Characterization of novel RFamide peptides in the central nervous system of the brown hagfish: Isolation, localization, and functional analysis

Endocrinology

Volumn 152, Issue 11, 2011, Pages 4252-4264

  Osugi, Tomohiro ^a   Uchida, Katsuhisa ^b,c   Nozaki, Masumi ^b   Tsutsui, Kazuyoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE; ARGININE; COMPLEMENTARY DNA; GLUTAMINE; GONADOTROPIN; GONADOTROPIN BETA; MESSENGER RNA; NEUROPEPTIDE; NEUROPEPTIDE AF; NEUROPEPTIDE FF; PEPTIDE; PHENYLALANINE; PROLINE; RFAMIDE PEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN; BRAIN REGION; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; HAGFISH; HYPOPHYSIS; HYPOTHALAMUS; IMMUNOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR CLONING; MOLECULAR PHYLOGENY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; VERTEBRATE;

ANIMALS; BRAIN; FEMALE; HAGFISHES; MALE; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; PITUITARY GLAND; RNA, MESSENGER;

EID: 80054925597     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2011-1375     Document Type: Article

References (79)

1. Price DA, Greenberg MJ 1977 Structure of a molluscan cardioexcitatory neuropeptide. Science 197:670-671
2. López-Vera E, Aguilar MB, Heimer de la Cotera EP 2008 FMRFamide and related peptides in the phylum mollusca. Peptides 29: 310-317
3. Ukena T, Tsutsui K 2005 A new member of the hypothalamic RFamide peptide family, LPXRF-amide peptides: structure, localization, and function. Mass Spectrom Rev 24:469-486
4. Tsutsui K, Ukena K 2006 Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity. Peptides 27:1121-1129
5. Tsutsui K 2009 A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): biosynthesis, mode of action and functional significance. Prog Neurobiol 88:76-88
6. Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ 2010 Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrinol 31:284-295
7. Yang HYT, Fratta W, Majane EA, Costa E 1985 Isolation, sequencing, synthesis, and pharmacological characterization of two brain neuropeptides that modulate the action of morphine. Proc Natl Acad Sci USA 82:7757-7761
8. Burlet-Schiltz O, Mazarguil H, Sol JC, Chaynes P, Monsarrat B, Zajac JM, Roussin A 2002 Identification of neuropeptide FF-related peptides in human cerebrospinal fluid by mass spectrometry. FEBS Lett 532:313-318
9. Bonnard E, Burlet-Schiltz O, Monsarrat B, Girard JP, Zajac JM 2003 Identification of proNeuropeptide FFA peptides processed in neuronal and non-neuronal cells and in nervous tissue. Eur J Biochem 270:4187-4199
10. Perry SJ, Yi-Kung Huang E, Cronk D, Bagust J, Sharma R, Walker RJ, Wilson S, Burke JF 1997 A human gene encoding morphine modulating peptides related to NPFF and FMRFamide. FEBS Lett 409:426-430
11. Vilim FS, Aarnisalo AA, Nieminen ML, Lintunen M, Karlstedt K, Kontinen VK, Kalso E, States B, Panula P, Ziff E 1999 Gene for pain modulatory neuropeptide NPFF: induction in spinal cord by noxious stimuli. Mol Pharmacol 55:804-811
12. Liu Q, Guan XM, Martin WJ, McDonald TP, Clements MK, Jiang Q, Zeng Z, Jacobson M, Williams Jr DL, Yu H, Bomford D, Figueroa D, Mallee J, Wang R, Evans J, Gould R, Austin CP 2001 Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem 276:36961-36969
13. Roumy M, Lorenzo C, Mazères S, Bouchet S, Zajac JM, Mollereau C 2007 Physical association between neuropeptide FF and μ-opioid receptors as a possible molecular basis for anti-opioid activity. J Biol Chem 282:8332-8342
14. Kalliomäki ML, Panula P 2004 Neuropeptide FF, but not prolactinreleasing peptide, mRNA is differentially regulated in the hypothalamic and medullary neurons after salt loading. Neuroscience 124: 81-87
15. Goncharuk VD, Buijs RM, Mactavish D, Jhamandas JH 2006 Neuropeptide FF distribution in the human and rat forebrain: a comparative immunohistochemical study. JCompNeurol 496:572-593
16. Panula P, Aarnisalo AA, Wasowicz K 1996 Neuropeptide FF, a mammalian neuropeptide with multiple functions. Prog Neurobiol 48:461-487
17. Jhamandas JH, MacTavish D 2003 Central administration of neuropeptide FF causes activation of oxytocin paraventricular hypothalamic neurones that project to the brainstem. J Neuroendocrinol 15:24-32
18. Jhamandas JH, MacTavish D, Harris KH 2006 Neuropeptide FF (NPFF) control of magnocellular neurosecretory cells of the rat hypothalamic paraventricular nucleus (PVN). Peptides 27:973-979
19. Kotlinska J, Pachuta A, Dylag T, Silberring J 2007 The role of neuropeptide FF (NPFF) in the expression of sensitization to hyperlocomotor effect of morphine and ethanol. Neuropeptides 41:51-58
20. Oehlmann VD, Korte H, Sterner C, Korsching SI 2002 A neuropeptide FF-related gene is expressed selectively in neurons of the terminal nerve in Danio rerio. Mech Dev 117:357-361
21. Janvier P 2006 Modern look for ancient lamprey. Nature 443:921-924
22. Osugi T, Ukena K, Sower SA, Kawauchi H, Tsutsui K 2006 Evolutionary origin and divergence of PQRFamide peptides and LPXRFamide peptides in the RFamide peptide family: Insights from novel lamprey RFamide peptides. FEBS J 273:1731-1743
23. Jirikowski G, Erhart G, Grimmelikhuwijzen CJ, Triepel J, Patzner RA1984 FMRF-amide-like immunoreactivity in brain and pituitary of the hagfish Eptatretus burgeri (Cyclostomata). Cell Tissue Res 237:363-366
24. Chiba A, Honma Y 1992 FMRFamide-immunoreactive structures in the brain of the brown hagfish, Paramyxine atami: relationship with neuropeptide Y-immunoreactive structures. Histochemistry 98:33-38
25. Wicht H, Northcutt RG 1992 FMRFamide-like immunoreactivity in the brain of the Pacific hagfish, Eptatretus stouti (Myxinoidea). Cell Tissue Res 270:443-449
26. Forey P, Janvier P 1993 Agnathans and the origin of jawed vertebrates. Nature 361:129-134
27. Janvier P 2008 Early jawless vertebrates and cyclostome origins. Zoolog Sci 25:1045-1056
28. Heimberg AM, Cowper-Sal-lari R, Sémon M, Donoghue PC, Peterson KJ 2010 microRNAs reveal the interrelationships of hagfish, lampreys, and gnathostomes and the nature of the ancestral vertebrate. Proc Natl Acad Sci USA 107:19379-19383
29. Gorbman A, Kobayashi H, Honma Y, Matsuyama M 1990 The hagfishery of Japan. Fisheries 15:12-18
30. Honma Y 1998 Asian hagfish and their fisheries biology. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H, eds. The biology of hagfishes. London: Chapman, Hall; 45-56
31. Miki M, Shimotani T, Uchida K, Hirano S, Nozaki M 2006 Immunohistochemical detection of gonadotropin-like material in the pituitary of brown hagfish (Paramyxine atami) correlated with their gonadal functions and effect of estrogen treatment. Gen Comp Endocrinol 148:15-21
32. Uchida K, Moriyama S, Chiba H, Shimotani T, Honda K, Miki M, Takahashi A, Sower SA, Nozaki M 2010 Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish. Proc Natl Acad Sci USA 107:15832-15837
33. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ 2000 A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun 275:661-667
34. Koda A, Ukena K, Teranishi H, Ohta S, Yamamoto K, Kikuyama S, Tsutsui K 2002 A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology 143: 411-419
35. Ukena K, Iwakoshi E, Minakata H, Tsutsui K 2002 A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett 512: 255-258
36. Ukena K, Koda A, Yamamoto K, Kobayashi T, Iwakoshi-Ukena E, Minakata H, Kikuyama S, Tsutsui K 2003 Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinology 144:3879-3884
37. Sawada K, Ukena K, Satake H, Iwakoshi E, Minakata H, Tsutsui K 2002 Novel fish hypothalamic neuropeptide. Cloning of a cDNA encoding the precursor polypeptide and identification and localization of the mature peptide. Eur J Biochem 269:6000-6008
38. Nielsen H, Engelbrecht J, Brunak S, von Heijne G 1997 Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1-6
39. Nozaki M, Shimotani T, Uchida K 2007 Gonadotropin-like and adrenocorticotropin-like cells in the pituitary gland of hagfish, Paramyxine atami: immunohistochemistry in combination with lectin histochemistry. Cell Tissue Res 328:563-572
40. Romeis B 1948 Microskopische Technik 15 verb. Munich: 8 Auflage. Leibnit Verlag
41. Ukena K, Ubuka T, Tsutsui K 2003 Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res 312:73-79
42. Nozaki M, Oshima Y, Miki M, Shimotani T, Kawauchi H, Sower SA 2005 Distribution of immunoreactive adenohypophysial cell types in the pituitaries of the Atlantic and the Pacific hagfish, Myxine glutinosa and Eptatretus burgeri. Gen Comp Endocrinol 143:142-150
43. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA, Wang A, Chowdhury VS, Tsutsui K, Bentley GE 2009 Gonadotropininhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 517:841-855
44. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE 2009 Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS One 4:e8400
45. 4- isomerase in the rat Purkinje neuron during neonatal life. Endocrinology 40:805-813
46. Sawada K, Ukena K, Kikuyama S, Tsutsui K 2002 Identification of a cDNA encoding a novel amphibian growth hormone-releasing peptide and localization of its transcript. J Endocrinol 174:395-402
47. Ubuka T, Bentley GE, Ukena K, Wingfield JC, Tsutsui K 2005 Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc Natl Acad Sci USA 102:3052-3057
48. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, Osugi T, Chowdhury VS, Tsutsui K, Bentley GE 2008 Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology 149: 268-278
49. von Heijne G 1986 A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683-4690
50. Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H 2010 Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol 22:716-727
51. Kivipelto L, Majane EA, Yang HYT, Panula P 1989 Immunohistochemical distribution and partial characterization of FLFQPQRFamide like peptides in the central nervous system of rats. J Comp Neurol 286:269-287
52. López JM, Moreno N, Morona R, Muñoz M, González A 2006 Spatiotemporal sequence of appearance of NPFF-immunoreactive structures in the developing central nervous system of Xenopus laevis. Peptides 27:1036-1053
53. Brazeau P, Böhlen P, Esch F, Ling N, Wehrenberg WB, Guillemin R 1984 Growth hormone-releasing factor from ovine and caprine hypothalamus: isolation, sequence analysis and total synthesis. Biochem Biophys Res Commun 125:606-614
54. VandePol CJ, Leidy Jr JW, Finger TE, Robbins RJ 1986 Immunohistochemical localization of GRF-containing neurons in rat brain. Neuroendocrinology 42:143-147
55. Maruyama M, Matsumoto H, Fujiwara K, Kitada C, Hinuma S, Onda H, Fujino M, Inoue K 1999 Immunocytochemical localization of prolactin-releasing peptide in the rat brain. Endocrinology 140: 2326-2333
56. Moriyama S, Ito T, Takahashi A, Amano M, Sower SA, Hirano T, Yamamori K, Kawauchi H 2002 A homolog of mammalian PRLreleasing peptide (fish arginyl-phenylalanyl-amide peptide) is a major hypothalamic peptide of PRL release in teleost fish. Endocrinology 143:2071-2079
57. Moriyama S, Kasahara M, Amiya N, Takahashi A, Amano M, Sower SA, Yamamori K, Kawauchi H 2007 RFamide peptides inhibit the expression of melanotropin and growth hormone genes in the pituitary of an Agnathan, the sea lamprey, Petromyzon marinus. Endocrinology 148:3740-3749
58. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K 2005 Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 146:4431-4436
59. Gutiérrez-Pascual E, Martínez-Fuentes AJ, Pinilla L, Tena-Sempere M, Malagón MM, Castaño JP 2007 Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion. J Neuroendocrinol 19:521-530
60. Panula P, Kalso E, Nieminen M, Kontinen VK, Brandt A, Pertovaara A 1999 Neuropeptide FF and modulation of pain. Brain Res 848: 191-196
61. Johnson MA, Tsutsui K, Fraley GS 2007 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
62. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, Tsutsui K 2008 Hypophysiotropic role of RFamide-related peptide- 3 in the inhibition of LH secretion in female rats. J Endocrinol 199:105-112
63. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ 2009 Effect of RF-amide-related peptide-3 on luteinizing hormone and folliclestimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology 150:5549-5556
64. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, Yamamoto N 2009 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
65. 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 2010 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
66. King JA, Millar RP 1980 Comparative aspects of luteinizing hormone- releasing hormone structure and function in vertebrate phylogeny. Endocrinology 106:707-717
67. Jackson IMD 1980 Distribution and evolutionary significance of the hypophysiotropic hormones of the hypothalamus. Front Horm Res 6:35-69
68. Braun CB, Wicht H, Northcutt RG 1995 Distribution of gonadotropin- releasing hormone immunoreactivity in the brain of the Pacific Hagfish, Eptatretus stouti (craniata: Myxinoidea). J Comp Neurol 353:464-476
69. Sower SA, Nozaki M, Knox CJ, Gorbman A 1995 The occurrence and distribution of GnRH in the brain of Atlantic hagfish, an Agnatha, determined by chromatography and immunocytochemistry. Gen Comp Endocrinol 97:300-307
70. Kavanaugh SI, Powell ML, Sower SA 2005 Seasonal changes in gonadotropin-releasing hormone in the Atlantic hagfish Myxine glutinosa. Gen Comp Endocrinol 140:136-143
71. Gorbman A 1995 Olfactory origins and evolution of the brain-pituitary endocrine system: facts and speculation. Gen Comp Endocrinol 97:171-178
72. Nozaki M 2008 The hagfish pituitary gland and its putative adenohypophysial hormones. Zoolog Sci 25:1028-1036
73. Tsukahara T, Gorbman A, Kobayashi H 1986 Median eminence equivalence of the neurohypophysis of the hagfish. Gen Comp Endocrinol 61:348-354
74. Nozaki M, Gorbman A, Sower SA 1994 Diffusion between the neurohypophysis and the adenohypophysis of lampreys, Petromyzon marinus. Gen Comp Endocrinol 96:385-391
75. Elshourbagy NA, Ames RS, Fitzgerald LR, Foley JJ, Chambers JK, Szekeres PG, Evans NA, Schmidti DB, Buckleyi PT, Dytko GM, Murdock PR, Milligan G, Groarke DA, Tan KB, Shabon U, Nuthulaganti P, Wang DY, Wilson S, Bergsma DJ, Saraui HM 2000 Receptor for the pain modulatory neuropeptides FF and AF is an orphan G protein-coupled receptor. J Biol Chem 275:25965-25971
76. 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 2000 Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J Biol Chem 275:39324-39331
77. Ikemoto T, Park MK 2005 Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. J Reprod Dev 51:359-377
78. Bonnard E, Burlet-Schiltz O, Francés B, Mazarguil H, Monsarrat B, Zajac JM, Roussin A 2001 Identification of neuropeptide FF-related peptides in rodent spinal cord. Peptides 22:1085-1092
79. Satake H, Hisada M, Kawada T, Minakata H, Ukena K, Tsutsui K 2001 Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem J 354:379-385