Luteinizing hormone stimulates mammalian target of rapamycin signaling in bovine luteal cells via pathways independent of AKT and mitogen-activated protein kinase: Modulation of glycogen synthase kinase 3 and AMP-activated protein kinase

Endocrinology

Volumn 151, Issue 6, 2010, Pages 2846-2857

  Hou, Xiaoying ^a,b   Arvisais, Edward W ^b   Davis, John S ^a,b,c  

^a VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

^b Olson Center for Women's Health   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC AMP; FORSKOLIN; GLYCOGEN SYNTHASE KINASE 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 4E BINDING PROTEIN 1; LUTEINIZING HORMONE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE; PROTEIN KINASE B; RAPAMYCIN; S6 KINASE; ANDROSTANE DERIVATIVE; CYCLIC AMP; ENZYME INHIBITOR; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; WORTMANNIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; LUTEAL CELL; NONHUMAN; PRIORITY JOURNAL; PROGESTERONE RELEASE; PROGESTERONE SYNTHESIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CATTLE; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; IMMUNOPRECIPITATION; METABOLISM; PHOSPHORYLATION; PREGNANCY; RADIOIMMUNOASSAY; WESTERN BLOTTING;

AMP-ACTIVATED PROTEIN KINASES; ANDROSTADIENES; ANIMALS; BLOTTING, WESTERN; CATTLE; CELLS, CULTURED; CYCLIC AMP; ENZYME INHIBITORS; FEMALE; GLYCOGEN SYNTHASE KINASE 3; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEAL CELLS; LUTEINIZING HORMONE; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PREGNANCY; PROGESTERONE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RADIOIMMUNOASSAY; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 77954517914     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-1032     Document Type: Article

References (75)

1. Berisha B, Schams D 2005 Ovarian function in ruminants. Domest Anim Endocrinol 29:305-317
2. Davis JS, Rueda BR 2002 The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci 7:d1949-d1978
3. Stocco C, Telleria C, Gibori G 2007 The molecular control of corpus luteum formation, function, and regression. Endocr Rev 28:117-149
4. Marsh JM 1976 The role of cyclic AMP in gonadal steroidogenesis. Biol Reprod 14:30-53
5. Niswender GD 2002 Molecular control of luteal secretion of progesterone. Reproduction 123:333-339
6. Ascoli M, Fanelli F, Segaloff DL 2002 The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev 23:141-174
7. Chin EC, Abayasekara DR 2004 Progesterone secretion by luteinizing human granulosa cells: a possible cAMP-dependent but PKAindependent mechanism involved in its regulation. J Endocrinol 183: 51-60
8. Davis JS 1994 Mechanisms of hormone action: luteinizing hormone receptors and second-messenger pathways. Curr Opin Obstet Gynecol 6:254-261
9. Needle E, Piparo K, Cole D, Worrall C, Whitehead I, Mahon G, Goldsmith LT 2007 Protein kinase A-independent cAMP stimulation of progesterone in a luteal cell model is tyrosine kinase dependent but phosphatidylinositol-3-kinase and mitogen-activated protein kinase independent. Biol Reprod 77:147-155
10. Salvador LM, Maizels E, Hales DB, Miyamoto E, Yamamoto H, Hunzicker-Dunn M 2002 Acute signaling by the LH receptor is independent of protein kinase C activation. Endocrinology 143: 2986-2994
11. Christenson LK, Devoto L 2003 Cholesterol transport and steroidogenesis by the corpus luteum. Reprod Biol Endocrinol 1:90
12. Agca C, Ries JE, Kolath SJ, Kim JH, Forrester LJ, Antoniou E, Whitworth KM, Mathialagan N, Springer GK, Prather RS, Lucy MC 2006 Luteinization of porcine preovulatory follicles leads to systematic changes in follicular gene expression. Reproduction 132: 133-145
13. Bogan RL, Murphy MJ, Stouffer RL, Hennebold JD 2008 Systematic determination of differential gene expression in the primate corpus luteum during the luteal phase of the menstrual cycle. Mol Endocrinol 22:1260-1273
14. Priyanka S, Jayaram P, Sridaran R, Medhamurthy R 2009 Genomewide gene expression analysis reveals a dynamic interplay between luteotropic and luteolytic factors in the regulation of corpus luteum function in the bonnet monkey (Macaca radiata). Endocrinology 150:1473-1484
15. Xu J, Stouffer RL, Searles RP, Hennebold JD 2005 Discovery of LH-regulated genes in the primate corpus luteum. Mol Hum Reprod 11:151-159
16. Yadav VK, Muraly P, Medhamurthy R 2004 Identification of novel genes regulated by LH in the primate corpus luteum: insight into their regulation during the late luteal phase. Mol Hum Reprod 10: 629-639
17. Proud CG 2007 Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403: 217-234
18. Inoki K, Corradetti MN, Guan KL 2005 Dysregulation of the TSCmTOR pathway in human disease. Nat Genet 37:19-24
19. Martin DE, Hall MN 2005 The expanding TOR signaling network. Curr Opin Cell Biol 17:158-166
20. Wullschleger S, Loewith R, Hall MN 2006 TOR signaling in growth and metabolism. Cell 124:471-484
21. Guertin DA, Sabatini DM 2007 Defining the role of mTOR in cancer. Cancer Cell 12:9-22
22. Yang Q, Guan KL 2007 Expanding mTOR signaling. Cell research 17:666-681
23. Jacinto E, Loewith R, Schmidt A, Lin S, Rüegg MA, Hall A, Hall MN 2004 Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6:1122-1128
24. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument- Bromage H, Tempst P, Sabatini DM 2004 Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14: 1296-1302
25. Dancey JE 2006 Therapeutic targets:MTORand related pathways. Cancer Biol Ther 5:1065-1073
26. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM 2006 Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22:159-168
27. Li Y, Corradetti MN, Inoki K, Guan KL 2004 TSC2: filling the GAP in the mTOR signaling pathway. Trends Biochem Sci 29:32-38
28. Alam H, Maizels ET, Park Y, Ghaey S, Feiger ZJ, Chandel NS, Hunzicker-Dunn M 2004 Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/ AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. J Biol Chem 279: 19431-19440
29. Kayampilly PP, Menon KM 2007 Follicle-stimulating hormone increases tuberin phosphorylation and mammalian target of rapamycin signaling through an extracellular signal-regulated kinasedependent pathway in rat granulosa cells. Endocrinology 148: 3950-3957
30. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO, Guan KL 2006 TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell 126:955-968
31. Sugden PH, Fuller SJ, Weiss SC, Clerk A 2008 Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis. Br J Pharmacol 153(Suppl 1):S137-S153
32. Fang X, Yu SX, Lu Y, Bast Jr RC, Woodgett JR, Mills GB 2000 Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci USA 97:11960-11965
33. Roy L, McDonald CA, Jiang C, Maroni D, Zeleznik AJ, Wyatt TA, Hou X, Davis JS 2009 Convergence of 3′,5′-cyclic adenosine 5′- monophosphate/protein kinase A and glycogen synthase kinase-3β/ β-catenin signaling in corpus luteum progesterone synthesis. Endocrinology 150:5036-5045
34. Hurley RL, Barré LK, Wood SD, Anderson KA, Kemp BE, Means AR, Witters LA 2006 Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem 281:36662-36672
35. Chakravorty A, Joslyn MI, Davis JS 1993 Characterization of insulin and insulin-like growth factor-I actions in the bovine luteal cell: regulation of receptor tyrosine kinase activity, phosphatidylinositol- 3-kinase, and deoxyribonucleic acid synthesis. Endocrinology 133: 1331-1340
36. Chen D, Fong HW, Davis JS 2001 Induction of c-fos and c-jun messenger ribonucleic acid expression by prostaglandin F2α is mediated by a protein kinase C-dependent extracellular signal-regulated kinase mitogen-activated protein kinase pathway in bovine luteal cells. Endocrinology 142:887-895
37. Arvisais EW, Romanelli A, Hou X, Davis JS 2006 AKT-independent phosphorylation of TSC2 and activation of mTOR and ribosomal protein S6 kinase signaling by prostaglandin F2α. J Biol Chem 281: 26904-26913
38. Holz MK, Ballif BA, Gygi SP, Blenis J 2005 mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569-580
39. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument- Bromage H, Tempst P, Sabatini DM 2002 mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163-175
40. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr SA, Sabatini DM 2007 PRAS 40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol Cell 25:903-915
41. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J 2004 Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 101:13489-13494
42. Cohen P, Goedert M 2004 GSK3 inhibitors: development and therapeutic potential. Nat Rev 3:479-487
43. Kahn BB, Alquier T, Carling D, Hardie DG 2005 AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15-25
44. Tee AR, Blenis J 2005 mTOR, translational control and human disease. Semin Cell Dev Biol 16:29-37
45. Inoki K, Zhu T, Guan KL 2003 TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590
46. Fumagalli S, Thomas G 2000 S6 phosphorylation and signal transduction. In: Sonenberg N, Hershey JWB, Mathews MB, eds. Translational control of gene expression. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 695-717
47. Martin KA, Blenis J 2002 Coordinate regulation of translation by the PI 3-kinase and mTOR pathways. Adv Cancer Res 86:1-39
48. Meyuhas O, Hornstein E 2000 Translational control of TOP mRNAs. In: Sonenberg N, Hershey JWB, Mathews MB, eds. Translational control of gene expression. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 671-693
49. Hay N, Sonenberg N 2004 Upstream and downstream of mTOR. Genes Dev 18:1926-1945
50. Alessi DR, Kozlowski MT, Weng QP, Morrice N, Avruch J 1998 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr Biol 8:69-81
51. Pullen N, Thomas G 1997 The modular phosphorylation and activation of p70s6k. FEBS Lett 410:78-82
52. Schalm SS, Tee AR, Blenis J 2005 Characterization of a conserved C-terminal motif (RSPRR) in ribosomal protein S6 kinase 1 required for its mammalian target of rapamycin-dependent regulation. J Biol Chem 280:11101-11106
53. Dennis PB, Pullen N, Pearson RB, Kozma SC, Thomas G 1998 Phosphorylation sites in the autoinhibitory domain participate in p70(S6K) activation loop phosphorylation. J Biol Chem 273:14845-14852
54. Lécureuil C, Tesseraud S, Kara E, Martinat N, Sow A, Fontaine I, Gauthier C, Reiter E, Guillou F, Crépieux P 2005 Follicle-stimulating hormone activates p70 ribosomal protein S6 kinase by protein kinase A-mediated dephosphorylation of Thr 421/Ser 424 in primary Sertoli cells. Mol Endocrinol 19:1812-1820
55. Ahn JH, McAvoy T, Rakhilin SV, Nishi A, Greengard P, Nairn AC 2007 Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56δ subunit. Proc Natl Acad Sci USA 104:2979-2984
56. Flynn MP, Maizels ET, Karlsson AB, McAvoy T, Ahn JH, Nairn AC, Hunzicker-Dunn M 2008 Luteinizing hormone receptor activation in ovarian granulosa cells promotes protein kinase A-dependent dephosphorylation of microtubule-associated protein 2D. Mol Endocrinol 22:1695-1710
57. Lin TA, Lawrence Jr JC 1996 Control of the translational regulators PHAS-I and PHAS-II by insulin and cAMP in 3T3-L1 adipocytes. J Biol Chem 271:30199-30204
58. Jenö P, Ballou LM, Novak-Hofer I, Thomas G 1988 Identification and characterization of a mitogen-activated S6 kinase. Proc Natl Acad Sci USA 85:406-410
59. Ferrari S, Thomas G 1994 S6 phosphorylation and the p70S6K/ p85S6K. Crit Rev Biochem Mol Biol 29:385-413
60. Jefferies HB, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, Thomas G 1997 Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J 16:3693-3704
61. Terada N, Patel HR, Takase K, Kohno K, Nairn AC, Gelfand EW 1994 Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc Natl Acad Sci USA 91:11477-11481
62. Stolovich M, Tang H, Hornstein E, Levy G, Cohen R, Bae SS, Birnbaum MJ, Meyuhas O 2002 Transduction of growth or mitogenic signals into translational activation of TOP mRNAs is fully reliant on the phosphatidylinositol 3-kinase-mediated pathway but requires neither S6K1 nor rpS6 phosphorylation. Mol Cell Biol 22: 8101-8113
63. Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M 2006 S6K1- and βTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 314: 467-471
64. Gingras AC, Raught B, Sonenberg N 2001 Regulation of translation initiation by FRAP/mTOR. Genes Dev 15:807-826
65. Richter JD, Sonenberg N 2005 Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433:477-480
66. Hansel W, Alila HW, Dowd JP, Milvae RA 1991 Differential origin and control mechanisms in small and large bovine luteal cells. J Reprod Fertil Suppl 43:77-89
67. Meyer GT, Bruce NW 1980 Quantitative cell changes and vascularisation in the early corpus luteum of the pregnant rat. Anat Rec 197:369-374
68. Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW 2000 Mechanisms controlling the function and life span of the corpus luteum. Physiol Rev 80:1-29
69. Oliveira SM, Ehtisham J, Redwood CS, Ostman-Smith I, Blair EM, Watkins H 2003 Mutation analysis of AMP-activated protein kinase subunits in inherited cardiomyopathies: implications for kinase function and disease pathogenesis. J Mol Cell Cardiol 35:1251-1255
70. Tosca L, Chabrolle C, Uzbekova S, 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
71. Tosca L, Froment P, Solnais P, Ferré P, Foufelle F, Dupont J 2005 Adenosine 5′-monophosphate-activated protein kinase regulates progesterone secretion in rat granulosa cells. Endocrinology 146: 4500-4513
72. Hardie DG 2008 AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 32(Suppl 4):S7-S12
73. 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
74. Payne AH, Hales DB 2004 Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947-970
75. González-Fernández R, Martínez-Galisteo E, Gaytán F, Bárcena JA, Sánchez-Criado JE 2008 Changes in the proteome of functional and regressing corpus luteum during pregnancy and lactation in the rat. Biol Reprod 79:100-114