Reduced glutathione increases quercetin stimulatory effects on HDL- or apoA1-mediated cholesterol efflux from J774A.1 macrophages

Free Radical Research

Volumn 48, Issue 12, 2014, Pages 1462-1472

  Rosenblat, M ^a   Volkova, N ^a   Khatib, S ^b,c   Mahmood, S ^b   Vaya, J ^b,c   Aviram, M ^a  

^a RAMBAM MEDICAL CENTER   (Israel)

^b MIGAL GALILEE TECHNOLOGY CENTER   (Israel)

^c TEL HAI COLLEGE   (Israel)

Author keywords

ABCA1; Cholesterol efflux; GSH; Macrophages; Oxidative stress; Quercetin

Indexed keywords

APOLIPOPROTEIN A1; CHOLESTEROL; GLUTATHIONE; HIGH DENSITY LIPOPROTEIN; QUERCETIN;

ANIMAL; CELL LINE; DOSE RESPONSE; DRUG EFFECTS; MACROPHAGE; METABOLISM; MOUSE;

ANIMALS; APOLIPOPROTEIN A-I; CELL LINE; CHOLESTEROL; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; LIPOPROTEINS, HDL; MACROPHAGES; MICE; QUERCETIN;

EID: 84908679387     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.963574     Document Type: Article

References (46)

1. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011;145:341-355.
2. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011;473:317-325.
3. Aeddula NR, Trivedi N, Pathireddy S. Cholesterol efflux capacity and atherosclerosis. N Engl J Med 2011;364:1472-1473.
4. Rifici VA, Khachadurian AK. Oxidation of high density lipoproteins: characterization and eff ects on cholesterol efflux from J774 macrophages. Biochim Biophys Acta 1996;1299:87-94.
5. Marcil V, Delvin E, Sané AT, Tremblay A, Levy E. Oxidative stress influences cholesterol efflux in THP-1 macrophages: role of ATP-binding cassette A1 and nuclear factors. Cardiovasc Res 2006;72:473-482.
6. Mackness B, Beltran-Debon R, Aragones G, Joven J, Camps J, Mackness M. Human tissue distribution of paraoxonases 1 and 2 mRNA. IUBMB Life 2010;62:480-482.
7. Rosenblat M, Elias A, Volkova N, Aviram M. Monocytemacrophage membrane possesses free radicals scavenging activity: stimulation by polyphenols or by paraoxonase 1 (PON1). Free Radic Res 2013;47:257-267.
8. Rozenberg O, Shih DM, Aviram M. Paraoxonase 1 (PON1) attenuates macrophage oxidative status: studies in PON1 transfected cells and in PON1 transgenic mice. Atherosclerosis 2005;181:9-18.
9. Rosenblat M, Gaidukov L, Khersonsky O, Vaya J, Oren R, Tawfik DS, Aviram M. The catalytic histidine dyad of high density lipoprotein-associated serum paraoxonase-1 (PON1) is essential for PON1-mediated inhibition of low density lipoprotein oxidation and stimulation of macrophage cholesterol efflux. J Biol Chem 2006;281:7657-7665.
10. Cohen E, Aviram M, Khatib S, Rabin A, Mannheim D, Karmeli R, Vaya J. Increased levels of human carotid lesion linoleic acid hydroperoxide in symptomatic and asymptomatic patients is inversely correlated with serum HDL and paraoxonase 1 activity. J Lipids 2012;2012:762560.
11. Rosenblat M, Volkova N, Coleman R, Aviram M. Anti-oxidant and anti-atherogenic properties of liposomal glutathione: studies in vitro, and in the atherosclerotic apolipoprotein E-deficient mice. Atherosclerosis 2007;195:e61-e68.
12. Siasos G, Tousoulis D, Tsigkou V, Kokkou E, Oikonomou E, Vavuranakis M, et al. Flavonoids in atherosclerosis: an overview of their mechanisms of action. Curr Med Chem 2013;20:2641-2660.
13. Loke WM, Proudfoot JM, Hodgson JM, McKinley AJ, Hime N, Magat M, et al. Specific dietary polyphenols attenuate atherosclerosis in apolipoprotein E-knockout mice by alleviating inflammation and endothelial dysfunction. Arterioscler Thromb Vasc Biol 2010;30:749-757.
14. Rosenblat M, Volkova N, Attias J, Mahamid R, Aviram M. Consumption of polyphenolic-rich beverages (mostly pomegranate and black currant juices) by healthy subjects for a short term increased serum antioxidant status, and the serum's ability to attenuate macrophage cholesterol accumulation. Food Funct 2010;1:99-109.
15. Bischoff SC. Quercetin: potentials in the prevention and therapy of disease. Curr Opin Clin Nutr Metab Care 2008;11:733-740.
16. Aviram R, Aviram M. Onion juice polyphenols inhibits LDL oxidation: stimulatory eff ect of juice storage and of the onion outer peel juice. Free Radic Res 2002;36:69-70.
17. Kleemann R, Verschuren L, Morrison M, Zadelaar S, van Erk MJ, Wielinga PY, Kooistra T. Anti-inflammatory, anti-proliferative and anti-atherosclerotic eff ects of quercetin in human in vitro and in vivo models. Atherosclerosis 2011;218:44-52.
18. Hayek T, Fuhrman B, Vaya J, Rosenblat M, Belinky P, Coleman R, et al. 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 1997;17:2744-2752.
19. Chang YC, Lee TS, Chiang AN. Quercetin enhances ABCA1 expression and cholesterol efflux through a p38-dependent pathway in macrophages. J Lipid Res 2012;53:1840-1850.
20. Blois MS. Antioxidant determination by the use of a stable free radical. Nature 1958;181:1199-1200.
21. Aviram M. Plasma lipoprotein separation by discontinuous density gradient ultracentrifugation in hyperlipoproteinemic patients. Biochem Med 1983;30:111-118.
22. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
23. LeBel CP, Ischiropoulos H, Bondy SC. Evaluation of the probe 2', 7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 1992;5:227-231.
24. El-Saadani M, Esterbauer N, El-Sayed M, Goher M, Nassar AY, Jurgens G. Spectrophotometric assay for lipid peroxides in serum lipoproteins using commercially available reagent. J Lipid Res 1989;30:627-630.
25. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: application to mammalian blood and other tissues. Anal Biochem 1969;27:502-522.
26. Koren E, Kohen R, Ginsburg I. Polyphenols enhance total oxidant-scavenging capacities of human blood by binding to red blood cells. Exp Biol Med 2010;235:689-699.
27. Efrat M, Aviram M. Macrophage paraoxonase 1 (PON1) binding sites. Biochem Biophys Res Commun 2008;376:105-110.
28. Gu X, Kozarsky K, Krieger M. Scavenger receptor class B, type I-mediated [3H] cholesterol efflux to high and low density lipoproteins is dependent on lipoprotein binding to the receptor. J Biol Chem 2000;275:29939-30001.
29. Rosenblat M, Vaya J, Shih D, Aviram M. Paraoxonase 1 (PON1) enhances HDL-mediated macrophage cholesterol efflux via the ABCA1 transporter in association with increased HDL binding to the cells: a possible role for lysophosphatidylcholine. Atherosclerosis 2005;179:69-77.
30. Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Bio 2010;30:139-143.
31. Ye D, Lammers B, Zhao Y, Meurs L, Van Berkel TJ, Van Eck M. ATP-binding cassette transporter A1 and G1, HDL metabolism, cholesterol efflux, and inflammation: important targets for treatment of atherosclerosis. Cur Drug Targets 2011;12:647-660.
32. Shao B. Site-specific oxidation of apolipoprotein A-I impairs cholesterol export by ABCA1, a key cardioprotective function of HDL. Biochim Biophys Acta 2012;1821:490-501.
33. Chinetti G, Lestavel S, Bocher V, Remaley AT, Neve B, Torra IP, et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med 2001;7:53-58.
34. Liu Y, Tang C. Regulation of ABCA1 functions by signaling pathways. Biochim Biophys Acta 2012;1821:522-529.
35. Tang C, Vaughan AM, Oram JF. Janus kinase 2 modulates the apolipoprotein interactions with ABCA1 required for removing cellular cholesterol. J Bio Chem 2004;279:7622-7628.
36. Hu XM, Yuan B, Tanaka S, Zhou Q, Onda K, Toyoda H, Hirano T. Involvement of oxidative stress associated with glutathione depletion and p38 mitogen-activated protein kinase activation in arsenic disulfide-induced diff erentiation in HL-60 cells. Leuk Lymphoma 2014;55:392-404.
37. Meister A, Anderson ME. Glutathione. Annu Rev Biochem 1983;52:711-760.
38. Jones DP, Carlson JL, Mody VC, Cai J, Lynn MJ, Sternberg P. Redox state of glutathione in human plasma. Free Radic Biol Med 2000;28:625-635.
39. Gould NS, Min E, Day BJ. Macropinocytosis of extracellular glutathione ameliorates tumor necrosis factor α release in activated macrophages. PLoS One 2011;6:e25704.
40. Rouzer CA, Scott WA, Griffith OW, Hamill AL, Cohn ZA. Glutathione metabolism in resting and phagocytizing peritoneal macrophages. J Biol Chem 1982;257:2002-2008.
41. Bannai S, Tateishi N. Role of membrane transport in metabolism and function of glutathione in mammals. J Membrane Biol 1986;89:1-8.
42. Wang NI, Lan D, Chen W, Matsuuara F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc Natl Acad Sci U S A 2004;101:9774.
43. Yassine HN, Belopolskaya A, Schall C, Stump CS, Lau SS, Reaven PD. Enhanced cholesterol efflux to HDL through the ABCA1 transporter in hypertriglyceridemia of type 2 diabetes. Metabolism 2014;63:727-734.
44. Bogani P, Canavesti M, Hagen TM, Visioli F, Bellosta S. Thiol supplementation inhibits metalloproteinase activity independent of glutathione status. Biochem Biophys Res Commun 2007;363:651-655.
45. Pereira RB, Sousa C, Costa A, Andrade PB, Valentão P. Glutathione and the antioxidant potential of binary mixtures with flavonoids: synergisms and antagonisms. Molecules 2013;18:8858-8872.
46. Boots AW, Kubben N, Haenen GR, Bast A. Oxidized quercetin reacts with thiols rather than with ascorbate: implication for quercetin supplementation. Biochem Biophys Res Commun 2003;308:560-565.