Impaired oxidoreduction by 11β-hydroxysteroid dehydrogenase 1 results in the accumulation of 7-oxolithocholic acid

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2874-2883

  Penno, Carlos A ^a   Morgan, Stuart A ^b   Vuorinen, Anna ^c   Schuster, Daniela ^c   Lavery, Gareth G ^b   Odermatt, Alex ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Bile acid; Biomarker; Glucocorticoid; Metabolic disease; Metabolism; Species

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 7 OXOLITHOCHOLIC ACID; 7 OXOLITHOCHOLIC ACID OXIDOREDUCTASE; BIOLOGICAL MARKER; GLYCINE; LITHOCHOLIC ACID; OXIDOREDUCTASE; TAURINE; UNCLASSIFIED DRUG;

11BETA HYDROXYSTEROID DEHYDROGENASE DEFICIENCY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOG; EMBRYO; ENZYME ACTIVITY; ENZYME DEFICIENCY; GUINEA PIG; HAMSTER; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID STORAGE; LIVER MICROSOME; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; RAT; SPECIES DIFFERENCE;

BILE ACID; BIOMARKER; GLUCOCORTICOID; METABOLIC DISEASE; METABOLISM; SPECIES;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANIMALS; CRICETINAE; DOGS; GUINEA PIGS; HUMANS; LITHOCHOLIC ACID; MALE; MESOCRICETUS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSOMES, LIVER; MOLECULAR DOCKING SIMULATION; OXIDATION-REDUCTION; RATS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SPECIES SPECIFICITY;

EID: 84884133611     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M042499     Document Type: Article

References (55)

1. Odermatt, A., A. G. Atanasov, Z. Balazs, R. A. S. Schweizer, L. G. Nashev, D. Schuster, and T. Langer. 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.
2. Tomlinson, J. W., and P. M. Stewart. 2007. Modulation of glucocorticoid action and the treatment of type-2 diabetes. Best Pract. Res. Clin. Endocrinol. Metab. 21: 607-619.
3. Tomlinson, J. W., E. A. Walker, I. J. Bujalska, N. Draper, G. G. Lavery, M. S. Cooper, M. Hewison, and P. M. Stewart. 2004. 11β- hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr. Rev. 25: 831-866.
4. Kotelevtsev, Y., M. C. Holmes, A. Burchell, P. M. Houston, D. Schmoll, P. Jamieson, R. Best, R. Brown, C. R. W. Edwards, J. R. Seckl, et al. 1997. 11β-Hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc. Natl. Acad. Sci. USA. 94: 14924-14929.
5. Morton, N. M., M. C. Holmes, C. Fiévet, B. Staels, A. Tailleux, J. J. Mullins, and J. R. Seckl. 2001. Improved lipid and lipoprotein profile, hepatic insulin sensitivity, and glucose tolerance in 11β-hydroxysteroid dehydrogenase type 1 null mice. J. Biol. Chem. 276: 41293-41300.
6. Morton, N. M., J. M. Paterson, H. Masuzaki, M. C. Holmes, B. Staels, C. Fievet, B. R. Walker, J. S. Flier, J. J. Mullins, and J. R. Seckl. 2004. Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes. 53: 931-938.
7. Wamil, M., J. H. Battle, S. Turban, T. Kipari, D. Seguret, R. de Sousa Peixoto, Y. B. Nelson, D. Nowakowska, D. Ferenbach, L. Ramage, et al. 2011. Novel fat depot-specific mechanisms underlie resistance to visceral obesity and inflammation in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes. 60: 1158-1167.
8. Masuzaki, H., J. Paterson, H. Shinyama, N. M. Morton, J. J. Mullins, J. R. Seckl, and J. S. Flier. 2001. A transgenic model of visceral obesity and the metabolic syndrome. Science. 294: 2166-2170.
9. Masuzaki, H., H. Yamamoto, C. J. Kenyon, J. K. Elmquist, N. M. Morton, J. M. Paterson, H. Shinyama, M. G. F. Sharp, S. Fleming, J. J. Mullins, et al. 2003. Transgenic amplification of glucocorticoid action in adipose tissue causes high blood pressure in mice. J. Clin. Invest. 112: 83-90.
10. Paterson, J. M., N. M. Morton, C. Fievet, C. J. Kenyon, M. C. Holmes, B. Staels, J. R. Seckl, and J. J. Mullins. 2004. Metabolic syndrome without obesity: hepatic overexpression of 11β-hydroxysteroid dehydrogenase type 1 in transgenic mice. Proc. Natl. Acad. Sci. USA. 101: 7088-7093.
11. Boyle, C. D., and T. J. Kowalski. 2009. 11β-hydroxysteroid dehydrogenase type 1 inhibitors: a review of recent patents. Expert Opin. Ther. Pat. 19: 801-825.
12. Hughes, K. A., S. P. Webster, and B. R. Walker. 2008. 11β-hydroxysteroid dehydrogenase type 1 (11β-HSD1) inhibitors in type 2 diabetes mellitus and obesity. Expert Opin. Investig. Drugs. 17: 481-496.
13. Hadoke, P. W. F., J. Iqbal, and B. R. Walker. 2009. Therapeutic manipulation of glucocorticoid metabolism in cardiovascular disease. Br. J. Pharmacol. 156: 689-712.
14. Rosenstock, J., S. Banarer, V. A. Fonseca, S. E. Inzucchi, W. Sun, W. Yao, G. Hollis, R. Flores, R. Levy, W. V. Williams, et al. 2010. The 11β-hydroxysteroid dehydrogenase type 1 inhibitor INCB13739 improves hyperglycemia in patients with type 2 diabetes inadequately controlled by metformin monotherapy. Diabetes Care. 33: 1516-1522.
15. Thomas, M. P., and B. V. L. Potter. 2011. Crystal structures of 11β- hydroxysteroid dehydrogenase type 1 and their use in drug discovery. Future Med. Chem. 3: 367-390.
16. Tiganescu, A., A. A. Tahrani, S. A. Morgan, M. Otranto, A. Desmouliere, L. Abrahams, Z. Hassan-Smith, E. A. Walker, E. H. Rabbitt, M. S. Cooper, et al. 2013. 11β-Hydroxysteroid dehydrogenase blockade prevents age-induced skin structure and function defects. J. Clin. Invest. 123: 3051-3060.
17. Gathercole, L. L., G. G. Lavery, S. A. Morgan, M. S. Cooper, A. J. Sinclair, J. W. Tomlinson, and P. M. Stewart. 2013. 11β-Hydroxysteroid dehydrogenase 1: translational and therapeutic aspects. Endocr. Rev. 34: 525-555.
18. Harno, E., and A. White. 2010. Will treating diabetes with 11β- HSD1 inhibitors affect the HPA axis? Trends Endocrinol. Metab. 21: 619-627.
19. Odermatt, A., and L. G. Nashev. 2010. The glucocorticoidactivating enzyme 11β-hydroxysteroid dehydrogenase type 1 has broad substrate specificity: Physiological and toxicological considerations. J. Steroid Biochem. Mol. Biol. 119: 1-13.
20. Muller, C., D. Pompon, P. Urban, and R. Morfin. 2006. Interconversion of 7α- and 7β-hydroxy-dehydroepiandrosterone by the human 11β-hydroxysteroid dehydrogenase type 1. J. Steroid Biochem. Mol. Biol. 99: 215-222.
21. Nashev, L. G., C. Chandsawangbhuwana, Z. Balazs, A. G. Atanasov, B. Dick, F. J. Frey, M. E. Baker, and A. Odermatt. 2007. Hexose-6-phosphate dehydrogenase modulates 11β-hydroxysteroid dehydrogenase type 1-dependent metabolism of 7-keto- and 7 -hydroxy-neurosteroids. PLoS ONE. 2: e561.
22. Hult, M., B. Elleby, N. Shafqat, S. Svensson, A. Rane, H. Jörnvall, L. Abrahmsen, and U. Oppermann. 2004. Human and rodent type 1 11β-hydroxysteroid dehydrogenases are 7β-hydroxycholesterol dehydrogenases involved in oxysterol metabolism. Cell. Mol. Life Sci. 61: 992-999.
23. Schweizer, R. A. S., M. Zürcher, Z. Balazs, B. Dick, and A. Odermatt. 2004. Rapid hepatic metabolism of 7-ketocholesterol by 11β-hydroxysteroid dehydrogenase type 1. J. Biol. Chem. 279: 18415-18424.
24. Hennebert, O., C. Pernelle, C. Ferroud, and R. Morfin. 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.
25. Hennebert, O., S. Le Mée, C. Pernelle, and R. Morfin. 2007. 5α- Androstane-3β, 7α, 17β-triol and 5α-androstane- 3β,7β,17β-triol as substrates for the human 11β- hydroxysteroid dehydrogenase type 1. Steroids. 72: 855-864.
26. Odermatt, A., T. Da Cunha, C. A. Penno, C. Chandsawangbhuwana, C. Reichert, A. Wolf, M. Dong, and M. E. Baker. 2011. Hepatic reduction of the secondary bile acid 7-oxolithocholic acid is mediated by 11beta-hydroxysteroid dehydrogenase 1. Biochem. J. 436: 621-629.
27. Fukiya, S., M. Arata, H. Kawashima, D. Yoshida, M. Kaneko, K. Minamida, J. Watanabe, Y. Ogura, K. Uchida, K. Itoh, 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.
28. Macdonald, I. A., C. N. Williams, D. E. Mahony, and W. M. Christie. 1975. NAD- and NADP-dependent 7alpha-hydroxysteroid dehydrogenases from bacteroides fragilis. Biochim. Biophys. Acta. 384: 12-24.
29. Arampatzis, S., B. Kadereit, D. Schuster, Z. Balazs, R. A. S. Schweizer, F. J. Frey, T. Langer, and A. Odermatt. 2005. Comparative enzymology of 11β-hydroxysteroid dehydrogenase type 1 from six species. J. Mol. Endocrinol. 35: 89-101.
30. Odermatt, A., P. Arnold, A. Stauffer, B. M. Frey, and F. J. Frey. 1999. The N-terminal anchor sequences of 11β-hydroxysteroid dehydrogenases determine their orientation in the endoplasmic reticulum membrane. J. Biol. Chem. 274: 28762-28770.
31. Penno, C. A., D. Arsenijevic, T. Da Cunha, G. A. Kullak-Ublick, J-P. Montani, and A. Odermatt. 2013. Quantification of multiple bile acids in uninephrectomized rats using ultra-performance liquid chromatography- tandem mass spectrometry. Anal. Methods. 5: 1155-1164.
32. Senesi, S., B. Legeza, Z. Balázs, M. Csala, P. Marcolongo, É. Kereszturi, P. Szelényi, C. Egger, R. Fulceri, J. Mandl, 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.
33. Lavery, G. G., A. E. Zielinska, L. L. Gathercole, B. Hughes, N. Semjonous, P. Guest, K. Saqib, M. Sherlock, G. Reynolds, S. A. Morgan, et al. 2012. Lack of significant metabolic abnormalities in mice with liver-specific disruption of 11β-hydroxysteroid dehydrogenase type 1. Endocrinology. 153: 3236-3248.
34. Verdonk, M. L., J. C. Cole, M. J. Hartshorn, C. W. Murray, and R. D. Taylor. 2003. Improved protein-ligand docking using GOLD. Proteins. 52: 609-623.
35. Jones, G., P. Willett, R. C. Glen, A. R. Leach, and R. Taylor. 1997. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267: 727-748.
36. Berman, H. M., J. Westbrook, Z. Feng, G. Gililand, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28: 235-242.
37. Wu, X., K. Kavanagh, S. Svensson, B. Elleby, M. Hult, F. Von Delft, B. Marsden, H. Jornvall, L. Abrahmsen, and U. Oppermann. The high resolution structures of human, murine and guinea pig 11β-hydroxysteroid dehydrogenase type 1 reveal critical differences in active site architecture. [no journal] Epub ahead of print. 2004;doi: 10.2210/pdb2bel/pdb.
38. Cheng, H., J. Hoffman, P. Le, S. K. Nair, S. Cripps, J. Matthews, C. Smith, M. Yang, S. Kupchinsky, K. Dress, et al. 2010. The development and SAR of pyrrolidine carboxamide 11β-HSD1 inhibitors. Bioorg. Med. Chem. Lett. 20: 2897-2902.
39. Clarke, J. L., and P. J. Mason. 2003. Murine hexose-6-phosphate dehydrogenase: a bifunctional enzyme with broad substrate specificity and 6-phosphogluconolactonase activity. Arch. Biochem. Biophys. 415: 229-234.
40. Meyer, A., A. Vuorinen, A. E. Zielinska, T. Da Cunha, P. Strajhar, G. G. Lavery, D. Schuster, and A. Odermatt. 2013. Carbonyl reduction of triadimefon by human and rodent 11β-hydroxysteroid dehydrogenase 1. Biochem. Pharmacol. 85: 1370-1378.
41. Hermanowski-Vosatka, A., J. M. Balkovec, K. Cheng, H. Y. Chen, M. Hernandez, G. C. Koo, C. B. Le Grand, Z. Li, J. M. Metzger, S. S. Mundt, et al. 2005. 11β-HSD1 inhibition ameliorates metabolic syndrome and prevents progression of atherosclerosis in mice. J. Exp. Med. 202: 517-527.
42. Tint, G. S., G. R. Xu, A. K. Batta, S. Shefer, W. Niemann, and G. Salen. 1990. Ursodeoxycholic acid, chenodeoxycholic acid, and 7-ketolithocholic acid are primary bile acids of the guinea pig. J. Lipid Res. 31: 1301-1306.
43. Oppermann, U. C., C. Filling, K. D. Berndt, B. Persson, J. Benach, R. Ladenstein, and H. Jornvall. 1997. Active site directed mutagenesis of 3β/17β-hydroxysteroid dehydrogenase establishes differential effects on short-chain dehydrogenase/reductase reactions. Biochemistry. 36: 34-40.
44. Kavanagh, K. L., H. Jornvall, B. Persson, and U. Oppermann. 2008. Medium- and short-chain dehydrogenase/reductase gene and protein families: the SDR superfamily: functional and structural diversity within a family of metabolic and regulatory enzymes. Cell. Mol. Life Sci. 65: 3895-3906.
45. Harris, H. J., Y. Kotelevtsev, J. J. Mullins, J. R. Seckl, and M. C. Holmes. 2001. Intracellular regeneration of glucocorticoids by 11β-hydroxysteroid dehydrogenase (11β-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11β-HSD-1-deficient mice. Endocrinology. 142: 114-120.
46. Carter, R. N., J. M. Paterson, U. Tworowska, D. J. Stenvers, J. J. Mullins, J. R. Seckl, and M. C. Holmes. 2009. Hypothalamicpituitary- adrenal axis abnormalities in response to deletion of 11β- HSD1 is strain-dependent. J. Neuroendocrinol. 21: 879-887.
47. Abrahams, L., N. M. Semjonous, P. Guest, A. Zielinska, B. Hughes, G. G. Lavery, and P. M. Stewart. 2012. Biomarkers of hypothalamicpituitary- adrenal axis activity in mice lacking 11β-HSD1 and H6PDH. J. Endocrinol. 214: 367-372.
48. Semjonous, N. M., M. Sherlock, P. Jeyasuria, K. L. Parker, E. A. Walker, P. M. Stewart, and G. G. Lavery. 2011. Hexose-6-phosphate dehydrogenase contributes to skeletal muscle homeostasis independent of 11β- hydroxysteroid dehydrogenase type 1. Endo crinology. 152: 93-102.
49. Rogoff, D., J. W. Ryder, K. Black, Z. Yan, S. C. Burgess, D. R. McMillan, and P. C. White. 2007. Abnormalities of glucose homeostasis and the hypothalamic-pituitary-adrenal axis in mice lacking hexose-6-phosphate dehydrogenase. Endocrinology. 148: 5072-5080.
50. Salen, G., D. Verga, A. Batta, G. Tint, and S. Shefer. 1982. Effect of 7-ketolithocholic acid on bile acid metabolism in humans. Gastroenterology. 83: 341-347.
51. Makishima, M., T. T. Lu, W. Xie, G. K. Whitfield, H. Domoto, R. M. Evans, M. R. Haussler, and D. J. Mangelsdorf. 2002. Vitamin D receptor as an intestinal bile acid sensor. Science. 296: 1313-1316.
52. Garcia-Canaveras, J. C., M. T. Donato, J. V. Castell, and A. Lahoz. 2012. Targeted profiling of circulating and hepatic bile acids in human, mouse and rat using an UPLC-MRM-MS-validated method. J. Lipid Res. 53: 2231-2241.
53. Guertin, F., A. Loranger, G. Lepage, C. C. Roy, I. M. Yousef, N. Domingo, F. Chanussot, H. Lafont, and B. Tuchweber. 1995. Bile formation and hepatic plasma membrane composition in guineapigs and rats. Comp. Biochem. Physiol. B. 111: 523-531.
54. Cowles, R. L., J-Y. Lee, D. D. Gallaher, C. L. Stuefer-Powell, and T. P. Carr. 2002. Dietary stearic acid alters gallbladder bile acid composition in hamsters fed cereal-based diets. J. Nutr. 132: 3119-3122.
55. Washizu, T., I. Tomoda, and J. J. Kaneko. 1991. Serum bile acid composition of the dog, cow, horse and human. J. Vet. Med. Sci. 53: 81-86.