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Oxidative Medicine and Cellular Longevity
Volume 2013 (2013), Article ID 793525, 13 pages
http://dx.doi.org/10.1155/2013/793525
Research Article

Resveratrol Suppresses PAI-1 Gene Expression in a Human In Vitro Model of Inflamed Adipose Tissue

1Division of Pediatric Endocrinology and Diabetes, Department of Pediatrics and Adolescent Medicine, Ulm University Medical Center, Eythstraße 24, 89075 Ulm, Germany
2Department of Biochemistry and Biocenter Oulu, University of Oulu, P.O.B. 3000, 90014 Oulu, Finland

Received 22 March 2013; Revised 7 May 2013; Accepted 8 May 2013

Academic Editor: Nilanjana Maulik

Copyright © 2013 Ivana Zagotta et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. D. De Ferranti and S. K. Osganian, “Epidemiology of paediatric metabolic syndrome and type 2 diabetes mellitus,” Diabetes and Vascular Disease Research, vol. 4, no. 4, pp. 285–296, 2007. View at Google Scholar
  2. A. de Hamsten, G. Walldius, G. Dahlen et al., “Plasminogen activator inhibitor in plasma: risk factor for recurrent myocardial infarction,” The Lancet, vol. 2, no. 8549, pp. 3–9, 1987. View at Google Scholar · View at Scopus
  3. I. Juhan-Vague, C. Roul, M. C. Alessi, J. P. Ardissone, M. Heim, and P. Vague, “Increased plasminogen activator inhibitor activity in non insulin dependent diabetic patients: relationship with plasma insulin,” Thrombosis and Haemostasis, vol. 61, no. 3, pp. 370–373, 1989. View at Google Scholar · View at Scopus
  4. D. J. Schneider, T. K. Nordt, and B. E. Sobel, “Attenuated fibrinolysis and accelerated atherogenesis in type II diabetic patients,” Diabetes, vol. 42, no. 1, pp. 1–7, 1993. View at Google Scholar · View at Scopus
  5. I. Juhan-Vague and M. C. Alessi, “PAI-1, obesity, insulin resistance and risk of cardiovascular events,” Thrombosis and Haemostasis, vol. 78, no. 1, pp. 656–660, 1997. View at Google Scholar · View at Scopus
  6. C. Dellas and D. J. Loskutoff, “Historical analysis of PAI-1 from its discovery to its potential role in cell motility and disease,” Journal of Thrombosis and Haemostasis, vol. 93, pp. 631–640, 2005. View at Google Scholar
  7. H. R. Lijnen, L. Nelles, B. Van Hoef, E. Demarsin, and D. Collen, “Characterization of a chimeric plasminogen activator consisting of amino acids 1 to 274 of tissue-type plasminogen activator and amino acids 138 to 411 of single-chain urokinase-type plasminogen activator,” Journal of Biological Chemistry, vol. 263, no. 35, pp. 19083–19091, 1988. View at Google Scholar · View at Scopus
  8. H. P. Kohler and P. J. Grant, “Plasminogen-activator inhibitor type 1 and coronary artery disease,” The New England Journal of Medicine, vol. 342, no. 24, pp. 1792–1801, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. L. R. Lund, B. Georg, L. S. Nielsen, M. Mayer, K. Dano, and P. A. Andreasen, “Plasminogen activator inhibitor type 1: cell-specific and differentiation-induced expression and regulation in human cell lines, as determined by enzyme-linked immunosorbent assay,” Molecular and Cellular Endocrinology, vol. 60, no. 1, pp. 43–53, 1988. View at Google Scholar · View at Scopus
  10. E. Y. Dimova, U. Möller, S. Herzig et al., “Transcriptional regulation of plasminogen activator inhibitor-I expression by insulin-like growth factor-I via MAP kinases and hypoxia-inducible factor-I in HepG2 cells,” Thrombosis and Haemostasis, vol. 93, no. 6, pp. 1176–1184, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. T. Kietzmann, U. Roth, and K. Jungermann, “Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia-inducible factor-1 in rat hepatocytes,” Blood, vol. 94, no. 12, pp. 4177–4185, 1999. View at Google Scholar · View at Scopus
  12. T. Kietzmann, A. Samoylenko, U. Roth, and K. Jungermann, “Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes,” Blood, vol. 101, no. 3, pp. 907–914, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. E. Y. Dimova and T. Kietzmann, “The MAPK pathway and HIF-1 are involved in the induction of the human PAI-1 gene expression by insulin in the human hepatoma cell line HepG2,” Annals of the New York Academy of Sciences, vol. 1090, pp. 355–367, 2006. View at Google Scholar
  14. E. Y. Dimova and T. Kietzmann, “Metabolic, hormonal and environmental regulation of plasminogen activator inhibitor-1 (PAI-1) expression: lessons from the liver,” Thrombosis and Haemostasis, vol. 100, no. 6, pp. 992–1006, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Gonzalez, B. M. del Mar, A. Pons, I. Llompart, and J. A. Tur, “Inflammatory markers and metabolic syndrome among adolescents,” European Journal of Clinical Nutrition, vol. 66, pp. 1141–1145, 2012. View at Google Scholar
  16. F. Samad and D. J. Loskutoff, “Tissue distribution and regulation of plasminogen activator inhibitor-1 in obese mice,” Molecular Medicine, vol. 2, no. 5, pp. 568–582, 1996. View at Google Scholar · View at Scopus
  17. M. Cigolini, G. Targher, A. I. Bergamo, M. Tonoli, G. Agostino, and G. De Sandre, “Visceral fat accumulation and its relation to plasma hemostatic factors in healthy men,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 16, pp. 368–374, 1996. View at Google Scholar
  18. P. Vague, I. Juhan-Vague, V. Chabert, M. C. Alessi, and C. Atlan, “Fat distribution and plasminogen activator inhibitor activity in nondiabetic obese women,” Metabolism, vol. 38, no. 9, pp. 913–915, 1989. View at Google Scholar · View at Scopus
  19. K. Landin, L. Stigendal, E. Eriksson et al., “Abdominal obesity is associated with an impaired fibrinolytic activity and elevated plasminogen activator inhibitor-1,” Metabolism, vol. 39, no. 10, pp. 1044–1048, 1990. View at Publisher · View at Google Scholar · View at Scopus
  20. J. B. McGill, D. J. Schneider, C. L. Arfken, C. L. Lucore, and B. E. Sobel, “Factors responsible for impaired fibrinolysis in obese subjects and NIDDM patients,” Diabetes, vol. 43, no. 1, pp. 104–109, 1994. View at Google Scholar · View at Scopus
  21. P. Eriksson, S. Reynisdottir, F. Lönnqvist, V. Stemme, A. Hamsten, and P. Arner, “Adipose tissue secretion of plasminogen activator inhibitor-1 in non- obese and obese individuals,” Diabetologia, vol. 41, no. 1, pp. 65–71, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Samad and D. J. Loskutoff, “The fat mouse: a powerful genetic model to study elevated plasminogen activator inhibitor 1 in obesity/NIDDM,” Thrombosis and Haemostasis, vol. 78, no. 1, pp. 652–655, 1997. View at Google Scholar · View at Scopus
  23. T. Skurk and H. Hauner, “Obesity and impaired fibrinolysis: role of adipose production of plasminogen activator inhibitor-1,” International Journal of Obesity, vol. 28, pp. 1357–1364, 2004. View at Publisher · View at Google Scholar
  24. L. Ma, S. Mao, K. L. Taylor et al., “Prevention of obesity and insulin resistance in mice lacking plasminogen activator inhibitor 1,” Diabetes, vol. 53, no. 2, pp. 336–346, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Hoffstedt, I. Andersson, L. Persson, B. Isaksson, and P. Arner, “The common-675 4G/5G polymorphism in the plasminogen activator inhibitor-1 gene is strongly associated with obesity,” Diabetologia, vol. 45, no. 4, pp. 584–587, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. A. R. Folsom, H. T. Qamhieh, R. R. Wing et al., “Impact of weight loss on plasminogen activator inhibitor (PAI-1), factor VII, and other hemostatic factors in moderately overweight adults,” Arteriosclerosis and Thrombosis, vol. 13, no. 2, pp. 162–169, 1993. View at Google Scholar · View at Scopus
  27. M. C. Alessi and I. Juhan-Vague, “PAI-1 and the metabolic syndrome,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, pp. 2200–2207, 2006. View at Google Scholar
  28. P. Signorelli and R. Ghidoni, “Resveratrol as an anticancer nutrient: molecular basis, open questions and promises,” Journal of Nutritional Biochemistry, vol. 16, no. 8, pp. 449–466, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. J. A. Baur, K. J. Pearson, N. L. Price et al., “Resveratrol improves health and survival of mice on a high-calorie diet,” Nature, vol. 444, no. 7117, pp. 337–342, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Lagouge, C. Argmann, Z. Gerhart-Hines et al., “Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α,” Cell, vol. 127, no. 6, pp. 1109–1122, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. K. J. Pearson, J. A. Baur, K. N. Lewis et al., “Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span,” Cell Metabolism, vol. 8, no. 2, pp. 157–168, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. J. L. Barger, T. Kayo, J. M. Vann et al., “A low dose of dietary resveratrol partially mimics caloric restriction and retards aging parameters in mice,” PLoS ONE, vol. 3, no. 6, Article ID e2264, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Sun, F. Zhang, X. Ge et al., “SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B,” Cell Metabolism, vol. 6, no. 4, pp. 307–319, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. M. C. Aubin, C. Lajoie, R. Clement, H. Gosselin, A. Calderone, and L. P. Perrault, “Female rats fed a high-fat diet were associated with vascular dysfunction and cardiac fibrosis in the absence of overt obesity and hyperlipidemia: therapeutic potential of resveratrol,” Journal of Pharmacology and Experimental Therapeutics, vol. 325, pp. 961–968, 2008. View at Google Scholar
  35. J. Shang, L. Chen, F. Xiao, H. Sun, H. Ding, and H. Xiao, “Resveratrol improves non-alcoholic fatty liver disease by activating AMP-activated protein kinase,” Acta Pharmacologica Sinica, vol. 29, no. 6, pp. 698–706, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. J. Shang, L. Chen, and F. Xiao, “Resveratrol improves high-fat induced nonalcoholic fatty liver in rats,” Chinese Journal of Hepatology, vol. 16, no. 8, pp. 616–619, 2008. View at Google Scholar · View at Scopus
  37. K. K. Rocha, G. A. Souza, G. X. Ebaid, F. R. Seiva, A. C. Cataneo, and E. L. Novelli, “Resveratrol toxicity: effects on risk factors for atherosclerosis and hepatic oxidative stress in standard and high-fat diets,” Food and Chemical Toxicology, vol. 47, no. 6, pp. 1362–1367, 2009. View at Google Scholar
  38. L. Rivera, R. Morón, A. Zarzuelo, and M. Galisteo, “Long-term resveratrol administration reduces metabolic disturbances and lowers blood pressure in obese Zucker rats,” Biochemical Pharmacology, vol. 77, no. 6, pp. 1053–1063, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. G. Ramadori, L. Gautron, T. Fujikawa, C. R. Vianna, J. K. Elmquist, and R. Coppari, “Central administration of resveratrol improves diet-induced diabetes,” Endocrinology, vol. 150, no. 12, pp. 5326–5333, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Timmers, E. Konings, L. Bilet et al., “Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans,” Cell Metabolism, vol. 14, no. 5, pp. 612–622, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Tome-Carneiro, M. Gonzalvez, M. Larrosa et al., “Grape resveratrol increases serum adiponectin and downregulates inflammatory genes in peripheral blood mononuclear cells: a triple-blind, placebo-controlled, one-year clinical trial in patients with stable coronary artery disease,” Cardiovascular Drugs and Therapy, vol. 27, no. 1, pp. 37–48, 2013. View at Google Scholar
  42. M. M. Poulsen, P. F. Vestergaard, B. F. Clasen et al., “An investigator-initiated, randomized, placebo-controlled clinical trial of substrate metabolism, insulin sensitivity, and body composition,” Diabetes, vol. 62, no. 4, pp. 1186–1195, 2013. View at Google Scholar
  43. P. Fischer-Posovszky, F. S. Newell, M. Wabitsch, and H. E. Tornqvist, “Human SGBS cells: a unique tool for studies of human fat cell biology,” Obesity Facts, vol. 1, no. 4, pp. 184–189, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. H. Hauner, T. Skurk, and M. Wabitsch, “Cultures of human adipose precursor cells,” Methods in Molecular Biology, vol. 155, pp. 239–247, 2001. View at Google Scholar · View at Scopus
  45. P. Kotnik, M. Keuper, M. Wabitsch, and P. Fischer-Posovszky, “Interleukin-1beta downregulates RBP4 secretion in human adipocytes,” PLoS One, vol. 8, Article ID e57796, 2013. View at Google Scholar
  46. K. R. Laderoute, K. Amin, J. M. Calaoagan et al., “5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments,” Molecular and Cellular Biology, vol. 26, no. 14, pp. 5336–5347, 2006. View at Publisher · View at Google Scholar · View at Scopus
  47. K. J. Livak and T. D. Schmittgen, “Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method,” Methods, vol. 25, no. 4, pp. 402–408, 2001. View at Google Scholar
  48. M. F. Gregor and G. S. Hotamisligil, “Inflammatory mechanisms in obesity,” Annual Review of Immunology, vol. 29, pp. 415–445, 2011. View at Google Scholar
  49. M. Keuper, A. Dzyakanchuk, K. E. Amrein, M. Wabitsch, and P. Fischer-Posovszky, “THP-1 macrophages and SGBS adipocytes: a new human in vitro model system of inflamed adipose tissue,” Frontiers in Endocrinology, vol. 2, p. 89, 2011. View at Google Scholar
  50. F. Picard, M. Kurtev, N. Chung et al., “Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-γ,” Nature, vol. 429, no. 771, p. 776, 2004. View at Google Scholar · View at Scopus
  51. P. Fischer-Posovszky, V. Kukulus, D. Tews et al., “Resveratrol regulates human adipocyte number and function in a Sirt1-dependent manner,” The American Journal of Clinical Nutrition, vol. 92, pp. 5–15, 2010. View at Google Scholar
  52. A. Wang, M. Liu, X. Liu et al., “Up-regulation of adiponectin by resveratrol: the essential roles of the Akt/FOXO1 and amp-activated protein kinase signaling pathways and DsbA-L,” Journal of Biological Chemistry, vol. 286, no. 1, pp. 60–66, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Chen, Z. Li, W. Li, Z. Shan, and W. Zhu, “Resveratrol inhibits cell differentiation in 3T3-L1 adipocytes via activation of AMPK,” Canadian Journal of Physiology and Pharmacology, vol. 89, no. 11, pp. 793–799, 2011. View at Publisher · View at Google Scholar
  54. A. Lasa, M. Schweiger, P. Kotzbeck et al., “Resveratrol regulates lipolysis via adipose triglyceride lipase,” The Journal of Nutritional Biochemistry, vol. 23, no. 4, pp. 379–384, 2012. View at Google Scholar
  55. I. Mader, M. Wabitsch, K. Debatin, P. Fischer-Posovszky, and S. Fulda, “Identification of a novel proapoptotic function of resveratrol in fat cells: SIRT1-independent sensitization to TRAIL-induced apoptosis,” FASEB Journal, vol. 24, no. 6, pp. 1997–2009, 2010. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Miranda, A. González-Rodríguez, J. Revuelta-Cervantes, C. M. Rondinone, and A. M. Valverde, “Beneficial effects of PTP1B deficiency on brown adipocyte differentiation and protection against apoptosis induced by pro- and anti-inflammatory stimuli,” Cellular Signalling, vol. 22, no. 4, pp. 645–659, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. L. Kang, W. Heng, A. Yuan, L. Baolin, and H. Fang, “Resveratrol modulates adipokine expression and improves insulin sensitivity in adipocytes: relative to inhibition of inflammatory responses,” Biochimie, vol. 92, no. 7, pp. 789–796, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. K. Esposito, M. Ciotola, and D. Giugliano, “Rosiglitazone cools down inflammation in the metabolic syndrome,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 26, pp. 1413–1414, 2005. View at Google Scholar
  59. A. Fernández-Sánchez, E. Madrigal-Santillán, M. Bautista et al., “Inflammation, oxidative stress, and obesity,” International Journal of Molecular Sciences, vol. 12, no. 5, pp. 3117–3132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  60. E. Y. Dimova, A. Samoylenko, and T. Kietzmann, “Oxidative stress and hypoxia: implications for plasminogen activator inhibitor-1 expression,” Antioxidants and Redox Signaling, vol. 6, no. 4, pp. 777–791, 2004. View at Publisher · View at Google Scholar · View at Scopus
  61. R. Samarakoon, J. M. Overstreet, and P. J. Higgins, “TGF-beta signaling in tissue fibrosis: redox controls, target genes and therapeutic opportunities,” Cellular Signalling, vol. 25, no. 1, pp. 264–268, 2013. View at Google Scholar
  62. M. B. Sporn and K. T. Liby, “NRF2 and cancer: the good, the bad and the importance of context,” Nature Reviews Cancer, vol. 12, pp. 564–571, 2012. View at Google Scholar
  63. G. S. Hotamisligil, “Inflammation and metabolic disorders,” Nature, vol. 444, no. 7121, pp. 860–867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  64. C. J. Lyon and W. A. Hsueh, “Effect of plasminogen activator inhibitor-1 in diabetes mellitus and cardiovascular disease,” The American Journal of Medicine, vol. 115, Supplement 1, no. 8, pp. 62–68, 2003. View at Google Scholar
  65. P. E. Morange, M. C. Alessi, M. Verdier, D. Casanova, G. Magalon, and I. Juhan-Vague, “PAI-1 produced ex vivo by human adipose tissue is relevant to PAI-1 blood level,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 19, no. 5, pp. 1361–1365, 1999. View at Google Scholar · View at Scopus
  66. I. Shimomura, T. Funahashi, M. Takahashi et al., “Enhanced expression of PAI-1 in visceral fat: possible contributor to vascular disease in obesity,” Nature Medicine, vol. 2, no. 7, pp. 800–803, 1996. View at Publisher · View at Google Scholar · View at Scopus
  67. D. J. Loskutoff and F. Samad, “The adipocyte and hemostatic balance in obesity studies of PAI-1,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 18, pp. 1–6, 1998. View at Google Scholar
  68. J. Ahn, H. Lee, S. Kim, and T. Ha, “Resveratrol inhibits TNF-α-induced changes of adipokines in 3T3-L1 adipocytes,” Biochemical and Biophysical Research Communications, vol. 364, no. 4, pp. 972–977, 2007. View at Google Scholar
  69. J. Olholm, S. K. Paulsen, K. B. Cullberg, B. Richelsen, and S. B. Pedersen, “Anti-inflammatory effect of resveratrol on adipokine expression and secretion in human adipose tissue explants,” International Journal of Obesity, vol. 34, pp. 1546–1553, 2010. View at Google Scholar
  70. G. C. Yen, Y. C. Chen, W. T. Chang, and C. L. Hsu, “Effects of polyphenolic compounds on tumor necrosis factor-α (TNF-α)-induced changes of adipokines and oxidative stress in 3T3-L1 adipocytes,” Journal of Agricultural and Food Chemistry, vol. 59, no. 2, pp. 546–551, 2011. View at Google Scholar
  71. A. Rosenow, J. P. Noben, J. Jocken et al., “Resveratrol-induced changes of the human adipocyte secretion profile,” Journal of Proteome Research, vol. 11, no. 9, pp. 4733–4743, 2012. View at Publisher · View at Google Scholar
  72. V. W. Dolinsky and J. R. B. Dyck, “Calorie restriction and resveratrol in cardiovascular health and disease,” Biochimica et Biophysica Acta, vol. 1812, no. 11, pp. 1477–1489, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. J. R. Speakman and S. E. Mitchell, “Caloric restriction,” Molecular Aspects of Medicine, vol. 32, no. 3, pp. 159–221, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Szkudelska and T. Szkudelski, “Resveratrol, obesity and diabetes,” European Journal of Pharmacology, vol. 635, no. 1–3, pp. 1–8, 2010. View at Publisher · View at Google Scholar · View at Scopus
  75. K. T. Howitz, K. J. Bitterman, H. Y. Cohen et al., “Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan,” Nature, vol. 425, no. 6954, pp. 191–196, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. X. Zhu, Q. Liu, M. Wang et al., “Activation of Sirt1 by resveratrol inhibits TNF-α induced inflammation in Fibroblasts,” PLoS ONE, vol. 6, no. 10, Article ID e27081, 2011. View at Publisher · View at Google Scholar · View at Scopus
  77. Q. Q. Lin, C. F. Yan, R. Lin et al., “SIRT1 regulates TNF-α-induced expression of CD40 in 3T3-L1 adipocytes via NF-κB pathway,” Cytokine, vol. 60, no. 2, pp. 447–455, 2012. View at Google Scholar
  78. X. Hou, S. Xu, K. A. Maitland-Toolan et al., “SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase,” Journal of Biological Chemistry, vol. 283, no. 29, pp. 20015–20026, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. M. Zang, S. Xu, K. A. Maitland-Toolan et al., “Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-deficient mice,” Diabetes, vol. 55, no. 8, pp. 2180–2191, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. I. P. Salt and T. M. Palmer, “Exploiting the anti-inflammatory effects of AMP-activated protein kinase activation,” Expert Opinion on Investigational Drugs, vol. 21, no. 8, pp. 1155–1167, 2012. View at Google Scholar
  81. S. Bijland, S. J. Mancini, and I. P. Salt, “Role of AMP-activated protein kinase in adipose tissue metabolism and inflammation,” Clinical Science, vol. 124, pp. 491–507, 2013. View at Google Scholar
  82. A. Görlach, I. Diebold, V. B. Schini-Kerth et al., “Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells role of the p22phox-containing NADPH oxidase,” Circulation Research, vol. 89, no. 1, pp. 47–54, 2001. View at Google Scholar · View at Scopus
  83. K. W. Kang, S. J. Lee, and S. G. Kim, “Molecular mechanism of Nrf2 activation by oxidative stress,” Antioxidants and Redox Signaling, vol. 7, no. 11-12, pp. 1664–1673, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. H. Ghanim, C. L. Sia, K. Korzeniewski et al., “A resveratrol and polyphenol preparation suppresses oxidative and inflammatory stress response to a high-fat, high-carbohydrate meal,” Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 5, pp. 1409–1414, 2011. View at Publisher · View at Google Scholar · View at Scopus
  85. P. E. Morange, H. R. Lijnen, M. C. Alessi, F. Kopp, D. Collen, and I. Juhan-Vague, “Influence of PAI-1 on adipose tissue growth and metabolic parameters in a murine model of diet-induced obesity,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 20, no. 4, pp. 1150–1154, 2000. View at Google Scholar · View at Scopus
  86. D. J. Loskutoff, K. Fujisawa, and F. Samad, “The fat mouse: a powerful genetic model to study hemostatic gene expression in obesity/NIDDM,” Annals of the New York Academy of Sciences, vol. 902, pp. 272–281, 2000. View at Google Scholar
  87. M. Pandey, D. J. Loskutoff, and F. Samad, “Molecular mechanisms of tumor necrosis factor-α-mediated plasminogen activator inhibitor-1 expression in adipocytes,” FASEB Journal, vol. 19, no. 10, pp. 1317–1319, 2005. View at Publisher · View at Google Scholar · View at Scopus
  88. A. M. Gonzales and R. A. Orlando, “Curcumin and resveratrol inhibit nuclear factor-κB-mediated cytokine expression in adipocytes,” Nutrition and Metabolism, vol. 5, article 17, 2008. View at Google Scholar
  89. J. K. Kundu and Y. Surh, “Molecular basis of chemoprevention by resveratrol: NF-κB and AP-1 as potential targets,” Mutation Research, vol. 555, no. 1-2, pp. 65–80, 2004. View at Publisher · View at Google Scholar · View at Scopus
  90. P. T. Pfluger, D. Herranz, S. Velasco-Miguel, M. Serrano, and M. H. Tschop, “Sirt1 protects against high-fat diet-induced metabolic damage,” Proceedings of the National Academy of Sciences of the United States of America PNAS, vol. 105, no. 28, pp. 9793–9798, 2008. View at Google Scholar
  91. T. Yoshizaki, J. C. Milne, T. Imamura et al., “SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes,” Molecular and Cellular Biology, vol. 29, no. 5, pp. 1363–1374, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Salminen, J. M. T. Hyttinen, and K. Kaarniranta, “AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan,” Journal of Molecular Medicine, vol. 89, no. 7, pp. 667–676, 2011. View at Publisher · View at Google Scholar · View at Scopus
  93. O. N. Ozes, L. D. Mayo, J. A. Gustin, S. R. Pfeffer, L. M. Pfeffer, and D. B. Donner, “NF-κB activation by tumour necrosis factor requires tie Akt serine-threonine kinase,” Nature, vol. 401, no. 6748, pp. 82–85, 1999. View at Publisher · View at Google Scholar · View at Scopus
  94. L. V. Madrid, M. W. Mayo, J. Y. Reuther, and A. S. Baldwin Jr., “Akt stimulates the transactivation potential of the RelA/p65 subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen-activated protein kinase p38,” Journal of Biological Chemistry, vol. 276, no. 22, pp. 18934–18940, 2001. View at Publisher · View at Google Scholar · View at Scopus
  95. S. K. Manna, A. Mukhopadhyay, and B. B. Aggarwal, “Resveratrol suppresses TNF-induced activation of nuclear transcription factors NF-κB, activator protein-1, and apoptosis: potential role of reactive oxygen intermediates and lipid peroxidation,” Journal of Immunology, vol. 164, no. 12, pp. 6509–6519, 2000. View at Google Scholar · View at Scopus
  96. J. J. Heynekamp, W. M. Weber, L. A. Hunsaker et al., “Substituted trans-stilbenes, including analogues of the natural product resveratrol, inhibit the human tumor necrosis factor alpha-induced activation of transcription factor nuclear factor κB,” Journal of Medicinal Chemistry, vol. 49, no. 24, pp. 7182–7189, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. N. H. Nam, “Naturally occurring NF-κB inhibitors,” in Mini-Reviews in Medicinal Chemistry, vol. 6, pp. 945–951, 2006. View at Publisher · View at Google Scholar
  98. J. Zhu, W. Yong, X. Wu et al., “Anti-inflammatory effect of resveratrol on TNF-α-induced MCP-1 expression in adipocytes,” Biochemical and Biophysical Research Communications, vol. 369, no. 2, pp. 471–477, 2010. View at Google Scholar
  99. A. Kumar and S. S. Sharma, “NF-κB inhibitory action of resveratrol: a probable mechanism of neuroprotection in experimental diabetic neuropathy,” Biochemical and Biophysical Research Communications, vol. 394, no. 2, pp. 360–365, 2010. View at Google Scholar
  100. S. Kim, Y. Jin, Y. Choi, and T. Park, “Resveratrol exerts anti-obesity effects via mechanisms involving down-regulation of adipogenic and inflammatory processes in mice,” Biochemical Pharmacology, vol. 81, no. 11, pp. 1343–1351, 2011. View at Publisher · View at Google Scholar · View at Scopus