Tomato extract and the carotenoids lycopene and lutein improve endothelial function and attenuate inflammatory NF-κB signaling in endothelial cells

Journal of Hypertension

Volumn 31, Issue 3, 2013, Pages 521-529

  Armoza, Anna ^a   Haim, Yulia ^a   Basiri, Asher ^a   Wolak, Talya ^a   Paran, Esther ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Adhesion; Carotenoids; Endothelial cells; Endothelin 1; Inflammation; Lutein; Lycopene; NF B signaling; Nitric oxide; Tomato oleoresin

Indexed keywords

ENDOTHELIN 1; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; LYCOPENE; NITRIC OXIDE; OLEORESIN; PLANT EXTRACT; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; XANTHOPHYLL; CAROTENOID;

ARTICLE; BLOOD PRESSURE; CELL ADHESION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LEUKOCYTE; PRIORITY JOURNAL; TOMATO; UBIQUITINATION; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; METABOLISM; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

CAROTENOIDS; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HUMANS; LUTEIN; LYCOPERSICON ESCULENTUM; NF-KAPPA B; PLANT EXTRACTS; SIGNAL TRANSDUCTION;

EID: 84877312778     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0b013e32835c1d01     Document Type: Article

References (67)

1. Rader DJ, Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature 2008; 451:904-913. (Pubitemid 351301745)
2. Bazzano LA, He J, Ogden LG, Loria CM, Vupputuri S, Myers L, et al. Fruit and vegetable intake and risk of cardiovascular disease in US adults: the first National Health and Nutrition Examination Survey Epidemiologic Follow-up Study. Am J Clin Nutr 2002; 76:93-99. (Pubitemid 34686554)
3. Nothlings U, Schulze MB, Weikert C, Boeing H, van der Schouw YT, Bamia C, et al. Intake of vegetables, legumes, and fruit, and risk for all-cause, cardiovascular, and cancer mortality in a European diabetic population. J Nutr 2008; 138:775-781.
4. Cox BD, Whichelow MJ, Prevost AT. Seasonal consumption of salad vegetables and fresh fruit in relation to the development of cardiovascular disease and cancer. Public Health Nutr 2000; 3:19-29. (Pubitemid 30214554)
5. Takachi R, Inoue M, Ishihara J, Kurahashi N, Iwasaki M, Sasazuki S, et al. Fruit and vegetable intake and risk of total cancer and cardiovascular disease: Japan public health center-based prospective study. Am J Epidemiol 2008; 167:59-70.
6. Engelhard YN, Gazer B, Paran E. Natural antioxidants from tomato extract reduce blood pressure inpatients with grade-1 hypertension: a double-blind, placebo-controlled pilot study. Am Heart J 2006; 151.
7. Rissanen TH, Voutilainen S, Nyyssonen K, Lakka TA, Sivenius J, Salonen R, et al. Low serum lycopene concentration is associated with an excess incidence of acute coronary events and stroke: the Kuopio Ischaemic Heart Disease Risk Factor Study. Br J Nutr 2001; 85:749-754. (Pubitemid 32586506)
8. Rissanen T, Voutilainen S, Nyyssonen K, Salonen R, Salonen JT. Low plasma lycopene concentration is associated with increased intimamedia thickness of the carotid artery wall. Arterioscler Thromb Vasc Biol 2000; 20:2677-2681.
9. Dwyer JH, Paul-Labrador MJ, Fan J, Shircore AM, Bairey CN, Dwyer KM. Progression of carotid intima-media thickness and plasma antioxidants: The Los Angeles Atherosclerosis Study. Arterioscler Thromb Vasc Biol 2004; 24:313-319. (Pubitemid 38197584)
10. Heber D, Lu QY. Overview of mechanisms of action of lycopene. Exp Biol Med 2002; 227:920-923. (Pubitemid 35340348)
11. Tapiero H, Townsend DM, Tew KD. The role of carotenoids in the prevention of human pathologies. Biomed Pharmacother 2004; 58:100-110. (Pubitemid 38264535)
12. Palozza P, Parrone N, Simone RE, Catalano A. Lycopene in atherosclerosis prevention: an integrated scheme of the potential mechanisms of action from cell culture studies. Arch Biochem Biophys 2010; 504:26-33.
13. Sindhu ER, Preethi KC, Kuttan R. Antioxidant activity of carotenoid lutein in vitro and in vivo. Ind J Exp Biol 2010; 48:843-848.
14. Balestrieri ML, De Prisco R, Nicolaus B, Pari P, Moriello VS, Strazzullo G, et al. Lycopene in association with alpha-tocopherol or tomato lipophilic extracts enhances acyl-platelet-activating factor biosynthesis in endothelial cells during oxidative stress. Free Radic Biol Med 2004; 36:1058-1067. (Pubitemid 38418025)
15. Dimascio P, Kaiser SP, Thomas PA, Sies H. Biological significance of active oxigen species - in vitro studies on singlet oxygen-induced DNA damage and on the singlet oxigen quenching ability of carotenoids, tocopherols and thiols. Biol React Intermediates Iv 1991; 283:71-77.
16. Mueller L, Boehm V. Antioxidant activity of beta-carotene compounds in different in vitro assays. Molecules 2011; 16:1055-1069.
17. Khoo HE, Prasad KN, Kong KW, Jiang YM, Ismail A. Carotenoids and their isomers: color pigments in fruits and vegetables. Molecules 2011; 16:1710-1738.
18. Hung CF, Huang TF, Chen BH, Shieh JM, Wu PH, Wu WB. Lycopene inhibits TNF-alpha-induced endothelial ICAM-1 expression and mono-cyte- endothelial adhesion. Eur J Pharmacol 2008; 586:275-282.
19. Graydon R, Gilchrist S, Young IS, Obermuller-Jevic U, Hasselwander O, Woodside JV. Effect of lycopene supplementation on insulin-like growth factor-1 and insulin-like growth factor binding protein-3: a double-blind, placebo-controlled trial. Eur J Clin Nutr 2007; 61:1196-1200. (Pubitemid 47521551)
20. Feng D, Ling WH, Duan RD. Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappa B in macrophages. Inflamm Res 2010; 59:115-121.
21. Bessler H, Salman H, Bergman M, Alcalay Y, Djaldetti M. In vitro effect of lycopene on cytokine production by human peripheral blood mononuclear cells. Immunolog Investig 2008; 37:183-190. (Pubitemid 351499569)
22. Lo HM, Hung CF, Tseng YL, Chen BH, Jian JS, Wu WB. Lycopene binds PDGF-BB and inhibits PDGF-BB-induced intracellular signaling transduction pathway in rat smooth muscle cells. Biochem Pharmacol 2007; 74:54-63.
23. 2 and TNF-alpha and its effects on ICAM-1 expression in endothelial cells. Am J Physiol Lung Cell Molec Physiol 2000; 279:L302-L311.
24. Vallabhapurapu S, Karin M. Regulation and function of NF-kappa B transcription factors in the immune system. Ann Rev Immunol 2009; 27:693-733.
25. Siebenlist U, Franzoso G, Brown K. Structure, regulation and function of NF-kappa-B. Ann Rev Cell Biol 1994; 10:405-455.
26. Dugas TR, Morel DW, Harrison EH. Impact of LDL carotenoid and alpha-tocopherol content on LDL oxidation by endothelial cells in culture. J Lipid Res 1998; 39:999-1007. (Pubitemid 28222004)
27. Lee DK, Grantham RN, Mannion JD, Trachte AL. Carotenoids enhance phosphorylation of Akt and suppress tissue factor activity in human endothelial cells. J Nutr Biochem 2006; 17:780-786. (Pubitemid 44557051)
28. Martin KR, Wu D, Meydani M. The effect of carotenoids on the expression of cell surface adhesion molecules and binding of monocytes to human aortic endothelial cells. Atherosclerosis 2000; 150:265-274. (Pubitemid 30336538)
29. 2-induced oxidative injury and apoptosis in human endothelial cells. Cardiovasc Drugs Ther 2009; 23:439-448.
30. Chen L-P, He S-Y, Zheng H, Dai Y-L. Effects and mechanisms of lycopene on the proliferation of vascular smooth muscle cells. Chinese J Natural Med 2010; 8:218-222.
31. Paran E, Engelhard YN, Hazan-Hallevy I, Sharoni Y, Levy J. Effect of standardized tomato extract on blood pressure, endothelial function and plasma lycopene levels in treated hypertensive patients. Am J Hypertens 2005; 18:213A-A.
32. Paran E, Novack V, Engelhard YN, Hazan-Halevy I. The effects of natural antioxidants from tomato extract in treated but uncontrolled hypertensive patients. Cardiovasc Drugs Ther 2009; 23:145-151.
33. Jaffe EA, Nachman RL, Becker CG, Minick CR. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J Clin Invest 1973; 52:2745-2756.
34. Lundberg JO, Weitzberg E. NO generation from nitrite and its role in vascular control. Arterioscler Thromb Vasc Biol 2005; 25:915-922. (Pubitemid 40627834)
35. Boyum A. Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol 1976; Suppl 5:9-15.
36. Hallevi H, Hazan-Halevy I, Paran E. Modification of neutrophil adhesion to human endothelial cell line in acute ischemic stroke by dipyridamole and candesartan. Eur J Neurol 2007; 14:1002-1007. (Pubitemid 47300773)
37. Rahman A, Kefer J, Bando M, Niles WD, Malik AB. E-selectin expression in human endothelial cells by TNF-alpha-induced oxidant generation and NF-kappa B activation. Am J Physiol Lung Cell Molec Physiol 1998; 275:L533-L544.
38. Surette ME, Dallaire N, Jean N, Picard S, Borgeat P. Mechanisms of the priming effect of lipopolysaccharides on the biosynthesis of leukotriene B-4 in chemotactic peptide-stimulated human neutrophils. FASEB J 1998; 12:1521-1531. (Pubitemid 28506721)
39. Moon MK, Lee YJ, Kim JS, Kang DG, Lee HS. Effect of caffeic acid on tumor necrosis factor-alpha-induced vascular inflammation in human umbilical vein endothelial cells. Biol Pharmaceut Bull 2009; 32:1371-1377.
40. Chai H, Wo LK, Fu Y, Xie T, Wang QY, Huang LF. S-allyl-L-cysteine sulfoxide inhibits tumor necrosis factor-alpha induced monocyte adhesion and intercellular cell adhesion molecule-1 expression in human umbilical vein endothelial cells. Adv Integrative Anat Evolution Biol 2010; 293:421-430.
41. Chang W-C, Chen C-H, Lee M-F, Chang T, Yu Y-M. Chlorogenic acid attenuates adhesion molecules upregulation in IL-1 beta-treated endothelial cells. Eur J Nutr 2010; 49:267-275.
42. Choi YW, Kim HJ, Park SS, Chung JH, Lee HW, Oh SO, et al. Inhibition of endothelial cell adhesion by the new anti-inflammatory agent alpha-isocubebene. Vasc Pharmacol 2009; 51:215-224.
43. Chung B-H, Lee JJ, Kim J-D, Jeoung D, Lee H, Choe J, et al. Angiogenic activity of sesamin through the activation of multiple signal pathways. Biochem Biophys Res Commun 2010; 391.
44. Hwang JH, Lee SH, Rha SJ, Yoon HS, Shin JH, Lee JH, et al. Characterization of angiogenesis inhibitor effect of green tea seed extract. Animal Cells Syst 2009; 13:133-139.
45. Lee W-J, Ou H-C, Hsu W-C, Chou M-M, Tseng J-J, Hsu S-L, et al. Ellagic acid inhibits oxidized LDL-mediated LOX-1 expression, ROS generation, and inflammation in human endothelial cells. J Vasc Surg 2010; 52:1290-1300.
46. Speciale A, Canali R, Chirafisi J, Saija A, Virgili F, Cimino F. Cyanidin-3-O-glucoside protection against TNF-alpha-induced endothelial dysfunction: involvement of nuclear factor-kappa B signaling. J Agric Food Chem 2010; 58:12048-12054.
47. Ying Z, Kampfrath T, Sun Q, Parthasarathy S, Rajagopalan S. Evidence that alpha-lipoic acid inhibits NF-kappa B activation independent of its antioxidant function. Inflamm Res 2011; 60:219-225.
48. Yoon JJ, Lee YJ, Kim JS, Kang DG, Lee HS. Protective role of betulinic acid on TNF-alpha-induced cell adhesion molecules in vascular endothelial cells. Biochem Biophys Res Commun 2010; 391.
49. Yu YM, Lin CH, Chan HC, Tsai HD. Carnosic acid reduces cytokineinduced adhesion molecules expression and monocyte adhesion to endothelial cells. Eur J Nutr 2009; 48:101-106.
50. Connor CA, Kroon PA, Hughes DA. Apple procyanidins inhibit TNF alpha-induced pro-inflammatory effects in human umbilical vascular endothelial cells. Proc Nutr Soc 2007; 66:80A-A.
51. Manna C, Napoli D, Cacciapuoti G, Porcelli M, Zappia V. Olive oil phenolic compounds inhibit homocysteine-induced endothelial cell adhesion regardless of their different antioxidant activity. J Agric Food Chem 2009; 57:3478-3482.
52. Ou HC, Lee WJ, Lee IT, Chiu TH, Tsai KL, Lin CY, et al. Ginkgo biloba extract attenuates oxLDL-induced oxidative functional damages in endothelial cells. J Appl Physiol 2009; 106:1674-1685.
53. Kuo W-W, Huang C-Y, Chung J-G, Yang S-F, Tsai K-L, Chiu T-H, et al. Crude extracts of Solanum lyratum protect endothelial cells against oxidized low-density lipoprotein-induced injury by direct antioxidant action. J Vasc Surg 2009; 50:849-860.
54. Suganuma H, Inakuma T. Protective effect of dietary tomato against endothelial dysfunction in hypercholesterolemic mice. Biosci Biotechnol Biochem 1999; 63:78-82. (Pubitemid 129555240)
55. Stangl V, Kuhn C, Hentschel S, Jochmann N, Jacob C, Bohm V, et al. Lack of effects of tomato products on endothelial function in human subjects: results of a randomised, placebo-controlled cross-over study. Br J Nutr 2011; 105:263-267.
56. Hu MY, Li YL, Jiang CH, Liu ZQ, Qu SL, Huang YM. Comparison of lycopene and fluvastatin effects on atherosclerosis induced by a high-fat diet in rabbits. Nutrition 2008; 24:1030-1038.
57. Liu XJ, Qu D, He F, Lu QH, Wang J, Cai DL. Effect of lycopene on the vascular endothelial function and expression of inflammatory agents in hyperhomocysteinemic rats. Asia Pacific J Clin Nutr 2007; 16:244-248. (Pubitemid 46524608)
58. Mann GE, Rowlands DJ, Li FYL, de Winter P, Siow RCM. Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression. Cardiovasc Res 2007; 75:261-274. (Pubitemid 46964821)
59. Zhang XS, Ren JH, Lu JP, Fan Y. Atorvastatin protects against angiotensin II-induced injury and dysfunction in human umbilical vein endothelial cells through bradykinin 2 receptors. J Cardiovasc Pharmacol 2010; 56:171-176.
60. Kataoka H, Murakami R, Numaguchi Y, Okumura K, Murohara T. Angiotensin II type 1 receptor blockers prevent tumor necrosis factor-alpha-mediated endothelial nitric oxide synthase reduction and superoxide production in human umbilical vein endothelial cells. Eur J Pharmacol 2010; 636:36-41.
61. McCarty MF. Scavenging of peroxynitrite-derived radicals by flavonoids may support endothelial NO synthase activity, contributing to the vascular protection associated with high fruit and vegetable intakes. Med Hypotheses 2008; 70:170-181.
62. Kim JH, Na HJ, Kim CK, Kim JY, Ha KS, Lee H, et al. The nonprovitarnin A carotenoid, lutein, inhibits NF-kappa B-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-kappa B-inducing kinase pathways: role of H2O2 in NF-kappa B activation. Free Radic Biol Med 2008; 45:885-896.
63. Fuhrman B, Volkova N, Rosenblat M, Aviram M. Lycopene synergistically inhibits LDL oxidation in combination with vitamin E, glabridin, rosmarinic acid, carnosic acid, or garlic. Antiox Redox Signal 2000; 2:491-506.
64. Erdman JW Jr, Ford NA, Lindshield BL. Are the health attributes of lycopene related to its antioxidant function? Arch Biochem Biophys 2009; 483:229-235.
65. Mordente A, Guantario B, Meucci E, Silvestrini A, Lombardi E, Martorana GE, et al. Lycopene and cardiovascular diseases: an update. Curr Med Chem 2011; 18:1146-1163.
66. Menshikova EB, Tkachev VO, Zenkov NK. Redox-dependent signaling system Nrf2/ARE in inflammation. Molec Biol 2010; 44:343-357.
67. Walter MH, Strack D. Carotenoids and their cleavage products: biosynthesis and functions. Natural Product Rep 2011; 28:663-692.