The GnRH receptor and the response of gonadotrope cells to GnRH pulse frequency code. A story of an atypical adaptation of cell function relying on a lack of receptor homologous desensitization

Folia Histochemica et Cytobiologica

Volumn 47, Issue 5, 2009, Pages

  Counis, Raymond ^a   Garrel, Ghislaine ^a   Laverriere, Jean Noël ^a   Simon, Violaine ^a   Bleux, Christian ^a   Magre, Solange ^a   Cohen Tannoudji, Joëlle ^a  

^a Groupe Hospitalier Pitié Salpêtrière   (France)

Author keywords

Gene activation inactivation; GnRH; GnRH receptor; GnRH receptor structure; Signaling network

Indexed keywords

ACTIVIN; EARLY GROWTH RESPONSE FACTOR 1; FOLLISTATIN; FOLLITROPIN; FOLLITROPIN BETA SUBUNIT; G PROTEIN COUPLED RECEPTOR; GONADORELIN RECEPTOR; LUTEINIZING HORMONE; LUTEINIZING HORMONE BETA SUBUNIT; GONADORELIN;

AUTOREGULATION; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; DESENSITIZATION; ENDOCYTOSIS; FEEDBACK SYSTEM; GENE ACTIVATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GONADOTROPIN SECRETING CELL; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; HYPOTHALAMUS; NEUROSECRETORY CELL; NONHUMAN; OVARY CYCLE; PULSE RATE; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; GENE EXPRESSION REGULATION; HYPOPHYSIS; METABOLISM;

MAMMALIA;

ANIMALS; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; PITUITARY GLAND; RECEPTORS, LHRH;

EID: 75949117797     PISSN: 02398508     EISSN: None     Source Type: Journal    
DOI: 10.2478/v10042-009-0109-9     Document Type: Review

References (49)

1. Knobil E. Neuroendocrine control of the menstrual cycle. Recent Prog Horm Res. 1980;36:53-88.
2. Sarkar DK, Chiappa SA, Fink G, Sherwood NM. Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature. 1976;264:461-463.
3. Xia L, Van Vugt D, Alston EJ, Luckhaus J, Ferin M. A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. Endocrinology. 1992;131:2812-2820.
4. Caraty A, Antoine C, Delaleu B et al. Nature and bioactivity of gonadotropin-releasing hormone (GnRH) secreted during the GnRH surge. Endocrinology. 1995;136:3452-3460
5. Counis R. Gonadotropin synthesis. In: Neill J, Knobil E, eds. Encyclopedia of Reproduction. Vol.2. Acad. Press; 1999:507-520.
6. 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.
7. 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.
8. Lalloz MRA, Detta A, Clayton RN. Gonadotropin-releasing hormone desensitization preferentially inhibits expression of the luteinizing hormone ?-subunit gene in vivo. Endocrinology. 1988;122:1689-1694. (Pubitemid 18092006)
9. Rodin DA, Lalloz MRA, Clayton RN. Gonadotropin-releasing hormone regulates follicle-stimulating hormone ?-subunit gene expression in the male rat. Endocrinology. 1988;125:1282-1289.
10. Lerrant Y, Kottler ML, Bergametti F, Moumni M, Blumberg-Tick J, Counis R. Expression of gonadotropin-releasing hormone (GnRH) receptor gene is altered by GnRH agonist desensitization in a manner similar to that of gonadotropin ?-subunit genes in normal and castrated rat pituitary. Endocrinology. 1995;136:2803-2808.
11. Lahlou N, Roger M, Chaussain J, et al. Gonadotropin and alpha-subunit secretion during long-term suppression by DTrp6-luteinizing hormone releasing hormone microcapsules as treatment of precocious puberty. J Clin Endocrinol Metab. 1987;65:946-953.
12. Hazum E, Cuatrecasas P, Marian J, Conn PM. Receptor mediated internalization of fluorescent gonadotropin-releasing hormone by pituitary gonadotropes. Proc Natl Acad sci USA. 1980;77:6692-6695.
13. Andrews WV, Staley DD, Huckel WR, Conn PM. Stimulation of luteinizing hormone (LH) release and phospholipid breakdown by guanosine triphosphate in permeabilized pituitary gonadotropes: antagonist action suggests association of a G protein and gonadotropin-releasing hormone receptor. Endocrinology. 1986;119:2537-2546.
14. Granger A, Ngô-Muller V, Bleux C, et al. The promoter of the rat GnRH receptor gene directs the expression of the human placental alkaline phosphatase reporter gene in gonadotrope cells in the anterior pituitary gland as well as in multiple extrapituitary tissues. Endocrinology. 2004;145:983-993.
15. Stojilkovic S, Reinhardt J, Catt KJ. Gonadotropin-releasing hormone receptors: structure and signal transduction pathways. Endocr Rev. 1994;15:462-499.
16. Naor Z, Benard O, Seger R. Activation of MAPK cascades by G protein-coupled receptors: the case of gonadotropin-releasing hormone. Trends Endocrinol Metab. 2000;11:91-99.
17. Sundaresan S, Colin IM, Pestell RG, Jameson JL. Stimulation of mitogen-activated protein kinase by gonadotropin-releasing hormone: evidence for the involvement of protein kinase C. Endocrinology. 1996;137:304-311.
18. Ceccattelli S, Hulting AL, Zhang X, Gustafsson L, Villar M, Hökfelt T. Nitric oxide synthase in the rat anterior pituitary gland and the role of nitric oxide in regulation of luteinizing hormone secretion. Proc Natl Acad Sci USA. 1993;90:11292-11296.
19. Lozach A, Garrel G, Lerrant Y, Bérault A, Counis R. GnRHdependent up-regulation of nitric oxide synthase I level in pituitary gonadotrophs mediates cGMP elevation during rat proestrus. Mol Cell Endocrinol. 1998;143:43-51.
20. Lariviere S, Garrel G, Simon V, et al. Gonadotropin-releasing hormone couples to 3',5'-cyclic adenosine-5'-monophosphate pathway through novel protein kinase C delta and-epsilon in LβT2 gonadotrope cells. Endocrinology. 2007;148:1099-1107.
21. 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 beta LßT2 cells. J Biol Chem. 2002;277:32099-32108.
22. Starzec A, Jutisz M, Counis R. Cyclic adenosine monophosphate and phorbol ester, like gonadotropin-releasing hormone, stimulate the biosynthesis of luteinizing hormone polypeptide chains in a nonadditive manner. Mol Endocrinol. 1989;3:618-624.
23. Starzec A, Moumni M, d'Angelo-Bernard G, Lerrant Y, Jutisz M, Counis R. Cyclic AMP enhances gene expression, synthesis and release of newly synthesized α and luteinizing hormone β subunits in cultured rat anterior pituitary cells. Neurochem Int. 1989;15:259-264.
24. Horton CD, Halvorson LM. The cAMP signaling system regulates LHβgene expression: roles of early growth response protein-1, SP1 and steroidogenic factor-1. J Mol Endocrinol. 2004;32:291-306.
25. Kakar SS, Winters SJ, Zacharias W, Miller DM, Flynn S. Identification of distinct gene expression profiles associated with treatment of LbetaT2 cells with gonadotropin-releasing hormone agonist using microarray analysis. Gene. 2003;308:67-77.
26. 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.
27. Garrel G, Lerrant Y, Siriostis C, et al. Evidence that gonadotropin-releasing hormone stimulates gene expression and levels of active nitric oxide synthase type I in pituitary gonadotrophs, a process altered by desensitization and, indirectly, by gonadal steroids. Endocrinology. 1998;139:2163-2170.
28. Bachir LK, Garrel G, Lozach A, Laverriere JN, Counis R. The rat pituitary promoter of the neuronal nitric oxide synthase gene contains an Sp1-, LIM homeodomain-dependent enhancer and a distinct bipartite gonadotropin-releasing hormone-responsive region. Endocrinology. 2003;144:3995-4007.
29. Garrel G, Lerrant Y, Ribot G, Counis R. Messenger ribonucleic acids for alpha-and beta-isoforms of cyclic adenosine 3',5'-monophosphate-dependent protein kinase subunits present in the anterior pituitary: regulation of RII beta and C alpha gene expression by the cyclic nucleotide and phorbol ester. Endocrinology. 1993;133:1010-1019.
30. Harris D, Reiss N, Naor Z. Differential activation of protein kinase C δ and ε gene expression by gonadotropin-releasing hormone in αT3-1 cells. Autoregulation by protein kinase C. J Biol Chem. 1997;272:13534-13540. (Pubitemid 27224782)
31. Xie J, Bliss SP, Nett TM, Ebersole BJ, Sealfon SC, Roberson MS. Transcript profiling of immediate early genes reveals a unique role for activating transcription factor 3 in mediating activation of the glycoprotein hormone ?-subunit promoter by gonadotropin-releasing hormone. Mol Endocrinol. 2005;19:2624-2638.
32. Hamid T, Malik MT, Millar RP, Kakar SS. Protein kinase A serves as a primary pathway in activation of Nurr77 expression by gonadotropin-releasing hormone in the LβT2 mouse pituitary gonadotroph tumor cell line. Int J Oncology. 2008;33:1055-1064.
33. Yasin M, Dalkin AC, Haisenleder DJ, Kerrigan JR, Marshall JC. Gonadotropin-releasing hormone (GnRH) pulse pattern regulates GnRH receptor gene expression : augmentation by estradiol. Endocrinology. 1995;136:1559-1564.
34. Millar RP, Lu ZL, Pawson AJ, Flanagan CA, Morgan K, Maudsley SR. Gonadotropin-releasing hormone receptors. Endocr Rev. 2004;25:235-275.
35. Ferguson SS, Barak LS, Zhang J, Caron MG. G protein-coupled receptor regulation: role of G protein-coupled receptor kinases and β-arrestins. Can J Physiol Pharmacol. 1996;74:1095-1110. (Pubitemid 27047505)
36. Lefkowitz RJ. G protein-coupled receptors. III. New roles for receptor kinases and β-arrestins in receptor signaling and desensitization. J Biol Chem. 1998;273:186673-218680
37. Lethimonier C, Madigou T, Munoz-Cueto JA, Lareyre JJ, Kah O. Evolutionary aspects of GnRHs, GnRH neurohormonal systems and GnRH receptors in teleost fish. Gen Comp Endocrinol. 2004;135:1-16.
38. Davidson JS, Wakefield IK, Millar RP. Absence of rapid desensitization of the mouse gonadotropin-releasing hormone receptor. Biochem J. 1994;300:299-302.
39. Pawson AJ, Katz A, Sun YM, et al. Contrasting internalization kinetics of human and chicken gonadotropin-releasing hormone receptors mediated by C-terminal tail. J Endocrinol. 1998 ;156:R9-R12.
40. Pawson AJ, Faccenda E, Maudsley S, Lu ZL, Naor Z, Millar RP. Mammalian type I gonadotropin-releasing hormone receptors undergo slow, constitutive, agonist-independent internalization. Endocrinology. 2008;149:1415-1422.
41. McArdle CA, Franklin J, Green L, Hislop JN. Signalling, cycling and desensitisation of gonadotropin-releasing hormone receptors. J Endocrinol. 2002;173:1-11. (Pubitemid 34428886)
42. 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.
43. Topilko P, Schneider-Maunoury S, Levi G, et al. Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Egr-1)-targetted mice. Mol Endocrinol. 1998;12:107-122.
44. 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.
45. 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.
46. Kumbrink J, Gerlinger M, Johnson JP. Egr-1 induces the expression of its corepressor Nab2 by activation of the Nab2 promoter thereby establishing a negative feedback loop. J Biol Chem. 2005;280:42785-42793.
47. Besecke LM, Guendner MJ, Schneyer AL, Bauer DA, Jameson JL, Weiss J. Gonadotropin-releasing hormone regulates follicle stimulating hormone-beta gene expression through an activin/follistatin autocrine or paracrine loop. Endocrinology. 1996;137:3667-3673.
48. Dalkin AC, Haisenleder DJ, Gilrain JT, Aylor K, Yasin M, Marshall JC. Gonadotropin releasing hormone regulation of gonadotropin subunit gene expression in female rats: actions on follicle-stimulating hormone beta messenger ribonucleic acid (mRNA) involve differential expression of pituitary activin (beta-B) and follistatin mRNAs. Endocrinology. 1999;140: 903-908.
49. Winters SJ, Ghooray D, Fujii Y, Moore Jr JP, Nevitt JR, Kakar SS. Transcriptional regulation of follistatin expression by GnRH in mouse gonadotrope cell lines: evidence for a role for cAMP signaling. Mol Cell Endocrinol. 2007;271:45-54.