Sulforaphane reduces vascular inflammation in mice and prevents TNF-α-induced monocyte adhesion to primary endothelial cells through interfering with the NF-κB pathway

Journal of Nutritional Biochemistry

Volumn 25, Issue 8, 2014, Pages 824-833

  Nallasamy, Palanisamy ^a   Si, Hongwei ^b   Babu, Pon Velayutham Anandh ^c   Pan, Dengke ^d   Fu, Yu ^e   Brooke, Elizabeth A S ^a   Shah, Halley ^a   Zhen, Wei ^e   Zhu, Hong ^f   Liu, Dongmin ^e   Li, Yunbo ^f   Jia, Zhenquan ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

^b TENNESSEE STATE UNIVERSITY   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d INSTITUTE OF PLANT PROTECTION   (China)

^e VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^f Sampson Regional Medical Center Dermatology Residency Director   (United States)

Author keywords

In vivo; Physiological concentrations; Sulforaphane; TNF ; Vascular inflammation

Indexed keywords

CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SULFORAPHANE; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; ISOTHIOCYANIC ACID DERIVATIVE; SULFORAFAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ADHESION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DIET SUPPLEMENTATION; DIETARY INTAKE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; SHEAR FLOW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULITIS; ANIMAL; AORTA; C57BL MOUSE; CYTOLOGY; DIET THERAPY; DRUG EFFECTS; ENDOTHELIUM CELL; METABOLISM; PATHOLOGY; VASCULAR ENDOTHELIUM;

ANIMALIA; MUS;

ANIMALS; AORTA; CELL ADHESION; CHEMOKINES; DIETARY SUPPLEMENTS; E-SELECTIN; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOTHIOCYANATES; MALE; MICE, INBRED C57BL; MONOCYTES; NF-KAPPA B; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1; VASCULITIS;

EID: 84903756114     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2014.03.011     Document Type: Article

References (53)

1. Hansson G.K., Robertson A.K., Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol 2006, 1:297-329.
2. Packard R.R., Libby P. Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction. Clin Chem 2008, 54:24-38.
3. Pearson T.A., Mensah G.A., Alexander R.W., Anderson J.L., Cannon R.O., Criqui M., et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 2003, 107:499-511.
4. Mayer K., Merfels M., Muhly-Reinholz M., Gokorsch S., Rosseau S., Lohmeyer J., et al. Omega-3 fatty acids suppress monocyte adhesion to human endothelial cells: role of endothelial PAF generation. Am J Physiol Heart Circ Physiol 2002, 283:H811-H818.
5. Chen J.W., Chen Y.H., Lin F.Y., Chen Y.L., Lin S.J. Ginkgo biloba extract inhibits tumor necrosis factor-alpha-induced reactive oxygen species generation, transcription factor activation, and cell adhesion molecule expression in human aortic endothelial cells. Arterioscler Thromb Vasc Biol 2003, 23:1559-1566.
6. Carluccio M.A., Siculella L., Ancora M.A., Massaro M., Scoditti E., Storelli C., et al. Olive oil and red wine antioxidant polyphenols inhibit endothelial activation: antiatherogenic properties of Mediterranean diet phytochemicals. Arterioscler Thromb Vasc Biol 2003, 23:622-629.
7. Gerthoffer W.T. Mechanisms of vascular smooth muscle cell migration. Circ Res 2007, 100:607-621.
8. Ridker P.M., Hennekens C.H., Buring J.E., Rifai N. C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med 2000, 342:836-843.
9. Mukherjee T.K., Nathan L., Dinh H., Reddy S.T., Chaudhuri G. 17-epiestriol, an estrogen metabolite, is more potent than estradiol in inhibiting vascular cell adhesion molecule 1 (VCAM-1) mRNA expression. J Biol Chem 2003, 278:11746-11752.
10. Boyle E.M., Kovacich J.C., Canty T.G., Morgan E.N., Chi E., Verrier E.D., et al. Inhibition of nuclear factor-kappa B nuclear localization reduces human E-selectin expression and the systemic inflammatory response. Circulation 1998, 98:II282-II288.
11. Yerneni K.K., Bai W., Khan B.V., Medford R.M., Natarajan R. Hyperglycemia-induced activation of nuclear transcription factor kappaB in vascular smooth muscle cells. Diabetes 1999, 48:855-864.
12. Lee Y.R., Noh E.M., Han J.H., Kim J.M., Hwang B.M., Kim B.S., et al. Sulforaphane controls TPA-induced MMP-9 expression through the NF-kappaB signaling pathway, but not AP-1, in MCF-7 breast cancer cells. BMB Rep 2013, 46:201-206.
13. Suppipat K., Park C.S., Shen Y., Zhu X., Lacorazza H.D. Sulforaphane induces cell cycle arrest and apoptosis in acute lymphoblastic leukemia cells. PLoS One 2012, 7:e51251.
14. Hahm E.R., Chandra-Kuntal K., Desai D., Amin S., Singh S.V. Notch activation is dispensable for d,l-sulforaphane-mediated inhibition of human prostate cancer cell migration. PLoS One 2012, 7:e44957.
15. Bai Y., Cui W., Xin Y., Miao X., Barati M.T., Zhang C., et al. Prevention by sulforaphane of diabetic cardiomyopathy is associated with up-regulation of Nrf2 expression and transcription activation. J Mol Cell Cardiol 2013, 57:82-95.
16. de Souza C.G., Sattler J.A., de Assis A.M., Rech A., Perry M.L., Souza D.O. Metabolic effects of sulforaphane oral treatment in streptozotocin-diabetic rats. J Med Food 2012, 15:795-801.
17. Song M.Y., Kim E.K., Moon W.S., Park J.W., Kim H.J., So H.S., et al. Sulforaphane protects against cytokine- and streptozotocin-induced beta-cell damage by suppressing the NF-kappaB pathway. Toxicol Appl Pharmacol 2009, 235:57-67.
18. Jayakumar T., Chen W.F., Lu W.J., Chou D.S., Hsiao G., Hsu C.Y., et al. A novel antithrombotic effect of sulforaphane via activation of platelet adenylate cyclase: ex vivo and in vivo studies. J Nutr Biochem 2013, 24:1086-1095.
19. Kivela A.M., Makinen P.I., Jyrkkanen H.K., Mella-Aho E., Xia Y., Kansanen E., et al. Sulforaphane inhibits endothelial lipase expression through NF-kappaB in endothelial cells. Atherosclerosis 2010, 213:122-128.
20. Kwon J.S., Joung H., Kim Y.S., Shim Y.S., Ahn Y., Jeong M.H., et al. Sulforaphane inhibits restenosis by suppressing inflammation and the proliferation of vascular smooth muscle cells. Atherosclerosis 2012, 225:41-49.
21. Kim J.Y., Park H.J., Um S.H., Sohn E.H., Kim B.O., Moon E.Y., et al. Sulforaphane suppresses vascular adhesion molecule-1 expression in TNF-alpha-stimulated mouse vascular smooth muscle cells: involvement of the MAPK, NF-kappaB and AP-1 signaling pathways. Vasc Pharmacol 2012, 56:131-141.
22. Miao X., Bai Y., Sun W., Cui W., Xin Y., Wang Y., et al. Sulforaphane prevention of diabetes-induced aortic damage was associated with the up-regulation of Nrf2 and its down-stream antioxidants. Nutrition & Metabolism 2012, 9:84.
23. Senanayake G.V., Banigesh A., Wu L., Lee P., Juurlink B.H. The dietary phase 2 protein inducer sulforaphane can normalize the kidney epigenome and improve blood pressure in hypertensive rats. Am J Hypertens 2012, 25:229-235.
24. Lin W., Wu R.T., Wu T., Khor T.O., Wang H., Kong A.N. Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem Pharmacol 2008, 76:967-973.
25. Li Y., Zhang T., Korkaya H., Liu S., Lee H.F., Newman B., et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res 2010, 16:2580-2590.
26. Babu P.V., Si H., Fu Z., Zhen W., Liu D. Genistein prevents hyperglycemia-induced monocyte adhesion to human aortic endothelial cells through preservation of the cAMP signaling pathway and ameliorates vascular inflammation in obese diabetic mice. J Nutr 2012, 142:724-730.
27. Jia Z., Babu P.V., Si H., Nallasamy P., Zhu H., Zhen W., et al. Genistein inhibits TNF-alpha-induced endothelial inflammation through the protein kinase pathway A and improves vascular inflammation in C57BL/6 mice. Int J Cardiol 2013, 168:2637-2645.
28. Babu P.V., Si H., Liu D. Epigallocatechin gallate reduces vascular inflammation in db/db mice possibly through an NF-kappaB-mediated mechanism. Mol Nutr Food Res 2012, 56:1424-1432.
29. Srinivasan S., Bolick D.T., Hatley M.E., Natarajan R., Reilly K.B., Yeh M., et al. Glucose regulates interleukin-8 production in aortic endothelial cells through activation of the p38 mitogen-activated protein kinase pathway in diabetes. J Biol Chem 2004, 279:31930-31936.
30. Thompson S.G., Kienast J., Pyke S.D., Haverkate F., van de Loo J.C. Hemostatic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. European Concerted Action on Thrombosis and Disabilities Angina Pectoris Study Group. N Engl J Med 1995, 332:635-641.
31. Danesh J., Wheeler J.G., Hirschfield G.M., Eda S., Eiriksdottir G., Rumley A., et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med 2004, 350:1387-1397.
32. Deckert-Schluter M., Bluethmann H., Kaefer N., Rang A., Schluter D. Interferon-gamma receptor-mediated but not tumor necrosis factor receptor type 1- or type 2-mediated signaling is crucial for the activation of cerebral blood vessel endothelial cells and microglia in murine toxoplasma encephalitis. Am J Pathol 1999, 154:1549-1561.
33. Shaposhnik Z., Wang X., Lusis A.J. Arterial colony stimulating factor-1 influences atherosclerotic lesions by regulating monocyte migration and apoptosis. J Lipid Res 2010, 51:1962-1970.
34. Wu D., Nishimura N., Kuo V., Fiehn O., Shahbaz S., Van Winkle L., et al. Activation of aryl hydrocarbon receptor induces vascular inflammation and promotes atherosclerosis in apolipoprotein E-/- mice. Arterioscler Thromb Vasc Biol 2011, 31:1260-1267.
35. Genkinger J.M., Platz E.A., Hoffman S.C., Comstock G.W., Helzlsouer K.J. 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, 160:1223-1233.
36. Lockheart M.S., Steffen L.M., Rebnord H.M., Fimreite R.L., Ringstad J., Thelle D.S., et al. Dietary patterns, food groups and myocardial infarction: a case-control study. Br J Nutr 2007, 98:380-387.
37. Saha S., Hollands W., Teucher B., Needs P.W., Narbad A., Ortori C.A., 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 2012, 56:1906-1916.
38. Ye L., Dinkova-Kostova A.T., Wade K.L., Zhang Y., Shapiro T.A., 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.
39. Norata G.D., Cattaneo P., Poletti A., Catapano A.L. The androgen derivative 5alpha-androstane-3beta,17beta-diol inhibits tumor necrosis factor alpha and lipopolysaccharide induced inflammatory response in human endothelial cells and in mice aorta. Atherosclerosis 2010, 212:100-106.
40. Hu R., Khor T.O., Shen G., Jeong W.S., Hebbar V., Chen C., et al. Cancer chemoprevention of intestinal polyposis in ApcMin/+mice by sulforaphane, a natural product derived from cruciferous vegetable. Carcinogenesis 2006, 27:2038-2046.
41. Myzak M.C., Dashwood W.M., Orner G.A., Ho E., Dashwood R.H. Sulforaphane inhibits histone deacetylase in vivo and suppresses tumorigenesis in Apc-minus mice. Faseb J 2006, 20:506-508.
42. Shen G., Khor T.O., Hu R., Yu S., Nair S., Ho C.T., et al. Chemoprevention of familial adenomatous polyposis by natural dietary compounds sulforaphane and dibenzoylmethane alone and in combination in ApcMin/+mouse. Cancer Res 2007, 67:9937-9944.
43. Galkina E., Ley K. Vascular adhesion molecules in atherosclerosis. Arterioscler Thromb Vasc Biol 2007, 27:2292-2301.
44. Gerszten R.E., Garcia-Zepeda E.A., Lim Y.C., Yoshida M., Ding H.A., Gimbrone M.A., et al. MCP-1 and IL-8 trigger firm adhesion of monocytes to vascular endothelium under flow conditions. Nature 1999, 398:718-723.
45. Hong J.J., Jeong T.S., Choi J.H., Park J.H., Lee K.Y., Seo Y.J., et al. Hematein inhibits tumor necrotic factor-alpha-induced vascular cell adhesion molecule-1 and NF-kappaB-dependent gene expression in human vascular endothelial cells. Biochem Biophys Res Commun 2001, 281:1127-1133.
46. O'Brien K.D., Allen M.D., McDonald T.O., Chait A., Harlan J.M., Fishbein D., et al. Vascular cell adhesion molecule-1 is expressed in human coronary atherosclerotic plaques. Implications for the mode of progression of advanced coronary atherosclerosis. J Clin Invest 1993, 92:945-951.
47. Hegazy D.M., O'Reilly D.A., Yang B.M., Hodgkinson A.D., Millward B.A., Demaine A.G. NFkappaB polymorphisms and susceptibility to type 1 diabetes. Genes Immun 2001, 2:304-308.
48. Li Y., Reddy M.A., Miao F., Shanmugam N., Yee J.K., Hawkins D., et al. Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. J Biol Chem 2008, 283:26771-26781.
49. Paria B.C., Malik A.B., Kwiatek A.M., Rahman A., May M.J., Ghosh S., et al. Tumor necrosis factor-alpha induces nuclear factor-kappaB-dependent TRPC1 expression in endothelial cells. J Biol Chem 2003, 278:37195-37203.
50. Gerritsen M.E., Williams A.J., Neish A.S., Moore S., Shi Y., Collins T. CREB-binding protein/p300 are transcriptional coactivators of p65. Proc Natl Acad Sci U S A 1997, 94:2927-2932.
51. Brown K., Gerstberger S., Carlson L., Franzoso G., Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 1995, 267:1485-1488.
52. Ouchi N., Kihara S., Arita Y., Okamoto Y., Maeda K., Kuriyama H., et al. Adiponectin, an adipocyte-derived plasma protein, inhibits endothelial NF-kappaB signaling through a cAMP-dependent pathway. Circulation 2000, 102:1296-1301.
53. Read M.A., Whitley M.Z., Williams A.J., Collins T. NF-kappa B and I kappa B alpha: an inducible regulatory system in endothelial activation. J Exp Med 1994, 179:503-512.