Extracellular signal-regulated kinase, Jun N-terminal kinase, p38, and c-Src are involved in gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone follicle-stimulating hormone β-subunit promoter

Endocrinology

Volumn 145, Issue 5, 2004, Pages 2228-2244

  Bonfil, David ^a   Chuderland, Dana ^a   Kraus, Sarah ^b   Shahbazian, David ^a   Friedberg, Ilan ^a   Seger, Rony ^b   Naor, Zvi ^a,c  

^a TEL AVIV UNIVERSITY   (Israel)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^c MRC Reproductive Biology Unit   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CALCIUM ION; FOLLITROPIN BETA SUBUNIT; GLYCOPROTEIN; GONADORELIN; IONOPHORE; ISOPROTEIN; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C ACTIVATOR; RAF PROTEIN; RAS PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR AP 1;

ARTICLE; DOWN REGULATION; ENZYME ACTIVITY; GENETIC TRANSFECTION; HORMONAL REGULATION; HORMONE ACTION; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; REPORTER GENE; SHEEP;

ANIMALS; BIOLOGICAL TRANSPORT; BUSERELIN; CALCIUM; CELL LINE; CELL NUCLEUS; DYNAMINS; ENZYME ACTIVATION; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GONADOTROPIN-RELEASING HORMONE; IONOMYCIN; IONOPHORES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE 4; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROMOTER REGIONS (GENETICS); PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; SHEEP; TETRADECANOYLPHORBOL ACETATE;

EID: 2042441750     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2003-1418     Document Type: Article

References (65)

1. Pierce JG, Parsons TF 1981 Glycoprotein hormones: structure and function. Annu Rev Biochem 50:465-495
2. Gharib SD, Wierman ME, Badger TM, Chin WW 1987 Sex steroid hormone regulation of follicle-stimulating hormone subunit messenger ribonucleic acid (mRNA) levels in the rat. J Clin Invest 80:294-299
3. Brown P, McNeilly AS 1999 Transcriptional regulation of pituitary gonadotrophin subunit genes. Rev Reprod 4:117-124
4. Counis R 2002 Gonadotropin biosynthesis. In: Neill J, Knobil E, eds. Encyclopedia of reproduction. Vol. 2. New York: Academic Press; 507-520
5. Naor Z 1990 Signal transduction mechanisms of Ca2+ mobilizing hormones: the case of gonadotropin-releasing hormone. Endocr Rev 11:326-353
6. Stojilkovic SS, Reinhart J, Catt KJ 1994 Gonadotropin-releasing hormone receptors: structure and signal transduction pathways. Endocr Rev 15:462-499
7. Mitchell R, Sim PJ, Leslie T, Johnson MS, Thomson FJ 1994 Activation of MAP kinase associated with the priming effect of LHRH. J Endocrinol 140:R15-R18
8. Roberson MS, Misra-Press A, Laurance ME, Stork PJ, Maurer RA 1995 A role for mitogen-activated protein kinase in mediating activation of the glycoprotein hormone α-subunit promoter by gonadotropin-releasing hormone. Mol Cell Biol 15:3531-3539
9. Sundaresan S, Colin IM, Pestell RG, Jameson JL 1996 Stimulation of mitogen-activated protein kinase by gonadotropin-releasing hormone: evidence for the involvement of protein kinase C. Endocrinology 137:304-311
10. Reiss N, Llevi LN, Shacham S, Harris D, Seger R, Naor Z 1997 Mechanism of mitogen-activated protein kinase activation by gonadotropin-releasing hormone in the pituitary of αT3-1 cell line: differential roles of calcium and protein kinase C. Endocrinology 138:1673-1682
11. Sealfon SC, Weinstein H, Millar RP 1997 Molecular mechanisms of ligand interaction with the gonadotropin-releasing hormone receptor. Endocr Rev 18:180-205
12. Naor Z 1997 GnRH receptor signaling: cross-talk of Ca2+ and protein kinase C. Eur J Endocrinol 136:123-127
13. Levi NL, Hanoch T, Benard O, Rozenblat M, Harris D, Reiss N, Naor Z, Seger R 1998 Stimulation of Jun N-terminal kinase (JNK) by gonadotropin- releasing hormone in pituitary αT3-1 cell line is mediated by protein kinase C, c-Src, and CDC42. Mol Endocrinol 12:815-824
14. Roberson MS, Zhang T, Li HL, Mulvaney JM 1999 Activation of the p38 mitogen-activated protein kinase pathway by gonadotropin-releasing hormone. Endocrinology 140:1310-1318
15. Mulvaney JM, Zhang T, Fewtrell C, Roberson MS 1999 Calcium influx through L-type channels is required for selective activation of extracellular signal-regulated kinase by gonadotropin-releasing hormone. J Biol Chem 274:29796-29804
16. Grosse R, Schmid A, Schoneberg T, Herrlich A, Muhn P, Schultz G, Gudermann T 2000 Gonadotropin-releasing hormone receptor initiates multiple signaling pathways by exclusively coupling to G(q/11) proteins. J Biol Chem 275:9193-9200
17. Mulvaney JM, Roberson MS 2000 Divergent signaling pathways requiring discrete calcium signals mediate concurrent activation of two mitogen-activated protein kinases by gonadotropin-releasing hormone. J Biol Chem 275:14182-14189
18. Naor Z, Benard O, Seger R 2000 Activation of MAPK cascades by G-protein-coupled receptors: the case of gonadotropin-releasing hormone receptor. Trends Endocrinol Metab 11:91-99
19. Shacham S, Harris D, Ben Shlomo H, Cohen I, Bonfil D, Przedecki F, Lewy H, Ashkenazi IE, Seger R, Naor Z 2001 Mechanism of GnRH receptor signaling on gonadotropin release and gene expression in pituitary gonadotrophs. Vitam Horm 63:63-90
20. Kraus S, Naor Z, Seger R 2001 Intracellular signaling pathways mediated by the gonadotropin-releasing hormone (GnRH) receptor. Arch Med Res 32:499-509
21. Pearson G, Robinson F, Beers GT, Xu BE, Karandikar M, Berman K, Cobb MH 2001 Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev 22:153-183
22. Yokoi T, Ohmichi M, Tasaka K, Kimura A, Kanda Y, Hayakawa J, Tahara M, Hisamoto K, Kurachi H, Murata Y 2000 Activation of the luteinizing hormone beta promoter by gonadotropin-releasing hormone requires c-Jun NH2-terminal protein kinase. J Biol Chem 275:21639-21647
23. Benard O, Naor Z, Seger R 2001 Role of dynamin, Src, and Ras in the protein kinase C-mediated activation of ERK by gonadotropin-releasing hormone. J Biol Chem 276:4554-4563
24. Kraus S, Benard O, Naor Z, Seger R 2003 c-SRC is activated by EGF-receptor in a pathway that mediates JNK and ERK activation by gonadotropin releasing hormone in COS-7 cell. J Biol Chem 278:32618-32630
25. Weck J, Fallest PC, Pitt LK, Shupnik MA 1998 Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways. Mol Endocrinol 12:451-457
26. Call GB, Wolfe MW 1999 Gonadotropin-releasing hormone activates the equine luteinizing hormone β-promoter through a protein kinase C/mitogen-activated protein kinase pathway. Biol Reprod 61:715-723
27. Harris D, Bonfil D, Chuderland D, Kraus S, Seger R, Naor Z 2002 Activation of MAPK cascades by GnRH: ERK and Jun N-terminal kinase are involved in basal and GnRH-stimulated activity of the glycoprotein hormone LHβ-subunit promoter. Endocrinology 143:1018-1025
28. Harris D, Chuderland D, Kraus S, Seger R, Naor Z 2003 Extracellular signal-regulated kinase (ERK) and c-Src, but not Jun N-terminal kinase (JNK), are involved in basal and GnRH-stimulated activity of the glycoprotein hormone α-subunit promoter. Endocrinology 144:612-622
29. Heckert LL, Schultz K, Nilson JH 1996 The cAMP response elements of the alpha subunit gene bind similar proteins in trophoblasts and gonadotropes but have distinct functional sequence requirements. J Biol Chem 271:31650-31656
30. Ben Menahem D, Naor Z 1994 Regulation of gonadotropin mRNA levels in cultured rat pituitary cells by gonadotropin-releasing hormone (GnRH): role for Ca2+ and protein kinase C. Biochemistry 33:3698-3704
31. Saunders BD, Sabbagh E, Chin WW, Kaiser UB 1998 Differential use of signal transduction pathways in the gonadotropin-releasing hormone-mediated regulation of gonadotropin subunit gene expression. Endocrinology 139:1835-1843
32. Vasilyev VV, Pernasetti F, Rosenberg SB, Barsoum MJ, Austin DA, Webster NJ, Mellon PL 2002 Transcriptional activation of the ovine follicle-stimulating hormone-beta gene by gonadotropin-releasing hormone involves multiple signal transduction pathways. Endocrinology 143:1651-1659
33. Haisenleder DJ, Cox ME, Parsons SJ, Marshall JC 1998 Gonadotropin- releasing hormone pulses are required to maintain activation of mitogen-activated protein kinase: role in stimulation of gonadotrope gene expression. Endocrinology 139:3104-3111
34. Liu F, Usui I, Evans LG, Austin DA, Mellon PL, Olefsky JM, Webster NJ 2002 Involvement of both Gq/11 and Gs proteins in gonadotropin-releasing hormone receptor-mediated signaling in LβT2 cells. J Biol Chem 277:32099-32108
35. Van Biesen T, Hawes BE, Luttrell DK, Krueger KM, Touhara K, Porfiri E, Sakaue M, Luttrell LM, Lefkowitz RJ 1995 Receptor-tyrosine-kinase- and Gβ γ-mediated MAP kinase activation by a common signalling pathway. Nature 376:781-784
36. Daub H, Weiss FU, Wallasch C, Ullrich A 1996 Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379:557-560
37. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A 1999 EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884-888
38. Pierce KL, Lefkowitz RJ 2001 Classical and new roles of β-arrestins in the regulation of G-protein-coupled receptors. Nat Rev Neurosci 2:727-733
39. Crespo P, Cachero TG, Xu N, Gutkind JS 1995 Dual effect of β-adrenergic receptors on mitogen-activated protein kinase. Evidence for a β γ-dependent activation and a Gα s-cAMP-mediated inhibition. J Biol Chem 270:25259-25265
40. Avidor-Reiss T, Nevo I, Levy R, Pfeuffer T, Vogel Z 1996 Chronic opioid treatment induces adenylyl cyclase V superactivation. Involvement of Gβγ. J Biol Chem 271:21309-21315
41. Ferguson SS, Downey III WE, Colapietro AM, Barak LS, Menard L, Caron MG 1996 Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 271:363-366
42. Daaka Y, Luttrell LM, Ahn S, Della Rocca GJ, Ferguson SS, Caron MG, Lefkowitz RJ 1998 Essential role for G protein-coupled receptor endocytosis in the activation of mitogen-activated protein kinase. J Biol Chem 273:685-688
43. Pierce KL, Tohgo A, Ahn S, Field ME, Luttrell LM, Lefkowitz RJ 2001 Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: a co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J Biol Chem 276:23155-23160
44. Pernasetti F, Vasilyev VV, Rosenberg SB, Bailey JS, Huang HJ, Miller WL, Mellon PL 2001 Cell-specific transcriptional regulation of follicle-stimulating hormone-β by activin and gonadotropin-releasing hormone in the LβT2 pituitary gonadotrope cell model. Endocrinology 142:2284-2295
45. Huang HJ, Sebastian J, Strahl BD, Wu JC, Miller WL 2001 The promoter for the ovine follicle-stimulating hormone-β gene (FSHβ) confers FSHβ-like expression on luciferase in transgenic mice: regulatory studies in vivo and in vitro. Endocrinology 142:2260-2266
46. Huang HJ, Sebastian J, Strahl BD, Wu JC, Miller WL 2001 Transcriptional regulation of the ovine follicle-stimulating hormone-β gene by activin and gonadotropin-releasing hormone (GnRH): involvement of two proximal activator protein-1 sites for GnRH stimulation. Endocrinology 142:2267-2274
47. Haisenleder DJ, Dalkin AC, Ortolano GA, Marshall JC, Shupnik MA 1991 A pulsatile gonadotropin-releasing hormone stimulus is required to increase transcription of the gonadotropin subunit genes: evidence for differential regulation of transcription by pulse frequency in vivo. Endocrinology 128:509-517
48. Kaiser UB, Sabbagh E, Saunders BD, Chin WW 1998 Identification of reacting deoxyribonudeic acid elements that mediate gonadotropin-releasing hormone stimulation of the rat luteinizing hormone β-subunit gene. Endocrinology 139:2443-2451
49. Ben Menahem D, Shraga Z, Lewy H, Limor R, Hammel I, Stein R, Naor Z 1992 Dissociation between release and gene expression of gonadotropin α-subunit in gonadotropin-releasing hormone-stimulated αT3-1 cell line. Biochemistry 31:12893-12898
50. Ben Menahem D, Shraga-Levine Z, Mellon PL, Naor Z 1995 Mechanism of action of gonadotropin-releasing hormone upon gonadotropin α-subunit mRNA levels in the αT3-1 cell line: role of Ca2+ and protein kinase C. Biochem J 309:325-329
51. Naor Z, Azrad A, Limor R, Zakut H, Lotan M 1986 Gonadotropin-releasing hormone activates a rapid Ca2+-independent phosphodiester hydrolysis of polyphosphoinositides in pituitary gonadotrophs. J Biol Chem 261:12506-12512
52. Harris D, Reiss N, Naor Z 1997 Differential activation of protein kinase Cδ and ε gene expression by gonadotropin-releasing hormone in αT3-1 cells. Autoregulation by protein kinase C. J Biol Chem 272:13534-13540
53. Turgeon JL, Kimura Y, Waring DW, Mellon PL 1996 Steroid and pulsatile gonadotropin-releasing hormone (GnRH) regulation of luteinizing hormone and GnRH receptor in a novel gonadotrope cell line. Mol Endocrinol 10:439-450
54. Thomas P, Mellon PL, Turgeon J, Waring DW 1996 The L βT2 clonal gonadotrope: a model for single cell studies of endocrine cell secretion. Endocrinology 137:2979-2989
55. Liu F, Austin DA, Mellon PL, Olefsky JM, Webster NJ 2002 GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells. Mol Endocrinol 16:419-434
56. Shah BH, Soh J-W, Catt KJ 2003 Dependence of gonadotropin-releasing hormone-induced neuronal MAPK signaling on epidermal growth factor receptor transactivation. J Biol Chem 278:2866-2875
57. Hamilton M, Liao J, Cathcart MK, Wolfman A 2001 Constitutive association of c-N-ras with c-raf-1 and protein kinase Cε in latent signaling modules. J Biol Chem 276:29079-29090
58. Miller WL, Shafiee-Kermani F, Strahl BD, Huang HJ 2002 The nature of FSH induction by GnRH. Trends Endocrinol Metab 13:257-263
59. Dalkin AC, Burger LL, Aylor KW, Haisenleder DJ, Workman LJ, Cho S, Marshall JC 2001 Regulation of gonadotropin subunit gene transcription by gonadotropin-releasing hormone: measurement of primary transcript ribonucleic acids by quantitative reverse transcription-polymerase chain reaction assays. Endocrinology 142:139-146
60. Weiss J, Crowley Jr WF, Halvorson LM, Jameson JL 1993 Perifusion of rat pituitary cells with gonadotropin-releasing hormone, activin, and inhibin reveals distinct effects on gonadotropin gene expression and secretion. Endocrinology 132:2307-2311
61. Coss D, Rosenberg SB, Bender CE, Mellon PL, GnRH induces the mouse FSHβ gene in LβT2 cells through overlapping AP1 and NFY binding sites. Program of the 84th Annual Meeting of The Endocrine Society, San Francisco, CA, 2002, p 187 (Abstract)
62. Rosenberg SB, Coss D, McGillivray, Mellon PL, Roles for SF-1 and NFY in the regulation of the mouse FSHβ gene in LβT2 cells. Program of the 84th Annual Meeting of The Endocrine Society, San Francisco, CA, p 187, 2002 (Abstract)
63. Halvorson LM, Kaiser UB, Chin WW 1999 The protein kinase C system acts through the early growth response protein 1 to increase LHβ gene expression in synergy with steroidogenic factor-1. Mol Endocrinol 13:106-116
64. Zakaria MM, Jeong K-H, Lacza C, Kaiser UB 2002 Pituitary homebox 1 activates the rat FSH (rFSHβ) gene through both direct and indirect interactions with the rFSHβ gene promoter. Mol Endocrinol 16:1840-1852
65. Coss D, Jacobs SBR, Bender CE, Mellon PL 2004 A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone β gene by gonadotropin-releasing hormone. J Biol Chem 279:152-162