Purified human paraoxonase-1 interacts with plasma membrane lipid rafts and mediates cholesterol efflux from macrophages

Free Radical Biology and Medicine

Volumn 52, Issue 8, 2012, Pages 1372-1381

  Berrougui, Hicham ^a   Loued, Soumaya ^a   Khalil, Abdelouahed ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Cholesterol efflux; Free radicals; HDL; Lipid raft; Macrophages; Paraoxonase 1

Indexed keywords

ABC TRANSPORTER A1; ARYLDIALKYLPHOSPHATASE 1; CHOLESTEROL; CYCLODEXTRIN; HIGH DENSITY LIPOPROTEIN;

ADULT; ARTICLE; CELL MEMBRANE; CHOLESTEROL TRANSPORT; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LIPID RAFT; MACROPHAGE; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; UPREGULATION;

ADULT; ARYLDIALKYLPHOSPHATASE; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; BIOLOGICAL TRANSPORT; CELL LINE; CHOLESTEROL; DNA PRIMERS; HUMANS; IMMUNOPRECIPITATION; MACROPHAGES; MEMBRANE MICRODOMAINS; POLYMERASE CHAIN REACTION;

EID: 84859001444     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.01.019     Document Type: Article

References (59)

1. Cuchel, M.; Rader, D. J. Macrophage reverse cholesterol transport: key to the regression of atherosclerosis? Circulation 113:2548-2555; 2006.
2. Ruano, J.; Lopez-Miranda, J.; Fuentes, F.; Moreno, J. A.; Bellido, C.; Perez-Martinez, P.; Lozano, A.; Gomez, P.; Jimenez, Y.; Perez Jimenez, F. Phenolic content of virgin olive oil improves ischemic reactive hyperemia in hypercholesterolemic patients. J. Am. Coll. Cardiol. 46:1864-1868; 2005.
3. Tall, A. R.; Costet, P.; Wang, N. Regulation and mechanisms of macrophage cholesterol efflux. J. Clin. Invest. 110:899-904; 2002.
4. Yancey, P. G.; Bortnick, A. E.; Kellner-Weibel, G.; de la Llera-Moya, M.; Phillips, M. C.; Rothblat, G. H. Importance of different pathways of cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23:712-719; 2003.
5. Smith, J. D. Insight into ABCG1-mediated cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 26:1198-1200; 2006.
6. Favari, E.; Lee, M.; Calabresi, L.; Franceschini, G.; Zimetti, F.; Bernini, F.; Kovanen, P. T. Depletion of pre-β-high density lipoprotein by human chymase impairs ATP-binding cassette transporter A1- but not scavenger receptor class B type Imediated lipid efflux to high density lipoprotein. J. Biol. Chem. 279:9930-9936; 2004.
7. Baldan, A.; Bojanic, D. D.; Edwards, P. A. The ABCs of sterol transport. J. Lipid Res. 50:S80-S85 (Suppl.); 2009.
8. Gu, F.; Jones, M. K.; Chen, J.; Patterson, J. C.; Catte, A.; Jerome, W. G.; Li, L.; Segrest, J. P. Structures of discoidal high density lipoproteins: a combined computational-experimental approach. J. Biol. Chem. 285:4652-4665; 2010.
9. Vaisar, T.; Pennathur, S.; Green, P. S.; Gharib, S. A.; Hoofnagle, A. N.; Cheung, M. C.; Byun, J.; Vuletic, S.; Kassim, S.; Singh, P.; Chea, H.; Knopp, R. H.; Brunzell, J.; Geary, R.; Chait, A.; Zhao, X. Q.; Elkon, K.; Marcovina, S.; Ridker, P.; Oram, J. F.; Heinecke, J. W. Shotgun proteomics implicates protease inhibition and complement activation in the antiinflammatory properties of HDL. J. Clin. Invest. 117:746-756; 2007.
10. Visioli, F.; Poli, A.; Gall, C. Antioxidant and other biological activities of phenols from olives and olive oil. Med. Res. Rev. 22:65-75; 2002.
11. Costa, L. G.; Vitalone, A.; Cole, T. B.; Furlong, C. E. Modulation of paraoxonase (PON1) activity. Biochem. Pharmacol. 69:541-550; 2005.
12. James, R. W.; Brulhart-Meynet, M. C.; Singh, A. K.; Riederer, B.; Seidler, U.; Out, R.; Van Berkel, T. J.; Deakin, S. The scavenger receptor class B, type I is a primary determinant of paraoxonase-1 association with high-density lipoproteins. Arterioscler. Thromb. Vasc. Biol. 30:2121-2127; 2010.
13. Deakin, S.; Moren, X.; James, R. W. Very low density lipoproteins provide a vector for secretion of paraoxonase-1 from cells. Atherosclerosis 179:17-25; 2005.
14. Jaouad, L.; Milochevitch, C.; Khalil, A. PON1 paraoxonase activity is reduced during HDL oxidation and is an indicator of HDL antioxidant capacity. Free Radic. Res. 37:77-83; 2003.
15. Marsillach, J.; Aragones, G.; Mackness, B.; Mackness, M.; Rull, A.; Beltran-Debon, R.; Pedro-Botet, J.; Alonso-Villaverde, C.; Joven, J.; Camps, J. Decreased paraoxonase-1 activity is associated with alterations of high-density lipoprotein particles in chronic liver impairment. Lipids Health Dis. 9:46; 2010.
16. Fuhrman, B.; Volkova, N.; Aviram, M. Oxidative stress increases the expression of the CD36 scavenger receptor and the cellular uptake of oxidized low-density lipoprotein in macrophages from atherosclerotic mice: protective role of antioxidants and of paraoxonase. Atherosclerosis 161:307-316; 2002.
17. Rozenberg, O.; Shih, D. M.; Aviram, M. Paraoxonase 1 (PON1) attenuates macrophage oxidative status: studies in PON1 transfected cells and in PON1 transgenic mice. Atherosclerosis 181:9-18; 2005.
18. Watson, A. D.; Berliner, J. A.; Hama, S. Y.; La Du, B. N.; Faull, K. F.; Fogelman, A. M.; Navab, M. Protective effect of high density lipoprotein associated paraoxonase: inhibition of the biological activity of minimally oxidized low density lipoprotein. J. Clin. Invest. 96:2882-2891; 1995.
19. Jaouad, L.; de Guise, C.; Berrougui, H.; Cloutier, M.; Isabelle, M.; Fulop, T.; Payette, H.; Khalil, A. Age-related decrease in high-density lipoproteins antioxidant activity is due to an alteration in PON1's free sulfhydryl groups. Atherosclerosis 185: 191-200; 2006.
20. Tward, A.; Xia, Y. R.; Wang, X. P.; Shi, Y. S.; Park, C.; Castellani, L. W.; Lusis, A. J.; Shih, D. M. Decreased atherosclerotic lesion formation in human serum paraoxonase transgenic mice. Circulation 106:484-490; 2002.
21. Shih, D. M.; Gu, L.; Xia, Y. R.; Navab, M.; Li, W. F.; Hama, S.; Castellani, L. W.; Furlong, C. E.; Costa, L. G.; Fogelman, A. M.; Lusis, A. J. Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394:284-287; 1998.
22. Mackness, B.; Hunt, R.; Durrington, P. N.; Mackness, M. I. Increased immunolocalization of paraoxonase, clusterin, and apolipoprotein A-I in the human artery wall with the progression of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 17: 1233-1238; 1997.
23. Tavori, H.; Khatib, S.; Aviram, M.; Vaya, J. Characterization of the PON1 active site using modeling simulation, in relation to PON1 lactonase activity. Bioorg. Med. Chem. 16:7504-7509; 2008.
24. Navab, M.; Hama, S. Y.; Hough, G. P.; Hedrick, C. C.; Sorenson, R.; La Du, B. N.; Kobashigawa, J. A.; Fonarow, G. C.; Berliner, J. A.; Laks, H.; Fogelman, A. M. High density associated enzymes: their role in vascular biology. Curr. Opin. Lipidol. 9: 449-456; 1998.
25. Rosenblat, M.; Gaidukov, L.; Khersonsky, O.; Vaya, J.; Oren, R.; Tawfik, D. S.; 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. 281:7657-7665; 2006.
26. Rosenblat, M.; Vaya, J.; Shih, D.; Aviram, M. Paraoxonase 1 (PON1) enhances HDLmediated macrophage cholesterol efflux via the ABCA1 transporter in association with increased HDL binding to the cells: a possible role for lysophosphatidylcholine. Atherosclerosis 179:69-77; 2005.
27. Pike, L. J.; Han, X.; Chung, K. N.; Gross, R. W. Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis. Biochemistry 41:2075-2088; 2002.
28. Gaus, K.; Kritharides, L.; Schmitz, G.; Boettcher, A.; Drobnik, W.; Langmann, T.; Quinn, C. M.; Death, A.; Dean, R. T.; Jessup, W. Apolipoprotein A-1 interaction with plasma membrane lipid rafts controls cholesterol export from macrophages. FASEB J. 18:574-576; 2004.
29. Gillotte, K. L.; Davidson, W. S.; Lund-Katz, S.; Rothblat, G. H.; Phillips, M. C. Removal of cellular cholesterol by pre-β-HDL involves plasma membrane microsolubilization. J. Lipid Res. 39:1918-1928; 1998.
30. Gargalovic, P.; Dory, L. Caveolins and macrophage lipid metabolism. J. Lipid Res. 44:11-21; 2003.
31. Rees, D.; Sloane, T.; Jessup, W.; Dean, R. T.; Kritharides, L. Apolipoprotein A-I stimulates secretion of apolipoprotein E by foam cell macrophages. J. Biol. Chem. 274: 27925-27933; 1999.
32. Sattler, W.; Mohr, D.; Stocker, R. Rapid isolation of lipoproteins and assessment of their peroxidation by high-performance liquid chromatography postcolumn chemiluminescence. Methods Enzymol. 233:469-489; 1994.
33. Gan, K. N.; Smolen, A.; Eckerson, H. W.; La Du, B. N. Purification of human serum paraoxonase/arylesterase: evidence for one esterase catalyzing both activities. Drug Metab. Dispos. 19:100-106; 1991.
34. Eckerson,H.W.;Wyte, C.M.; La Du, B.N. The human serumparaoxonase/ arylesterase polymorphism. Am. J. Hum. Genet. 35:1126-1138; 1983.
35. Hajj Hassan, H.; Blain, S.; Boucher, B.; Denis, M.; Krimbou, L.; Genest, J. Structural modification of plasma HDL by phospholipids promotes efficient ABCA1-mediated cholesterol release. J. Lipid Res. 46:1457-1465; 2005.
36. Fortin, C. F.; Larbi, A.; Lesur, O.; Douziech, N.; Fulop Jr., T. Impairment of SHP-1 down-regulation in the lipid rafts of human neutrophils under GM-CSF stimulation contributes to their age-related, altered functions. J. Leukocyte Biol. 79: 1061-1072; 2006.
37. Abe-Dohmae, S.; Kato, K. H.; Kumon, Y.; Hu, W.; Ishigami, H.; Iwamoto, N.; Okazaki, M.; Wu, C. A.; Tsujita, M.; Ueda, K.; Yokoyama, S. Serum amyloid A generates high density lipoprotein with cellular lipid in an ABCA1- or ABCA7-dependent manner. J. Lipid Res. 47:1542-1550; 2006.
38. Hu, W.; Abe-Dohmae, S.; Tsujita, M.; Iwamoto, N.; Ogikubo, O.; Otsuka, T.; Kumon, Y.; Yokoyama, S. Biogenesis of HDL by SAA is dependent on ABCA1 in the liver in vivo. J. Lipid Res. 49:386-393; 2008.
39. Parra, S.; Alonso-Villaverde, C.; Coll, B.; Ferre, N.; Marsillach, J.; Aragones, G.; Mackness, M.; Mackness, B.; Masana, L.; Joven, J.; Camps, J. Serum paraoxonase-1 activity and concentration are influenced by human immunodeficiency virus infection. Atherosclerosis 194:175-181; 2007.
40. Seres, I.; Paragh, G.; Deschene, E.; Fulop Jr., T.; Khalil, A. Study of factors influencing the decreased HDL associated PON1 activity with aging. Exp. Gerontol. 39: 59-66; 2004.
41. Attia, N.; Fournier, N.; Vedie, B.; Cambillau, M.; Beaune, P.; Ziegler, O.; Grynberg, A.; Paul, J. L.; Guerci, B. Impact of android overweight or obesity and insulin resistance on basal and postprandial SR-BI and ABCA1-mediated serum cholesterol efflux capacities. Atherosclerosis 209:422-429; 2010.
42. Efrat, M.; Aviram, M. Macrophage paraoxonase 1 (PON1) binding sites. Biochem. Biophys. Res. Commun. 376:105-110; 2008.
43. Blumrich, M.; Petzinger, E. Two distinct types of SH-groups are necessary for bumetanide and bile acid uptake into isolated rat hepatocytes. Biochim. Biophys. Acta 1149:278-284; 1993.
44. Gaus, K.; Gooding, J. J.; Dean, R. T.; Kritharides, L.; Jessup, W. A kinetic model to evaluate cholesterol efflux from THP-1 macrophages to apolipoprotein A-1. Biochemistry 40:9363-9373; 2001.
45. Fuhrman, B.; Gantman, A.; Aviram, M. Paraoxonase 1 (PON1) deficiency in mice is associated with reduced expression of macrophage SR-BI and consequently the loss of HDL cytoprotection against apoptosis. Atherosclerosis 211:61-68; 2010.
46. de Beer, M. C.; Ji, A.; Jahangiri, A.; Vaughan, A. M.; de Beer, F. C.; van der Westhuyzen, D. R.; Webb, N. R. ATP binding cassette G1-dependent cholesterol efflux during inflammation. J. Lipid Res. 52:345-353; 2011.
47. Remaley, A. T.; Stonik, J. A.; Demosky, S. J.; Neufeld, E. B.; Bocharov, A. V.; Vishnyakova, T. G.; Eggerman, T. L.; Patterson, A. P.; Duverger, N. J.; Santamarina- Fojo, S.; Brewer Jr., H. B. Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 280:818-823; 2001.
48. Moreno, J. A.; Perez-Jimenez, F.; Marin, C.; Perez-Martinez, P.; Moreno, R.; Gomez, P.; Jimenez-Gomez, Y.; Paniagua, J. A.; Lairon, D.; Lopez-Miranda, J. The apolipoprotein E gene promoter (-219G/T) polymorphism determines insulin sensitivity in response to dietary fat in healthy young adults. J. Nutr. 135:2535-2540; 2005.
49. Xie, Q.; Zhao, S. P.; Li, F. D-4F, an apolipoprotein A-I mimetic peptide, promotes cholesterol efflux from macrophages via ATP-binding cassette transporter A1. Tohoku J. Exp. Med. 220:223-228; 2010.
50. Harel, M.; Aharoni, A.; Gaidukov, L.; Brumshtein, B.; Khersonsky, O.; Meged, R.; Dvir, H.; Ravelli, R. B.; McCarthy, A.; Toker, L.; Silman, I.; Sussman, J. L.; Tawfik, D. S. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11:412-419; 2004.
51. Perez-Jimenez, F.; Lopez-Miranda, J. University of Health Sciences: a blow of hope. Med. Clin. (Barcelona) 125:477; 2005.
52. Hou, M.; Xia,M.; Zhu, H.;Wang, Q.; Li, Y.; Xiao, Y.; Zhao, T.; Tang, Z.;Ma, J.; Ling,W. Lysophosphatidylcholine promotes cholesterol efflux from mouse macrophage foam cells via PPARγ-LXRα-ABCA1-dependent pathway associated with apoE. Cell Biochem. Funct. 25:33-44; 2007.
53. Sorenson, R. C.; Primo-Parmo, S. L.; Kuo, C. L.; Adkins, S.; Lockridge, O.; La Du, B. N. Reconsideration of the catalytic center and mechanism of mammalian paraoxonase/ arylesterase. Proc. Natl. Acad. Sci. U. S. A. 92:7187-7191; 1995.
54. Aviram, M.; Billecke, S.; Sorenson, R.; Bisgaier, C.; Newton, R.; Rosenblat, M.; Erogul, J.; Hsu, C.; Dunlop, C.; La Du, B. 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. 18:1617-1624; 1998.
55. Fu, Y. Rate-limiting factors of cholesterol efflux in reverse cholesterol transport: acceptors and donors. Clin. Exp. Pharmacol. Physiol. 37:703-709; 2010.
56. Wang, N.; Lan, D.; Chen, W.; Matsuura, F.; Tall, A. R. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. U. S. A. 101:9774-9779; 2004.
57. Drobnik, W.; Borsukova, H.; Bottcher, A.; Pfeiffer, A.; Liebisch, G.; Schutz, G. J.; Schindler, H.; Schmitz, G. Apo AI/ABCA1-dependent and HDL3-mediated lipid efflux from compositionally distinct cholesterol-based microdomains. Traffic 3: 268-278; 2002.
58. Mendez, A. J.; Lin, G.; Wade, D. P.; Lawn, R. M.; Oram, J. F. Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J. Biol. Chem. 276:3158-3166; 2001.
59. Deakin, S. P.; Bioletto, S.; Bochaton-Piallat, M. L.; James, R. W. HDL-associated paraoxonase-1 can redistribute to cell membranes and influence sensitivity to oxidative stress. Free Radic. Biol. Med. 50:102-109; 2011.