Plant-Derived Phenolics Inhibit the Accrual of Structurally Characterised Protein and Lipid Oxidative Modifications

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Soler Cantero, Arantza ^a   Jové, Mariona ^a   Cacabelos, Daniel ^a   Boada, Jordi ^a   Naudí, Alba ^a   Romero, Maria Paz ^a   Cassanyé, Anna ^a   Serrano, José C E ^a   Arola, Lluis ^b   Valls, Josep ^c   Bellmunt, Maria Josep ^a   Prat, Joan ^a   Pamplona, Reinald ^a   Portero Otin, Manuel ^a   Motilva, Maria José ^a  

^a UNIVERSITY OF LLEIDA   (Spain)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c Shirota Functional Foods SL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1 PALMITOYLLYSOLECITHIN; 1 STEAROYLGLYCEROPHOSPHOCHOLINE; ACTEOSIDE; ALDEHYDE DERIVATIVE; ALPHA TOCOPHEROL; AMINOADIPIC SEMIALDEHYDE; ANTIOXIDANT; APIGENIN; APOPROTEIN; CAFFEIC ACID; COPPER ION; FERULIC ACID; GALLIC ACID; GLUTAMIC SEMIALDEHYDE; GRAPE SEED EXTRACT; HYDROXYTYROSOL; LOW DENSITY LIPOPROTEIN; LUTEOLIN; LYSOPHOSPHATIDYLCHOLINE; OLEUROPEIN; OXIDIZED LOW DENSITY LIPOPROTEIN; PARA COUMARIC ACID; PHOSPHORYLCHOLINE; PINORESINOL; RUTOSIDE; TYROSOL; UNCLASSIFIED DRUG; VANILLIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG EFFICACY; DRUG SCREENING; FOOD COMPOSITION; HAMSTER; HUMAN; HYPERCHOLESTEROLEMIA; IN VIVO STUDY; LIPID OXIDATION; LIPID STORAGE; LIPIDOMICS; MALE; NONHUMAN; PHYTOCHEMISTRY; PROTEIN MODIFICATION; STRUCTURE ACTIVITY RELATION;

ALDEHYDES; ANIMAL FEED; ANIMALS; ANTIOXIDANTS; CELL SURVIVAL; COPPER; CRICETINAE; HUMANS; LIPIDS; LIPOPROTEINS, LDL; LYSINE; MALE; MALONDIALDEHYDE; MASS SPECTROMETRY; MESOCRICETUS; OXYGEN; PHENOL; PHOSPHOLIPIDS; PLANT EXTRACTS; PLANTS;

CRICETINAE;

EID: 84865613130     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043308     Document Type: Article

References (67)

1. Goldstein JL, Brown MS, (1977) The low-density lipoprotein pathway and its relation to atherosclerosis. Annu Rev Biochem 46: 897-930.
2. Goldstein JL, Ho YK, Basu SK, Brown MS, (1979) Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci U S A 76 (1) (): 333-337.
3. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL, (1989) Beyond cholesterol. modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 320 (14) (): 915-924.
4. Hazell LJ, Arnold L, Flowers D, Waeg G, Malle E, et al. (1996) Presence of hypochlorite-modified proteins in human atherosclerotic lesions. J Clin Invest 97 (6) (): 1535-1544.
5. Hazen SL, Heinecke JW, (1997) 3-chlorotyrosine, a specific marker of myeloperoxidase-catalyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima. J Clin Invest 99 (9) (): 2075-2081.
6. Leeuwenburgh C, Hardy MM, Hazen SL, Wagner P, Oh-ishi S, et al. (1997) Reactive nitrogen intermediates promote low density lipoprotein oxidation in human atherosclerotic intima. J Biol Chem 272 (3) (): 1433-1436.
7. Berliner JA, Heinecke JW, (1996) The role of oxidized lipoproteins in atherogenesis. Free Radic Biol Med 20 (5) (): 707-727.
8. Esterbauer H, Gebicki J, Puhl H, Jurgens G, (1992) The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radic Biol Med 13 (4) (): 341-390.
9. Hazell LJ, Stocker R, (1993) Oxidation of low-density lipoprotein with hypochlorite causes transformation of the lipoprotein into a high-uptake form for macrophages. Biochem J 290 (Pt 1Pt 1) (): 165-172.
10. Stupans I, Kirlich A, Tuck KL, Hayball PJ, (2002) Comparison of radical scavenging effect, inhibition of microsomal oxygen free radical generation, and serum lipoprotein oxidation of several natural antioxidants. J Agric Food Chem 50 (8) (): 2464-2469.
11. Carluccio MA, Siculella L, Ancora MA, Massaro M, Scoditti E, et al. (2003) Olive oil and red wine antioxidant polyphenols inhibit endothelial activation: Antiatherogenic properties of mediterranean diet phytochemicals. Arterioscler Thromb Vasc Biol 23 (4) (): 622-629.
12. Grassi D, Aggio A, Onori L, Croce G, Tiberti S, et al. (2008) Tea, flavonoids, and nitric oxide-mediated vascular reactivity. J Nutr 138 (8) (): 1554S-1560S.
13. Natella F, Nardini M, Belelli F, Scaccini C, (2007) Coffee drinking induces incorporation of phenolic acids into LDL and increases the resistance of LDL to ex vivo oxidation in humans. Am J Clin Nutr 86 (3) (): 604-609.
14. Nakagawa K, Ninomiya M, Okubo T, Aoi N, Juneja LR, et al. (1999) Tea catechin supplementation increases antioxidant capacity and prevents phospholipid hydroperoxidation in plasma of humans. J Agric Food Chem 47 (10) (): 3967-3973.
15. Kamiyama M, Kishimoto Y, Tani M, Andoh K, Utsunomiya K, et al. (2009) Inhibition of low-density lipoprotein oxidation by nagano purple grape (vitis viniferaxVitis labrusca). J Nutr Sci Vitaminol (Tokyo) 55 (6) (): 471-478.
16. Hayek T, Fuhrman B, Vaya J, Rosenblat M, Belinky P, et al. (1997) Reduced progression of atherosclerosis in apolipoprotein E-deficient mice following consumption of red wine, or its polyphenols quercetin or catechin, is associated with reduced susceptibility of LDL to oxidation and aggregation. Arterioscler Thromb Vasc Biol 17 (11) (): 2744-2752.
17. Ness AR, Powles JW, (1997) Fruit and vegetables, and cardiovascular disease: A review. Int J Epidemiol 26 (1) (): 1-13.
18. Abbey M, Nestel PJ, Baghurst PA, (1993) Antioxidant vitamins and low-density-lipoprotein oxidation. Am J Clin Nutr 58 (4) (): 525-532.
19. Jialal I, Grundy SM, (1993) Effect of combined supplementation with alpha-tocopherol, ascorbate, and beta carotene on low-density lipoprotein oxidation. Circulation 88 (6) (): 2780-2786.
20. Suarna C, Hood RL, Dean RT, Stocker R, (1993) Comparative antioxidant activity of tocotrienols and other natural lipid-soluble antioxidants in a homogeneous system, and in rat and human lipoproteins. Biochim Biophys Acta 1166 (2-3) (): 163-170.
21. Hou L, Zhou B, Yang L, Liu ZL, (2004) Inhibition of human low density lipoprotein oxidation by flavonols and their glycosides. Chem Phys Lipids 129 (2) (): 209-219.
22. Chen CY, Milbury PE, Chung SK, Blumberg J, (2007) Effect of almond skin polyphenolics and quercetin on human LDL and apolipoprotein B-100 oxidation and conformation. J Nutr Biochem 18 (12) (): 785-794.
23. Oorni K, Pentikainen MO, Annila A, Kovanen PT, (1997) Oxidation of low density lipoprotein particles decreases their ability to bind to human aortic proteoglycans. dependence on oxidative modification of the lysine residues. J Biol Chem 272 (34) (): 21303-21311.
24. Wagner P, Heinecke JW, (1997) Copper ions promote peroxidation of low density lipoprotein lipid by binding to histidine residues of apolipoprotein B100, but they are reduced at other sites on LDL. Arterioscler Thromb Vasc Biol 17 (11) (): 3338-3346.
25. Yan LJ, Lodge JK, Traber MG, Packer L, (1997) Apolipoprotein B carbonyl formation is enhanced by lipid peroxidation during copper-mediated oxidation of human low-density lipoproteins. Arch Biochem Biophys 339 (1) (): 165-171.
26. Terra X, Pallares V, Ardevol A, Blade C, Fernandez-Larrea J, et al. (2011) Modulatory effect of grape-seed procyanidins on local and systemic inflammation in diet-induced obesity rats. J Nutr Biochem 22 (4) (): 380-387.
27. Artajo LS, Romero MP, Morello JR, Motilva MJ, (2006) Enrichment of refined olive oil with phenolic compounds: Evaluation of their antioxidant activity and their effect on the bitter index. J Agric Food Chem 54 (16) (): 6079-6088.
28. Auger C, Gerain P, Laurent-Bichon F, Portet K, Bornet A, et al. (2004) Phenolics from commercialized grape extracts prevent early atherosclerotic lesions in hamsters by mechanisms other than antioxidant effect. J Agric Food Chem 52 (16) (): 5297-5302.
29. Wikoff WR, Gangoiti JA, Barshop BA, Siuzdak G, (2007) Metabolomics identifies perturbations in human disorders of propionate metabolism. Clin Chem 53 (12) (): 2169-2176.
30. Balla G, Jacob HS, Eaton JW, Belcher JD, Vercellotti GM, (1991) Hemin: A possible physiological mediator of low density lipoprotein oxidation and endothelial injury. Arterioscler Thromb 11 (6) (): 1700-1711.
31. Pamplona R, Dalfo E, Ayala V, Bellmunt MJ, Prat J, et al. (2005) Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation. effects of alzheimer disease and identification of lipoxidation targets. J Biol Chem 280 (22) (): 21522-21530.
32. Watson AD, Leitinger N, Navab M, Faull KF, Horkko S, et al. (1997) Structural identification by mass spectrometry of oxidized phospholipids in minimally oxidized low density lipoprotein that induce monocyte/endothelial interactions and evidence for their presence in vivo. J Biol Chem 272 (21) (): 13597-13607.
33. Benzie IF, Strain JJ, (1996) The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": The FRAP assay. Anal Biochem 239 (1) (): 70-76.
34. Pulido R, Bravo L, Saura-Calixto F, (2000) Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J Agric Food Chem 48 (8) (): 3396-3402.
35. Bouguerne B, Belkheiri N, Bedos-Belval F, Vindis C, Uchida K, et al. (2011) Antiatherogenic effect of bisvanillyl-hydralazone, a new hydralazine derivative with antioxidant, carbonyl scavenger, and antiapoptotic properties. Antioxid Redox Signal 14 (11) (): 2093-2106.
36. Goya L, Delgado-Andrade C, Rufian-Henares JA, Bravo L, Morales FJ, (2007) Effect of coffee melanoidin on human hepatoma HepG2 cells. protection against oxidative stress induced by tert-butylhydroperoxide. Mol Nutr Food Res 51 (5) (): 536-545.
37. Goya L, Mateos R, Bravo L, (2007) Effect of the olive oil phenol hydroxytyrosol on human hepatoma HepG2 cells. protection against oxidative stress induced by tert-butylhydroperoxide. Eur J Nutr 46 (2) (): 70-78.
38. Xia J, Psychogios N, Young N, Wishart DS, (2009) MetaboAnalyst: A web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37 (Web Server issue): W652-60.
39. Berlett BS, Stadtman ER, (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272 (33) (): 20313-20316.
40. Vissers MN, Zock PL, Katan MB, (2004) Bioavailability and antioxidant effects of olive oil phenols in humans: A review. Eur J Clin Nutr 58 (6) (): 955-965.
41. Leenen R, Roodenburg AJ, Vissers MN, Schuurbiers JA, van Putte KP, et al. (2002) Supplementation of plasma with olive oil phenols and extracts: Influence on LDL oxidation. J Agric Food Chem 50 (5) (): 1290-1297.
42. Covas MI, Miro-Casas E, Fito M, Farre-Albadalejo M, Gimeno E, et al. (2003) Bioavailability of tyrosol, an antioxidant phenolic compound present in wine and olive oil, in humans. Drugs Exp Clin Res 29 (5-6) (): 203-206.
43. Covas MI, (2007) Olive oil and the cardiovascular system. Pharmacol Res 55 (3) (): 175-186.
44. Di Benedetto R, Vari R, Scazzocchio B, Filesi C, Santangelo C, et al. (2007) Tyrosol, the major extra virgin olive oil compound, restored intracellular antioxidant defences in spite of its weak antioxidative effectiveness. Nutr Metab Cardiovasc Dis 17 (7) (): 535-545.
45. Briante R, Febbraio F, Nucci R, (2004) Antioxidant/prooxidant effects of dietary non-flavonoid phenols on the Cu2+-induced oxidation of human low-density lipoprotein (LDL). Chem Biodivers 1 (11) (): 1716-1729.
46. Mazziotti A, Mazzotti F, Pantusa M, Sportelli L, Sindona G, (2006) Pro-oxidant activity of oleuropein determined in vitro by electron spin resonance spin-trapping methodology. J Agric Food Chem 54 (20) (): 7444-7449.
47. Menendez JA, Vazquez-Martin A, Colomer R, Brunet J, Carrasco-Pancorbo A, et al. (2007) Olive oil's bitter principle reverses acquired autoresistance to trastuzumab (herceptin) in HER2-overexpressing breast cancer cells. BMC Cancer 7: 80.
48. Hamdi HK, Castellon R, (2005) Oleuropein, a non-toxic olive iridoid, is an anti-tumor agent and cytoskeleton disruptor. Biochem Biophys Res Commun 334 (3) (): 769-778.
49. Rice-Evans CA, Miller NJ, Paganga G, (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20 (7) (): 933-956.
50. Bors W, Heller W, Michel C, Saran M, (1990) Flavonoids as antioxidants: Determination of radical-scavenging efficiencies. Methods Enzymol 186: 343-355.
51. Kostyuk VA, Kraemer T, Sies H, Schewe T, (2003) Myeloperoxidase/nitrite-mediated lipid peroxidation of low-density lipoprotein as modulated by flavonoids. FEBS Lett 537 (1-3) (): 146-150.
52. Brown JE, Khodr H, Hider RC, Rice-Evans CA, (1998) Structural dependence of flavonoid interactions with Cu2+ ions: Implications for their antioxidant properties. Biochem J 330 (Pt 3Pt 3) (): 1173-1178.
53. Jeong YJ, Choi YJ, Choi JS, Kwon HM, Kang SW, et al. (2007) Attenuation of monocyte adhesion and oxidised LDL uptake in luteolin-treated human endothelial cells exposed to oxidised LDL. Br J Nutr 97 (3) (): 447-457.
54. Brenes M, Garcia A, Garcia P, Rios JJ, Garrido A, (1999) Phenolic compounds in spanish olive oils. J Agric Food Chem 47 (9) (): 3535-3540.
55. Chen CC, Chen HY, Shiao MS, Lin YL, Kuo YH, et al. (1999) Inhibition of low density lipoprotein oxidation by tetrahydrofurofuran lignans from forsythia suspensa and magnolia coco. Planta Med 65 (8) (): 709-711.
56. Vuorela S, Kreander K, Karonen M, Nieminen R, Hamalainen M, et al. (2005) Preclinical evaluation of rapeseed, raspberry, and pine bark phenolics for health related effects. J Agric Food Chem 53 (15) (): 5922-5931.
57. Hou Z, Sang S, You H, Lee MJ, Hong J, et al. (2005) Mechanism of action of (-)-epigallocatechin-3-gallate: Auto-oxidation-dependent inactivation of epidermal growth factor receptor and direct effects on growth inhibition in human esophageal cancer KYSE 150 cells. Cancer Res 65 (17) (): 8049-8056.
58. Long LH, Clement MV, Halliwell B, (2000) Artifacts in cell culture: Rapid generation of hydrogen peroxide on addition of (-)-epigallocatechin, (-)-epigallocatechin gallate, (+)-catechin, and quercetin to commonly used cell culture media. Biochem Biophys Res Commun 273 (1) (): 50-53.
59. Hsieh CL, Yen GC, Chen HY, (2005) Antioxidant activities of phenolic acids on ultraviolet radiation-induced erythrocyte and low density lipoprotein oxidation. J Agric Food Chem 53 (15) (): 6151-6155.
60. Hseu YC, Chang WH, Chen CS, Liao JW, Huang CJ, et al. (2008) Antioxidant activities of toona sinensis leaves extracts using different antioxidant models. Food Chem Toxicol 46 (1) (): 105-114.
61. Laranjinha JA, Almeida LM, Madeira VM, (1994) Reactivity of dietary phenolic acids with peroxyl radicals: Antioxidant activity upon low density lipoprotein peroxidation. Biochem Pharmacol 48 (3) (): 487-494.
62. Pannala AS, Rice-Evans CA, Halliwell B, Singh S, (1997) Inhibition of peroxynitrite-mediated tyrosine nitration by catechin polyphenols. Biochem Biophys Res Commun 232 (1) (): 164-168.
63. Locatelli C, Rosso R, Santos-Silva MC, de Souza CA, Licinio MA, et al. (2008) Ester derivatives of gallic acid with potential toxicity toward L1210 leukemia cells. Bioorg Med Chem 16 (7) (): 3791-3799.
64. Hsu CL, Lo WH, Yen GC, (2007) Gallic acid induces apoptosis in 3T3-L1 pre-adipocytes via a fas- and mitochondrial-mediated pathway. J Agric Food Chem 55 (18) (): 7359-7365.
65. Agarwal C, Tyagi A, Agarwal R, (2006) Gallic acid causes inactivating phosphorylation of cdc25A/cdc25C-cdc2 via ATM-Chk2 activation, leading to cell cycle arrest, and induces apoptosis in human prostate carcinoma DU145 cells. Mol Cancer Ther 5 (12) (): 3294-3302.
66. Vieira O, Escargueil-Blanc I, Meilhac O, Basile JP, Laranjinha J, et al. (1998) Effect of dietary phenolic compounds on apoptosis of human cultured endothelial cells induced by oxidized LDL. Br J Pharmacol 123 (3) (): 565-573.
67. Fukuzawa K, Matsuura K, Tokumura A, Suzuki A, Terao J, (1997) Kinetics and dynamics of singlet oxygen scavenging by alpha-tocopherol in phospholipid model membranes. Free Radic Biol Med 22 (5) (): 923-930.