Gonadotropin-inhibitory hormone inhibits gnrh-induced gonadotropin subunit gene transcriptions by inhibiting AC/cAMP/PKA-dependent ERK pathway in LβT2 Cells

Endocrinology

Volumn 153, Issue 5, 2012, Pages 2332-2343

  Son, You Lee ^a   Ubuka, Takayoshi ^a   Millar, Robert P ^b,c,d   Kanasaki, Haruhiko ^e   Tsutsui, Kazuyoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c UNIVERSITY OF PRETORIA   (South Africa)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e SHIMANE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GONADORELIN; GONADOTROPIN; GONADOTROPIN INHIBITORY HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CELL LINE; ENZYME INHIBITION; GENETIC TRANSCRIPTION; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADENYLATE CYCLASE; AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GONADOTROPHS; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS, PITUITARY; HYPOTHALAMIC HORMONES; MICE; MOLECULAR SEQUENCE DATA; NEURONS; NEUROPEPTIDES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84860318195     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1904     Document Type: Article

References (63)

1. Matsuo H, Baba Y, Nair RM, Arimura A, Schally AV 1971 Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem Biophys Res Commun 43:1334-1339
2. Burgus R, Butcher M, Amoss M, Ling N, Monahan M, Rivier J, Fellows R, Blackwell R, Vale W, Guillemin R 1972 Primary struc ture of the ovine hypothalamic luteinizing hormone-releasing factor (LRF) (LH-hypothalamus-LRF-gas chromatography-mass spectrometry-decapeptide-Edman degradation). Proc Natl Acad Sci USA 69:278-282
3. Millar RP, Lu ZL, Pawson AJ, Flanagan CA, Morgan K, Maudsley SR 2004 Gonadotropin-releasing hormone receptors. Endocr Rev 25:235-275 (Pubitemid 38501395)
4. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ 2000 Anovel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661-667
5. Ukena K, Tsutsui K 2005 A new member of the hypothalamic RFamide peptide family, LPXRF-amide peptides: structure, localization, and function. Mass Spectrom Rev 24:469-486 (Pubitemid 41083798)
6. Tsutsui K 2009 A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): biosynthesis, mode of action and functional significance. Prog Neurobiol 88:76-88
7. Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ 2010 Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrinol 31:284-295
8. Fukusumi S, Habata Y, Yoshida H, Iijima N, Kawamata Y, Hosoya M, Fujii R, Hinuma S, Kitada C, Shintani Y, Suenaga M, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M 2001 Characteristics and distribution of endogenous RFamide-related peptide-1. Biochim Biophys Acta 1540:221-232 (Pubitemid 32913631)
9. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA, Wang A, Chowdhury VS, Tsutsui K, Bentley GE 2009 Gonadotropininhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 517:841-855
10. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE 2009 Identification of human Gn IH homologs, RFRP-1 and RFRP-3, and the cognate re ceptor, GPR147 in the human hypothalamic pituitary axis. PLo S One 4:e8400
11. Ukena K, Iwakoshi E, Minakata H, Tsutsui K 2002 A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett 512:255-258 (Pubitemid 34164490)
12. Yoshida H, Habata Y, Hosoya M, Kawamata Y, Kitada C, Hinuma S 2003 Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim Biophys Acta 1593:151-157 (Pubitemid 36173483)
13. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K 2012 Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 153:373-385
14. Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC, Ubuka T, Iqbal J, Li Q, Tilbrook A, Morgan K, Pawson AJ, Tsutsui K, Millar RP, Bentley GE 2008 Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149: 5811-5821
15. Gibson EM, Humber SA, Jain S, Williams 3rd WP, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ 2008 Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteiniz ing hormone surge. Endocrinology 149:4958-4969
16. Johnson MA, Tsutsui K, Fraley GS 2007 Rat RFamide-related pep tide-3 stimulates GH secretion, inhibits LH secretion, and has vari able effects on sex behavior in the adult male rat. Horm Behav 51:171-180 (Pubitemid 44838645)
17. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R 2006 Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 103:2410-2415 (Pubitemid 43271683)
18. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K 2008 Hypophysiotropic role of RFamide-related pep tide-3 in the inhibition of LH secretion in female rats. J Endocrinol 199:105-112
19. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N 2009 Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) se cretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol 36:219-224
20. Ubuka T, Ukena K, Sharp PJ, Bentley GE, Tsutsui K 2006 Gonad otropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 147:1187-1194 (Pubitemid 43244351)
21. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ 2009 Effect of RF-amide-related peptide-3 on luteinizing hormone and folliclestimulating hormone synthesis and secretion in ovine pituitary go nadotropes. Endocrinology 150:5549-5556
22. Ciccone NA, Dunn IC, Boswell T, Tsutsui K, Ubuka T, Ukena K, Sharp PJ 2004 Gonadotrophin inhibitory hormone depresses gonadotrophin α and follicle-stimulating hormone β subunit expres sion in the pituitary of the domestic chicken. J Neuroendocrinol 16:999-1006 (Pubitemid 40214445)
23. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, Osugi T, Chowdhury VS, Tsutsui K, Bentley GE 2008 Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology 149: 268-278
24. Elshourbagy NA, Ames RS, Fitzgerald LR, Foley JJ, Chambers JK, Szekeres PG, Evans NA, Schmidt DB, Buckley PT, Dytko GM, Murdock PR, Milligan G, Groarke DA, Tan KB, Shabon U, Nuthulaganti P, Wang DY, Wilson S, Bergsma DJ, Sarau HM 2000 Receptor for the pain modulatory neuropeptides FF and AF is an orphan G protein-coupled receptor. J Biol Chem 275:25965-25971
25. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, Fujii R, Watanabe T, Kikuchi K, Terao Y, Yano T, Yamamoto T, Kawamata Y, Habata Y, Asada M, Kitada C, Kurokawa T, Onda H, Nishimura O, Tanaka M, Ibata Y, Fujino M 2000 New neuro peptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2:703-708
26. Parker RM, Copeland NG, Eyre HJ, Liu M, Gilbert DJ, Crawford J, Couzens M, Sutherland GR, Jenkins NA, Herzog H 2000 Mo lecular cloning and characterisation of GPR74 a novel G-protein coupled receptor closest related to the Y-receptor family. Brain Res Mol Brain Res 77:199-208 (Pubitemid 30317347)
27. Mollereau C, Mazarguil H, Marcus D, Quelven I, Kotani M, Lannoy V, Dumont Y, Quirion R, Detheux M, Parmentier M, Zajac JM 2002 Pharmacological characterization of human NPFF(1) and NPFF(2) receptors expressed in CHO cells by using NPY Y(1) receptor antagonists. Eur J Pharmacol 451:245-256 (Pubitemid 35254027)
28. Yin H, Ukena K, Ubuka T, Tsutsui K 2005 A novel G proteincoupled receptor for gonadotropin-inhibitory hormone in the Jap anese quail (Coturnix japonica): identification, expression and bind ing activity. J Endocrinol 184:257-266 (Pubitemid 40207580)
29. Gouardères C, Mazarguil H, Mollereau C, Chartrel N, Leprince J, Vaudry H, Zajac JM 2007 Functional differences between NPFF1 and NPFF2 receptor coupling: high intrinsic activities of RFamiderelated peptides on stimulation of [35S]GTPγS binding. Neurophar macology 52:376-386 (Pubitemid 46123357)
30. Shimizu M, Bédécarrats GY 2010 Activation of the chicken gonad otropin-inhibitory hormone receptor reduces gonadotropin releas ing hormone receptor signaling. Gen Comp Endocrinol 167:331-337
31. 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-re leasing hormone in the LβT2 pituitary gonadotrope cell model. En docrinology 142:2284-2295 (Pubitemid 32473082)
32. Newton CL, Whay AM, McArdle CA, Zhang M, van Koppen CJ, van de Lagemaat R, Segaloff DL, Millar RP 2011 Rescue of expres sion and signaling of human luteinizing hormone G protein-coupled receptor mutants with an allosterically binding small-molecule ag onist. Proc Natl Acad Sci USA 108:7172-7176
33. Bentley GE, Tsutsui K, Kriegsfeld LJ 2010 Recent studies of gonad otropin-inhibitory hormone (Gn IH) in the mammalian hypothala mus, pituitary and gonads. Brain Res 1364:62-71
34. Borgeat P, Chavancy G, Dupont A, Labrie F, Arimura A, Schally AV 1972 Stimulation of adenosine 3':5'-cyclic monophosphate accu mulation in anterior pituitary gland in vitro by synthetic luteinizing hormone-releasing hormone. Proc Natl Acad Sci USA 69:2677-2681
35. Horton CD, Halvorson LM 2004 The cAMP signaling system reg ulates LHβ gene expression: roles of early growth response protein-1, SP1 and steroidogenic factor-1. J Mol Endocrinol 32:291-306 (Pubitemid 38312638)
36. Larivière S, Garrel G, Simon V, Soh JW, Laverrière JN, Counis R, Cohen-Tannoudji J 2007 Gonadotropin-releasing hormone couples to 3',5'-cyclic adenosine-5'-monophosphate pathway through novel protein kinase Cδ and -ε in LβT2 gonadotrope cells. Endocrinology 148:1099-1107
37. Tsutsumi R, Mistry D, Webster NJ 2010 Signaling responses to pulsatile gonadotropin-releasing hormone in LβT2 gonadotrope cells. J Biol Chem 285:20262-20272
38. Liu F, Usui I, Evans LG, Austin DA, Mellon PL, Olefsky JM, Web ster NJ 2002 Involvement of both G(q/11) and G(s) proteins in gonadotropin-releasing hormone receptor-mediated signaling in LβT2 cells. J Biol Chem 277:32099-32108 (Pubitemid 34969022)
39. Horn F, Bilezikjian LM, Perrin MH, Bosma MM, Windle JJ, Huber KS, Blount AL, Hille B, Vale W, Mellon PL 1991 Intracellular re sponses to gonadotropin-releasing hormone in a clonal cell line of the gonadotrope lineage. Mol Endocrinol 5:347-355 (Pubitemid 21923699)
40. Conn PM, Morrell DV, Dufau ML, Catt KJ 1979 Gonadotropinreleasing hormone action in cultured pituicytes: independence of luteinizing hormone release and adenosine 3',5'-monophosphate production. Endocrinology 104:448-453 (Pubitemid 9135858)
41. Théoleyre M, Bérault A, Garnier J, Jutisz M 1976 Binding of go nadotropin-releasing hormone (LH-RH) to the pituitary plasma membranes and the problem of adenylate cyclase stimulation. Mol Cell Endocrinol 5:365-377
42. Grosse R, Schmid A, Schöneberg 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 (Pubitemid 30185136)
43. Naidich M, Shterntal B, Furman R, Pawson AJ, Jabbour HN, Mor gan K, Millar RP, Jia J, Tomic M, Stojilkovic S, Stern N, Naor Z 2010 Elucidation of mechanisms of the reciprocal cross talk between gonadotropin-releasing hormone and prostaglandin receptors. Endocrinology 151:2700-2712
44. Bliss SP, Navratil AM, Xie J, Roberson MS 2010 Gn RH signaling, the gonadotrope and endocrine control of fertility. Front Neuroendocrinol 31:322-340
45. 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 (Pubitemid 30165715)
46. Kanasaki H, Mutiara S, Oride A, Purwana IN, Miyazaki K 2009 Pulse frequency-dependent gonadotropin gene expression by ade nylate cyclase-activating polypeptide 1 in perifused mouse pituitary gonadotroph LβT2 cells. Biol Reprod 81:465-472
47. Chen J, An BS, Cheng L, Hammond GL, Leung PC 2009 Gonado tropin-releasing hormone-mediatedphosphorylation of estrogen receptor-α contributes to fosB expression in mouse gonadotrophs. Endocrinology 150:4583-4593
48. Coss D, Hand CM, Yaphockun KK, Ely HA, Mellon PL 2007 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 21:3071-3086 (Pubitemid 350223516)
49. Henderson HL, Townsend J, Tortonese DJ 2008 Direct effects of prolactin and dopamine on the gonadotroph response to Gn RH. J Endocrinol 197:343-350 (Pubitemid 351696247)
50. Naor Z 2009 Signaling by G-protein-coupled receptor (GPCR): studies on the Gn RH receptor. Front Neuroendocrinol 30:10-29
51. Dobkin-Bekman M, Naidich M, Pawson AJ, Millar RP, Seger R, Naor Z 2006 Activation of mitogen-activated protein kinase (MAPK) by Gn RH is cell-context dependent. Mol Cell Endocrinol 252:184-190
52. Stanislaus D, Ponder S, Ji TH, Conn PM 1998 Gonadotropin-re leasing hormone receptor couples to multiple G proteins in rat go nadotrophs and in GGH3 cells: evidence from palmitoylation and overexpression of G proteins. Biol Reprod 59:579-586 (Pubitemid 28395073)
53. Han XB, Conn PM 1999 The role of protein kinases A and C pathways in the regulation of mitogen-activated protein kinase activation in response to gonadotropin-releasing hormone receptor activation. Endocrinology 140:2241-2251 (Pubitemid 30636465)
54. Yoshimura M, Cooper DM 1993 Type-specific stimulation of adenylylcyclase by protein kinase C. J Biol Chem 268:4604-4607 (Pubitemid 23081567)
55. Kawabe J, Iwami G, Ebina T, Ohno S, Katada T, Ueda Y, Homcy CJ, Ishikawa Y 1994 Differential activation of adenylyl cyclase by protein kinase C isoenzymes. J Biol Chem 269:16554-16558 (Pubitemid 24200406)
56. Nelson EJ, Hellevuo K, Yoshimura M, Tabakoff B 2003 Ethanolinduced phosphorylation and potentiation of the activity of type 7 adenylyl cyclase. Involvement of protein kinase CS. J Biol Chem 278:4552-4560 (Pubitemid 36805609)
57. Liu F, Austin DA, Webster NJ 2003 Gonadotropin-releasing hor mone-desensitized LβT2 gonadotrope cells are refractory to acute protein kinase C, cyclic AMP, and calcium-dependent signaling. Endocrinology 144:4354-4365 (Pubitemid 37204835)
58. Bonfil D, Chuderland D, Kraus S, Shahbazian D, Friedberg I, Seger R, Naor Z 2004 Extracellular signal-regulated kinase, Jun N-terminal kinase, p38, and c-Src are involved in gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone folliclestimulating hormone β-subunit promoter. Endocrinology 145: 2228-2244 (Pubitemid 38535052)
59. 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
60. Gur G, Bonfil D, Safarian H, Naor Z, Yaron Z 2002 Gn RH sig naling pathways regulate differentially the tilapia gonadotropin subunit genes. Mol Cell Endocrinol 189:125-134 (Pubitemid 34229170)
61. Baccarini M 2005 Second nature: biological functions of the Raf-1 "kinase". FEBS Lett 579:3271-3277 (Pubitemid 40804674)
62. Kovalovsky D, Refojo D, Liberman AC, Hochbaum D, Pereda MP, Coso OA, Stalla GK, Holsboer F, Arzt E 2002 Activation and in duction of NUR77/NURR1 in corticotrophs by CRH/cAMP: in volvement of calcium, protein kinase A, and MAPK pathways. Mol Endocrinol 16:1638-1651 (Pubitemid 34746009)
63. Romano D, Pertuit M, Rasolonjanahary R, Barnier JV, Magalon K, Enjalbert A, Gerard C 2006 Regulation of the RAP1/RAF-1/extracellularly regulated kinase-1/2 cascade and prolactin release by the phosphoinositide 3-kinase/AKT pathway in pituitary cells. Endocrinology 147:6036-6045 (Pubitemid 44833523)