Inherited and acquired interactions between ACHE and PON1 polymorphisms modulate plasma acetylcholinesterase and paraoxonase activities

Journal of Neurochemistry

Volumn 92, Issue 5, 2005, Pages 1216-1227

  Bryk, Boris ^a,b   Benmoyal Segal, Liat ^a   Podoly, Erez ^a,c   Livnah, Oded ^a,c   Eisenkraft, Arik ^b   Luria, Shai ^b   Cohen, Amir ^b   Yehezkelli, Yoav ^b   Hourvitz, Ariel ^b   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b MEDICAL CORPS   (Israel)

^c Wolfson Ctr for Appl Struct Biol   (Israel)

Author keywords

Acetylcholinesterase; Arylesterase; Butyrylcholinesterase; Gene environment interactions; Paraoxonase; Structure function relationships

Indexed keywords

ACETYLCHOLINESTERASE; ARYLDIALKYLPHOSPHATASE; ARYLESTERASE; GENE PRODUCT; ORGANOPHOSPHATE INHIBITABLE ACETYLCHOLINESTERASE; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CHROMOSOME 7Q; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BLOOD LEVEL; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FEMALE; GENE; GENE EXPRESSION; GENE LOCUS; GENE STRUCTURE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HUMAN; HYDROLYSIS; MALE; MOLECULAR MODEL; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PON1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION;

ACETYLCHOLINESTERASE; ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AMINO ACID MOTIFS; ANIMALS; ARYLDIALKYLPHOSPHATASE; BUTYRYLCHOLINESTERASE; CARBOXYLIC ESTER HYDROLASES; CERCOPITHECUS AETHIOPS; COS CELLS; FEMALE; GENE FREQUENCY; GENOTYPE; HUMANS; MALE; MIDDLE AGED; MODELS, MOLECULAR; MUTATION; PHENOTYPE; POLYMORPHISM, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 20044382046     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02959.x     Document Type: Article

References (55)

1. Aviram M., Rosenblat M., Bisgaier C. L., Newton R. S., Primo-Parmo S. L. and La Du B. N. (1998) Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. J. Clin. Invest. 101, 1581-1590.
2. Bartels C. F., Zelinski T. and Lockridge O. (1993) Mutation at codon 322 in the human acetylcholinesterase (ACHE) gene accounts for YT blood group polymorphism. Am. J. Hum. Genet. 52, 928-936.
3. Berkowitz G. S., Wetmur J. G., Birman-Deych E., Obel J., Lapinski R. H., Godbold J. H., Holzman I. R. and Wolff M. S. (2004) In utero pesticide exposure, maternal paraoxonase activity, and head circumference. Environ. Health Perspect. 112, 388-391.
4. Brenner T., Hamra-Amitay Y., Evron T., Boneva N., Seidman S. and Soreq H. (2003) The role of readthrough acetylcholinesterase in the pathophysiology of myasthenia gravis. Faseb J. 17, 214-222.
5. Brophy V. H., Jampsa R. L., Clendenning J. B., McKinstry L. A., Jarvik G. P. and Furlong C. E. (2001) Effects of 5′ regulatory-region polymorphisms on paraoxonase-gene (PON1) expression. Am. J. Hum. Genet. 68, 1428-1436.
6. Cohen O., Reichenberg A., Perry C., Ginzberg D., Pollmacher T., Soreq H. and Yirmiya R. (2003) Endotoxin-induced changes in human working and declarative memory associate with cleavage of plasma 'readthrough' acetylcholinesterase. J. Mol. Neurosci. 21, 199-212.
7. Costa L. G., Cole T. B., Jarvik G. P. and Furlong C. E. (2003) Functional genomics of the paraoxonase (PON1) polymorphism: effects on pesticide sensitivity, cardiovascular disease, and drug metabolism. Annu. Rev. Med. 54, 371-392.
8. Davies H. G., Richter R. J., Keifer M., Broomfield C. A., Sowalla J. and Furlong C. E. (1996) The effect of the human serum paraoxonase polymorphism is reversed with diazoxon, soman and sarin. Nat. Genet. 14, 334-336.
9. 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 position-107, implicating the Sp1 transcription factor. Biochem. J. 372, 643-649.
10. Devlin B. and Risch N. (1995) A comparison of linkage disequilibrium measures for fine-scale mapping. Genomics 29, 311-322.
11. Doctor B. P., Raveh L., Wolfe A. D., Maxwell D. M. and Ashani Y. (1991) Enzymes as pretreatment drugs for organophosphate toxicity. Neurosci. Biobehav. Rev. 15, 123-128.
12. Draganov D. I. and La Du B. N. (2004) Pharmacogenetics of paraoxonases: a brief review. Naunyn Schmiedebergs Arch. Pharmacol. 369, 78-88.
13. Draganov D. I., Stetson P. L., Watson C. E., Billecke S. S. and La Du B. N. (2000) Rabbit serum paraoxonase 3 (PON3) is a high density lipoprotein-associated lactonase and protects low-density lipoprotein against oxidation. J. Biol. Chem. 275, 33 435-33 442.
14. Ehrlich G., Ginzberg D., Loewenstein Y., Click D., Kerem B., Ben Ari S., Zakut H. and Soreq H. (1994) Population diversity and distinct haplotype frequencies associated with ACHE and BCHE genes of Israeli Jews from trans-Caucasian Georgia and from Europe. Genomics 22, 288-295.
15. Eiden L. E. (1998) The cholinergic gene locus. J. Neurochem. 70, 2227-2240.
16. Ellman G. L., Courtney D., Andres V. J. and Featherstone R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
17. Furlong C. E., Richter R. J., Seidel S. L., Costa L. G. and Motulsky A. G. (1989) Spectrophotometric assays for the enzymatic hydrolysis of the active metabolites of chlorpyrifos and parathion by plasma paraoxonase/arylesterase. Anal. Biochem. 180, 242-247.
18. Garin M. C., James R. W., Dussoix P., Blanche H., Passa P., Froguel P. and RuiZ. J. (1997) Paraoxonase polymorphism Met-Leu54 is associated with modified serum concentrations of the enzyme. A possible link between the paraoxonase gene and increased risk of cardiovascular disease in diabetes. J. Clin. Invest. 99, 62-66.
19. Click D., Ben Moyal L. and Soreq H. (2003) Genetic variation in butyrylcholinesterase and the physiological consequences for acetylcholinesterase function, in Butyrylcholinesterase: Function and Inhibition (Giacobini, E., ed.), pp. 55-67, Martin Dunitz, London.
20. Guex N. and Peitsch M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18, 2714-2723.
21. Harel M., Aharoni A., Gaidukov L. et al. (2004) Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11, 412-419.
22. Jarvik G. P., Jampsa R., Richter R. J., Carlson C. S., Rieder M. J., Nickerson D. A. and Furlong C. E. (2003) Novel paraoxonase (PON1) nonsense and missense mutations predicted by functional genomic assay of PON1 status. Pharmacogenetics 13, 291-295.
23. Kaufer D., Friedman A., Seidman S. and Soreq H. (1998) Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature 393, 373-377.
24. Keeler J. R., Hurst C. G. and Dunn M. A. (1991) Pyridostigmine used as a nerve agent pre-treatment under wartime conditions. JAMA 266, 693-695.
25. Kuo C. L. and La Du B. N. (1998) Calcium binding by human and rabbit serum paraoxonases. Structural stability and enzymatic activity. Drug Metab. Dispos. 26, 653-660.
26. La Du B. N., Billecke S., Hsu C., Haley R. W. and Broomfield C. A. (2001) Serum paraoxonase (PON1) isozymes: the quantitative analysis of isozymes affecting individual sensitivity to environmental chemicals. Drug Metab. Dispos. 29, 566-569.
27. 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.
28. Leviev I., Deakin S. and James R. W. (2001) Decreased stability of the M54 isoform of paraoxonase as a contributory factor to variations in human serum paraoxonase concentrations. J. Lipid Res. 42, 528-535.
29. Li W. F., Costa L. G., Richter R. J., Hagen T., Shih D. M., Tward A., Lusis A. J. and Furlong C. E. (2000) Catalytic efficiency determines the in-vivo efficacy of PON1 for detoxifying organophosphorus compounds. Pharmacogenetics 10, 767-779.
30. Mackness B., Davies G. K., Turkic W., Lee E., Roberts D. H., Hill E., Roberts C., Durrington P. N. and Mackness M. I. (2001) Paraoxonase status in coronary heart disease: are activity and concentration more important than genotype? Arterioscler. Thromb. Vasc. Biol. 21, 1451-1457.
31. Mackness M. I., Mackness B. and Durrington P. N. (2002) Paraoxonase and coronary heart disease. Atheroscler. Suppl. 3, 49-55.
32. Meshorer E., Erb C., Gazit R., Pavlovsky L., Kaufer D., Friedman A., Glick D., Ben-Arie N. and Soreq H. (2002) Alternative splicing and neuritic mRNA translocation under long-term neuronal hypersensitivity. Science 295, 508-512.
33. Ng C. J., Wadleigh D. J., Gangopadhyay A., Hama S., Grijalva V. R., Navab M., Fogelman A. M. and Reddy S. T. (2001) 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. 276, 44 444-44 449.
34. Oda M. N., Bielicki J. K., Berger T. and Forte T. M. (2001) Cysteine substitutions in apolipoprotein A-I primary structure modulate paraoxonase activity. Biochemistry 40, 1710-1718.
35. Ordentlich A., Barak D., Kronman C., Ariel N., Segall Y., Velan B. and Shafferman A. (1998) Functional characteristics of the oxyanion hole in human acetylcholinesterase. J. Biol. Chem. 273, 19 509-19 517.
36. Palmer A. M. (2003) Cholinergic therapies for Alzheimer's disease: progress and prospects. Curr. Opin. Invest. Drugs 4, 820-825.
37. Pick M., Flores-Flores C., Grisaru D., Shochat S., Deutsch V. and Soreq H. (2004) Blood cells-specific acetylcholinesterase splice variations under changing stimuli. Int. J. Dev. Neurosci. 22, 523-531.
38. Poulsen M. E. and Andersen J. H. (2003) Results from the monitoring of pesticide residues in fruit and vegetables on the Danish market, 2000-01. Food Addit Contam 20, 742-757.
39. Reddy S. T., Wadleigh D. J., Grijalva V. et al. (2001) Human paraoxonase-3 is an HDL-associated enzyme with biological activity similar to paraoxonase-1 protein but is not regulated by oxidized lipids. Arterioscler. Thromb. Vasc. Biol. 21, 542-547.
40. Rozenberg O., Rosenblat M., Coleman R., Shih D. M. and Aviram M. (2003) Paraoxonase (PON1) deficiency is associated with increased macrophage oxidative stress: studies in PON1-knockout mice. Free Radic. Biol. Med. 34, 774-784.
41. Ryan T. M., Sun C. W., Ren J. and Townes T. M. (2000) Human γ-globin gene promoter element regulates human β-globin gene developmental specificity. Nucleic Acids Res. 28, 2736-2740.
42. Sekar K., Yu B. Z., Rogers J., Lutton J., Liu X., Chen X., Tsai M. D., Jain M. K. and Sundaralingam M. (1997) Phospholipase A2 engineering. Structural and functional roles of the highly conserved active site residue aspartate-99. Biochemistry 36, 3104-3114.
43. Seres I., Paragh G., Deschene E., Fulop T. Jr and Khalil A. (2004) Study of factors influencing the decreased HDL associated PON1 activity with aging. Exp. Gerontol. 39, 59-66.
44. Shapira M., Tur-Kaspa I., Bosgraaf L., Livni N., Grant A. D., Grisaru D., Korner M., Ebstein R. P. and Soreq H. (2000) A transcription-activating polymorphism in the ACHE promoter associated with acute sensitivity to anti-acetylcholinesterases. Hum. Mol. Genet. 9, 1273-1281.
45. Shapira M., Click D., Gilbert J. P. and Soreq H. (2001) Autism, stress and chromosome 7 genes, in The Research Basis of Autism Intervention (Schloper E., Marcus L., Shulman C. and Yirmiya N., ed.), pp. 103-113. Kluwer Academic/Plenum Publishers, New York.
46. Shih D. M., Gu L., Xia Y. R. et al. (1998) Mice lacking serum paraoxonase are susceptible to organophosphate toxicity and atherosclerosis. Nature 394, 284-287.
47. Shostak S. (2003) Locating gene-environment interaction: at the intersections of genetics and public health. Soc. Sci. Med. 56, 2327-2342.
48. Sklan E. H., Lowenthal A., Korner M. et al. (2004) Acetylcholinesterase/ paraoxonase genotype and expression predict anxiety scores in Health, Risk Factors, Exercise Training, and Genetics Study. Proc. Natl Acad. Sci. USA 101, 5512-5517.
49. Slatkin M, and Excoffier L. (1996) Testing for linkage disequilibrium in genotypic data using the expectation-maximization algorithm. Heredity 76, 377-383.
50. Sorensen K., Brodbeck U., Rasmussen A. G. and Norgaard-Pedersen B. (1986) Normal human serum contains two forms of acetylcholinesterase. Clin. Chim. Acta 158, 1-6.
51. Soreq H. and Seidman S. (2001) Acetylcholinesterase: new roles for an old actor. Nat. Rev. Neurosci. 2, 294-302.
52. Suehiro T., Nakamura T., Inoue M., Shiinoki T., Ikeda Y., Kumon Y., Shindo M., Tanaka H. and Hashimoto K. (2000) A polymorphism upstream from the human paraoxonase (PON1) gene and its association with PON1 expression. Atherosclerosis 150, 295-298.
53. Sussman J. L., Harel M., Frolow F., Oefner C., Goldman A., Toker L. and Silman I. (1991) Atomic structure of acetylcholinesterase from Torpedo califomica: a prototypic acetylcholine-binding protein. Science 253, 872-879.
54. Weiner L., Kreimer D., Roth E. and Silman I. (1994) Oxidative stress transforms acetylcholinesterase to a molten-globule-like state. Biochem. Biophys. Res. Commun. 198, 915-922.
55. Zakut H., Even L., Birkenfeld S., Malinger G., Zisling R. and Soreq H. (1988) Modified properties of serum cholinesterases in primary carcinomas. Cancer 61, 727-737.