Paraoxonase (PON1 and PON3) polymorphisms: Impact on liver expression and atorvastatin-lactone hydrolysis

Frontiers in Pharmacology

Volumn JUL, Issue , 2011, Pages

  Riedmaier, Stephan ^a   Klein, Kathrin ^a   Winter, Stefan ^a   Hofmann, Ute ^a   Schwab, Matthias ^a,b   Zanger, Ulrich M ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Atorvastatin lactone; Myopathy; Paraoxonase; Pharmacogenetics; Pon1; Pon3; Rhabdomyolysis; Snp

Indexed keywords

ARYLDIALKYLPHOSPHATASE; ARYLDIALKYLPHOSPHATASE 1; ARYLDIALKYLPHOSPHATASE 3; ATORVASTATIN; BILIRUBIN; C REACTIVE PROTEIN; GAMMA GLUTAMYLTRANSFERASE; LACTONE; OMEPRAZOLE; PANTOPRAZOLE; UNCLASSIFIED DRUG;

ARTICLE; BILE DUCT CARCINOMA; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; CHOLESTASIS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; GENE; GENE LOCUS; GENE SEQUENCE; HAPLOTYPE; HEREDITY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROLYSIS; LIVER; LIVER CELL CARCINOMA; LIVER MICROSOME; NUCLEOTIDE SEQUENCE; PON1 GENE; PON3 GENE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; SINGLE NUCLEOTIDE POLYMORPHISM;

EID: 84863819484     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2011.00041     Document Type: Article

References (57)

1. André, S., Kozár, T., Kojima, S., Unverzagt, C., and Gabius, H.-J. (2009). From structural to functional glycomics: core substitutions as molecular switches for shape and lectin affinity of N-glycans. Biol. Chem. 390, 557-565.
2. Aragones, G., Guardiola, M., Barreda, M., Marsillach, J., Beltran-Debon, R., Rull, A., Mackness, B., Mackness, M., Joven, J., Simo, J. M., and Camps, J. (2011). Measurement of serum paraoxonase-3 concentration: method evaluation, reference values and influence of genotypes in a population-based study. J. Lipid Res. 52, 1055-1061.
3. Araoud, M., Neffeti, F., Douki, W., Najjar, M. F., and Kenani, A. (2010). Paraoxonase 1 correlates with butyrylcholinesterase and gamma glutamyl transferase in workers chronically exposed to pesticides. J. Occup. Health 52, 383-388.
4. Baer, A. N., and Wortmann, R. L. (2007). Myotoxicity associated with lipid-lowering drugs. Curr. Opin. Rheumatol. 19, 67-73.
5. Banerjee, I. (2010). Relationship between paraoxonase 1 (PON1) gene polymorphisms and susceptibility of stroke: a meta-analysis. Eur. J. Epidemiol. 25, 449-458.
6. Barrett, J. C., Fry, B., Maller, J., and Daly, M. J. (2005). Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265.
7. Billecke, S., Draganov, D., Counsell, R., Stetson, P., Watson, C., Hsu, C., and La Du, B. N. (2000). Human serum paraoxonase (PON1) isozymes Q and R hydrolyze lactones and cyclic carbonate esters. Drug Metab. Dispos. 28, 1335-1342.
8. Bouman, H. J., Schömig, E., van Werkum,J.W.,Velder,J.,Hackeng,C. M., Hirschhäuser, C., Waldmann, C., Schmalz, H.-G., Ten Berg, J. M., and Taubert, D. (2011). Paraoxonase1 is a major determinant of clopidogrel efficacy. Nat. Med. 17, 110-116.
9. Campo, S., Sardo, A. M., Campo, G. M., Avenoso, A., Castaldo, M., D'Ascola, A., Giunta, E., Calatroni, A., and Saitta, A. (2004). Identification of paraoxonase 3 gene (PON3) missense mutations in a population of southern Italy. Mutat. Res. 546, 75-80.
10. Camps, J., Marsillach, J., and Joven, J. (2009). Measurement of serum paraoxonase-1 activity in the evaluation of liver function. World J. Gastroenterol. 15, 1929-1933.
11. Carlson, C. S., Heagerty, P. J., Hatsukami, T. S., Richter, R. J., Ranchalis, J., Lewis, J., Bacus, T. J., McKinstry, L. A., Schellenberg, G. D., Rieder, M., Nickerson, D., Furlong, C. E., Chait, A., and Jarvik, G. P. (2006). TagSNP analyses of the PON gene cluster: effects on PON1 activity, LDL oxidative susceptibility, and vascular disease. J. Lipid Res. 47, 1014-1024.
12. Costa, L. G., and Furlong, C. E. (2002). Paraoxonase (PON1) in Health and Disease: Basic and Clinical Aspects. Norwell, MA: Springer.
13. Dahabreh, I. J., Kitsios, G. D., Kent, D. M., and Trikalinos, T. A. (2010). Paraoxonase 1 polymorphisms and ischemic stroke risk: a systematic review and meta-analysis. Genet. Med. 12, 606-615.
14. Deakin, S., Leviev, I., Brulhart-Meynet, M.-C., and James, R. W. (2003). Paraoxonase-1 promoter haplotypes and serum paraoxonase: a predominant role for polymorphic position107, implicating the Sp1 transcription factor. Biochem. J. 372, 643-649.
15. Draganov, D. I. (2010). Lactonases with organophosphatase activity: structural and evolutionary perspectives. Chem. Biol. Interact. 187, 370-372.
16. Draganov,D. I., and La Du, B. N. (2004). Pharmacogenetics of paraoxonases: a brief review. Naunyn Schmiedebergs Arch. Pharmacol. 369, 78-88.
17. Draganov, D. I., Teiber, J. F., Speelman, A., Osawa, Y., Sunahara, R., and La Du, B. N. (2005). Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificities. J. Lipid Res. 46, 1239-1247.
18. Erlich, P. M., Lunetta, K. L., Cupples, L. A., Huyck, M., Green, R. C., Baldwin, C. T., and Farrer, L. A. (2006). Polymorphisms in the PON gene cluster are associated withAlzheimer disease. Hum. Mol. Genet. 15, 77-85.
19. Furlong, C. E., Richter, R. J., Chapline, C., and Crabb, J. W. (1991). Purification of rabbit and human serum paraoxonase. Biochemistry 30, 10133-10140.
20. Gan, K. N., Smolen, A., Eckerson, H. W., and La Du, B. N. (1991). Purification of human serum paraoxonase/arylesterase. Evidence for one esterase catalyzing both activities. Drug Metab. Dispos. 19, 100-106.
21. Gomes, A. M., Winter, S., Klein, K., Turpeinen, M., Schaeffeler, E., Schwab, M., and Zanger, U. M. (2009). Pharmacogenomics of human liver cytochrome P450 oxidoreductase: multifactorial analysis and impact on microsomal drug oxidation. Pharmacogenomics 10, 579-599.
22. Gonzalvo, M. C., Gil, F., Hernandez, A. F., Rodrigo, L., Villanueva, E., and Pla, A. (1998). Human liver paraoxonase (PON1): subcellular distribution and characterization. J. Biochem. Mol. Toxicol. 12, 61-69.
23. Goosen, T. C., Bauman, J. N., Davis, J. A., Yu, C., Hurst, S. I., Williams, J. A., and Loi, C.-M. (2007). Atorvastatin glucuronidation is minimally and nonselectively inhibited by the fibrates gemfibrozil, fenofibrate, and fenofibric acid. Drug Metab. Dispos. 35, 1315-1324.
24. Gouédard, C., Barouki, R., and Morel, Y. (2004). Dietary polyphenols increase paraoxonase 1 gene expression by an aryl hydrocarbon receptor-dependent mechanism. Mol. Cell. Biol. 24, 5209-5222.
25. Han, C. Y., Chiba, T., Campbell, J. S., Fausto, N., Chaisson, M., Orasanu, G., Plutzky, J., and Chait, A. (2006). Reciprocal and coordinate regulation of serum amyloid A versus apolipoprotein A-I and paraoxonase-1 by inflammation in murine hepatocytes. Arterioscler. Thromb. Vasc. Biol. 26, 1806-1813.
26. Hardy-Weinberg Equilibrium. (2011). Available at: http://ihg2.helmholtzmuenchen.de/cgi-bin/hw/hwa1.pl
27. Harel, M., Aharoni, A., Gaidukov, L., Brumshtein, B., Khersonsky, O., Meged, R., Dvir, H., Ravelli, R. B. G., McCarthy, A., Toker, L., Silman, I., Sussman, J. L., and Tawfik, D. S. (2004). Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11, 412-419.
28. Hermann, M., Bogsrud, M. P., Molden, E., Asberg, A., Mohebi, B. U., Ose, L., and Retterstøl, K. (2006). Exposure of atorvastatin is unchanged but lactone and acid metabolites are increased several-fold in patients with atorvastatin-induced myopathy. Clin. Pharmacol. Ther. 79, 532-539.
29. Jacobsen, W., Kuhn, B., Soldner, A., Kirchner, G., Sewing, K. F., Kollman, P. A., Benet, L. Z., and Christians, U. (2000). Lactonization is the critical first step in the disposition of the 3-hydroxy-3-methylglutarylCoA reductase inhibitor atorvastatin. Drug Metab. Dispos. 28, 1369-1378.
30. Kantola, T., Kivistö, K. T., and Neuvonen, P. J. (1998). Erythromycin and verapamil considerably increase serum simvastatin and simvastatin acid concentrations. Clin. Pharmacol. Ther. 64, 177-182.
31. Kearney, A. S., Crawford, L. F., Mehta, S. C., and Radebaugh, G. W. (1993). The interconversion kinetics, equilibrium, and solubilities of the lactone and hydroxyacid forms of the HMG-CoA reductase inhibitor, CI-981. Pharm. Res. 10, 1461-1465.
32. Lang, T., Klein, K., Fischer, J., Nüssler, A. K., Neuhaus, P., Hofmann, U., Eichelbaum, M., Schwab, M., and Zanger, U. M. (2001). Extensive genetic polymorphism in the human CYP2B6 gene with impact on expression and function in human liver. Pharmacogenetics 11, 399-415.
33. Law, M., and Rudnicka, A. R. (2006). Statin safety: a systematic review. Am. J. Cardiol. 97, 52C-60C.
34. Leviev, I., and James, R. W. (2000). Promoter polymorphisms of human paraoxonase PON1 gene and serum paraoxonase activities and concentrations. Arterioscler. Thromb. Vasc. Biol. 20, 516-521.
35. Liu, T., Qian, W.-J., Gritsenko, M. A., Camp, D. G., Monroe, M. E., Moore, R. J., and Smith, R. D. (2005). Human plasma N-glycoproteome analysis by immunoaffinity subtraction, hydrazide chemistry, and mass spectrometry. J. Proteome Res. 4, 2070-2080.
36. Lu, H., Zhu, J., Zang, Y., Ze, Y., and Qin, J. (2006). Cloning, purification, and refolding of human paraoxonase-3 expressed in Escherichia coli and its characterization. Protein Expr. Purif. 46, 92-99.
37. Mackness, B., Hine, D., McElduff, P., and Mackness, M. (2006). High Creactive protein and low paraoxonase 1 in diabetes as risk factors for coronary heart disease. Atherosclerosis 186, 396-401.
38. Marcoff, L., and Thompson, P. D. (2007). The role of coenzyme Q10 in statin-associated myopathy: a systematic review. J. Am. Coll. Cardiol. 49, 2231-2237.
39. Marsillach, J., Aragonès, G., Beltrán, R., Caballeria, J., Pedro-Botet, J., Morcillo-Suárez, C., Navarro, A., Joven, J., and Camps, J. (2009). The measurement of the lactonase activity of paraoxonase-1 in the clinical evaluation of patients with chronic liver impairment. Clin. Biochem. 42, 91-98.
40. Neuvonen, P. J., Niemi, M., and Backman, J. T. (2006). Drug interactions with lipid-lowering drugs: mechanisms and clinical relevance. Clin. Pharmacol. Ther. 80, 565-581.
41. Nicolet, Y., Lockridge, O., Masson, P., Fontecilla-Camps, J. C., and Nachon, F. (2003). Crystal structure of human butyrylcholinesterase and of its complexes with substrate and products. J. Biol. Chem. 278, 41141-41147.
42. Nies,A. T.,Koepsell,H.,Winter,S.,Burk, O., Klein, K., Kerb, R., Zanger, U. M., Keppler, D., Schwab, M., and Schaeffeler, E. (2009). Expression of organic cation transporters OCT1 (SLC22A1) and OCT3 (SLC22A3) is affected by genetic factors and cholestasis in human liver. Hepatology 50, 1227-1240.
43. Prueksaritanont, T., Subramanian, R., Fang, X., Ma, B., Qiu, Y., Lin, J. H., Pearson, P. G., and Baillie, T. A. (2002). Glucuronidation of statins in animals and humans: a novel mechanism of statin lactonization. Drug Metab. Dispos. 30, 505-512.
44. Ranade, K., Kirchgessner, T. G., Iakoubova, O. A., Devlin, J. J., DelMonte, T., Vishnupad, P., Hui, L., Tsuchihashi, Z., Sacks, F. M., Sabatine, M. S., Braunwald, E., White, T. J., Shaw, P. M., and Dracopoli, N. C. (2005). Evaluation of the paraoxonases as candidate genes for stroke: Gln192Arg polymorphism in the paraoxonase 1 gene is associated with increased risk of stroke. Stroke 36, 2346-2350.
45. Riedmaier, S., Klein, K., Hofmann, U., Keskitalo, J. E., Neuvonen, P. J., Schwab, M., Niemi, M., and Zanger, U. M. (2010). UDPglucuronosyltransferase (UGT) polymorphisms affect atorvastatin lactonization in vitro and in vivo. Clin. Pharmacol. Ther. 87, 65-73.
46. Saeed, M., Siddique, N., Hung, W. Y., Usacheva, E., Liu, E., Sufit, R. L., Heller, S. L., Haines, J. L., Pericak-Vance, M., and Siddique, T. (2006). Paraoxonase cluster polymorphisms are associated with sporadic ALS. Neurology 67, 771-776.
47. Sanghera,D. K.,Manzi,S.,Minster,R. L., Shaw, P., Kao, A., Bontempo, F., and Kamboh, M. I. (2008). Genetic variation in the paraoxonase-3 (PON3) gene is associated with serum PON1 activity. Ann. Hum. Genet. 72, 72-81.
48. Sardo, M. A., Campo, S., Bonaiuto, M., Bonaiuto, A., Saitta, C., Trimarchi, G., Castaldo, M., Bitto, A., Cinquegrani, M., and Saitta, A. (2005). Antioxidant effect of atorvastatin is independent of PON1 gene T(-107)C, Q192R and L55M polymorphisms in hypercholestero-laemic patients. Curr.Med.Res. Opin. 21, 777-784.
49. Shitara, Y., and Sugiyama, Y. (2006). Pharmacokinetic and pharmacodynamic alterations of 3-hydroxy-3-methylglutaryl coenzyme A (HMG-CoA) reductase inhibitors: drug-drug interactions and interindividual differences in transporter and metabolic enzyme functions. Pharmacol. Ther. 112, 71-105.
50. Silva, M. A., Swanson, A. C., Gandhi, P. J., and Tataronis, G. R. (2006). Statin-related adverse events: a meta-analysis. Clin. Ther. 28, 26-35.
51. Skottheim, I. B., Gedde-Dahl, A., Hejazifar, S., Hoel, K., and Asberg, A. (2008). Statin induced myotoxicity: the lactone forms are more potent than the acid forms in human skeletal muscle cells in vitro. Eur. J. Pharm. Sci. 33, 317-325.
52. Suchocka,Z.,Swatowska,J.,Pachecka,J., and Suchocki, P. (2006). RP-HPLC determination of paraoxonase 3 activity in human blood serum. J. Pharm. Biomed. Anal. 42, 113-119.
53. Testa, B., and Mayer, J. M. (2003). Hydrolysis in drug and prodrug metabolism: chemistry, biochemistry, and enzymology. Zürich: Helvetica Chimica Acta.
54. The R Project for Statistical Computing. (2011). Available at: http://www.rproject.org/
55. Thompson, P. D., Clarkson, P., and Karas, R. H. (2003). Statinassociated myopathy. JAMA 289, 1681-1690.
56. Van Lenten, B. J., Wagner, A. C., Navab, M., and Fogelman, A. M. (2001). Oxidized phospholipids induce changes in hepatic paraoxonase and ApoJ but not monocyte chemoattractant protein-1 via interleukin-6. J. Biol. Chem. 276, 1923-1929.
57. Wang, X., Fan, Z., Huang, J., Su, S., Yu, Q., Zhao, J., Hui, R., Yao, Z., Shen, Y., Qiang, B., and Gu, D. (2003). Extensive association analysis between polymorphisms of PON gene cluster with coronary heart disease in Chinese Han population. Arterioscler. Thromb. Vasc. Biol. 23, 328-334.