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Review Article

Protective role of sulphoraphane against vascular complications in diabetes

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Pages 2329-2339 | Received 07 Aug 2015, Accepted 31 Dec 2015, Published online: 03 Feb 2016

References

  • Angeloni C, Malaguti M, Rizzo B, Barbalace MC, Fabbri D, Hrelia S. 2015. Neuroprotective effect of sulforaphane against methylglyoxal cytotoxicity. Chem Res Toxicol. 28:1234–1245.
  • Asakage M, Tsuno NH, Kitayama J, Tsuchiya T, Yoneyama S, Yamada J, Okaji Y, Kaisaki S, Osada T, Takahashi K, et al.. 2006. Sulforaphane induces inhibition of human umbilical vein endothelial cells proliferation by apoptosis. Angiogenesis 9:83–91.
  • Annabi B, Rojas-Sutterlin S, Laroche M, Lachambre MP, Moumdjian R, Béliveau R. 2008. The diet-derived sulforaphane inhibits matrix metalloproteinase-9-activated human brain microvascular endothelial cell migration and tubulogenesis. Mol Nutr Food Res. 52:692–700.
  • Bäck M, Hansson GK. 2015. Anti-inflammatory therapies for atherosclerosis. Nat Rev Cardiol. 12:199–211.
  • Bahadoran Z, Tohidi M, Nazeri P, Mehran M, Azizi F, Mirmiran P. 2012. Effect of broccoli sprouts on insulin resistance in type 2 diabetic patients: a randomized double-blind clinical trial. Int J Food Sci Nutr. 63:767–771.
  • Bai Y, Cui W, Xin Y, Miao X, Barati MT, Zhang C, Chen Q, Tan Y, Cui T, Zheng Y, et al, et al. 2013. Prevention by sulforaphane of diabetic cardiomyopathy is associated with up-regulation of Nrf2 expression and transcription activation. J Mol Cell Cardiol. 57:82–95.
  • Bhakkiyalakshmi E, Sireesh D, Rajaguru P, Paulmurugan R, Ramkumar KM. 2015. The emerging role of redox-sensitive Nrf2-Keap1 pathway in diabetes. Pharmacol Res. 91:104–114.
  • Chen XL, Dodd G, Kunsch C. 2009. Sulforaphane inhibits TNF-alpha-induced activation of p38 MAP kinase and VCAM-1 and MCP-1 expression in endothelial cells. Inflamm Res. 58:513–521.
  • Chuang WY, Kung PH, Kuo CY, Wu CC. 2013. Sulforaphane prevents human platelet aggregation through inhibiting the phosphatidylinositol 3-kinase/Akt pathway. Thromb Haemost. 109:1120–1130.
  • Cui W, Bai Y, Miao X, Luo P, Chen Q, Tan Y, Rane MJ, Miao L, Cai L. 2012. Prevention of diabetic nephropathy by sulforaphane: possible role of Nrf2 upregulation and activation. Oxid Med Cell Longev. 2012:821936.
  • Daffu G, del Pozo CH, O'Shea KM, Ananthakrishnan R, Ramasamy R, Schmidt AM. 2013. Radical roles for RAGE in the pathogenesis of oxidative stress in cardiovascular diseases and beyond. Int J Mol Sci. 14:19891–19910.
  • Davis R, Singh KP, Kurzrock R, Shankar S. 2009. Sulforaphane inhibits angiogenesis through activation of FOXO transcription factors. Oncol Rep. 22:1473–1478.
  • De Souza CG, Sattler JA, De Assis AM, Rech A, Perry ML, Souza DO. 2012. Metabolic effects of sulforaphane oral treatment in streptozotocin-diabetic rats. J Med Food. 15:795–801.
  • Dinkova-Kostova AT, Kostov RV. 2012. Glucosinolates and isothiocyanates in health and disease. Trends Mol Med. 18:337–347.
  • Du XL, Edelstein D, Rossetti L, Fantus IG, Goldberg H, Ziyadeh F, Wu J, Brownlee M. 2000. Hyperglycemia-induced mitochondrial superoxide overproduction activates the hexosamine pathway and induces plasminogen activator inhibitor-1 expression by increasing Sp1 glycosylation. Proc Natl Acad Sci USA. 97:12222–12226.
  • Emerging Risk Factors Collaboration, Seshasai SR, Kaptoge S, Thompson A, Di Angelantonio E, Gao P, Sarwar N, Whincup PH, Mukamal KJ, Gillum RF, Holme I. 2011, et al. Diabetes mellitus, fasting glucose, and risk of cause-specific death. N Engl J Med.. 364:829–841.
  • Fukami K, Matsui T, Yamagishi S. 2014b. Sulforaphane inhibits formation of advanced glycation end products in vitro. Diabetes Frontier Online 1:e1–e001.
  • Fukami K, Yamagishi S, Okuda S. 2014a. Role of AGEs-RAGE system in cardiovascular disease. Curr Pharm Des. 20:2395–2402.
  • Fukushima Y, Daida H, Morimoto T, Kasai T, Miyauchi K, Yamagishi S, Takeuchi M, Hiro T, Kimura T, Nakagawa Y, et al. 2013. Relationship between advanced glycation end products and plaque progression in patients with acute coronary syndrome: the JAPAN-ACS sub-study. Cardiovasc Diabetol. 12:5.
  • Griendling KK, Sorescu D, Ushio-Fukai M. 2000. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 86:494–501.
  • Guerrero-Beltrán CE, Calderón-Oliver M, Pedraza-Chaverri J, Chirino YI. 2012. Protective effect of sulforaphane against oxidative stress: recent advances. Exp Toxicol Pathol. 64:503–508.
  • Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, et al. 2003. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med. 9:294–299.
  • Higashimoto Y, Matsui T, Nishino Y, Taira J, Inoue H, Takeuchi M, Yamagishi S. 2013. Blockade by phosphorothioate aptamers of advanced glycation end products-induced damage in cultured pericytes and endothelial cells. Microvasc Res. 90:64–70.
  • Hung CN, Huang HP, Wang CJ, Liu KL, Lii CK. 2014. Sulforaphane inhibits TNF-α-induced adhesion molecule expression through the Rho A/ROCK/NF-κB signaling pathway. J Med Food. 17:1095–1102.
  • Hyogo H, Yamagishi S, Iwamoto K, Arihiro K, Takeuchi M, Sato T, Ochi H, Nonaka M, Nabeshima Y, Inoue M, et al. 2007. Elevated levels of serum advanced glycation end products in patients with non-alcoholic steatohepatitis. J Gastroenterol Hepatol. 22:1112–1119.
  • International Diabetes Federation. 2013. IDF diabetes atlas. 6th ed. Brussels, Belgium: International Diabetes Federation.
  • Ishibashi Y, Matsui T, Takeuchi M, Yamagishi S. 2010. Glucagon-like peptide-1 (GLP-1) inhibits advanced glycation end product (AGE)-induced up-regulation of VCAM-1 mRNA levels in endothelial cells by suppressing AGE receptor (RAGE) expression. Biochem Biophys Res Commun. 391:1405–1408.
  • Ishibashi Y, Matsui T, Ueda S, Fukami K, Yamagishi S. 2014. Advanced glycation end products potentiate citrated plasma-evoked oxidative and inflammatory reactions in endothelial cells by upregulating protease-activated receptor-1 expression. Cardiovasc Diabetol. 13:60.
  • Jayakumar T, Chen WF, Lu WJ, Chou DS, Hsiao G, Hsu CY, Sheu JR, Hsieh CY. 2013. A novel antithrombotic effect of sulforaphane via activation of platelet adenylate cyclase: ex vivo and in vivo studies. J Nutr Biochem. 24:1086–1095.
  • Jiménez-Osorio AS, González-Reyes S, Pedraza-Chaverri J. 2015. Natural Nrf2 activators in diabetes. Clin Chim Acta. 448:182–192.
  • Jinnouchi Y, Yamagishi S, Takeuchi M, Ishida S, Jinnouchi Y, Jinnouchi J, Imaizumi T. 2006. Atorvastatin decreases serum levels of advanced glycation end products (AGEs) in patients with type 2 diabetes. Clin Exp Med. 6:191–193.
  • Kajikawa M, Nakashima A, Fujimura N, Maruhashi T, Iwamoto Y, Iwamoto A, Matsumoto T, Oda N, Hidaka T, Kihara Y, et al. 2015. Ratio of serum levels of AGEs to soluble form of RAGE is a predictor of endothelial function. Diabetes Care 38:119–125.
  • Kaminski BM, Steinhilber D, Stein JM, Stein JM, Ulrich S. 2012. Phytochemicals resveratrol and sulforaphane as potential agents for enhancing the anti-tumor activities of conventional cancer therapies. Curr Pharm Biotechnol. 13:137–146.
  • Kim JY, Park HJ, Um SH, Sohn EH, Kim BO, Moon EY, Rhee DK, Pyo S. 2012. Sulforaphane suppresses vascular adhesion molecule-1 expression in TNF-α-stimulated mouse vascular smooth muscle cells: involvement of the MAPK, NF-κB and AP-1 signaling pathways. Vascul Pharmacol. 56:131–141.
  • Kivelä AM, Mäkinen PI, Jyrkkänen HK, Mella-Aho E, Xia Y, Kansanen E, Leinonen H, Verma IM, Ylä-Herttuala S, Levonen AL. 2010. Sulforaphane inhibits endothelial lipase expression through NF-κB in endothelial cells. Atherosclerosis 213:122–128.
  • Konić-Ristić A, Srdić-Rajić T, Kardum N, Aleksić-Veličković V, Kroon PA, Hollands WJ, Needs PW, Boyko N, Hayran O, Jorjadze M, et al. 2013. Effects of bioactive-rich extracts of pomegranate, persimmon, nettle, dill, kale and Sideritis and isolated bioactives on arachidonic acid induced markers of platelet activation and aggregation. J Sci Food Agric. 93:3581–3587.
  • Ku SK, Bae JS. 2014. Antithrombotic activities of sulforaphane via inhibiting platelet aggregation and FIIa/FXa. Arch Pharm Res. 37:1454–1463.
  • Ku SK, Han MS, Bae JS. 2014. Sulforaphane inhibits endothelial protein C receptor shedding in vitro and in vivo. Vascul Pharmacol. 63:13–18.
  • Kunsch C, Medford RM. 1999. Oxidative stress as a regulator of gene expression in the vasculature. Circ Res. 85:753–766.
  • Kwon JS, Joung H, Kim YS, Shim YS, Ahn Y, Jeong MH, Kee HJ. 2012. Sulforaphane inhibits restenosis by suppressing inflammation and the proliferation of vascular smooth muscle cells. Atherosclerosis 225:41–49.
  • Li B, Tian S, Liu X, He C, Ding Z, Shan Y. 2015. Sulforaphane protected the injury of human vascular endothelial cell induced by LPC through up-regulating endogenous antioxidants and phase II enzymes. Food Funct. 6:1984–1991.
  • Liu YC, Hsieh CW, Weng YC, Chuang SH, Hsieh CY, Wung BS. 2008. Sulforaphane inhibition of monocyte adhesion via the suppression of ICAM-1 and NF-kappaB is dependent upon glutathione depletion in endothelial cells. Vascul Pharmacol. 48:54–61.
  • Loukine L, Waters C, Choi BC, Ellison J. 2012. Impact of diabetes mellitus on life expectancy and health-adjusted life expectancy in Canada. Popul Health Metr. 10:7.
  • Maeda S, Matsui T, Ojima A, Takeuchi M, Yamagishi S. 2014. Sulforaphane inhibits advanced glycation end product-induced pericyte damage by reducing expression of receptor for advanced glycation end products. Nutr Res. 34:807–813.
  • Medina S, Domínguez-Perles R, Moreno DA, García-Viguera C, Ferreres F, Gil JI, Gil-Izquierdo Á. 2015. The intake of broccoli sprouts modulates the inflammatory and vascular prostanoids but not the oxidative stress-related isoprostanes in healthy humans. Food Chem. 173:1187–1194.
  • Nakamura K, Yamagishi S, Adachi H, Matsui T, Kurita-Nakamura Y, Takeuchi M, Inoue H, Imaizumi T. 2008. Circulating advanced glycation end products (AGEs) and soluble form of receptor for AGEs (sRAGE) are independent determinants of serum monocyte chemoattractant protein-1 (MCP-1) levels in patients with type 2 diabetes. Diabetes Metab Res Rev. 24:109–114.
  • Nakamura K, Yamagishi S, Matsui T, Yoshida T, Takenaka K, Jinnouchi Y, Yoshida Y, Ueda S, Adachi H, Imaizumi T. 2007. Pigment epithelium-derived factor inhibits neointimal hyperplasia after vascular injury by blocking NADPH oxidase-mediated reactive oxygen species generation. Am J Pathol. 170:2159–2170.
  • Nallasamy P, Si H, Babu PV, Pan D, Fu Y, Brooke EA, Shah H, Zhen W, Zhu H, Liu D, et al. 2014. Sulforaphane reduces vascular inflammation in mice and prevents TNF-α-induced monocyte adhesion to primary endothelial cells through interfering with the NF-κB pathway. J Nutr Biochem. 25:824–833.
  • Nathan DM, DCCT/EDIC Research Group. 2014. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care 37:9–16.
  • Negi G, Kumar A, Sharma SS. 2011. Nrf2 and NF-κB modulation by sulforaphane counteracts multiple manifestations of diabetic neuropathy in rats and high glucose-induced changes. Curr Neurovasc Res. 8:294–304.
  • Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al. 2000. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404:787–790.
  • Nishikawa T, Tsuno NH, Okaji Y, Sunami E, Shuno Y, Sasaki K, Hongo K, Kaneko M, Hiyoshi M, Kawai K, et al. 2010. The inhibition of autophagy potentiates anti-angiogenic effects of sulforaphane by inducing apoptosis. Angiogenesis 13:227–238.
  • Nishikawa T, Tsuno NH, Tsuchiya T, Yoneyama S, Yamada J, Shuno Y, Okaji Y, Tanaka J, Kitayama J, Takahashi K, et al. 2009. Sulforaphane stimulates activation of proapoptotic protein bax leading to apoptosis of endothelial progenitor cells. Ann Surg Oncol. 16:534–543.
  • Oh CH, Shin JI, Mo SJ, Yun SJ, Kim SH, Rhee YH. 2013. Antiplatelet activity of L-sulforaphane by regulation of platelet activation factors, glycoprotein IIb/IIIa and thromboxane A2. Blood Coagul Fibrinol. 24:498–504.
  • Ojima A, Ishibashi Y, Matsui T, Maeda S, Nishino Y, Takeuchi M, Fukami K, Yamagishi S. 2013. Glucagon-like peptide-1 receptor agonist inhibits asymmetric dimethylarginine generation in the kidney of streptozotocin-induced diabetic rats by blocking advanced glycation end product-induced protein arginine methyltranferase-1 expression. Am J Pathol. 182:132–141.
  • Orlidge A, D'Amore PA. 1987. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol. 105:1455–1462.
  • Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME. 2008. Soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J. 22:3716–3727.
  • Rhodes ET, Prosser LA, Hoerger TJ, Lieu T, Ludwig DS, Laffel LM. 2012. Estimated morbidity and mortality in adolescents and young adults diagnosed with Type 2 diabetes mellitus. Diabet Med. 29:453–463.
  • Shan Y, Lin N, Yang X, Tan J, Zhao R, Dong S, Wang S. 2012. Sulphoraphane inhibited the expressions of intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 through MyD88-dependent toll-like receptor-4 pathway in cultured endothelial cells. Nutr Metab Cardiovasc Dis. 22:215–222.
  • Shan Y, Zhao R, Geng W, Lin N, Wang X, Du X, Wang S. 2010. Protective effect of sulforaphane on human vascular endothelial cells against lipopolysaccharide-induced inflammatory damage. Cardiovasc Toxicol. 10:139–145.
  • Shang G, Tang X, Gao P, Guo F, Liu H, Zhao Z, Chen Q, Jiang T, Zhang N, Li H. 2015. Sulforaphane attenuation of experimental diabetic nephropathy involves GSK-3 beta/Fyn/Nrf2 signaling pathway. J Nutr Biochem. 26:596–606.
  • Sourris KC, Forbes JM. 2009. Interactions between advanced glycation end-products (AGE) and their receptors in the development and progression of diabetic nephropathy-are these receptors valid therapeutic targets. Curr Drug Targets. 10:42–50.
  • Tahara N, Tahara A, Honda A, Nitta Y, Kodama N, Yamagishi S, Imaizumi T. 2014. Molecular imaging of vascular inflammation. Curr Pharm Des. 20:2439–2447.
  • Tahara N, Yamagishi S, Matsui T, Takeuchi M, Nitta Y, Kodama N, Mizoguchi M, Imaizumi T. 2012a. Serum levels of advanced glycation end products (AGEs) are independent correlates of insulin resistance in nondiabetic subjects. Cardiovasc Ther. 30:42–48.
  • Tahara N, Yamagishi S, Takeuchi M, Honda A, Tahara A, Nitta Y, Kodama N, Mizoguchi M, Kaida H, Ishibashi M, et al. 2012b. Positive association between serum level of glyceraldehyde-derived advanced glycation end products and vascular inflammation evaluated by [(18)F]fluorodeoxyglucose positron emission tomography. Diabetes Care 35:2618–2625.
  • Tahara N, Yamagishi SI, Kodama N, Tahara A, Honda A, Nitta Y, Igata S, Matsui T, Takeuchi M, Kaida H, et al. 2015. Clinical and biochemical factors associated with area and metabolic activity in the visceral and subcutaneous adipose tissues by FDG-PET/CT. J Clin Endocrinol Metab. 100:E739–E747.
  • Takenaka K, Yamagishi S, Matsui T, Nakamura K, Imaizumi T. 2006. Role of advanced glycation end products (AGEs) in thrombogenic abnormalities in diabetes. Curr Neurovasc Res. 3:73–77.
  • Takeuchi M, Yamagishi S. 2009. Involvement of toxic AGEs (TAGE) in the pathogenesis of diabetic vascular complications and Alzheimer's disease. J Alzheimers Dis. 16:845–858.
  • The Diabetes Control and Complications Trial Research Group. 1993. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 329:977–986.
  • Tortorella SM, Royce SG, Licciardi PV, Karagiannis TC. 2015. Dietary sulforaphane in cancer chemoprevention: the role of epigenetic regulation and HDAC inhibition. Antioxid Redox Signal. 22:1382–1424.
  • Turin TC, Murakami Y, Miura K, Rumana N, Kadota A, Ohkubo T, Okamura T, Okayama A, Ueshima H; NIPPON DATA 80 Group. 2012. Diabetes and life expectancy among Japanese-NIPPON DATA80. Diabetes Res Clin Pract. 96:e18–e22.
  • Ueda S, Yamagishi S, Matsui T, Noda Y, Ueda S, Jinnouchi Y, Sasaki K, Takeuchi M, Imaizumi T. 2012. Serum levels of advanced glycation end products (AGEs) are inversely associated with the number and migratory activity of circulating endothelial progenitor cells in apparently healthy subjects. Cardiovasc Ther. 30:249–254.
  • UK Prospective Diabetes Study (UKPDS) Group. 1998. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk complications in patients with type 2 diabetes (UKPDS 33). Lancet 352:837–853.
  • Velmurugan GV, Sundaresan NR, Gupta MP, Gupta MP, White C. 2013. Defective Nrf2-dependent redox signalling contributes to microvascular dysfunction in type 2 diabetes. Cardiovasc Res. 100:143–150.
  • Vincent AM, Kato K, McLean LL, Soules ME, Feldman EL. 2009. Sensory neurons and Schwann cells respond to oxidative stress by increasing antioxidant defense mechanisms. Antioxid Redox Signal. 11:425–438.
  • Vlassara H, Uribarri J. 2014. Advanced glycation end products (AGE) and diabetes: cause, effect, or both? Curr Diab Rep. 14:453.
  • Wang Y, Zhang Z, Sun W, Tan Y, Liu Y, Zheng Y, Liu Q, Cai L, Sun J. 2014. 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.
  • Writing Group for the DCCT/EDIC Research Group. 2015. Association between 7 years of intensive treatment of type 1 diabetes and long-term mortality. JAMA 313:45–53.
  • Xu j, Kulkarni SR, Donepudi AC, More VR, Slitt AL. 2012. Enhanced Nrf2 activity worsens insulin resistance, impairs lipid accumulation in adipose tissue, and increases hepatic steatosis in leptin-deficient mice. Diabetes 61:3208–3218.
  • Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ. 2008. Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes 57:2809–2817.
  • Yamagishi S. 2011. Role of advanced glycation end products (AGEs) in osteoporosis in diabetes. Curr Drug Targets. 12:2096–2102.
  • Yamagishi S. 2012. Potential clinical utility of advanced glycation end product cross-link breakers in age-and diabetes-associated disorders. Rejuvenation Res. 15:564–572.
  • Yamagishi S, Adachi H, Takeuchi M, Enomoto M, Furuki K, Matsui T, Nakamura K, Imaizumi T. 2007. Serum level of advanced glycation end-products (AGEs) is an independent determinant of plasminogen activator inhibitor-1 (PAI-1) in nondiabetic general population. Horm Metab Res. 39:845–848.
  • Yamagishi S, Amano S, Inagaki Y, Okamoto T, Takeuchi M, Makita Z. 2002. Beraprost sodium, a prostaglandin I2 analogue, protects against advanced gycation end products-induced injury in cultured retinal pericytes. Mol Med. 8:546–550.
  • Yamagishi S, Fujimori H, Yonekura H, Yamamoto Y, Yamamoto H. 1998. Advanced glycation endproducts inhibit prostacyclin production and induce plasminogen activator inhibitor-1 in human microvascular endothelial cells. Diabetologia 41:1435–1441.
  • Yamagishi S, Imaizumi T. 2005. Diabetic vascular complications: pathophysiology, biochemical basis and potential therapeutic strategy. Curr Pharm Des. 11:2279–2299.
  • Yamagishi S, Kobayashi K, Yamamoto H. 1993. Vascular pericytes not only regulate growth, but also preserve prostacyclin-producing ability and protect against lipid peroxide-induced injury of co-cultured endothelial cells. Biochem Biophys Res Commun. 190:418–425.
  • Yamagishi SI, Matsui T. 2010a. Anti-atherothrombogenic properties of PEDF. Curr Mol Med. 10:284–291.
  • Yamagishi S, Matsui T. 2010b. Soluble form of a receptor for advanced glycation end products (sRAGE) as a biomarker. Front Biosci (Elite Ed). 2:1184–1195.
  • Yamagishi S, Matsui T. 2015. Protective role of sodium-glucose cotransporter 2 (SGLT2) inhibition against vascular complications in diabetes. Rejuvenation Res. doi: 10.1089/rej.2015.1738.
  • Yamagishi S, Matsui T, Fukami K. 2015a. Role of receptor for advanced glycation end products (RAGE) and its ligands in cancer risk. Rejuvenation Res. 18:48–56.
  • Yamagishi S, Matsui T, Takenaka K, Nakamura K, Takeuchi M, Inoue H. 2009. Pigment epithelium-derived factor (PEDF) prevents platelet activation and aggregation in diabetic rats by blocking deleterious effects of advanced glycation end products (AGEs). Diabetes Metab Res Rev. 25:266–271.
  • Yamagishi S, Nakamura K, Matsui T. 2008. Role of oxidative stress in the development of vascular injury and its therapeutic intervention by nifedipine. Curr Med Chem. 15:172–177.
  • Yamagishi S, Nishino Y, Ojima A, Matsui T, Nishi H. 2015b. Oral consumption of sulforaphane precursor-rich broccoli supersprouts decreases serum levels of advanced glycation end products in humans. Diabetes Frontier Online 2:e1–e011.
  • Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, Morito N, Nakano T, Ojima M, Shimohata H, et al. 2008. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 13:1159–1170.
  • Yoo SH, Lim Y, Kim SJ, Yoo KD, Yoo HS, Hong JT, Lee MY, Yun YP. 2013. Sulforaphane inhibits PDGF-induced proliferation of rat aortic vascular smooth muscle cell by up-regulation of p53 leading to G1/S cell cycle arrest. Vascul Pharmacol. 59:44–51.
  • Zakkar M, Van der Heiden K, Luong le A, Chaudhury H, Cuhlmann S, Hamdulay SS, Krams R, Edirisinghe I, Rahman I, Carlsen H, et al. 2009. Activation of Nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler Thromb Vasc Biol. 29:1851–1857.
  • Zhang Z, Wang S, Zhou S, Yan X, Wang Y, Chen J, Mellen N, Kong M, Gu J, Tan Y, et al. 2014. 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.
  • Zhao XD, Zhou YT, Lu XJ. 2013. Sulforaphane enhances the activity of the Nrf2-ARE pathway and attenuates inflammation in OxyHb-induced rat vascular smooth muscle cells. Inflamm Res. 62:857–863.
  • Zheng H, Whitman SA, Wu W, Wondrak GT, Wong PK, Fang D, Zhang DD. 2011. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes 60:3055–3066.
  • Zhu H, Jia Z, Strobl JS, Ehrich M, Misra HP, Li Y. 2008. Potent induction of total cellular and mitochondrial antioxidants and phase 2 enzymes by cruciferous sulphoraphane in rat aortic smooth muscle cells: cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol. 8:115–125.

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