The RFamide neuropeptide 26RFa and its role in the control of neuroendocrine functions

Frontiers in Neuroendocrinology

Volumn 32, Issue 4, 2011, Pages 387-397

  Chartrel, Nicolas ^a   Alonzeau, Jessy ^a   Alexandre, David ^a   Jeandel, Lydie ^a   Alvear Perez, Rodrigo ^b   Leprince, Jérôme ^a   Boutin, Jean ^c   Vaudry, Hubert ^a   Anouar, Youssef ^a   Llorens Cortes, Catherine ^b  

^a UNIVERSITÉ DE ROUEN   (France)

^b l'alimentation et l'Environnement   (France)

^c INSTITUT DE RECHERCHES SERVIER   (France)

Author keywords

Evolution; Feeding behavior; G protein coupled receptor; Hypothalamo pituitary gonadal axis; Hypothalamus; Neuropeptide; RFamide peptide; Vertebrate

Indexed keywords

AMINE; ARGININE; G PROTEIN COUPLED RECEPTOR; LIGAND; NEUROPEPTIDE; PHENYLALANINE; RFAMIDE NEUROPEPTIDE 26RFA; UNCLASSIFIED DRUG;

ARTERIAL PRESSURE; BIOLOGICAL ACTIVITY; BIRD; CARBOXY TERMINAL SEQUENCE; EVOLUTION; FEEDING BEHAVIOR; FISH; HUMAN; MAMMAL; NEUROENDOCRINE FUNCTION; NEUROENDOCRINE SYSTEM; NOCICEPTION; NONHUMAN; OSSIFICATION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; REVIEW; STEROIDOGENESIS; UPREGULATION; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; HUMANS; MODELS, BIOLOGICAL; NEUROENDOCRINE CELLS; NEUROPEPTIDES; RECEPTORS, G-PROTEIN-COUPLED; TISSUE DISTRIBUTION; VERTEBRATES;

EID: 80053113944     PISSN: 00913022     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.yfrne.2011.04.001     Document Type: Review

References (79)

1. Askwith C.C., Cheng C., Ikuma M., Benson C., Price M.P., Welsh M.J. Neuropeptide FF and FMRFamide potentiate acid-evoked currents from sensory neurons and proton-gated DEG/EnaC channels. Neuron 2000, 26:133-141.
2. Bäckberg M., Hervieu G., Wilson S., Meister B. Orexin receptor-1 (OX-R1) immunoreactivity in chemically identified neurons of the hypothalamus: focus on orexin targets involved in control of food and water intake. Eur. J. Neurosci. 2002, 15:315-328.
3. Baldock P.A., Sainsbury A., Couzens M., Enriquez R.F., Thomas G.P., Gardiner E.M., Herzog H. Hypothalamic Y2 receptors regulate bone formation. J. Clin. Invest. 2002, 109:915-921.
4. Baribault H., Danao J., Gupte J., Yang L., Sun B., Richards W., Tian H. The G-protein-coupled receptor GPR103 regulates bone formation. Mol. Cell. Biol. 2006, 26:709-717.
5. Beck B. KO's and organization of peptidergic feeding behavior mechanisms. Neurosci. Biobehav. Rev. 2001, 25:143-158.
6. Beck B., Richy S. Suppression of QRFP 43 in the hypothalamic ventromedial nucleus of Long-Evans rats fed a high-fat diet. Biochem. Biophys. Res. Commun. 2009, 383:78-82.
7. Bohlooly Y.M., Mahlapuu M., Andersen H., Astrand A., Hjorth S., Svensson L., Tornell J., Snaith M.R., Morgan D.G., Ohlsson C. Osteoporosis in MCHR1-deficient mice. Biochem. Biophys. Res. Commun. 2004, 318:964-969.
8. Bonini J.A., Jones K.A., Adham N., Forray C., Artymyshyn R., Durkin M.M., Smith K.E., Tamm J.A., Boteju L.W., Lakhlani P.P., Raddatz R., Yao W.J., Ogozalek K.L., Boyle N., Kouranova E.V., Quan Y., Vaysse P.J., Wetzel J.M., Branchek T.A., Gerald C., Borowsky B. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J. Biol. Chem. 2000, 275:39324-39331.
9. Bowman J.W., Friedman A.R., Thompson D.P., Ichpurani A.K., Kellman M.F., Marks N., Maule A.G., Geary T.G. Structure-activity relationships of KNEFIRFamide (AF1), a nematode FMRFamide-related peptide, on Ascaris suum muscle. Peptides 1996, 17:381-387.
10. Bruzzone F., Lectez B., Tollemer H., Leprince J., Dujardin C., Rachidi W., Chatenet D., Baroncini M., Beauvillain J.C., Vallarino M., Vaudry H., Chartrel N. Anatomical distribution and biochemical characterization of the novel RFamide peptide 26RFa in the human hypothalamus and spinal cord. J. Neurochem. 2006, 99:616-627.
11. Bruzzone F., Lectez B., Alexandre D., Jégou S., Mounien L., Tollemer H., Chatenet D., Leprince J., Vallarino M., Vaudry H., Chartrel N. Distribution of 26RFa binding sites and GPR103 mRNA in the central nervous system of the rat. J. Comp. Neurol. 2007, 503:573-591.
12. Chartrel N., Dujardin C., Leprince J., Desrues L., Tonon M.C., Cellier E., Jouenne T., Simonnet G., Vaudry H. Isolation, characterization and distribution of a novel neuropeptide, Rana RFamide (R-RFa), in the brain of the European green frog Rana esculenta. J. Comp. Neurol. 2002, 448:111-127.
13. Chartrel N., Dujardin C., Anouar Y., Leprince J., Decker A., Clerens S., Do-Régo J.C., Vandesande F., Llorens-Cortes C., Costentin J., Beauvillain J.C., Vaudry H. Identification of 26RFa, a hypothalamic neuropeptide of the RFamide peptide family with orexigenic activity. Proc. Natl. Acad. Sci. USA 2003, 100:15247-15252.
14. Chartrel N., Bruzzone F., Leprince J., Tollemer H., Anouar Y., Do-Rego J.C., Ségalas-Milazzo I., Guilhaudis L., Cosette P., Jouenne T., Simmonet G., Beauvillain J.C., Costentin J., Vaudry H. Structure and functions of the novel RFamide neuropeptides R-RFa and 26RFa in vertebrates. Peptides 2006, 27:1110-1120.
15. Chartrel N., Tsutsui K., Costentin J., Vaudry H. The RFamide-related peptides. Handbook of Biologically Active Peptides 2006, 779-786. Academic press, San Diego. A.J. Kastin (Ed.).
16. Ciriello J., McMurray J.C., Babic T., de Oliveira C.V. Collateral axonal projections from hypothalamic hypocretin neurons to cardiovascular sites in nucleus ambiguus and nucleus tractus solitarius. Brain Res. 2003, 991:133-141.
17. Cottrell G.A., Schot L.P., Dockray G.J. Identification and probable role of a single neuron containing the neuropeptide Helix FMRFamide. Nature 1983, 304:638-640.
18. Dockray G.J., Vaillant C., Williams R.G. New vertebrate brain-gut peptide related to a molluscan neuropeptide and an opioid peptide. Nature 1981, 293:656-657.
19. Dockray G.J. The expanding family of -RFamide peptides and their effects on feeding behavior. Exp. Physiol. 2004, 89:229-235.
20. Do Rego J.C., Leprince J., Chartrel N., Vaudry H., Costentin J. Behavioral effects of 26RFamide and related peptides. Peptides 2006, 27:2715-2721.
21. Dube M.G., Horvath T.L., Kalra P.S. Evidence of NPY Y5 receptor involvement in food intake elicited by orexin A in sated rats. Peptides 2000, 21:1557-1560.
22. Ducy P., Amling M., Takeda S., Priemel M., Schilling A.F., Beil F.T., Shen J., Vinson C., Rueger J.M., Karsenty G. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000, 100:197-207.
23. Egido E.M., Hernández R., Leprince J., Chartrel N., Vaudry H., Marco J., Silvestre R.A. 26RFa, a novel orexigenic neuropeptide, inhibits insulin secretion in the rat pancreas. Peptides 2007, 28:725-730.
24. Elefteriou F., Karsenty G. Bone mass regulation by leptin: a hypothalamic control of bone formation. Pathol. Biol. (Paris) 2004, 52:148-153.
25. Elefteriou F., Ahn J.D., Takeda S., Starbuck M., Yang X., Liu X., Kondo H., Richards W.G., Bannon T.W., Noda M., Clement K., Vaisse C., Karsenty G. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature 2005, 434:514-520.
26. Elshourbagy N.A., Ames R.S., Fitzgerald L.R., Foley J.J., Chambers J.K., Szekeres P.G., Evans N.A., Schmidt D.B., Buckley P.T., Dytko G.M., Murdock P.R., Milligan G., Groarke D.A., Tan K.B., Shabon U., Nuthulaganti P., Wang D.Y., Wilson S., Bergsma D.J., Sarau H.M. Receptor for the pain modulatory neuropeptides FF and AF is an orphan G protein-coupled receptor. J. Biol. Chem. 2000, 275:25965-25971.
27. Engström M., Brandt A., Wurster S., Savola J.M., Panula P. Prolactin releasing peptide has high affinity and efficacy at neuropeptide FF2 receptors. J. Pharmacol. Exp. Ther. 2003, 305:825-832.
28. Fang Q., Liu Q., Jiang T.N., Li Y.L., Yan X., Wang R. Cardiovascular effects of intravenous administered 26RFa, a novel RFamide peptide ligand for GPR103, in anaesthetized rats. Eur. J. Pharmacol. 2009, 621:61-66.
29. Finkelstein J.S., Dawson-Hughes B. Osteoporosis. Cecil Textbook of Medicine 2000, 1366-1373. W.B. Saunders Co., Philadelphia. 21st ed. L. Goldman, J.C. Bennett (Eds.).
30. Fukusumi S., Fujii R., Hinuma S. Recent advances in mammalian RFamide peptides: the discovery and functional analyses of PrRP, RFRPs and QRFP. Peptides 2006, 27:1073-1086.
31. Fukusumi S., Yoshida H., Fujii R., Maruyama M., Komatsu H., Habata Y., Shintani Y., Hinuma S., Fujino M. A new peptidic ligand and its receptor regulating adrenal function in rats. J. Biol. Chem. 2003, 278:46387-46395.
32. Gensure R.C., Shimizu N., Tsang J., Gardella T.J. Identification of a contact site for residue 19 of parathyroid hormone (PTH) and PTH-related protein analogs in transmembrane domain two of the type 1 PTH receptor. Mol. Endocrinol. 2003, 17:2647-2658.
33. Gorwood P., Kipman A., Foulon C. The human genetics of anorexia nervosa. Eur. J. Pharmacol. 2003, 480:163-170.
34. Gouardères C., Puget A., Zajac J.M. Detailed distribution of neuropeptide FF receptors (NPFF1 and NPFF2) in the rat, mouse, octodon, rabbit, guinea pig, and marmoset monkey brains: a comparative autoradiographic study. Synapse 2004, 51:249-269.
35. 35S]GTPγS binding. Neuropharmacology 2007, 52:376-386.
36. Gu W., Geddes B.J., Zhang C., Foley K.P., Stricker-Krongrad A. The prolactin-releasing peptide receptor (GPR10) regulates body weight homeostasis in mice. J. Mol. Neurosci. 2004, 22:93-103.
37. Hernandez C., Carrasco E., Casamitjana R., Deulofeu R., Garcia-Arumi J., Simo R. Somatostatin variants in the vitreous fluid: a comparative study between diabetic patients with proliferative diabetic retinopathy and nondiabetic control subjects. Diabet. Care 2005, 28:1941-1947.
38. Jiang Y., Luo L., Gustafson E.L., Yadav D., Laverty M., Murgolo N., Vassileva G., Zeng M., Laz T.M., Behan J., Qiu P., Wang L., Wang S., Bayne M., Greene J., Monsma F., Zhang F.L. Identification and characterization of a novel RF-amide peptide ligand for orphan G-protein-coupled receptor SP9155. J. Biol. Chem. 2003, 278:27652-27657.
39. Kampe J., Wiedmer P., Pfluger P.T., Castaneda T.R., Burget L., Mondala H., Kerr J., Liaw C., Oldfield B.J., Tschöp M.H., Bagnol D. Effect of central administration of QRFP(26) peptide on energy balance and characterization of a second QRFP receptor in rat. Brain Res. 2006, 1119:133-149.
40. Karsenty G. Leptin controls bone formation through a hypothalamic relay. Recent Prog. Horm. Res. 2001, 56:401-415.
41. Koch G., Chen M.L., Sharla R., Walker R.J. The actions of neuroactive peptides on the isolated heart of the giant African snail, Achatina fulica. Comp. Biochem. Physiol. C 1993, 106:359-365.
42. Lawrence C.B., Liu Y.L., Stock M.J., Luckman S.M. Anorectic actions of prolactin-releasing peptide are mediated by corticotropin-releasing hormone receptors. Am. J. Physiol. 2004, 286:R101-R107.
43. Lawrence C.B., Ellacott K.L., Luckman S.M. PRL-releasing peptide reduces food intake and may mediate satiety signaling. Endocrinology 2002, 143:360-367.
44. Lectez B., Jeandel L., El-Yamani F.Z., Arthaud S., Alexandre D., Mardargent A., Jégou S., Mounien L., Bizet P., Magoul R., Anouar Y., Chartrel N. The orexigenic activity of the hypothalamic neuropeptide 26RFa is mediated by the neuropeptide Y and proopiomelanocortin neurons of the arcuate nucleus. Endocrinology 2009, 150:2342-2350.
45. Lee D.K., Nguyen T., Lynch K.R., Cheng R., Vanti W.B., Arkhitko O., Lewis T., Evans J.F., George S.R., O'Dowd B.F. Discovery and mapping of ten novel G protein-coupled receptor genes. Gene 2001, 275:83-91.
46. Lesser W., Greenberg M.J. Cardiac regulation by endogenous small cardioactive peptides and FMRFamide-related peptides in the snail Helix aspersa. J. Exp. Biol. 1993, 178:205-230.
47. Li C., Kyuhyung K., Nelson L.S. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res. 1999, 848:26-34.
48. Linacre B., Kellett E., Saunders S., Bright K., Benjamin P.R., Burke J.F. Cardioactive neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) and novel related peptides are encoded in multiple copies by a single gene in the snail Lymnea stagnalis. J. Neurosci. 1990, 10:412-419.
49. Liu Y., Zhang Y., Li S., Huang W., Liu X., Lu D., Meng Z., Lin H. Molecular cloning and functional characterization of the first non-mammalian 26RFa/QRFP orthologue in goldfish, Carassius auratus. Mol. Endocrinol. 2009, 303:82-90.
50. López M., Seoane L.M., García Medel C., Diéguez C., Señarís R. Neuropeptide Y, but not agouti-related peptide or melanin-concentrating hormone, is a target peptide for orexin-A feeding actions in the rat hypothalamus. Neuroendocrinology 2002, 75:34-44.
51. Moriya R., Sano H., Umeda T., Ito M., Takahashi Y., Matsuda M., Ishihara A., Kanatani A., Iwaasa H. RFamide peptide QRFP43 causes obesity with hyperphagia and reduced thermogenesis in mice. Endocrinology 2006, 147:2916-2922.
52. Mulumba M., Jossart C., Granata R., Gallo D., Escher E., Ghigo E., Servant M.J., Marleau S., Ong H. GPR103b functions in the peripheral regulation of adipogenesis. Mol. Endocrinol. 2010, 24:1615-1625.
53. Murase T., Arima H., Kondo K., Oiso Y. Neuropeptide FF reduces food intake in rats. Peptides 1996, 17:353-354.
54. Navarro V.M., Fernández-Fernández R., Nogueiras R., Vigo E., Tovar S., Chartrel N., Le Marec O., Leprince J., Aguilar E., Pinilla L., Dieguez C., Vaudry H., Tena-Sempere M. Novel role of 26RFa, a hypothalamic RFamide orexigenic peptide, as putative regulator of the gonadotropic axis. J. Physiol. 2006, 573:237-249.
55. Nelson L.S., Rosoff M.L., Li C. Disruption of a neuropeptide gene, flp-1, causes multiple behavioural defects in Caenorhabditis elegans. Science 1998, 281:1686-1690.
56. Nichols R., Demers L.A., Larsen B.M., Robinson D., Converso K., Russell M.W., Westfall M.V. Human RFamide-related peptide-1 diminishes cellular and integrated cardiac contractile performance. Peptides 2010, 31:2067-2074.
57. Patel S.R., Murphy K.G., Thompson E.L., Patterson M., Curtis A.E., Ghatei M.A., Bloom S.R. Pyroglutamylated RFamide peptide 43 stimulates the hypothalamic-pituitary-gonadal axis via gonadotropin-releasing hormone in rats. Endocrinology 2008, 149:4747-4754.
58. Pineda R., Aguilar E., Pinilla L., Tena-Sempere M. Physiological role of the kisspeptin/GPR54 system in the neuroendocrine control of reproduction. Prog. Brain Res. 2010, 181:55-77.
59. Price D.A., Greenberg M. Structure of a molluscan cardioexcitatory neuropeptide. Science 1977, 197:670-671.
60. Primeaux S.D., Blackmon C., Barnes M.J., Braymer D., Bray G.A. Central administration of the RFamide peptides, QRFP-26 and QRFP-43, increases high fat food intake in rats. Peptides 2008, 29:1994-2000.
61. Sakai T., Satake H., Minakata H., Takeda M. Characterization of crustacean cardioactive peptide as a novel insect midgut factor: isolation, localization and stimulation of α-amylase activity and gut contraction. Endocrinology 2004, 145:5671-5678.
62. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., Williams S.C., Richarson J.A., Kozlowski G.P., Wilson S., Arch J.R., Buckingham R.E., Haynes A.C., Carr S.A., Annan R.S., McNulty D.E., Liu W.S., Terrett J.A., Elshourbagy N.A., Bergsma D.J., Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behaviour. Cell 1998, 92:573-585.
63. Salzet M., Bulet P., Wattez C., Malecha J. FMRFamide-related peptides in the sex segmental ganglia of the Pharyngobdellid leech, Erpobdella octoculata, identification and involvement in the control of hydric balance. Eur. J. Biochem. 1994, 221:269-275.
64. Schaefer M., Picciotto M.R., Kreiner T., Kaldany R.R., Taussig R., Scheller R.H. Aplysia neurons express a gene encoding multiple FMRFamide neuropeptides. Cell 1985, 41:457-467.
65. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno J.S., Shagoury J.K., Bo-Abbas Y., Kuohung W., Schwinof K.M., Hendrick A.G., Zahn D., Dixon J., Kaiser U.B., Slaugenhaupt S.A., Gusella J.F., O'Rahilly S., Carlton M.B., Crowley W.F., Aparicio S.A., Colledge W.H. The GPR54 gene as a regulator of puberty. New Engl. J. Med. 2003, 349:1614-1627.
66. Steppan C.M., Crawford D.T., Chidsey-Frink K.L., Ke H., Swick A.G. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul. Pept. 2000, 92:73-78.
67. Sunter D., Hewson A.K., Lynam S., Dickson S.L. Intracerebroventricular injection of neuropeptide FF, an opioid modulating neuropeptide, acutely reduces food intake and stimulates water intake in the rat. Neurosci. Lett. 2001, 313:145-148.
68. Takayasu S., Sakurai T., Iwasaki S., Teranishi H., Yamanaka A., Williams S.C., Iguchi H., Kawasawa Y.I., Ikeda Y., Sakakibara I., Ohno K., Ioka R.X., Murakami S., Dohmae N., Xie J., Suda T., Motoike T., Ohuchi T., Yanagisawa M., Sakai J. A neuropeptide ligand of the G protein-coupled receptor GPR103 regulates feeding, behavioral arousal, and blood pressure in mice. Proc. Natl. Acad. Sci. USA 2006, 103:7438-7443.
69. Takeda S. Central control of bone metabolism. Clin. Calcium 2005, 15:797-804.
70. Thuau R., Guilhaudis L., Ségalas-Milazzo I., Chartrel N., Oulyadi H., Boivin S., Fournier A., Leprince J., Davoust D., Vaudry H. Structural studies on 26RFa, a novel human RFamide-related peptide with orexigenic activity. Peptides 2005, 26:779-789.
71. Troger J., Neyer S., Heufler C., Huemer H., Schmid E., Griesser U., Kralinger M., Kremser B., Baldissera I., Kieselbach G. Substance P and vasointestinal polypeptide in the streptozotocin-induced diabetic rat retina. Invest. Ophthalmol. Vis. Sci. 2001, 42:1045-1050.
72. Tsutsui K., Bentley G.E., Bedecarrats G., Osugi T., Ubuka T., Kriegsfeld L.J. Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front. Neuroendocrinol. 2010, 31:284-295.
73. Ukena K., Tachibana T., Iwakoshi-Ukena E., Saito Y., Minakata H., Kawaguchi R., Osugi T., Tobari Y., Leprince J., Vaudry H., Tsutsui K. Identification, localization, and function of a novel hypothalamic neuropeptide, 26RFa, and its cognate receptor, G protein-coupled receptor-103. Endocrinology 2010, 151:2255-2264.
74. Wade G.N., Jones J.E. Neuroendocrinology of nutritional infertility. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R1277-R1296.
75. Weber E., Evans C.J., Samuelsson S.J., Barchas J.D. Novel peptide neuronal system in rat brain and pituitary. Science 1981, 214:1248-1251.
76. Yamamoto T., Wada T., Miyazaki R. Analgesic effects of intrathecally administered 26RFa, an intrinsic agonist for GPR103, on formalin test and carrageenan test in rats. Neuroscience 2008, 157:214-222.
77. Yamamoto T., Miyazaki R., Yamada T. Intracerebroventricular administration of 26RFa produces an analgesic effect in the rat formalin test. Peptides 2009, 30:1683-1688.
78. Yamanaka A., Kunii K., Nambu T., Tsujino N., Sakai A., Matsuzaki I., Miwa Y., Goto K., Sakurai T. Orexin-induced food intake involves neuropeptide Y pathway. Brain Res. 2000, 859:404-409.
79. Zhang Q., Qiu P., Arreaza M.G., Simon J.S., Golovko A., Laverty M., Vassileva G., Gustafson E.L., Rojas-Triana A., Bober L.A., Hedrick J.A., Monsma F.J., Greene J.R., Bayne M.L., Murgolo N.J. P518/Qrfp sequence polymorphisms in SAMP6 osteopenic mouse. Genomics 2007, 90:629-635.