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PPAR Research
Volume 2016, Article ID 7359521, 13 pages
http://dx.doi.org/10.1155/2016/7359521
Research Article

Caffeic Acid Phenethyl Ester Regulates PPAR’s Levels in Stem Cells-Derived Adipocytes

1Department of Drug Science, Biochemistry Section, University of Catania, Viale Andrea Doria 6, 95125 Catania, Italy
2Department of Surgery and Medical Specialties, Section of Hematology, University of Catania, Via Salvatore Citelli 6, 95124 Catania, Italy
3IRCCS “S. Donato” Hospital, San Donato Milanese, Piazza Edmondo Malan, 20097 Milan, Italy
4Department of Biomedicine and Biotechnologies, University of Catania, Viale Andrea Doria 6, 95125 Catania, Italy

Received 27 July 2015; Accepted 30 December 2015

Academic Editor: Paulina Ormazabal

Copyright © 2016 Luca Vanella 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. M. Esteve Ràfols, “Adipose tissue: cell heterogeneity and functional diversity,” Endocrinologia y Nutricion, vol. 61, no. 2, pp. 100–112, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Chiarugi and T. Fiaschi, “Adiponectin in health and diseases: from metabolic syndrome to tissue regeneration,” Expert Opinion on Therapeutic Targets, vol. 14, no. 2, pp. 193–206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. V. Andrade-Oliveira, N. O. Câmara, and P. M. Moraes-Vieira, “Adipokines as drug targets in diabetes and underlying disturbances,” Journal of Diabetes Research, vol. 2015, Article ID 681612, 11 pages, 2015. View at Publisher · View at Google Scholar
  4. F. Bonomini, L. F. Rodella, and R. Rezzani, “Metabolic syndrome, aging and involvement of oxidative stress,” Aging and Disease, vol. 6, no. 2, pp. 109–120, 2015. View at Publisher · View at Google Scholar
  5. I. M. Wahba and R. H. Mak, “Obesity and obesity-initiated metabolic syndrome: mechanistic links to chronic kidney disease,” Clinical Journal of the American Society of Nephrology, vol. 2, no. 3, pp. 550–562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. I. Barbagallo, A. Nicolosi, G. Calabrese et al., “The role of the heme oxygenase system in the metabolic syndrome,” Current Pharmaceutical Design, vol. 20, no. 31, pp. 4970–4974, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Shuster, M. Patlas, J. H. Pinthus, and M. Mourtzakis, “The clinical importance of visceral adiposity: a critical review of methods for visceral adipose tissue analysis,” British Journal of Radiology, vol. 85, no. 1009, pp. 1–10, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. A. C. Cordeiro, A. R. Qureshi, B. Lindholm et al., “Visceral fat and coronary artery calcification in patients with chronic kidney disease,” Nephrology Dialysis Transplantation, vol. 28, supplement 4, pp. iv152–iv159, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Pasini, V. Flati, S. Paiardi et al., “Intracellular molecular effects of insulin resistance in patients with metabolic syndrome,” Cardiovascular Diabetology, vol. 9, article 46, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Nicolai, M. Li, D. H. Kim et al., “Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats,” Hypertension, vol. 53, no. 3, pp. 508–515, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Makki, P. Froguel, and I. Wolowczuk, “Adipose tissue in obesity-related inflammation and insulin resistance: cells, cytokines, and chemokines,” ISRN Inflammation, vol. 2013, Article ID 139239, 12 pages, 2013. View at Publisher · View at Google Scholar
  12. J. J. Senn, P. J. Klover, I. A. Nowak, and R. A. Mooney, “Interleukin-6 induces cellular insulin resistance in hepatocytes,” Diabetes, vol. 51, no. 12, pp. 3391–3399, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Yasui, E. Nishiyama, S. Juman et al., “Caffeic acid phenethyl ester suppresses oxidative stress in 3T3-L1 adipocytes,” Journal of Asian Natural Products Research, vol. 15, no. 11, pp. 1189–1196, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Juman, N. Yasui, H. Okuda et al., “Caffeic acid phenethyl ester inhibits differentiation to adipocytes in 3T3-l1 mouse fibroblasts,” Biological & Pharmaceutical Bulletin, vol. 33, no. 9, pp. 1484–1488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. H. R. Yilmaz, E. Uz, N. Yucel, I. Altuntas, and N. Ozcelik, “Protective effect of caffeic acid phenethyl ester (CAPE) on lipid peroxidation and antioxidant enzymes in diabetic rat liver,” Journal of Biochemical and Molecular Toxicology, vol. 18, no. 4, pp. 234–238, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. U. Koltuksuz, S. Özen, E. Uz et al., “Caffeic acid phenethyl ester prevents intestinal reperfusion injury in rats,” Journal of Pediatric Surgery, vol. 34, no. 10, pp. 1458–1462, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. M. K. Ozer, H. Parlakpinar, N. Vardi, Y. Cigremis, M. Ucar, and A. Acet, “Myocardial ischemia/reperfusion-induced oxidative renal damage in rats: protection by caffeic acid phenethyl ester (Cape),” Shock, vol. 24, no. 1, pp. 97–100, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Natarajan, S. Singh, T. R. Burke Jr., D. Grunberger, and B. B. Aggarwal, “Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 17, pp. 9090–9095, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. F. Salomone, I. Barbagallo, L. Puzzo, C. Piazza, and G. Li Volti, “Efficacy of adipose tissue-mesenchymal stem cell transplantation in rats with acetaminophen liver injury,” Stem Cell Research, vol. 11, no. 3, pp. 1037–1044, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Ranganathan, R. Unal, I. Pokrovskaya et al., “The lipogenic enzymes DGAT1, FAS, and LPL in adipose tissue: effects of obesity, insulin resistance, and TZD treatment,” Journal of Lipid Research, vol. 47, no. 11, pp. 2444–2450, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Borén, M.-R. Taskinen, S.-O. Olofsson, and M. Levin, “Ectopic lipid storage and insulin resistance: a harmful relationship,” Journal of Internal Medicine, vol. 274, no. 1, pp. 25–40, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. A. G. Dulloo, V. Antic, and J.-P. Montani, “Ectopic fat stores: housekeepers that can overspill into weapons of lean body mass destruction,” International Journal of Obesity, vol. 28, supplement 4, pp. S1–S2, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Gustafson, S. Hedjazifar, S. Gogg, A. Hammarstedt, and U. Smith, “Insulin resistance and impaired adipogenesis,” Trends in Endocrinology and Metabolism, vol. 26, no. 4, pp. 193–200, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Gustafson, A. Hammarstedt, S. Hedjazifar, and U. Smith, “Restricted adipogenesis in hypertrophic obesity: the role of WISP2, WNT, and BMP4,” Diabetes, vol. 62, no. 9, pp. 2997–3004, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. S. H. Shin, S. G. Seo, S. Min et al., “Caffeic acid phenethyl ester, a major component of propolis, suppresses high fat diet-induced obesity through inhibiting adipogenesis at the mitotic clonal expansion stage,” Journal of Agricultural and Food Chemistry, vol. 62, no. 19, pp. 4306–4312, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. N. G. Abraham and A. Kappas, “Pharmacological and clinical aspects of heme oxygenase,” Pharmacological Reviews, vol. 60, no. 1, pp. 79–127, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. I. Barbagallo, G. Marrazzo, A. Frigiola, A. Zappala, and G. Li Volti, “Role of carbon monoxide in vascular diseases,” Current Pharmaceutical Biotechnology, vol. 13, no. 6, pp. 787–796, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Sorrenti, F. Mazza, A. Campisi et al., “Heme oxygenase induction by cyanidin-3-O-β-glucoside in cultured human endothelial cells,” Molecular Nutrition and Food Research, vol. 51, no. 5, pp. 580–586, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. I. Barbagallo, F. Galvano, A. Frigiola et al., “Potential therapeutic effects of natural heme oxygenase-1 inducers in cardiovascular diseases,” Antioxidants & Redox Signaling, vol. 18, no. 5, pp. 507–521, 2013. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Kushida, G. LiVolti, A. I. Goodman, and N. G. Abraham, “TNF-α-mediated cell death is attenuated by retrovirus delivery of human heme oxygenase-1 gene into human microvessel endothelial cells,” Transplantation Proceedings, vol. 34, no. 7, pp. 2973–2978, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Novo, F. Cappello, M. Rizzo et al., “Hsp60 and heme oxygenase-1 (Hsp32) in acute myocardial infarction,” Translational Research, vol. 157, no. 5, pp. 285–292, 2011. View at Publisher · View at Google Scholar
  32. D. Sacerdoti, C. Colombrita, M. H. Ghattas et al., “Heme oxygenase-1 transduction in endothelial cells causes downregulation of monocyte chemoattractant protein-1 and of genes involved in inflammation and growth,” Cellular and Molecular Biology, vol. 51, no. 4, pp. 363–370, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Cao, S. J. Peterson, K. Sodhi et al., “Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet,” Hypertension, vol. 60, no. 2, pp. 467–475, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Burgess, M. Li, L. Vanella et al., “Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice,” Hypertension, vol. 56, no. 6, pp. 1124–1130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Eljaafari, M. Robert, M. Chehimi et al., “Adipose tissue-derived stem cells from obese subjects contribute to inflammation and reduced insulin response in adipocytes through differential regulation of the Th1/Th17 balance and monocyte activation,” Diabetes, vol. 64, no. 7, pp. 2477–2488, 2015. View at Publisher · View at Google Scholar
  36. L. Vanella, K. Sodhi, D. H. Kim et al., “Increased heme-oxygenase 1 expression in mesenchymal stem cell-derived adipocytes decreases differentiation and lipid accumulation via upregulation of the canonical Wnt signaling cascade,” Stem Cell Research and Therapy, vol. 4, no. 2, article 28, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. A. H. Berg, T. P. Combs, and P. E. Scherer, “ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism,” Trends in Endocrinology and Metabolism, vol. 13, no. 2, pp. 84–89, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. H. S. Sul, “Minireview: pref-1: role in adipogenesis and mesenchymal cell fate,” Molecular Endocrinology, vol. 23, no. 11, pp. 1717–1725, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. S. Rahman, P. J. Czernik, Y. Lu, and B. Lecka-Czernik, “β-catenin directly sequesters adipocytic and insulin sensitizing activities but not osteoblastic activity of PPARγ2 in marrow mesenchymal stem cells,” PLoS ONE, vol. 7, no. 12, Article ID e51746, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. H. Choi, S.-S. Choi, E. S. Kim et al., “Thrap3 docks on phosphoserine 273 of PPARγ and controls diabetic gene programming,” Genes & Development, vol. 28, no. 21, pp. 2361–2369, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Jéquier, “Leptin signaling, adiposity, and energy balance,” Annals of the New York Academy of Sciences, vol. 967, pp. 379–388, 2002. View at Google Scholar · View at Scopus
  42. R. H. Lustig, S. Sen, J. E. Soberman, and P. A. Velasquez-Mieyer, “Obesity, leptin resistance, and the effects of insulin reduction,” International Journal of Obesity, vol. 28, no. 10, pp. 1344–1348, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Li, K. Guo, L. Vanella, S. Taketani, Y. Adachi, and S. Ikehara, “Stem cell transplantation upregulates Sirt1 and antioxidant expression, ameliorating fatty liver in type 2 diabetic mice,” International Journal of Biological Sciences, vol. 11, no. 4, pp. 472–481, 2015. View at Publisher · View at Google Scholar
  44. H. H. Zhang, X. J. Ma, L. N. Wu et al., “SIRT1 attenuates high glucose-induced insulin resistance via reducing mitochondrial dysfunction in skeletal muscle cells,” Experimental Biology and Medicine, vol. 240, no. 5, pp. 557–565, 2015. View at Publisher · View at Google Scholar
  45. V. Pazienza, M. Borghesan, T. Mazza et al., “SIRT1-metabolite binding histone macroH2A1.1 protects hepatocytes against lipid accumulation,” Aging, vol. 6, no. 1, pp. 35–47, 2014. View at Google Scholar · View at Scopus
  46. L. Serrano-Marco, M. R. Chacón, E. Maymó-Masip et al., “TNF-alpha inhibits PPARbeta/delta activity and SIRT1 expression through NF-kappaB in human adipocytes,” Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids, vol. 1821, no. 9, pp. 1177–1185, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Okazaki, Y. Iwasaki, M. Nishiyama et al., “PPARbeta/delta regulates the human SIRT1 gene transcription via Sp1,” Endocrine Journal, vol. 57, no. 5, pp. 403–413, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. L.-J. Sun, S.-C. Li, Y.-H. Zhao, J.-W. Yu, P. Kang, and B.-Z. Yan, “Silent information regulator 1 inhibition induces lipid metabolism disorders of hepatocytes and enhances hepatitis C virus replication,” Hepatology Research, vol. 43, no. 12, pp. 1343–1351, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. V. A. Payne, W.-S. Au, S. L. Gray et al., “Sequential regulation of diacylglycerol acyltransferase 2 expression by CAAT/enhancer-binding protein beta (C/EBPbeta) and C/EBPalpha during adipogenesis,” The Journal of Biological Chemistry, vol. 282, no. 29, pp. 21005–21014, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. M. Hoch, A. N. Eberle, R. Peterli et al., “LPS induces interleukin-6 and interleukin-8 but not tumor necrosis factor-α in human adipocytes,” Cytokine, vol. 41, no. 1, pp. 29–37, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Tous, R. Ferrer-Lorente, and L. Badimon, “Selective inhibition of sphingosine kinase-1 protects adipose tissue against LPS-induced inflammatory response in zucker diabetic fatty rats,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 307, no. 5, pp. E437–E446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. A. H. Berg, Y. Lin, M. P. Lisanti, and P. E. Scherer, “Adipocyte differentiation induces dynamic changes in NF-kappaB expression and activity,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 287, no. 6, pp. E1178–E1188, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Chung, K. LaPoint, K. Martinez, A. Kennedy, M. B. Sandberg, and M. K. McIntosh, “Preadipocytes mediate lipopolysaccharide-induced inflammation and insulin resistance in primary cultures of newly differentiated human adipocytes,” Endocrinology, vol. 147, no. 11, pp. 5340–5351, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. D. Langin, “Adipose tissue lipolysis as a metabolic pathway to define pharmacological strategies against obesity and the metabolic syndrome,” Pharmacological Research, vol. 53, no. 6, pp. 482–491, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. N. Stefan, K. Kantartzis, J. Machann et al., “Identification and characterization of metabolically benign obesity in humans,” Archives of Internal Medicine, vol. 168, no. 15, pp. 1609–1616, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. A. R. Nawrocki, M. W. Rajala, E. Tomas et al., “Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists,” The Journal of Biological Chemistry, vol. 281, no. 5, pp. 2654–2660, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J.-Y. Kim, E. van de Wall, M. Laplante et al., “Obesity-associated improvements in metabolic profile through expansion of adipose tissue,” Journal of Clinical Investigation, vol. 117, no. 9, pp. 2621–2637, 2007. View at Publisher · View at Google Scholar · View at Scopus