Advertisement

Cardiovascular Drugs and Therapy

, Volume 23, Issue 6, pp 501–510 | Cite as

Benefits and Difficulties in Measuring HDL Subfractions and Human Paraoxonase-1 Activity During Statin Treatment

  • Mariann Harangi
  • Ildikó Seres
  • János Harangi
  • György Paragh
Article

Abstract

Dyslipidaemia including decreased high density lipoprotein cholesterol concentration is one of several factors that have been implicated in increased cardiovascular risk. Since their introduction in the 1980s, 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase inhibitors (statins) have emerged as the one of the best-selling class of medications to date, with numerous trials demonstrating powerful efficacy in preventing cardiovascular diseases. Although statins have been shown to modestly raise or not alter HDL-cholesterol, their effect on HDL subfractions and on HDL-associated enzymes including human paraoxonase-1 (PON1) has not yet been fully explored. This review summarizes the currently availabe data on the effect of statins on HDL subfractions and on PON1 activity with a particular emphasis on the clinical relevance of these effects. Moreover, methodological problems of HDL subfraction and PON1 activity determinations are also discussed.

Key words

Statin High-density lipoprotein subfractions Paraoxonase 

References

  1. 1.
    Scandinavian Simvastatin Survival Study Group. Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4 S). Lancet. 1994;344:1383–9.Google Scholar
  2. 2.
    The Long-Term Intervention with Pravastatin in Ischaemic Disease (LIPID) Study Group. Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels. N Engl J Med. 1998;339:1349–57.CrossRefGoogle Scholar
  3. 3.
    Downs JR, Clearfield M, Weis S, Whitney E, Shapiro DR, Beere PA, et al. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA. 1998;279:1615–22.CrossRefPubMedGoogle Scholar
  4. 4.
    Sacks FM, Pfeffer MA, Moye LA, Rouleau JL, Rutherford JD, Cole TG, et al. The effect of pravastatin on coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events Trial investigators. N Engl J Med. 1996;335:1001–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Shepherd J. Cobbe SM, Ford I, Isles CG, Lorimer AR, MacFarlane PW, McKillop JH. Packard CJ. Prevention of coronary heart disease with pravastatin in men with hypercholesterolemia. West of Scotland Coronary Prevention Study Group. N Engl J Med. 1995;333:1301–7.Google Scholar
  6. 6.
    Castelli WP, Garrison RJ, Wilson PW, Abbott RD, Kalousdian S, Kannel WB. Incidence of coronary heart disease and lipoprotein cholesterol levels. The Framingham Study. JAMA. 1986;256:2835–8.Google Scholar
  7. 7.
    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.Google Scholar
  8. 8.
    Goldbourt U, Yaari S, Medalie JH. Isolated low HDL cholesterol as a risk factor for coronary heart disease mortality. A 21-year follow-up of 8000 men. Arterioscler Thromb Vasc Biol. 1997;17:107–13.PubMedGoogle Scholar
  9. 9.
    Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults. Executive Summary of the Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). JAMA 2001;285:2486–97Google Scholar
  10. 10.
    Tavintharan S, Lim SC, Sum CF. Patients with low levels of high-density lipoprotein cholesterol: to treat or not to treat? Singapore Med J. 2005;46:519–28.PubMedGoogle Scholar
  11. 11.
    Briel M, Ferreira-Gonzalez I, You JJ, Karanicolas PJ, Akl EA, Wu P, Blechacz B, Bassler D, Wei X, Sharman A, Whitt I, Alves da Silva S, Khalid Z, Nordmann AJ, Zhou Q, Walter SD, Vale N, Bhatnagar N, O’Regan C, Mills EJ, Bucher HC, Montori VM, Guyatt GH. Association between change in high density lipoprotein cholesterol and cardiovascular disease morbidity and mortality: systematic review and meta-regression analysis. BMJ 2009 Feb 16;338:b92. doi: 10.1136/bmj.b92.
  12. 12.
    Movva R, Rader DJ. Laboratory assessment of HDL heterogeneity and function. Clin Chem. 2008;54:788–800.CrossRefPubMedGoogle Scholar
  13. 13.
    Li Z, McNamara JR, Ordovas JM, Schaefer EJ. Analysis of high density lipoproteins by a modified gradient gel electrophoresis method. J Lipid Res. 1994;35:1698–711.PubMedGoogle Scholar
  14. 14.
    Blanche PJ, Gong EL, Forte TM, Nichols AV. Characterization of human high-density lipoproteins by gradient gel electrophoresis. Biochim Biophys Acta. 1981;665:408–19.PubMedGoogle Scholar
  15. 15.
    Asztalos BF, Sloop CH, Wong L, Roheim PS. Two-dimensional electrophoresis of plasma lipoproteins: recognition of new apo A-I-containing subpopulations. Biochim Biophys Acta. 1993;1169:291–300.PubMedGoogle Scholar
  16. 16.
    Cheung MC, Albers JJ. Characterization of lipoprotein particles isolated by immunoaffinity chromatography. Particles containing A-I and A-II and particles containing A-I but no A-II. J Biol Chem. 1984;259:12201–9.PubMedGoogle Scholar
  17. 17.
    Kontush A, Chapman MJ. Functionally defective high-density lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev. 2006;58:342–74.CrossRefPubMedGoogle Scholar
  18. 18.
    Salonen JT, Salonen R, Seppänen K, Rauramaa R, Tuomilehto J. HDL, HDL2, and HDL3 subfractions, and the risk of acute myocardial infarction. A prospective population study in eastern Finnish men. Circulation. 1991;84:129–39.PubMedGoogle Scholar
  19. 19.
    Lamarche B, Moorjani S, Cantin B, Dagenais GR, Lupien PJ, Després JP. Associations of HDL2 and HDL3 subfractions with ischemic heart disease in men. Prospective results from the Québec Cardiovascular Study. Arterioscler Thromb Vasc Biol. 1997;17:1098–105.PubMedGoogle Scholar
  20. 20.
    Stampfer MJ, Sacks FM, Salvini S, Willett WC, Hennekens CH. A prospective study of cholesterol, apolipoproteins, and the risk of myocardial infarction. N Engl J Med. 1991;325:373–81.PubMedCrossRefGoogle Scholar
  21. 21.
    Sweetnam PM, Bolton CH, Yarnell JW, Bainton D, Baker IA, Elwood PC, et al. Associations of the HDL2 and HDL3 cholesterol subfractions with the development of ischemic heart disease in British men. The Caerphilly and Speedwell Collaborative Heart Disease Studies. Circulation. 1994;90:769–74.PubMedGoogle Scholar
  22. 22.
    Yu S, Yarnell JW, Sweetnam P, Bolton CH. High density lipoprotein subfractions and the risk of coronary heart disease: 9-years follow-up in the Caerphilly Study. Atherosclerosis. 2003;166:331–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Vekic J, Topic A, Zeljkovic A, Jelic-Ivanovic Z, Spasojevic-Kalimanovska V. LDL and HDL subclasses and their relationship with Framingham risk score in middle-aged Serbian population. Clin Biochem. 2007;40:310–6.CrossRefPubMedGoogle Scholar
  24. 24.
    Asztalos BF, Batista M, Horvath KV, Cox CE, Dallal GE, Morse JS, et al. Change in alpha1 HDL concentration predicts progression in coronary artery stenosis. Arterioscler Thromb Vasc Biol. 2003;23:847–52.CrossRefPubMedGoogle Scholar
  25. 25.
    Asztalos BF, Cupples LA, Demissie S, Horvath KV, Cox CE, Batista MC, et al. High-density lipoprotein subpopulation profile and coronary heart disease prevalence in male participants of the Framingham Offspring Study. Arterioscler Thromb Vasc Biol. 2004;24:2181–7.CrossRefPubMedGoogle Scholar
  26. 26.
    Asztalos BF, Collins D, Cupples LA, Demissie S, Horvath KV, Bloomfield HE, et al. Schaefer EJ.Value of high-density lipoprotein (HDL) subpopulations in predicting recurrent cardiovascular events in the Veterans Affairs HDL Intervention Trial. Arterioscler Thromb Vasc Biol. 2005;25:2185–91.CrossRefPubMedGoogle Scholar
  27. 27.
    Rosenson RS, Otvos JD, Freedman DS. Relations of lipoprotein subclass levels and low-density lipoprotein size to progression of coronary artery disease in the Pravastatin Limitation of Atherosclerosis in the Coronary Arteries (PLAC-I) trial. Am J Cardiol. 2002;90:89–94.CrossRefPubMedGoogle Scholar
  28. 28.
    van der Steeg WA, Holme I, Boekholdt SM, Larsen ML, Lindahl C, Stroes ES, et al. High-density lipoprotein cholesterol, high-density lipoprotein particle size, and apolipoprotein A-I: significance for cardiovascular risk: the IDEAL and EPIC-Norfolk studies. J Am Coll Cardiol. 2008;51:634–42.CrossRefPubMedGoogle Scholar
  29. 29.
    Franceschini G, Sirtori M, Vaccarino V, Gianfranceschi G, Chiesa G, Sirtori CR. Plasma lipoprotein changes after treatment with pravastatin and gemfibrozil in patients with familial hypercholesterolemia. J Lab Clin Med. 1989;114:250–9.PubMedGoogle Scholar
  30. 30.
    Guérin M, Dolphin PJ, Talussot C, Gardette J, Berthézène F, Chapman MJ. Pravastatin modulates cholesteryl ester transfer from HDL to apoB-containing lipoproteins and lipoprotein subspecies profile in familial hypercholesterolemia. Arterioscler Thromb Vasc Biol. 1995;15:1359–68.PubMedGoogle Scholar
  31. 31.
    Broyles FE, Walden CE, Hunninghake DB, Hill-Williams D, Knopp RH. Effect of fluvastatin on intermediate density lipoprotein (remnants) and other lipoprotein levels in hypercholesterolemia. Am J Cardiol. 1995;76:129A–35A.CrossRefPubMedGoogle Scholar
  32. 32.
    Homma Y, Ozawa H, Kobayashi T, Yamaguchi H, Sakane H, Nakamura H. Effects of simvastatin on plasma lipoprotein subfractions, cholesterol esterification rate, and cholesteryl ester transfer protein in type II hyperlipoproteinemia. Atherosclerosis. 1995;114:223–34.CrossRefPubMedGoogle Scholar
  33. 33.
    Lijnen P, Echevaría-Vázquez D, Petrov V. Influence of cholesterol-lowering on plasma membrane lipids and function. Methods Find Exp Clin Pharmacol. 1996;18:123–36.PubMedGoogle Scholar
  34. 34.
    Mölgaard J, Wärjerstam-Elf S, Olsson AG. Efficacy and safety of simvastatin for high-risk hypercholesterolemia. Am J Cardiol. 1999;83:1043–8.CrossRefPubMedGoogle Scholar
  35. 35.
    Guerin M, Lassel TS, Le Goff W, Farnier M, Chapman MJ. Action of atorvastatin in combined hyperlipidemia: preferential reduction of cholesteryl ester transfer from HDL to VLDL1 particles. Arterioscler Thromb Vasc Biol. 2000;20:189–97.PubMedGoogle Scholar
  36. 36.
    Schaefer EJ, McNamara JR, Tayler T, Daly JA, Gleason JA, Seman LJ, et al. Effects of atorvastatin on fasting and postprandial lipoprotein subclasses in coronary heart disease patients versus control subjects. Am J Cardiol. 2002;90:689–96.CrossRefPubMedGoogle Scholar
  37. 37.
    Asztalos BF, Horvath KV, McNamara JR, Roheim PS, Rubinstein JJ, Schaefer EJ. Effects of atorvastatin on the HDL subpopulation profile of coronary heart disease patients. J Lipid Res. 2002;43:1701–7.CrossRefPubMedGoogle Scholar
  38. 38.
    Brousseau ME, Schaefer EJ, Wolfe ML, Bloedon LT, Digenio AG, Clark RW, et al. Effects of an inhibitor of cholesteryl ester transfer protein on HDL cholesterol. N Engl J Med. 2004;350:1505–15.CrossRefPubMedGoogle Scholar
  39. 39.
    Kawano M, Nagasaka S, Yagyu H, Ishibashi S. Pitavastatin decreases plasma prebeta1-HDL concentration and might promote its disappearance rate in hypercholesterolemic patients. J Atheroscler Thromb. 2008;15:41–6.PubMedGoogle Scholar
  40. 40.
    Saougos VG, Tambaki AP, Kalogirou M, Kostapanos M, Gazi IF, Wolfert RL, et al. Differential effect of hypolipidemic drugs on lipoprotein-associated phospholipase A2. Arterioscler Thromb Vasc Biol. 2007;27:2236–43.CrossRefPubMedGoogle Scholar
  41. 41.
    Kostapanos MS, Milionis HJ, Filippatos TD, Christogiannis LG, Bairaktari ET, Tselepis AD, et al. Dose-dependent effect of rosuvastatin treatment on HDL-subfraction phenotype in patients with primary hyperlipidemia. J Cardiovasc Pharmacol Ther. 2009;14:5–13.CrossRefPubMedGoogle Scholar
  42. 42.
    Harangi M, Mirdamadi HZ, Seres I, Sztanek F, Mornár M, Kassai A, et al. Atorvastatin effect on the distribution of HDL subfractions and human paraoxonase activity. Transl Res. 2009;153:190–8.CrossRefPubMedGoogle Scholar
  43. 43.
    Rizzo M, Berneis K. The clinical relevance of low-density-lipoproteins size modulation by statins. Cardiovasc Drugs Ther. 2006;20:205–17.CrossRefPubMedGoogle Scholar
  44. 44.
    Mackness B, Durrington PN, Mackness MI. The paraoxonase gene family and coronary heart disease. Curr Opin Lipidol. 2002;13:357–62.CrossRefPubMedGoogle Scholar
  45. 45.
    Kelso GJ, Stuart WD, Richter RJ, Furlong CE, Jordan-Starck TC, Harmony JA. Apolipoprotein J is associated with paraoxonase in human plasma. Biochemistry. 1994;33:832–9.CrossRefPubMedGoogle Scholar
  46. 46.
    La Du BN, Adkins S, Kuo CL, Lipsig D. Studies on human serum paraoxonase/arylesterase. Chem Biol Interact. 1993;87:25–34.CrossRefPubMedGoogle Scholar
  47. 47.
    Rainwater DL, Rutherford S, Dyer TD, Rainwater ED, Cole SA, Vandeberg JL, et al. Determinants of variation in human serum paraoxonase activity. Heredity. 2009;102:147–54.CrossRefPubMedGoogle Scholar
  48. 48.
    Regieli JJ, Jukema JW, Doevendans PA, Zwinderman AH, Kastelein JJ, Grobbee DE, et al. Paraoxonase variants relate to 10-year risk in coronary artery disease: impact of a high-density lipoprotein-bound antioxidant in secondary prevention. J Am Coll Cardiol. 2009;54:1238–45.CrossRefPubMedGoogle Scholar
  49. 49.
    Koubaa N, Nakbi A, Hammami S, Attia N, Mehri S. Ben Hamda K, Ben Farhat M, Miled A, Hammami M. Association of homocysteine thiolactonase activity and PON1 polymorphisms with the severity of acute coronary syndrome. Clin Biochem. 2009;42:771–6.CrossRefPubMedGoogle Scholar
  50. 50.
    Leviev I, James RW. Promoter polymorphisms of human paraoxonase PON1 gene and serum paraoxonase activities and concentrations. Arterioscler Thromb Vasc Biol. 2000;20:516–21.PubMedGoogle Scholar
  51. 51.
    Draganov DI, Teiber JF, Speelman A, Osawa Y, Sunahara R, La Du BN. Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificities. J Lipid Res. 2005;46:1239–47.CrossRefPubMedGoogle Scholar
  52. 52.
    Mackness B, Mackness MI, Arrol S, Turkie W, Durrington PN. Effect of the human serum paraoxonase 55 and 192 genetic polymorphisms on the protection by high density lipoprotein against low density lipoprotein oxidative modification. FEBS Lett. 1998;423:57–60.CrossRefPubMedGoogle Scholar
  53. 53.
    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.CrossRefPubMedGoogle Scholar
  54. 54.
    Harangi M, Seres I, Magyar MT, Csipo I, Sipka S, Valikovics A, et al. Association between human paraoxonase 1 activity and intima-media thickness in subjects under 55 years of age with carotid artery disease. Cerebrovasc Dis. 2008;25:122–8.CrossRefPubMedGoogle Scholar
  55. 55.
    She ZG, Zheng W, Wei YS, Chen HZ, Wang AB, Li HL, et al. Human paraoxonase gene cluster transgenic overexpression represses atherogenesis and promotes atherosclerotic plaque stability in ApoE-null mice. Circ Res. 2009;104:1160–8.CrossRefPubMedGoogle Scholar
  56. 56.
    Mackness B, Mackness MI, Arrol S, Turkie W, Durrington PN. Effect of the molecular polymorphisms of human paraoxonase (PON1) on the rate of hydrolysis of paraoxon. Br J Pharmacol. 1997;122:265–8.CrossRefPubMedGoogle Scholar
  57. 57.
    Atmeh RF, Shepherd J, Packard CJ. Subpopulations of apolipoprotein A-I in human high-density lipoproteins. Their metabolic properties and response to drug therapy. Biochim Biophys Acta. 1983;751:175–88.PubMedGoogle Scholar
  58. 58.
    Moren X, Deakin SP, Liu ML, Taskinen MR, James RW. HDL subfraction distribution of paraoxonase-1 and its relevance to enzyme activity and resistance to oxidative stress. J Lipid Res. 2008;49:1246–53.CrossRefPubMedGoogle Scholar
  59. 59.
    Paragh G, Harangi M, Seres I. Effect of lipid lowering medications on PON1. In: Mackness B, Mackness M, Aviram M, Paragh G, editors. The paraoxonases: their role in disease development and xenobiotic metabolism. Springer; 2008. pp. 251–66.Google Scholar
  60. 60.
    Tomás M, Sentí M, García-Faria F, Vila J, Rorrents A, Covas M, et al. Effect of simvastatin therapy on paraoxonase activity and related lipoproteins in familial hypercholesterolemic patiens. Arterioscler Thromb Vasc Biol. 2000;20:2113–9.PubMedGoogle Scholar
  61. 61.
    Balogh Z, Fülöp P, Seres I, Harangi M, Katona E, Kosztáczky B, et al. Effects of simvastatin on serum paraoxonase activity. Clin Drug Invest. 2001;21:505–10.CrossRefGoogle Scholar
  62. 62.
    Tsimihodimos V, Karabina SAP, Tambaki AP, Bairaktari E, Goudevenos JA, Chapman MJ, et al. Atorvastatin preferentially reduces LDL-associated platelet-activating factor acetylhydrolase activity in dyslipidemias of type IIa and type IIb. Arterioscler Throm Vasc Biol. 2002;22:306–11.CrossRefGoogle Scholar
  63. 63.
    Fuhrman B, Koren L, Volkova N, Keidar S, Hayek T, Aviram M. Atorvastatin therapy in hypercholesterolemic patients suppresses cellular uptake of oxidized-LDL by differentiating monocytes. Atherosclerosis. 2002;164:179–85.CrossRefPubMedGoogle Scholar
  64. 64.
    Deakin S, Leviev I, Guernier S, James RW. Simvastatin modulates expression of the PON1 gene and increases serum paraoxonase. A role for sterol reulatory element-binding protein-2. Arterioscler Throm Vasc Biol. 2003;23:2083–9.CrossRefGoogle Scholar
  65. 65.
    Kural BV, Orem C, Uydu HA, Alver A, Orem A. The effects of lipid-lowering therapy on paraoxonase activities and their relationships with the antioxidant system in patients with dyslipidemia. Coron Artery Dis. 2004;15:277–83.CrossRefPubMedGoogle Scholar
  66. 66.
    Paragh G, Törőcsik D, Seres I, Harangi M, Illyés L, Balogh Z, et al. Effect of short term treatment with simvastatin and atorvastatin on lipids and paraoxonase activity in patients with hyperlipoproteinaemia. Curr Med Res Opin. 2004;20:1321–27.CrossRefPubMedGoogle Scholar
  67. 67.
    Harangi M, Seres I, Varga Z, Emri G, Szilvássy Z, Paragh G, et al. Atorvastatin effect on high-density lipoprotein-associated paraoxonase activity and oxidative DNA damage. Eur J Clin Pharmacol. 2004;60:685–91.CrossRefPubMedGoogle Scholar
  68. 68.
    Sardo MA, Campo S, Bonaiuto M, Bonaiuto A, Saitta C, Trimarchi G, et al. Antioxidant effect of atorvastatin is independent of PON1 gene T(-107)C, Q192R and L55M polymorphisms in hypercholesterolaemic patients. Curr Med Res Opin. 2005 May;21(5):777–84.CrossRefPubMedGoogle Scholar
  69. 69.
    Kassai A, Illyés L, Mirdamadi HZ, Seres I, Kalmár T, Audikovszky M, et al. The effect of atorvastatin therapy on lecithin:cholesterol acyltransferase, cholesteryl ester transfer protein and the antioxidant paraoxonase. Clin Biochem. 2007;40:1–5.CrossRefPubMedGoogle Scholar
  70. 70.
    Bergheanu SC, Van Tol A, Dallinga-Thie GM, Liem A, Dunselman PH, Van der Bom JG, et al. Effect of rosuvastatin versus atorvastatin treatment on paraoxonase-1 activity in men with established cardiovascular disease and a low HDL-cholesterol. Curr Med Res Opin. 2007;23:2235–40.CrossRefPubMedGoogle Scholar
  71. 71.
    Christidis DS, Liberopoulos EN, Kakafika AI, Miltiadous GA, Liamis GL, Kakaidi B, et al. Effect of paraoxonase 1 polymorphisms on the response of lipids and lipoprotein-associated enzymes to treatment with fluvastatin. Arch Med Res. 2007;38:403–10.CrossRefPubMedGoogle Scholar
  72. 72.
    Mirdamadi HZ, Sztanek F, Derdak Z, Seres I, Harangi M, Paragh G. The human paraoxonase-1 phenotype modifies the effect of statins on paraoxonase activity and lipid parameters. Br J Clin Pharmacol. 2008;66:366–74.CrossRefPubMedGoogle Scholar
  73. 73.
    Ota K, Suehiro T, Arii K, Ikeda Y, Kumon Y, Osaki F, et al. Effect of pitavastatin on transactivation of human serum paraoxonase 1 gene. Metabolism. 2005;54:142–50.CrossRefPubMedGoogle Scholar
  74. 74.
    Gouédard C, Koum-Besson N, Barouki R, Morel Y. Opposite regulation of the human paraoxonase-1 gene PON-1 by fenofibrate and statins. Mol Pharmacol. 2003;63:945–56.CrossRefPubMedGoogle Scholar
  75. 75.
    Malin R, Laaksonen R, Knuuti J, Janatuinen T, Vesalainen R, Nuutila P, et al. Paraoxonase genotype modifies the effect of pravastatin on high-density lipoprotein cholesterol. Pharmacogenetics. 2001;11:625–33.CrossRefPubMedGoogle Scholar
  76. 76.
    Deakin S, Guernier S, James RW. Pharmacogenetic interaction between paraoxonase 1 gene promoter polymorphism C-107 T and statin. Pharmacogen Genom. 2007;17:451–7.CrossRefGoogle Scholar
  77. 77.
    Fu R, Sun YM, Su Y, Wu Y, Luan Y. Effect of statin therapy on plasma high-density lipoprotein-cholesterol levels is modified by paraoxonase 1 in Chinese patients with coronary heart disease. Clin Exp Pharmacol Physiol. 2008;35:982–3.CrossRefPubMedGoogle Scholar
  78. 78.
    Lindgren FT, Elliott HA, Gofman JW. The ultracentrifugal characterization and isolation of human blood lipids andlipoproteins, with applications to the study of atherosclerosis. J Phys Colloid Chem. 1951;55:80–93.CrossRefPubMedGoogle Scholar
  79. 79.
    Kirstein P, Carlson K. Determination of the cholesterol content of high density lipoprotein subfractions HDL2 and HDL3, without contamination of Lp(a), in human plasma. Clin Chim Acta. 1981;113:123–34.CrossRefPubMedGoogle Scholar
  80. 80.
    Warnick GR, Benderson J, Albers JJ. Dextran sulfate-Mg2+ precipitation procedure for quantitation of high-density-lipoprotein cholesterol. Clin Chem. 1982;28:1379–88.PubMedGoogle Scholar
  81. 81.
    Gidez LI, Miller GJ, Burstein M, Slagle S, Eder HA. Separation and quantitation of subclasses of human plasma high density lipoproteins by a simple precipitation procedure. J Lipid Res. 1982;23:1206–23.PubMedGoogle Scholar
  82. 82.
    Kulkarni KR. Cholesterol profile measurement by vertical auto profile method. Clin Lab Med. 2006;26:787–802.CrossRefPubMedGoogle Scholar
  83. 83.
    Warnick GR, McNamara JR, Boggess CN, Clendenen F, Williams PT. Landolt CC.Polyacrylamide gradient gel electrophoresis of lipoprotein subclasses. Clin Lab Med. 2006;26:803–46.CrossRefPubMedGoogle Scholar
  84. 84.
    Waymack PP. A Perspective on HDL-LDL Subclass, Subspecies and Subfraction Analyses and Challenges for Standardization. http://www.fda.gov/ohrms/dockets/ac/06/slides/2006-4263s1_04_Waymack-Guest.pdf Accessed 6 Dec 2006.
  85. 85.
    Fisman EZ, Adler Y, Tenenbaum A. Statins research unfinished saga: desirability versus feasibility. Cardiovasc Diabetol. 2005;4:8.CrossRefPubMedGoogle Scholar
  86. 86.
    Pedersen TR, Kjekshus J, Berg K, Haghfelt T, Faergeman O, Faergeman G, et al. Wedel H; Scandinavian Simvastatin Survival Study Group. Randomised trial of cholesterol lowering in 4444 patients with coronary heart disease: the Scandinavian Simvastatin Survival Study (4 S). Atheroscler Suppl. 2004;5:81–7.CrossRefPubMedGoogle Scholar
  87. 87.
    Sirtori CR. Tissue selectivity of hydroxymethylglutaryl coenzyme A (HMG CoA) reductase inhibitors. Pharmacol Ther. 1993;60:431–59.CrossRefPubMedGoogle Scholar
  88. 88.
    Sviridov D, Mukhamedova N, Remaley AT, Chin-Dusting J, Nestel P. Antiatherogenic functionality of high density lipoprotein: how much versus how good. J Atheroscler Thromb. 2008;15:52–62.PubMedGoogle Scholar
  89. 89.
    Vincent-Viry M, Sass C, Bastien S, Aguillon D, Siest G, Visvikis S. PON1-192 phenotype and genotype assessments in 918 subjects of the Stanislas Cohort Study. Clin Chem Lab Med. 2003;41:535–40.CrossRefPubMedGoogle Scholar
  90. 90.
    Paragh G, Seres I, Harangi M, Pocsai Z, Asztalos L, Locsey L, et al. Discordance in Human Paraoxonase-1 Gene between Phenotypes and Genotypes in Chronic Kidney Disease. Nephron Clin Pract. 2009;113:46–53.CrossRefGoogle Scholar
  91. 91.
    Camps J, Marsillach J, Joven J. Pharmacological and lifestyle factors modulating serum paraoxonase-1 activity. Mini Rev Med Chem. 2009;9:911–20.PubMedGoogle Scholar
  92. 92.
    Duell PB, Oram JF, Bierman EL. Nonenzymatic glycosylation of HDL resulting in inhibition of high-affinity binding to cultured human fibroblasts. Diabetes. 1990;39:1257–63.CrossRefPubMedGoogle Scholar
  93. 93.
    Wang WQ, Merriam DL, Moses AS, Francis GA. Enhanced cholesterol efflux by tyrosyl radical-oxidized high density lipoprotein is mediated by apolipoprotein AI-AII heterodimers. J Biol Chem. 1998;273:17391–8.CrossRefPubMedGoogle Scholar
  94. 94.
    Khovidhunkit W, Memon RA, Feingold KR, Grunfeld C. Infection and inflammation-induced proatherogenic changes of lipoproteins. J Infect Dis. 2000;181:S462–72.CrossRefPubMedGoogle Scholar
  95. 95.
    Cabana VG, Lukens JR, Rice KS, Hawkins TJ, Getz GS. HDL content and composition in acute phase response in three species: triglyceride enrichment of HDL a factor in its decrease. J Lipid Res. 1996;37:2662–74.PubMedGoogle Scholar
  96. 96.
    Van Lenten BJ, Wagner AC, Nayak DP, Hama S, Navab M, Fogelman AM. HDL loses its anti-inflammatory properties during acute influenza A infection. Circulation. 2001;103:2283–8.PubMedGoogle Scholar
  97. 97.
    Superko HR, Enas EA, Kotha P, Bhat NK, Garrett B. High-density lipoprotein subclass distribution in individuals of Asian Indian descent: the National Asian Indian Heart Disease Project. Prev Cardiol. 2005;8:81–6.CrossRefPubMedGoogle Scholar
  98. 98.
    Martinelli N, Girelli D, Olivieri O, Guarini P, Bassi A, Trabetti E, et al. Novel serum paraoxonase activity assays are associated with coronary artery disease. Clin Chem Lab Med. 2009;47:432–40.CrossRefPubMedGoogle Scholar
  99. 99.
    Mackness B, Mackness M. High-density lipoprotein: why all the fuss? Ann Clin Biochem. 2009;46:5–7.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Mariann Harangi
    • 1
  • Ildikó Seres
    • 1
  • János Harangi
    • 2
  • György Paragh
    • 1
  1. 1.First Department of Medicine, Medical and Health Sciences CenterUniversity of DebrecenDebrecenHungary
  2. 2.Research Laboratory for ChromatographyDebrecenHungary

Personalised recommendations