GnRH pulse frequency-dependent stimulation of FSHβ transcription is mediated via activation of PKA and CREB

Molecular Endocrinology

Volumn 27, Issue 4, 2013, Pages 606-618

  Thompson, Iain R ^a   Ciccone, Nick A ^a   Xu, Shuyun ^a   Zaytseva, Sofiya ^a   Carroll, Rona S ^a   Kaiser, Ursula B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FOLLITROPIN; GONADORELIN; LUTEINIZING HORMONE; RECOMBINANT FOLLITROPIN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; HYPOTHALAMUS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; GENE EXPRESSION REGULATION; GENES, DOMINANT; GONADOTROPIN-RELEASING HORMONE; MICE; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84875506273     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2012-1281     Document Type: Article

References (76)

1. Burger LL, Haisenleder DJ, Dalkin AC, Marshall JC. Regulation of gonadotropin subunit gene transcription. J Mol Endocrinol. 2004; 33:559-584.
2. Seminara SB, Hayes FJ, Crowley WF Jr. Gonadotropin-releasing hormone deficiency in the human (idiopathic hypogonadotropic hypogonadism and Kallmann's syndrome): pathophysiological and genetic considerations. Endocr Rev. 1998;19:521-539.
3. Ehrmann DA. Polycystic ovary syndrome. N Engl J Med. 2005;352: 1223-1236.
4. Blank SK, McCartney CR, Helm KD, Marshall JC. Neuroendocrine effects of androgens in adult polycystic ovary syndrome and female puberty. Semin Reprod Med. 2007;25:352-359.
5. Dunaif A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev. 1997; 18:774-800.
6. Hoffman LK, Ehrmann DA. Cardiometabolic features of polycystic ovary syndrome. Nat Clin Pract Endocrinol Metab. 2008;4:215- 222.
7. Gharib SD, Wierman ME, Shupnik MA, Chin WW. Molecular biology of the pituitary gonadotropins. Endocr Rev. 1990;11:177- 199.
8. Wildt L, Hausler A, Marshall G, et al. Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the rhesus monkey. Endocrinology. 1981;109:376-385.
9. Savoy-Moore RT, Swartz KH. Several GnRH stimulation frequencies differentially release FSH and LH from isolated, perfused rat anterior pituitary cells. Adv Exp Med Biol. 1987;219:641-645.
10. Dalkin AC, Haisenleder DJ, Ortolano GA, Ellis TR, Marshall JC. The frequency of gonadotropin-releasing-hormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression. Endocrinology. 1989;125:917-924.
11. Haisenleder DJ, Dalkin AC, Ortolano GA, Marshall JC, Shupnik MA. 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. 1991;128:509-517.
12. Weiss J, Duca KA, Crowley WF Jr. Gonadotropin-releasing hormone-induced stimulation and desensitization of free α-subunit secretion mirrors luteinizing hormone and follicle-stimulating hormone in perifused rat pituitary cells. Endocrinology 1990;127: 2364-2371.
13. Landy H, Boepple PA, Mansfield MJ, et al. Altered patterns of pituitary secretion and renal excretion of free α-subunit during gonadotropin-releasing hormone agonist-induced pituitary desensitization. J Clin Endocrinol Metab 1991;72:711-717.
14. Ciccone NA, Lacza CT, Hou MY, et al. A composite element that binds basic helix loop helix and basic leucine zipper transcription factors is important for gonadotropin-releasing hormone regulation of the follicle-stimulating hormone β gene. Mol Endocrinol. 2008;22:1908-1923.
15. Coss D, Jacobs SB, Bender CE, Mellon PL. A novel AP-1 site is critical for maximal induction of the follicle-stimulating hormone β gene by gonadotropin-releasing hormone. J Biol Chem. 2004;279: 152-162.
16. Wang Y, Fortin J, Lamba P, et al. Activator protein-1 and smad proteins synergistically regulate human follicle-stimulating hormone β-promoter activity. Endocrinology. 2008;149:5577-5591.
17. Ciccone NA, Xu S, Lacza CT, Carroll RS, Kaiser UB. Frequencydependent regulation of follicle-stimulating hormone β by pulsatile gonadotropin-releasing hormone is mediated by functional antagonism of bZIP transcription factors. Mol Cell Biol. 2010;30:1028- 1040.
18. Zakaria MM, Jeong KH, Lacza C, Kaiser UB. Pituitary homeobox 1 activates the rat FSHβ (rFSHβ) gene through both direct and indirect interactions with the rFSHβ gene promoter. Mol Endocrinol. 2002;16:1840-1852.
19. Kaiser UB, Sabbagh E, Katzenellenbogen RA, Conn PM, Chin WW. A mechanism for the differential regulation of gonadotropin subunit gene expression by gonadotropin-releasing hormone. Proc Natl Acad Sci USA. 1995;92:12280-12284.
20. Kaiser UB, Jakubowiak A, Steinberger A, Chin WW. Regulation of rat pituitary gonadotropin-releasing hormone receptor mRNA levels in vivo and in vitro. Endocrinology. 1993;133:931-934.
21. Kaiser UB, Jakubowiak A, Steinberger A, Chin WW. Differential effects of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro. Endocrinology. 1997;138:1224- 1231.
22. Bedecarrats GY, Kaiser UB. Differential regulation of gonadotropin subunit gene promoter activity by pulsatile gonadotropin-releasing hormone (GnRH) in perifused L β T2 cells: role of GnRH receptor concentration. Endocrinology. 2003;144:1802-1811.
23. Coss D, Hand CM, Yaphockun KK, Ely HA, Mellon PL. p38 mitogen-activated protein kinase is critical for synergistic induction of the FSH(β) gene by gonadotropin-releasing hormone and activin through augmentation of c-Fos induction and Smad phosphorylation. Mol Endocrinol. 2007;21:3071-3086.
24. Do MH, Santos SJ, Lawson MA. GNRH induces the unfolded protein response in the LβT2 pituitary gonadotrope cell line. Mol Endocrinol. 2009;23:100-112.
25. Zhang H, Bailey JS, Coss D, et al. Activin modulates the transcriptional response of LβT2 cells to gonadotropin-releasing hormone and alters cellular proliferation. Mol Endocrinol. 2006;20:2909- 2930.
26. Jakubowiak A, Janecki A, Steinberger A. Similar effects of inhibin and cycloheximide on gonadotropin release in superfused pituitary cell cultures. Biol Reprod. 1989;41:454-463.
27. Haisenleder DJ, Burger LL, Aylor KW, Dalkin AC, Marshall JC. Gonadotropin-releasing hormone stimulation of gonadotropin subunit transcription: evidence for the involvement of calcium/calmodulin-dependent kinase II (Ca/CAMK II) activation in rat pituitaries. Endocrinology. 2003;144:2768-2774.
28. Haisenleder DJ, Ferris HA, Shupnik MA. The calcium component of gonadotropin-releasing hormone-stimulated luteinizing hormone subunit gene transcription is mediated by calcium/calmodulin-dependent protein kinase type II. Endocrinology. 2003;144: 2409-2416.
29. Duan WR, Ito M, Park Y, Maizels ET, Hunzicker-Dunn M, Jameson JL. GnRH regulates early growth response protein 1 transcription through multiple promoter elements. Mol Endocrinol. 2002; 16:221-233.
30. Grafer CM, Thomas R, Lambrakos L, Montoya I, White S, Halvorson LM. GnRH stimulates expression of PACAP in the pituitary gonadotropes via both the PKA and PKC signaling systems. Mol Endocrinol. 2009;23:1022-1032.
31. Kanasaki H, Bedecarrats GY, Kam KY, Xu S, Kaiser UB. Gonadotropin-releasing hormone pulse frequency-dependent activation of extracellular signal-regulated kinase pathways in perifused LβT2 cells. Endocrinology. 2005;146:5503-5513.
32. Call GB, Wolfe MW. Gonadotropin-releasing hormone activates the equine luteinizing hormone β promoter through a protein kinase C/mitogen-activated protein kinase pathway. Biol Reprod. 1999;61:715-723.
33. Yokoi T, Ohmichi M, Tasaka K, et al. Activation of the luteinizing hormone β promoter by gonadotropin-releasing hormone requires c-Jun NH2-terminal protein kinase. J Biol Chem. 2000;275: 21639-21647.
34. Mulvaney JM, Zhang T, Fewtrell C, Roberson MS. Calcium influx through L-type channels is required for selective activation of extracellular signal-regulated kinase by gonadotropin-releasing hormone. J Biol Chem. 1999;274:29796-29804.
35. Armstrong SP, Caunt CJ, Fowkes RC, Tsaneva-Atanasova K, McArdle CA. Pulsatile and sustained gonadotropin-releasing hormone (GnRH) receptor signaling: does the ERK signaling pathway decode GnRH pulse frequency? J Biol Chem. 2010;285:24360- 24371.
36. Naor Z, Harris D, Shacham S. Mechanism of GnRH receptor signaling: combinatorial cross-talk of Ca2+ and protein kinase C. Front Neuroendocrinol. 1998;19:1-19.
37. Halvorson LM, Kaiser UB, Chin WW. 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. 1999;13:106-116.
38. Klausen C, Booth M, Habibi HR, Chang JP. Extracellular signalregulated kinase mediates gonadotropin subunit gene expression and LH release responses to endogenous gonadotropin-releasing hormones in goldfish. Gen Comp Endocrinol. 2008;158:36-46.
39. Weck J, Fallest PC, Pitt LK, Shupnik MA. Differential gonadotropin-releasing hormone stimulation of rat luteinizing hormone subunit gene transcription by calcium influx and mitogen-activated protein kinase-signaling pathways. Mol Endocrinol. 1998;12:451- 457.
40. Duan WR, Shin JL, Jameson JL. Estradiol suppresses phosphorylation of cyclic adenosine 3',5'-monophosphate response element binding protein (CREB) in the pituitary: evidence for indirect action via gonadotropin-releasing hormone. Mol Endocrinol. 1999;13: 1338-1352.
41. Woodford TA, Correll LA, McKnight GS, Corbin JD. Expression and characterization of mutant forms of the type I regulatory subunit of cAMP-dependent protein kinase. The effect of defective cAMP binding on holoenzyme activation. J Biol Chem. 1989;264: 13321-13328.
42. Liu F, Usui I, Evans LG, et al. Involvement of both G(q/11) and G(s) proteins in gonadotropin-releasing hormone receptor-mediated signaling in L β T2 cells. J Biol Chem. 2002;277:32099-32108.
43. Lariviere S, Garrel G, Simon V, et al. Gonadotropin-releasing hormone couples to 3',5'-cyclic adenosine-5'-monophosphate pathway through novel protein kinase Cdelta and -epsilon in LβT2 gonadotrope cells. Endocrinology. 2007;148:1099-1107.
44. Garrel G, McArdle CA, Hemmings BA, Counis R. Gonadotropinreleasing hormone and pituitary adenylate cyclase-activating polypeptide affect levels of cyclic adenosine 3',5'-monophosphate-dependent protein kinase A (PKA) subunits in the clonal gonadotrope αT3-1 cells: evidence for cross-talk between PKA and protein kinase C pathways. Endocrinology. 1997;138:2259-2266.
45. Borgeat P, Chavancy G, Dupont A, Labrie F, Arimura A, Schally AV. Stimulation of adenosine 3':5'-cyclic monophosphate accumulation in anterior pituitary gland in vitro by synthetic luteinizing hormone-releasing hormone. Proc Natl Acad Sci USA. 1972;69: 2677-2681.
46. Burger LL, Haisenleder DJ, Aylor KW, Marshall JC. Regulation of intracellular signaling cascades by GNRH pulse frequency in the rat pituitary: roles for CaMK II, ERK, and JNK activation. Biol Reprod. 2008;79:947-953.
47. Burger LL, Haisenleder DJ, Aylor KW, Marshall JC. Regulation of Lhb and Egr1 gene expression by GNRH pulses in rat pituitaries is both c-Jun N-terminal kinase (JNK)- and extracellular signal-regulated kinase (ERK)-dependent. Biol Reprod. 2009;81:1206-1215.
48. Haisenleder DJ, Workman LJ, Burger LL, Aylor KW, Dalkin AC, Marshall JC. Gonadotropin subunit transcriptional responses to calcium signals in the rat: evidence for regulation by pulse frequency. Biol Reprod. 2001;65:1789-1793.
49. Burger LL, Dalkin AC, Aylor KW, Haisenleder DJ, Marshall JC. GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes-assessment by primary transcript assay provides evidence for roles of GnRH and follistatin. Endocrinology. 2002;143:3243-3249.
50. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G. Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature. 1977;269:338-340.
51. Charlton HM, Halpin DM, Iddon C, et al. The effects of daily administration of single and multiple injections of gonadotropinreleasing hormone on pituitary and gonadal function in the hypogonadal (hpg) mouse. Endocrinology. 1983;113:535-544.
52. Alarid ET, Windle JJ, Whyte DB, Mellon PL. Immortalization of pituitary cells at discrete stages of development by directed oncogenesis in transgenic mice. Development. 1996;122:3319-3329.
53. Windle JJ, Weiner RI, Mellon PL. Cell lines of the pituitary gonadotrope lineage derived by targeted oncogenesis in transgenic mice. Mol Endocrinol. 1990;4:597-603.
54. Harris D, Chuderland D, Bonfil D, Kraus S, Seger R, Naor Z. Extracellular signal-regulated kinase and c-Src, but not Jun N-terminal kinase, are involved in basal and gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone α-subunit promoter. Endocrinology. 2003;144:612-622.
55. Liu F, Austin DA, Mellon PL, Olefsky JM, Webster NJ. GnRH activates ERK1/2 leading to the induction of c-fos and LHβ protein expression in LβT2 cells. Mol Endocrinol. 2002;16:419-434.
56. Stojilkovic SS, Catt KJ. Expression and signal transduction pathways of gonadotropin-releasing hormone receptors. Recent Prog Horm Res. 1995;50:161-205.
57. Stojilkovic SS, Catt KJ. Novel aspects of GnRH-induced intracellular signaling and secretion in pituitary gonadotrophs. J Neuroendocrinol. 1995;7:739-757.
58. Ando H, Hew CL, Urano A. Signal transduction pathways and transcription factors involved in the gonadotropin-releasing hormone-stimulated gonadotropin subunit gene expression. Comp Biochem Physiol B Biochem Mol Biol. 2001;129:525-532.
59. Lawson MA, Tsutsumi R, Zhang H, et al. Pulse sensitivity of the luteinizing hormone β promoter is determined by a negative feedback loop Involving early growth response-1 and Ngfi-A binding protein 1 and 2. Mol Endocrinol. 2007;21:1175-1191.
60. Mistry DS, Tsutsumi R, Fernandez M, et al. Gonadotropin-releasing hormone pulse sensitivity of follicle-stimulating hormone-β gene is mediated by differential expression of positive regulatory activator protein 1 factors and corepressors SKIL and TGIF1. Mol Endocrinol. 2011;25:1387-1403.
61. Haisenleder DJ, Burger LL, Walsh HE, et al. Pulsatile gonadotropin-releasing hormone stimulation of gonadotropin subunit transcription in rat pituitaries: evidence for the involvement of Jun N-terminal kinase but not p38. Endocrinology. 2008;149:139- 145.
62. Kwok RP, Lundblad JR, Chrivia JC, et al. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature. 1994;370: 223-226.
63. Halvorson LM, Ito M, Jameson JL, Chin WW. Steroidogenic factor-1 and early growth response protein 1 act through two com posite DNA binding sites to regulate luteinizing hormone β-subunit gene expression. J Biol Chem. 1998;273:14712-14720.
64. Kaiser UB, Halvorson LM, Chen MT. Sp1, steroidogenic factor 1 (SF-1), and early growth response protein 1 (egr-1) binding sites form a tripartite gonadotropin-releasing hormone response element in the rat luteinizing hormone-β gene promoter: an integral role for SF-1. Mol Endocrinol. 2000;14:1235-1245.
65. Tremblay JJ, Drouin J. Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx1 and SF-1 to enhance luteinizing hormone β gene transcription. Mol Cell Biol. 1999;19: 2567-2576.
66. Dorn C, Ou Q, Svaren J, Crawford PA, Sadovsky Y. Activation of luteinizing hormone β gene by gonadotropin-releasing hormone requires the synergy of early growth response-1 and steroidogenic factor-1. J Biol Chem. 1999;274:13870-13876.
67. Wolfe MW, Call GB. Early growth response protein 1 binds to the luteinizing hormone-β promoter and mediates gonadotropin-releasing hormone-stimulated gene expression. Mol Endocrinol. 1999;13:752-763.
68. Lee SL, Sadovsky Y, Swirnoff AH, et al. Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science. 1996;273:1219-1221.
69. Topilko P, Schneider-Maunoury S, Levi G, et al. Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Egr-1)-targeted mice. Mol Endocrinol. 1998;12:107-122.
70. Tsutsumi R, Mistry D, Webster NJ. Signaling responses to pulsatile gonadotropin-releasing hormone in LβT2 gonadotrope cells. J Biol Chem. 2010;285:20262-20272.
71. Garrel G, Simon V, Thieulant ML, et al. Sustained gonadotropinreleasing hormone stimulation mobilizes the cAMP/PKA pathway to induce nitric oxide synthase type 1 expression in rat pituitary cells in vitro and in vivo at proestrus. Biol Reprod. 2010;82:1170- 1179.
72. Winters SJ, Ghooray D, Fujii Y, Moore JP Jr., Nevitt JR, Kakar SS. Transcriptional regulation of follistatin expression by GnRH in mouse gonadotroph cell lines: evidence for a role for cAMP signaling. Mol Cell Endocrinol. 2007;271:45-54.
73. Mulvaney JM, Roberson MS. Divergent signaling pathways requiring discrete calcium signals mediate concurrent activation of two mitogen-activated protein kinases by gonadotropin-releasing hormone. J Biol Chem. 2000;275:14182-14189.
74. Armstrong SP, Caunt CJ, Fowkes RC, Tsaneva-Atanasova K, McArdle CA. Pulsatile and sustained gonadotropin-releasing hormone (GnRH) receptor signaling: does the Ca2+/NFAT signaling pathway decode GnRH pulse frequency? J Biol Chem. 2009;284: 35746-35757.
75. Tsaneva-Atanasova K, Caunt CJ, Armstrong SP, Perrett RM, McArdle CA. Decoding neurohormone pulse frequency by convergent signalling modules. Biochem Soc Trans. 2012;40:273-278.
76. Tsaneva-Atanasova K, Mina P, Caunt CJ, Armstrong SP, McArdle CA. Decoding GnRH neurohormone pulse frequency by convergent signalling modules. J R Soc Interface /R Soc. 2012;9:170-182.