Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of GnIH, in the control of gonadotropin secretion in the rat: In vivo and in vitro studies

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 1, 2010, Pages

  Pineda, R ^a,b   Garcia Galiano, D ^a,b   Sanchez Garrido, M A ^a,b   Romero, M ^a   Ruiz Pino, F ^a   Aguilar, E ^a,b,c   Dijcks, F A ^d   Blomenrohr M ^d   Pinilla, L ^a,b   Van Noort, P I ^d   Tena Sempere, M ^a,b,c  

^a UNIVERSITY OF CÓRDOBA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d NV ORGANON   (Netherlands)

Author keywords

Gonadotropin inhibitory hormone; Gonadotropin releasing hormone; Neuropeptide FF; Receptor; RF amide related peptide; RF9

Indexed keywords

FOLLITROPIN; GONADOTROPIN; LUTEINIZING HORMONE; NEUROPEPTIDE; NEUROPEPTIDE FF; RF AMIDE RELATED PEPTIDE 3; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FEMALE; FOLLITROPIN RELEASE; GONADOTROPIN RELEASE; IN VITRO STUDY; IN VIVO STUDY; LUTEINIZING HORMONE RELEASE; MALE; MAMMAL; NONHUMAN; PRIORITY JOURNAL; RAT; SCREENING TEST;

ANIMALS; AREA UNDER CURVE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FOLLICLE STIMULATING HORMONE; LUTEINIZING HORMONE; MALE; NEUROPEPTIDES; PITUITARY GLAND; RATS; RATS, WISTAR;

EID: 77953421665     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00108.2010     Document Type: Article

References (32)

1. Anderson GM, Relf HL, Rizwan MZ, Evans JJ. Central and peripheral effects of RFamide-related peptide-3 on luteinizing hormone and prolactin secretion in rats. Endocrinology 150: 1834-1840, 2009.
2. Bonini JA, Jones KA, Adham N, Forray C, Artymyshyn R, Durkin MM, Smith KE, Tamm JA, Boteju LW, Lakhlani PP, Raddatz R, Yao WJ, Ogozalek KL, Boyle N, Kouranova EV, Quan Y, Vaysse PJ, Wetzel JM, Branchek TA, Gerald C, Borowsky B. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J Biol Chem 275: 39324-39331, 2000.
3. Clarke IJ, Qi Y, Puspita Sari I, Smith JT. Evidence that RF-amide related peptides are inhibitors of reproduction in mammals. Front Neuroendocrinol 30: 371-378, 2009.
4. 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. 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, 2008.
5. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin- releasing hormone neuron firing in the mouse. Endocrinology 150: 2799-2804, 2009.
6. Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology 149: 4958-4969, 2008.
7. Herbison AE. Physiology of the gonadotropin-releasing hormone neuronal network. In: The Physiology of Reproduction, edited by Neill JD. San Diego, CA: Elsevier, 2006, p. 1415-1482.
8. 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. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2: 703-708, 2000.
9. Johnson MA, Fraley GS. Rat RFRP-3 alters hypothalamic GHRH expression and growth hormone secretion but does not affect KiSS-1 gene expression or the onset of puberty in male rats. Neuroendocrinology 88: 305-315, 2008.
10. Johnson MA, Tsutsui K, Fraley GS. Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav 51: 171-180, 2007. (Pubitemid 44838645)
11. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N. Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest Anim Endocrinol 36: 219-224, 2009.
12. Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hormone in male rats. Proc Natl Acad Sci USA 106: 11324-11329, 2009.
13. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 103: 2410-2415, 2006. (Pubitemid 43271683)
14. Legagneux K, Bernard-Franchi G, Poncet F, La Roche A, Colard C, Fellmann D, Pralong F, Risold PY. Distribution and genesis of the RFRP-producing neurons in the rat brain: comparison with melanin-concentrating hormone- and hypocretin-containing neurons. Neuropeptides 43: 13-19, 2009.
15. Millar RP. Gonadotropin releasing hormone. In: Handbook of Biologically Active Peptides, edited by Kastin AJ. San Diego, CA: Academic, 2006, p. 635-644.
16. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol 199: 105-112, 2008.
17. Navarro VM, Castellano JM, Fernández-Fernández R, Tovar S, Roa J, Mayen A, Barreiro ML, Casanueva FF, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146: 1689-1697, 2005.
18. Navarro VM, Castellano JM, Fernández-Fernández R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 146: 156-163, 2005.
19. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz- Pino F, Aguilar E, Dijcks FA, Blomenröhr M, Pinilla L, van Noort PI, Tena-Sempere M. Characterization of the potent gonadotropin-releasing activity of RF9, a selective antagonist of RF-amide-related peptides and neuropeptide FF receptors: physiological and pharmacological implications. Endocrinology 151: 1902-1913, 2010.
20. Revel FG, Saboureau M, Pevet P, Simonneaux V, Mikkelsen JD. RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology 149: 902-912, 2008.
21. Rizwan MZ, Porteous R, Herbison AE, Anderson GM. Cells expressing RFamide-related peptide-1/3, the mammalian gonadotropin-inhibitory hormone orthologs, are not hypophysiotropic neuroendocrine neurons in the rat. Endocrinology 150: 1413-1420, 2009.
22. Roa J, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front Neuroendocrinol 29: 48-69, 2008.
23. Roa J, Vigo E, Castellano JM, Gaytan F, Garcia-Galiano D, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M. Follicle-stimulating hormone responses to kisspeptin in the female rat at the preovulatory period: modulation by estrogen and progesterone receptors. Endocrinology 149: 5783-5790, 2008.
24. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M. Opposite roles of estrogen receptor (ER)-alpha and ERbeta in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 149: 1627-1637, 2008.
25. Samson WK, Keown C, Samson CK, Samson HW, Lane B, Baker JR, Taylor MM. Prolactin-releasing peptide and its homolog RFRP-1 act in hypothalamus but not in anterior pituitary gland to stimulate stress hormone secretion. Endocrine 20: 59-66, 2003.
26. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology: 5549-5556, 2009.
27. Simonin F, Schmitt M, Laulin JP, Laboureyras E, Jhamandas JH, MacTavish D, Matifas A, Mollereau C, Laurent P, Parmentier M, Kieffer BL, Bourguignon JJ, Simonnet G. RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc Natl Acad Sci USA 103: 466-471, 2006.
28. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149: 5770-5782, 2008.
29. Tsutsui K, Osugi T. Evolutionary origin and divergence of GnIH and its homologous peptides. Gen Comp Endocrinol 161: 30-33, 2009.
30. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275: 661-667, 2000.
31. Wu M, Dumalska I, Morozova E, van den Pol AN, Alreja M. Gonadotropin inhibitory hormone inhibits basal forebrain vGluT2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J Physiol 587: 1401-1411, 2009.
32. Zajac JM. Neuropeptide FF: new molecular insights. Trends Pharmacol Sci 22: 63, 2001.