Resveratrol Preserves Mitochondrial Function, Stimulates Mitochondrial Biogenesis, and Attenuates Oxidative Stress in Regulatory T Cells of Mice Fed a High-Fat Diet

Journal of Food Science

Volumn 79, Issue 9, 2014, Pages H1823-H1831

  Wang, Bin ^a   Sun, Jin ^a   Ma, Yuhua ^a   Wu, Guirong ^a   Tian, Yingjie ^a   Shi, Yonghui ^a   Le, Guowei ^a  

^a JIANGNAN UNIVERSITY   (China)

Author keywords

High fat diet; Mitochondria; Oxidative stress; Regulatory T cells; Resveratrol

Indexed keywords

MUS; VITACEAE;

ANTIOXIDANT; REACTIVE OXYGEN METABOLITE; RESVERATROL; STILBENE DERIVATIVE;

ADVERSE EFFECTS; ANIMAL; APOPTOSIS; C57BL MOUSE; DRUG EFFECTS; DRUG SCREENING; IMMUNOLOGY; LIPID DIET; MALE; METABOLIC DISEASES; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MOUSE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; REGULATORY T LYMPHOCYTE;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; DIET, HIGH-FAT; DRUG EVALUATION, PRECLINICAL; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; METABOLIC DISEASES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; STILBENES; T-LYMPHOCYTES, REGULATORY;

EID: 84921927792     PISSN: 00221147     EISSN: 17503841     Source Type: Journal    
DOI: 10.1111/1750-3841.12555     Document Type: Article

References (53)

1. Almeida A, Allen KL, Bates TE, Clark JB. 1995. Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. J Neurochem 65(4):1698-703.
2. Ballal K, Wilson CR, Harmancey R, Taegtmeyer H. 2010. Obesogenic high fat western diet induces oxidative stress and apoptosis in rat heart. Mol Cell Biochem 344(1-2):221-30.
3. Banham AH. 2006. Cell-surface IL-7 receptor expression facilitates the purification of FOXP3(+) regulatory T cells. Trends Immunol 27(12):541-4.
4. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, Sinclair DA. 2006. Resveratrol improves health and survival of mice on high-calorie diet. Nature 444(7117):337-42.
5. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, Bateman AC, Clough GF, Poston L, Hanson MA, McConnell JM, Byrne CD. 2009. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50(6):1796-808.
6. Bujanda L, Hijona E, Larzabal M, Beraza M, Aldazabal P, Garcia-Urkia N, Sarasqueta C, Cosme A, Irastorza B, González A, Arenas JI Jr. 2008. Resveratrol inhibits nonalcoholic fatty liver disease in rats. BMC Gastroenterol 8:40.
7. Cenesiz S, Yarim GF, Karabulut AB, Ara C. 2007. Changing of antioxidant enzyme activity on the biliary obstructed rats treated with resveratrol. Dtsch Tierarztl Wochenschr 114(9):345-8.
8. Chen LL, Zhang HH, Zheng J, Hu X, Kong W, Hu D, Wang SX, Zhang P. 2011. Resveratrol attenuates high-fat diet-induced insulin resistance by influencing skeletal muscle lipid transport and subsarcolemmal mitochondrial β-oxidation. Metabolism 60(11):1598-609.
9. Cheng AS, Cheng YH, Chiou CH, Chang TL. 2012. Resveratrol upregulates Nrf2 expression to attenuate methylglyoxal-induced insulin resistance in Hep G2 cells. J Agric Food Chem 60(36):9180-7.
10. Cui J, Le GW, Yang RL, Shi YH. 2009. Lipoic acid attenuates high fat diet-induced chronic oxidative stress and immunosuppression in mice jejunum: A microarray analysis. Cell Immunol 260(1):44-50.
11. Cui J, Xiao Y, Shi YH, Wang B, Le GW. 2012. Lipoic acid attenuates high-fat-diet-induced oxidative stress and B-cell-related immune depression. Nutrition 28(3):275-80.
12. Das N, Sikder K, Bhattacharjee S, Majumdar SB, Ghosh S, Majumdar S, Dey S. 2013. Quercetin alleviates inflammation after short-term treatment in high-fat-fed mice. Food Funct 4(6):889-98.
13. Frankel EN, Kanner J, German JB, Parks E, Kinsella JE. 1993. Inhibition of oxidation of human low-density lipoprotein by phenolic substances in red wine. Lancet 341(8843):454-7.
14. Gehm BD, McAndrews JM, Chien PY, Jameson JL. 1997. Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Natl Acad Sci USA 94(25):14138-43.
15. Gomez-Zorita S, Fernandez-Quintela A, Macarulla MT, Aguirre L, Hijona E, Bujanda L, Milagro F, Martínez JA, Portillo MP. 2012. Resveratrol attenuates steatosis in obese Zucker rats by decreasing fatty acid availability and reducing oxidative stress. Br J Nutr 107(2):202-10.
16. Green DR, Reed JC. 1998. Mitochondria and apoptosis. Science 281(5381):1309-12.
17. Gri G, Piconese S, Frossi B, Manfroi V, Merluzzi S, Tripodo C, Viola A, Odom S, Rivera J, Colombo MP, Pucillo CE. 2008. CD4+CD25 +regulatory T cells suppress mast cell degranulation and allergic responses through OX40-OX40L interaction. Immunity 29(5):771-81.
18. Harikumar KB, Aggarwal BB. 2008. Resveratrol: a multitargeted agent for age-associated chronic diseases. Cell Cycle 7(8):1020-35.
19. Harper ME, Dent R, Monemdjou S, Bezaire V, Van Wyck L, Wells G, Kavaslar G N, Gauthier A, Tesson F, McPherson R. 2002. Decreased mitochondrial proton leak and reduced expression of uncoupling protein 3 in skeletal muscle of obese diet-resistant women. Diabetes 51(8):2459-66.
20. Hildeman DA. 2004. Regulation of T-cell apoptosis by reactive oxygen species. Free Radic Biol Med 36(12):1496-504.
21. Hori S, Nomura T, Sakaguchi S. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299(5609):1057-61.
22. Hsu YT, Wolter KG, Youle RJ. 1997. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc Natl Acad Sci USA 94(8):3668-72.
23. Ikeyama S, Kokkonen G, Shack S, Wang XT, Holbrook NJ. 2002. Loss in oxidative stress tolerance with aging linked to reduced extracellular signal-regulated kinase and Akt kinase activities. FASEB J 16(1):114-6.
24. Jaburek M, Miyamoto S, Di Mascio P, Garlid KD, Jezek P. 2004. Hydroperoxy fatty acid cycling mediated by mitochondrial uncoupling protein UCP2. J Biol Chem 279(51):53097-102.
25. Jaffar Z, Ferrini ME, Girtsman TA, Roberts K. 2009. Antigen-specific Treg regulate Th17-mediated lung neutrophilic inflammation, B-cell recruitment and polymeric IgA and IgM levels in the airways. Eur J Immunol 39(12):3307-14.
26. Karaouzene N, Merzouk H, Aribi M, Merzouk SA, Berrouiguet AY, Tessier C, Narce M. 2011. Effects of the association of aging and obesity on lipids, lipoproteins and oxidative stress biomarkers: a comparison of older with young men. Nutr Metab Cardiovasc Dis 21(10):792-9.
27. Karbowski M, Youle RJ. 2003. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ 10(8):870-80.
28. Kensler TW, Wakabayashi N, Biswal S. 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 47:89-116.
29. Kim S, Jin Y, Choi Y, Park T. 2011. Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice. Biochem Pharmacol 81(11):1343-51.
30. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. 2006. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127(6):1109-22.
31. Lee KY, Koh SH, Noh MY, Park KW, Lee YJ, Kim SH. 2007. Glycogen synthase kinase-3beta activity plays very important roles in determining the fate of oxidative stress-inflicted neuronal cells. Brain Res 1129(1):89-99.
32. Li LX, Skorpen F, Egeberg K, Jorgensen IH, Grill V. 2002. Induction of uncoupling protein 2 mRNA in beta-cells is stimulated by oxidation of fatty acids but not by nutrient oversupply. Endocrinology 143(4):1371-7.
33. Lu KT, Ko MC, Chen BY, Huang JC, Hsieh CW, Lee MC, Chiou RY, Wung BS, Peng CH, Yang YL. 2008. Neuroprotective effects of resveratrol on MPTP-induced neuron loss mediated by free radical scavenging. J Agric Food Chem 56(16):6910-3.
34. Maloy KJ, Powrie F. 2001. Regulatory T cells in the control of immune pathology. Nat Immunol 2(9):816-22.
35. Martinez-Abundis E, Correa F, Pavon N, Zazueta C. 2009. Bax distribution into mitochondrial detergent-resistant microdomains is related to ceramide and cholesterol content in postischemic hearts. FEBS J 276(19):5579-88.
36. Meiler F, Zumkehr J, Klunker S, Ruckert B, Akdis CA, Akdis M. 2008. In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J Exp Med 205(12):2887-98.
37. Nishiumi S, Bessyo H, Kubo M, Aoki Y, Tanaka A, Yoshida K, Ashida H. 2010. Green and black tea suppress hyperglycemia and insulin resistance by retaining the expression of glucose transporter 4 in muscle of high-fat diet-fed C57BL/6J mice. J Agric Food Chem 58(24):12916-23.
38. Nonaka M, Pawankar R, Fukumoto A, Yagi T. 2008. Heterogeneous response of nasal and lung fibroblasts to transforming growth factor-beta 1. Clin Exp Allergy 38(5):812-21.
39. Piantadosi CA, Zhang J. 1996. Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke 27(2):327-31.
40. Poulsen MM, Larsen JØ, Hamilton-Dutoit S, Clasen BF, Jessen N, Paulsen SK, Kjær TN, Richelsen B, Pedersen SB. 2012. Resveratrol up-regulates hepatic uncoupling protein 2 and prevents development of nonalcoholic fatty liver disease in rats fed a high-fat diet. Nutr Res 32(9):701-8.
41. Regnault TR, Zhao L, Chiu JS, Gottheil SK, Foran A, Yee SP. 2010. Peroxisome proliferator-activated receptor -β/δ, -γ agonists and resveratrol modulate hypoxia induced changes in nuclear receptor activators of muscle oxidative metabolism. PPAR Res 2010:129173.
42. Rojo AI, Rada P, Egea J, Rosa AO, López MG, Cuadrado A. 2008. Functional interference between glycogen synthase kinase-3 beta and the transcription factor Nrf2 in protection against kainate-induced hippocampal cell death. Mol Cell Neurosci 39(1):125-32.
43. Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takahashi T. 2001. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 182:18-32.
44. Sakaguchi S, Wing K, Yamaguchi T. 2009. Dynamics of peripheral tolerance and immune regulation mediated by Treg. Eur J Immunol 39(9):2331-6.
45. Salinas M, Diaz R, Abraham NG, Ruiz de Galarreta CM, Cuadrado A. 2003. Nerve growth factor protects against 6-hydroxydopamine-induced oxidative stress by increasing expression of heme oxygenase-1 in a phosphatidylinositol 3-kinase-dependent manner. J Biol Chem 278(16):13898-904.
46. Soumyarani VS, Jayakumari N. 2012. Oxidatively modified high density lipoprotein promotes inflammatory response in human monocytes-macrophages by enhanced production of ROS, TNF-α, MMP-9, and MMP-2. Mol Cell Biochem 366(1-2):277-85.
47. Szkudelska K, Szkudelski T. 2010. Resveratrol, obesity and diabetes. Eur J Pharmacol 635(1-3):1-8.
48. Trayhurn P, Wood IS. 2004. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 92(3):347-55.
49. Um JH, Park SJ, Kang H, Yang S, Foretz M, McBurney MW, Kim MK, Viollet B, Chung JH. 2010. AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol. Diabetes 59(3):554-63.
50. Vetterli L, Brun T, Giovannoni L, Bosco D, Maechler P. 2011. Resveratrol potentiates glucose-stimulated insulin secretion in INS-1E beta-cells and human islets through a SIRT1-dependent mechanism. J Biol Chem 286(8):6049-60.
51. Vial G, Dubouchaud H, Couturier K, Cottet-Rousselle C, Taleux N, Athias A, Galinier A, Casteilla L, Leverve XM. 2011. Effects of a high-fat diet on energy metabolism and ROS production in rat liver. J Hepatol 54(2):348-56.
52. Wang B, Sun J, Li XH, Zhou QQ, Bai J, Shi YH, Le GW. 2013. Resveratrol prevents suppression of regulatory T-cell production, oxidative stress, and inflammation of mice prone or resistant to high-fat diet-induced obesity. Nutr Res 33(11):971-81.
53. Zamzami N, Kroemer G. 2001. The mitochondrion in apoptosis: how Pandora's box opens. Nat Rev Mol Cell Biol 2(1):67-71.