Phosphoenolpyruvate carboxykinaseandglucose-6-phosphatase are required for steroidogenesis in testicular leydig cells

Journal of Biological Chemistry

Volumn 287, Issue 50, 2012, Pages 41875-41887

  Ahn, Seung Won ^a   Gang, Gil Tae ^b   Tadi, Surendar ^b   Nedumaran, Balachandar ^a   Kim, Yong Deuk ^a   Park, Ji Hoon ^b   Kweon, Gi Ryang ^b   Koo, Seung Hoi ^c   Lee, Keesook ^a   Ahn, Ryun Sup ^d   Yim, Yong Hyeon ^e   Lee, Chul Ho ^b   Harris, Robert A ^f   Choi, Hueng Sik ^a  

^a Chonnam National University   (South Korea)

^b Chungnam National University   (South Korea)

^c Sungkyunkwan University   (South Korea)

^d Graduate School of Complementary and Alternative Medicine   (South Korea)

^e Korea Research Institute of Standards and Science   (South Korea)

^f INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMP-ACTIVATED PROTEIN KINASE; CONSTITUTIVELY ACTIVES; COREPRESSORS; CYCLIC AMP (CAMP); GLUCOSE-6-PHOSPHATASE; LEYDIG CELLS; OVER-EXPRESSION; PHOSPHOENOLPYRUVATE CARBOXYKINASE; PHOSPHOENOLPYRUVATES; PROMOTER ACTIVITIES;

CELLS; CHEMICAL ACTIVATION; ENZYME ACTIVITY; MAMMALS; TRANSCRIPTION FACTORS;

ENZYME INHIBITION;

ADENOSINE TRIPHOSPHATE; CHORIONIC GONADOTROPIN; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GLUCOSE 6 PHOSPHATASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIVER RECEPTOR HOMOLOG 1; NUCLEAR RECEPTOR DAX 1; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TRANSCRIPTION FACTOR; CELL RECEPTOR; NR0B1 PROTEIN, HUMAN; NR0B1 PROTEIN, MOUSE; NR5A2 PROTEIN, HUMAN; NR5A2 PROTEIN, MOUSE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP);

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GLUCOSE 6 PHOSPHATASE GENE; HUMAN; HUMAN CELL; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PEPCK GENE; PRIORITY JOURNAL; PROMOTER REGION; PUBERTY; STEROIDOGENESIS; ANIMAL; BIOSYNTHESIS; CYTOLOGY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; METABOLISM; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CYCLIC AMP; DAX-1 ORPHAN NUCLEAR RECEPTOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE-6-PHOSPHATASE; HELA CELLS; HUMANS; LEYDIG CELLS; MALE; MICE; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PROMOTER REGIONS, GENETIC; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84871345637     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.421552     Document Type: Article

References (47)

1. Yánez, A. J., Nualart, F., Droppelmann, C., Bertinat, R., Brito, M., Concha, I. I., and Slebe, J. C. (2003) Broad expression of fructose-1,6-bisphosphatase and phosphoenolpyruvate carboxykinase provide evidence for gluconeogenesis in human tissues other than liver and kidney. J. Cell. Physiol. 197, 189-197 (Pubitemid 37485247)
2. Hanson, R. W., and Reshef, L. (2003) Glyceroneogenesis revisited. Biochimie 85, 1199-1205 (Pubitemid 38096343)
3. Pilkis, S. J., and Granner, D. K. (1992) Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu. Rev. Physiol. 54, 885-909
4. Hanson, R. W., and Reshef, L. (1997) Regulation of phosphoenolpyruvate carboxykinase (GTP) gene expression. Annu. Rev. Biochem. 66, 581-611 (Pubitemid 27274668)
5. Shaywitz, A. J., and Greenberg, M. E. (1999) CREB. A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861 (Pubitemid 29449210)
6. Lalli, E., and Alonso, J. (2010) Targeting DAX-1 in embryonic stem cells and cancer. Expert Opin. Ther. Targets 14, 169-177
7. Nedumaran, B., Hong, S., Xie, Y. B., Kim, Y. H., Seo, W. Y., Lee, M. W., Lee, C. H., Koo, S. H., and Choi, H. S. (2009) DAX-1 acts as a novel corepressor of orphan nuclear receptor HNF4α and negatively regulates gluconeogenic enzyme gene expression. J. Biol. Chem. 284, 27511-27523
8. Stocco, D. M., Wang, X., Jo, Y., and Manna, P. R. (2005) Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression. More complicated than we thought. Mol. Endocrinol. 19, 2647-2659 (Pubitemid 41577240)
9. 2O) induces orphan nuclear receptor Nur77 gene expression and increases steroidogenesis in mouse testicular Leydig cells. Mol. Cells 26, 74-80
10. Sewer, M. B., and Waterman, M. R. (2002) cAMP-dependent transcription of steroidogenic genes in the human adrenal cortex requires a dual-specificity phosphatase in addition to protein kinase A. J. Mol. Endocrinol. 29, 163-174 (Pubitemid 34965754)
11. Clark, B. J., Ranganathan, V., and Combs, R. (2001) Steroidogenic acute regulatory protein expression is dependent upon post-translational effects of cAMP-dependent protein kinase A. Mol. Cell. Endocrinol. 173, 183-192 (Pubitemid 32153695)
12. Stocco, D. M., Clark, B. J., Reinhart, A. J., Williams, S. C., Dyson, M., Dassi, B., Walsh, L. P., Manna, P. R., Wang, X. J., Zeleznik, A. J., and Orly, J. (2001) Elements involved in the regulation of the StAR gene. Mol. Cell. Endocrinol. 177, 55-59 (Pubitemid 32506805)
13. Song, K. H., Park, J. I., Lee, M. O., Soh, J., Lee, K., and Choi, H. S. (2001) LH induces orphan nuclear receptor Nur77 gene expression in testicular Leydig cells. Endocrinology 142, 5116-5123 (Pubitemid 33131937)
14. Freeman, D. A., and Ontko, J. A. (1992) Accumulation and mobilization of triglycerides and cholesteryl esters in Leydig tumor cells. J. Lipid Res. 33, 1139-1146
15. Song, K. H., Park, Y. Y., Park, K. C., Hong, C. Y., Park, J. H., Shong, M., Lee, K., and Choi, H. S. (2004) The atypical orphan nuclear receptor DAX-1 interacts with orphan nuclear receptor Nur77 and represses its transactivation. Mol. Endocrinol. 18, 1929-1940 (Pubitemid 39022610)
16. Rommerts, F. F., Cooke, B. A., Van der Kemp, J. W., and Van der Molen, H. J. (1973) Effect of luteinizing hormone on 3′,5′-cyclic AMP and testosterone production in isolated interstitial tissue of rat testis. FEBS Lett. 33, 114-118
17. Amrolia, P., Sullivan, M. H., Garside, D., Baldwin, S. A., and Cooke, B. A. (1988) An investigation of glucose uptake in relation to steroidogenesis in rat testis and tumour Leydig cells. Biochem. J. 249, 925-928 (Pubitemid 18042807)
18. Leiderman, B., and Mancini, R. E. (1969) Glycogen content in the rat testis from postnatal to adult ages. Endocrinology 85, 607-609
19. Chen, Y., Nagpal, M. L., and Lin, T. (2003) Expression and regulation of glucose transporter 8 in rat Leydig cells. J. Endocrinol. 179, 63-72 (Pubitemid 37321568)
20. Doege, H., Schürmann, A., Bahrenberg, G., Brauers, A., and Joost, H. G. (2000) GLUT8, a novel member of the sugar transport facilitator family with glucose transport activity. J. Biol. Chem. 275, 16275-16280 (Pubitemid 30366941)
21. Nehar, D., Mauduit, C., Boussouar, F., and Benahmed, M. (1998) Interleukin 1α stimulates lactate dehydrogenase A expression and lactate production in cultured porcine Sertoli cells. Biol. Reprod. 59, 1425-1432 (Pubitemid 28549859)
22. Hardie, D. G. (2004) The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 117, 5479-5487
23. Lizcano, J. M., Göransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Mäkelä, T. P., Hardie, D. G., and Alessi, D. R. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843 (Pubitemid 38418750)
24. Tosca, L., Chabrolle, C., Uzbekova, S., and Dupont, J. (2007) Effects of metformin on bovine granulosa cells steroidogenesis. Possible involvement of adenosine 5′-monophosphate-activated protein kinase (AMPK). Biol. Reprod. 76, 368-378
25. Lin, X., Takemori, H., Katoh, Y., Doi, J., Horike, N., Makino, A., Nonaka, Y., and Okamoto, M. (2001) Salt-inducible kinase is involved in the ACTH/cAMP-dependent protein kinase signaling in Y1 mouse adrenocortical tumor cells. Mol. Endocrinol. 15, 1264-1276 (Pubitemid 32703476)
26. Liang, T., Raugi, G. J., and Blum, J. J. (1976) Inhibition of P-enolpyruvate carboxykinase and of glyconeogenesis in Tetrahymena by 3-mercaptopicolinic acid. J. Protozool. 23, 473-477
27. Arion, W. J., Canfield, W. K., Ramos, F. C., Su, M. L., Burger, H. J., Hemmerle, H., Schubert, G., Below, P., and Herling, A. W. (1998) Chlorogenic acid analogue S 3483: a potent competitive inhibitor of the hepatic and renal glucose-6-phosphatase systems. Arch. Biochem. Biophys. 351, 279-285 (Pubitemid 28368637)
28. Hong, C. Y., Park, J. H., Ahn, R. S., Im, S. Y., Choi, H. S., Soh, J., Mellon, S. H., and Lee, K. (2004) Molecular mechanism of suppression of testicular steroidogenesis by proinflammatory cytokine tumor necrosis factor α. Mol. Cell. Biol. 24, 2593-2604 (Pubitemid 38381254)
29. Kim, Y. D., Park, K. G., Lee, Y. S., Park, Y. Y., Kim, D. K., Nedumaran, B., Jang, W. G., Cho, W. J., Ha, J., Lee, I. K., Lee, C. H., and Choi, H. S. (2008) Metformin inhibits hepatic gluconeogenesis through AMP-activated protein kinase-dependent regulation of the orphan nuclear receptor SHP. Diabetes 57, 306-314
30. Chakravarty, K., Leahy, P., Becard, D., Hakimi, P., Foretz, M., Ferre, P., Foufelle, F., and Hanson, R. W. (2001) Sterol regulatory element-binding protein-1c mimics the negative effect of insulin on phosphoenolpyruvate carboxykinase (GTP) gene transcription. J. Biol. Chem. 276, 34816-34823
31. Caron, K. M., Ikeda, Y., Soo, S. C., Stocco, D. M., Parker, K. L., and Clark, B. J. (1997) Characterization of the promoter region of the mouse gene encoding the steroidogenic acute regulatory protein. Mol. Endocrinol. 11, 138-147 (Pubitemid 27057427)
32. Chanda, D., Li, T., Song, K. H., Kim, Y. H., Sim, J., Lee, C. H., Chiang, J. Y., and Choi, H. S. (2009) Hepatocyte growth factor family negatively regulates hepatic gluconeogenesis via induction of orphan nuclear receptor small heterodimer partner in primary hepatocytes. J. Biol. Chem. 284, 28510-28521
33. Clem, B. F., Hudson, E. A., and Clark, B. J. (2005) Cyclic adenosine 3′,5′-monophosphate (cAMP) enhances cAMP-responsive element-binding (CREB) protein phosphorylation and phospho-CREB interaction with the mouse steroidogenic acute regulatory protein gene promoter. Endocrinology 146, 1348-1356 (Pubitemid 40289322)
34. Ascoli, M. (1981) Characterization of several clonal lines of cultured Leydig tumor cells. Gonadotropin receptors and steroidogenic responses. Endocrinology 108, 88-95
35. Inoue, Y., Kurihara, R., Tsuchida, A., Hasegawa, M., Nagashima, T., Mori, T., Niidome, T., Katayama, Y., and Okitsu, O. (2008) Efficient delivery of siRNA using dendritic poly(L-lysine) for loss-of-function analysis. J. Control Release 126, 59-66 (Pubitemid 351163418)
36. Koo, S. H., Flechner, L., Qi, L., Zhang, X., Screaton, R. A., Jeffries, S., Hedrick, S., Xu, W., Boussouar, F., Brindle, P., Takemori, H., and Montminy, M. (2005) The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 437, 1109-1111
37. Lee, J. M., Seo, W. Y., Song, K. H., Chanda, D., Kim, Y. D., Kim, D. K., Lee, M. W., Ryu, D., Kim, Y. H., Noh, J. R., Lee, C. H., Chiang, J. Y., Koo, S. H., and Choi, H. S. (2010) AMPK-dependent repression of hepatic gluconeogenesis via disruption of CREB·CRTC2 complex by orphan nuclear receptor small heterodimer partner. J. Biol. Chem. 285, 32182-32191
38. Chanda, D., Xie, Y. B., and Choi, H. S. (2010) Transcriptional corepressor SHP recruits SIRT1 histone deacetylase to inhibit LRH-1 transactivation. Nucleic Acids Res. 38, 4607-4619
39. Quinn, P. G., Wong, T. W., Magnuson, M. A., Shabb, J. B., and Granner, D. K. (1988) Identification of basal and cyclic AMP regulatory elements in the promoter of the phosphoenolpyruvate carboxykinase gene. Mol. Cell. Biol. 8, 3467-3475
40. Rommerts, F. F., van Roemburg, M. J., Lindh, L. M., Hegge, J. A., and van der Molen, H. J. (1982) The effects of short term culture and perifusion on LH-dependent steroidogenesis in isolated rat Leydig cells. J. Reprod. Fertil. 65, 289-297 (Pubitemid 12013217)
41. Kim, G. S., Lee, G. Y., Nedumaran, B., Park, Y. Y., Kim, K. T., Park, S. C., Lee, Y. C., Kim, J. B., and Choi, H. S. (2008) The orphan nuclear receptor DAX-1 acts as a novel transcriptional corepressor of PPARγ. Biochem. Biophys. Res. Commun. 370, 264-268
42. Wicks, W. D., and McKibbin, J. B. (1972) Evidence for translational regulation of specific enzyme synthesis by N6,O2′-dibutyryl cyclic AMP in hepatoma cell cultures. Biochem. Biophys. Res. Commun. 48, 205-211
43. Yang, J., Kalhan, S. C., and Hanson, R. W. (2009) What is the metabolic role of phosphoenolpyruvate carboxykinase? J. Biol. Chem. 284, 27025-27029
44. She, P., Shiota, M., Shelton, K. D., Chalkley, R., Postic, C., and Magnuson, M. A. (2000) Phosphoenolpyruvate carboxykinase is necessary for the integration of hepatic energy metabolism. Mol. Cell. Biol. 20, 6508-6517 (Pubitemid 30650237)
45. Burgess, S. C., Hausler, N., Merritt, M., Jeffrey, F. M., Storey, C., Milde, A., Koshy, S., Lindner, J., Magnuson, M. A., Malloy, C. R., and Sherry, A. D. (2004) Impaired tricarboxylic acid cycle activity in mouse livers lacking cytosolic phosphoenolpyruvate carboxykinase. J. Biol. Chem. 279, 48941-48949 (Pubitemid 39625775)
46. Moyle, W. R., and Armstrong, D. T. (1970) Stimulation of testosterone biosynthesis by luteinizing hormone in transplantable mouse Leydig cell tumors. Steroids 15, 681-693
47. Owen, O. E., Kalhan, S. C., and Hanson, R. W. (2002) The key role of anaplerosis and cataplerosis for citric acid cycle function. J. Biol. Chem. 277, 30409-30412 (Pubitemid 34970728)