Biochemistry and physiology of hexose-6-phosphate knockout mice

Molecular and Cellular Endocrinology

Volumn 336, Issue 1-2, 2011, Pages 213-218

  Zielinska, Agnieszka E ^a   Walker, Elizabeth A ^a   Stewart, Paul M ^a   Lavery, Gareth G ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Endoplasmic reticulum; Glucocorticoid; Knockout mice; Metabolism; Muscle

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; GLUCOCORTICOID; GLUCOSE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

BIOCHEMISTRY; CORTICOSTEROID METABOLISM; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; ENZYME REGULATION; GLUCOSE HOMEOSTASIS; KNOCKOUT MOUSE; MOLECULAR MECHANICS; MOUSE; MUSCLE FUNCTION; MYOPATHY; NONHUMAN; OXIDATION REDUCTION STATE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; UNFOLDED PROTEIN RESPONSE;

ANIMALS; CARBOHYDRATE DEHYDROGENASES; ENDOPLASMIC RETICULUM; GLUCOCORTICOIDS; HUMANS; MICE; MICE, KNOCKOUT; MUSCULAR DISEASES; PHENOTYPE;

EID: 79952072191     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.12.004     Document Type: Review

References (54)

1. Al-Shanti N., Stewart C.E. Ca2+/calmodulin-dependent transcriptional pathways: potential mediators of skeletal muscle growth and development. Biol. Rev. Camb. Philos. Soc. 2009, 84:637-652.
2. Atanasov A.G., Nashev L.G., Gelman L., Legeza B., Sack R., Portmann R., Odermatt A. Direct protein-protein interaction of 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the endoplasmic reticulum lumen. Biochim. Biophys. Acta 2008, 1783:1536-1543.
3. Atanasov A.G., Nashev L.G., Schweizer R.A., Frick C., Odermatt A. Hexose-6-phosphate dehydrogenase determines the reaction direction of 11beta-hydroxysteroid dehydrogenase type 1 as an oxoreductase. FEBS Lett. 2004, 571:129-133.
4. Balazs Z., Nashev L.G., Chandsawangbhuwana C., Baker M.E., Odermatt A. Hexose-6-phosphate dehydrogenase modulates the effect of inhibitors and alternative substrates of 11beta-hydroxysteroid dehydrogenase 1. Mol. Cell. Endocrinol. 2009, 301:117-122.
5. Banhegyi G., Csala M., Benedetti A. Hexose-6-phosphate dehydrogenase: linking endocrinology and metabolism in the endoplasmic reticulum. J. Mol. Endocrinol. 2009, 42:283-289.
6. Biason-Lauber A., Suter S.L., Shackleton C.H., Zachmann M. Apparent cortisone reductase deficiency: a rare cause of hyperandrogenemia and hypercortisolism. Horm. Res. 2000, 53:260-266.
7. Bublitz C., Steavenson S. The pentose phosphate pathway in the endoplasmic reticulum. J. Biol. Chem. 1988, 263:12849-12853.
8. Bujalska I.J., Draper N., Michailidou Z., Tomlinson J.W., White P.C., Chapman K.E., Walker E.A., Stewart P.M. Hexose-6-phosphate dehydrogenase confers oxo-reductase activity upon 11 beta-hydroxysteroid dehydrogenase type 1. J. Mol. Endocrinol. 2005, 34:675-684.
9. Bujalska I.J., Hewitt K.N., Hauton D., Lavery G.G., Tomlinson J.W., Walker E.A., Stewart P.M. Lack of hexose-6-phosphate dehydrogenase impairs lipid mobilization from mouse adipose tissue. Endocrinology 2008, 149:2584-2591.
10. Bujalska I.J., Kumar S., Hewison M., Stewart P.M. Differentiation of adipose stromal cells: the roles of glucocorticoids and 11beta-hydroxysteroid dehydrogenase. Endocrinology 1999, 140:3188-3196.
11. Bujalska I.J., Kumar S., Stewart P.M. Does central obesity reflect Cushing's disease of the omentum?. Lancet 1997, 349:1210-1213.
12. Bujalska I.J., Walker E.A., Hewison M., Stewart P.M. A switch in dehydrogenase to reductase activity of 11 beta-hydroxysteroid dehydrogenase type 1 upon differentiation of human omental adipose stromal cells. J. Clin. Endocrinol. Metab. 2002, 87:1205-1210.
13. Carter R.N., Paterson J.M., Tworowska U., Stenvers D.J., Mullins J.J., Seckl J.R., Holmes M.C. Hypothalamic-pituitary-adrenal axis abnormalities in response to deletion of 11beta-HSD1 is strain-dependent. J. Neuroendocrinol. 2009, 21:879-887.
14. Chou J.Y., Matern D., Mansfield B.C., Chen Y.T. Type I glycogen storage diseases: disorders of the glucose-6-phosphatase complex. Curr. Mol. Med. 2002, 2:121-143.
15. Clarke J.L., Mason P.J. Murine hexose-6-phosphate dehydrogenase: a bifunctional enzyme with broad substrate specificity and 6-phosphogluconolactonase activity. Arch. Biochem. Biophys. 2003, 415:229-234.
16. Csala M., Banhegyi G., Benedetti A. Endoplasmic reticulum: a metabolic compartment. FEBS Lett. 2006, 580:2160-2165.
17. Czegle I., Piccirella S., Senesi S., Csala M., Mandl J., Banhegyi G., Fulceri R., 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. 2006, 248:24-25.
18. Draper N., Walker E.A., Bujalska I.J., Tomlinson J.W., Chalder S.M., Arlt W., Lavery G.G., Bedendo O., Ray D.W., Laing I., Malunowicz E., White P.C., Hewison M., Mason P.J., Connell J.M., Shackleton C.H., Stewart P.M. Mutations in the genes encoding 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase interact to cause cortisone reductase deficiency. Nat. Genet. 2003, 34:434-439.
19. Fraser R., Ingram M.C., Anderson N.H., Morrison C., Davies E., Connell J.M. Cortisol effects on body mass, blood pressure, and cholesterol in the general population. Hypertension 1999, 33:1364-1368.
20. Gathercole L.L., Stewart P.M. Targeting the pre-receptor metabolism of cortisol as a novel therapy in obesity and diabetes. J. Steroid Biochem. Mol. Biol. 2010, 122:21-27.
21. Harris H.J., Kotelevtsev Y., Mullins J.J., Seckl J.R., Holmes M.C. Intracellular regeneration of glucocorticoids by 11beta-hydroxysteroid dehydrogenase (11beta-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11beta-HSD-1-deficient mice. Endocrinology 2001, 142:114-120.
22. Hewitt K.N., Walker E.A., Stewart P.M. Minireview: hexose-6-phosphate dehydrogenase and redox control of 11β-hydroxysteroid dehydrogenase type 1 activity. Endocrinology 2005, 146:2539-2543.
23. Hotamisligil G.S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 2010, 140:900-917.
24. Jamieson A., Wallace A.M., Andrew R., Nunez B.S., Walker B.R., Fraser R., White P.C., Connell J.M. Apparent cortisone reductase deficiency: a functional defect in 11beta-hydroxysteroid dehydrogenase type 1. J. Clin. Endocrinol. Metab. 1999, 84:3570-3574.
25. Jang C., Obeyesekere V.R., Dilley R.J., Alford F.P., Inder W.J. 11Beta hydroxysteroid dehydrogenase type 1 is expressed and is biologically active in human skeletal muscle. Clin. Endocrinol. (Oxf.) 2006, 65:800-805.
26. Kotelevtsev Y., Holmes M.C., Burchell A., Houston P.M., Schmoll D., Jamieson P., Best R., Brown R., Edwards C.R., Seckl J.R., Mullins J.J. 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. 1997, 94:14924-14929.
27. Lavery G.G., Hauton D., Hewitt K.N., Brice S.M., Sherlock M., Walker E.A., Stewart P.M. Hypoglycemia with enhanced hepatic glycogen synthesis in recombinant mice lacking hexose-6-phosphate dehydrogenase. Endocrinology 2007, 148:6100-6106.
28. Lavery G.G., Walker E.A., Draper N., Jeyasuria P., Marcos J., Shackleton C.H., Parker K.L., White P.C., Stewart P.M. Hexose-6-phosphate dehydrogenase knock-out mice lack 11 beta-hydroxysteroid dehydrogenase type 1-mediated glucocorticoid generation. J. Biol. Chem. 2006, 281:6546-6551.
29. Lavery G.G., Walker E.A., Tiganescu A., Ride J.P., Shackleton C.H., Tomlinson J.W., Connell J.M., Ray D.W., Biason-Lauber A., Malunowicz E.M., Arlt W., Stewart P.M. Steroid biomarkers and genetic studies reveal inactivating mutations in hexose-6-phosphate dehydrogenase in patients with cortisone reductase deficiency. J. Clin. Endocrinol. Metab. 2008, 93:3827-3832.
30. Lavery G.G., Walker E.A., Turan N., Rogoff D., Ryder J.W., Shelton J.M., Richardson J.A., Falciani F., White P.C., Stewart P.M., Parker K.L., McMillan D.R. Deletion of hexose-6-phosphate dehydrogenase activates the unfolded protein response pathway and induces skeletal myopathy. J. Biol. Chem. 2008, 283:8453-8461.
31. Malunowicz E.M., Romer T.E., Urban M., Bossowski A. 11Beta-hydroxysteroid dehydrogenase type 1 deficiency ('apparent cortisone reductase deficiency') in a 6-year-old boy. Horm. Res. 2003, 59:205-210.
32. Mandl J., Meszaros T., Banhegyi G., Hunyady L., Csala M. Endoplasmic reticulum: nutrient sensor in physiology and pathology. Trends Endocrinol. Metab. 2009, 20:194-201.
33. Mason P.J., Stevens D., Diez A., Knight S.W., Scopes D.A., Vulliamy T.J. Human hexose-6-phosphate dehydrogenase (glucose 1-dehydrogenase) encoded at 1p36: coding sequence and expression. Blood Cells Mol. Dis. 1999, 25:30-37.
34. Masuzaki H., Paterson J., Shinyama H., Morton N.M., Mullins J.J., Seckl J.R., Flier J.S. A transgenic model of visceral obesity and the metabolic syndrome. Science 2001, 294:2166-2170.
35. Miclet E., Stoven V., Michels P.A., Opperdoes F.R., Lallemand J.Y., Duffieux F. NMR spectroscopic analysis of the first two steps of the pentose-phosphate pathway elucidates the role of 6-phosphogluconolactonase. J. Biol. Chem. 2001, 276:34840-34846.
36. Morton N.M. Obesity and corticosteroids: 11beta-hydroxysteroid type 1 as a cause and therapeutic target in metabolic disease. Mol. Cell. Endocrinol. 2010, 316:154-164.
37. Olson E.N., Williams R.S. Remodeling muscles with calcineurin. Bioessays 2000, 22:510-519.
38. Ozols J. Isolation and the complete amino acid sequence of lumenal endoplasmic reticulum glucose-6-phosphate dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:5302-5306.
39. Paterson J.M., Holmes M.C., Kenyon C.J., Carter R., Mullins J.J., Seckl J.R. Liver-selective transgene rescue of hypothalamic-pituitary-adrenal axis dysfunction in 11beta-hydroxysteroid dehydrogenase type 1-deficient mice. Endocrinology 2007, 148:961-966.
40. Phillipou G., Higgins B.A. A new defect in the peripheral conversion of cortisone to cortisol. J. Steroid Biochem. 1985, 22:435-436.
41. Phillipov G., Palermo M., Shackleton C.H. Apparent cortisone reductase deficiency: a unique form of hypercortisolism. J. Clin. Endocrinol. Metab. 1996, 81:3855-3860.
42. Piccirella S., Czegle I., Lizak B., Margittai E., Senesi S., Papp E., Csala M., Fulceri R., Csermely P., Mandl J., Benedetti A., Banhegyi G. Uncoupled redox systems in the lumen of the endoplasmic reticulum. Pyridine nucleotides stay reduced in an oxidative environment. J. Biol. Chem. 2006, 281:4671-4677.
43. Rogoff D., Black K., McMillan D.R., White P.C. Contribution of hexose-6-phosphate dehydrogenase to NADPH content and redox environment in the endoplasmic reticulum. Redox Rep. 2010, 15:64-70.
44. Rogoff D., Ryder J.W., Black K., Yan Z., Burgess S.C., McMillan D.R., White P.C. Abnormalities of glucose homeostasis and the hypothalamic-pituitary-adrenal axis in mice lacking hexose-6-phosphate dehydrogenase. Endocrinology 2007, 148:5072-5080.
45. Ryder J.W., Bassel-Duby R., Olson E.N., Zierath J.R. Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J. Biol. Chem. 2003, 278:44298-44304.
46. Saito A., Seiler S., Chu A., Fleischer S. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell Biol. 1984, 99:875-885.
47. Sawada H., Hara A., Hayashibara M., Nakayama T., Usui S., Saeki T. Microsomal reductase for aromatic aldehydes and ketones in guinea pig liver. Purification, characterization, and functional relationship to hexose-6-phosphate dehydrogenase. J. Biochem. 1981, 90:1077-1085.
48. Semjonous N.M., Sherlock M., Jeyasuria P., Parker K.L., Walker E.A., Stewart P.M., Lavery G.G. Hexose-6-phosphate dehydrogenase contributes to skeletal muscle homeostasis independent of 11-hydroxysteroid dehydrogenase type 1. Endocrinology 2010, November. (Epub ahead of print).
49. Senesi S., Csala M., Marcolongo P., Fulceri R., Mandl J., Banhegyi G., Benedetti A. Hexose-6-phosphate dehydrogenase in the endoplasmic reticulum. Biol. Chem. 2010, 391:1-8.
50. Sousa Peixoto R.A., Turban S., Battle J.H., Chapman K.E., Seckl J.R., Morton N.M. Preadipocyte 11beta-hydroxysteroid dehydrogenase type 1 is a keto-reductase and contributes to diet-induced visceral obesity in vivo. Endocrinology 2008, 149:1861-1868.
51. Sriburi R., Jackowski S., Mori K., Brewer J.W. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 2004, 167:35-41.
52. Szaraz P., Banhegyi G., Benedetti A. Altered redox state of luminal pyridine nucleotides facilitates the sensitivity towards oxidative injury and leads to endoplasmic reticulum stress dependent autophagy in HepG2 cells. Int. J. Biochem. Cell Biol. 2010, 42:157-166.
53. Walker B.R. Cortisol-cause and cure for metabolic syndrome?. Diabet. Med. 2006, 23:1281-1288.
54. Zhang Y.L., Zhong X., Gjoka Z., Li Y., Stochaj W., Stahl M., Kriz R., Tobin J.F., Erbe D., Suri V. H6PDH interacts directly with 11beta-HSD1: implications for determining the directionality of glucocorticoid catalysis. Arch. Biochem. Biophys. 2009, 483:45-54.