In silico prediction of human sulfotransferase 1E1 activity guided by pharmacophores from molecular dynamics simulations

Journal of Biological Chemistry

Volumn 291, Issue 1, 2016, Pages 58-71

  Rakers, Christin ^a   Schumacher, Fabian ^d,e   Meinl, Walter ^b,c   Glatt, Hansruedi ^c   Kleuser, Burkhard ^d   Wolber, Gerhard ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b Departments of Molecular Toxicology   (Germany)

^c GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^d UNIVERSITY OF POTSDAM   (Germany)

^e UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTIFICIAL INTELLIGENCE; DETOXIFICATION; FORECASTING; HEALTH RISKS; LEARNING SYSTEMS; LIGANDS; METABOLITES; PHARMACODYNAMICS; PHYSIOLOGY; RISK ASSESSMENT;

BIOCHEMICAL ASSAY; ENDOMETRIAL CANCER; GENOTOXIC EFFECTS; MACHINE LEARNING TECHNIQUES; MOLECULAR DYNAMICS SIMULATIONS; PHYSIOLOGICAL PROCESS; PROTEIN CONFORMATION; REACTIVE METABOLITES;

MOLECULAR DYNAMICS;

SULFOTRANSFERASE; SULFOTRANSFERASE 1E1; UNCLASSIFIED DRUG; ENZYME INHIBITOR; ESTRONE SULFOTRANSFERASE; LIGAND;

ARTICLE; BACTERIAL STRAIN; CLASSIFICATION; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ASSAY; ENZYME METABOLISM; ENZYME STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LIGAND BINDING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOLECULAR DOCKING; MOLECULAR DYNAMICS; NONHUMAN; PHARMACOPHORE; PREDICTION; PRIORITY JOURNAL; PROTEIN CONFORMATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SCREENING; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DOSE RESPONSE; ENZYME SPECIFICITY; IC50; MACHINE LEARNING; PRECLINICAL STUDY; PROTEIN DATABASE; REPRODUCIBILITY; STRUCTURAL HOMOLOGY; SUPPORT VECTOR MACHINE; TANDEM MASS SPECTROMETRY; X RAY CRYSTALLOGRAPHY;

CHROMATOGRAPHY, LIQUID; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; HUMANS; INHIBITORY CONCENTRATION 50; LIGANDS; MACHINE LEARNING; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; REPRODUCIBILITY OF RESULTS; STRUCTURAL HOMOLOGY, PROTEIN; SUBSTRATE SPECIFICITY; SULFOTRANSFERASES; SUPPORT VECTOR MACHINE; TANDEM MASS SPECTROMETRY;

EID: 84952915659     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.685610     Document Type: Article

References (72)

1. Guengerich, F. P. (2008) Cytochrome P450 and chemical toxicology. Chem. Res. Toxicol. 21, 70-83
2. Kirchmair, J., Williamson, M. J., Tyzack, J. D., Tan, L., Bond, P. J., Bender, A., and Glen, R. C. (2012) Computational prediction of metabolism: sites, products, SAR, P450 enzyme dynamics, and mechanisms. J. Chem. Inf. Model. 52, 617-648
3. Kirchmair, J., Göller, A. H., Lang, D., Kunze, J., Testa, B., Wilson, I. D., Glen, R. C., and Schneider, G. (2015) Predicting drug metabolism: experiment and/or computation? Nat. Rev. Drug Discov. 14, 387-404
4. Testa, B., Pedretti, A., and Vistoli, G. (2012) Reactions and enzymes in the metabolism of drugs and other xenobiotics. Drug Discov. Today 17, 549-560
5. Moroy, G., Martiny, V. Y., Vayer, P., Villoutreix, B. O., and Miteva, M. A. (2012) Toward in silico structure-based ADMET prediction in drug discovery. Drug Discov. Today 17, 44-55
6. Allali-Hassani, A., Pan, P. W., Dombrovski, L., Najmanovich, R., Tempel, W., Dong, A., Loppnau, P., Martin, F., Thornton, J., Thonton, J., Edwards, A. M., Bochkarev, A., Plotnikov, A. N., Vedadi, M., and Arrowsmith, C. H. (2007) Structural and chemical profiling of the human cytosolic sulfotransferases. PLos Biol. 5, e97
7. Zhang, H., Varlamova, O., Vargas, F. M., Falany, C. N., Leyh, T. S., and Varmalova, O. (1998) Sulfuryl transfer: the catalytic mechanism of human estrogen sulfotransferase. J. Biol. Chem. 273, 10888-10892
8. Kauffman, F. C. (2004) Sulfonation in pharmacology and toxicology. Drug Metab. Rev. 36, 823-843
9. Jancova, P., Anzenbacher, P., and Anzenbacherova, E. (2010) Phase II drug metabolizing enzymes. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech. Repub. 154, 103-116
10. Glatt, H. (2000) Sulfotransferases in the bioactivation of xenobiotics. Chem. Biol. Interact. 129, 141-170
11. Reinen, J., and Vermeulen, N. P. (2015) Biotransformation of endocrine disrupting compounds by selected phase I and phase II enzymes: formation of estrogenic and chemically reactive metabolites by cytochromes P450 and sulfotransferases. Curr. Med. Chem. 22, 500-527
12. Bamforth, K. J., Dalgliesh, K., and Coughtrie, M. W. (1992) Inhibition of human liver steroid sulfotransferase activities by drugs: a novel mechanism of drug toxicity? Eur. J. Pharmacol. 228, 15-21
13. Vietri, M., De Santi, C., Pietrabissa, A., Mosca, F., and Pacifici, G. M. (2000) Inhibition of human liver phenol sulfotransferase by nonsteroidal antiinflammatory drugs. Eur. J. Clin. Pharmacol. 56, 81-87
14. Gibb, C., Glover, V., and Sandler, M. (1987) In vitro inhibition of phenolsulphotransferase by food and drink constituents. Biochem. Pharmacol. 36, 2325-2330
15. Bamforth, K. J., Jones, A. L., Roberts, R. C., and Coughtrie, M. W. (1993) Common food additives are potent inhibitors of human liver 17α-ethinyloestradiol and dopamine sulphotransferases. Biochem. Pharmacol. 46, 1713-1720
16. Coughtrie, M. W., and Johnston, L. E. (2001) Interactions between dietary chemicals and human sulfotransferases: molecular mechanisms and clinical significance. Drug Metab. Dispos. 29, 522-528
17. Kester, M. H., Bulduk, S., Tibboel, D., Meinl, W., Glatt, H., Falany, C. N., Coughtrie, M. W., Bergman, A., Safe, S. H., Kuiper, G. G., Schuur, A. G., Brouwer, A., and Visser, T. J. (2000) Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology 141, 1897-1900
18. Ohkimoto, K., Sakakibara, Y., Suiko, M., Yoshikawa, H., Liu, M.-C., and Tamura, H. (2005) Biocides, tributyltin and triphenyltin, as possible inhibitors of the human sulfotransferase involved in the estrogen homeostasis. Pestic. Biochem. Physiol. 81, 32-38
19. Steventon, G. B., Heafield, M. T., Waring, R. H., and Williams, A. C. (1989) Xenobiotic metabolism in Parkinson's disease. Neurology 39, 883-887
20. Falany, J. L., and Falany, C. N. (1996) Expression of cytosolic sulfotransferases in normal mammary epithelial cells and breast cancer cell lines. Cancer Res. 56, 1551-1555
21. Li, L., and Falany, C. N. (2007) Elevated hepatic SULT1E1 activity in mouse models of cystic fibrosis alters the regulation of estrogen responsive proteins. J. Cyst. Fibros. 6, 23-30
22. Pasqualini, J. R. (2009) Breast cancer and steroid metabolizing enzymes: the role of progestogens. Maturitas 65, S17-21
23. Rižner, T. L. (2013) Estrogen biosynthesis, phase I and phase II metabolism, and action in endometrial cancer. Mol. Cell. Endocrinol. 381, 124-139
24. Pasqualini, J. R. (2009) Estrogen sulfotransferases in breast and endometrial cancers. Ann. N.Y. Acad. Sci. 1155, 88-98
25. Lin, E. S., Yang, Y. S., and Yang, J. M. (2003) Modeling the binding and inhibition mechanism of nucleotides and sulfotransferase using molecular docking. J. Chin. Chem. Soc. 50, 655-663
26. Iyer, L. V., Ramamoorthy, A., Rutkowska, E., Furimsky, A. M., Tang, L., Catz, P., Green, C. E., Jozwiak, K., and Wainer, I. W. (2012) The stereoselective sulfate conjugation of 4'-methoxyfenoterol stereoisomers by sulfotransferase enzymes. Chirality 24, 796-803
27. Lin, P., Yang, W., Pedersen, L. C., Negishi, M., and Pedersen, L. G. (2006) Searching for the minimum energy path in the sulfuryl transfer reaction catalyzed by human estrogen sulfotransferase: role of enzyme dynamics. Int. J. Quantum Chem. 106, 2981-2998
28. Martiny, V. Y., Carbonell, P., Lagorce, D., Villoutreix, B. O., Moroy, G., and Miteva, M. A. (2013) In silico mechanistic profiling to probe small molecule binding to sulfotransferases. PLoS ONE 8, e73587
29. Pedersen, L. C., Petrotchenko, E., Shevtsov, S., and Negishi, M. (2002) Crystal structure of the human estrogen sulfotransferase-PAPS complex: evidence for catalytic role of Ser137 in the sulfuryl transfer reaction. J. Biol. Chem. 277, 17928-17932
30. Bowers, K. J., Chow, E., Xu, H., Dror, R. O., Eastwood, M. P., Gregersen, B., Klepeis, J. L., Kolossvary, I., Moraes, M., and Sacerdoti, F. D. (2006) Scalable algorithms for molecular dynamics simulations on commodity clusters. in SC 2006 Conference, Proceedings of the ACM/IEEE, Tampa, Florida, Nov. 11-17, 2006, IEEE, Piscataway, New Jersey
31. Jorgensen, W. L., Maxwell, D. S., and Tirado-Rives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236
32. Li, H., Robertson, A. D., and Jensen, J. H. (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins Struct. Funct. Bioinf. 61, 704-721
33. Berendsen, H. J., van der Spoel, D., and van Drunen, R. (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91, 43-56
34. Schomburg, I., Chang, A., and Schomburg, D. (2002) BRENDA, enzyme data and metabolic information. Nucleic Acids Res. 30, 47-49
35. Sadowski, J., Gasteiger, J., and Klebe, G. (1994) Comparison of automatic three-dimensional model builders using 639 X-ray structures. J. Chem. Inf. Comput. Sci. 34, 1000-1008
36. Halgren, T. A. (1996) Merck molecular force field: I. basis, form, scope, parameterization, and performance of MMFF94. J. Comput. Chem. 17, 490-519
37. Reed, M. C., Lieb, A., and Nijhout, H. F. (2010) The biological significance of substrate inhibition: a mechanism with diverse functions. Bioessays 32, 422-429
38. Wu, B. (2011) Substrate inhibition kinetics in drug metabolism reactions. Drug Metab. Rev. 43, 440-456
39. Irwin, J. J., and Shoichet, B. K. (2005) ZINC-a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 45, 177-182
40. Berthold, M. R., Cebron, N., Dill, F., Gabriel, T. R., Kötter, T., Meinl, T., Ohl, P., Sieb, C., Thiel, K., and Wiswedel, B. (2008) KNIME: The Konstanz information miner. in Data analysis, machine learning and applications, pp. 319-326, Springer, New York
41. Mysinger, M. M., Carchia, M., Irwin, J. J., and Shoichet, B. K. (2012) Directory of useful decoys, enhanced (DUD-E): better ligands and decoys for better benchmarking. J. Med. Chem. 55, 6582-6594
42. Jones, G., Willett, P., Glen, R. C., Leach, A. R., and Taylor, R. (1997) Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748
43. Korb, O., Stützle, T., and Exner, T. E. (2009) Empirical scoring functions for advanced protein-ligand docking with PLANTS. J. Chem. Inf. Model. 49, 84-96
44. Shevtsov, S., Petrotchenko, E. V., Pedersen, L. C., and Negishi, M. (2003) Crystallographic analysis of a hydroxylated polychlorinated biphenyl (OH-PCB) bound to the catalytic estrogen binding site of human estrogen sulfotransferase. Environ. Health Perspect. 111, 884-888
45. Wolber, G., and Langer, T. (2005) LigandScout: 3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. J. Chem. Inf. Model. 45, 160-169
46. Wolber, G., Dornhofer, A. A., and Langer, T. (2006) Efficient overlay of small organic molecules using 3D pharmacophores. J. Comput. Aided Mol. Des. 20, 773-788
47. Wolber, G., Seidel, T., Bendix, F., and Langer, T. (2008) Molecule-pharmacophore superpositioning and pattern matching in computational drug design. Drug Discov. Today 13, 23-29
48. Knox, C., Law, V., Jewison, T., Liu, P., Ly, S., Frolkis, A., Pon, A., Banco, K., Mak, C., Neveu, V., Djoumbou, Y., Eisner, R., Guo, A. C., and Wishart, D. S. (2011) DrugBank 3.0: a comprehensive resource for "omics" research on drugs. Nucleic Acids Res. 39, D1035-1041
49. Witten, I. H., and Frank, E. (2005) Data Mining: Practical Machine Learning Tools and Techniques, pp. 65-69 and 214, Morgan Kaufmann Publishers, Burlington, Massachusetts
50. Hagen, M., Pabel, U., Landsiedel, R., Bartsch, I., Falany, C. N., and Glatt, H. (1998) Expression of human estrogen sulfotransferase in Salmonella typhimurium: differences between hHST and hEST in the enantioselective activation of 1-hydroxyethylpyrene to a mutagen. Chem. Biol. Interact. 109, 249-253
51. Meinl, W., Meerman, J. H., and Glatt, H. (2002) Differential activation of promutagens by alloenzymes of human sulfotransferase 1A2 expressed in Salmonella typhimurium. Pharmacogenetics 12, 677-689
52. Meinl, W., Pabel, U., Osterloh-Quiroz, M., Hengstler, J. G., and Glatt, H. (2006) Human sulphotransferases are involved in the activation of aristolochic acids and are expressed in renal target tissue. Int. J. Cancer 118, 1090-1097
53. Reinen, J., Vriese, E., Glatt, H., and Vermeulen, N. P. (2006) Development and validation of a fluorescence HPLC-based screening assay for inhibition of human estrogen sulfotransferase. Anal. Biochem. 357, 85-92
54. Engst, W., Pabel, U., and Glatt, H. (2002) Conjugation of 4-nitrophenol and 4-hydroxylonazolac in V79-derived cells expressing individual forms of human sulphotransferases. Environ. Toxicol. Pharmacol. 11, 243-250
55. Tibbs, Z. E., Rohn-Glowacki, K. J., Crittenden, F., Guidry, A. L., and Falany, C. N. (2015) Structural plasticity in the human cytosolic sulfotransferase dimer and its role in substrate selectivity and catalysis. Drug Metab. Pharmacokinet. 30, 3-20
56. Cook, I., Wang, T., Almo, S. C., Kim, J., Falany, C. N., and Leyh, T. S. (2013) The gate that governs sulfotransferase selectivity. Biochemistry 52, 415-424
57. Cook, I., Wang, T., Almo, S. C., Kim, J., Falany, C. N., and Leyh, T. S. (2013) Testing the sulfotransferase molecular pore hypothesis. J. Biol. Chem. 288, 8619-8626
58. Wang, T., Cook, I., and Leyh, T. S. (2014) 3'-Phosphoadenosine 5'-phosphosulfate allosterically regulates sulfotransferase turnover. Biochemistry 53, 6893-6900
59. Mortier, J., Rakers, C., Bermudez, M., Murgueitio, M. S., Riniker, S., and Wolber, G. (2015) The impact of molecular dynamics on drug design: applications for the characterization of ligand-macromolecule complexes. Drug Discov. Today. 20, 686-702
60. Gosavi, R. A., Knudsen, G. A., Birnbaum, L. S., and Pedersen, L. C. (2013) Mimicking of estradiol binding by flame retardants and their metabolites: a crystallographic analysis. Environ. Health Perspect. 121, 1194-1199
61. Warren, G. L., Andrews, C. W., Capelli, A.-M., Clarke, B., LaLonde, J., Lambert, M. H., Lindvall, M., Nevins, N., Semus, S. F., Senger, S., Tedesco, G., Wall, I. D., Woolven, J. M., Peishoff, C. E., and Head, M. S. (2006) A critical assessment of docking programs and scoring functions. J. Med. Chem. 49, 5912-5931
62. Blomhoff, R., and Blomhoff, H. K. (2006) Overview of retinoid metabolism and function. J. Neurobiol. 66, 606-630
63. Cook, I., Wang, T., Falany, C. N., and Leyh, T. S. (2013) High accuracy in silico sulfotransferase models. J. Biol. Chem. 288, 34494-34501
64. Cook, I. T., Leyh, T. S., Kadlubar, S. A., and Falany, C. N. (2010) Structural rearrangement of SULT2A1: effects on dehydroepiandrosterone and raloxifene sulfation. Horm. Mol. Biol. Clin. Investig. 1, 81-87
65. Feixas, F., Lindert, S., Sinko, W., and McCammon, J. A. (2014) Exploring the role of receptor flexibility in structure-based drug discovery. Biophys. Chem. 186, 31-45
66. Najmanovich, R. J., Allali-Hassani, A., Morris, R. J., Dombrovsky, L., Pan, P. W., Vedadi, M., Plotnikov, A. N., Edwards, A., Arrowsmith, C., and Thornton, J. M. (2007) Analysis of binding site similarity, small-molecule similarity and experimental binding profiles in the human cytosolic sulfotransferase family. Bioinformatics 23, e104-109
67. Meng, S., Wu, B., Singh, R., Yin, T., Morrow, J. K., Zhang, S., and Hu, M. (2012) SULT1A3-mediated regiospecific 7-O-sulfation of flavonoids in Caco-2 cells can be explained by the relevant molecular docking studies. Mol. Pharm. 9, 862-873
68. Butt, C. M., and Stapleton, H. M. (2013) Inhibition of thyroid hormone sulfotransferase activity by brominated flame retardants and halogenated phenolics. Chem. Res. Toxicol. 26, 1692-1702
69. Tian, X., Huo, X., Dong, P., Wu, B., Wang, X., Wang, C., Liu, K., and Ma, X. (2015) Sulfation of melatonin: enzymatic characterization, differences of organs, species and genders, and bioactivity variation. Biochem. Pharmacol. 94, 282-296
70. Kim, H. J., Cho, J. H., and Klaassen, C. D. (1995) Depletion of hepatic 3'-Phosphoadenosine 5'-phosphosulfate (PAPS) and sulfate in rats by xenobiotics that are sulfated. J. Pharmacol. Exp. Ther. 275, 654-658
71. Klaassen, C. D., and Boles, J. W. (1997) Sulfation and sulfotransferases 5: the importance of 3'-Phosphoadenosine 5'-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J. 11, 404-418
72. Wang, T., Cook, I., Falany, C. N., and Leyh, T. S. (2014) Paradigms of sulfotransferase catalysis: the mechanism of SULT2A1. J. Biol. Chem. 289, 26474-26480