Reactive oxygen species (ROS) play a critical role in the cAMP-induced activation of ras and the phosphorylation of ERK1/2 in leydig cells

Molecular Endocrinology

Volumn 25, Issue 5, 2011, Pages 885-893

  Ping, Tai ^a   Ascoli, Mario ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GLUTATHIONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVATION; LEYDIG CELL; MITOCHONDRIAL ENERGY TRANSFER; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACETYLCYSTEINE; ANIMALS; ANTIMYCIN A; CARBONYL CYANIDE M-CHLOROPHENYL HYDRAZONE; CELL LINE; CHORIONIC GONADOTROPIN; CYCLIC AMP; CYCLIC CMP; ENZYME ACTIVATION; GLUTATHIONE; LEYDIG CELLS; MALE; MICE; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; OLIGOMYCINS; PHOSPHORYLATION; PROGESTERONE; RAS PROTEINS; REACTIVE OXYGEN SPECIES; ROTENONE; UNCOUPLING AGENTS;

EID: 79955750716     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0489     Document Type: Article

References (49)

1. Hirakawa T, Ascoli M 2003 The lutropin/choriogonadotropin receptor (LHR)-induced phosphorylation of the extracellular signal regulated kinases (ERKs) in Leydig cells is mediated by a protein kinase A-dependent activation of Ras. Mol Endocrinol 17:2189-2200
2. Martinelle N, Holst M, Sö der O, Svechnikov K 2004 Extracellular signal-regulated kinases are involved in the acute activation of steroidogenesis in immature rat Leydig cells by human chorionic gonadotropin. Endocrinology 145:4629-4634
3. Evaul K, Hammes SR 2008 Cross-talk between G protein-coupled and epidermal growth factor receptors regulates gonadotropinmediated steroidogenesis in Leydig cells. J Biol Chem 283:27525-27533
4. Shiraishi K, Ascoli M 2007 Lutropin/choriogonadotropin (LH/CG) stimulate the proliferation of primary cultures of rat Leydig cells through a pathway that involves activation of the ERK1/2 cascade. Endocrinology 148:3214-3225
5. Manna PR, Huhtaniemi IT, Stocco DM 2009 Mechanisms of protein kinase C signaling in the modulation of 3,5-cyclic adenosine monophosphate-mediated steroidogenesis in mouse gonadal cells. Endocrinology 150:3308-3317
6. Tai P, Shiraishi K, Ascoli M 2009 Activation of the lutropin/choriogonadotropin receptor (LHR) inhibits apoptosis of immature Leydig cells in primary culture. Endocrinology 150:3766-3773
7. Shiraishi K, Ascoli M 2006 Activation of the lutropin/choriogonadotropin receptor (LHR) in MA-10 cells stimulates tyrosine kinase cascades that activate Ras and the extracellular signal regulated kinases (ERK1/2). Endocrinology 147:3419-3427
8. Galet C, Ascoli M 2008 Arrestin-3 is essential for the activation of Fyn by the luteinizing hormone receptor (LHR) in MA-10 cells. Cell Signal 20:1822-1829
9. Shiraishi K, Ascoli M 2008 A co-culture system reveals the involvement of intercellular pathways as mediators of the lutropin receptor (LHR)-stimulated ERK1/2 phosphorylation in Leydig cells. Exp Cell Res 314:25-37
10. Mizutani T, Shiraishi K, Welsh T, Ascoli M 2006 Activation of the lutropin/choriogonadotropin receptor (LHR) in MA-10 cells leads to the tyrosine phosphorylation of the focal adhesion kinase (FAK) by a pathway that involves Src family kinases. Mol Endocrinol 20:619-630
11. Swinnen JV, D'Souza B, Conti M, Ascoli M 1991 Attenuation of cAMP-mediated responses in MA-10 Leydig tumor cells by genetic manipulation of a cAMP-phosphodiesterase. J Biol Chem 266: 14383-14389
12. Ascoli M 2007 Immortalized Leydig cell lines as models for studying Leydig cell physiology. In: Payne AH, Hardy MP, eds. The Leydig cell in health and disease. New York: Humana Press; 373-392
13. Dyson MT, Kowalewski MP, Manna PR, Stocco DM 2009 The differential regulation of steroidogenic acute regulatory proteinmediated steroidogenesis by type I and type II PKA in MA-10 cells. Mol Cell Endocrinol 300:94-103
14. Manna PR, Dyson MT, Stocco DM 2009 Regulation of the steroidogenic acute regulatory protein gene expression: present and future perspectives. Mol Hum Reprod 15:321-333
15. Dexter RN, Fishman LM, Ney RL, Liddle GW 1967 Inhibition of adrenal corticosteroid synthesis by aminoglutethimide: studies on the mechanims of action. J Clin Endocrinol Metab 27:473-480
16. Ascoli M, Freeman DA, Sheets JJ, Vickery LE 1983 Inhibition of steroidogenesis in cultured Leydig tumor cells by 22-amino-23,24-Bisnor-5-Cholen-3β-Ol and (20R)20-phenyl-5-pregnene-3β20-diol. Endocrinology 113:127-132
17. Allen JA, Shankara T, Janus P, Buck S, Diemer T, Hales KH, Hales DB 2006 Energized, polarized, and actively respiring mitochondria are required for acute Leydig cell steroidogenesis. Endocrinology 147:3924-3935
18. Kadenbach B 2003 Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim Biophys Acta 1604:77-94
19. Brand MD, Affourtit C, Esteves TC, Green K, Lambert AJ, Miwa S, Pakay JL, Parker N 2004 Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins. Free Radic Biol Med 37:755-767
20. Storozhevykh TP, Senilova YE, Persiyantseva NA, Pinelis VG, Pomytkin IA 2007 Mitochondrial respiratory chain is involved in insulin-stimulated hydrogen peroxide production and plays an integral role in insulin receptor autophosphorylation in neurons. BMC Neurosci 8:84
21. Forman HJ 2010 Reactive oxygen species andα,β-unsaturated aldehydes as second messengers in signal transduction. Ann NY Acad Sci 1203:35-44
22. Holz GG, Chepurny OG, Schwede F 2008 Epac-selective cAMP analogs: New tools with which to evaluate the signal transductionproperties of cAMP-regulated guanine nucleotide exchange factors. Cell Signal 20:10-20
23. Gloerich M, Bos JL 2010 Epac: Defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50:355-375
24. Bedard K, Krause KH 2007 The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313
25. Chen H, Zhou L, Lin CY, Beattie MC, Liu J, Zirkin BR 2010 Effect of glutathione redox state on Leydig cell susceptibility to acute oxidative stress. Mol Cell Endocrinol 323:147-154
26. Hanukoglu I 2006 Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev 38:171-196
27. Veal EA, Day AM, Morgan BA 2007 Hydrogen peroxide sensing and signaling. Mol Cell 26:1-14
28. Cho SH, Lee CH, Ahn Y, Kim H, Kim H, Ahn CY, Yang KS, Lee SR 2004 Redox regulation of PTEN and protein tyrosine phosphatases in H2O2-mediated cell signaling. FEBS Lett 560:7-13
29. Tonks NK 2005 Redox redux: revisiting PTPs and the control of cell signaling. Cell 121:667-670
30. Lambert AJ, Brand MD 2009 Reactive oxygen species production by mitochondria. Methods Mol Biol 554:165-181
31. Livigni A, Scorziello A, Agnese S, Adornetto A, Carlucci A, Garbi C, Castaldo I, Annunziato L, Avvedimento EV, Feliciello A 2006 Mitochondrial AKAP121 links cAMP and src signaling to oxidative metabolism. Mol Biol Cell 17:263-271
32. Dyson MT, Jones JK, Kowalewski MP, Manna PR, Alonso M, Gottesman ME, Stocco DM 2008 Mitochondrial A-kinase anchoring protein 121 binds type II protein kinase A and enhances steroidogenic acute regulatory protein-mediated steroidogenesis in MA-10 mouse Leydig tumor cells. Biol Reprod 78:267-277
33. Stocco DM 2007 The role of StAR in Leydig cell steroidogenesis. In: Payne AH, Hardy MP, eds. The Leydig cell in health and disease. Totowa, NJ: Humana Press; 149-155
34. Carlucci A, Lignitto L, Feliciello A 2008 Control of mitochondria dynamics and oxidative metabolism by cAMP, AKAPs and the proteasome. Trends Cell Biol 18:604-613
35. Cullen PJ, Lockyer PJ 2002 Integration of calcium and Ras signaling. Nat Rev Mol Cell Biol 3:339-348
36. Buday L, Downward J 2008 Many faces of Ras activation. Biochim Biophys Acta 1786:178-187
37. Myers TJ, Brennaman LH, Stevenson M, Higashiyama S, Russell WE, Lee DC, Sunnarborg SW 2009 Mitochondrial reactive oxygen species mediate GPCR-induced TACE/ADAM17-dependent transforming growth factor- shedding. Mol Biol Cell 20:5236-5249
38. Diemer T, Allen JA, Hales KH, Hales DB 2003 Reactive oxygen disrupts mitochondria in MA-10 tumor Leydig cells and inhibits steroidogenic acute regulatory (StAR) Protein and steroidogenesis. Endocrinology 144:2882-2891
39. Chen H, Cangello D, Benson S, Folmer J, Zhu H, Trush MA, Zirkin BR 2001 Age-related increase in mitochondrial superoxide generation in the testosterone-producing cells of Brown Norway rat testes: relationship to reduced steroidogenic function? Exp Gerontol 36:1361-1373
40. Midzak AS, Chen H, Papadopoulos V, Zirkin BR 2009 Leydig cell aging and the mechanisms of reduced testosterone synthesis. Mol Cell Endocrinol 299:23-31
41. Ascoli M 1981 Characterization of several clonal lines of cultured Leydig tumor cells: gonadotropin receptors and steroidogenic responses. Endocrinology 108:88-95
42. Hirakawa T, Galet C, Ascoli M 2002 MA-10 cells transfected with the human lutropin/choriogonadotropin receptor (hLHR). A novel experimental paradigm to study the functional properties of the hLHR. Endocrinology 143:1026-1035
43. O'Shaughnessy PJ, Baker PJ, Heikkilä M, Vainio S, McMahon AP 2000 Localization of 17β-hydroxysteroid dehydrogenase/17-ketosteroid reductase isoform expression in the developing mouse testis-androstenedione is the major androgen secreted by fetal/neonatal Leydig cells. Endocrinology 141:2631-2637
44. Swinnen JV, Joseph DR, Conti M 1989 The mRNA encoding a high-affinity cAMP phosphodiesterase is regulated by hormones and cAMP. Proc Natl Acad Sci USA 86:8197-8201
45. van Triest M, Bos JL 2004 Pull-down assays for guanoside 5-triphosphate-bound Ras-like guanosine 5-triphosphatases. Methods Mol Biol 250:97-102
46. Levinthal DJ, Defranco DB 2005 Reversible oxidation of ERKdirected protein phosphatases drives oxidative toxicity in neurons. J Biol Chem 280:5875-5883
47. Laakko T, Juliano RL 2003 Adhesion regulation of stromal cellderived factor-1 activation of ERK in lymphocytes by phosphatases. J Biol Chem 278:31621-31628
48. Wardman P 2007 Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic Biol Med 43:995-1022
49. Fan J, Traore K, Li W, Amri H, Huang H, Wu C, Chen H, Zirkin B, Papadopoulos V 2010 Molecular mechanisms mediating the effect of mono-(2-ethylhexyl) phthalate on hormone-stimulated steroidogenesis in MA-10 mouse tumor Leydig Cells. Endocrinology 151: 3348-3362