The influence of sulforaphane on vascular health and its relevance to nutritional approaches to prevent cardiovascular disease

EPMA Journal

Volumn 2, Issue 1, 2011, Pages 9-14

  Evans, Paul C ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cardiovascular; Nutrition; Preventative medicine; Sulforaphane

Indexed keywords

ALPHA TOCOPHEROL; ANTIOXIDANT; CD36 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; OXIDIZED LOW DENSITY LIPOPROTEIN; OXIDIZING AGENT; PROBUCOL; REACTIVE OXYGEN METABOLITE; SCAVENGER RECEPTOR A; STAT3 PROTEIN; SULFORAPHANE; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; ATHEROGENESIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR RISK; CORONARY ARTERY ATHEROSCLEROSIS; FOOD INTAKE; HEART PROTECTION; HUMAN; MOLECULAR PATHOLOGY; NONHUMAN; NUTRITIONAL SUPPORT; PRIORITY JOURNAL; REVIEW; RISK REDUCTION; VEGETABLE; VITAMIN SUPPLEMENTATION;

EID: 79955656232     PISSN: 18785077     EISSN: 18785085     Source Type: Journal    
DOI: 10.1007/s13167-011-0064-3     Document Type: Review

References (85)

1. Badimon L, Vilahur G, Padro T. Nutraceuticals and atherosclerosis: human trials. Cardiovasc Ther. 2010; 28: 202-15.
2. Libby P. Inflammation in atherosclerosis. Nature. 2002; 420: 868-74.
3. Glass CK, Witztum JL. Atherosclerosis. The road ahead. Cell. 2001; 104: 503-16.
4. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis. Annu Rev Immunol. 2009; 27: 165-97.
5. Yeh M, Leitinger N, de Martin R, et al. Increased transcription of IL-8 in endothelial cells is differentially regulated by TNF-alpha and oxidized phospholipids. Arterioscler Thromb Vasc Biol. 2001; 21: 1585-91.
6. Cominacini L, Pasini AF, Garbin U, et al. Oxidized low density lipoprotein (ox-LDL) binding to ox-LDL receptor-1 in endothelial cells induces the activation of NF-kappa B through an increased production of intracellular reactive oxygen species. J Biol Chem. 2000; 275: 12633-8.
7. Yeh M, Gharavi NM, Choi J, et al. Oxidized phospholipids increase interleukin 8 (IL-8) synthesis by activation of the c-src/signal transducers and activators of transcription (STAT)3 pathway. J Biol Chem. 2004; 279: 30175-81.
8. Lin SJ, Shyue SK, Liu RL, et al. Adenovirus-mediated overexpression of catalase attenuates oxLDL-induced apoptosis in human aortic endothelial cells via AP-1 and C-Jun N-terminal kinase/extracellular signal-regulated kinase mitogen-activated protein kinase pathways. J Mol Cell Cardiol. 2004; 36: 129-39.
9. Huber J, Furnkranz A, Bochkov VN, et al. Specific monocyte adhesion to endothelial cells induced by oxidized phospholipids involves activation of cPLA(2) and lipoxygenase. J Lipid Res. 2006; 47: 1054-62.
10. Mattaliano MD, Huard C, Cao W, et al. LOX-1-dependent transcriptional regulation in response to oxidized LDL treatment of human aortic endothelial cells. Am J Physiol Cell Physiol. 2009; 296: C1329-37.
11. Li DY, Mehta JL. Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of human coronary artery endothelial cells-evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arterioscler Thromb Vasc Biol. 2000; 20: 1116-22.
12. Kamata H, Honda S, Maeda S, Chang LF, Hirata H, Karin M. Reactive oxygen species promote TNF alpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell. 2005; 120: 649-61.
13. Enesa K, Ito K, Luong LA, et al. Hydrogen peroxide prolongs nuclear localization of NF-kappa B in activated cells by suppressing negative regulatory mechanisms. J Biol Chem. 2008; 283: 18582-90.
14. Ito K, Hanazawa T, Tomita K, Barnes PJ, Adcock IM. Oxidative stress reduces histone deacetylase 2 activity and enhances IL-8 gene expression: role of tyrosine nitration. Biochem Biophys Res Commun. 2004; 315: 240-5.
15. Dimmeler S, Haendeler J, Galle J, Zeiher AM. Oxidized low-density lipoprotein induces apoptosis of human endothelial cells by activation of CPP32-like proteases-a mechanistic clue to the 'response to injury' hypothesis. Circulation. 1997; 95: 1760-3.
16. Foteinos G, Hu YH, Xiao QZ, Metzler B, Xu QB. Rapid endothelial turnover in atherosclerosis-prone areas coincides with stem cell repair in apolipoprotein E-deficient mice. Circulation. 2008; 117: 1856-63.
17. Stoneman VEA, Bennett MR. Role of apoptosis in atherosclerosis and its therapeutic implications. Clin Sci. 2004; 107: 343-54.
18. Cosentino F, Hurlimann D, Gatti CD, et al. Chronic treatment with tetrahydrobiopterin reverses endothelial dysfunction and oxidative stress in hypercholesterolaemia. Heart. 2008; 94: 487-92.
19. Crabtree MJ, Tatham AL, Hale AB, Alp NJ, Channon KM. Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: relative importance of the denovo biopterin synthesis versus salvage pathways. J Biol Chem. 2009; 284: 28128-36.
20. Maziere C, Maziere JC. Activation of transcription factors and gene expression by oxidized low-density lipoprotein. Free Radic Biol Med. 2009; 46: 127-37.
21. Ishigaki Y, Oka Y, Katagiri H. Circulating oxidized LDL: a biomarker and a pathogenic factor. Curr Opin Lipidol. 2009; 20: 363-9.
22. Schmitz G, Grandl M. Role of redox regulation and lipid rafts in macrophages during Ox-LDL-mediated foam cell formation. Antioxid Redox Signal. 2007; 9: 1499-518.
23. Collot-Teixeira S, Martin J, Dennott-Roe C, Poston R, McGregor JL. CD36 and macrophages in atherosclerosis. Cardiovasc Res. 2007; 75: 468-77.
24. Rahaman SO, Lennon DJ, Febbraio M, Podrez EA, Hazen SL, Silverstein RL. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 2006; 4: 211-21.
25. Janabi M, Yamashita S, Hirano K, et al. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler Thromb Vasc Biol. 2000; 20: 1953-60.
26. Hakala JK, Lindstedt KA, Kovanen PT, Pentikainen MO. Low-density lipoprotein modified by macrophage-derived lysosomal hydrolases induces expression and secretion of IL-8 via p38 MAPK and NF-kappa B by human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol. 2006; 26: 2504-9.
27. Kusuhara M, Chait A, Cader A, Berk BC. Oxidized LDL stimulates mitogen-activated protein kinases in smooth muscle cells and macrophages. Arterioscler Thromb Vasc Biol. 1997; 17: 141-8.
28. Jovinge S, Ares MPS, Kallin B, Nilsson J. Human monocytes/macrophages release TNF-alpha in response to Ox-LDL. Arterioscler Thromb Vasc Biol. 1996; 16: 1573-9.
29. Kris-Etherton PM, Lichtenstein AH, Howard BV, Steinberg D, Witztum JL. Antioxidant vitamin supplements and cardiovascular disease. Circulation. 2004; 110: 637-41.
30. Katsiki N, Manes C. Is there a role for supplemented antioxidants in the prevention of atherosclerosis? Clin Nutr. 2009; 28: 3-9.
31. Willcox BJ, Curb JD, Rodriguez BL. Antioxidants in cardiovascular health and disease: key lessons from epidemiologic studies. Am J Cardiol. 2008; 101: 75D-86D.
32. Marui N, Offermann MK, Swerlick R, et al. Vascular cell-adhesion molecule-1 (Vcam-1) gene-transcription and expression are regulated through an antioxidant sensitive mechanism in human vascular endothelial-cells. J Clin Invest. 1993; 92: 1866-74.
33. Kaneko M, Hayashi J, Saito I, Miyasaka N. Probucol downregulates E-selectin expression on cultured human vascular endothelial cells. Arterioscler Thromb Vasc Biol. 1996; 16: 1047-51.
34. Bowie AG, O'Neill LAJ. Vitamin C inhibits NF-kappa B activation by TNF via the activation of p38 mitogen-activated protein kinase. J Immunol. 2000; 165: 7180-8.
35. Chen JW, Lin FY, Chen YH, Wu TC, Chen YL, Lin SJ. Carvedilol inhibits tumor necrosis factor-alpha-induced endothelial transcription factor activation, adhesion molecule expression, and adhesiveness to human mononuclear cells. Arterioscler Thromb Vasc Biol. 2004; 24: 2075-81.
36. Carcamo JM, Pedraza A, Borquez-Ojeda O, Golde DW. Vitamin C suppresses TNF alpha-induced NF kappa B activation by inhibiting I kappa B alpha phosphorylation. Biochemistry. 2002; 41: 12995-3002.
37. Fox ES, Brower JS, Bellezzo JM, Leingang KA. N-acetylcysteine and alpha-tocopherol reverse the inflammatory response in activated rat Kupffer cells. J Immunol. 1997; 158: 5418-23.
38. Victor VM, De La Fuente M. N-acetylcysteine improves in vitro the function of macrophages from mice with endotoxin-induced oxidative stress. Free Radic Res. 2002; 36: 33-45.
39. Carcamo J, Borquez-Ojeda O, Golde D. Vitamin C inhibits granulocyte macrophage-colony-stimulating factor-induced signaling pathways. Blood. 2002; 99: 3205-12.
40. Lee KH, Lim SY, Kang SM, et al. Antiproliferative mechanisms of raxofelast (IRFI-016) in H2O2-stimulated rat aortic smooth muscle cells. Eur J Pharmacol. 2004; 484: 119-25.
41. Konneh MK, Rutherford C, Li SR, Anggard EE, Ferns GAA. Vitamin-e inhibits the intimal response to balloon catheter injury in the carotid-artery of the cholesterol-fed rat. Atherosclerosis. 1995; 113: 29-39.
42. Orozco LD, Kapturczak MH, Barajas B, et al. Heme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis. Circ Res. 2007; 100: 1703-11.
43. Lewis P, Stefanovic N, Pete J, et al. Lack of the antioxidant enzyme glutathione peroxidase-1 accelerates atherosclerosis in diabetic apolipoprotein E-deficient mice. Circulation. 2007; 115: 2178-87.
44. Juan SH, Lee TS, Tseng KW, et al. Adenovirus-mediated heme oxygenase-1 gene transfer inhibits the development of atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2001; 104: 1519-25.
45. Zhang HF, Luo Y, Zhang W, et al. Endothelial-specific expression of mitochondrial thioredoxin improves endothelial cell function and reduces atherosclerotic lesions. Am J Pathol. 2007; 170: 1108-20.
46. Yang H, Roberts LJ, Shi MJ, et al. Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res. 2004; 95: 1075-81.
47. Kaneda H, Ohno M, Taguchi J, et al. Heme oxygenase-1 gene promoter polymorphism is associated with coronary artery disease in Japanese patients with coronary risk factors. Arterioscler Thromb Vasc Biol. 2002; 22: 1680-5.
48. Chen YH, Lin SJ, Lin MW, et al. Microsatellite polymorphism in promoter of heme oxygenase-1 gene is associated with susceptibility to coronary artery disease in type 2 diabetic patients. Hum Genet. 2002; 111: 1-8.
49. Stephens NG, Parsons A, Schofield PM, et al. Randomised controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet. 1996; 347: 781-6.
50. Boaz M, Smetana S, Weinstein T, et al. Secondary prevention with antioxidants of cardiovascular disease in endstage renal disease (SPACE): randomised placebo-controlled trial. Lancet. 2000; 356: 1213-8.
51. Witting PK, Pettersson K, Letters J, Stocker R. Site-specific antiatherogenic effect of probucol in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2000; 20: E26-33.
52. Schneider JE, Berk BC, Gravanis MB, et al. Probucol decreases neointimal formation in a swine model of coronary-artery balloon injury-a possible role for antioxidants in restenosis. Circulation. 1993; 88: 628-37.
53. Tardif JC, Cote G, Lesperance J, et al. Probucol and multivitamins in the prevention of restenosis after coronary angioplasty. N Engl J Med. 1997; 337: 365-72.
54. Sawayama Y, Shimizu C, Maeda N, et al. Effects of Probucol and pravastatin on common carotid atherosclerosis in patients with asymptomatic hypercholesterolemia-Fukuoka Atherosclerosis Trial (FAST). J Am Coll Cardiol. 2002; 39: 610-6.
55. Wu BJ, Kathir K, Witting PK, et al. Antioxidants protect from atherosclerosis by a heme oxygenase-1 pathway that is independent of free radical scavenging. J Exp Med. 2006; 203: 1117-27.
56. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamato M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 2002; 62: 5196-203.
57. Xue MZ, Qian QW, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ. Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes. 2008; 57: 2809-17.
58. Itoh K, Chiba T, Takahashi S, et al. An Nrf2 small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997; 236: 313-22.
59. Kensler TW, Wakabayash N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47: 89-116.
60. Yochum L, Kushi LH, Meyer K, Folsom AR. Dietary flavonoid intake and risk of cardiovascular disease in postmenopausal women. Am J Epidemiol. 1999; 149: 943-9.
61. Genkinger JM, Platz EA, Hoffman SC, Comstock GW, Helzlsouer KJ. Fruit, vegetable, and antioxidant intake and all-cause, cancer, and cardiovascular disease mortality in a community-dwelling population in Washington County, Maryland. Am J Epidemiol. 2004; 160: 1223-33.
62. Hung HC, Joshipura KJ, Jiang R, et al. Fruit and vegetable intake and risk of major chronic disease. J Natl Cancer Inst. 2004; 96: 1577-84.
63. Cornelis MC, El-Sohemy A, Campos H. GSTT1 genotype modifies the association between cruciferous vegetable intake and the risk of myocardial infarction. Am J Clin Nutr. 2007; 86: 752-8.
64. Wu LY, Ashraf MHN, Facci M, et al. Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci USA. 2004; 101: 7094-9.
65. Riedl MA, Saxon A, Diaz-Sanchez D. Oral sulforaphane increases Phase II antioxidant enzymes in the human upper airway. Clin Immunol. 2009; 130: 244-51.
66. Ye LX, Dinkova-Kostova AT, Wade KL, Zhang YS, Shapiro TA, Talalay P. Quantitative determination of dithiocarbamates in human plasma, serum, erythrocytes and urine: pharmacokinetics of broccoli sprout isothiocyanates in humans. Clin Chim Acta. 2002; 316: 43-53.
67. Hanlon N, Coldham N, Gielbert A, Sauer MJ, Ioannides C. Repeated intake of broccoli does not lead to higher plasma levels of sulforaphane in human volunteers. Cancer Lett. 2009; 284: 15-20.
68. Yanaka A, Fahey JW, Fukumoto A, et al. Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in helicobacter pylori-infected mice and humans. Cancer Prev Res. 2009; 2: 353-60.
69. Myzak MC, Tong P, Dashwood WM, Dashwood RH, Ho E. Sulforaphane retards the growth of human PC-3 xenografts and inhibits HDAC activity in human subjects. Exp Biol Med. 2007; 232: 227-34.
70. Zakkar M, van der Heiden K, Luong LA, et al. Activation of nrf2 in endothelial cells protects arteries from exhibiting a proinflammatory state. Arterioscler Thromb Vasc Biol. 2009; 29: 1851-7.
71. Chen XL, Dodd G, Kunsch C. Sulforaphane inhibits TNF-alpha-induced activation of p38 MAP kinase and VCAM-1 and MCP-1 expression in endothelial cells. Inflamm Res. 2009; 58: 513-21.
72. Zhu H, Jia Z, Strobl JS, Ehrich M, Misra HP, Li Y. Potent induction of total cellular and mitochondrial antioxidants and phase 2 enzymes by cruciferous sulforaphane in rat aortic smooth muscle cells: cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol. 2008; 8: 115-25.
73. Wu L, Juurlink BH. The impaired glutathione system and its up-regulation by sulforaphane in vascular smooth muscle cells from spontaneously hypertensive rats. J Hypertens. 2001; 19: 1819-25.
74. Liu YC, Hsieh CW, Weng YC, Chuang SH, Hsieh CY, Wung BS. Sulforaphane inhibition of monocyte adhesion via the suppression of ICAM-1 and NF-kappaB is dependent upon glutathione depletion in endothelial cells. Vascul Pharmacol. 2008; 48: 54-61.
75. Guerrero-Beltrán C.E Calderón-Oliver M, Pedraza-Chaverri J, Chirino YI. Protective effect of sulforaphane against oxidative stress: Recent advances. Exp Toxicol Pathol. 2010; doi: 10. 1016/j. etp. 2010. 11. 005.
76. Davies PF. Endothelial mechanisms of flow-mediated athero-protection and susceptibility. Circ Res. 2007; 101: 10-2.
77. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP. Hemodynamic shear stresses in mouse aortas-implications for atherogenesis. Arterioscler Thromb Vasc Biol. 2007; 27: 346-51.
78. Zakkar M, Chaudhury H, Sandvik G, et al. Increased endothelial mitogen-activated protein kinase phosphatase-1 expression suppresses proinflammatory activation at sites that are resistant to atherosclerosis. Circ Res. 2008; 103: 726-32.
79. Dai GH, Kaazempur-Mofrad MR, Natarajan S, et al. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and -resistant regions of human vasculature. Proc Natl Acad Sci USA. 2004; 101: 14871-6.
80. Levonen AL, Inkala M, Heikura T, et al. Nrf2 gene transfer induces antioxidant enzymes and suppresses smooth muscle cell growth in vitro and reduces oxidative stress in rabbit aorta in vivo. Arterioscler Thromb Vasc Biol. 2007; 27: 741-7.
81. Sussan TE, Jun J, Thimmulappa R, et al. Disruption of Nrf2, a key inducer of antioxidant defenses, attenuates ApoE-mediated atherosclerosis in mice. PLoS ONE. 2008; 3: e3791.
82. Nishikawa T, Tsuno NH, Okaji Y, et al. The inhibition of autophagy potentiates anti-angiogenic effects of sulforaphane by inducing apoptosis. Angiogenesis. 2010; 13: 227-38.
83. Nishikawa T, Tsuno NH, Tsuchiya T, et al. Sulforaphane stimulates activation of proapoptotic protein bax leading to apoptosis of endothelial progenitor cells. Ann Surg Oncol. 2009; 16: 534-43.
84. Asakage M, Tsuno NH, Kitayama J, et al. Sulforaphane induces inhibition of human umbilical vein endothelial cells proliferation by apoptosis. Angiogenesis. 2006; 9: 83-91.
85. Maruyama A, Tsukamoto S, Nishikawa K, et al. Nrf2 regulates the alternative first exons of CD36 in macrophages through specific antioxidant response elements. Arch Biochem Biophys. 2008; 477: 139-45.