RF9 acts as a KISS1R agonist in vivo and in vitro

Endocrinology

Volumn 156, Issue 12, 2015, Pages 4639-4648

  Min, Le ^a   Leon, Silvia ^b,c   Li, Huan ^a   Pinilla, Leonor ^b,c   Carroll, Rona S ^a   Tena Sempere, Manuel ^b,c,d   Kaiser, Ursula B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CÓRDOBA   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; INTERFERON REGULATORY FACTOR 9; KISSPEPTIN 10; MITOGEN ACTIVATED PROTEIN KINASE; NEUROPEPTIDE FF; NEUROPEPTIDE FF RECEPTOR 1; RECEPTOR; UNCLASSIFIED DRUG; ADAMANTANE; ADAMANTYLCARBONYL-ARGINYL-PHENYLALANINAMIDE; CALCIUM; DIPEPTIDE; G PROTEIN COUPLED RECEPTOR; INOSITOL PHOSPHATE; KISS1 PROTEIN, HUMAN; KISS1R PROTEIN, HUMAN; KISS1R PROTEIN, MOUSE; KISSPEPTIN; LUTEINIZING HORMONE; NEUROPEPTIDE; NEUROPEPTIDE FF RECEPTOR; NEUROPEPTIDE RECEPTOR; RADIOACTIVE IODINE; RFAMIDE PEPTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; EC50; ENZYME PHOSPHORYLATION; FEMALE; GONADOTROPIN RELEASE; IN VITRO STUDY; IN VIVO STUDY; LUTEINIZING HORMONE RELEASE; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; RADIOASSAY; SECRETION (PROCESS);

ADAMANTANE; ANIMALS; CALCIUM; CHO CELLS; CRICETULUS; DIPEPTIDES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; IN VITRO TECHNIQUES; INOSITOL PHOSPHATES; IODINE RADIOISOTOPES; KISSPEPTINS; LUTEINIZING HORMONE; MICE; MICE, KNOCKOUT; NEURONS; NEUROPEPTIDES; RADIOLIGAND ASSAY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE;

EID: 84948134436     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1635     Document Type: Article

References (45)

1. Tsutsui K, Saigoh E, Ukena K, et al. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun. 2000;275:661-667.
2. Ukena K, Tsutsui K. Distribution of novel RFamide-related peptidelike immunoreactivity in the mouse central nervous system. Neurosci Lett. 2001;300:153-156.
3. Kriegsfeld LJ, Mei DF, Bentley GE, et al. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A. 2006;103:2410-2415.
4. Ubuka T, Morgan K, Pawson AJ, et al. Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One. 2009;4:e8400.
5. 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. 2007; 51:171-180.
6. Rizwan MZ, Poling MC, Corr M, et al. RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology. 2012;153: 3770-3779.
7. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, et al. Characterization of the inhibitory roles of RFRP3, the mammalian ortholog of Gn IH, in the control of gonadotropin secretion in the rat: In vivo and in vitro studies. Am J Physiol Endocrinol Metab. 2010;299: E39-E46.
8. 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. 2009;150:2799-2804.
9. Simonin F, Schmitt M, Laulin JP, et al. RF9, a potent and selective neuropeptide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc Natl Acad Sci U S A. 2006;103:466-471.
10. Yang HY, Fratta W, Majane EA, Costa E. Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci U S A. 1985;82:7757-7761.
11. Caraty A, Blomenröhr M, Vogel GM, Lomet D, Briant C, Beltramo M. RF9 powerfully stimulates gonadotrophin secretion in the ewe: Evidence for a seasonal threshold of sensitivity. J Neuroendocrinol. 2012;24:725-736.
12. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, et al. 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. 2010;151:1902-1913.
13. Glanowska KM, Burger LL, Moenter SM. Development of gonadotropin- releasing hormone secretion and pituitary response. J Neurosci. 2014;34:15060-15069.
14. García -Galiano D, van Ingen Schenau D, Leon S, Krajnc-Franken MA, et al. Kisspeptin signaling is indispensable for neurokinin B, but not glutamate, stimulation of gonadotropin secretion in mice. Endocrinology. 2012;153:316-328.
15. Saito TH, Nakane R, Akazome Y, Abe H, Oka Y. Electrophysiological analysis of the inhibitory effects of FMRFamide-like peptides on the pacemaker activity of gonadotropin-releasing hormone neurons. J Neurophysiol. 2010;104:3518-3529.
16. León S, García-Galiano D, Ruiz-Pino F, et al. Physiological roles of gonadotropin-inhibitory hormone signaling in the control of mammalian reproductive axis: Studies in the NPFF1 receptor null mouse. Endocrinology. 2014;155:2953-2965.
17. Liu X, Herbison AE. RF9 excitation of GnRH neurons is dependent upon Kiss1r in the adult male and female mouse. Endocrinology. 2014;155:4915-4924.
18. Sahin Z, Canpolat S, Ozcan M, Ozgocer T, Kelestimur H. Kisspeptin antagonist prevents RF9-induced reproductive changes in female rats. Reproduction. 2015;149(5):465-473.
19. Kuohung W, Burnett M, Mukhtyar D, et al. A high-throughput small-molecule ligand screen targeted to agonists and antagonists of the G-protein-coupled receptor GPR54. J Biomol Screen. 2010;15: 508-517.
20. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614-1627.
21. Min L, Soltis K, Reis AC, et al. Dynamic kisspeptin receptor trafficking modulates kisspeptin-mediated calcium signaling. Mol Endocrinol. 2014;28:16-27.
22. Bianco SD, Vandepas L, Correa-Medina M, et al. KISS1R intracellular trafficking and degradation: Effect of the Arg386Pro diseaseassociated mutation. Endocrinology. 2011;152:1616-1626.
23. Ahow M, Min L, Pampillo M, et al. KISS1R signals independently of Gαq/11 and triggers LH secretion via the β-arrestin pathway in the male mouse. Endocrinology. 2014;155:4433-4446.
24. Kirilov M, Clarkson J, Liu X, et al. Dependence of fertility on kisspeptin- Gpr54 signaling at the GnRH neuron. Nat Commun. 2013; 4:2492.
25. Ohtaki T, Shintani Y, Honda S, et al. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature. 2001;411:613-617.
26. Kotani M, Detheux M, Vandenbogaerde A, et al. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem. 2001; 276:34631-34636.
27. May LT, Leach K, Sexton PM, Christopoulos A. Allosteric modulation of G protein-coupled receptors. Annu Rev Pharmacol Toxicol. 2007;47:1-51.
28. Kriegsfeld LJ, Ubuka T, Bentley GE, Tsutsui K. Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals. Front Neuroendocrinol. 2015;37:65-75.
29. Bentley GE, Perfito N, Ukena K, Tsutsui K, Wingfield JC. Gonadotropin- inhibitory peptide in song sparrows (Melospiza melodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J Neuroendocrinol. 2003;15:794-802.
30. Chowdhury VS, Yamamoto K, Ubuka T, Bentley GE, Hattori A, Tsutsui K. Melatonin stimulates the release of gonadotropin-inhibitory hormone by the avian hypothalamus. Endocrinology. 2010; 151:271-280.
31. Tsutsui K, Osugi T. Evolutionary origin and divergence of GnIH and its homologous peptides. Gen Comp Endocrinol. 2009;161: 30-33.
32. Kriegsfeld LJ, Gibson EM, Williams WP 3rd, et al. The roles of RFamide-related peptide-3 in mammalian reproductive function and behaviour. J Neuroendocrinol. 2010;22:692-700.
33. Clarke IJ, Sari IP, Qi Y, et al. Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology. 2008;149:5811-5821.
34. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-amiderelated peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology. 2009;150:5549-5556.
35. Kadokawa H, Shibata M, Tanaka Y, et al. 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. 2009;36:219-224.
36. Ubuka T, Inoue K, Fukuda Y, et al. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology. 2012;153:373-385.
37. Gojska NM, Friedman Z, Belsham DD. Direct regulation of gonadotrophin- releasing hormone (GnRH) transcription by RF-amiderelated peptide-3 and kisspeptin in a novel GnRH-secreting cell line, mHypoA-GnRH/GFP. J Neuroendocrinol. 2014;26:888-897.
38. Poling MC, Kim J, Dhamija S, Kauffman AS. Development, sex steroid regulation, and phenotypic characterization of RFamiderelated peptide (Rfrp) gene expression and RFamide receptors in the mouse hypothalamus. Endocrinology. 2012;153:1827-1840.
39. Murakami M, Matsuzaki T, Iwasa T, et al. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol. 2008;199:105-112.
40. Ancel C, Bentsen AH, Sébert ME, Tena-Sempere M, Mikkelsen JD, Simonneaux V. Stimulatory effect of RFRP-3 on the gonadotrophic axis in the male Syrian hamster: The exception proves the rule. Endocrinology. 2012;153:1352-1363.
41. Maletínská L, Tichá A, Nagelová V, et al. Neuropeptide FF analog RF9 is not an antagonist of NPFF receptor and decreases food intake in mice after its central and peripheral administration. Brain Res. 2013;1498:33-40.
42. Oishi S, Misu R, Tomita K, et al. Activation of Neuropeptide FF Receptors by Kisspeptin Receptor Ligands. ACS Med Chem Lett. 2011;2:53-57.
43. Kim JS, Brownjohn PW, Dyer BS, et al. Anxiogenic and Stressor Effects of the Hypothalamic Neuropeptide RFRP-3 are Overcome by a Novel Antagonist. Endocrinology. 2015:en20151532.
44. Liu X, Herbison A. Kisspeptin regulation of arcuate neuron excitability in kisspeptin receptor knockout mice. Endocrinology. 2015; 156:1815-1827.
45. Thompson EL, Patterson M, Murphy KG, et al. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic- pituitary-gonadal axis. J Neuroendocrinol. 2004;16:850-858.