The antioxidant properties of high-density lipoproteins in atherosclerosis

Panminerva Medica

Volumn 54, Issue 2, 2012, Pages 83-90

  Mackness, B ^a   Mackness, M ^b  

^a Private Practitioner   (Spain)

^b NONE   (Spain)

Author keywords

Atherosclerosis; HDL; Lipoproteins; Oxidation; Reduction

Indexed keywords

EID: 84862542056     PISSN: 00310808     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. Gordon DJ, Probstfield JL, Garrison RJ, Neaton JD, Castelli WP, Knoke JD et al. High-density lipoprotein cholesterol and cardiovascular disease. Four prospective American studies. Circulation 1989;79:8-15. (Pubitemid 19043669)
2. Shah PK. Evolving concepts on benefits and risks associated with therapeutic strategies to raise HDL. Curr Opin Cardiol 2010;25:6038.
3. nd edition. London: Butterworth Heinemann; 1995.
4. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol modifications of low-density lipoprotein that increase its atherogenicity. New Engl J Med1989;320:915-24. (Pubitemid 19101597)
5. Lusis AJ. Atherosclerosis. Nature 2000;407:233-41.
6. Chisholm GM, Penn MS. Oxidised lipoproteins and atherosclerosis. In: Fuster V, Ross R, Topol EJ, editor. Atherosclerosis and coronary artery disease. Philadelphia: Lippincott-Raven; 1996. p. 129-49.
7. Endemann G, Stanton LW, Madden KS, Bryant CM, White RT, Protter AA. CD36 is a receptor for oxidised low density lipoprotein. J Biol Chem 1993;268:11811-6. (Pubitemid 23168135)
8. Rice-Evans C, Bruckdorfer KR. Free radicals, lipoproteins and cardiovascular dysfunction. Molec Aspects Med 1992; 13:1.
9. Esterbauer H, Gebicki J, Puhl H, Jurgens G. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Rad Biol Med 1992;13:341-50.
10. Meister A. On the antioxidant effects of ascorbic acid and glutathione. Biochem Pharmacol 1992;44:1905-11.
11. Mackness MI, Durrington PN. High density lipoprotein, its enzymes and its potential to influence lipid peroxidation. Atherosclerosis 1995;115:243-53.
12. Klimov AN, Kozhemyakin LA, Pleskov VM, Andreeva LI. Antioxidative effect of high density lipoproteins in the oxidation of low density lipoproteins. Bull Exp Biol Med (Russ) 1987;103:550-6.
13. 2+-catalysed oxidation of human low-density lipoprotein. FEBS Letts 1989;257:435-8.
14. Mackness MI, Abbott CA, Arrol S, Durrington PN. The role of high density lipoprotein and lipid-soluble antioxidant vitamins in inhibiting low-density lipoprotein oxidation. Biochem J 1993;294:829-35.
15. Parthasarathy S, Barnett J, Fong LG. High-density lipoprotein inhibits the oxidative modification of low-density lipoprotein. Biochim Biophys Acta 1990;1044:275-83. (Pubitemid 20151285)
16. Klimov AN, Gurevich VS, Nikiforova AA, Shatilina LV, Kuzmin AA, Plavinsky SL et al. Antioxidative activity of high-density lipoproteins in vivo. Atherosclerosis 1993;100:13-9.
17. Klimov AN, Nikiforova AA, Kuzmin AA, Kuznetsov AS, Mackness MI. Is high density lipoprotein a scavenger for oxidised phospholipids of low density lipoprotein? Advances in Lipoprotein and Atherosclerosis Research, Diagnostics and Treatment. Jena: Gustav Fischer Verlag; 1998. p. 78-82.
18. Eisenberg S. High density lipoprotein metabolism. J Lipid Res 1984;25:1017-58.
19. Chander R, Kapoor NK. High density lipoprotein is a scavenger of superoxide ions. Biochem Pharmacol 1990;40:1663-8.
20. Kunitake ST, Jarvis MR, Hamilton RL, Kane JP. Binding of transition metals by apolipoprotein A-I containing plasma lipoproteins:Inhibition of oxidation of low density lipoproteins. Proc Natl Acad Sci USA 1992;89:6993-7.
21. Navab M, Hama SY, Anantharamaiah GM, Hassan K, Hough GP, Watson AD et al Normal high density lipoprotein inhibits three steps in the formation of mildly oxidised low density lipoprotein: steps 2 and 3. J Lipid Res 2000;41:1495-508.
22. Sattler W, Stocker R. Greater selective uptake by Hep G2 cells of high density lipoprotein cholesterylester hydroperoxides than unoxidised cholesterylesters. Biochem J 1993;294:771-6.
23. Hessler JR, Morel DW, Lewis LJ, Chisholm GM. Lipoprotein oxidation and lipoprotein induced cytotoxicity. Arteriosclerosis 1983;3:215-22.
24. Hessler JR, Robertson AL, Chisholm GM. LDL-induced cytotoxicity and its inhibition by HDL in human vascular smooth muscle and endothelial cells in culture. Atherosclerosis 1979;32:213-29. (Pubitemid 9129780)
25. Morel DW, Hessler JR, Chisholm GM. Low density lipoprotein cytotoxicity induced by free radical peroxidation of lipid. J Lipid Res 1983;24:1070-6. (Pubitemid 13002345)
26. Chung BH, Segrest JP, Smith K, Griffin FM, Brouillette CG. Lipolytic surface remnants of triglyceride-rich lipoproteins are cytotoxic to macrophages but not in the presence of high density lipoprotein. J Clin Invest 1989;83:1363-74. (Pubitemid 19113054)
27. Zwijsen RML, De Haan LHJ, Kuivenhoven JA, Nusselder ICJ. Modulation of low-density lipoprotein induced inhibition of intracellular communications by antioxidants and high density lipoproteins. Fd Chem Toxic 1991;29:615-20.
28. Schmidt K, Klatt P, Graier WF, Kostner GM, Kukovetz WR. High density lipoprotein antagonizes the inhibitory effects of oxidised low density lipoprotein and lysolecithin on soluble gyanyl cyclase. Biochem Biophys Res Comms 1992;182:302-8.
29. Navab M, Imes SS, Hama SY, Hough GP, Ross LA, Bork RW et al. Monocyte Transmigration induced by modification of low density lipoprotein in cocultures of human aortic wall cells is due to indue-. tion of monocyte chemotactic protein 1 synthesis and is abolished by high density lipoprotein. J Clin Invest 1991;88:2039-46.
30. Vaisar T, Pennathur S, Green PS, Gharib SA, Hoofnagle AN, Cheung MC. Shotgun proteomics implicates protease inhibition and complement activation in the anti-inflammatory properties of HDL. J Clin Invest 2007;117:746-56. (Pubitemid 46348533)
31. Garner B, Waldeck AR, Witting PK, Rye KA, Stocker R. Oxidation of high density lipoproteins II. Evidence for direct reduction of lipid hydroperoxides by methionine residues of apolipoproteins Al and All. J Biol Chem 1998;273:6088-95. (Pubitemid 28144688)
32. Klimov AN, Nikiforova AA, Pleskov VM, Kuz'min AA, Kalashnikova NN, Antipova TO. The protective action of high-density lipoproteins, their subfractions and lecithin-cholesterol acyltransferase in the peroxide modification of low-density lipoproteins. Biokkimiya 1989;54:118-23. (Pubitemid 19038428)
33. Vohl M-C, Neville TA-M, Kumarathasan R, Braschi S, Sparks DL. A novel lecithin-cholesterol acyltransferase antioxidant activity prevents the formation of oxidised lipids during lipoprotein oxidation. Biochemistry 1999;32:5976-81.
34. Hine D, Mackness B, Mackness M. Coincubation of PON1, APO A1 and LCAT increases the time HDL is able to prevent LDL oxidation. IUBMB Life 2011; in press
35. Howlader Z, Kamiyama S, Shirakawa H, Murakami Y, Ito M, Komai H el al. Detoxification of oxidised LDL by transferring its oxidation products to lecithin: cholesterol acyltransferase. Biochem Biophys Res Comm 2002;291:758-63. (Pubitemid 34694339)
36. Goyal J, Wang K, Liu M, Subbaiah PV. Novel function of lecithincholesterol acyltransferase. Hydrolysis of oxidised polar phospholipids generated during lipoprotein oxidation. J Biol Chem 1997;272:16231-9. (Pubitemid 27276442)
37. Nagata Y, Yamamoto Y, Niki E. Reaction of phosphatidylcholine hydroperoxide in human plasma: the role of lecithin: cholesterol acyltransferase. Arch Biochem Biophys 1996;329:24-30. (Pubitemid 26143393)
38. Jimi S, Uesugi N, Saku K, habe H, Zhang B, Arakawa K et al. Possible induction of renal dysfunction in patients with lecithin: cholesterol acyltransferase deficiency by oxidised phoshocholine in glomeruli. Arterioscl Thromb Vase Biol 1999;19:794-801. (Pubitemid 29135186)
39. Ng DS, Maguire GF, Wylie J, Ravandi A, Xuan W, Ahmed Z et al. Oxidative stress is markedly elevated in lecithin: cholesterol acyltransferase deficient mice and is paradoxically reversed in apolipoprotein knockout background in association with a reduction in atherosclerosis. J Biol Chem 2002;277:11715-20. (Pubitemid 34952725)
40. Mertens A, Verhamme P, Bielicki JK, Phillips MC, Quarck R, Verreth W et al. Increased low density lipoprotein oxidation and impaired high density lipoprotein antioxidant defense are associated with increased macrophage homing and atherosclerosis in dyslipidemic obese mice. LCAT gene transfer decreases atherosclerosis. Circulation 2003;107:1640-6 (Pubitemid 36397333)
41. 3 particles in type 2 diabetes: relationship to elevated oxidative stress and hyperglycaemia. Diabetologia 2005;48:529-38
42. Rappelle PJWH, de Boer JF, Perton FG, Annema W, de Vries R, Dullaart RPF et al. Increased LCAT activity and hyperglycaemia decrease the antioxidative functionality of HDL. Eur J Clin Invest 2011 [Epub ahead of print].
43. Primo-Parma SL, Sorenson RC, Teiber J, La Du BN. The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics 1996;33:498-509.
44. Rodriguez-Sanabria F, Rull A, Beltran-Debon R, Aragonés G, Camps J, Mackness B et al. Tissue distribution and expression of paraoxonases and chemokines in the mouse: the ubiquitous and joint localisation suggest a systemic and coordinated role. J Mol Histol 2010;41:379-86.
45. Marsillach J, Camps J, Beltran-Debon R, Rull A, Aragones G, Maestre-Martinez C et al. Immunohistochemical analysis of paraoxonases 1 and 3 in human atheromatous plaques. Eur J Clin Invest 2011;41:308-14.
46. Ng CJ, Wadleigh DJ, Gangopadhyay A, Hama S, Grijalva VR, Navab M et al. Paraoxonase-2 is a ubiquitously expressed protein with antioxidant properties and is capable of preventing cell-mediated oxidative modification of low density lipoprotein. J Biol Chem 2001;276:4444-9.
47. Aviram M, Rosenblat M. Paraoxonases 1, 2, and 3, oxidative stress, and macrophage foam cell formation during atherosclerosis development. Free Radie Biol Med 2004;37:1304-16. (Pubitemid 39349234)
48. Kim JB, Xia Y-R, Romanoski CE, Lee S, Meng YH, Shi Y-S et al. paraoxonase-2 modulates stress response of endothelial cells to oxidised phospholipids and a bacterial quorum sensing molecule. Arterioscl Thromd Vase Biol 2011 [Epub ahead of print].
49. Koren-Gluzer M, Aviram M, Meilin E, Hayek T. The antioxidant HDL-associated paraoxonase-1 (PON1) attenuates diabetes development and stimulates ß-cell insulin release. Atherosclerosis 2011 [Epub ahead of print].
50. Mackness MI, Arrol S, Durrington PN. Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Letts 1991;286:152-4.
51. Aviram M, Billecke S, Sorenson R, Bisgaier C, Newton R, Rosenblat M el al. Paraoxonase active site required for protection against LDL oxidation involves its free sulphydryl group and is different from that required for its arylesterase/paraoxonase activities: selective action of human paraoxonase alloenzymes Q and R. Arterioscl Thromb Vase Biol 1998;10:1617-24. (Pubitemid 28465415)
52. Watson AD, Berliner JA, Hama SY, La Du BN, Fault KF, Fogelman AM et al. Protective effect of high density lipoprotein associated paraoxonase - Inhibition of the biological activity of minimally oxidised low-density lipoprotein. J Clin Invest 1995;96:2882-91.
53. Ahmed Z, Ravandi A, Maguire GF, Emili A, Draganov D, La Du BN et al. Apolipoprotein AI promotes the formation of phosphatidylcholine core aldehydes that are hydrolysed by paraoxonase (PON1) during high density lipoprotein oxidation with a peroxynitrite donor. J Biol Chem 2001;276:24473-81.
54. Draganov DI, La Du BN. Pharmacogenetics of paraoxonase:a brief review. Naunyn-Schmiedeberg's Arch Pharmacol 2004;369:7888.
55. Aviram M, Rosenblat M, Bisgaier CL, Newton RS, Primo-Parmo SL, La Du BN. Paraoxonase inhibits high-density lipoprotein and preserves its functions. J Clin Invest 1998;101:1581-90.
56. Mastorikuo M, Mackness B, Liu Y, Mackness M. Glycation of paraoxonase-1 inhibits its activity and impairs the ability of HDL to metabolise membrane lipid hydroperoxides. Diabetic Med 2008;25:1049-55.
57. Tavori H, Aviram M, Khatib S, Musa R, Mannheim D, Karmeli R et al. Paraoxonase 1 protects macrophages from atherogenicity of a specific triglyceride isolated from human carotid lesion. Free Rad Biol Med 2011;51:234-42.
58. Mackness B, Hine D, Liu Y, Mastorikou M, Mackness M. Paraoxonase 1 inhibits oxidised LDL-induced MCP-I production by endothelial cells. BBRC 2004;318:680-3. (Pubitemid 38624207)
59. Mackness B, Durrington PN, Mackness MI. Polymorphisms of paraoxonase genes and low-density lipoprotein lipid peroxidation. Lancet 1999;353:468-9. (Pubitemid 29067347)
60. Mackness B, Davies GK, Turkie W, Lee E, Roberts DH, Hill E et al. Paraoxonase status in coronary heart disease. Are activity and concentration more important than genotype? Arterioscler Thromb Vase Biol 2001;21:1451-7. (Pubitemid 34219807)
61. Wheeler JG, Keavney BD, Watkins H, Collins R, Danesh J. Four paraoxonase gene polymorphisms in 11212 cases of coronary heart disease and 12786 controls: meta-analysis of 43 studies. Lancet 2004;363:689-95. (Pubitemid 38296555)
62. Mackness B, Durrington P, McElduff P, Yamell J, Azam N, Watt M et al. Low paraoxonase activity predicts coronary events in the Caerphilly Prospective Study. Circulation 2003;107:2775-9. (Pubitemid 36705985)
63. Bhattacharyya T, Nicholls SJ, Topol EJ, Zhang R, Yang X, Schmitt D et al. Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. JAMA 2008;299:1265-76. (Pubitemid 351439073)
64. van Himbergen TM, van der Schouw YT, Voorbij HAM, van Tits LJH, Stalenhoef AFH et al. Paraoxonase (PON1) and the risk for coronary heart disease and myocardial infarction in a general population of Dutch women. Atherosclerosis 2008;198:408-14.
65. Ikeda Y, Inoue M, Suehiro T, Arii K, Kumon Y, Hashimoto K. Low human paraoxonase predicts cardiovascular events in Japanese patients with type 2 diabetes. Acta Diabetol 2009;46:239-42.
66. Troughton JA, Woodside JV, Yarnell JWG, Arveiler D, Amouyel P, Ferneres J et al. Paraoxonase activity and coronary heart disease in healthy middle-aged males:The PRIME study. Atherosclerosis 2008;197:556-63 (Pubitemid 351417899)
67. Birjmohun RS, Vergeer M, Stroes ES, Sandhu MS, Ricketts SL, Tanck MW et al. Both paraoxonase-1 genotype and activity do not predict the risk of future coronary artery disease; the EPIC- Norfolk prospective population study. PLoS One 2009;4:e6809.
68. Ikeda Y, Suehiro T, Itahara T, Inui Y, Chikazawa H, Inoue M et al. Human serum paraoxonase concentration predicts cardiovascular mortality in hemodialysis patients. Clin Nephrol 2007;67:358-65 (Pubitemid 46894800)
69. Shih DM, Gu L, Xia Y-R, Navab M, Li W-F, Hama S et al. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 1998;394:284-7. (Pubitemid 28335041)
70. Tward A, Xia YR, Wang XP, Shi YS, Park C, Castellani LW et al. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation 2002;106:484-90. (Pubitemid 34803695)
71. Rozenberg O, Shih DM, AviramM. Paraoxonase 1 (PON1) attenuates macrophage oxidative status: studies in PON1 transfected cells and in PON1 transgenic mice. Atherosclerosis 2005;181:9-18. (Pubitemid 40804688)
72. Mackness B, Quarck R, Verreth W, Mackness M, Holvoet P. Human paraoxonase-1 overexpression inhibits atherosclerosis in a mouse model of metabolic syndrome. Arterioscler Thromb Vase Biol 2006;26:1545-50. (Pubitemid 44288981)
73. Guns P-J, Van Assche T, Verreth W, Fransen P, Mackness B, Mackness M et al. Paraoxonase 1 gene transfer lowers vascular oxidative stress and improves vasomotor function in apolipoprotein Edeficient mice with pre-existing atherosclerosis. Br J Pharmacol 2008;153:508-16. (Pubitemid 351199014)
74. Rozenberg O, Shiner M, Aviram M, Hayek T. Paraoxonase 1 (PON1) attenuates diabetes development in mice through its antioxidative properties. Free Rad Biol Med 2008;44:1951-9.
75. Reddy ST, Wadleigh DJ, Grijalva V, Ng C, Hama S, Gangopadhyay A et al. Human paraoxonase-3 is an HDL-associated enzyme with biological activity similar to paraoxonase-1 protein but is not regulated by oxidised lipids. Arterioscl Thromb Vase Biol 2001;21:542-7. (Pubitemid 32323386)
76. Draganov DI, Stetson PL, Watson CE, Billecke SS, La Du BN. Rabbit serum paraoxonase 3 (PON3) is a high density lipoproteinassociated lactonase and protects low density lipoprotein against oxidation. J Biol Chem 2000;275:33435-442.
77. Liu Y, Mackness B, Mackness M. Comparison of the ability of paraoxonases 1 and 3 to attenuate the in vitro oxidation of low- density lipoprotein and reduce macrophage oxidative stress. Free Rad Biol Med 2008;45:743-8.
78. Aragones G, Guardiola M, Barreda M, Marsillach J, Debon RB, Rull A et al. Measurement of serum PON-3 concentration: method evaluation, reference values, and the influence of genotypes in a population based study. J Lipid Res 2011;52:1055-61.
79. Shih CM, Xia YR, Wang XP, Wang SS, Bourquard N, Fogelman AM et al. Decreased obesity and atherosclerosis in human paraoxonase 3 transgenic mice. Circ Res 2007;100:1200-1207 (Pubitemid 46684133)
80. Ng CJ, Bourquard N, Hama SY, Shih D, Grijalva VR, Navab M et al. Adenovirus-mediated expression of human paraoxonase 3 protects against the progression of atherosclerosis in apolipoptotein Edeficient mice. Arterioscl Thromb Vase Biol 2007;27:1368-74. (Pubitemid 46809427)
81. Rull A, Garcia R, Sender LF, Heredia AG, Aragones G, Debon RB et al. Serum paraoxonase-3 concentration is associated with insulin sensitivity in peripheral vascular disease and with inflammation in coronary artery disease. Atherosclerosis 2011 [Epub ahead of print].
82. Kempster SL, Belteki G, Licence D, Charnock-Jones DS, Smith GCS. Disruption of paraoxonase 3 impairs proliferation and antioxidant defenses in human A549 cells and causes embryonic lethality in mice. Am J Physiol Endocrinol Metab 2011 [Epub ahead of print].
83. Hine D, Mackness B, Mackness M. Cholesteryl-ester transfer protein enhances the ability of high-density lipoprotein to inhibit lowdensity lipoprotein oxidation. IUBMB Life 2011;63:772-4.
84. Yan D, Navab M, Bruce C, Fogelman AM, Jiang XC. PLTP deficiency improves the anti-inflammatory properties of HDL and reduces the ability of LDL to induce monocyte chemotactic activity. J Lipid Res 2004;45:1852-8. (Pubitemid 40990877)
85. Schlitt A, Liu J, Yan D, Mondragon-Escorpizo M, Norm AJ, Jiang XC. Anti-inflammatory effects of phospholipid transfer protein (PLTP) deficiency in mice. Biochim Biophys Acta 2005;1733:187-91.
86. Ahmed MS, Ji JZ, Meng QM. Lipoprotein-associated phospholipase A2:How effective as a risk marker of cardiovascular disease and as a therapeutic target? Inflamm Allergy-Drug Targets 2011; 10:236-46.