Sulfation through the looking glass - Recent advances in sulfotransferase research for the curious

Pharmacogenomics Journal

Volumn 2, Issue 5, 2002, Pages 297-308

  Coughtrie, M W H ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Development; Pharmacogenetics; Structural biology; Sulfation; Sulfotransferase

Indexed keywords

ESTROGEN SULFOTRANSFERASE; HORMONE; NEUROTRANSMITTER; SULFOTRANSFERASE; XENOBIOTIC AGENT;

BREAST CANCER; CANCER SUSCEPTIBILITY; CATALYSIS; COLORECTAL CANCER; CRYSTAL STRUCTURE; CYTOSOL; DETOXIFICATION; DEVELOPMENT; DRUG DESIGN; DRUG DEVELOPMENT; ENZYME ACTIVITY; ENZYME POLYMORPHISM; ENZYME SPECIFICITY; GENE EXPRESSION; GENOTYPE; HUMAN; KNOCKOUT GENE; MEDICAL RESEARCH; METABOLISM; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SULFATION; X RAY; ANIMAL; CHEMISTRY; GENETICS; METHODOLOGY; PHARMACEUTICS; PHARMACOGENETICS;

ANIMALS; HUMANS; PHARMACOGENETICS; SULFOTRANSFERASES; TECHNOLOGY, PHARMACEUTICAL;

EID: 0036448454     PISSN: 1470269X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.tpj.6500117     Document Type: Review

References (96)

1. Robbins PW, Lipmann F. Isolation and identification of active sulfate. J Biol Chem 1957; 229: 837-851.
2. Klaassen CD, Boles JW. The importance of 3′-phosphoadenosine 5′-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J 1997; 11: 404-418.
3. Dousa MK, Tyce GM. Free and conjugated plasma catecholamines, DOPA and 3-O-methyldopa in humans and various animal species. Proc Soc Exp Biol Med 1988; 188: 427-434.
4. Eisenhofer G, Coughtrie MWH, Goldstein DS. Dopamine sulphate: an enigma resolved. Clin Exp Pharmacol Physiol 1999; 26: S41-S53.
5. Ogura K, Kajita J, Narihata H, Watabe T, Ozawa S, Nagata K et al. Cloning and sequence analysis of a rat liver cDNA encoding hydroxysteroid sulfotranferase. Biochem Biophys Res Commun 1989; 165: 168-174.
6. Ogura K, Kajita J, Narihata H, Watabe T, Ozawa S, Nagata K et al. cDNA cloning of the hydroxysteroid sulfotransferase STa sharing a strong homology in amino acid sequence with the senescence marker protein SMP-2 in rat livers. Biochem Biophys Res Commun 1990; 166: 1494-1500.
7. Watabe T, Ogura K, Satsukawa M, Okuda H, Hiratsuka A. Molecular cloning and functions of rat liver hydroxysteroid sulfotransferases catalysing covalent binding of carcinogenic polycyclic arylmethanols to DNA. Chem Biol Interact 1994; 92: 87-105.
8. Otterness DM, Wieben ED, Wood TC, Watson RWG, Madden BJ, McCormick DJ et al. Human liver dehydroepiandrosterone sulfotransferase: molecular cloning and expression of cDNA. Mol Pharmacol 1992; 41: 865-872.
9. Barker EV, Hume R, Hallas A, Coughtrie MWH. Dehydroepiandrosterone sulfotransferase in the developing human fetus-quantitative biochemical and immunological characterization of the hepatic, renal, and adrenal enzymes. Endocrinology 1994; 134: 982-989.
10. Hume R, Barker EV, Coughtrie MWH. Differential expression and immunohistochemical localization of the phenol and hydroxysteroid sulfotransferase enzyme families in the developing lung. Histochem Cell Biol 1996; 105: 147-152.
11. Hume R, Coughtrie MWH. Phenolsulfotransferase-localization in kidney during human embryonic and fetal development. Histochem J 1994; 26: 850-855.
12. Richard K, Hume R, Kaptein E, Stanley EL, Visser TJ, Coughtrie MWH. Sulfation of thyroid hormone and dopamine during human development-ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung and brain. J Clin Endocrinol Metab 2001; 86: 2734-2742.
13. Stanley EL. Expression and function of iodothyronine metabolising enzymes during human placental and fetal development. PhD Thesis, University of Dundee, 2001.
14. Hakkola J, Pelkonen O, Pasanen M, Raunio H. Xenobiotic-metabolizing cytochrome P450 enzymes in the human feto-placental unit: role in intrauterine toxicity. Crit Rev Toxicol 1998; 28 : 35-72.
15. Coughtrie MWH, Burchell B, Leakey JEA, Hume R. The inadequacy of perinatal glucuronidation-immunoblot analysis of the developmental expression of individual UDP-glucuronosyltransferase isoenzymes in rat and human-liver microsomes. Mol Pharmacol 1988; 34: 729-735.
16. Varin L, Marsolais F, Richard M, Rouleau M. Biochemistry and molecular biology of plant sulfotransferases. FASEB J 1997; 11: 517-525.
17. Weinshilboum RM, Otterness DM, Aksoy IA, Wood TC, Her C, Raftogianis RB. Sulfotransferase molecular biology: cDNAs and genes. FASEB J 1997; 11: 3-14.
18. Her C, Kaur GP, Athwal RS, Weinshilboum RM. Human sulfotransferase SULT1C1: cDNA cloning, tissue-specific expression and chromosomal localization. Genomics 1997; 41: 467-470.
19. Sakakibara Y, Yanagishita M, Katafuchi J, Ringer DP, Takami Y, Nakayama T et al. Molecular cloning, expression, and characterization of novel human SULT1C sulfotransferases that catalyze sulfonation of N-hydroxy-2-acetylaminofluorene. J Biol Chem 1998; 273: 33929-33935.
20. Parker CR, Falany CN, Stockard CR, Stankovic AK, Grizzle WE. Immunohistochemical localization of dehydroepiandrosterone sulfotransferase in human fetal tissues. J Clin Endocrinol Metab 1994; 78: 234-236.
21. Song WC, Melner MH. Editorial: steroid transformation enzymes as critical regulators of steroid action in vivo. Endocrinology 2000; 141: 1587-1589.
22. Buirchell BJ, Hähnel R. Metabolism of estradiol-17b in human endometrium during the menstrual cycle. J Steroid Biochem 1975; 6: 1489-1494.
23. Rubin GL, Harrold AJ, Mills JA, Falany CN, Coughtrie MWH. Regulation of sulfotransferase expression in the endometrium during the menstrual cycle, by oral contraceptives and during early pregnancy. Mol Human Reprod 1999; 5: 995-1002.
24. Tseng L, Liu HC. Stimulation of arylsulfotransferase activity by progestins in human endometrium in vitro. J Clin Endocrinol Metab 1981; 53: 418-421.
25. Falany JL, Falany CN. Regulation of estrogen sulfotransferase in human endometrial adenocarcinoma cells by progesterone. Endocrinology 1996; 137: 1395-1401.
26. Kester MHA, Bulduk S, Tibboel D, Meinl W, Glatt H, Falany CN et al. Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology 2000; 141: 1897-1900.
27. Safe SH. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit Rev Toxicol 1994; 24: 87-149.
28. Falany CN, Xie XW, Wang J, Ferrer J, Falany JL. Molecular cloning and expression of novel sulphotransferase-like cDNAs from human and rat brain. Biochem J 2000; 346: 857-864.
29. Hume R, Coughtrie MWH, Burchell B. Differential localization of UDP-glucuronosyltransferase in kidney during human embryonic and fetal development. Arch Toxicol 1995; 69: 242-247.
30. Kakuta Y, Pedersen LG, Carter CW, Negishi M, Pedersen LC. Crystal structure of estrogen sulphotransferase. Nature Struct Biol 1997; 4: 904-908.
31. Dajani R, Cleasby A, Neu M, Wonacott AJ, Jhoti H, Hood AM et al. X-ray crystal structure of human dopamine sulfotransferase, SULT1A3: molecular modelling and QSAR analysis demonstrate a molecular basis for sulfotransferase substrate specificity. J Biol Chem 1999; 274: 37862-37868.
32. Bidwell LM, McManus ME, Gaedigk A, Kakuta Y, Negishi M, Pedersen L et al. Crystal structure of human catecholamine sulfotransferase. J Mol Biol 1999; 293: 521-530.
33. Pedersen LC, Petrotchenko EV, Negishi M. Crystal structure of SULT2A3, human hydroxysteroid sulfotransferase. FEBS Lett 2000; 475: 61-64.
34. Kakuta Y, Sueyoshi T, Negishi M, Pedersen LC. Crystal structure of the sulfotransferase domain of human heparan sulfate N-deacetylase/N-sulfotransferase 1. J Biol Chem 1999; 274: 10673-10676.
35. Pakhomova S, Kobayashi M, Buck J, Newcomer ME. A helical lid converts a sulfotransferase to a dehydratase. Nat Struct Biol 2001; 8: 447-451.
36. Yoshinari K, Petrotchenko EV, Pedersen LC, Negishi M. Crystal structure-based studies of cytosolic sulfotransferase. J Biochem Molec Toxicol 2001; 15: 67-75.
37. Kakuta Y, Petrotchenko EV, Pedersen LC, Negishi M. The sulfuryl transfer mechanism: crystal structure of a vanadate complex of estrogen sulfotransferase and mutational analysis. J Biol Chem 1998; 273: 27325-27330.
38. 146, governs the substrate specificity of a human dopamine sulfotransferase, SULT1A3. Mol Pharmacol 1998; 54: 942-948.
39. Brix LA, Barnett AC, Duggleby RG, Leggett B, McManus ME. Analysis of the substrate specificity of human sulfotransferases SULT1A1 and SULT1A3: site-directed mutagenesis and kinetic studies. Biochemistry 1999; 38: 10474-10479.
40. Brix LA, Duggleby RG, Gaedigk A, McManus ME. Structural characterization of human aryl sulphotransferases. Biochem J 1999; 337: 337-343.
41. Petrotchenko EV, Doerflein ME, Kakuta Y, Pedersen LC, Negishi M. Substrate gating confers steroid specificity to estrogen sulfotransferase. J Biol Chem 1999; 274: 30019-30022.
42. Weinshilboum R. Phenol sulfotransferase inheritance. Cell Mol Neurobiol 1988; 8: 27-33.
43. Weinshilboum R. Sulfotransferase pharmacogenetics. Pharmac Ther 1990; 45: 93-107.
44. Weinshilboum R, Aksoy I. Sulfation pharmacogenetics in humans. Chem Biol Interact 1994; 92: 233-246.
45. Glatt H, Engelke CEH, Pabel U, Teubner W, Jones AL, Coughtrie MWH et al. Sulfotransferases: genetics and role in toxicology. Toxicol Lett 2000; 112: 341-348.
46. Price RA, Spielman RS, Lucena AL, van Loon JA, Baidak BL, Weinshilboum RM. Genetic polymorphism for human platelet thermostable phenol sulfotransferase (TS PST) activity. Genetics 1989; 122: 905-914.
47. Reiter C, Weinshilboum R. Platelet phenol sulfotransferase activity: correlation with sulfate conjugation of acetaminophen. Clin Pharmacol Ther 1982; 32: 612-621.
48. Bonham-Carter SM, Rein G, Glover V, Sandler M, Caldwell J. Human platelet phenol sulphotransferase M and P: substrate specificities and correlation with in vivo sulphoconjugation of paracetamol and salicylamide. Br J Clin Pharmacol 1983; 15: 323-330.
49. van Loon JA, Weinshilboum RM. Human platelet phenol sulfotransferase: familial variation in thermal stability of the TS form. Biochem Genet 1984; 22: 997-1014.
50. Jones AL, Roberts RC, Coughtrie MWH. The human phenolsulfotransferase polymorphism is determined by the level of expression of the enzyme protein. Biochem J 1993; 296: 287-290.
51. Stanley EL, Hume R, Visser TJ, Coughtrie MWH. Differential expression of sulfotransferase enzymes involved in thyroid hormone metabolism during human placental development. J Clin Endocrinol Metab 2001; 86: 5944-5955.
52. Raftogianis RB, Wood TC, Otterness DM, van Loon JA, Weinshilboum RM. Phenol sulfotransferase pharmacogenetics in humans: association of common SULT1A1 alleles with TS PST phenotype. Biochem Biophys Res Commun 1997; 239: 298-304.
53. Raftogianis RB, Wood TC, Weinshilboum RM. Human phenol sulfotransferases SULT1A2 and SULT1A1. Genetic polymorphisms, allozyme properties, and human liver genotype-phenotype correlations. Biochem Pharmacol 1999; 58: 605-616.
54. Nowell S, Ambrosone CB, Ozawa S, MacLeod SL, Mrackova G, Williams S et al. Relationship of phenol sulfotransferase activity (SULT1A1) genotype to sulfotransferase phenotype in platelet cytosol. Pharmacogenetics 2000; 10: 789-797.
55. Ozawa S, Shimizu M, Katoh T, Miyajima A, Ohno Y, Matsumoto Y et al. Sulfating-activity and stability of cDNA-expressed allozymes of human phenol sulfotransferase, ST1A3*1 (213Arg) and ST1A3*2 (213His), both of which exist in Japanese as well as Caucasians. J Biochem 1999; 126: 271-277.
56. Li X, Clemens DL, Cole JR, Anderson RJ. Characterization of human liver thermostable phenol sulfotransferase (SULT1A1) allozymes with 3,3′,5′-triiodothyronine as the substrate. J Endocrinol 2001; 171: 525-532.
57. Raftogianis RB. Human sulfotransferases and cellular response to estrogens and antiestrogens. Drug Metab Rev 2001; 33: 10.
58. Petrotchenko EV, Pedersen LC, Borchers CH, Tomer KB, Negishi M. The dimerization motif of cytosolic sulfotransferases. FEBS Lett 2001; 490: 39-43.
59. Kester MHA, Kaptein E, Roest TJ, van Dijk CH, Tibboel D, Meinl W et al. Characterization of human iodothyronine sulfotransferases. J Clin Endocrinol Metab 1999; 84: 1357-1364.
60. Coughtrie MWH, Gilissen RAHJ, Shek B, Strange RC, Fryer AA, Jones PW et al. Phenol sulphotransferase SULT1A1 polymorphism: molecular diagnosis and allele frequencies in Caucasian and African populations. Biochem J 1999; 337: 45-49.
61. Frame LT, Gatlin TL, Kadlubar FF, Lang NP. Metabolic differences and their impact on human disease-Sulfotransferase and colorectal cancer. Environ Toxicol Pharmacol 1997; 4: 277-281.
62. Bamber DE, Fryer AA, Strange RC, Elder JB, Deakin M, Rajagopal R et al. Phenol sulphotransferase SULT1A1*1 genotype is associated with reduced risk of colorectal cancer. Pharmacogenetics 2001; 11: 679-685.
63. Seth P, Lunetta KL, Bell DW, Gray H, Nasser SM, Rhei E et al. Phenol sulfotransferases: hormonal regulation, polymorphism, and age of onset of breast cancer. Cancer Res 2000; 60: 6859-6863.
64. Zheng W, Xie DW, Cerhan JR, Sellers TA, Wen WQ, Folsom AR. Sulfotransferase 1A1 polymorphism, endogenous estrogen exposure, well-done meat intake, and breast cancer risk. Cancer Epidem Biomar 2001; 10: 89-94.
65. Chou HC, Lang NP, Kadlubar FF. Metabolic activation of the N-hydroxy derivative of the carcinogen 4-aminobiphenyl by human tissue sulfotransferases. Carcinogenesis 1995; 16: 413-417.
66. Steiner M, Bastian M, Schulz WA, Pulte T, Franke KH, Rohring A et al. Phenol sulphotransferase SULT1A1 polymorphism in prostate cancer: lack of association. Arch Toxicol 2000; 74: 222-225.
67. Kalow W, Bertilsson L. Interethnic factors affecting drug response. Advanc Drug Res 1994; 23: 1-53.
68. Nebert DW, Menon AG. Pharmacogenomics, ethnicity, and susceptibility genes. Pharmacogenomics J 2001; 1: 19-22.
69. Zhu X, Veronese ME, Iocco P, McManus ME. cDNA cloning and expression of a new form of human aryl sulfotransferase. Int J Biochem Cell Biol 1996; 28: 565-571.
70. Engelke CEH, Meinl W, Boeing H, Glatt H. Association between functional genetic polymorphisms of human sulfotransferases 1A1 and 1A2. Pharmacogenetics 2000; 10: 163-169.
71. Dooley TP, Haldeman-Cahill R, Joiner J, Wilborn TW. Expression profiling of human sulfotransferase and sulfatase gene superfamilies in epithelial tissues and cultured cells. Biochem Biophys Res Commun 2000; 277: 236-245.
72. Carlini EJ, Raftogianis RB, Wood TC, Jin F, Zheng W, Rebbeck TR et al. Sulfation pharmacogenetics: SULT1A1 and SULT1A2 allele frequencies in Caucasian, Chinese and African-American subjects. Pharmacogenetics 2001; 11: 57-68.
73. Iida A, Sekine A, Saito S, Kitamura Y, Kitamoto T, Osawa S et al. Catalog of 320 single nucleotide polymorphisms (SNPs) in 20 quinone oxidoreductase and sulfotransferase genes. J Hum Genet 2001; 46: 225-240.
74. Freimuth RR, Eckloff B, Wieben ED, Weinshilboum RM. Human sulfotransferase SULT1C1 pharmacogenetics: gene resequencing and functional genomic studies. Pharmacogenetics 2001; 11: 747-756.
75. Freimuth RR, Raftogianis RB, Wood TC, Moon E, Kim UJ, Xu J et al. Human sulfotransferases SULT1C1 and SULT1C2: cDNA characterization, gene cloning, and chromosomal localization. Genomics 2000; 65: 157-165.
76. Yoshinari K, Nagata K, Shimada M, Yamazoe Y. Molecular characterization of ST1C1-related human sulfotransferase. Carcinogenesis 1998; 19: 951-953.
77. Li XY, Clemens DL, Anderson RJ. Sulfation of iodothyronines by human sulfotransferase 1C1 (SULT1C1). Biochem Pharmacol 2000; 60: 1713-1716.
78. Song W-C, Qian YM, Li AP. Estrogen sulfotransferase expression in the human liver: marked interindividual variation and lack of gender specificity. J Pharmacol Exp Ther 1998; 284: 1197-1202.
79. Rotter JI, Wong FL, Lifrak ET, Parker LN. A genetic component to the variation of dehydroepiandrosterone sulfate. Metabolism 1985; 34: 731-736.
80. Aksoy IA, Sochorová V, Weinshilboum RM. Human liver dehydroepiandrosterone sulfotransferase-nature and extent of individual variation. Clin Pharmacol Ther 1993; 54: 498-506.
81. Wood TC, Her C, Aksoy I, Otterness DM, Weinshilboum RM. Human dehydroepiandrosterone sulfotransferase pharmacogenetics: quantitative western analysis and gene sequence polymorphisms. J Steroid Biochem Mol Biol 1996; 59: 467-478.
82. Nagata K, Yamazoe Y. Pharmacogenetics of sulfotransferase. Annu Rev Pharmacol Toxicol 2000; 40: 159-176.
83. Thomae BA, Eckloff BW, Freimuth RR, Wieben ED, Weinshilboum RM. Human sulfotransferase SULT2A1 pharmacogenetics: genotype-to-phenotype studies. Pharmacogenomics J 2002; 2: 48-56.
84. Ingelman-Sundberg M. Implications of polymorphic cytochrome P450-dependent drug metabolism for drug development. Drug Metab Dispos 2001; 29: 570-573.
85. Hodgson J. ADMET-turning chemicals into drugs. Nat Biotechnol 2001; 19: 722-726.
86. Funk C, Ponelle C, Scheuermann G, Pantze M. Cholestatic potential of troglitazone as a possible factor contributing to troglitazone-induced hepatotoxicity: In vivo and in vitro interaction at the canalicular bile salt export pump (Bsep) in the rat. Mol Pharmacol 2001; 59: 627-635.
87. Keppler D, Kamisako T, Leier I, Cui Y, Nies AT, Tsujii H et al. Localization, substrate specificity, and drug resistance conferred by conjugate export pumps of the MRP family. Adv Enzyme Regul 2000; 40: 339-349.
88. Suzuki H, Sugiyama Y. Transport of drugs across the hepatic sinusoidal membrane: sinusoidal drug influx and efflux in the liver. Semin Liver Dis 2000; 20: 251-263.
89. Kullak-Ublick GA, Stieger B, Hagenbuch B, Meier PJ. Hepatic transport of bile salts. Semin Liver Dis 2000; 20: 273-292.
90. Qian YM, Sun XJ, Tong MH, Li XP, Richa J, Song WC. Targeted disruption of the mouse estrogen sulfotransferase gene reveals a role of estrogen metabolism in intracrine and paracrine estrogen regulation. Endocrinology 2001; 142: 5342-5350.
91. Song W-C, Qian Y, Sun X, Negishi M. Cellular localization and regulation of expression of testicular estrogen sulfotransferase. Endocrinology 1997; 138: 5006-5012.
92. Borthwick EB, Burchell A, Coughtrie MWH. Differential expression of hepatic estrogen, phenol and dehydroepiandrosterone sulfotransferases in genetically-obese diabetic (ob/ob) male and female mice. J Endocrinol 1995; 144: 31-37.
93. Meloche CA, Falany CN. Expression of SULT2B1b in hormonally regulated human tissues. Drug Metab Rev 2001; 33: 230.
94. Geese WJ, Raftogianis RB. Biochemical characterization and tissue distribution of human SULT2B1. Biochem Biophys Res Commun 2001; 288: 280-289.
95. Javitt NB, Lee YC, Shimizu C, Fuda H, Strott CA. Cholesterol and hydroxycholesterol sulfotransferases: identification, distinction from dehydroepiandrosterone sulfotransferase, and differential tissue expression. Endocrinology 2001; 142: 2978-2984.
96. Ozawa S, Tang Y-M, Yamazoe Y, Kato R, Lang NP, Kadlubar FF. Genetic polymorphism in human liver phenol sulfotransferases involved in the bioactivation of N-hydroxy derivatives of carcinogenic arylamines and heterocyclic amines. Chem Biol Interact 1998; 109: 237-248. x