Human serum paraoxonase 1 decreases macrophage cholesterol biosynthesis: Possible role for its phospholipase-A2-like activity and lysophosphatidylcholine formation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 3, 2003, Pages 461-467

  Rozenberg, Orit ^a   Shih, Diana M ^b   Aviram, Michael ^a  

^a RAMBAM MEDICAL CENTER   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cholesterol biosynthesis; Lysophosphatidylcholine; Macrophage; Paraoxonase; Phospholipase A2

Indexed keywords

ARACHIDONIC ACID; ARYLDIALKYLPHOSPHATASE; CHOLESTEROL; LANOSTEROL; LINOLEIC ACID; LYSOPHOSPHATIDYLCHOLINE; MESSENGER RNA; MEVALONIC ACID; PHOSPHOLIPASE A2; POLYUNSATURATED FATTY ACID;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVITY; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MASS SPECTROMETRY; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPECTROPHOTOMETRY; THIN LAYER CHROMATOGRAPHY;

ANIMALS; ARTERIOSCLEROSIS; ARYLDIALKYLPHOSPHATASE; CATTLE; CELLS, CULTURED; CHO CELLS; CHOLESTEROL; CHOLESTEROL, HDL; CRICETINAE; ESTERASES; FATTY ACIDS; HUMANS; LYSOPHOSPHATIDYLCHOLINES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PHOSPHOLIPASES A; RNA, MESSENGER;

EID: 0037341390     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000060462.35946.B3     Document Type: Article

References (44)

1. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell. 2001;104:503-516.
2. Aviram M. Macrophage foam cell formation during early atherogenesis is determined by the balance between pro-oxidants and anti-oxidants in arterial cells and blood lipoproteins. Antiox Redox Signal. 1999;1:585-594.
3. Kruth HS, Huang W, Ishii I, Zhang WY. Macrophage foam cell formation with native low density lipoprotein. J Biol Chem. 2002;277:34573-34580.
4. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol: modifications of LDL that increase its atherogenicity. N Engl J Med. 1989;320:915-924.
5. Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M. Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ Res. 2002;90:270-276.
6. Keidar S, Attias J, Heinrich R, Coleman R, Aviram M, Angiotensin-II atherogenicity in apolipoprotein E-deficient mice is associated with increased cellular cholesterol biosynthesis. Atherosclerosis. 1999;146:249-257.
7. Aviram M, Hardak E, Vaya J, Mahmood S, Milo S, Hoffman A, Billicke S, Draganov D, Rosenblat M. Human serum PON1 Q and R selectively decrease lipid peroxides in human coronary and carotid atherosclerotic lesions: PON1 esterase and peroxidase-like activities. Circulation. 2000;101:2510-2517.
8. Mackness B, Hunt R, Durrington PN, Mackness MI. Increased immunolocalization of paraoxonase, clusterin, and apolipoprotein A-I in the human artery wall with the progression of atherosclerosis. Arterioscler Thromb Vasc Biol. 1997;17:1233-1238.
9. Tward A, Xia YR, Wang XP, Shi YS, Park C, Castellani LW, Lusis AJ, Shih DM. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation. 2002;106:484-490.
10. Aviram M. Does paraoxonase play a role in susceptibility to cardiovascular disease? Mol Med Today. 1999;5:381-386.
11. Aviram M, Rosenblat M, Bisgaier CL, Newton RS, Primo-Parmo SL, La Du BN. Paraoxonase inhibits HDL oxidation and preserves its functions: a possible peroxidative role for paraoxonase. J Clin Invest. 1998;101:1581-1590.
12. Durrington PN, Mackness B, Mackness MI. Paraoxonase and atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:473-480.
13. Ayub A, Mackness MI, Arrol S, Mackness B, Patel J, Durrington PN. Serum paraoxonase after myocardial infarction. Arterioscler Thromb Vasc Biol. 1999;19:330-335.
14. Shih DM, Gu L, Hama S, Xia YR, Navab M, Fogelman AM, Lusis AJ. Genetic-dietary regulation of serum paraoxonase expression and its role in atherogenesis in a mouse model. J Clin Invest. 1996;97:1630-1639.
15. Shih DM, Gu L, Xia YR, Navab M, Li WF, Hama S, Castellani LW, Furlong CE, Costa LG, Fogelman AM, Lusis AJ. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature. 1998;394:284-287.
16. Shih DM, Xia YR, Wang XP, Miller E, Castellani LW, Subbanagounder G, Cheroutre H, Faull KF, Berliner JA, Witztum JL, Lusis AJ. Combined serum paraoxonase knockout/apolipoprotein E-knockout mice exhibit increased lipoprotein oxidation and atherosclerosis. J Biol Chem. 2000;275:17527-17535.
17. Gan K, Smolen A, Eckerson HW, La Du BN. Purification of human serum paraoxonase/arylesterase: evidence for one esterase catalyzing both activities. Drug Metab Dispos. 1991;19:100-106.
18. Costa LG, Li WF, Richter RJ, Shih DM, Lusis A, Furlong CE. The role of PON1 in the detoxication of organophosphates and its human polymorphism. Chem Biol Interact. 1999;119-120:429-438.
19. Aviram M, Billecke S, Sorenson R, Bisgaier C, Newton R, Rosenblat M, Erogul J, Hsu C, Dunlop C, La Du BN. Paraoxonase active site required for protection against LDL oxidation involves its free sulfhydryl group and is different from that required for its arylesterase/paraoxonase activities: selective action of human paraoxonase allozymes Q and R. Arterioscler Thromb Vasc Biol. 1998;18:1617-1624.
20. Navab M, Berliner JA, Watson AD, Hama SY, Territo MC, Lusis AJ, Shih DM, Van Lenten BJ, Frank JS, Demer LL, Edwards PA, Fogelman AM, The yin and yang of oxidation in the development of the fatty streak. Arterioscler Thromb Vasc Biol. 1996;16:831-842.
21. Billecke S, Draganov D, Counsell R, Stetson P, Watson C, Hsu C, La Du BN. Human serum PON1 isozymes Q and R hydrolyze lactones and cyclic carbonate esters. Drug Metab Dispos. 2000;28:1335-1342.
22. Ahmed Z, Ravandi A, Maguire GF, Emili A, Draganov D, La Du BN, Kuksis A, Connelly PW. Apolipoprotein A-I promotes the formation of phosphatidylcholine core aldehydes that are hydrolyzed by paraoxonase (PON-1) during HDL oxidation with a peroxynitrite donor. J Biol Chem. 2001;276:24473-24481.
23. Ahmed Z, Ravandi A, Maguire GF, Emili A, Draganov D, La Du BN, Kuksis A, Connelly PW. Multiple substrates for paraoxonase-1 during oxidation of phosphatidylcholine by peroxynitrite. Biochem Biophys Res Commun. 2002;290:391-396.
24. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
25. Goldshmidt O, Zcharia E, Abramovich R, Metzger S, Aingorn H, Friedmann Y, Schirrmacher V, Mitrani E, Vlodavsky I. Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc Natl Acad Sci U S A. 2002;99:10031-10036.
26. Lowry OH, Rosebrough NJ, Farr L, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-275.
27. Kaplan M, Aviram M, Knopf C, Keidar S, Angiotensin-II reduces macrophage cholesterol efflux: a role for the AT-1 receptor but not for the ABC1 transporter. Biochem Biophys Res Commun. 2002;290:1529-1534.
28. Vesterqvist O, Sargent CA, Grover GJ, Warrack BM, DiDonato GC, Ogletree ML. Characterization of rabbit myocardial phospholipase-A2 activity using endogenous phospholipid substrates. Anal Biochem. 1994;217:210-219.
29. Rosenblat M, Aviram M. Oxysterol-induced activation of macrophage NADPH-oxidase enhances cell-mediated oxidation of LDL in the atherosclerotic apolipoprotein E deficient mouse: inhibitory role for vitamin E. Atherosclerosis. 2002;160:69-80.
30. Aviram M, Rosenblat M, Billecke S, Erogul J, Sorenson R, Bisgaier CL, Newton RS, La Du B. Human serum PON1 is inactivated by Ox-LDL and preserved by antioxidants. Free Radic Biol Med. 1999;26:892-904.
31. Primo-Parmo SL, Sorenson RC, Teiber J, La Du BN. The human serum paraoxonase/arylesterase gene (PON1) is one member of a multigene family. Genomics. 1996;33:498-507.
32. Shin BA, Kim YR, Lee IS, Sung CK, Hong J, Sim CJ, Im KS, Jung JH. Lyso-PAF analogues and lysophosphatidylcholines from the marine sponge Spirastrella abata as inhibitors of cholesterol biosynthesis. J Natl Prod. 1999;62:1554-1557.
33. Mackness MI, Mackness B, Arrol S, Wood G, Bhatnagar D, Durrington PN. Presence of paraoxonase in human interstitial fluid. FEBS Lett. 1997;416:377-380.
34. Keller-Weibel G, Yancey PG, Jerome WG, Walser T, Mason RP, Phillips MC, Rothblat GH. Crystallization of free cholesterol in model macrophage foam cells. Arterioscler Thromb Vasc Biol. 1999;19:1891-1898.
35. Sato R, Goldstein JL, Brown MS. Replacement of serine-871 of hamster 3-hydroxy-3-methylglutaryl-CoA-reductase prevents phosphorylation by AMP-activated kinase and blocks inhibition of sterol synthesis induced by ATP depletion. Proc Natl Acad Sci U S A. 1993;90:9261-9265.
36. McTaggart F, Buckett L, Davidson R, Holdgate G, McCormick A, Snhneck D, Smith G, Warwick M. Preclinical and clinical pharmacology of Rosuvastatin, a new 3-hydroxy-3-methylglutaryl-CoA-reductase inhibitor. Am J Cardiol. 2001;87:28B-32B.
37. Koh KK. Effects of statins on vascular wall: vasomotor function, inflammation, and plaque stability. Cardiovasc Res. 2000;47:648-657.
38. Watson AD, Berliner JA, Hama SY, La Du BN, Faull KF, Fogelman AM, Navab M. Protective effect of HDL associated paraoxonase: inhibition of the biological activity of minimally Ox-LDL. J Clin Invest. 1995;96:2882-2891.
39. Petrovic N, Grove C, Langton PE, Misso NL, Thompson PJ. A simple assay for a human serum phospholipase-A2 that is associated with HDLs. J Lipid Res. 2001;42:1706-1713.
40. Schmitz G, Robenek H, Lohmann U, Assmann G. Interaction of HDLs with cholesteryl ester-laden macrophages: biochemical and morphological characterization of cell surface receptor binding, endocytosis and resecretion of HDLs by macrophages. EMBO J. 1985;4:613-622.
41. Sorenson RC, Bisgaier CL, Aviram M, Hsu C, Billecke S, La Du BN. Human serum Paraoxonase/Arylesterase's retained hydrophobic N-terminal leader sequence associates with HDLs by binding phospholipids: apolipoprotein A-I stabilizes activity. Arterioscler Thromb Vasc Biol. 1999;19:2214-2225.
42. Deakin S, Leviev I, Gomaraschi M, Calabresi L, Franceschini G, James RW. Enzymatically active paraoxonase-1 is located at the external membrane of producing cells and released by a high affinity, saturable, desorption mechanism. J Biol Chem. 2002;277:4301-4308.
43. Rozenberg O, Rosenblat M, Coleman R, Shih DM, Aviram M. Paraoxonase (PON1) deficiency is associated with increased macrophage oxidative stress: studies in PON1-knockout mice. Free Radic Biol Med. In press.
44. Rosenblat M, Draganov D, Watson CE, Bisgaier CL, La Du BN, Aviram M. Mouse macrophage paraoxonase 2 activity is increased whereas cellular paraoxonase 3 activity is decreased under oxidative stress. Arterioscler Thromb Vasc Biol. 2003;23:468-474.