Int J Endocrinol. 2014;2014:175080. doi: 10.1155/2014/175080.
  17. Okuno Y, Matsuda M, Kobayashi H, et al. Adipose expression of catalase is regulated via a novel remote PPARγ-responsive region. Biochem Biophys Res Commun. 2008;366(3):698−704. doi: 10.1016/j.bbrc.2007.12.001.
  18. Kobayashi H, Matsuda M, Fukuhara A, et al. Dysregulated glutathione metabolism links to impaired insulin action in adipocytes. Am J Physiol Endocrinol Metab. 2009;296(6):E1326−E1334. doi: 10.1152/ajpendo.90921.2008.
  19. Hatami M, Saidijam M, Yadegarzari R, et al. Peroxisome proliferator-activated receptor-γgene expression and its association with oxidative stress in patients with metabolic syndrome. Chonnam Med J. 2016;52(3):201−206. doi: 10.4068/cmj.2016.52.3.201.
  20. Беспалова И.Д. Воспалительный процесс в патогенезе метаболического синдрома: дис. ... докт. мед. наук. — Томск; ٢٠١٦. [Bespalova ID. Vospalitel’nyi protsess v patogeneze metabolicheskogo sindroma. [dissertation] Tomsk; 2016. (In Russ).] Доступно по: http://www.ssmu.ru/upload/filesarchive/files/Dissertacija_Bespalova_I_D__na_sai__t_file_1_3223.pdf. Ссылка активна на 23.01.2017.
  21. Alberti KG, Zimmet P, Shaw J. Metabolic syndrome ― a new world-wide definition. A consensus statement from the International Diabetes Federation. Diabet Med. 2006;23(5):469−480. doi: 10.1111/j.1464-5491.2006.01858.x.
  22. Model MA, Kukuruga MA, Todd RF. A sensitive flow cytometric method for measuring the oxidative burst. J Immunol Methods. 1997;202(2):105−111. doi: 10.1016/s0022-1759(96)00241-4.
  23. Sun M, Huang X, Yan Y, et al. Rac1 is a possible link between obesity and oxidative stress in Chinese overweight adolescents. Obesity (Silver Spring). 2012;20(11):2233−2240. doi: 10.1038/oby.2012.63.
  24. Karbownik-Lewinska M, Szosland J, Kokoszko-Bilska A, et al. Direct contribution of obesity to oxidative damage to macromolecules. Neuro Endocrinol Lett. 2012;33(4):453−461.
  25. Habib SA, Saad EA, Elsharkawy AA, Attia ZR. Pro-inflammatory adipocytokines, oxidative stress, insulin, Zn and Cu: Interrelations with obesity in Egyptian non-diabetic obese children and adolescents. Adv Med Sci. 2015;60(2):179−185. doi: 10.1016/j.advms.2015.02.002.
  26. Pandey G, Shihabudeen MS, David HP, et al. Association between hyperleptinemia and oxidative stress in obese diabetic subjects. J Diabetes Metab Disord. 2015;14:24. doi: 10.1186/s40200-015-0159-9.
  27. Becer E, Çırakoğlu A. Association of the Ala16Val MnSOD gene polymorphism with plasma leptin levels and oxidative stress biomarkers in obese patients. Gene. 2015;568(1):35−39. doi: 10.1016/j.gene.2015.05.009.
  28. Беспалова И.Д., Калюжин В.В., Рязанцева Н.В., и др. Влияние гиперлептинемии на качество жизни больных гипертонической болезнью с метаболическим синдромом // Артериальная гипертензия. ― 2013. ― Т.19. ― №5 ― С. 428—434. [Bespalova ID, Kalyuzhin VV, Ryazantseva NV, et al. The effect of the hyperleptinemia on the quality of life of hypertensive patients with metabolic syndrome. Arterialnaya gipertenziya. 2013;19(5):428−434. (In Russ).]
  29. Kim SH, Chung JH, Song SW, et al. Relationship between deep subcutaneous abdominal adipose tissue and metabolic syndrome: a case control study. Diabetol Metab Syndr. 2016;8:10. doi: 10.1186/s13098-016-0127-7.
  30. Velarde GP, Sherazi S, Kraemer DF, et al. Clinical and biochemical markers of cardiovascular structure and function in women with the metabolic syndrome. Am J Cardiol. 2015;116(11):1705−1710. doi: 10.1016/j.amjcard.2015.09.010.
  31. Lee SW, Jo HH, Kim MR, et al. Association between osteocalcin and metabolic syndrome in postmenopausal women. Arch Gynecol Obstet. 2015;292(3):673−681. doi: 10.1007/s00404-015-3656-7.
  32. Yoon CY, Kim YL, Han SH, et al. Hypoadiponectinemia and the presence of metabolic syndrome in patients with chronic kidney disease: results from the KNOW-CKD study. Diabetol Metab Syndr. 2016;8:75. doi: 10.1186/s13098-016-0191-z.
  33. Mlinar B, Marc J. New insights into adipose tissue dysfunction in insulin resistance. Clin Chem Lab Med. 2011;49(12):1925−1935. doi: 10.1515/CCLM.2011.697.
  34. Murdolo G, Bartolini D, Tortoioli C, et al. Lipokines and oxysterols: novel adipose-derived lipid hormones linking adipose dysfunction and insulin resistance. Free Radic Biol Med. 2013;65:811−820. doi: 10.1016/j.freeradbiomed.2013.08.007.
  35. Nolan JJ, O’Gorman DJ. Pathophysiology of the metabolic syndrome. In: Beck-Nielsen H, editor. The metabolic syndrome: pharmacology and clinical aspects. Wien: Springer-Verlag; 2013. p. 17−42. doi: 10.1007/978-3-7091-1331-8_3.
  36. Gonzalez-Jimenez E, Schmidt-Riovalle J, Sinausía L, et al. Predictive value of ceruloplasmin for metabolic syndrome in adolescents. Biofactors. 2016;42(2):163−170. doi: 10.1002/biof.1258.
  37. Christiana UI, Casimir AE, Nicholas AA, et al. Plasma levels of inflammatory cytokines in adult Nigerians with the metabolic syndrome. Niger Med J. 2016;57(1):64−68. doi: 10.4103/0300-1652.180569.
  38. Soares AF, Guichardant M, Cozzone D, et al. Effects of oxidative stress on adiponectin secretion and lactate production in 3T3-L1 adipocytes. Free Radic Biol Med. 2005;38(7):882−889. doi: 10.1016/j.freeradbiomed.2004.12.010.
  39. Chen B, Lam KS, Wang Y, et al. Hypoxia dysregulates the production of adiponectin and plasminogen activator inhibitor-1 independent of reactive oxygen species in adipocytes. Biochem Biophys Res Commun. 2006;341(2):549−556. doi: 10.1016/j.bbrc.2006.01.004.
  40. Monickaraj F, Aravind S, Nandhini P, et al. Accelerated fat cell aging links oxidative stress and insulin resistance in adipocytes. J Biosci. 2013;38(1):113−122. doi: 10.1007/s12038-012-9289-0.
  41. Fukushima M, Okamoto Y, Katsumata H, et al. Growth hormone ameliorates adipose dysfunction during oxidative stress and inflammation and improves glucose tolerance in obese mice. Horm Metab Res. 2014;46(9):656−662. doi: 10.1055/s-0034-1381998.
  42. Pan Y, Qiao QY, Pan LH, et al. Losartan reduces insulin resistance by inhibiting oxidative stress and enhancing insulin signaling transduction. Exp Clin Endocrinol Diabetes. 2015;123(3):170−177. doi: 10.1055/s-0034-1395658.
  43. Kowalska K, Olejnik A. Cranberries (Oxycoccus quadripetalus) inhibit pro-inflammatory cytokine and chemokine expression in 3T3-L1 adipocytes. Food Chem. 2016;196:1137−1143. doi: 10.1016/j.foodchem.2015.10.069.
  44. Rudich A, Kozlovsky N, Potashnik R, Bashan N. Oxidant stress reduces insulin responsiveness in 3T3-L1 adipocytes. Am J Physiol. 1997;272(5 Pt 1):E935−E940.
  45. Rudich A, Tirosh A, Potashnik R, et al. Prolonged oxidative stress impairs insulin-induced GLUT4 translocation in 3T3-L1 adipocytes. Diabetes. 1998;47(10):1562−1569. doi: 10.2337/diabetes.47.10.1562.
  46. Tirosh A, Potashnik R, Bashan N, Rudich A. Oxidative stress disrupts insulin-induced cellular redistribution of insulin receptor substrate-1 and phosphatidylinositol 3-kinase in 3T3-L1 adipocytes. A putative cellular mechanism for impaired protein kinase B activation and GLUT4 translocation. J Biol Chem. 1999;274(15):10595−10602. doi: 10.1074/jbc.274.15.10595.
  47. Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC-δ activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab. 2003;285(2):E295−E302. doi: 10.1152/ajpendo.00044.2003.
  48. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature. 2006;440(7086):944−948. doi: 10.1038/nature04634.
  49. Guo H, Ling W, Wang Q, et al. Cyanidin 3-glucoside protects 3T3-L1 adipocytes against H2O2- or TNF-α-induced insulin resistance by inhibiting c-Jun NH2-terminal kinase activation. Biochem Pharmacol. 2008;75(6):1393−1401. doi: 10.1016/j.bcp.2007.11.016.
  50. Matsuda M, Shimomura I. Increased oxidative stress in obesity: implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obes Res Clin Pract. 2013;7(5):e330−e341. doi: 10.1016/j.orcp.2013.05.004.
  51. Kameji H, Mochizuki K, Miyoshi N, Goda T. β-Carotene accumulation in 3T3-L1 adipocytes inhibits the elevation of reactive oxygen species and the suppression of genes related to insulin sensitivity induced by tumor necrosis factor-α. Nutrition. 2010;26(11−12):1151−1156. doi: 10.1016/j.nut.2009.09.006.
  52. Yen GC, Chen YC, Chang WT, Hsu CL. Effects of polyphenolic compounds on tumor necrosis factor-α (TNF-α)-induced changes of adipokines and oxidative stress in 3T3-L1 adipocytes. J Agric Food Chem. 2011;59(2):546−551. doi: 10.1021/jf1036992.
  53. Eriksson JW. Metabolic stress in insulin’s target cells leads to ROS accumulation ― a hypothetical common pathway causing insulin resistance. FEBS Lett. 2007;581(19):3734−3742. doi: 10.1016/j.febslet.2007.06.044.
  54. Kazakou P, Kyriazopoulou V, Michalaki M, et al. Activated hypothalamic pituitary adrenal axis in patients with metabolic syndrome. Horm Metab Res. 2012;44(11):839−844. doi: 10.1055/s-0032-1311632.
  55. Nagasawa K, Matsuura N, Takeshita Y, et al. Attenuation of cold stress-induced exacerbation of cardiac and adipose tissue pathology and metabolic disorders in a rat model of metabolic syndrome by the glucocorticoid receptor antagonist RU486. Nutr Diabetes. 2016;6:e207. doi: 10.1038/nutd.2016.14.
  56. Bailey CJ. Treatment with metformin. In: Beck-Nielsen H, editor. The metabolic syndrome: pharmacology and clinical aspects. Wien: Springer-Verlag; 2013. p. 99−116. doi: 10.1007/978-3-7091-1331-8_8.
  57. Carillon J, Knabe L, Montalban A, et al. Curative diet supplementation with a melon superoxide dismutase reduces adipose tissue in obese hamsters by improving insulin sensitivity. Mol Nutr Food Res. 2014;58(4):842−850. doi: 10.1002/mnfr.201300466.
  58. Gao M, Zhao Z, Lv P, et al. Quantitative combination of natural anti-oxidants prevents metabolic syndrome by reducing oxidative stress. Redox Biol. 2015;6:206−217. doi: 10.1016/j.redox.2015.06.013.
  59. Vazquez Prieto MA, Bettaieb A, Rodriguez Lanzi C, et al. Catechin and quercetin attenuate adipose inflammation in fructose-fed rats and 3T3-L1adipocytes. Mol Nutr Food Res. 2015;59(4):622−633. doi: 10.1002/mnfr.201400631.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2017 "Paediatrician" Publishers LLC



This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies