A comparative study of the sulfation of bile acids and a bile alcohol by the Zebra danio (Danio rerio) and human cytosolic sulfotransferases (SULTs)

Journal of Steroid Biochemistry and Molecular Biology

Volumn 127, Issue 3-5, 2011, Pages 307-314

  Kurogi, Katsuhisa ^a   Krasowski, Matthew D ^b   Injeti, Elisha ^a   Liu, Ming Yih ^c   Williams, Frederick E ^a   Sakakibara, Yoichi ^d   Suiko, Masahito ^d   Liu, Ming Cheh ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

^b UNIVERSITY OF IOWA HOSPITALS AND CLINICS   (United States)

^c NATIONAL SYNCHROTRON RADIATION RESEARCH CENTER   (Taiwan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

Bile acid; Sulfation; Sulfotransferase; Zebra danio

Indexed keywords

5ALPHA PETROMYZONOL; ALCOHOL; BILE ACID; LITHOCHOLIC ACID; SULFOTRANSFERASE; SULFOTRANSFERASE 2A1; SULFOTRANSFERASE 3 ST2; SULFOTRANSFERASE 3 ST3; UNCLASSIFIED DRUG;

ARTICLE; COMPARATIVE STUDY; CYTOSOL; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PH; SULFATION; VERTEBRATE; ZEBRA FISH;

ANIMALS; BILE ACIDS AND SALTS; CHOLESTANOLS; CYTOSOL; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; SUBSTRATE SPECIFICITY; SULFATES; SULFOTRANSFERASES; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 81255188598     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.07.011     Document Type: Article

References (63)

1. G.A. Haslewood Bile salt evolution J. Lipid Res. 8 1967 535 550
2. A.F. Hofmann, L.R. Hagey, and M.D. Krasowski Bile salts of vertebrates: structural variation and possible evolutionary significance J. Lipid Res. 51 2010 226 246
3. L.R. Hagey, N. Vidal, A.F. Hofmann, and M.D. Krasowski Evolutionary diversity of bile salts in reptiles and mammals, including analysis of ancient human and extinct giant ground sloth coprolites BMC Evol. Biol. 10 2010 133
4. L.R. Hagey, P.R. Møller, A.F. Hofmann, and M.D. Krasowski Diversity of bile salts in fish and amphibians: evolution of a complex biochemical pathway Physiol. Biochem. Zool. 83 2010 308 321
5. L.R. Hagey, N. Vidal, A.F. Hofmann, and M.D. Krasowski Complex evolution of bile salts in birds Auk. 127 2010 820 831
6. S. Kuroki, K. Shimazu, M. Kuwabara, M. Une, K. Kihira, T. Kuramoto, and T. Hoshita Identification of bile alcohols in human bile J. Lipid Res. 26 1985 230 240 (Pubitemid 15078103)
7. M. Yoshida, M. Murata, K. Inaba, and M. Morisawa A chemoattractant for ascidian spermatozoa is a sulfated steroid Proc. Natl. Acad. Sci. U.S.A. 99 2002 14831 14836 (Pubitemid 35334569)
8. D.L. Motola, C.L. Cummins, V. Rottiers, K.K. Sharma, T. Li, Y. Li, K. Suino-Powell, H.E. Xu, R.J. Auchus, A. Antebi, and D.J. Mangelsdorf Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans Cell 124 2006 1209 1223
9. D.W. Russel The enzymes, regulation, and genetics of bile acid synthesis Annu. Rev. Biochem. 72 2003 137 174
10. B. Borgstrom, J.A. Barrowman, and M. Lindstrom Roles of bile acids in intestinal lipid digestion and absorption H. Danielsson, J. Sjovall, Sterols and Bile Acids 1985 Elsevier Amsterdam 405 425
11. A.F. Hofmann The continuing importance of bile acids in liver and intestinal disease Arch. Intern. Med. 159 1999 2647 2658
12. P. Fickert, A. Fuchsbichler, H.C. Marschall, M. Wangner, G. Zollner, R. Kruse, K. Zatloukat, H. Jaeschke, H. Denk, and M. Trauner Lithocholic acid feeding induces segmental bile duct obstruction and destructive cholangitis in mice Am. J. Pathol. 168 2006 410 422 (Pubitemid 43271140)
13. A.F. Hofmann Detoxification of lithocholic acid, a toxic bile acid: relevance to drug hepatotoxicity Drug Metab. Rev. 36 2004 703 722 (Pubitemid 39453070)
14. G.M. Mulder, and W.B. Jakoby Sulfation in conjugation reactions G.J. Mulder, Drug Metabolism 1990 Taylor and Francis London 107 161
15. R. Weinshilboum, and D.M. Otterness Sulfotransferase enzyme conjugation-deconjugation reactions F.C. Kaufman, Drug Metabolism and Toxicity 1994 Springer Verlag Berlin 45 78
16. F. Lipmann Biological sulfate activation and transfer Science 128 1958 575 580
17. R.L. Blanchard, R.R. Freimuth, J. Buck, R.M. Weinshilboum, and M.W.H. Coughtrie A proposed nomenclature system for the cytosolic sulfotransferase (SULT) superfamily Pharmacogenetics 14 2004 199 211 (Pubitemid 38373115)
18. I. Makino, K. Shinozaki, S. Nakagawa, and K. Mashimo Measurement of sulfated and nonsulfated bile acids in human serum and urine J. Lipid Res. 15 1974 132 138
19. B. Alme, A. Bremmelgaard, J. Sjovall, and P. Thomassen Analysis of metabolic profiles of bile acids in urine using a lipophilic anion exchanger and computerized gas-liquid chromatography-mass spectrometry J. Lipid Res. 18 1977 339 362 (Pubitemid 8114142)
20. A. Radominska, K.A. Comer, P. Zimniak, J. Falany, M. Iscan, and C.N. Falany Human liver steroid sulphotransferase sulphates bile acids Biochem. J. 272 1990 597 604
21. D.M. Otterness, E.D. Wieben, T.C. Wood, W.G. Watson, B.J. Madden, D.J. McCormick, and R.M. Weinshilboum Human liver dehydroepiandrosterone sulfotransferase: molecular cloning and expression of cDNA Mol. Pharmacol. 41 1992 865 872 (Pubitemid 23023329)
22. T. Goto, F. Holzinger, L.R. Hagey, C. Cerr, H.T. Ton-Nu, C.D. Schteingart, J.H. Steinbach, B.L. Shneider, and A.F. Hofmann Physicochemical and physiological properties of 5alpha-cyprinol sulfate, the toxic bile salt of cyprinid fish J. Lipid Res. 44 2003 1643 1651 (Pubitemid 37185874)
23. I.G. Anderson, T. Briggs, and G.A.D. Haslewood Comparative studies of 'bile salts.' 18. The chemistry of cyprinol Biochem. J. 90 1964 303 308
24. E.J. Reschly, N. Ai, S. Ekins, W.J. Welsh, L.R. Hagey, A.F. Hofmann, and M.D. Krasowski Evolution of the bile salt nuclear receptor FXR in vertebrates J. Lipid Res. 49 2008 1577 1587
25. T. Sugahara, C.C. Liu, T.G. Pai, P. Collodi, M. Suiko, Y. Sakakibara, K. Nishiyama, and M.C. Liu Sulfation of hydroxychlorobiphenyls. Molecular cloning, expression, and functional characterization of zebrafish SULT1 sulfotransferases Eur. J. Biochem. 70 2003 2404 2411 (Pubitemid 36645358)
26. T. Sugahara, C.C. Liu, G. Cater, T.G. Pai, and M.C. Liu cDNA cloning, expression, and functional characterization of a zebrafish SULT1 cytosolic sulfotransferase Arch. Biochem. Biophys. 414 2003 67 73 (Pubitemid 36555446)
27. M.Y. Liu, Y.S. Yang, T. Sugahara, S. Yasuda, and M.C. Liu Identification of a novel zebrafish SULT1 cytosolic sulfotransferase: cloning expression, characterization, and developmental expression study Arch. Biochem. Biophys. 437 2005 10 19 (Pubitemid 40463676)
28. S. Yasuda, A.P. Kumar, M.Y. Liu, M. Suiko, L. Chen, and M.C. Liu Identification of a novel thyroid hormone-sufating cytosolic sulfotransferase, SULT1 ST5, from zebrafish FEBS J. 272 2005 3828 3837
29. S. Yasuda, C.C. Liu, S. Takahashi, M. Suiko, L. Cheh, R. Snow, and M.C. Liu Identification of a novel estrogen-sufating cytosolic SULT from zebrafish: molecular cloning expression, characterization, and ontogeny study Biochem. Biophys. Res. Commun. 330 2005 219 225 (Pubitemid 40394955)
30. T.A. Liu, S. Bhuiyan, R. Snow, S. Yasuda, T. Yasuda, Y.S. Yang, F.E. Williams, M.Y. Liu, M. Suiko, G. Carter, and M.C. Liu Identification and characterization of two novel cytosolic sulfotransferases, SULT1 ST7 and SULT1 ST8, from zebrafish Aquat. Toxicol. 89 2008 94 102
31. T. Sugahara, Y.S. Yang, C.C. Liu, T.G. Pai, and M.C. Liu Sulphonation of dehydroepiandrosterone and neurosteroid: molecular cloning expression, and functional characterization of a novel zebrafish SULT2 cytosolic sulphotransferase Biochem. J. 375 2003 785 791 (Pubitemid 37433529)
32. S. Yasuda, M.Y. Liu, Y.S. Yang, R. Snow, S. Takahashi, and M.C. Liu Identification of novel hydroxysteroid-sulfating cytosolic SULTs, SULT2 ST2 and SULT2 ST3, from zebrafish: cloning expression, characterization, and developmental expression Arch. Biochem. Biophys. 455 2006 1 9 (Pubitemid 44602009)
33. T. Yasuda, S. Yasuda, F.E. Williams, M.Y. Liu, Y. Sakakibara, S. Bhuiyan, R. Snow, G. Carter, and M.C. Liu Characterization and ontogenic study of novel steroid-sufating SULT3 sulfotransferases from zebrafish Mol. Cell Endocrinol. 294 2008 29 36
34. S. Yasuda, M. Burgess, T. Yasuda, M.Y. Liu, S. Bhuiyan, F.E. Williams, K. Kurogi, Y. Sakakibara, M. Suiko, and M.C. Liu A novel hydroxysteroid-sulfating cytosolic sulfotransferase, SULT3 ST3, from zebrafish: identification, characterization, and ontogenic study Drug Metab. Lett. 3 4 2009 217 227
35. T. Sugahara, C.C. Liu, T.G. Pai, and M.C. Liu Molecular cloning, expression, and functional characterization of a novel zebrafish cytosolic sulfotransferase Biochem. Biophys. Res. Commun. 300 2003 725 730 (Pubitemid 36268897)
36. T.A. Liu, S. Bhuiyan, M.Y. Liu, T. Sugahara, Y. Sakakibara, M. Suiko, S. Yasuda, Y. Kakuta, M. Kimura, F.E. Williams, and M.C. Liu Zebrafish as a model for the study of the phase II cytosolic sulfotransferases Curr. Drug. Metab. 11 6 2010 538 546
37. M. Suiko, Y. Sakakibara, and M.C. Liu Sulfation of environmental estrogen-like chemicals by human cytosolic sulfotransferases Biochem. Biophys. Res. Commun. 267 2000 80 84 (Pubitemid 30072511)
38. T.G. Pai, T. Sugahara, M. Suiko, Y. Sakakibara, F. Xu, and M.C. Liu Differential xenoestrogen-sulfating activities of the human cytosolic sulfotransferase: molecular cloning expression, and purification of human SULT2B1a and SULT2B1b sulfotransferases Biochim. Biophys. Acta 1573 2002 165 170 (Pubitemid 35217937)
39. Y. Sakakibara, Y. Takami, T. Nakayama, M. Suiko, and M.C. Liu Localization and functional analysis of the substrate specificity/catalytic domains of human M-form and P-form phenol sulfotransferases J. Biol. Chem. 273 1998 6242 6247 (Pubitemid 28144711)
40. Y. Sakakibara, K. Yanagisawa, J. Katafuchi, D.P. Ringer, Y. Takami, T. Nakayama, M. Suiko, and M.C. Liu Molecular cloning, expression, and characterization of novel human SULT1C sulfotransferases that catalyze the sulfonation of N-hydroxy-2-acetylaminofluorene J. Biol. Chem. 273 1998 33929 33935
41. Y. Sakakibara, M. Suiko, T.G. Pai, T. Nakayama, Y. Takami, J. Katafuchi, and M.C. Liu Highly conserved mouse and human brain sulfotransferases: molecular cloning expression, and functional characterization Gene 285 2002 39 47 (Pubitemid 34246319)
42. M.C. Liu, and F. Lipmann Decrease of tyrosine-O-sulfate-containing proteins found in rat fibroblasts infected with Rouse sarcoma virus or Fujinami sarcoma virus Proc. Natl. Acad. Sci. U.S.A. 81 1984 3695 3698 (Pubitemid 14087790)
43. K. Yanagisawa, Y. Sakakibara, M. Suiko, Y. Takami, T. Nakayama, H. Nakajima, K. Takayanagi, Y. Natori, and M.C. Liu cDNA cloning, expression, and characterization of the human bifunctional ATP sulfurylase/adenosine 5′-phosphosulfate kinase enzyme Biosci. Biotechnol. Biochem. 62 1998 1037 1040 (Pubitemid 128473741)
44. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
45. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
46. R.H. Palmer Bile acid sulfates. II. Formation, metabolism, and excretion of lithocholic acid sulfates in the rat J. Lipid Res. 12 1971 680 687
47. A.E. Cowen, M.G. Korman, A.F. Hofman, O.W. Cass, and S.B. Coffin Metabolism of lithocholate in healthy man. II. Enterohepatic circulation Gastroenterology 69 1975 67 76
48. I.M. Yousef, S.G. Barnwell, B. Tuchweber, A. Weber, and C.C. Roy Effect of complete sulfation of bile acids on bile formation in rats Hepatology 7 1987 535 542 (Pubitemid 17073161)
49. H. Takikawa, J. Tomita, T. Takemura, and M. Yamanaka Cytotoxic effect and uptake mechanism by isolated rat hepatocytes of lithocholate and its glucuronide and sulfate Biochim. Biophys. Acta 1091 1991 173 178
50. A. Takahashi, N. Tanida, A. Kawaura, M. Nishikawa, and T. Shimoyama Sulphated bile acid per se inhibits colonic carcinogenesis in mice Eur. J. Cancer Prev. 2 1993 161 167
51. W. Li, A.P. Scott, M.J. Siefkes, H. Yan, Q. Liu, S.S. Yun, and D.A. Gage Bile acid secreted by male sea lamprey that acts as a sex pheromone Science 296 2002 138 141 (Pubitemid 34280072)
52. W.C. Michel, and L.L. Lubomudrov Specificity and sensitivity of the olfactory organ of the zebrafish, danio renio J. Comp. Physiol. A 177 1995 191 199
53. M. Huertas, L. Hagey, A.F. Hofmann, J. Cerd, A.V.M. Canário, and P.C. Hubbard Olfactory sensitivity to bile fluid and bile salts in the European eel (Anguilla anguilla), goldfish (Carassius auratus) and Mozambique tilapia (Oreochromis mossambicus) suggests a;broad range' sensitivity not confined to those produced by conspecifics alone J. Exp. Biol. 213 2009 308 317
54. J. Huang, S.P. Bathena, J. Tong, M. Roth, B. Hagenbuch, and Y. Alnouti Kinetic analysis of bile acid sulfation by stably expressed human sulfotransferase 2A1 (SULT2A1) Xenobiotica 40 2010 184 194
55. B. Strandvik, and S.A. Wikström Tetrahydroxylated bile acids in healthy newborns Eur. J. Clin. Invest. 12 1982 301 305 (Pubitemid 12024503)
56. M.Y. El-Mir, M.D. Badia, N. Luengo, M.J. Monte, and J.J. Marin Increased levels of typically fetal bile acid species in patients with hepatocellular carcinoma Clin. Sci. 100 2001 499 508 (Pubitemid 32434115)
57. P. Stärkel, T. Shindano, Y. Horsmans, J.F. Gigot, M. Fernandez-Tagarro, J.J.G. Marin, and M.J. Monte Foetal 'flat' bile acids reappear during human liver regeneration after surgery Eur. J. Clin. Invest. 39 2009 58 64
58. J.J. Cali, C.L. Hsieh, U. Francke, and D.W. Russell Mutations in the bile acid biosynthetic enzyme sterol 27-hydroxylase underlie cerebrotendinous xanthomatosis J. Biol. Chem. 266 1991 7779 7783 (Pubitemid 21906434)
59. M. Asakawa, T. Noguchi, H. Seto, K. Furihata, K. Fujikawa, and K. Hashimoto Structure of the toxin isolated from carp (Cyprinus carpio) bile Tpoxicon 28 1990 1063 1069 (Pubitemid 20330358)
60. K. Hattori, N. Motohashi, I. Kobayashi, T. Tohya, M. Oikawa, and H.O. Tamura Cloning, expression, and characterization of cytosolic sulfotransferase isozymes from Drosophila melanogaster Biosci. Biotechnol. Biochem. 72 2008 540 547 (Pubitemid 351353663)
61. K. Hattori, M. Hirayama, H. Suzuki, H. Hamamoto, K. Sekimizu, and H.O. Tamura Cloning and expression of a novel sulfotransferase with unique substrate specificity from Bombyx mori Biosci. Biotechnol. Biochem. 71 2007 1044 1051 (Pubitemid 46650931)
62. K. Hattori, M. Inoue, T. Inoue, H. Arai, and H.O. Tamura A novel sulfotransferase abundantly expressed in the dauer larvae of Caenorhabditis elegans J. Biochem. 139 2006 355 362 (Pubitemid 43667099)
63. J.M. Kornprobst, C. Sallenave, and G. Barnathan Sulfated compounds from marine organisms Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 119 1998 1 51 (Pubitemid 28101939)