Broccoli sprout extract prevents diabetic cardiomyopathy via Nrf2 activation in db/db T2DM mice

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Xu, Zheng ^a,b   Wang, Shudong ^a,b   Ji, Honglei ^a   Zhang, Zhiguo ^a   Chen, Jing ^b   Tan, Yi ^b,c   Wintergerst, Kupper ^b,c   Zheng, Yang ^a   Sun, Jian ^a   Cai, Lu ^b,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOTHIOCYANIC ACID DERIVATIVE; NFE2L2 PROTEIN, MOUSE; PLANT EXTRACT; SULFORAFAN; TRANSCRIPTION FACTOR NRF2;

AGONISTS; ANIMAL; BRASSICA; CHEMISTRY; DIABETIC CARDIOMYOPATHY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONOBESE DIABETIC MOUSE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOLOGY;

ANIMALS; BRASSICA; DIABETES MELLITUS, TYPE 2; DIABETIC CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; ISOTHIOCYANATES; MICE; MICE, INBRED NOD; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT EXTRACTS;

EID: 84979530422     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep30252     Document Type: Article

References (52)

1. Amos, A. F., McCarty, D. J. & Zimmet, P. The rising global burden of diabetes and its complications: estimates and projections to the year 2010. Diabet Med. 14 Suppl 5, S1-S85 (1997).
2. Boudina, S. & Abel, E. D. Diabetic cardiomyopathy revisited. Circulation. 115, 3213-3223 (2007).
3. Monkemann, H. et al. Early molecular events in the development of the diabetic cardiomyopathy. Amino Acids. 23, 331-336 (2002).
4. Cai, L. & Kang, Y. J. Oxidative stress and diabetic cardiomyopathy: a brief review. Cardiovasc Toxicol. 1, 181-193 (2001).
5. Hamblin, M. et al. Alterations in the diabetic myocardial proteome coupled with increased myocardial oxidative stress underlies diabetic cardiomyopathy. J Mol Cell Cardiol. 42, 884-895 (2007).
6. Cai, L. et al. Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol. 48, 1688-1697 (2006).
7. Adeghate, E. Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol Cell Biochem. 261, 187-191 (2004).
8. Chen, Y., Saari, J. T. & Kang, Y. J. Weak antioxidant defenses make the heart a target for damage in copper-deficient rats. Free Radic Biol Med. 17, 529-536 (1994).
9. Cai, L. Diabetic cardiomyopathy and its prevention by metallothionein: experimental evidence, possible mechanisms and clinical implications. Curr Med Chem. 14, 2193-2203 (2007).
10. Harvey, C. J. et al. Targeting Nrf2 signaling improves bacterial clearance by alveolar macrophages in patients with COPD and in a mouse model. Sci Transl Med. 3, 78ra32 (2011).
11. Nguyen, T., Nioi, P. & Pickett, C. B. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem. 284, 13291-13295 (2009).
12. Sykiotis, G. P., Habeos, I. G., Samuelson, A. V. & Bohmann, D. The role of the antioxidant and longevity-promoting Nrf2 pathway in metabolic regulation. Curr Opin Clin Nutr Metab Care. 14, 41-48 (2011).
13. Li, J., Ichikawa, T., Janicki, J. S. & Cui, T. Targeting the Nrf2 pathway against cardiovascular disease. Expert Opin Ther Targets. 13, 785-794 (2009).
14. de Haan, J. B. Nrf2 activators as attractive therapeutics for diabetic nephropathy. Diabetes. 60, 2683-2684 (2011).
15. Li, B., Liu, S., Miao, L. & Cai, L. Prevention of diabetic complications by activation of Nrf2: diabetic cardiomyopathy and nephropathy. Exp Diabetes Res. 2012, 216512 (2012).
16. Juge, N., Mithen, R. F. & Traka, M. Molecular basis for chemoprevention by sulforaphane: a comprehensive review. Cell Mol Life Sci. 64, 1105-1127 (2007).
17. Fahey, J. W. & Talalay, P. Antioxidant functions of sulforaphane: a potent inducer of Phase II detoxication enzymes. Food Chem Toxicol. 37, 973-979 (1999).
18. Zheng, H. et al. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes. 60, 3055-3066 (2011).
19. Cui, W. et al. Prevention of diabetic nephropathy by sulforaphane: possible role of Nrf2 upregulation and activation. Oxid Med Cell Longev. 2012, 821936 (2012).
20. Bai, Y. et al. Prevention by sulforaphane of diabetic cardiomyopathy is associated with up-regulation of Nrf2 expression and transcription activation. J Mol Cell Cardiol. 57, 82-95 (2013).
21. de Souza, C. G. et al. Metabolic effects of sulforaphane oral treatment in streptozotocin-diabetic rats. J Med Food. 15, 795-801 (2012).
22. Negi, G., Kumar, A. & Sharma, S. S. Nrf2 and NF-kappaB modulation by sulforaphane counteracts multiple manifestations of diabetic neuropathy in rats and high glucose-induced changes. Curr Neurovasc Res. 8, 294-304 (2011).
23. Heber, D. et al. Sulforaphane-rich broccoli sprout extract attenuates nasal allergic response to diesel exhaust particles. Food Funct. 5, 35-41 (2014).
24. Riedl, M. A., Saxon, A. & Diaz-Sanchez, D. Oral sulforaphane increases Phase II antioxidant enzymes in the human upper airway. Clin Immunol. 130, 244-251 (2009).
25. Shapiro, T. A. et al. Safety, tolerance, and metabolism of broccoli sprout glucosinolates and isothiocyanates: a clinical phase I study. Nutr Cancer. 55, 53-62 (2006).
26. Saha, S. et al. Isothiocyanate concentrations and interconversion of sulforaphane to erucin in human subjects after consumption of commercial frozen broccoli compared to fresh broccoli. Mol Nutr Food Res. 56, 1906-1916 (2012).
27. Meyer, M. et al. Sulforaphane induces SLPI secretion in the nasal mucosa. Respir Med. 107, 472-475 (2013).
28. Kensler, T. W. et al. Modulation of the metabolism of airborne pollutants by glucoraphanin-rich and sulforaphane-rich broccoli sprout beverages in Qidong, China. Carcinogenesis. 33, 101-107 (2012).
29. Zhang, Z. et al. Sulforaphane prevents the development of cardiomyopathy in type 2 diabetic mice probably by reversing oxidative stress-induced inhibition of LKB1/AMPK pathway. J Mol Cell Cardiol. 77, 42-52 (2014).
30. He, X., Kan, H., Cai, L. & Ma, Q. Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J Mol Cell Cardiol. 46, 47-58 (2009).
31. Wang, Y. et al. Sulforaphane attenuation of type 2 diabetes-induced aortic damage was associated with the upregulation of Nrf2 expression and function. Oxid Med Cell Longev. 2014, 123963 (2014).
32. Jiang, X., Bai, Y., Zhang, Z. G., Xin, Y. & Cai, L. Protection by sulforaphane from type 1 diabetes-induced testicular apoptosis is associated with the up-regulation of Nrf2 expression and function. Toxicol Appl Pharmacol. 279, 198-210 (2014).
33. Wu, H. et al. Metallothionein plays a prominent role in the prevention of diabetic nephropathy by sulforaphane via up-regulation of Nrf2. Free Radic Biol Med. 89, 431-442 (2015).
34. Wang, Y. et al. Sulforaphane reduction of testicular apoptotic cell death in diabetic mice is associated with the upregulation of Nrf2 expression and function. Am J Physiol Endocrinol Metab. 307, E14-E23 (2014).
35. Velmurugan, G. V., Sundaresan, N. R., Gupta, M. P. & White, C. Defective Nrf2-dependent redox signalling contributes to microvascular dysfunction in type 2 diabetes. Cardiovasc Res. 100, 143-150 (2013).
36. Rajendran, P. et al. Nrf2 status affects tumor growth, HDAC3 gene promoter associations, and the response to sulforaphane in the colon. Clin Epigenetics. 7, 102 (2015).
37. Houghton, C. A., Fassett, R. G. & Coombes, J. S. Sulforaphane and Other Nutrigenomic Nrf2 Activators: Can the Clinician's Expectation Be Matched by the Reality? Oxid Med Cell Longev. 2016, 7857186 (2016).
38. Houghton, C. A., Fassett, R. G. & Coombes, J. S. Sulforaphane: translational research from laboratory bench to clinic. Nutr Rev. 71, 709-726 (2013).
39. Li, F., Hullar, M. A., Beresford, S. A. & Lampe, J. W. Variation of glucoraphanin metabolism in vivo and ex vivo by human gut bacteria. Br J Nutr. 106, 408-416 (2011).
40. Glade, M. J. & Meguid, M. M. A Glance at⋯ Broccoli, glucoraphanin, and sulforaphane. Nutrition. 31, 1175-1178 (2015).
41. Gawlik-Dziki, U. et al. Anticancer and antioxidant activity of bread enriched with broccoli sprouts. Biomed Res Int. 2014, 608053 (2014).
42. Munday, R. et al. Inhibition of urinary bladder carcinogenesis by broccoli sprouts. Cancer Res. 68, 1593-1600 (2008).
43. Li, Y. et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res. 16, 2580-2590 (2010).
44. Shiina, A. et al. An Open Study of Sulforaphane-rich Broccoli Sprout Extract in Patients with Schizophrenia. Clin Psychopharmacol Neurosci. 13, 62-67 (2015).
45. Amjad, A. I. et al. Broccoli-Derived Sulforaphane and Chemoprevention of Prostate Cancer: From Bench to Bedside. Curr Pharmacol Rep. 1, 382-390 (2015).
46. Fofaria, N. M., Ranjan, A., Kim, S. H. & Srivastava, S. K. Mechanisms of the Anticancer Effects of Isothiocyanates. Enzymes. 37, 111-137 (2015).
47. Gupta, P., Kim, B., Kim, S. H. & Srivastava, S. K. Molecular targets of isothiocyanates in cancer: recent advances. Mol Nutr Food Res. 58, 1685-1707 (2014).
48. Li, Y. et al. Kinetics of sulforaphane in mice after consumption of sulforaphane-enriched broccoli sprout preparation. Mol Nutr Food Res. 57, 2128-2136 (2013).
49. Guerrero-Beltran, C. E., Calderon-Oliver, M., Pedraza-Chaverri, J. & Chirino, Y. I. Protective effect of sulforaphane against oxidative stress: recent advances. Exp Toxicol Pathol. 64, 503-508 (2012).
50. Basu, R. et al. Type 1 diabetic cardiomyopathy in the Akita (Ins2(WT/C96Y)) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am J Physiol Heart Circ Physiol. 297, H2096-H2108 (2009).
51. Yang, J. L. et al. Angiotensin II plays a critical role in diabetic pulmonary fibrosis most likely via activation of NADPH oxidasemediated nitrosative damage. Am J Physiol Endocrinol Metab. 301, E132-E144 (2011).
52. Jiang, X. et al. Protective effect of FGF21 on type 1 diabetes-induced testicular apoptotic cell death probably via both mitochondrialand endoplasmic reticulum stress-dependent pathways in the mouse model. Toxicol Lett. 219, 65-76 (2013).