The microsomal enzyme 17β-hydroxysteroid dehydrogenase 3 faces the cytoplasm and uses NADPH generated by glucose-6-phosphate dehydrogenase

Endocrinology

Volumn 154, Issue 1, 2013, Pages 205-213

  Legeza, Balázs ^a   Balázs, Zoltán ^a   Nashev, Lyubomir G ^a   Odermatt, Alex ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYANDROSTENEDIONE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; ANTIBODY; DIGITONIN; GLUCOCORTICOID; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; PROTEINASE K; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL PERMEABILIZATION; CELL STRAIN HEK293; CYTOPLASM; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GLYCOSYLATION; HUMAN; HUMAN CELL; LEYDIG CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; 17-HYDROXYSTEROID DEHYDROGENASES; ANIMALS; CARBOHYDRATE DEHYDROGENASES; CELL LINE; CYTOPLASM; HUMANS; MALE; MICE; MICROSOMES; MODELS, BIOLOGICAL; NADP; PROTEIN BINDING;

EID: 84871694333     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1778     Document Type: Article

References (47)

1. Geissler WM, Davis DL, Wu L, Bradshaw KD, Patel S, Mendonca BB, Elliston KO, Wilson JD, Russell DW, Andersson S 1994 Male pseudohermaphroditism caused by mutations of testicular 17β-hydroxysteroid dehydrogenase 3. Nat Genet 7:34-39
2. Sha JA, Dudley K, Rajapaksha WR, O'Shaughnessy PJ 1997 Sequence of mouse 17β-hydroxysteroid dehydrogenase type 3 cDNA and tissue distribution of the type 1 and type 3 isoform mRNAs. J Steroid Biochem Mol Biol 60:19-24 (Pubitemid 27217239)
3. Mustonen MV, Poutanen MH, Isomaa VV, Vihko PT, Vihko RK 1997 Cloning of mouse 17β-hydroxysteroid dehydrogenase type 2, and analysing expression of the mRNAs for types 1, 2, 3, 4 and 5 in mouse embryos and adult tissues. Biochem J 325(Pt 1):199-205 (Pubitemid 27322704)
4. Andersson S, Geissler WM, Wu L, Davis DL, Grumbach MM, New MI, Schwarz HP, Blethen SL, Mendonca BB, Bloise W, Witchel SF, Cutler Jr GB, Griffin JE, Wilson JD, Russel DW 1996 Molecular genetics and pathophysiology of 17β-hydroxysteroid dehydrogenase 3 deficiency. J Clin Endocrinol Metab 81:130-136 (Pubitemid 26035013)
5. Nashev LG, Schuster D, Laggner C, Sodha S, Langer T, Wolber G, Odermatt A 2010 The UV-filter benzophenone-1 inhibits 17β-hydroxysteroid dehydrogenase type 3: virtual screening as a strategy to identify potential endocrine disrupting chemicals. Biochem Pharmacol 79:1189-1199
6. Lo S, Alléra A, Albers P, Heimbrecht J, Jantzen E, Klingmüller D, Steckelbroeck S 2003 Dithioerythritol (DTE) prevents inhibitory effects of triphenyltin (TPT) on the key enzymes of the human sex steroid hormone metabolism. J Steroid Biochem Mol Biol 84:569-576 (Pubitemid 36603324)
7. Ohno S, Nakajima Y, Nakajin S 2005 Triphenyltin and tributyltin inhibit pig testicular 17β-hydroxysteroid dehydrogenase activity and suppress testicular testosterone biosynthesis. Steroids 70:645-651 (Pubitemid 40909883)
8. Yuan K, Zhao B, Li XW, Hu GX, Su Y, Chu Y, Akingbemi BT, Lian QQ, Ge RS 2012 Effects of phthalates on 3β-hydroxysteroid dehydrogenase and 17β-hydroxysteroid dehydrogenase 3 activities in human and rat testes. Chem Biol Interact 195:180-188
9. Orr TE, Mann DR 1990 Effects of restraint stress on plasma LH and testosterone concentrations, Leydig cell LH/hCG receptors, and in vitro testicular steroidogenesis in adult rats. Horm Behav 24:324-341 (Pubitemid 20319011)
10. Orr TE, Mann DR 1992 Role of glucocorticoids in the stress-induced suppression of testicular steroidogenesis in adult male rats. Horm Behav 26:350-363
11. Fenster L, Katz DF, Wyrobek AJ, Pieper C, Rempel DM, Oman D, Swan SH 1997 Effects of psychological stress on human semen quality. J Androl 18:194-202 (Pubitemid 27204229)
12. Smals AG, Kloppenborg PW, Benraad TJ 1977 Plasma testosterone profiles in Cushing's syndrome. J Clin Endocrinol Metab 45:240-245 (Pubitemid 8162809)
13. Nakashima A, Koshiyama K, Uozumi T, Monden Y, Hamanaka Y 1975 Effects of general anaesthesia and severity of surgical stress on serum LH and testosterone in males. Acta Endocrinol (Copenh) 78:258-269
14. Monder C, Sakai RR, Miroff Y, Blanchard DC, Blanchard RJ 1994 Reciprocal changes in plasma corticosterone and testosterone in stressed male rats maintained in a visible burrow system: evidence for a mediating role of testicular 11β-hydroxysteroid dehydrogenase. Endocrinology 134:1193-1198
15. Hardy MP, Sottas CM, Ge R, McKittrick CR, Tamashiro KL, McEwen BS, Haider SG, Markham CM, Blanchard RJ, Blanchard DC, Sakai RR 2002 Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biol Reprod 67:1750-1755 (Pubitemid 35388004)
16. Orr TE, Taylor MF, Bhattacharyya AK, Collins DC, Mann DR 1994 Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17,20-lyase without affecting the binding of LH/hCG receptors. J Androl 15:302-308 (Pubitemid 24256643)
17. Hales DB, Payne AH 1989 Glucocorticoid-mediated repression of P450scc mRNA and de novo synthesis in cultured Leydig cells. Endocrinology 124:2099-2104 (Pubitemid 19132003)
18. Hu GX, Lian QQ, Lin H, Latif SA, Morris DJ, Hardy MP, Ge RS 2008 Rapid mechanisms of glucocorticoid signaling in the Leydig cell. Steroids 73:1018-1024
19. Latif SA, Shen M, Ge RS, Sottas CM, Hardy MP, Morris DJ 2011 Role of 11β-OH-C(19) and C(21) steroids in the coupling of 11β-HSD1 and 17β-HSD3 in regulation of testosterone biosynthesis in rat Leydig cells. Steroids 76:682-689
20. Odermatt A, Nashev LG 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
21. Balázs Z, Nashev LG, Chandsawangbhuwana C, Baker ME, Odermatt A 2009 Hexose-6-phosphate dehydrogenase modulates the effect of inhibitors and alternative substrates of 11β-hydroxysteroid dehydrogenase 1. Mol Cell Endocrinol 301:117-122
22. Jamieson PM, Chapman KE, Edwards CR, Seckl JR 1995 11β- Hydroxysteroid dehydrogenase is an exclusive 11β-reductase in primary cultures of rat hepatocytes: effect of physicochemical and hormonal manipulations. Endocrinology 136:4754-4761 (Pubitemid 3002167)
23. Thieringer R, Le Grand CB, Carbin L, Cai TQ, Wong B, Wright SD, Hermanowski-Vosatka A 2001 11β-Hydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J Immunol 167:30-35 (Pubitemid 32567757)
24. Ge RS, Hardy MP 2000 Initial predominance of the oxidative activity of type I 11β-hydroxysteroid dehydrogenase in primary rat Leydig cells and transfected cell lines. J Androl 21:303-310 (Pubitemid 30123712)
25. Leckie CM, Welberg LA, Seckl JR 1998 11β-Hydroxysteroid dehydrogenase is a predominant reductase in intact rat Leydig cells. J Endocrinol 159:233-238 (Pubitemid 28520175)
26. Ferguson SE, Pallikaros Z, Michael AE, Cooke BA 1999 The effects of different culture media, glucose, pyridine nucleotides and adenosine on the activity of 11β-hydroxysteroid dehydrogenase in rat Leydig cells. Mol Cell Endocrinol 158:37-44
27. Odermatt A, Arnold P, Stauffer A, Frey BM, Frey FJ 1999 The N-terminal anchor sequences of 11β-hydroxysteroid dehydrogenases determine their orientation in the endoplasmic reticulum membrane. J Biol Chem 274:28762-28770
28. Mziaut H, Korza G, Hand AR, Gerard C, Ozols J 1999 Targeting proteins to the lumen of endoplasmic reticulum using N-terminal domains of 11β-hydroxysteroid dehydrogenase and the 50-kDa esterase. J Biol Chem 274:14122-14129
29. Frick C, Atanasov AG, Arnold P, Ozols J, Odermatt A 2004 Appropriate function of 11β-hydroxysteroid dehydrogenase type 1 in the endoplasmic reticulum lumen is dependent on its N-terminal region sharing similar topological determinants with 50-kDa esterase. J Biol Chem 279:31131-31138 (Pubitemid 39037775)
30. Ozols J 1995 Lumenal orientation and post-translational modifications of the liver microsomal 11β-hydroxysteroid dehydrogenase. J Biol Chem 270:2305-2312
31. Atanasov AG, Nashev LG, Gelman L, Legeza B, Sack R, Portmann R, Odermatt A 2008 Direct protein-protein interaction of 11β-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the endoplasmic reticulum lumen. Biochim Biophys Acta 1783:1536-1543
32. Atanasov AG, Nashev LG, Schweizer RA, Frick C, Odermatt A 2004 Hexose-6-phosphate dehydrogenase determines the reaction direction of 11β-hydroxysteroid dehydrogenase type 1 as an oxoreductase. FEBS Lett 571:129-133 (Pubitemid 38992936)
33. Bánhegyi G, Benedetti A, Fulceri R, Senesi S 2004 Cooperativity between 11β-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the lumen of the endoplasmic reticulum. J Biol Chem 279:27017-27021 (Pubitemid 38812537)
34. Senesi S, Legeza B, Balázs Z, Csala M, Marcolongo P, Kereszturi E, Szelényi P, Egger C, Fulceri R, Mandl J, Giunti R, Odermatt A, Bánhegyi G, Benedetti A 2010 Contribution of fructose-6-phosphate to glucocorticoid activation in the endoplasmic reticulum: possible implication in the metabolic syndrome. Endocrinology 151:4830-4839
35. Mindnich R, Haller F, Halbach F, Moeller G, Hrabé de Angelis M, Adamski J 2005 Androgen metabolism via 17β-hydroxysteroid dehydrogenase type 3 in mammalian and non-mammalian vertebrates: comparison of the human and the zebrafish enzyme. J Mol Endocrinol 35:305-316 (Pubitemid 41556178)
36. Kozak M 1987 At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J Mol Biol 196:947-950
37. Ascoli M 1981 Regulation of gonadotropin receptors and gonadotropin responses in a clonal strain of Leydig tumor cells by epidermal growth factor. J Biol Chem 256:179-183 (Pubitemid 12207104)
38. Zhang M, Hu P, Napoli JL 2004 Elements in the N-terminal signaling sequence that determine cytosolic topology of short-chain dehydrogenases/ reductases: studies with retinol dehydrogenase type 1 and cis-retinol/androgen dehydrogenase type 1. J Biol Chem 279:51482-51489 (Pubitemid 40021773)
39. Lavery GG, Walker EA, Turan N, Rogoff D, Ryder JW, Shelton JM, Richardson JA, Falciani F, White PC, Stewart PM, Parker KL, McMillan DR 2008 Deletion of hexose-6-phosphate dehydrogenase activates the unfolded protein response pathway and induces skeletal myopathy. J Biol Chem 283:8453-8461
40. Semjonous NM, Sherlock M, Jeyasuria P, Parker KL, Walker EA, Stewart PM, Lavery GG 2011 Hexose-6-phosphate dehydrogenase contributes to skeletal muscle homeostasis independent of 11β-hydroxysteroid dehydrogenase type 1. Endocrinology 152:93-102
41. Lavery GG, Walker EA, Draper N, Jeyasuria P, Marcos J, Shackleton CH, Parker KL, White PC, Stewart PM 2006 Hexose-6-phosphate dehydrogenase knock-out mice lack 11β-hydroxysteroid dehydrogenase type 1-mediated glucocorticoid generation. J Biol Chem 281:6546-6551 (Pubitemid 43847588)
42. Draper N, Walker EA, Bujalska IJ, Tomlinson JW, Chalder SM, Arlt W, Lavery GG, Bedendo O, Ray DW, Laing I, Malunowicz E, White PC, Hewison M, Mason PJ, Connell JM, Shackleton CH, Stewart PM 2003 Mutations in the genes encoding 11β-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase interact to cause cortisone reductase deficiency. Nat Genet 34:434-439 (Pubitemid 36935337)
43. Skarydová L, Wsól V 2012 Human microsomal carbonyl reducing enzymes in the metabolism of xenobiotics: well-known and promising members of the SDR superfamily. Drug Metab Rev 44:173-191
44. Bray JE, Marsden BD, Oppermann U 2009 The human short-chain dehydrogenase/reductase (SDR) superfamily: a bioinformatics summary. Chem Biol Interact 178:99-109
45. Wang X, Walsh LP, Reinhart AJ, Stocco DM 2000 The role of arachidonic acid in steroidogenesis and steroidogenic acute regulatory (StAR) gene and protein expression. J Biol Chem 275:20204-20209 (Pubitemid 30441632)
46. Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP 2002 Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 143:130-138 (Pubitemid 34056411)
47. Gao HB, Tong MH, Hu YQ, You HY, Guo QS, Ge RS, Hardy MP 2003 Mechanisms of glucocorticoid-induced Leydig cell apoptosis. Mol Cell Endocrinol 199:153-163 (Pubitemid 36170299)