Hepatic reduction of the secondary bile acid 7-oxolithocholic acid is mediated by 11β-hydroxysteroid dehydrogenase 1

Biochemical Journal

Volumn 436, Issue 3, 2011, Pages 621-629

  Odermatt, Alex ^a   Da Cunha, Thierry ^a   Penno, Carlos A ^a,b   Chandsawangbhuwana, Charlie ^c   Reichert, Christian ^a   Wolf, Armin ^b   Dong, Min ^b   Baker, Michael E ^c  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

11 hydroxysteroid dehydrogenase; 7 oxolithocholic acid; Bile acid; Glucocorticoid; Liver; Metabolism

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 7 OXOLITHOCHOLIC ACID; BILE ACID; CHENODEOXYCHOLIC ACID; CORTISONE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLYCINE; HYDROCORTISONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TAURINE; UNCLASSIFIED DRUG;

ARTICLE; BILE ACID METABOLISM; CONTROLLED STUDY; CORTICOSTEROID METABOLISM; ENDOPLASMIC RETICULUM; ENZYME BINDING; ENZYME INHIBITION; ENZYME LOCALIZATION; HORMONE METABOLISM; HUMAN; HUMAN TISSUE; HYDROCORTISONE BLOOD LEVEL; LIVER MICROSOME; MALE; PRIORITY JOURNAL;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANIMALS; BILE ACIDS AND SALTS; CORTISONE; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; HYDROCORTISONE; KINETICS; LITHOCHOLIC ACID; MALE; MICE; MICROSOMES, LIVER; NADP; OXIDATION-REDUCTION; RATS; RECOMBINANT PROTEINS;

ANIMALIA;

EID: 79957749029     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110022     Document Type: Article

References (51)

1. Hofmann, A. F. and Hagey, L. R. (2008) Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell. Mol. Life Sci. 65, 2461-2483
2. Russell, D. W. (2003) The enzymes, regulation, and genetics of bile acid synthesis. Annu. Rev. Biochem. 72, 137-174
3. Rossi, S. S., Converse, J. L. and Hofmann, A. F. (1987) High pressure liquid chromatographic analysis of conjugated bile acids in human bile: simultaneous resolution of sulfated and unsulfated lithocholyl amidates and the common conjugated bile acids. J. Lipid Res. 28, 589-595
4. van Berge Henegouwen, G. P., Brandt, K. H., Eyssen, H. and Parmentier, G. (1976) Sulphated and unsulphated bile acids in serum, bile, and urine of patients with cholestasis. Gut 17, 861-869 (Pubitemid 8005662)
5. Ridlon, J. M., Kang, D. J. and Hylemon, P. B. (2006) Bile salt biotransformations by human intestinal bacteria. J. Lipid Res. 47, 241-259
6. Hofmann, A. F. (1990) Bile acid secretion, bile flow and biliary lipid secretion in humans. Hepatology 12, 17S-22S
7. Fukiya, S., Arata, M., Kawashima, H., Yoshida, D., Kaneko, M., Minamida, K., Watanabe, J., Ogura, Y., Uchida, K., Itoh, K. et al. (2009) Conversion of cholic acid and chenodeoxycholic acid into their 7-oxo derivatives by Bacteroides intestinalis AM-1 isolated from human feces. FEMS Microbiol. Lett. 293, 263-270
8. Macdonald, I. A., Williams, C. N., Mahony, D. E. and Christie, W. M. (1975) NAD- and NADP-dependent 7α-hydroxysteroid dehydrogenases from Bacteroides fragilis. Biochim. Biophys. Acta 384, 12-24
9. Fedorowski, T., Salen, G., Tint, G. S. and Mosbach, E. (1979) Transformation of chenodeoxycholic acid and ursodeoxycholic acid by human intestinal bacteria. Gastroenterology 77, 1068-1073
10. MacDonald, I. A., Rochon, Y. P., Hutchison, D. M. and Holdeman, L. V. (1982) Formation of ursodeoxycholic acid from chenodeoxycholic acid by a 7β-hydroxysteroid dehydrogenase-elaborating Eubacterium aerofaciens strain cocultured with 7α-hydroxysteroid dehydrogenase-elaborating organisms. Appl. Environ. Microbiol. 44, 1187-1195
11. Hirano, S. and Masuda, N. (1981) Epimerization of the 7-hydroxy group of bile acids by the combination of two kinds of microorganisms with 7α- and 7β-hydroxysteroid dehydrogenase activity, respectively. J. Lipid Res. 22, 1060-1068
12. 14 in the rat. J. Biol. Chem. 230, 581-588
13. Fromm, H., Carlson, G. L., Hofmann, A. F., Farivar, S. and Amin, P. (1980) Metabolism in man of 7-ketolithocholic acid: precursor of cheno- and ursodeoxycholic acids. Am. J. Physiol. 239, G161-G166
14. Salen, G., Tint, G. S., Eliav, B., Deering, N. and Mosbach, E. H. (1974) Increased formation of ursodeoxycholic acid in patients treated with chenodeoxycholic acid. J. Clin. Invest. 53, 612-621
15. Fromm, H., Sarva, R. P. and Bazzoli, F. (1983) Formation of ursodeoxycholic acid from chenodeoxycholic acid in the human colon: studies of the role of 7-ketolithocholic acid as an intermediate. J. Lipid Res. 24, 841-853 (Pubitemid 13015566)
16. Amuro, Y., Yamade, W., Kudo, K., Yamamoto, T., Hada, T. and Higashino, K. (1989) Reduction of 7-ketolithocholic acid by human liver enzyme preparations in vitro. Am. J. Physiol 256, G67-G71
17. Odermatt, A., Atanasov, A. G., Balazs, Z., Schweizer, R. A., Nashev, L. G., Schuster, D. and Langer, T. (2006) Why is 11β-hydroxysteroid dehydrogenase type 1 facing the endoplasmic reticulum lumen? Physiological relevance of the membrane topology of 11β-HSD1. Mol. Cell. Endocrinol. 248, 15-23
18. Atanasov, A. G. and Odermatt, A. (2007) Readjusting the glucocorticoid balance: an opportunity for modulators of 11β-hydroxysteroid dehydrogenase type 1 activity? Endocr. Metab. Immune Disord. Drug Targets 7, 125-140
19. Hadoke, P. W., Iqbal, J. and Walker, B. R. (2009) Therapeutic manipulation of glucocorticoid metabolism in cardiovascular disease. Br. J. Pharmacol. 156, 689-712
20. Boyle, C. D. and Kowalski, T. J. (2009) 11β-Hydroxysteroid dehydrogenase type 1 inhibitors: a review of recent patents. Expert Opin. Ther. Pat. 19, 801-825
21. Hughes, K. A., Webster, S. P. and Walker, B. R. (2008) 11β-Hydroxysteroid dehydrogenase type 1 (11β-HSD1) inhibitors in type 2 diabetes mellitus and obesity. Expert Opin. Invest. Drugs 17, 481-496
22. Odermatt, A. and Nashev, L. G. (2010) The glucocorticoid-activating enzyme 11β-hydroxysteroid dehydrogenase type 1 has broad substrate specificity: physiological and toxicological considerations. J. Steroid Biochem. Mol. Biol. 119, 1-13
23. Senesi, S., Legeza, B., Balazs, Z., Csala, M., Marcolongo, P., Kereszturi, E., Szelenyi, P., Egger, C., Fulceri, R., Mandl, J. et al. (2010) Contribution of fructose 6-phosphate to glucocorticoid activation in the endoplasmic reticulum: possible implication in the metabolic syndrome. Endocrinology 151, 4830-4839
24. Gumy, C., Thurnbichler, C., Aubry, E. M., Balazs, Z., Pfisterer, P., Baumgartner, L., Stuppner, H., Odermatt, A. and Rollinger, J. M. (2009) Inhibition of 11β-hydroxysteroid dehydrogenase type 1 by plant extracts used as traditional antidiabetic medicines. Fitoterapia 80, 200-205
25. Schuster, D., Maurer, E. M., Laggner, C., Nashev, L. G., Wilckens, T., Langer, T. and Odermatt, A. (2006) The discovery of new 11β-hydroxysteroid dehydrogenase type 1 inhibitors by common feature pharmacophore modeling and virtual screening. J. Med. Chem. 49, 3454-3466
26. Zhang, J., Osslund, T. D., Plant, M. H., Clogston, C. L., Nybo, R. E., Xiong, F., Delaney, J. M. and Jordan, S. R. (2005) Crystal structure of murine 11β-hydroxysteroid dehydrogenase 1: an important therapeutic target for diabetes. Biochemistry 44, 6948-6957
27. Tanaka, N., Nonaka, T., Tanabe, T., Yoshimoto, T., Tsuru, D. and Mitsui, Y. (1996) Crystal structures of the binary and ternary complexes of 7α-hydroxysteroid dehydrogenase from Escherichia coli. Biochemistry 35, 7715-7730
28. Kanai, S., Sato, Y., Nokubo, M. and Kitani, K. (1989) Hepatic biotransformation and choleretic effect of 7-ketolithocholic acid in the rat. Lipids 24, 859-865 (Pubitemid 19262019)
29. Amuro, Y., Yamade, W., Nakano, T., Hayashi, E., Hada, T. and Higashino, K. (1985) Reduction of 7-ketolithocholic acid to chenodeoxycholic acid by rat liver preparations in vitro. Biochim. Biophys. Acta 841, 229-231
30. Clarke, J. L. and Mason, P. J. (2003) Murine hexose-6-phosphate dehydrogenase: a bifunctional enzyme with broad substrate specificity and 6-phosphogluconolactonase activity. Arch. Biochem. Biophys. 415, 229-234
31. Hult, M., Elleby, B., Shafqat, N., Svensson, S., Rane, A., Jornvall, H., Abrahmsen, L. and Oppermann, U. (2004) Human and rodent type 1 11β-hydroxysteroid dehydrogenases are 7β-hydroxycholesterol dehydrogenases involved in oxysterol metabolism. Cell. Mol. Life Sci. 61, 992-999
32. Schweizer, R. A., Zurcher, M., Balazs, Z., Dick, B. and Odermatt, A. (2004) Rapid hepatic metabolism of 7-ketocholesterol by 11β-hydroxysteroid dehydrogenase type 1: species-specific differences between the rat, human, and hamster enzyme. J. Biol. Chem. 279, 18415-18424
33. Nashev, L. G., Chandsawangbhuwana, C., Balazs, Z., Atanasov, A. G., Dick, B., Frey, F. J., Baker, M. E. and Odermatt, A. (2007) Hexose-6-phosphate dehydrogenase modulates 11β-hydroxysteroid dehydrogenase type 1-dependent metabolism of 7-keto- and 7β-hydroxy-neurosteroids. PLoS ONE 2, e561
34. Gomez-Sanchez, E. P., Romero, D. G., de Rodriguez, A. F., Warden, M. P., Krozowski, Z. and Gomez-Sanchez, C. E. (2008) Hexose-6-phosphate dehydrogenase and 11β-hydroxysteroid dehydrogenase-1 tissue distribution in the rat. Endocrinology 149, 525-533
35. Maser, E., Volker, B. and Friebertshauser, J. (2002) 11β- Hydroxysteroid dehydrogenase type 1 from human liver: dimerization and enzyme cooperativity support its postulated role as glucocorticoid reductase. Biochemistry 41, 2459-2465 (Pubitemid 34160910)
36. Ozols, J. (1995) Lumenal orientation and post-translational modifications of the liver microsomal 11β-hydroxysteroid dehydrogenase. J. Biol. Chem. 270, 2305-2312
37. Arampatzis, S., Kadereit, B., Schuster, D., Balazs, Z., Schweizer, R. A., Frey, F. J., Langer, T. and Odermatt, A. (2005) Comparative enzymology of 11β-hydroxysteroid dehydrogenase type 1 from six species. J. Mol. Endocrinol. 35, 89-101
38. Buhler, H., Perschel, F. H., Fitzner, R. and Hierholzer, K. (1994) Endogenous inhibitors of 11β-OHSD: existence and possible significance. Steroids 59, 131-135
39. Ackermann, D., Vogt, B., Escher, G., Dick, B., Reichen, J., Frey, B. M. and Frey, F. J. (1999) Inhibition of 11β-hydroxysteroid dehydrogenase by bile acids in rats with cirrhosis. Hepatology 30, 623-629 (Pubitemid 29409404)
40. Stauffer, A. T., Rochat, M. K., Dick, B., Frey, F. J. and Odermatt, A. (2002) Chenodeoxycholic acid and deoxycholic acid inhibit 11β- hydroxysteroid dehydrogenase type 2 and cause cortisol-induced transcriptional activation of the mineralocorticoid receptor. J. Biol. Chem. 277, 26286-26292
41. + in 17β-hydroxysteroid dehydrogenase. J. Biol. Chem. 273, 8145-8152
42. Jornvall, H., Persson, B., Krook, M., Atrian, S., Gonzalez-Duarte, R., Jeffery, J. and Ghosh, D. (1995) Short-chain dehydrogenases/reductases (SDR). Biochemistry 34, 6003-6013
43. Tanaka, N., Nonaka, T., Nakanishi, M., Deyashiki, Y., Hara, A. and Mitsui, Y. (1996) Crystal structure of the ternary complex of mouse lung carbonyl reductase at 1.8Å resolution: the structural origin of coenzyme specificity in the short-chain dehydrogenase/reductase family. Structure 4, 33-45 (Pubitemid 126658522)
44. Amuro, Y., Endo, T., Higashino, K., Uchida, K. and Yamamura, Y. (1981) Urinary and fecal keto bile acids in liver cirrhosis. Clin. Chim. Acta 114, 137-147
45. Bjorkhem, I., Angelin, B., Einarsson, K. and Ewerth, S. (1982) Fasting levels of monoketonic bile acids in human peripheral and portal circulation. J. Lipid Res. 23, 1020-1025 (Pubitemid 13207267)
46. Shiotsuki, H., Maeda, Y. and Chijiiwa, K. (2004) Purification and characterization of 7β-hydroxysteroid dehydrogenase from rabbit liver microsomes. J. Steroid Biochem. Mol. Biol. 91, 185-190
47. Song, W., Chen, J., Dean, W. L., Redinger, R. N. and Prough, R. A. (1998) Purification and characterization of hamster liver microsomal 7α-hydroxycholesterol dehydrogenase: similarity to type I 11β-hydroxysteroid dehydrogenase. J. Biol. Chem. 273, 16223-16228
48. Hennebert, O., Pernelle, C., Ferroud, C. and Morfin, R. (2007) 7α- and 7β-hydroxy-epiandrosterone as substrates and inhibitors for the human 11β-hydroxysteroid dehydrogenase type 1. J. Steroid Biochem. Mol. Biol. 105, 159-165
49. + and is stimulated by extracellular glucose. Mol. Cell. Endocrinol. 301, 137-141
50. Makishima, M., Okamoto, A. Y., Repa, J. J., Tu, H., Learned, R. M., Luk, A., Hull, M. V., Lustig, K. D., Mangelsdorf, D. J. and Shan, B. (1999) Identification of a nuclear receptor for bile acids. Science 284, 1362-1365 (Pubitemid 29289663)
51. Wang, H., Chen, J., Hollister, K., Sowers, L. C. and Forman, B. M. (1999) Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol. Cell 3, 543-553