Effects of polyphenolic derivatives on heme oxygenase-system in metabolic dysfunctions

Current Medicinal Chemistry

Volumn 25, Issue 13, 2018, Pages 1577-1595

  Pittala, Valeria ^a   Vanella, Luca ^a   Salerno, Loredana ^a   Romeo, Giuseppe ^a   Marrazzo, Agostino ^a   Di Giacomo, Claudia ^a   Sorrenti, Valeria ^a  

^a UNIVERSITY OF CATANIA   (Italy)

Author keywords

Diabetes; HO 1; Metabolic syndrome; NAFLD; NASH; Nrf2; Oxidative stress; Polyphenols

Indexed keywords

ANTIOXIDANT; BIOFLAVONOID; CAFFEIC ACID; CAFFEIC ACID PHENETHYL ESTER; CARNOSIC ACID; CARNOSOL; COUMARIN DERIVATIVE; CURCUMIN; ELLAGIC ACID; EPIGALLOCATECHIN GALLATE; ESCULETIN; FRAXETIN; GENISTEIN; HEME OXYGENASE 1; ISOENZYME; POLYPHENOL DERIVATIVE; QUERCETIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; POLYPHENOL; REACTIVE OXYGEN METABOLITE;

ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; BIOLOGICAL ACTIVITY; CARDIOVASCULAR DISEASE; CHEMICAL STRUCTURE; DRUG MECHANISM; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; INFORMATION RETRIEVAL; METABOLIC SYNDROME X; NONHUMAN; REVIEW; ANIMAL; DRUG EFFECT; ENZYME INDUCTION; HUMAN; METABOLIC DISORDER; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS;

ANIMALS; ANTIOXIDANTS; CARDIOVASCULAR DISEASES; ENZYME INDUCTION; HEME OXYGENASE-1; HUMANS; METABOLIC DISEASES; METABOLIC SYNDROME; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; POLYPHENOLS; REACTIVE OXYGEN SPECIES;

EID: 85034778307     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867324666170616110748     Document Type: Review

References (139)

1. Eckel, R.H.; Grundy, S.M.; Zimmet, P.Z.; The metabolic syndrome. Lancet, 2005, 365(9468), 1415-1428.
2. Imrie, H.; Abbas, A.; Kearney, M.; Insulin resistance, lipotoxicity and endothelial dysfunction. Biochim. Biophys. Acta, 2010, 1801(3), 320-326.
3. Dulloo, A.G.; Antic, V.; Montani, J.P.; Ectopic fat stores: housekeepers that can overspill into weapons of lean body mass destruction. Int. J. Obes. Relat. Metab. Disord., 2004, 28 Suppl 4, S1-2.
4. Francque, S.; Laleman, W.; Verbeke, L.; Van Steenkiste, C.; Casteleyn, C.; Kwanten, W.; Van Dyck, C.; D'Hondt, M.; Ramon, A.; Vermeulen, W.; De Winter, B.; Van Marck, E.; Van Marck, V.; Pelckmans, P.; Michielsen, P.; Increased intrahepatic resistance in severe steatosis: endothelial dysfunction, vasoconstrictor overproduction and altered microvascular architecture. Lab. Invest., 2012, 92(10), 1428-1439.
5. Yaghootkar, H.; Scott, R.A.; White, C.C.; Zhang, W.; Speliotes, E.; Munroe, P.B.; Ehret, G.B.; Bis, J.C.; Fox, C.S.; Walker, M.; Borecki, I.B.; Knowles, J.W.; Yerges- Armstrong, L.; Ohlsson, C.; Perry, J.R.; Chambers, J.C.; Kooner, J.S.; Franceschini, N.; Langenberg, C.; Hivert, M.F.; Dastani, Z.; Richards, J.B.; Semple, R.K.; Frayling, T.M.; Genetic evidence for a normal-weight "metabolically obese" phenotype linking insulin resistance, hypertension, coronary artery disease, and type 2 diabetes. Diabetes, 2014, 63(12), 4369-4377.
6. Sobrevia, L.; Mann, G.E.; Dysfunction of the endothelial nitric oxide signalling pathway in diabetes and hyperglycaemia. Exp. Physiol., 1997, 82(3), 423-452.
7. Evans, J.L.; Goldfine, I.D.; Maddux, B.A.; Grodsky, G.M.; Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr. Rev., 2002, 23(5), 599-622.
8. Ceriello, A.; dello Russo, P.; Amstad, P.; Cerutti, P.; High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes, 1996, 45(4), 471-477.
9. Kubes, P.; Suzuki, M.; Granger, D.N.; Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl. Acad. Sci. USA, 1991, 88(11), 4651-4655.
10. De Caterina, R.; Libby, P.; Peng, H.B.; Thannickal, V.J.; Rajavashisth, T.B.; Gimbrone, M.A., Jr.; Shin, W.S.; Liao, J.K.; Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J. Clin. Invest., 1995, 96(1), 60-68.
11. Bianchi, C.; Miccoli, R.; Del Prato, S.; Hyperglycemia and vascular metabolic memory: truth or fiction? Curr. Diab. Rep., 2013, 13(3), 403-410.
12. Abraham, N.G.; Tsenovoy, P.L.; McClung, J.; Drummond, G.S.; Heme oxygenase: a target gene for anti-diabetic and obesity. Curr. Pharm. Des., 2008, 14(5), 412-421.
13. Maines, M.D.; Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J., 1988, 2(10), 2557-2568.
14. Abraham, N.G.; Kappas, A.; Pharmacological and clinical aspects of heme oxygenase. Pharmacol. Rev., 2008, 60(2), 242-242.
15. Goodman, A.I.; Chander, P.N.; Rezzani, R.; Schwartzman, M.L.; Regan, R.F.; Rodella, L.; Turkseven, S.; Lianos, E.A.; Dennery, P.A.; Abraham, N.G.; Heme oxygenase-2 deficiency contributes to diabetes-mediated increase in superoxide anion and renal dysfunction. J. Am. Soc. Nephrol., 2006, 17(4), 1073-1081.
16. Li Volti, G.; Rodella, L.F.; Di Giacomo, C.; Rezzani, R.; Bianchi, R.; Borsani, E.; Gazzolo, D.; Motterlini, R.; Role of carbon monoxide and biliverdin in renal ischemia/ reperfusion injury. Nephron. Exp. Nephrol., 2006, 104(4), e135-139.
17. Dong, H.; Huang, H.; Yun, X.; Kim, D.S.; Yue, Y.; Wu, H.; Sutter, A.; Chavin, K.D.; Otterbein, L.E.; Adams, D.B.; Kim, Y.B.; Wang, H.; Bilirubin increases insulin sensitivity in leptin-receptor deficient and diet-induced obese mice through suppression of ER stress and chronic inflammation. Endocrinol., 2014, 155(3), 818-828.
18. Stec, D. E.; John, K.; Trabbic, C. J.; Luniwal, A.; Hankins, M. W.; Baum, J.; Hinds, T. D.; Bilirubin Binding to PPAR alpha Inhibits Lipid Accumulation. PLoS One, 2016, 11(4), 1-17.
19. Otterbein, L.E.; Foresti, R.; Motterlini, R.; Heme Oxygenase-1 and Carbon Monoxide in the Heart: The Balancing Act Between Danger Signaling and Pro-Survival. Circ. Res., 2016, 118(12), 1940-1959.
20. Tibullo, D.; Barbagallo, I.; Giallongo, C.; Vanella, L.; Conticello, C.; Romano, A.; Saccone, S.; Godos, J.; Di Raimondo, F.; Li Volti, G.; Heme oxygenase-1 nuclear translocation regulates bortezomibinduced cytotoxicity and mediates genomic instability in myeloma cells. Oncotarget, 2016.
21. Vanella, L.; Li Volti, G.; Guccione, S.; Rappazzo, G.; Salvo, E.; Pappalardo, M.; Forte, S.; Schwartzman, M.L.; Abraham, N.G.; Heme oxygenase-2/adiponectin proteinprotein interaction in metabolic syndrome. Biochem. Biophys. Res. Commun., 2013, 432(4), 606-611.
22. Salerno, L.; Pittala, V.; Romeo, G.; Modica, M.N.; Marrazzo, A.; Siracusa, M.A.; Sorrenti, V.; Di Giacomo, C.; Vanella, L.; Parayath, N.N.; Greish, K.; Novel imidazole derivatives as heme oxygenase-1 (HO-1) and heme oxygenase-2 (HO-2) inhibitors and their cytotoxic activity in human- derived cancer cell lines. Eur. J. Med. Chem., 2015, 96, 162-172
23. Peterson, S.J.; Kim, D.H.; Li, M.; Positano, V.; Vanella, L.; Rodella, L.F.; Piccolomini, F.; Puri, N.; Gastaldelli, A.; Kusmic, C.; L'Abbate, A.; Abraham, N.G.; The L-4F mimetic peptide prevents insulin resistance through increased levels of HO-1, pAMPK, and pAKT in obese mice. J. Lipid Res., 2009, 50(7), 1293-1304.
24. Ndisang, J.F.; Lane, N.; Syed, N.; Jadhav, A.; Upregulating the heme oxygenase system with hemin improves insulin sensitivity and glucose metabolism in adult spontaneously hypertensive rats. Endocrinol., 2010, 151(2), 549-560.
25. Tiwari, S.; Ndisang, J.F.; The heme oxygenase system and type-1 diabetes. Curr. Pharm. Des., 2014, 20(9), 1328-1337.
26. Sorrenti, V.; Guccione, S.; Di Giacomo, C.; Modica, M.N.; Pittala, V.; Acquaviva, R.; Basile, L.; Pappalardo, M.; Salerno, L.; Evaluation of Imidazole-Based Compounds as Heme Oxygenase-1 Inhibitors. Chem. Biol. Drug Des., 2012, 80(6), 876-886.
27. Salerno, L.; Pittala, V.; Romeo, G.; Modica, M.N.; Siracusa, M.A.; Di Giacomo, C.; Acquaviva, R.; Barbagallo, I.; Tibullo, D.; Sorrenti, V.; Evaluation of novel aryloxyalkyl derivatives of imidazole and 1,2,4-triazole as heme oxygenase- 1 (HO-1) inhibitors and their antitumor properties. Bioorg. Med. Chem., 2013, 21(17), 5145-5153.
28. Rucker, H.; Amslinger, S.; Identification of heme oxygenase-1 stimulators by a convenient ELISA-based bilirubin quantification assay. Free Rad. Biol. Med., 2015, 78, 135-146.
29. Vanella, L.; Di Giacomo, C.; Acquaviva, R.; Barbagallo, I.; Li Volti, G.; Cardile, V.; Abraham, N.G.; Sorrenti, V.; Effects of ellagic Acid on angiogenic factors in prostate cancer cells. Cancers, 2013, 5(2), 726-738.
30. Alam, J.; Stewart, D.; Touchard, C.; Boinapally, S.; Choi, A.M.; Cook, J.L.; Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem., 1999, 274(37), 26071-26078.
31. Park, S.H.; Jang, J.H.; Li, M.H.; Na, H.K.; Cha, Y.N.; Surh, Y.J.; Nrf2-mediated heme oxygenase-1 induction confers adaptive survival response to tetrahydropapaverolineinduced oxidative PC12 cell death. Antiox. Red. Sign., 2007, 9(12), 2075-2086.
32. Jimenez-Osorio, A.S.; Gonzalez-Reyes, S.; Garcia-Nino, W.R.; Moreno-Macias, H.; Rodriguez-Arellano, M.E.; Vargas-Alarcon, G.; Zuniga, J.; Barquera, R.; Pedraza-Chaverri, J.; Association of Nuclear Factor-Erythroid 2- Related Factor 2, Thioredoxin Interacting Protein, and Heme Oxygenase-1 Gene Polymorphisms with Diabetes and Obesity in Mexican Patients. Oxid. Med. Cell Longev., 2016, 2016, 7367641.
33. Yang, Y.C.; Lii, C.K.; Lin, A.H.; Yeh, Y.W.; Yao, H.T.; Li, C.C.; Liu, K.L.; Chen, H.W.; Induction of glutathione synthesis and heme oxygenase 1 by the flavonoids butein and phloretin is mediated through the ERK/Nrf2 pathway and protects against oxidative stress. Free Rad. Biol. Med., 2011, 51(11), 2073-2081.
34. Cheng, X.; Ku, C.H.; Siow, R.C.; Regulation of the Nrf2 antioxidant pathway by microRNAs: New players in micromanaging redox homeostasis. Free Rad. Biol. Med., 2013, 64, 4-11.
35. Do, M.T.; Kim, H.G.; Choi, J.H.; Jeong, H.G.; Metformin induces microRNA-34a to downregulate the Sirt1/Pgc-1alpha/Nrf2 pathway, leading to increased susceptibility of wild-type p53 cancer cells to oxidative stress and therapeutic agents. Free Rad. Biol. Med., 2014, 74, 21-34.
36. Xiao, S.; Wang, X.; Ni, H.; Li, N.; Zhang, A.; Liu, H.; Pu, F.; Xu, L.; Gao, J.; Zhao, Q.; Mu, Y.; Wang, C.; Sun, Y.; Du, T.; Xu, X.; Zhang, G.; Hiscox, J.A.; Goodfellow, I.G.; Zhou, E.M.; MicroRNA miR-24-3p promotes porcine reproductive and respiratory syndrome virus replication through suppression of heme oxygenase-1 expression. J. Virol., 2015, 89(8), 4494-4503.
37. Fiedler, J.; Stohr, A.; Gupta, S.K.; Hartmann, D.; Holzmann, A.; Just, A.; Hansen, A.; Hilfiker-Kleiner, D.; Eschenhagen, T.; Thum, T.; Functional microRNA library screening identifies the hypoxamir miR-24 as a potent regulator of smooth muscle cell proliferation and vascularization. Antiox. Red. Sign., 2014, 21(8), 1167-1176.
38. Skrzypek, K.; Tertil, M.; Golda, S.; Ciesla, M.; Weglarczyk, K.; Collet, G.; Guichard, A.; Kozakowska, M.; Boczkowski, J.; Was, H.; Gil, T.; Kuzdzal, J.; Muchova, L.; Vitek, L.; Loboda, A.; Jozkowicz, A.; Kieda, C.; Dulak, J.; Interplay between heme oxygenase-1 and miR-378 affects non-small cell lung carcinoma growth, vascularization, and metastasis. Antiox. Red. Sign., 2013, 19(7), 644-660.
39. Tyagi, S.; Gupta, P.; Saini, A.S.; Kaushal, C.; Sharma, S.; The peroxisome proliferator-activated receptor: A family of nuclear receptors role in various diseases. J. Adv. Pharm. Technol. Res., 2011, 2(4), 236-240.
40. Wang, X.; Wang, Z.; Liu, J.Z.; Hu, J.X.; Chen, H.L.; Li, W.L.; Hai, C.X.; Double antioxidant activities of rosiglitazone against high glucose-induced oxidative stress in hepatocyte. Toxicol. in Vitro, 2011, 25(4), 839-847.
41. Nicolai, A.; Li, M.; Kim, D.H.; Peterson, S.J.; Vanella, L.; Positano, V.; Gastaldelli, A.; Rezzani, R.; Rodella, L.F.; Drummond, G.; Kusmic, C.; L'Abbate, A.; Kappas, A.; Abraham, N.G.; Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesityinduced diabetic rats. Hypertension, 2009, 53(3), 508-515.
42. Salley, T.N.; Mishra, M.; Tiwari, S.; Jadhav, A.; Ndisang, J.F.; The heme oxygenase system rescues hepatic deterioration in the condition of obesity co-morbid with type-2 diabetes. PLoS One, 2013, 8(11), e79270.
43. Ndisang, J.F.; Jadhav, A.; Mishra, M.; The heme oxygenase system suppresses perirenal visceral adiposity, abates renal inflammation and ameliorates diabetic nephropathy in Zucker diabetic fatty rats. PLoS One, 2014, 9(1), e87936.
44. Abraham, N.G.; Rezzani, R.; Rodella, L.; Kruger, A.; Taller, D.; Li Volti, G.; Goodman, A.I.; Kappas, A.; Overexpression of human heme oxygenase-1 attenuates endothelial cell sloughing in experimental diabetes. Am. J. Physiol. Heart Circ. Physiol., 2004, 287(6), H2468-2477.
45. Tu, T.H.; Joe, Y.; Choi, H.S.; Chung, H.T.; Yu, R.; Induction of heme oxygenase-1 with hemin reduces obesityinduced adipose tissue inflammation via adipose macrophage phenotype switching. Mediators Inflamm., 2014, 2014, 290708.
46. Joe, Y.; Zheng, M.; Kim, S.K.; Kim, S.; Uddin, J.M.; Min, T.S.; Ryu, D.G.; Chung, H.T.; The role of carbon monoxide in metabolic disease. Ann. N. Y. Acad. Sci., 2011, 1229, 156-161.
47. Lancel, S.; Montaigne, D.; Marechal, X.; Marciniak, C.; Hassoun, S.M.; Decoster, B.; Ballot, C.; Blazejewski, C.; Corseaux, D.; Lescure, B.; Motterlini, R.; Neviere, R.; Carbon monoxide improves cardiac function and mitochondrial population quality in a mouse model of metabolic syndrome. PLoS One, 2012, 7(8), e41836.
48. Hosick, P.A.; AlAmodi, A.A.; Storm, M.V.; Gousset, M.U.; Pruett, B.E.; Gray, W., 3rd; Stout, J.; Stec, D.E.; Chronic carbon monoxide treatment attenuates development of obesity and remodels adipocytes in mice fed a high-fat diet. Int. J. Obes., 2014, 38(1), 132-139.
49. Cao, J.; Peterson, S.J.; Sodhi, K.; Vanella, L.; Barbagallo, I.; Rodella, L.F.; Schwartzman, M.L.; Abraham, N.G.; Kappas, A.; Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet. Hypertension, 2012, 60(2), 467-475.
50. Tiwari, S.; Ndisang, J.F.; Heme oxygenase system and hypertension: a comprehensive insight. Curr. Pharm. Des., 2014, 20(9), 1354-1369.
51. Ndisang, J.F.; Chibbar, R.; Heme Oxygenase Improves Renal Function by Potentiating Podocyte-Associated Proteins in Nomega-Nitro-l-Arginine-Methyl Ester (l-NAME)- Induced Hypertension. Am. J. Hypertens., 2015, 28(7), 930-942.
52. Li, N.; Yi, F.; dos Santos, E.A.; Donley, D.K.; Li, P.L.; Role of renal medullary heme oxygenase in the regulation of pressure natriuresis and arterial blood pressure. Hypertension, 2007, 49(1), 148-154.
53. Loboda, A.; Damulewicz, M.; Pyza, E.; Jozkowicz, A.; Dulak, J.; Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol. Life Sci., 2016, 73(17), 3221-4.
54. Shen, Y.; Ward, N.C.; Hodgson, J.M.; Puddey, I.B.; Wang, Y.; Zhang, D.; Maghzal, G.J.; Stocker, R.; Croft, K.D.; Dietary quercetin attenuates oxidant-induced endothelial dysfunction and atherosclerosis in apolipoprotein E knockout mice fed a high-fat diet: a critical role for heme oxygenase-1. Free Rad. Biol. Med., 2013, 65, 908-915.
55. Barbagallo, I.; Galvano, F.; Frigiola, A.; Cappello, F.; Riccioni, G.; Murabito, P.; D'Orazio, N.; Torella, M.; Gazzolo, D.; Volti, G.L.; Potential Therapeutic Effects of Natural Heme Oxygenase-1 Inducers in Cardiovascular Diseases. Antiox. Red. Sign., 2013, 18(5), 507-521.
56. Firn, R.D.; Jones, C.G.; Natural products - a simple model to explain chemical diversity. Nat. Prod. Rep., 2003, 20(4), 382-391.
57. Mennen, L.I.; Walker, R.; Bennetau-Pelissero, C.; Scalbert, A.; Risks and safety of polyphenol consumption. Am. J. Clin. Nutr., 2005, 81(1), 326s-329s.
58. Nabavi, S.M.; Daglia, M.; Sureda, A.; Dietary Polyphenols: Well beyond the Antioxidant Capacity (Part I). Curr. Pharm. Biotechnol., 2014, 15(4), 297-297.
59. Fernandez-Garcia, J.C.; Cardona, F.; Tinahones, F.J.; Inflammation, Oxidative Stress and Metabolic Syndrome: Dietary Modulation. Curr. Vasc. Pharmacol., 2013, 11(6), 906-919.
60. Martinez-Gonzalez, M.A.; Martin-Calvo, N.; The major European dietary patterns and metabolic syndrome. Rev. End. Met. Dis., 2013, 14(3), 265-271.
61. Cicero, A.F.; Colletti, A.; Role of phytochemicals in the management of metabolic syndrome. Phytomed., 2016, 23(11), 1134-44.
62. Saso, L.; Firuzi, O.; Pharmacological Applications of Antioxidants: Lights and Shadows. Curr. Drug Targ., 2014, 15(13), 1177-1199.
63. Pittala, V.; Salerno, L.; Romeo, G.; Modica, M.N.; Siracusa, M.A.; A Focus on Heme Oxygenase-1 (HO-1) Inhibitors. Curr. Med. Chem., 2013, 20(30), 3711-3732.
64. Dennery, P.A.; Signaling Function of Heme Oxygenase Proteins. Antiox. Red. Sign., 2014, 20(11), 1743-1753.
65. Abraham, N.G.; Junge, J.M.; Drummond, G.S.; Translational Significance of Heme Oxygenase in Obesity and Metabolic Syndrome. Trends Pharmacol. Sci., 2016, 37(1), 17-36.
66. Milobedzka, J.; Kostanecki, S.; Lampe, V.; Zur Kenntnis des Curcumins. Deut. Chem. Ges., 1910, 43, 2163-2170.
67. Payton, F.; Sandusky, P.; Alworth, W.L.; NMR study of the solution structure of curcumin. J. Nat. Prod., 2007, 70(2), 143-146.
68. Nabavi, S.F.; Thiagarajan, R.; Rastrelli, L.; Daglia, M.; Sobarzo-Sanchez, E.; Alinezhad, H.; Nabavi, S.M.; Curcumin: A Natural Product for Diabetes and its Complications. Curr. Top. Med. Chem., 2015, 15(23), 2445-2455.
69. Sahebkar, A.; Why it is necessary to translate curcumin into clinical practice for the prevention and treatment of metabolic syndrome? Biofactors, 2013, 39(2), 197-208.
70. Shehzad, A.; Lee, Y.S.; Molecular mechanisms of curcumin action: signal transduction. Biofactors, 2013, 39(1), 27-36.
71. Motterlini, R.; Foresti, R.; Bassi, R.; Green, C.J.; Curcumin, an antioxidant and anti-inflammatory agent, induces heme oxygenase-1 and protects endothelial cells against oxidative stress. Free Rad. Biol. Med., 2000, 28(8), 1303-1312.
72. Jeong, G.S.; Oh, G.S.; Pae, H.O.; Jeong, S.O.; Kim, Y.C.; Shin, M.K.; Seo, B.Y.; Han, S.Y.; Lee, H.S.; Jeong, J.G.; Koh, J.S.; Chung, H.T.; Comparative effects of curcuminoids on endothelial heme oxygenase-1 expression: orthomethoxy groups are essential to enhance heme oxygenase activity and protection. Exp. Mol. Med., 2006, 38(4), 393-400.
73. Pugazhenthi, S.; Akhov, L.; Selvaraj, G.; Wang, M.; Alam, J.; Regulation of heme oxygenase-1 expression by demethoxy curcuminoids through Nrf2 by a PI3-kinase/Aktmediated pathway in mouse beta-cells. Am. J. Physiol. Endocrinol. Metab., 2007, 293(3), E645-E655.
74. Kanitkar, M.; Bhonde, R.R.; Curcumin treatment enhances islet recovery by induction of heat shock response proteins, Hsp70 and heme oxygenase-1, during cryopreservation. Life Sci., 2008, 82(3-4), 182-189.
75. Rashid, K.; Sil, P.C.; Curcumin enhances recovery of pancreatic islets from cellular stress induced inflammation and apoptosis in diabetic rats. Toxicol. Appl. Pharmacol., 2015, 282(3), 297-310.
76. Brownlee, M.; Biochemistry and molecular cell biology of diabetic complications. Nature, 2001, 414(6865), 813-820.
77. Hassan, N.; El-Bassossy, H.M.; Zakaria, M.N.; Heme oxygenase- 1 induction protects against hypertension associated with diabetes: effect on exaggerated vascular contractility. N-S. Arch. Pharmacol., 2013, 386(3), 217-226.
78. El-Bassossy, H.M.; Hassan, N.; Zakaria, M.N.; Heme oxygenase- 1 alleviates vascular complications associated with metabolic syndrome: Effect on endothelial dependent relaxation and NO production. Chem. Biol. Interact., 2014, 223C, 109-115.
79. Zhang, X.; Liang, D.; Guo, L.; Liang, W.; Jiang, Y.; Li, H.; Zhao, Y.; Lu, S.; Chi, Z.H.; Curcumin protects renal tubular epithelial cells from high glucose-induced epithelial-tomesenchymal transition through Nrf2-mediated upregulation of heme oxygenase-1. Mol. Med. Rep., 2015, 12(1), 1347-1355.
80. Akbik, D.; Ghadiri, M.; Chrzanowski, W.; Rohanizadeh, R.; Curcumin as a wound healing agent. Life Sci., 2014, 116(1), 1-7.
81. Kant, V.; Gopal, A.; Kumar, D.; Pathak, N.N.; Ram, M.; Jangir, B.L.; Tandan, S.K.; Kumar, D.; Curcumin-induced angiogenesis hastens wound healing in diabetic rats. J. Surg. Res., 2015, 193(2), 978-988.
82. Lundvig, D.M.; Pennings, S.W.; Brouwer, K.M.; Mtaya- Mlangwa, M.; Mugonzibwa, E.; Kuijpers-Jagtman, A.M.; Wagener, F.A.; Von den Hoff, J.W.; Cytoprotective responses in HaCaT keratinocytes exposed to high doses of curcumin. Exp. Cell. Res., 2015, 336(2), 298-307.
83. Jais, A.; Einwallner, E.; Sharif O.; Gossens, K.; Lu T.T.; Soyal, S.M.; Medgyesi, D.; Neureiter, D.; Paier-Pourani, J.; Dalgaard, K.; Duvigneau, J.C.; Lindroos-Christensen, J.; Zapf, T.C.; Amann, S.; Saluzzo, S.; Jantscher, F.; Stiedl P.; Todoric, J.; Martins, R.; Oberkofler, H.; Müller, S.; Hauser- Kronberger C.; Kenner, L.; Casanova, E.; Sutterlüty-Fall, H.; Bilban, M.; Miller, K.;, Kozlov, A.V.; Krempler, F.; Knapp, S.; Lumeng, C.N.; Patsch, W.; Wagner, O.; Pospisilik, J.A.; Esterbauer, H.; Heme Oxygenase-1 Drives Metaflammation and Insulin Resistance in Mouse and Man. Cell, 2014, 158(1), 25-40.
84. He, H.J.; Wang, G.Y.; Gao, Y.; Ling, W.H.; Yu, Z.W.; Jin, T.R.; Curcumin attenuates Nrf2 signaling defect, oxidative stress in muscle and glucose intolerance in high fat diet-fed mice. World J. Diabetes, 2012, 3(5), 94-104.
85. Shao, W.; Yu, Z.; Chiang, Y.; Yang, Y.; Chai, T.; Foltz, W.; Lu, H.; Fantus, I.G.; Jin, T.; Curcumin prevents high fat diet induced insulin resistance and obesity via attenuating lipogenesis in liver and inflammatory pathway in adipocytes. PLoS One, 2012, 7(1), e28784.
86. Zeng, C.; Zhong, P.; Zhao, Y.; Kanchana, K.; Zhang, Y.; Khan, Z.A.; Chakrabarti, S.; Wu, L.; Wang, J.; Liang, G.; Curcumin protects hearts from FFA-induced injury by activating Nrf2 and inactivating NF-kappaB both in vitro and in vivo. J. Mol. Cell Cardiol., 2015, 79, 1-12.
87. Qian, Y.; Zhong, P.; Liang, D.; Xu, Z.; Skibba, M.; Zeng, C.; Li, X.; Wei, T.; Wu, L.; Liang, G.; A newly designed curcumin analog Y20 mitigates cardiac injury via antiinflammatory and anti-oxidant actions in obese rats. PLoS One, 2015, 10(3), e0120215.
88. Prasad, S.; Tyagi, A.K.; Aggarwal, B.B.; Recent developments in delivery, bioavailability, absorption and metabolism of curcumin: the golden pigment from golden spice. Cancer Res. Treat., 2014, 46(1), 2-18.
89. Modica, M.N.; Pittala, V.; Romeo, G.; Salerno, L.; Siracusa, M.A.; Serotonin 5-HT3 and 5-HT4 ligands: an update of medicinal chemistry research in the last few years. Curr. Med. Chem., 2010, 17(4), 334-362.
90. Abdel Aziz, M.T.; El-Asmar, M.F.; El-Ibrashy, I.N.; Rezq, A.M.; Al-Malki, A.L.; Wassef, M.A.; Fouad, H.H.; Ahmed, H.H.; Taha, F.M.; Hassouna, A.A.; Morsi, H.M.; Effect of novel water soluble curcumin derivative on experimental type- 1 diabetes mellitus (short term study). Diabetol. Metab. Syndr., 2012, 4(1), 30.
91. D'Andrea, G.; Quercetin: A flavonol with multifaceted therapeutic applications? Fitoterapia, 2015, 106, 256-271.
92. Leo, C.H.; Woodman, O.L.; Flavonols in the Prevention of Diabetes-induced Vascular Dysfunction. J. Cardiovasc. Pharmacol., 2015, 65(6), 532-544.
93. Mukhopadhyay, P.; Prajapati, A.K.; Quercetin in antidiabetic research and strategies for improved quercetin bioavailability using polymer-based carriers - a review. Rsc Adv., 2015, 5(118), 97547-97562.
94. Costa, L.G.; Garrick, J.M.; Roque, P.J.; Pellacani, C.; Mechanisms of Neuroprotection by Quercetin: Counteracting Oxidative Stress and More. Oxid. Med. Cell Longev., 2016, 2016, 2986796.
95. Panchal, S.K.; Poudyal, H.; Brown, L.; Quercetin ameliorates cardiovascular, hepatic, and metabolic changes in dietinduced metabolic syndrome in rats. J. Nutr., 2012, 142(6), 1026-1032.
96. Shi, Y.; Liang, X.C.; Zhang, H.; Wu, Q.L.; Qu, L.; Sun, Q.; Quercetin protects rat dorsal root ganglion neurons against high glucose-induced injury in vitro through Nrf-2/HO-1 activation and NF-kappaB inhibition. Acta Pharmacol. Sin., 2013, 34(9), 1140-1148.
97. Kim, C.S.; Kwon, Y.; Choe, S.Y.; Hong, S.M.; Yoo, H.; Goto, T.; Kawada, T.; Choi, H.S.; Joe, Y.; Chung, H.T.; Yu, R.; Quercetin reduces obesity-induced hepatosteatosis by enhancing mitochondrial oxidative metabolism via heme oxygenase-1. Nutr. Metab., 2015, 12.
98. Ann, J.Y.; Eo, H.; Lim, Y.; Mulberry leaves (Morus alba L.) ameliorate obesity-induced hepatic lipogenesis, fibrosis, and oxidative stress in high-fat diet-fed mice. Genes Nutr., 2015, 10(6).
99. Legeay, S.; Rodier, M.; Fillon, L.; Faure, S.; Clere, N.; Epigallocatechin Gallate: A Review of Its Beneficial Properties to Prevent Metabolic Syndrome. Nutrients, 2015, 7(7), 5443-5468.
100. Wu, C.C.; Hsu, M.C.; Hsieh, C.W.; Lin, J.B.; Lai, P.H.; Wung, B.S.; Upregulation of heme oxygenase-1 by epigallocatechin- 3-gallate via the phosphatidylinositol 3- kinase/Akt and ERK pathways. Life Sci., 2006, 78(25), 2889-2897.
101. Andreadi, C.K.; Howells, L.M.; Atherfold, P.A.; Manson, M.M.; Involvement of Nrf2, p38, B-Raf, and nuclear factorkappa B, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols. Mol. Pharmacol., 2006, 69(3), 1033-1040.
102. Romeo, L.; Intrieri, M.; D'Agata, V.; Mangano, N.G.; Oriani, G.; Ontario, M.L.; Scapagnini, G.; The Major Green Tea Polyphenol, (-)-Epigallocatechin-3-Gallate, Induces Heme Oxygenase in Rat Neurons and Acts as an Effective Neuroprotective Agent against Oxidative Stress. J. Am. College Nutr., 2009, 28(4), 492s-499s.
103. Liu, J.; Tang, Y.; Feng, Z.; Long, J.; (-)-Epigallocatechin-3- gallate attenuated myocardial mitochondrial dysfunction and autophagy in diabetic Goto-Kakizaki rats. Free Rad. Res., 2014, 48(8), 898-906.
104. Sampath, C.; Zhu, Y.D.; Sang, S.M.; Ahmedna, M.; Bioactive compounds isolated from apple, tea, and ginger protect against dicarbonyl induced stress in cultured human retinal epithelial cells. Phytomedicine, 2016, 23(2), 200-213.
105. Baker, W.; Robinson, R. CCCLIX.—Synthetical experiments in the isoflavone group. Part II. A synthesis of methylgenistein (methylprunetol) dimethyl ether and the constitution of prunetol (genistein). J. Chem. Soc., 1926, 129, 2713-2720.
106. Gilbert, E.R.; Liu, D.M.; Anti-diabetic functions of soy isoflavone genistein: mechanisms underlying its effects on pancreatic beta-cell function. Food Funct., 2013, 4(2), 200-212.
107. Zhai, X.; Lin, M.; Zhang, F.; Hu, Y.; Xu, X.; Li, Y.; Liu, K.; Ma, X.; Tian, X.; Yao, J.; Dietary flavonoid genistein induces Nrf2 and phase II detoxification gene expression via ERKs and PKC pathways and protects against oxidative stress in Caco-2 cells. Mol. Nutr. Food Res., 2013, 57(2), 249-259.
108. Bloedon, L.T.; Jeffcoat, A.R.; Lopaczynski, W.; Schell, M.J.; Black, T.M.; Dix, K.J.; Thomas, B.F.; Albright, C.; Busby, M.G.; Crowell, J.A.; Zeisel, S.H.; Safety and pharmacokinetics of purified soy isoflavones: single-dose administration to postmenopausal women. Am. J. Clin. Nutr., 2002, 76(5), 1126-1137.
109. Busby, M.G.; Jeffcoat, A.R.; Bloedon, L.T.; Koch, M.A.; Black, T.; Dix, K.J.; Heizer, W.D.; Thomas, B.F.; Hill, J.M.; Crowell, J.A.; Zeisel, S.H.; Clinical characteristics and pharmacokinetics of purified soy isoflavones: singledose administration to healthy men. Am. J. Clin. Nutr., 2002, 75(1), 126-136.
110. Zhang, T.; Wang, F.; Xu, H.X.; Yi, L.; Qin, Y.; Chang, H.; Mi, M.T.; Zhang, Q.Y.; Activation of nuclear factor erythroid 2-related factor 2 and PPAR gamma plays a role in the genistein-mediated attenuation of oxidative stressinduced endothelial cell injury. Br. J. Nutr., 2013, 109(2), 223-235.
111. Kim, M.J.; Lim, Y.; Protective Effect of Short-Term Genistein Supplementation on the Early Stage in Diabetes- Induced Renal Damage. Med. Infl., 2013, 2013, 510212.
112. Jeon, S.; Park, Y.J.; Kwon, Y.H.; Genistein alleviates the development of nonalcoholic steatohepatitis in ApoE-/- mice fed a high- fat diet. Mol. Nutr. Food Res., 2014, 58(4), 830-841.
113. Jaikang, C.; Chaiyasut, C.; Caffeic acid and its derivatives as heme oxygenase 1 inducer in Hep G2 cell line. J. Med. Plants Res., 2010, 4(10), 940-946.
114. Guo, X.; Shen, L.; Tong, Y.H.; Zhang, J.; Wu, G.; He, Q.; Yu, S.R.; Ye, X.W.; Zou, L.B.; Zhang, Z.Z.; Lian, X.Y.; Antitumor activity of caffeic acid 3,4-dihydroxyphenethyl ester and its pharmacokinetic and metabolic properties. Phytomedicine, 2013, 20(10), 904-912.
115. Bhattacharya, S.; Christensen, K.B.; Olsen, L.C.B.; Christensen, L.P.; Grevsen, K.; Faergeman, N.J.; Kristiansen, K.; Young, J.F.; Oksbjerg, N.; Bioactive components from flowers of sambucus nigra l. increase glucose uptake in primary porcine myotube cultures and reduce fat accumulation in Caenorhabditis elegans. J. Agric. Food Chem., 2013, 61(46), 11033-11040.
116. Cruz, L.C.; Ecker, A.; Dias, R.S.; Seeger, R.L.; Braga, M.M.; Boligon, A.A.; Martins, I.K.; Costa-Silva, D.G.; Barbosa, N.V.; Canedo, A.D.; Posser, T.; Franco, J.L.; Brazilian pampa biome honey protects against mortality, locomotor deficits and oxidative stress induced by hypoxia/ reperfusion in Adult Drosophila melanogaster. Neurochem. Res., 2016, 41(1-2), 116-129.
117. Viuda-Martos, M.; Ruiz-Navajas, Y.; Fernandez-Lopez, J.; Perez-Alvarez, J.A.; Functional properties of honey, propolis, and royal jelly. J. Food Sci., 2008, 73(9), R117-124.
118. Kim, J.K.; Jang, H.D.; Nrf2-mediated HO-1 induction coupled with the ERK signaling pathway contributes to indirect antioxidant capacity of caffeic acid phenethyl ester in HepG2 cells. Int. J. Mol. Sci., 2014, 15(7), 12149-12165.
119. Lee, Y.; Shin, D.H.; Kim, J.H.; Hong, S.; Choi, D.; Kim, Y.J.; Kwak, M.K.; Jung, Y.; Caffeic acid phenethyl estermediated Nrf2 activation and IkappaB kinase inhibition are involved in NFkappaB inhibitory effect: structural analysis for NFkappaB inhibition. Eur. J. Pharmacol., 2010, 643(1), 21-28.
120. Pittalà, V.; Salerno, L.; Romeo, G.; Acquaviva, R.; Di Giacomo, C.; Sorrenti, V. Therapeutic Potential of Caffeic Acid Phenethyl Ester (CAPE) in Diabetes. Curr. Med. Chem., 2016, 24, DOI: 10.2174/0929867324666161118120908.
121. Hassan, N.A.; El-Bassossy, H.M.; Mahmoud, M.F.; Fahmy, A.; Caffeic acid phenethyl ester, a 5-lipoxygenase enzyme inhibitor, alleviates diabetic atherosclerotic manifestations: effect on vascular reactivity and stiffness. Chem. Biol. Interact., 2014, 213, 28-36.
122. Wang, X.; Stavchansky, S.; Zhao, B.; Bynum, J.A.; Kerwin, S.M.; Bowman, P.D.; Cytoprotection of human endothelial cells from menadione cytotoxicity by caffeic acid phenethyl ester: the role of heme oxygenase-1. Eur. J. Pharmacol., 2008, 591(1-3), 28-35.
123. Medina, F.G.; Marrero, J.G.; Macias-Alonso, M.; Gonzalez, M.C.; Cordova-Guerrero, I.; Teissier Garcia, A.G.; Osegueda- Robles, S.; Coumarin heterocyclic derivatives: Chemical synthesis and biological activity. Nat. Prod. Rep., 2015, 32(10), 1472-1507.
124. Grover, J.; Jachak, S.M.; Coumarins as privileged scaffold for anti-inflammatory drug development. Rsc Adv., 2015, 5(49), 38892-38905.
125. Thuong, P.T.; Pokharel, Y.R.; Lee, M.Y.; Kim, S.K.; Bae, K.; Su, N.D.; Oh, W.K.; Kang, K.W.; Dual Anti-oxidative Effects of Fraxetin Isolated from Fraxinus rhinchophylla. Biol. Pharm. Bull., 2009, 32(9), 1527-1532.
126. Kim, Y.; Park, Y.; Namkoong, S.; Lee, J.; Esculetin inhibits the inflammatory response by inducing heme oxygenase-1 in cocultured macrophages and adipocytes. Food Funct., 2014, 5(9), 2371-2377.
127. Brieskorn, C.H.; Fuchs., A.; Brendenberg, J.B.; McChesney, J.D.; Wenkert, E.; The Structure of Carnosol. J. Org. Chem., 1964, 29, 2293–2298.
128. Satoh, T.; McKercher, S.R.; Lipton, S.A.; Nrf2/AREmediated antioxidant actions of pro-electrophilic drugs. Free Rad. Biol. Med., 2013, 65, 645-657.
129. Martin, D.; Rojo, A.I.; Salinas, M.; Diaz, R.; Gallardo, G.; Alam, J.; De Galarreta, C.M.; Cuadrado, A.; Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J. Biol. Chem., 2004, 279(10), 8919-8929.
130. Lian, K.C.; Chuang, J.J.; Hsieh, C.W.; Wung, B.S.; Huang, G.D.; Jian, T.Y.; Sun, Y.W.; Dual mechanisms of NFkappaB inhibition in carnosol-treated endothelial cells. Toxicol. Appl. Pharmacol., 2010, 245(1), 21-35.
131. Foresti, R.; Bucolo, C.; Platania, C.M.; Drago, F.; Dubois- Rande, J.L.; Motterlini, R.; Nrf2 activators modulate oxidative stress responses and bioenergetic profiles of human retinal epithelial cells cultured in normal or high glucose conditions. Pharmacol. Res., 2015, 99, 296-307.
132. Gu, L.; Deng, W.S.; Liu, Y.; Jiang, C.H.; Sun, L.C.; Sun, X.F.; Xu, Q.; Zhou, H.; Ellagic acid protects Lipopolysaccharide/ D-galactosamine-induced acute hepatic injury in mice. Int. Immunopharmacol., 2014, 22(2), 341-345.
133. Ding, Y.; Zhang, B.; Zhou, K.; Chen, M.; Wang, M.; Jia, Y.; Song, Y.; Li, Y.; Wen, A.; Dietary ellagic acid improves oxidant-induced endothelial dysfunction and atherosclerosis: role of Nrf2 activation. Int. J. Cardiol., 2014, 175(3), 508-514.
134. Waltenberger, B.; Mocan, A.; Šmejkal, K.; Heiss, E.H.; Atanasov, A.G.; Natural products to counteract the epidemic of cardiovascular and metabolic disorders. Molecules, 2016, 21(6), 1-33.
135. Vacca, R.A.; Valenti, D.; Caccamese, S.; Daglia, M.; Braidy, N.; Nabavi, S.M.; Plant polyphenols as natural drugs for the management of Down syndrome and related disorders. Neurosci. Biobehav. Rev., 2016, 71, 865-877.
136. D’Archivio, M.; Filesi, C.; Varì, R.; Scazzocchio, B.; Masella, R.; Bioavailability of the Polyphenols: Status and Controversies. Int. J. Mol. Sci., 2010, 11(4), 1321–1342.
137. Manach, C.; Scalbert, A.; Morand, C.; Christian Rémésy, and Liliana Jiménez Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr., 2004, 79, 727–47.
138. Barreca, D.; Bellocco, E.; D'Onofrio, G.; Nabavi, S.F.; Daglia, M.; Rastrelli, L.; Nabavi, S.M.; Neuroprotective Effects of Quercetin: From Chemistry to Medicine. CNS Neurol. Dis. Drug Targets, 2016, 15, 964-975.
139. Habauzit, V.; Morand, C.; Evidence for a protective effect of polyphenols-containing foods on cardiovascular health: an update for clinicians. Ther. Adv. Chronic. Dis., 2012, 3(2), 87-106.