Differential modulation of ROS signals and other mitochondrial parameters by the antioxidants MitoQ, resveratrol and curcumin in human adipocytes

Journal of Receptors and Signal Transduction

Volumn 33, Issue 5, 2013, Pages 304-312

  Hirzel, Estelle ^a   Lindinger, Peter W ^a,b   Maseneni, Swarna ^b   Giese, Maria ^c   Rhein, Véronique Virginie ^c,d   Eckert, Anne ^c   Hoch, Matthias ^a,e   Krähenbühl, Stephan ^b   Eberle, Alex N ^a,f  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b Department of Biomedicine and University Hospital ^*  (Japan)

^c UNIVERSITY OF BASEL   (Switzerland)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e ACTELION PHARMACEUTICALS LTD   (Switzerland)

^f Swiss Federal Institute of Technology Collegium Helveticum   (Switzerland)

Author keywords

Adipocyte; Antioxidant; Curcumin; Human mesenchymal stem cell; MitoQ; Reactive oxygen species; Resveratrol

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CURCUMIN; MITOQ; REACTIVE OXYGEN METABOLITE; RESVERATROL; UNCLASSIFIED DRUG;

ADIPOCYTE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MITOCHONDRIAL RESPIRATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; SIGNAL TRANSDUCTION;

ADIPOCYTES; ANTIOXIDANTS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL RESPIRATION; CURCUMIN; HUMANS; HYDROGEN PEROXIDE; MESENCHYMAL STROMAL CELLS; MITOCHONDRIA; ORGANOPHOSPHORUS COMPOUNDS; OXYGEN CONSUMPTION; REACTIVE OXYGEN SPECIES; STILBENES; UBIQUINONE;

EID: 84885014178     PISSN: 10799893     EISSN: 15324281     Source Type: Journal    
DOI: 10.3109/10799893.2013.822887     Document Type: Article

References (63)

1. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 2003;15:247-54. (Pubitemid 36332201)
2. Appel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 2004;55: 373-99. (Pubitemid 38940937)
3. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011;194:7-15.
4. Andriantsitohaina R, Duluc L, Garc?́a-Rodr?́guez JC, et al. Systems biology of antioxidants. Clin Sci 2012;123:173-92.
5. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012;48:158-67.
6. D'Autréaux B, Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 2007;8:813-24. (Pubitemid 47462134)
7. Tormos KV, Anso E, Hamanaka RB, et al. Mitochondrial complex III ROS regulate adipocyte differentiation. Cell Metab 2011;14: 537-44.
8. Furukawa S, Fujita T, Shimabukuro M, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-61. (Pubitemid 40385531)
9. Krawczyk SA, Haller JF, Ferrante T, et al. Reactive oxygen species facilitate translocation of hormone sensitive lipase to the lipid droplet during lipolysis in human differentiated adipocytes. PLoS One 2012;7:e34904.
10. Lu B, Ennis D, Lai R, et al. Enhanced sensitivity of insulin-resistant adipocytes to vanadate is associated with oxidative stress and decreased reduction of vanadate (\+5) to vanadyl (\+4). J Biol Chem 2001;276:35589-98.
11. Rocha VZ, Libby P. Obesity, inflammation, and atherosclerosis. Nat Rev Cardiol 2009;6:399-409.
12. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005;54:1615-25. (Pubitemid 40770750)
13. Haber CA, Lam TK, Yu Z, et al. N-acetylcysteine and taurine prevent hyperglycemia-induced insulin resistance in vivo: possible role of oxidative stress. Am J Physiol Endocrinol Metab 2003;285: E744-53. (Pubitemid 37176425)
14. Bindokas VP, Kuznetsov A, Sreenan S, et al. Visualizing superoxide production in normal and diabetic rat islets of Langerhans. J Biol Chem 2003;278:9796-801. (Pubitemid 36800480)
15. Talior I, Yarkoni M, Bashan N, Eldar-Finkelman H. Increased glucose uptake promotes oxidative stress and PKC-delta activation in adipocytes of obese, insulin-resistant mice. Am J Physiol Endocrinol Metab 2003;285:E295-302. (Pubitemid 36899702)
16. Naviaux K. Oxidative shielding or oxidative stress? J Pharmacol Exp Ther 2012;342:608-18
17. Riccioni G, D'Orazio N, Salvatore C, et al. Carotenoids and vitamins C and E in the prevention of cardiovascular disease. Int J Vitam Nutr Res 2012;82:15-26.
18. Surdo JL, Bauer SR. Quantitative approaches to detect donor and passage differences in adipogenic potential and clonogenicity in human bone marrow-derived mesenchymal stem cells. Tissue Eng Part C Methods 2012;18:1-13.
19. Gaiba S, França LP, França JP, Ferreira LM. Characterization of human adipose-derived stem cells. Acta Cir Bras 2012;27:471-6.
20. Hirzel E, Lindinger P, Hoch M, et al. Characterization of human bone marrow-derived mesenchymal stem cells as model for adipogenesis and adipocytes. [Submitted].
21. Kelso GF, Porteous CM, Coulter CV, et al. Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties. J Biol Chem 2001;276:4588-96.
22. Rodriguez-Cuenca S, Cochemé HM, Logan A, et al. Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice. Free Radic Biol Med 2010; 48:161-72.
23. Adlam VJ, Harrison JC, Porteous CM, et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 2005;19:1088-95. (Pubitemid 40946434)
24. Lowes DA, Thottakam BM, Webster NR, et al. The mitochondriatargeted antioxidant MitoQ protects against organ damage in a lipopolysaccharide- peptidoglycan model of sepsis. Free Radic Biol Med 2008;45:1559-65.
25. Graham D, Huynh NN, Hamilton CA, et al. Mitochondria-targeted antioxidant MitoQ10 improves endothelial function and attenuates cardiac hypertrophy. Hypertension 2009;54:322-8.
26. Lowes DA, Thottakam BM, Webster NR, et al. A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease. Mov Disord 2010;25:1670-4.
27. Gane EJ, Weilert F, Orr DW, et al. The mitochondria-targeted antioxidant mitoquinone decreases liver damage in a phase II study of hepatitis C patients. Liver Int 2010;30:1019-26.
28. Pervaiz S, Holme AL. Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal 2009;11:2851-97.
29. Szkudelska K, Nogowski L, Szkudelski T. Resveratrol, a naturally occurring diphenolic compound, affects lipogenesis, lipolysis and the antilipolytic action of insulin in isolated rat adipocytes. J Steroid Biochem Mol Biol 2009;113:17-24.
30. Baur JA, Pearson KJ, Price NL, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 2006;444: 337-42. (Pubitemid 44764104)
31. Alappat L, Awad AB. Curcumin and obesity: evidence and mechanisms. Nutr Rev 2010;68:729-38.
32. Weber WM, Hunsaker LA, Gonzales AM, et al. TPA-induced upregulation of activator protein-1 can be inhibited or enhanced by analogs of the natural product curcumin. Biochem Pharmacol 2006; 72:928-40. (Pubitemid 44374461)
33. Chun KS, Keum YS, Han SS, et al. Curcumin inhibits phorbol ester-induced expression of cyclooxygenase-2 in mouse skin through suppression of extracellular signal-regulated kinase activity and NF-kappaB activation. Carcinogenesis 2003;24:1515-24. (Pubitemid 37160842)
34. Zheng S, Yumei F, Chen A. De novo synthesis of glutathione is a prerequisite for curcumin to inhibit hepatic stellate cell (HSC) activation. Free Radic Biol Med 2007;43:444-53. (Pubitemid 46977625)
35. Jang EM, Choi MS, Jung UJ, et al. Beneficial effects of curcumin on hyperlipidemia and insulin resistance in high-fat-fed hamsters. Metabolism 2008;57:1576-83.
36. Ram?́rez-Boscá A, Soler A, Carrión MA, et al. An hydroalcoholic extract of curcuma longa lowers the apo B/apo A ratio. Implications for atherogenesis prevention. Mech Ageing Dev 2000;119:41-7.
37. Ramirez Boscá A, Soler A, Carrión-Gutiérrez MA, et al. An hydroalcoholic extract of Curcuma longa lowers the abnormally high values of human-plasma fibrinogen. Mech Ageing Dev 2000; 114:207-10. (Pubitemid 30232796)
38. Srinivasan M. Effect of curcumin on blood sugar as seen in a diabetic subject. Indian J Med Sci 1972;26:269-70.
39. Hoch M, Hirzel E, Lindinger P, et al. Weak functional coupling of the melanocortin-1 receptor expressed in human adipocytes. J Recept Signal Transduct Res 2008;28:485-504.
40. Gnaiger E. Mitochondrial pathways and respiratory control (Handbook for the oxygraph instrument). 1st ed. Innsbruck, Austria: OROBOROS MiPNet Publications; 2007.
41. Asin-Cayuela J, Manas AR, James AM, et al. Fine-tuning the hydrophobicity of a mitochondria-targeted antioxidant. FEBS Lett 2004;571:9-16. (Pubitemid 38992915)
42. James AM, Cocheme HM, Murphy MP. Mitochondria-targeted redox probes as tools in the study of oxidative damage and ageing. Mech Ageing Dev 2005;126:982-6. (Pubitemid 41033179)
43. James AM, Sharpley MS, Manas AR, et al. Interaction of the mitochondria-targeted antioxidant MitoQ with phospholipid bilayers and ubiquinone oxidoreductases. J Biol Chem 2007;282: 14708-18. (Pubitemid 47093346)
44. Biswas SK, McClure D, Jimenez LA, et al. Curcumin induces glutathione biosynthesis and inhibits NF-kappaB activation and interleukin-8 release in alveolar epithelial cells: mechanism of free radical scavenging activity. Antioxid Redox Signal 2005;7:32-41. (Pubitemid 40187923)
45. Beeson CC, Beeson GC, Schnellmann RG. A high-troughput respirometric assay for mitochondrial biogenesis and toxicity. Anal Biochem 2010;404:75-81.
46. Lagouge M, Argmann C, Gerhart-Hines Z, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1a. Cell 2006;127:1109-22. (Pubitemid 44894520)
47. Ligeret H, Barthélémy S, Bouchard Doulakas G, et al. Fluoride curcumin derivatives: New mitochondrial uncoupling agents. FEBS Lett 2004;569:37-42. (Pubitemid 38844589)
48. Szkudelska K, Nogowski L, Szkudelski T. Resveratrol and genistein as adenosine triphosphate-depleting agents in fat cells. Metabolism 2011;60:720-9.
49. Li H, Horke S, Förstermann U. Oxidative stress in vascular disease and its pharmacological prevention. Trends Pharmacol Sci 2013;34: 313-19.
50. Mitchell T, Rotaru D, Saba H, et al. The mitochondriatargeted antioxidant mitoquinone protects against cold storage injury of renal tubular cells and rat kidneys. J Pharmacol 2011;336: 682-92.
51. Pung YF, Rocic P, Murphy MP, et al. Resolution of mitochondrial oxidative stress rescues coronary collateral growth in Zucker obese fatty rats. Arterioscler Thromb Vasc Biol 2012;32:325-34.
52. Gruber J, Fong S, Chen C-B, et al. Mitochondria-targeted antioxidants and metabolic modulators as pharmacological interventions to slow ageing. Biotechnol Adv 2012;31:563-92.
53. He H-J, Wang G-Y, Gao Y, et al. Curcumin attenuates Nrf2 signaling defect, oxidative stress in muscle and glucose intolerance in high fat diet-fed mice. World J Diabetes 2012;3:94-104.
54. Paravicini TM, Touiz RM. NADPH oxidases, reactive oxygen species, and hypertension. Diab Care 2008;31:S170-80.
55. Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006;5:14.
56. Choi S-W, Friso S. Epigenetics, a new bridge between nutrition and health. Adv Nutr 2010;1:8-16.
57. Gerhauser C. Cancer chemoprevention and nutri-epigenetics: state of the art and future challenges. Top Curr Chem 2013;329:73-132.
58. Cantone I, Fisher AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol 2013;20:282-9.
59. Fischer-Posovszky P, Kukulus V, Tews D, et al. Resveratrol regulates human adipocyte number and function in a Sirt1-dependent manner. Am J Clin Nutr 2010;92:5-15.
60. Shao W, Yu Z, Chiang Y, et al. Curcumin prevents high fat diet induced insulin resistance and obesity via attenuating lipogenesis in liver and inflammatory pathway in adipocyte. PLoS One 2012;7: e28784.
61. Abdel Aziz MT, El-Asmar MF, El-Ibrashy IN, et al. Effect of a novel water-soluble curcumine derivative on experimental type-1 diabetes mellitus (short term study). Diabetol Metab Syndr 2012; 4:30.
62. Lim S, Rashid MA, Jang M, et al. Mitochondria-targeted antioxidants protect pancreatic b-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell Physiol Biochem 2011;28:873-86.
63. Chacko BK, Reily C, Srivastava A, et al. Prevention of diabetic nephropathy in Ins2\+/-(AkitaJ) mice by the mitochondria-targeted therapy MitoQ. Biochem J 2010;432:9-19.