Zebrafish as a model for the study of the phase II cytosolic sulfotransferases

Current Drug Metabolism

Volumn 11, Issue 6, 2010, Pages 538-546

  Liu, Tzu An ^a   Bhuiyan, Shakhawat ^b   Liu, Ming Yih ^c   Sugahara, Takuya ^a   Sakakibara, Yoichi ^d   Suiko, Masahito ^d   Yasuda, Shin ^a   Kakuta, Yoshimitsu ^e   Kimura, Makoto ^e   Williams, Frederick E ^a   Liu, Ming Cheh ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b Charles A Meyer Science and Mathematics Center   (United States)

^c NATIONAL SYNCHROTRON RADIATION RESEARCH CENTER   (Taiwan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e KYUSHU UNIVERSITY   (Japan)

Author keywords

Cytosolic sulfotransferase; Danio Rerio; Drug metabolism; Phase II enzyme; Sulfation; SULT; Zebrafish

Indexed keywords

CYTOSOLIC SULFOTRANSFERASE; SULFOTRANSFERASE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

CLONE; CYTOSOL; DRUG METABOLISM; EMBRYO DEVELOPMENT; ENZYME PURIFICATION; ENZYME SUBSTRATE; HUMAN; INFORMATION; LARVA; MATURATION; MOLECULAR CLONING; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; REVIEW; SULFATION; VERTEBRATE; XENOBIOTIC METABOLISM;

AMINO ACID SEQUENCE; ANIMALS; CYTOSOL; HUMANS; MODELS, ANIMAL; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; SULFOTRANSFERASES; ZEBRAFISH;

EID: 77954172988     PISSN: 13892002     EISSN: None     Source Type: Journal    
DOI: 10.2174/138920010791636158     Document Type: Review

References (76)

1. Baumann, E. Ueber sulfosauren im harn. Ber. Dtch. Chem. Ges., 1876, 54-58.
2. Nelson, S.D.; Gordon, W.P. Mammalian drug metabolism. J. Nat. Prod., 1983, 46, 71-78.
3. Chen, X.; Zhong, D.; Blume, H. Stereoselective pharmacokinetics of propafenone and its major metabolites in healthy Chinese volunteers. Eur. J. Pharm. Sci., 2000, 10, 11-16.
4. Mulder, G.J.; Jakoby, W.B. Sulfation. In: Conjugation Reactions in Drug Metabolism; Mulder, G.J., Jakoby, W., Eds.; Taylor and Francis: London, 1990; pp. 107-161.
5. Falany, C.N. Enzymology of human cytosolic sulfotransferases. FASEB J., 1997, 11, 206-216.
6. Weinshilboum, R.; Otterness, D. Sulfotransferase enzymes. In: Conjugation-Deconjugation Reactions in Drug Metabolism and Toxicity, Kaufmann, F.C., Ed.; Springer-Verlag: Berlin, 1994; pp. 45-78.
7. Duffel, M.W. Sulfotransferases. In. Comprehensive Toxicology, Guengerich, F.P., Ed.; Elsevier Science: Oxford, 1997; pp. 365-383.
8. Lipmann, F. Biological sulfate activation and transfer. Science, 1958, 128, 575-580.
9. Coughtrie, M.W.H.; Sharp, S.; Maxwell, K.; Innes, N.P. Biology and function of the reversible sulfation pathway catalysed by human sulfotransferases and sulfatases. Chem. Biol. Interact., 1998, 109, 3-27.
10. Beis, D.; Stainier, D.Y. In vivo cell biology: following the zebrafish trend. Trends Cell Biol., 2006, 16, 105-112.
11. Aleström, P.; Holter, J.L.; Nourizadeh-Lillabadi, R. Zebrafish in functional genomics and aquatic biomedicine. Trends Biotechnol., 2006, 24, 15-21.
12. Ingham PW. The power of the zebrafish for disease analysis. Hum. Mol. Genet., 2009, 18, R107-112.
13. Wixon, J. Featured organism: Danio rerio, the zebrafish. Yeast, 2000, 17, 225-231.
14. Postlethwait, J.H.; Woods, I.G.; Ngo-Hazelett, P.; Yan, Y.L.; Kelly, P.D.; Chu, F.; Huang, H.; Hill-Force, A.; Talbot, W.S. Zebrafish comparative genomics and the origins of vertebrate chromosomes. Genome Res., 2000, 10, 1890-1902.
15. Fekete, D.M. Developmental biology. Rocks that roll zebrafish. Science, 2003, 302, 241-242.
16. Key, B.; Devine, C.A. Zebrafish as an experimental model: strategies for developmental and molecular neurobiology studies. Method Cell Sci., 2003, 25, 1-6.
17. Barros, T.P.; Alderton, W.K.; Reynolds, H.M.; Roach, A.G.; Berghmans, S. Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br. J. Pharmacol., 2008, 154, 1400-1413.
18. Flinn, L.; Mortiboys, H.; Volkmann, K.; Köster, R.W.; Ingham, P.W.; Bandmann, O. Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio). Brain, 2009, 132, 1613-1623.
19. Phillips, W.; Michell, A.; Pruess, H.; Barker, R.A. Animal models of neurodegenerative diseases. Methods Mol. Biol., 2009, 549, 137-155.
20. Chico, T.J.; Ingham, P.W.; Crossman, D.C. Modeling cardiovascular disease in the zebrafish. Trends Cardiovasc. Med., 2008, 18, 150-155.
21. Milan, D.J.; Macrae, C.A. Zebrafish genetic models for arrhythmia. Prog. Biophys. Mol. Biol., 2008, 98, 301-308.
22. Martin, J.S.; Renshaw, S.A. Using in vivo zebrafish models to understand the biochemical basis of neutrophilic respiratory disease. Biochem. Soc. Trans., 2009, 37, 830-837.
23. Phelps, H.A.; Neely, M.N. Evolution of the zebrafish model: from development to immunity and infectious disease. Zebrafish, 2005, 2, 87-103.
24. Payne, E.; Look, T. Zebrafish modelling of leukaemias. Br. J. Haematol., 2009, 146, 247-256.
25. Feitsma, H.; Cuppen, E. Zebrafish as a cancer model. Mol. Cancer Res., 2008, 6, 685-694.
26. Berghmans, S.; Jette, C.; Langenau, D.; Hsu, K.; Stewart, R.; Look, T.; Kanki, J.P. Making waves in cancer research: new models in the zebrafish. Biotechniques, 2005, 39, 227-237.
27. Zebrafish Genome Resources, Available from: http://www.ncbi.nlm.nih.gov/ genome/guide/zebrafish/
28. Langheinrich, U. Zebrafish: a new model on the pharmaceutical catwalk. Bioessays, 2003, 25, 904-12.
29. Rubinstein, A.L. Zebrafish assays for drug toxicity screening. Expert. Drug Metab. Toxicol., 2006, 2, 231-240.
30. Kari, G.; Rodeck, U.; Dicker, A.P. Zebrafish: an emerging model system for human disease and drug discovery. Clin. Pharmacol. Ther., 2007, 82, 70-80.
31. Barros, T.P.; Alderton, W.K.; Reynolds, H.M.; Roach, A.G.; Berghmans, S. Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br. J. Pharmacol., 2008, 154, 1400-1413.
32. Rocke, J.; Lees, J.; Packham, I.; Chico T. The zebrafish as a novel tool for cardiovascular drug discovery. Recent Pat. Cardiovasc. Drug Discov., 2009, 4, 1-5.
33. Langheinrich, U.; Vacun, G.; Wagner, T. Zebrafish embryos express an orthologue of HERG and are sensitive toward a range of QT-prolonging drugs inducing severe arrhythmia, Toxicol. Appl. Pharmacol. 2003, 193, 370-382.
34. Milan, D.J.; Peterson, T.A.; Ruskin, J.N.; Peterson, R.T.; MacRae, C.A. Drugs that induce repolarization abnormalities cause bradycardia in zebrafish, Circulation, 2003, 107, 1355-1358.
35. Sugahara, T.; Liu, C.C.; Pai, T.G.; Collodi, P.; Suiko, M.; Sakakibara, Y.; Nishiyama, K.; Liu, M.C. Sulfation of hydroxychlorobiphenyls. Molecular cloning, expression, and functional characterization of zebrafish SULT1 sulfotransferases. Eur. J. Biochem., 2003, 270, 2404-2411.
36. Sugahara, T.; Liu, C.C.; Carter, G.; Pai, T.G.; Liu, M.C. cDNA cloning, expression, and functional characterization of a zebrafish SULT1 cytosolic sulfotransferase. Arch. Biochem. Biophys., 2003, 414, 67-73.
37. Liu, M.Y.; Yang, Y.S.; Sugahara, T.; Yasuda, S.; Liu, M.C. Identification of a novel zebrafish SULT1 cytosolic sulfotransferase: cloning, expression, characterization, and developmental expression study. Arch. Biochem. Biophy., 2005, 437, 10-19.
38. Yasuda, S.; Kumar, A.P.; Liu, M.Y.; Sakakibara, Y.; Suiko, M.; Chen, L.; Liu, M.C. Identification of a novel thyroid hormone-sulfating cytosolic sulfotransferase, SULT1 ST5, from zebrafish. FEBS J., 2005, 272, 3828-3837.
39. Yasuda, S.; Liu, C.C.; Takahashi, S.; Suiko, M.; Chen, L.; Snow, R.; Liu, M.C. Identification of a novel estrogen-sulfating cytosolic SULT from zebrafish: molecular cloning, expression, characterization, and ontogeny study. Biochem. Biophys. Res. Commun., 2005, 330, 219-225.
40. Liu, T.A.; Bhuiyan, S.; Snow, R.; Yasuda, S.; Yasuda, T.; Yang, Y.S.; Williams, F.E.; Liu, M.Y.; Suiko, M.; Carter, G.; Liu, M.C. Identification and characterization of two novel cytosolic sulfotransferases, SULT1 ST7 and SULT1 ST8, from zebrafish. Aquat. Toxicol., 2008, 89, 94-102.
41. Sugahara, T.; Yang, Y.S.; Liu, C.C.; Pai, T.G.; Liu, M.C. Sulphonation of dehydroepiandrosterone and neurosteroids: molecular cloning, expression, and functional characterization of a novel zebrafish SULT2 cytosolic sulfotransferase. Biochem. J., 2003, 375, 785-791.
42. Yasuda, S.; Liu, M.Y.; Yang, Y.S.; Snow, R.; Takahashi, S.; Liu, M.C. Identification of novel hydroxysteroid-sulfating cytosolic SULTs, SULT2 ST2 and SULT2 ST3, from zebrafish: cloning, expression, characterization, and developmental expression. Arch. Biochem. Biophys., 2006, 455, 1-9.
43. Yasuda, T.; Yasuda, S.; Williams, F.E.; Liu, M.Y.; Sakakibara, Y.; Bhuiyan, S.; Snow, R.; Carter, G.; Liu, M.C. Characterization and ontogenic study of novel steroid-sulfating SULT3 sulfotransferases from zebrafish. Mol. Cell. Endocrinol., 2008, 294, 29-36.
44. Yasuda, S.; Burgess, M.; Yasuda, T.; Liu, M.Y.; Bhuiyan, S.; Williams, F.E.; Kurogi, K.; Sakakibara, Y.; Suiko, M.; Liu, M.C. A novel hydroxysteroid-sulfating cytosolic sulfotransferase, SULT3 ST3, from zebrafish: identification, characterization, and ontogenic study. Drug Metab.Lett., 2009, 3, 217-227.
45. Sugahara, T.; Liu, C.C.; Pai, T.G.; Liu, M.C. Molecular cloning, expression, and functional characterization of a novel zebrafish cytosolic sulfotransferase. Biochem. Biophys. Res. Commun., 2003, 300, 725-730.
46. Yamazoe, Y.; Nagata, K.; Ozawa, S.; Kato, R. Structural similarity and diversity of sulfotransferases. Chem. Biol. Interact., 1994, 92, 107-117.
47. Weinshilboum, R.M.; Otterness, D.M.; Aksoy, I.A.; Wood, T.C.; Her, C.; Raftogianis, R.B. Sulfation and sulfotransferases 1: Sulfotransferase molecular biology: cDNAs and genes. FASEB J., 1997, 11, 3-14.
48. Wilborn, T.W.; Comer, K.A.; Dooley, T.P.; Reardon, I.M.; Heinrikson, R.L.; Falany, C.N. Sequence analysis and expression of the cDNA for the phenol-sulfating form of human liver phenol sulfotransferase. Mol. Pharmacol., 1994, 43, 70-77.
49. Veronese, M. E.; Burgess, W.; Zhu, X.; McManus, M.E. Functional characterization of two human sulphotransferase cDNAs that encode monoamine- and phenol-sulphating forms of phenol sulphotransferase: substrate kinetics, thermal-stability and inhibitor-sensitivity studies. Biochem. J., 1994, 302, 497-502.
50. Wood, T.C.; Aksoy, I.A.; Aksoy, S.; Weinshilboum, R.M. Human liver thermolabile phenol sulfotransferase: cDNA cloning, expression and characterization. Biochem. Biophys. Res. Commun., 1994, 198, 1119-1127. (Pubitemid 24172813)
51. Wang, J.; Falany, J.L.; Falany, C.N. Expression and characterization of a novel thyroid hormone-sulfating form of cytosolic sulfotransferase from human liver. Mol. Pharmacol., 1999, 53, 274-282.
52. Sakakibara, Y.; Yanagisawa, K.; Katafuchi, J.; Ringer, D.P.; Takami, Y.; Nakayama, T.; Suiko, M.; Liu, M.C. Molecular cloning, expression, and characterization of novel human SULT1C sulfotransferases that catalyze the sulfonation of N-hydroxy-2-acetylaminofluorene. J. Biol. Chem., 1998, 273, 33929-33935. (Pubitemid 129758348)
53. Her C.; Kaur, G.P.; Athwal, R.S.; Weinshilboum, R.M. Human sulfotransferase SULT1C1: cDNA cloning, tissue-specific expression, and chromosomal localization. Genomics, 1997, 41, 467-470.
54. Aksoy, I.A.; Wood, T.C.; Weinshilboum, R. Human liver estrogen sulfotransferase: identification by cDNA cloning and expression. Biochem. Biophys. Res. Commun., 1994, 200, 1621-1629. (Pubitemid 24181838)
55. Falany, C.N.; Vazquez, M.E.; Kalb, J.M. Purification and characterization of human liver dehydroepiandrosterone sulphotransferase. Biochem. J., 1989, 260, 641-646.
56. Otterness, D.M.; Wieben, E.D.; Wood, T.C.; Watson, W.G.; Madden, B.J.; McCormick, D.J.; Weinshilboum, R.M. Human liver dehydroepiandrosterone sulfotransferase: molecular cloning and expression of cDNA. Mol. Pharmacol., 1992, 41, 865-872. (Pubitemid 23023329)
57. Her, C.; Wood, T.C.; Eichler, E.E.; Mohrenweiser, H.W.; Ramagli, L.S.; Siciliano, M.J.; Weinshilboum, R.M. Human hydroxysteroid sulfotransferase SULT2B1: two enzymes encoded by a single chromosome 19 gene. Genomics, 1998, 53, 284-295.
58. Fuda, H.; Lee, Y.C.;Shimizu, C.; Javitt, N.B.; Strott, C.A. Mutational analysis of human hydroxysteroid sulfotransferase SULT2B1 isoforms reveals that exon 1B of the SULT2B1 gene produces cholesterol sulfotransferase, whereas exon 1A yields pregnenolone sulfotransferase. J. Biol. Chem., 2002, 277, 36161-36166.
59. Falany, C.N.; Xie, X.; Wang, J.; Ferrer, J.;Falany, J.L. Molecular cloning and expression of novel sulphotransferase-like cDNAs from human and rat brain. Biochem. J., 2000, 346, 857-864.
60. Sakakibara, Y.; Suiko, M.; Pai, T.G.; Nakayama, T.; Takami, Y.; Katafuchi, J.; Liu, M.C. Highly conserved mouse and human brain sulfotransferases: molecular cloning, expression, and functional characterization. Gene, 2002, 285, 39-47.
61. GenBank Accession # BC140797.
62. GenBank Accession # BI533409.
63. Negishi, M.; Pedersen, L.G.; Petrotchenko, E.; Shevtsov, S.; Gorokhov, A.; Kakuta, Y.; Pedersen, L.C.; Structure and Function of Sulfotransferases. Arch. Biochem. Biophys., 2001, 390, 149-157.
64. Kurogi, K.; Dillon, J.; Nasser, A.; Liu, M.Y.; Williams, F.E.; Sakakibara, Y.; Suiko, M.; Liu, M.C. Sulfation of Drug Compounds by the Zebrafish Cytosolic Sulfotransferases (SULTs). Drug Metab. Lett., 2010, 4, 62-68.
65. Brown, D.D. The role of thyroid hormone in zebrafish and axolotl development. Proc. Natl. Acad. Sci., 1997, 94, 13011-13016.
66. Sawyer, S.J.; Gerstner, K.A.; Callard, G.V. Real-time PCR analysis of cytochrome P450 aromatase expression in zebrafish: gene specific tissue distribution, sex differences, developmental programming, and estrogen regulation. Gen. Comp. Endocrinol., 2006, 147, 108-117.
67. Condeça, J.A.B.; Canario, A.V.M. In: Steroidogenesis during estrogen-induced sex inversion in the seabream, Sparus aurata. Goetz, F.W., Thomas P., Eds.; Proceeding of the Fifth International Symposium on the Reproductive Physiology of Fish, Austin, Texas, 1995; pp. 306.
68. Chang, C.F.; Lin, B.Y. Estradiol-17β stimulates aromatase activity and reversible sex change in protandrous black porgy, Acanthopagrus schlegeli. J. Exp. Zool., 1998, 280, 165-173.
69. Kimmel, C.B. Patterning the brain of the zebrafish embryo. Annu. Rev. Neurosci., 1993, 16, 707-732.
70. Easter, S. S.; Wilson, S. W.; Ross, L. S.; Burill, J. D. Tract formation in the brain of the zebrafish embryo. In: The Nerve Growth Cone. Letourneau, P. C., Kater, S. B., Macagno, E. R., Eds.; Raven: New York, 1992; pp. 337-351.
71. Wilson, S.W.; Ross, L.S.; Parrett, T.; Easter, S.S. Jr. The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development, 1990, 108, 121-45.
72. Strähle, U.; Blader, P. Early neurogenesis in the zebrafish embryo. FASEB J., 1994, 8, 692-698.
73. Hsu, H.J.; Hsu, N.C.; Hu, M.C.; Chung, B.C. Steroidogenesis in zebrafish and mouse models. Mol. Cell. Endocrinol., 2006, 248, 160-163.
74. Blanchard, R.L.; Freimuth, R.R.; Buck, J.; Weinshilboum, R.M.; Coughtrie, M.W. A proposed nomenclature system for the cytosolic sulfotransferase (SULT) superfamily. Pharmacogenetics, 2004, 14, 199-211.
75. Brodskiǐ, L.I.; Ivanov, V.V.; Kalaǐdzidis, IaL.; Leontovich, A.M.; Nikolaev, V.K.; Feranchuk, S.I.; Drachev, V.A. GeneBee-NET:Internet-based server for analyzing biopolymers structure. Biochemistry, 1995, 60, 923-928.
76. Nikolaev, V.K.; Leontovich, A.M.; Drachev, V.A.; Brodsky, L.I. Building multiple alignment using iterative analyzing biopolymers structure dynamic improvement of the initial motif alignment. Biochemistry, 1997, 62, 578-582.