From arylamine N-acetyltransferase to folate-dependent acetyl CoA hydrolase: Impact of folic acid on the activity of (HUMAN)NAT1 and its homologue (MOUSE)NAT2

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Laurieri, Nicola ^a,b   Dairou, Julien ^c   Egleton, James E ^a,b   Stanley, Lesley A ^d   Russell, Angela J ^a,b   Dupret, Jean Marie ^c   Sim, Edith ^a,e   Rodrigues Lima, Fernando ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Consultant in Investigative Toxicology ^*  (United Kingdom)

^e KINGSTON UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A HYDROLASE; ARYLAMINE ACETYLTRANSFERASE; ARYLAMINE ACETYLTRANSFERASE TYPE 1; ARYLAMINE ACETYLTRANSFERASE TYPE 2; FOLIC ACID; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ISOENZYME; N-ACETYLTRANSFERASE 1; N-HYDROXYARYLAMINE O-ACETYLTRANSFERASE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL METABOLISM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME RELEASE; ENZYME SPECIFICITY; HUMAN; NONHUMAN; PROTEIN HYDROLYSIS; XENOBIOTIC METABOLISM; ACETYLATION; ANIMAL; HYDROLYSIS; METABOLISM; MOUSE; NUCLEAR MAGNETIC RESONANCE;

ACETYL-COA HYDROLASE; ACETYLATION; ACETYLTRANSFERASES; ANIMALS; ARYLAMINE N-ACETYLTRANSFERASE; FOLIC ACID; HUMANS; HYDROLYSIS; ISOENZYMES; MICE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84900533452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096370     Document Type: Article

References (73)

1. Butcher NJ, Minchin RF (2012) Arylamine N-acetyltransferase 1: a novel drug target in cancer development. Pharmacol Rev 64: 147-165.
2. Sim E, Fakis G, Laurieri N, Boukouvala S (2012) Arylamine N-acetyltransferases-from drug metabolism and pharmacogenetics to identification of novel targets for pharmacological intervention. Adv Pharmacol 63: 169-205.
3. Sim E, Walters K, Boukouvala S (2008) Arylamine N-acetyltransferases: from structure to function. Drug Metab Rev 40: 479-510. (Pubitemid 352019961)
4. Hein DW (2009) N-acetyltransferase SNPs: emerging concepts serve as a paradigm for understanding complexities of personalized medicine. Expert Opin Drug Metab Toxicol 5: 353-366.
5. Sinclair JC, Sandy J, Delgoda R, Sim E, Noble ME (2000) Structure of arylamine N-acetyltransferase reveals a catalytic triad. Nat Struct Biol 7: 560-564. (Pubitemid 30445912)
6. Wu H, Dombrovsky L, Tempel W, Martin F, Loppnau P, et al. (2007) Structural basis of substrate-binding specificity of human arylamine N-acetyltransferases. J Biol Chem 282: 30189-30197. (Pubitemid 350035257)
7. Goodfellow GH, Dupret JM, Grant DM (2000) Identification of amino acids imparting acceptor substrate selectivity to human arylamine acetyltransferases NAT1 and NAT2. Biochem J 348: 159-166. (Pubitemid 30312144)
8. Sinclair J, Sim E (1997) A fragment consisting of the first 204 amino-terminal amino acids of human arylamine N-acetyltransferase one (NAT1) and the first transacetylation step of catalysis. Biochem Pharmacol 53: 11-16. (Pubitemid 26419781)
9. Derewlany LO, Knie B, Koren G (1994) Arylamine N-acetyltransferase activity of the human placenta. J Pharmacol Exp Ther 269: 756-760. (Pubitemid 24157347)
10. Derewlany LO, Knie B, Koren G (1994) Human placental transfer and metabolism of p-aminobenzoic acid. J Pharmacol Exp Ther 269: 761-765. (Pubitemid 24157348)
11. Smelt VA, Upton A, Adjaye J, Payton MA, Boukouvala S, et al. (2000) Expression of arylamine N-acetyltransferases in pre-term placentas and in human pre-implantation embryos. Hum Mol Genet 9: 1101-1107. (Pubitemid 30216016)
12. Pacifici GM, Bencini C, Rane A (1986) Acetyltransferase in humans: development and tissue distribution. Pharmacology 32: 283-291. (Pubitemid 16090382)
13. Minchin RF (1995) Acetylation of p-aminobenzoylglutamate, a folic acid catabolite, by recombinant human arylamine N-acetyltransferase and U937 cells. Biochem J 307: 1-3.
14. Ward A, Summers MJ, Sim E (1995) Purification of recombinant human N-acetyltransferase type 1 (NAT1) expressed in E. coli and characterization of its potential role in folate metabolism. Biochem Pharmacol 49: 1759-1767.
15. Minchin RF, Hanna PE, Dupret JM, Wagner CR, Rodrigues-Lima F, et al. (2007) Arylamine N-acetyltransferase I. Int J Biochem Cell Biol 39: 1999-2005. (Pubitemid 47369238)
16. Murphy M, Seagroatt V, Hey K, O'Donnell M, Godden M, et al. (1996) Neural tube defects 1974-94-down but not out. Arch Dis Child Fetal Neonatal Ed 75: F133-134.
17. Jensen LE, Hoess K, Mitchell LE, Whitehead AS (2006) Loss of function polymorphisms in NAT1 protect against spina bifida. Hum Genet 120: 52-57.
18. Erickson RP (2010) Genes, environment, and orofacial clefting: N-acetyltransferase and folic acid. J Craniofac Surg 21: 1384-1387.
19. Czeizel AE, Timar L, Sarkozi A (1999) Dose-dependent effect of folic acid on the prevention of orofacial clefts. Pediatrics 104: e66.
20. Kawamura A, Westwood I, Wakefield L, Long H, Zhang N, et al. (2008) Mouse N-acetyltransferase type 2, the homologue of human N-acetyltransferase type 1. Biochem Pharmacol 75: 1550-1560.
21. Boukouvala S, Price N, Sim E (2002) Identification and functional characterization of novel polymorphisms associated with the genes for arylamine N-acetyltransferases in mice. Pharmacogenetics 12: 385-394. (Pubitemid 34816418)
22. Martell KJ, Levy GN, Weber WW (1992) Cloned mouse N-acetyltransferases: enzymatic properties of expressed Nat-1 and Nat-2 gene products. Mol Pharmacol 42: 265-272. (Pubitemid 23026158)
23. Hein DW, Boukouvala S, Grant DM, Minchin RF, Sim E (2008) Changes in consensus arylamine N-acetyltransferase gene nomenclature. Pharmacogenet Genomics 18: 367-368. (Pubitemid 351367530)
24. Mitchell MK, Futscher BW, McQueen CA (1999) Developmental expression of N-acetyltransferases in C57BI/6 mice. Drug Metab Dispos 27: 261-264. (Pubitemid 29072082)
25. Stanley LA, Copp AJ, Pope J, Rolls S, Smelt V, et al. (1998) Immunochemical detection of arylamine N-acetyltransferase during mouse embryonic development and in adult mouse brain. Teratology 58: 174-182. (Pubitemid 28542486)
26. Ward A, Hickman D, Gordon JW, Sim E (1992) Arylamine N-acetyltransferase in human red blood cells. Biochem Pharmacol 44: 1099-1104.
27. Payton M, Smelt V, Upton A, Sim E (1999) A method for genotyping murine arylamine N-acetyltransferase type 2 (NAT2): a gene expressed in preimplantation embryonic stem cells encoding an enzyme acetylating the folate catabolite p-aminobenzoylglutamate. Biochem Pharmacol 58: 779-785. (Pubitemid 29329527)
28. Cornish VA, Pinter K, Boukouvala S, Johnson N, Labrousse C, et al. (2003) Generation and analysis of mice with a targeted disruption of the arylamine N-acetyltransferase Type 2 gene. Pharmacogenomics J 3: 169-177. (Pubitemid 36850158)
29. Wakefield L, Cornish V, Long H, Griffiths WJ, Sim E (2007) Deletion of a xenobiotic metabolizing gene in mice affects folate metabolism. Biochem Biophys Res Commun 364: 556-560. (Pubitemid 350030921)
30. Witham KL, Butcher NJ, Sugamori KS, Brenneman D, Grant DM, et al. (2013) 5-Methyl-tetrahydrofolate and the S-adenosylmethionine cycle in C57BL/6J Mouse Tissues: Gender differences and effects of arylamine N-acetyltransferase-1 deletion. PLoS One 8: e77923.
31. Wakefield L, Long H, Lack N, Sim E (2007) Ocular defects associated with a null mutation in the mouse arylamine N-acetyltransferase 2 gene. Mamm Genome 18: 270-276. (Pubitemid 46897403)
32. Cao W, Chau B, Hunter R, Strnatka D, McQueen CA, et al. (2005) Only low levels of exogenous N-acetyltransferase can be achieved in transgenic mice. Pharmacogenomics J 5: 255-261. (Pubitemid 41131717)
33. Erickson RP, Cao W, Acuna DK, Strnatka DW, Hunter RJ, et al. (2008) Confirmation of the role of N-acetyltransferase 2 in teratogen-induced cleft palate using transgenics and knockouts. Mol Reprod Dev 75: 1071-1076. (Pubitemid 351628592)
34. Sim E, Pinter K, Mushtaq A, Upton A, Sandy J, et al. (2003) Arylamine N-acetyltransferases: a pharmacogenomic approach to drug metabolism and endogenous function. Biochem Soc Trans 31: 615-619. (Pubitemid 36750741)
35. Sim E, Westwood I, Fullam E (2007) Arylamine N-acetyltransferases. Expert Opin Drug Metab Toxicol 3: 169-184. (Pubitemid 47316039)
36. Wakefield L, Boukouvala S, Sim E (2010) Characterisation of CpG methylation in the upstream control region of mouse Nat2: evidence for a gene-environment interaction in a polymorphic gene implicated in folate metabolism. Gene 452: 16-21.
37. Kim SJ, Kang HS, Chang HL, Jung YC, Sim HB, et al. (2008) Promoter hypomethylation of the N-acetyltransferase 1 gene in breast cancer. Oncol Rep 19: 663-668. (Pubitemid 351330433)
38. Adam PJ, Berry J, Loader JA, Tyson KL, Craggs G, et al. (2003) Arylamine N-acetyltransferase-1 is highly expressed in breast cancers and conveys enhanced growth and resistance to etoposide in vitro. Mol Cancer Res 1: 826-835. (Pubitemid 37174454)
39. Johansson I, Nilsson C, Berglund P, Lauss M, Ringner M, et al. (2012) Gene expression profiling of primary male breast cancers reveals two unique subgroups and identifies N-acetyltransferase-1 (NAT1) as a novel prognostic biomarker. Breast Cancer Res 14: R31.
40. Wakefield L, Robinson J, Long H, Ibbitt JC, Cooke S, et al. (2008) Arylamine N-acetyltransferase 1 expression in breast cancer cell lines: a potential marker in estrogen receptor-positive tumors. Genes Chromosomes Cancer 47: 118-126.
41. Russell AJ, Westwood IM, Crawford MH, Robinson J, Kawamura A, et al. (2009) Selective small molecule inhibitors of the potential breast cancer marker, human arylamine N-acetyltransferase 1, and its murine homologue, mouse arylamine N-acetyltransferase 2. Bioorg Med Chem 17: 905-918.
42. Ballester PJ, Westwood I, Laurieri N, Sim E, Richards WG (2010) Prospective virtual screening with Ultrafast Shape Recognition: the identification of novel inhibitors of arylamine N-acetyltransferases. J R Soc Interface 7: 335-342.
43. Tiang JM, Butcher NJ, Minchin RF (2010) Small molecule inhibition of arylamine N-acetyltransferase Type I inhibits proliferation and invasiveness of MDA-MB-231 breast cancer cells. Biochem Biophys Res Commun 393: 95-100.
44. Laurieri N, Crawford MH, Kawamura A, Westwood IM, Robinson J, et al. (2010) Small molecule colorimetric probes for specific detection of human arylamine N-acetyltransferase 1, a potential breast cancer biomarker. J Am Chem Soc 132: 3238-3239.
45. Laurieri N, Egleton JE, Varney A, Thinnes CC, Quevedo CE, et al. (2013) A novel color change mechanism for breast cancer biomarker detection: naphthoquinones as specific ligands of human arylamine N-acetyltransferase 1. PLoS One 8: e70600.
46. Dairou J, Atmane N, Dupret JM, Rodrigues-Lima F (2003) Reversible inhibition of the human xenobiotic-metabolizing enzyme arylamine N-acetyltransferase 1 by S-nitrosothiols. Biochem Biophys Res Commun 307: 1059-1065. (Pubitemid 36871678)
47. Westwood IM, Holton SJ, Rodrigues-Lima F, Dupret JM, Bhakta S, et al. (2005) Expression, purification, characterization and structure of Pseudomonas aeruginosa arylamine N-acetyltransferase. Biochem J 385: 605-612. (Pubitemid 40165095)
48. Sandy J, Mushtaq A, Kawamura A, Sinclair J, Sim E, et al. (2002) The structure of arylamine N-acetyltransferase from Mycobacterium smegmatis -an enzyme which inactivates the anti-tubercular drug, isoniazid. J Mol Biol 318: 1071-1083. (Pubitemid 35007369)
49. Fullam E, Kawamura A, Wilkinson H, Abuhammad A, Westwood I, et al. (2009) Comparison of the arylamine N-acetyltransferase from Mycobacterium marinum and Mycobacterium tuberculosis. Protein J 28: 281-293.
50. Abuhammad A, Lack N, Schweichler J, Staunton D, Sim RB, et al. (2011) Improvement of the expression and purification of Mycobacterium tuberculosis arylamine N-acetyltransferase (TBNAT) a potential target for novel antitubercular agents. Protein Expr Purif.
51. Sandy J, Holton S, Fullam E, Sim E, Noble M (2005) Binding of the antitubercular drug isoniazid to the arylamine N-acetyltransferase protein from Mycobacterium smegmatis. Protein Sci 14: 775-782. (Pubitemid 40283916)
52. Fullam E, Westwood IM, Anderton MC, Lowe ED, Sim E, et al. (2008) Divergence of cofactor recognition across evolution: Coenzyme A binding in a prokaryotic arylamine N-acetyltransferase. J Mol Biol 375: 178-191. (Pubitemid 350160690)
53. Wang H, Vath GM, Kawamura A, Bates CA, Sim E, et al. (2005) Overexpression, purification, and characterization of recombinant human arylamine N-acetyltransferase 1. Protein J 24: 65-77. (Pubitemid 40875246)
54. Grant DM, Blum M, Beer M, Meyer UA (1991) Monomorphic and polymorphic human arylamine N-acetyltransferases: a comparison of liver isozymes and expressed products of two cloned genes. Mol Pharmacol 39: 184-191.
55. Brooke EW, Davies SG, Mulvaney AW, Pompeo F, Sim E, et al. (2003) An approach to identifying novel substrates of bacterial arylamine N-acetyltransferases. Bioorg Med Chem 11: 1227-1234. (Pubitemid 36293519)
56. Andres HH, Klem AJ, Szabo SM, Weber WW (1985) New spectrophotometric and radiochemical assays for acetyl-CoA: arylamine N-acetyltransferase applicable to a variety of arylamines. Anal Biochem 145: 367-375. (Pubitemid 15100964)
57. Westwood IM, Kawamura A, Fullam E, Russell AJ, Davies SG, et al. (2006) Structure and mechanism of arylamine N-acetyltransferases. Curr Top Med Chem 6: 1641-1654. (Pubitemid 44304619)
58. Patel SS, Walt DR (1987) Substrate specificity of acetyl Coenzyme A synthetase. J Biol Chem 262: 7132-7134.
59. Wu WJ, Tonge PJ, Raleigh DP (1998) Stereospecific H-1 and C-13 NMR assignments of crotonyl CoA and hexadienoyl CoA: Conformational analysis and comparison with protein-CoA complexes. Journal of the American Chemical Society 120: 9988-9994. (Pubitemid 28473574)
60. Rossi C, Donati A, Sansoni MR (1993) Folic-Acid - Solution Structure and NMR Strategy for Conformational-Analysis. Spectrosc Lett 26: 1603-1611.
61. DeLano WL (2002) PyMOL: An open-source molecular graphics tool. DeLano Scientific, San Carlos, California, USA; http://www.ccp4.ac.uk/newsletters/ newsletter40/11-pymol.pdf.
62. Verdonk ML, Cole JC, Hartshorn MJ, Murray CW, Taylor RD (2003) Improved protein-ligand docking using GOLD. Proteins 52: 609-623. (Pubitemid 37034158)
63. Mushtaq A, Payton M, Sim E (2002) The COOH terminus of arylamine N-acetyltransferase from Salmonella typhimurium controls enzymic activity. J Biol Chem 277: 12175-12181. (Pubitemid 34952783)
64. Wang H, Liu L, Hanna PE, Wagner CR (2005) Catalytic mechanism of hamster arylamine N-acetyltransferase 2. Biochemistry 44: 11295-11306. (Pubitemid 41209065)
65. Wang H, Vath GM, Gleason KJ, Hanna PE, Wagner CR (2004) Probing the mechanism of hamster arylamine N-acetyltransferase 2 acetylation by active site modification, site-directed mutagenesis, and pre-steady state and steady state kinetic studies. Biochemistry 43: 8234-8246. (Pubitemid 38808279)
66. Jencks WP, Gresser M, Valenzuela MS, Huneeus FC (1972) Acetyl Coenzyme A: arylamine acetyltransferase. Measurement of the steady state concentration of the acetyl-enzyme intermediate. J Biol Chem 247: 3756-3760.
67. Claridge TDW, Davies SG, Polywka MEC, Roberts PM, Russell AJ, et al. (2008) "Pure by NMR"? Organic Letters 10: 5433-5436.
68. Abuhammad AM, Lowe ED, Fullam E, Noble M, Garman EF, et al. (2010) Probing the architecture of the Mycobacterium marinum arylamine N-acetyltransferase active site. Protein Cell 1: 384-392.
69. Matte C, Mackedanz V, Stefanello FM, Scherer EB, Andreazza AC, et al. (2009) Chronic hyperhomocysteinemia alters antioxidant defenses and increases DNA damage in brain and blood of rats: protective effect of folic acid. Neurochem Int 54: 7-13.
70. Moat SJ, Bonham JR, Cragg RA, Powers HJ (2000) Elevated plasma homocysteine elicits an increase in antioxidant enzyme activity. Free Radic Res 32: 171-179. (Pubitemid 30056793)
71. Egleton JE, Thinnes CC, Seden PT, Laurieri N, Lee SP, et al. (2014) Structure-activity relationships and colorimetric properties of specific probes for the putative cancer biomarker human arylamine N-acetyltransferase 1. Bioorg Med Chem In press.
72. Lam Y-F, Kotowycz G (1972) Self association of folic acid in aqueous solution by Proton Magnetic Resonance. Canadian Journal of Chemistry 50: 2357-2363.
73. Rossi C, Donati A, Sansoni MR (1993) Folic acid: Solution structure and NMR strategy for conformational analysis. Spectrosc Lett 26: 1603-1611.