Effect of 11β-hydroxysteroid dehydrogenase-1 inhibition on hepatic glucose metabolism in the conscious dog

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 5, 2010, Pages

  Edgerton, Dale S ^a   Basu, Rita ^b   Ramnanan, Christopher J ^a   Farmer, Tiffany D ^a   Neal, Doss ^a   Scott, Melanie ^a   Jacobson, Peer ^c   Rizza, Robert A ^b   Cherrington, Alan D ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Mayo Clinic   (United States)

^c ABBOTT LABORATORIES   (United States)

Author keywords

Cortisol; Endogenous glucose production; Glucocorticoids; Hepatic cortisol production

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; GLUCOSE 6 PHOSPHATASE; HYDROCORTISONE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); PLACEBO; SOMATOSTATIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; CONTROLLED STUDY; DOG; FEMALE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCOGENOLYSIS; INHIBITION KINETICS; INSULIN DEFICIENCY; LEAN BODY WEIGHT; LIPID METABOLISM; MALE; NONHUMAN; PRIORITY JOURNAL;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ANALYSIS OF VARIANCE; ANIMALS; DOGS; FEMALE; GLUCONEOGENESIS; GLUCOSE; HYDROCORTISONE; INSULIN; LIVER; MALE; RANDOM ALLOCATION; SOMATOSTATIN;

EID: 77950808186     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00740.2009     Document Type: Article

References (47)

1. Alberts P, Nilsson C, Selen G, Engblom LO, Edling NH, Norling S, Klingstrom G, Larsson C, Forsgren M, Ashkzari M, Nilsson CE, Fiedler M, Bergqvist E, Ohman B, Bjorkstrand E, Abrahmsen LB. Selective inhibition of 11 beta-hydroxysteroid dehydrogenase type 1 improves hepatic insulin sensitivity in hyperglycemic mice strains. Endocrinology 144: 4755-4762, 2003. (Pubitemid 37378389)
2. Andrew R, Smith K, Jones GC, Walker BR. Distinguishing the activities of 11beta-hydroxysteroid dehydrogenases in vivo using isotopically labeled cortisol. J Clin Endocrinol Metab 87: 277-285, 2002. (Pubitemid 34084702)
3. Andrews RC, Rooyackers O, Walker BR. Effects of the 11 betahydroxysteroid dehydrogenase inhibitor carbenoxolone on insulin sensitivity in men with type 2 diabetes. J Clin Endocrinol Metab 88: 285-291, 2003. (Pubitemid 36115179)
4. Basu R, Basu A, Grudzien M, Jung P, Jacobson P, Johnson M, Singh R, Sarr M, Rizza RA. Liver is the site of splanchnic cortisol production in obese nondiabetic humans. Diabetes 58: 39-45, 2009.
5. Basu R, Edgerton DS, Singh RJ, Cherrington A, Rizza RA. Splanchnic cortisol production in dogs occurs primarily in the liver: evidence for substantial hepatic specific 11beta hydroxysteroid dehydrogenase type 1 activity. Diabetes 55: 3013-3019, 2006. (Pubitemid 44923637)
6. Basu R, Singh RJ, Basu A, Chittilapilly EG, Johnson CM, Toffolo G, Cobelli C, Rizza RA. Splanchnic cortisol production occurs in humans: evidence for conversion of cortisone to cortisol via the 11-beta hydroxysteroid dehydrogenase (11beta-hsd) type 1 pathway. Diabetes 53: 2051-2059, 2004. (Pubitemid 38970754)
7. Brereton PS, van Driel RR, Suhaimi F, Koyama K, Dilley R, Krozowski Z. Light and electron microscopy localization of the 11beta-hydroxysteroid dehydrogenase type I enzyme in the rat. Endocrinology 142:1644-1651, 2001. (Pubitemid 32299695)
8. Dobbins RL, Davis SN, Neal DW, Cobelli C, Cherrington AD. Pulsatility does not alter the response to a physiological increment in glucagon in the conscious dog. Am J Physiol Endocrinol Metab 266: E467-E478, 1994. (Pubitemid 24115803)
9. Dunbar JC, Schultz S, Houser F, Walker J. Regulation of the hepatic response to glucagon: role of insulin, growth hormone and cortisol. Horm Res 31: 244-249, 1989. (Pubitemid 20002498)
10. Edgerton DS, Cardin S, Emshwiller M, Neal D, Chandramouli V, Schumann WC, Landau BR, Rossetti L, Cherrington AD. Small increases in insulin inhibit hepatic glucose production solely caused by an effect on glycogen metabolism. Diabetes 50: 1872-1882, 2001.
11. Edgerton DS, Jacobson PB, Opgenorth TJ, Zinker B, Beno D, von Geldern T, Ohman L, Scott M, Neal D, Cherrington AD. Selective antagonism of the hepatic glucocorticoid receptor reduces hepatic glucose production. Metabolism 55: 1255-1262, 2006.
12. Edgerton DS, Ramnanan CJ, Grueter CA, Johnson KM, Lautz M, Neal DW, Williams PE, Cherrington AD. Effects of insulin on the metabolic control of hepatic gluconeogenesis in vivo. Diabetes 58: 2766-2775, 2009.
13. Eigler N, Sacca L, Sherwin RS. Synergistic interactions of physiologic increments of glucagon, epinephrine, and cortisol in the dog: a model for stress-induced hyperglycemia. J Clin Invest 63: 114-123, 1979.
14. Goldstein RE, Abumrad NN, Lacy DB, Wasserman DH, Cherrington AD. Effects of an acute increase in epinephrine and cortisol on carbohydrate metabolism during insulin deficiency. Diabetes 44: 672-681, 1995.
15. Goldstein RE, Cherrington AD, Reed GW, Lacy DB, Wasserman DH, Abumrad NN. Effects of chronic hypercortisolemia on carbohydrate metabolism during insulin deficiency. Am J Physiol Endocrinol Metab 266: E618-E627, 1994.
16. Hermanowski-Vosatka A, Balkovec JM, Cheng K, Chen HY, Hernandez M, Koo GC, Le Grand CB, Li Z, Metzger JM, Mundt SS, Noonan H, Nunes CN, Olson SH, Pikounis B, Ren N, Robertson N, Schaeffer JM, Shah K, Springer MS, Strack AM, Strowski M, Wu K, Wu T, Xiao J, Zhang BB, Wright SD, Thieringer R. 11beta-HSD1 inhibition ameliorates metabolic syndrome and prevents progression of atherosclerosis in mice. J Exp Med 202: 517-527, 2005.
17. Hers HG, Hue L. Gluconeogenesis and related aspects of glycolysis. Annu Rev Biochem 52: 617-653, 1983.
18. Kotelevtsev Y, Holmes MC, Burchell A, Houston PM, Schmoll D, Jamieson P, Best R, Brown R, Edwards CR, Seckl JR, Mullins JJ. 11beta-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, 1997.
19. Lecavalier L, Bolli G, Gerich J. Glucagon-cortisol interactions on glucose turnover and lactate gluconeogenesis in normal humans. Am J Physiol Endocrinol Metab 258: E569-E575, 1990.
20. Liang Y, Osborne MC, Monia BP, Bhanot S, Watts LM, She P, DeCarlo SO, Chen X, Demarest K. Antisense oligonucleotides targeted against glucocorticoid receptor reduce hepatic glucose production and ameliorate hyperglycemia in diabetic mice. Metabolism 54: 848-855, 2005.
21. Lloyd B, Burrin J, Smythe P, Alberti KG. Enzymic fluorometric continuous-flow assays for blood glucose, lactate, pyruvate, alanine, glycerol, and 3-hydroxybutyrate. Clin Chem 24: 1724-1729, 1978.
22. Macfarlane DP, Forbes S, Walker BR. Glucocorticoids and fatty acid metabolism in humans: fuelling fat redistribution in the metabolic syndrome. J Endocrinol 197: 189-204, 2008.
23. Mari A. Estimation of the rate of appearance in the non-steady state with a two-compartment model. Am J Physiol Endocrinol Metab 263: E400-E415, 1992.
24. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, Flier JS. A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170, 2001.
25. Masuzaki H, Yamamoto H, Kenyon CJ, Elmquist JK, Morton NM, Paterson JM, Shinyama H, Sharp MG, Fleming S, Mullins JJ, Seckl JR, Flier JS. Transgenic amplification of glucocorticoid action in adipose tissue causes high blood pressure in mice. J Clin Invest 112: 83-90, 2003.
26. Moore MC, Satake S, Lautz M, Soleimanpour SA, Neal DW, Smith M, Cherrington AD. Nonesterified fatty acids and hepatic glucose metabolism in the conscious dog. Diabetes 53: 32-40, 2004.
27. Morton NM, Holmes MC, Fievet C, Staels B, Tailleux A, Mullins JJ, Seckl JR. Improved lipid and lipoprotein profile, hepatic insulin sensitivity, and glucose tolerance in 11beta-hydroxysteroid dehydrogenase type 1 null mice. J Biol Chem 276: 41293-41300, 2001.
28. Morton NM, Paterson JM, Masuzaki H, Holmes MC, Staels B, Fievet C, Walker BR, Flier JS, Mullins JJ, Seckl JR. Novel adipose tissuemediated resistance to diet-induced visceral obesity in 11 beta-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53: 931-938, 2004.
29. Nielsen MF, Caumo A, Chandramouli V, Schumann WC, Cobelli C, Landau BR, Vilstrup H, Rizza RA, Schmitz O. Impaired basal glucose effectiveness but unaltered fasting glucose release and gluconeogenesis during short-term hypercortisolemia in healthy subjects. Am J Physiol Endocrinol Metab 286: E102-E110, 2004.
30. Pagliassotti MJ, Holste LC, Moore MC, Neal DW, Cherrington AD. Comparison of the time courses of insulin and the portal signal on hepatic glucose and glycogen metabolism in the conscious dog. J Clin Invest 97:81-91, 1996. (Pubitemid 26021697)
31. Paterson JM, Morton NM, Fievet C, Kenyon CJ, Holmes MC, Staels B, Seckl JR, Mullins JJ. Metabolic syndrome without obesity: Hepatic overexpression of 11beta-hydroxysteroid dehydrogenase type 1 in transgenic mice. Proc Natl Acad Sci USA 101: 7088-7093, 2004. (Pubitemid 38596447)
32. Pilkis SJ, Granner DK. Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol 54: 885-909, 1992.
33. Plas C, Nunez J. Role of cortisol on the glycogenolytic effect of glucagon and on the glycogenic response to insulin in fetal hepatocyte culture. J Biol Chem 251: 1431-1437, 1976.
34. Quinkler M, Troeger H, Eigendorff E, Maser-Gluth C, Stiglic A, Oelkers W, Bähr V, Diederich S. Enhanced 11beta-hydroxysteroid dehydrogenase type 1 activity in stress adaptation in the guinea pig. J Endocrinol 176: 185-192, 2003. (Pubitemid 36284811)
35. Ricketts ML, Verhaeg JM, Bujalska I, Howie AJ, Rainey WE, Stewart PM. Immunohistochemical localization of type 1 11beta-hydroxysteroid dehydrogenase in human tissues. J Clin Endocrinol Metab 83: 1325-1335, 1998. (Pubitemid 28496416)
36. Samra JS, Clark ML, Humphreys SM, Macdonald IA, Matthews DR, Frayn KN. Effects of morning rise in cortisol concentration on regulation of lipolysis in subcutaneous adipose tissue. Am J Physiol Endocrinol Metab 271: E996-E1002, 1996. (Pubitemid 126815090)
37. Sandeep TC, Walker BR. Pathophysiology of modulation of local glucocorticoid levels by 11beta-hydroxysteroid dehydrogenases. Trends Endocrinol Metab 12: 446-453, 2001.
38. Satake S, Moore MC, Igawa K, Converse M, Farmer B, Neal DW, Cherrington AD. Direct and indirect effects of insulin on glucose uptake and storage by the liver. Diabetes 51: 1663-1671, 2002. (Pubitemid 34564276)
39. Schaeffer LD, Chenoweth M, Dunn A. Adrenal corticosteroid involvement in the control of liver glycogen phosphorylase activity. Biochim Biophys Acta 192: 292-303, 1969.
40. Schmoll D, Allan BB, Burchell A. Cloning and sequencing of the 5′ region of the human glucose-6-phosphatase gene: transcriptional regulation by cAMP, insulin and glucocorticoids in H4IIE hepatoma cells. FEBS Lett 383: 63-66, 1996. (Pubitemid 26092635)
41. Stewart PM, Boulton A, Kumar S, Clark PM, Shackleton CH. Cortisol metabolism in human obesity: impaired cortisone - >cortisol conversion in subjects with central adiposity. J Clin Endocrinol Metab 84: 1022-1027, 1999. (Pubitemid 29138237)
42. Stimson RH, Andersson J, Andrew R, Redhead DN, Karpe F, Hayes PC, Olsson T, Walker BR. Cortisol release from adipose tissue by 11beta-hydroxysteroid dehydrogenase type 1 in humans. Diabetes 58:46-53, 2009.
43. Stulnig TM, Waldhäusl W. 11beta-Hydroxysteroid dehydrogenase Type 1 in obesity and Type 2 diabetes. Diabetologia 47: 1-11, 2004. (Pubitemid 38141933)
44. Tomlinson JW, Sherlock M, Hughes B, Hughes SV, Kilvington F, Bartlett W, Courtney R, Rejto P, Carley W, Stewart PM. Inhibition of 11beta-hydroxysteroid dehydrogenase type 1 activity in vivo limits glucocorticoid exposure to human adipose tissue and decreases lipolysis. J Clin Endocrinol Metab 92: 857-864, 2007. (Pubitemid 46465655)
45. Tomlinson JW, Walker EA, Bujalska IJ, Draper N, Lavery GG, Cooper MS, Hewison M, Stewart PM. 11beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr Rev 25: 831-866, 2004. (Pubitemid 39366049)
46. Walker BR. Extra-adrenal regeneration of glucocorticoids by 11betahydroxysteroid dehydrogenase type 1: physiological regulator and pharmacological target for energy partitioning. Proc Nutr Soc 66: 1-8, 2007.
47. Watts LM, Manchem VP, Leedom TA, Rivard AL, McKay RA, Bao D, Neroladakis T, Monia BP, Bodenmiller DM, Cao JX, Zhang HY, Cox AL, Jacobs SJ, Michael MD, Sloop KW, Bhanot S. Reduction of hepatic and adipose tissue glucocorticoid receptor expression with antisense oligonucleotides improves hyperglycemia and hyperlipidemia in diabetic rodents without causing systemic glucocorticoid antagonism. Diabetes 54: 1846-1853, 2005.