Modification of microsomal 11β-HSD1 activity by cytosolic compounds: Glutathione and hexose phosphoesters

Journal of Steroid Biochemistry and Molecular Biology

Volumn 111, Issue 1-2, 2008, Pages 18-23

  McCormick, Kenneth L ^a   Wang, Xudong ^a   Mick, Gail J ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

11 Hydroxysteroid dehydrogenase; Glutathione; Hexose phosphates; Microsome; Redox

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; CORTICOSTERONE; CORTISONE; FRUCTOSE 6 PHOSPHATE; GLUCOCORTICOID; GLUTATHIONE; GLUTATHIONE REDUCTASE; HEXOSE PHOSPHATE; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; HEXOSE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSOL; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; LIVER MICROSOME; MALE; NONHUMAN; OBESITY; OXIDATION; OXIDATION REDUCTION REACTION; PROTEIN FUNCTION; RAT; SWINE; ANIMAL; ENZYMOLOGY; LIVER; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS; SUS;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANIMALS; CYTOSOL; GLUTATHIONE; HEXOSES; LIVER; MALE; MICROSOMES, LIVER; RATS; RATS, SPRAGUE-DAWLEY; SUS SCROFA;

EID: 47849106043     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2008.04.003     Document Type: Article

References (61)

1. Agarwal A.K., and Auchus R.J. Minireview: cellular redox state regulates hydroxysteroid dehydrogenase activity and intracellular hormone potency. Endocrinology 146 6 (2005) 2531-2538
2. Masuzaki H., Paterson J., Shinyama H., Morton N.M., Mullins J.J., Seckl J.R., and Flier J.S. A transgenic model of visceral obesity and the metabolic syndrome. Science 294 5549 (2001) 2166-2170
3. Lindsay R.S., Wake D.J., Nair S., Bunt J., Livingstone D.E., Permana P.A., Tataranni P.A., and Walker B.R. Subcutaneous adipose 11beta-hydroxysteroid dehydrogenase type 1 activity and messenger ribonucleic acid levels are associated with adiposity and insulinemia in Pima Indians and Caucasians. J. Clin. Endocrinol. Metab. 88 6 (2003) 2738-2744
4. Kotelevtsev Y., et al. 11beta-Hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc. Natl. Acad. Sci. U.S.A. 94 26 (1997) 14924-14929
5. Bujalska I.J., Kumar S., and Stewart P.M. Does central obesity reflect "Cushing's disease of the omentum"?. Lancet 349 9060 (1997) 1210-1213
6. Livingstone D.E., Jones G.C., Smith K., Jamieson P.M., Andrew R., Kenyon C.J., and Walker B.R. Understanding the role of glucocorticoids in obesity: tissue-specific alterations of corticosterone metabolism in obese Zucker rats. Endocrinology 141 2 (2000) 560-563
7. Tomlinson J.W., and Stewart P.M. The functional consequences of 11beta-hydroxysteroid dehydrogenase expression in adipose tissue. Horm. Metab. Res. 34 11-12 (2002) 746-751
8. Ozols J. Lumenal orientation and post-translational modifications of the liver microsomal 11beta-hydroxysteroid dehydrogenase. J. Biol. Chem. 270 17 (1995) 10360
9. Odermatt A., Atanasov A.G., Balazs Z., Schweizer R.A., Nashev L.G., Schuster D., and Langer T. Why is 11beta-hydroxysteroid dehydrogenase type 1 facing the endoplasmic reticulum lumen? Physiological relevance of the membrane topology of 11beta-HSD1. Mol. Cell. Endocrinol. 248 1-2 (2006) 15-23
10. Gerin I., and Van Schaftingen E. Evidence for glucose-6-phosphate transport in rat liver microsomes. FEBS Lett. 517 1-3 (2002) 257-260
11. St-Denis J.F., Berteloot A., Vidal H., Annabi B., and van de Werve G. Glucose transport and glucose-6-phosphate hydrolysis in intact rat liver microsomes. J. Biol. Chem. 270 36 (1995) 21092-21097
12. McCormick K.L., Wang X., and Mick G.J. Evidence that the 11beta-hydroxysteroid dehydrogenase (11beta-HSD1) is regulated by pentose pathway flux studies in rat adipocytes and microsomes. J. Biol. Chem. 281 1 (2006) 341-347
13. Takahashi T., and Hori S.H. Intramembraneous localization of rat liver microsomal hexose-6-phosphate dehydrogenase and membrane permeability to its substrates. Biochim. Biophys. Acta 524 2 (1978) 262-276
14. Atanasov A.G., Nashev L.G., Schweizer R.A., Frick C., and Odermatt A. Hexose-6-phosphate dehydrogenase determines the reaction direction of 11beta-hydroxysteroid dehydrogenase type 1 as an oxoreductase. FEBS Lett. 571 1-3 (2004) 129-133
15. Banhegyi G., Benedetti A., Fulceri R., and Senesi S. Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the lumen of the endoplasmic reticulum. J. Biol. Chem. 279 26 (2004) 27017-27021
16. Bujalska I.J., Draper N., Michailidou Z., Tomlinson J.W., White P.C., Chapman K.E., Walker E.A., and Stewart P.M. Hexose-6-phosphate dehydrogenase confers oxo-reductase activity upon 11 beta-hydroxysteroid dehydrogenase type 1. J. Mol. Endocrinol. 34 3 (2005) 675-684
17. Czegle I., Piccirella S., Senesi S., Csala M., Mandl J., Banhegyi G., Fulceri R., and Benedetti A. Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase is based on a common pyridine nucleotide pool in the lumen of the endoplasmic reticulum. Mol. Cell. Endocrinol. 248 1-2 (2006) 24-25
18. Hewitt K.N., Walker E.A., and Stewart P.M. Minireview: hexose-6-phosphate dehydrogenase and redox control of 11{beta}-hydroxysteroid dehydrogenase type 1 activity. Endocrinology 146 6 (2005) 2539-2543
19. Lavery G.G., Walker E.A., Draper N., Jeyasuria P., Marcos J., Shackleton C.H., Parker K.L., White P.C., and Stewart P.M. Hexose-6-phosphate dehydrogenase knock-out mice lack 11beta-hydroxysteroid dehydrogenase type 1-mediated glucocorticoid generation. J. Biol. Chem. 281 10 (2006) 6546-6551
20. Clarke J.L., and Mason P.J. Murine hexose-6-phosphate dehydrogenase: a bifunctional enzyme with broad substrate specificity and 6-phosphogluconolactonase activity. Arch. Biochem. Biophys. 415 2 (2003) 229-234
21. Marcolongo P., Piccirella S., Senesi S., Wunderlich L., Gerin I., Mandl J., Fulceri R., Banhegyi G., and Benedetti A. The glucose-6-phosphate transporter-hexose-6-phosphate dehydrogenase-11{beta}-hydroxysteroid dehydrogenase type 1 system of the adipose tissue. Endocrinology 148 5 (2007) 2487-2495
22. Casazza J.P., and Veech R.L. The content of pentose-cycle intermediates in liver in starved, fed ad libitum and meal-fed rats. Biochem. J. 236 3 (1986) 635-641
23. Raucy J.L., and Lasker J.M. Isolation of P450 enzymes from human liver. Methods Enzymol. 206 (1991) 577-587
24. Piccirella S., et al. Uncoupled redox systems in the lumen of the endoplasmic reticulum pyridine nucleotides stay reduced in an oxidative environment. J. Biol. Chem. 281 8 (2006) 4671-4677
25. Jessop C.E., and Bulleid N.J. Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J. Biol. Chem. 279 53 (2004) 55341-55347
26. 2+ sequestration are mutually enhanced in microsomes from liver, brain, and heart. Diabetes 47 6 (1998) 874-881
27. Arion W.J., Ballas L.M., Lange A.J., and Wallin B.K. Microsomal membrane permeability and the hepatic glucose-6-phosphatase system Interactions of the system with d-mannose 6-phosphate and d-mannose. J. Biol. Chem. 251 16 (1976) 4891-4897
28. Leuzzi R., Fulceri R., Marcolongo P., Banhegyi G., Zammarchi E., Stafford K., Burchell A., and Benedetti A. Glucose 6-phosphate transport in fibroblast microsomes from glycogen storage disease type 1b patients: evidence for multiple glucose 6-phosphate transport systems. Biochem. J. 357 Pt 2 (2001) 557-562
29. An J., Li Y., van De Werve G., and Newgard C.B. Overexpression of the P46 (T1) translocase component of the glucose-6-phosphatase complex in hepatocytes impairs glycogen accumulation via hydrolysis of glucose 1-phosphate. J. Biol. Chem. 276 14 (2001) 10722-10729
30. I.-B. Taljedal, Presence, induction and possible role of glucose 6-phosphatase in mammalian pancreatic islets. Biochem. J., 114 (2) (1969) 387-94.
31. Walker E.A., et al. 11beta-Hydroxysteroid dehydrogenase type 1 regulation by intracellular glucose 6-phosphate provides evidence for a novel link between glucose metabolism and hypothalamo-pituitary-adrenal axis function. J. Biol. Chem. 282 37 (2007) 27030-27036
32. Elliott S.S., Keim N.L., Stern J.S., Teff K., and Havel P.J. Fructose, weight gain, and the insulin resistance syndrome. Am. J. Clin. Nutr. 76 5 (2002) 911-922
33. Casazza J.P., and Veech R.L. The interdependence of glycolytic and pentose cycle intermediates in ad libitum fed rats. J. Biol. Chem. 261 2 (1986) 690-698
34. Mayes P. Intermediary metabolism of fructose. Am. J. Clin. Nutr. 58 5 (1993) 754S-765S
35. Wei Y., Wang D., and Pagliassotti M.J. Fructose selectively modulates c-jun N-terminal kinase activity and insulin signaling in rat primary hepatocytes. J. Nutr. 135 7 (2005) 1642-1646
36. Thresher J.S., Podolin D.A., Wei Y., Mazzeo R.S., and Pagliassotti M.J. Comparison of the effects of sucrose and fructose on insulin action and glucose tolerance. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 4 (2000) R1334-R1340
37. Sekar N., Li J., He Z., Gefel D., and Shechter Y. Independent signal-transduction pathways for vanadate and for insulin in the activation of glycogen synthase and glycogenesis in rat adipocytes. Endocrinology 140 3 (1999) 1125-1131
38. Sandeep T.C., Andrew R., Homer N.Z., Andrews R.C., Smith K., and Walker B.R. Increased in vivo regeneration of cortisol in adipose tissue in human obesity and effects of the 11beta-hydroxysteroid dehydrogenase type 1 inhibitor carbenoxolone. Diabetes 54 3 (2005) 872-879
39. Wake D.J., Homer N.Z., Andrew R., and Walker B.R. Acute in vivo regulation of 11beta-hydroxysteroid dehydrogenase type 1 activity by insulin and intralipid infusions in humans. J. Clin. Endocrinol. Metab. 91 11 (2006) 4682-4688
40. Ortmeyer H.K., and Bodkin N.L. Lack of defect in insulin action on hepatic glycogen synthase and phosphorylase in insulin-resistant monkeys. Am. J. Physiol. 274 6 Pt 1 (1998) G1005-G1010
41. Halimi S., Assimacopoulos-Jeannet F., Terrettaz J., and Jeanrenaud B. Differential effect of steady-state hyperinsulinaemia and hyperglycaemia on hepatic glycogenolysis and glycolysis in rats. Diabetologia 30 4 (1987) 268-272
42. Giaccari A., and Rossetti L. Predominant role of gluconeogenesis in the hepatic glycogen repletion of diabetic rats. J. Clin. Invest. 89 1 (1992) 36-45
43. Li Y., Mechin M.C., and van de Werve G. Diabetes affects similarly the catalytic subunit and putative glucose-6-phosphate translocase of glucose-6-phosphatase. J. Biol. Chem. 274 48 (1999) 33866-33868
44. Kalant N., Parniak M., and Lemieux M. Compartmentation of glucose 6-phosphate in hepatocytes. Biochem. J. 248 3 (1987) 927-931
45. Christ B., and Jungermann K. Sub-compartmentation of the 'cytosolic' glucose 6-phosphate pool in cultured rat hepatocytes. FEBS Lett. 221 2 (1987) 375-380
46. Romanelli A., St-Denis J.F., Vidal H., Tchu S., and van de Werve G. Absence of glucose uptake by liver microsomes: an explanation for the complete latency of glucose dehydrogenase. Biochem. Biophys. Res. Commun. 200 3 (1994) 1491-1497
47. Hwang C., Sinskey A.J., and Lodish H.F. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257 5076 (1992) 1496-1502
48. Banhegyi G., et al. Preferential transport of glutathione versus glutathione disulfide in rat liver microsomal vesicles. J. Biol. Chem. 274 18 (1999) 12213-12216
49. Lizak B., Czegle I., Csala M., Benedetti A., Mandl J., and Banhegyi G. Translocon pores in the endoplasmic reticulum are permeable to small anions. Am. J. Physiol. Cell Physiol. 291 3 (2006) C511-C517
50. Le Gall S., Neuhof A., and Rapoport T. The endoplasmic reticulum membrane is permeable to small molecules. Mol. Biol. Cell 15 2 (2004) 447-455
51. Hamman B.D., Chen J.C., Johnson E.E., and Johnson A.E. The aqueous pore through the translocon has a diameter of 40-60 A during cotranslational protein translocation at the ER membrane. Cell 89 4 (1997) 535-544
52. Polhuijs M., Lankhaar G., and Mulder G.J. Relationship between glutathione content in liver and glutathione conjugation rate in the rat in vivo. Effect of buthionine sulphoximine pretreatment on conjugation of the two 2-bromoisovalerylurea enantiomers during intravenous infusion. Biochem. J. 285 Pt 2 (1992) 401-404
53. Green R.M., Graham M., O'Donovan M.R., Chipman J.K., and Hodges N.J. Subcellular compartmentalization of glutathione: correlations with parameters of oxidative stress related to genotoxicity. Mutagenesis 21 6 (2006) 383-390
54. Browning J.D., and Horton J.D. Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114 2 (2004) 147-152
55. Furukawa S., et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 114 12 (2004) 1752-1761
56. Marfella R., Quagliaro L., Nappo F., Ceriello A., and Giugliano D. Acute hyperglycemia induces an oxidative stress in healthy subjects. J. Clin. Invest. 108 4 (2001) 635-636
57. Talior I., Tennenbaum T., Kuroki T., and Eldar-Finkelman H. PKC-delta-dependent activation of oxidative stress in adipocytes of obese and insulin-resistant mice: role for NADPH oxidase. Am. J. Physiol. Endocrinol. Metab. 288 2 (2005) E405-E411
58. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414 6865 (2001) 813-820
59. Kuroki T., Isshiki K., and King G.L. Oxidative stress: the lead or supporting actor in the pathogenesis of diabetic complications. J. Am. Soc. Nephrol. 14 8 Suppl. 3 (2003) S216-S220
60. Holt H.B., et al. Cortisol clearance and associations with insulin sensitivity, body fat and fatty liver in middle-aged men. Diabetologia 50 5 (2007) 1024-1032
61. Wake D.J., and Walker B.R. Inhibition of 11beta-hydroxysteroid dehydrogenase type 1 in obesity. Endocrine 29 1 (2006) 101-108