Neuropeptide RFRP inhibits the pacemaker activity of terminal nerve GnRH neurons

Journal of Neurophysiology

Volumn 109, Issue 9, 2013, Pages 2354-2363

  Umatani, Chie ^a   Abe, Hideki ^a   Oka, Yoshitaka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Dwarf gourami; Gonadotropin releasing hormone; Neuromodulation; Peptide; RFamide related peptide

Indexed keywords

GONADORELIN; NEUROPEPTIDE FF; TRANSIENT RECEPTOR POTENTIAL CANONICAL; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CEREBROSPINAL FLUID; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; MALE; NERVE CELL; NEUROMODULATION; NONHUMAN; PACEMAKER; PARACRINE SIGNALING; PRIORITY JOURNAL;

DWARF GOURAMI; GONADOTROPIN-RELEASING HORMONE; NEUROMODULATION; PEPTIDE; RFAMIDE-RELATED PEPTIDE;

ACTION POTENTIALS; ANIMALS; BARIUM; BIOLOGICAL CLOCKS; BORON COMPOUNDS; CRANIAL NERVES; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; LANTHANUM; NEURONS; NEUROPEPTIDES; PERCIFORMES; POTASSIUM; SODIUM; SYNAPSES; TRPC CATION CHANNELS;

EID: 84878505493     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00712.2012     Document Type: Article

References (43)

1. Abe H, Oka Y. Modulation of pacemaker activity by salmon gonadotropin releasing hormone (sGnRH) in terminal nerve (TN)-GnRH neurons. J Neurophysiol 83: 3196-3200, 2000.
2. Abe H, Oka Y. Neuromodulatory functions of terminal nerve-GnRH neurons. In: Fish Physiology. Sensory Systems Neuroscience, edited by Hara TJ and Zielenski B. San Diego, CA: Elsevier, 2006, vo. 25, p. 455-503.
3. Abe H, Oka Y. Primary culture of the isolated terminal nerve gonadotrophin releasing hormone neurons derived from adult teleost (dwarf gourami, Colisa lalia) brain for the study of peptide release mechanisms. J Neuroen docrinol 21: 489-505, 2009.
4. Abe H, Oka Y. Mechanisms of neuromodulation by a nonhypophysiotropic GnRH system controlling motivation of reproductive behavior in the teleost brain. J Reprod Dev 57: 665 674, 2011.
5. Adams PR, Brown DA. Luteinizing hormone-releasing factor and muscarinic agonists act on the same voltage-sensitive K-current in bullfrog sympa thetic neurones. Br J Pharmacol 68: 353-355, 1980.
6. Calisi RM, Rizzo NO, Bentley GE. Seasonal differences in hypothalamic EGR-1 and GnIH expression following capture-handling stress in house sparrows (Passer domesticus). Gen Comp Endocrinol 157: 283-287, 2008.
7. Chen JC, Lee WH, Chen PC, Tseng CP, Huang EY. Rat NPFF(1) receptor mediated signaling: functional comparison of neuropeptide FF (NPFF), FMRFamide and PFR(Tic)amide. Peptides 27: 1005-1014, 2006.
8. 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.
9. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonado tropin-releasing hormone neuron firing in the mouse. Endocrinology 150: 2799-2804, 2009.
10. Eisthen HL, Delay RJ, Wirsig-Wiechmann CR, Dionne VE. Neuromodu latory effects of gonadotropin releasing hormone on olfactory receptor neurons. J Neurosci 20: 3947-3955, 2000.
11. Fujita I, Sorensen PW, Stacey NE, Hara TJ. The olfactory system, not the terminal nerve, functions as the primary chemosensory pathway mediating responses to sex pheromones in male goldfish. Brain Behav Evol 38: 313-321, 1991.
12. Fukusumi S, Fujii R, Hinuma S. Recent advances in mammalian RFamide peptides: the discovery and functional analyses of PrRP, RFRPs and QRFP. Peptides 27: 1073-1086, 2006.
13. 3]NPFF. Brain Res Bull 42: 231-238, 1997.
14. 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 con taining carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol 2: 703-708, 2000.
15. Honore E. The neuronal background K2P channels: focus on TREK1. Nat Rev Neurosci 8: 251-261, 2007.
16. Ishizaki M, Iigo M, Yamamoto N, Oka Y. Different modes of gonadotropin releasing hormone (GnRH) release from multiple GnRH systems as revealed by radioimmunoassay using brain slices of a teleost, the dwarf gourami (Colisa lalia). Endocrinology 145: 2092-2103, 2004.
17. Johnson MA, Tsutsui K, Fraley GS. Rat RFamide-related peptide-3 stimu lates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm Behav 51: 171-180, 2007.
18. Kinoshita M, Kobayashi S, Urano A, Ito E. Neuromodulatory effects of gonadotropin-releasing hormone on retinotectal synaptic transmission in the optic tectum of rainbow trout. Eur J Neurosci 25: 480-484, 2007.
19. Kirby ED, Geraghty AC, Ubuka T, Bentley GE, Kaufer D. Stress increases putative gonadotropin inhibitory hormone and decreases luteinizing hor mone in male rats. Proc Natl Acad Sci USA 106: 11324-11329, 2009.
20. Kiya T, Oka Y. Glutamate receptors in the terminal nerve gonadotropin releasing hormone neurons of the dwarf gourami (teleost). Neurosci Lett 345: 113-116, 2003.
21. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K, Silver R. Identification and characterization of a gonadotro pin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 103: 2410-2415, 2006.
22. Lesage F. Pharmacology of neuronal background potassium channels. Neuro pharmacology 44: 1-7, 2003.
23. Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, Zeng Z, Jacobson M, Williams DL Jr, Yu H, Bomford D, Figueroa D, Mallee J, Wang R, Evans J, Gould R, Austin CP. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276: 36961 36969, 2001.
24. Matsumoto S, Yamamoto N, Akazome Y, Yamada S, Tsukamura H, Maeda K, Oka Y. Possible novel function of metastin neurons as dual neuromodulators in the vertebrate brain. Program of the 36th Annual Meeting of The Society for Neuroscience, Atlanta, GA, 2006, p. 658.6.
25. Mollereau C, Mazarguil H, Marcus D, Quelven I, Kotani M, Lannoy V, Dumont Y, Quirion R, Detheux M, Parmentier M, Zajac JM. Pharma cological characterization of human NPFF(1) and NPFF(2) receptors ex pressed in CHO cells by using NPY Y(1) receptor antagonists. Eur J Pharmacol 451: 245-256, 2002.
26. Nakane R, Oka Y. Excitatory action of GABA in the terminal nerve gonad otropin-releasing hormone neurons. J Neurophysiol 103: 1375-1384, 2010.
27. Oka Y. Physiology and release activity of GnRH neurons. Prog Brain Res 141: 259-281, 2002.
28. Oka Y, Ichikawa M. Ultrastructure of the ganglion cells of the terminal nerve in the dwarf gourami (Colisa lalia). J Comp Neurol 304: 161-71, 1991.
29. Oka Y, Matsushima T. Gonadotropin-releasing hormone (GnRH)-immuno reactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J Neurosci 13: 2161-2176, 1993.
30. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, Dijcks FA, Blomenrohr M, Pinilla L, van Noort PI, Tena-Sempere M. 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. Am J Physiol Endocrinol Metab 299: E39-E46, 2010.
31. Qiu J, Fang Y, Ronnekleiv OK, Kelly MJ. Leptin excites proopiomelano cortin neurons via activation of TRPC channels. J Neurosci 30: 1560-1565, 2010.
32. Rasolonjanahary R, Gerard C, Dufour MN, Homburger V, Enjalbert A, Guillon G. Evidence for a direct negative coupling between dopamine-D2 receptors and PLC by heterotrimeric Gi1/2 proteins in rat anterior pituitary cell membranes. Endocrinology 143: 747-754, 2002.
33. Roumy M, Zajac JM. Neuropeptide FF, pain and analgesia. Eur J Pharmacol 345: 1-11, 1998.
34. 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 Neuro physiol 104: 3518-3529, 2010.
35. Simonin F, Schmitt M, Laulin JP, Laboureyras E, Jhamandas JH, Mac Tavish D, Matifas A, Mollereau C, Laurent P, Parmentier M, Kieffer BL, Bourguignon JJ, Simonnet G. RF9, a potent and selective neuropep tide FF receptor antagonist, prevents opioid-induced tolerance associated with hyperalgesia. Proc Natl Acad Sci USA 103: 466-471, 2006.
36. 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.
37. Watkins DC, Moxham CM, Morris AJ, Malbon CC. Suppression of Gi alpha 2 enhances phospholipase C signalling. Biochem J 299: 593-596, 1994.
38. Xiao Z, Deng PY, Rojanathammanee L, Yang C, Grisanti L, Permpoon puttana K, Weinshenker D, Doze VA, Porter JE, Lei S. Noradrenergic depression of neuronal excitability in the entorhinal cortex via activation of TREK-2 K channels. J Biol Chem 284: 10980-10991, 2009.
39. Yamamoto N, Oka Y, Amano M, Aida K, Hasegawa Y, Kawashima S. Multiple gonadotropin-releasing hormone (GnRH)-immunoreactive systems in the brain of the dwarf gourami, Colisa lalia: immunohistochemistry and radioimmunoassay. J Comp Neurol 355: 354-368, 1995.
40. Yamamoto N, Oka Y, Kawashima S. Lesions of gonadotropin-releasing hormone-immunoreactive terminal nerve cells: effects on the reproduc tive behavior of male dwarf gouramis. Neuroendocrinology 65: 403 412, 1997.
41. Yang SN, Lu F, Wu JN, Liu DD, Hsieh WY. Activation of gonadotropin releasing hormone receptors induces a long-term enhancement of excitatory postsynaptic currents mediated by ionotropic glutamate receptors in the rat hippocampus. Neurosci Lett 260: 33-36, 1999.
42. Zeng Z, McDonald TP, Wang R, Liu Q, Austin CP. Neuropeptide FF receptor 2 (NPFF2) is localized to pain-processing regions in the primate spinal cord and the lower level of the medulla oblongata. J Chem Neuroanat 25: 269-278, 2003.
43. Zhang C, Roepke TA, Kelly MJ, Ronnekleiv OK. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 28: 4423 4434, 2008.