Structural and functional divergence of gonadotropin-inhibitory hormone from jawless fish to mammals

Frontiers in Endocrinology

Volumn 5, Issue OCT, 2014, Pages

  Ogawa, Satoshi ^a   Parhar, Ishwar S ^a  

^a MONASH UNIVERSITY MALAYSIA   (Malaysia)

Author keywords

GnRH; Gonadotropin; LPXRFa; Reproduction; Teleosts

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; GONADORELIN; GONADOTROPIN; GONADOTROPIN INHIBITORY HORMONE; GONADOTROPIN INHIBITORY HORMONE RECEPTOR 147; GONADOTROPIN INHIBITORY HORMONE RECEPTOR 74; GROWTH HORMONE RELEASING FACTOR DERIVATIVE; GROWTH HORMONE RELEASING PEPTIDE 1; GROWTH HORMONE RELEASING PEPTIDE 3; KISSPEPTIN; MELANIN CONCENTRATING HORMONE; NEUROPEPTIDE FF; NEUROPEPTIDE Y; OREXIN; OXYTOCIN; PEPTIDE; PRALMORELIN; PROOPIOMELANOCORTIN; RFAMIDE RELATED PEPTIDE 1; RFAMIDE RELATED PEPTIDE 2; RFAMIDE RELATED PEPTIDE 3; UNCLASSIFIED DRUG;

AMPHIBIA; BIRD; CELL PROLIFERATION; CELL SURVIVAL; ENZYME LOCALIZATION; FISH; GENE EXPRESSION; GOLDFISH; HAGFISH; HORMONE RELEASE; HORMONE SYNTHESIS; HUMAN; HYPOTHALAMUS NUCLEUS; IMMUNOREACTIVITY; MAMMAL; NERVOUS SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; OREOCHROMIS NILOTICUS; PETROMYZON; PHYLOGENETIC TREE; PROTEIN STRUCTURE; PUFFER FISH; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; SUPRACHIASMATIC NUCLEUS; ZEBRA FISH;

EID: 84919773873     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00177     Document Type: Review

References (141)

1. Belchetz P, Plant T, Nakai Y, Keogh E, Knobil E. Hypophysial responses to continuous and intermittent delivery of hypopthalamic gonadotropin-releasing hormone. Science (1978) 202:631-3. doi:10.1126/science.100883
2. Marshall JC, Kelch RP. Gonadotropin-releasing hormone: role of pulsatile secretion in the regulation of reproduction. N Engl J Med (1986) 315:1459-68. doi:10.1056/NEJM198612043152306
3. Schoech SJ, Rensel MA, Bridge ES, Boughton RK, Wilcoxen TE. Environment, glucocorticoids, and the timing of reproduction. Gen Comp Endocrinol (2009) 163:201-7. doi:10.1016/j.ygcen.2008.09.009
4. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum Reprod Update (2006) 12:631-9. doi:10.1093/humupd/dml023
5. Roseweir AK, Millar RP. The role of kisspeptin in the control of gonadotrophin secretion. Hum Reprod Update (2009) 15:203-12. doi:10.1093/humupd/dmn058
6. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology (2004) 80:264-72. doi:10.1159/000083140
7. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology (2006) 147:5817-25. doi:10.1210/en.2006-0787
8. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM. Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology (2008) 149:4387-95. doi:10.1210/en.2008-0438
9. Parhar IS, Ogawa S, Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology (2004) 145:3613-8. doi:10.1210/en.2004-0395
10. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, et al. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Biophys Res Commun (2000) 275:661-7. doi:10.1006/bbrc.2000.3350
11. Osugi T, Daukss D, Gazda K, Ubuka T, Kosugi T, Nozaki M, et al. Evolutionary origin of the structure and function of gonadotropin-inhibitory hormone: insights from lampreys. Endocrinology (2012) 153:2362-74. doi:10.1210/en.2011-2046
12. Tsutsui K, Osugi T. Evolutionary origin and divergence of GnIH and its homologous peptides. Gen Comp Endocrinol (2009) 161:30-3. doi:10.1016/j.ygcen.2008.10.002
13. Sawada K, Ukena K, Satake H, Iwakoshi E, Minakata H, Tsutsui K. Novel fish hypothalamic neuropeptide. Eur J Biochem (2002) 269:6000-8. doi:10.1046/j.1432-1033.2002.03351.x
14. Zhang Y, Li S, Liu Y, Lu D, Chen H, Huang X, et al. Structural diversity of the gnih/gnih receptor system in teleost: its involvement in early development and the negative control of LH release. Peptides (2010) 31:1034-43. doi:10.1016/j.peptides.2010.03.003
15. Shahjahan M, Ikegami T, Osugi T, Ukena K, Doi H, Hattori A, et al. Synchronised expressions of LPXRFamide peptide and its receptor genes: seasonal, diurnal and circadian changes during spawning period in grass puffer. J Neuroendocrinol (2011) 23:39-51. doi:10.1111/j.1365-2826.2010.02081.x
16. Biran J, Golan M, Mizrahi N, Ogawa S, Parhar I, Sivan BL. LPXRFa, the piscine ortholog of GnIH, and LPXRF receptor positively regulate gonadotropin secretion in tilapia (Oreochromis niloticus). Endocrinology (2014). doi:10.1210/en.2013-2047
17. Koda A, Ukena K, Teranishi H, Ohta S, Yamamoto K, Kikuyama S, et al. A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology (2002) 143:411-9. doi:10.1210/endo.143.2.8630
18. Chowdhury VS, Yamamoto K, Saeki I, Hasunuma I, Shimura T, Tsutsui K. Melatonin stimulates the release of growth hormone and prolactin by a possible induction of the expression of frog growth hormone-releasing peptide and its related peptide-2 in the amphibian hypothalamus. Endocrinology (2008) 149:962-70. doi:10.1210/en.2007-1427
19. Ukena K, Koda A, Yamamoto K, Kobayashi T, Iwakoshi-Ukena E, Minakata H, et al. Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinology (2003) 144:3879-84. doi:10.1210/en.2003-0359
20. Chartrel N, Dujardin C, Leprince J, Desrues L, Tonon MC, Cellier E, et al. 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) 448:111-27. doi:10.1002/cne.10253
21. Chowdhury VS, Ubuka T, Osugi T, Shimura T, Tsutsui K. Identification, localization and expression of LPXRFamide peptides, and melatonin-dependent induction of their precursor mRNA in the newt brain. J Endocrinol (2011) 209:211-20. doi:10.1530/JOE-10-0494
22. Bentley GE, Kriegsfeld LJ, Osugi T, Ukena K, O'Brien S, Perfito N, et al. Interactions of gonadotropin-releasing hormone (GnRH) and gonadotropin-inhibitory hormone (GnIH) in birds and mammals. J Exp Zool A Comp Exp Biol (2006) 305:807-14. doi:10.1002/jez.a.306
23. Bentley GE, Ubuka T, McGuire NL, Chowdhury VS, Morita Y, Yano T, et al. Gonadotropin-inhibitory hormone and its receptor in the avian reproductive system. Gen Comp Endocrinol (2008) 156:34-43. doi:10.1016/j.ygcen.2007.10.003
24. Satake H, Hisada M, Kawada T, Minakata H, Ukena K, Tsutsui K. Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem J (2001) 354:379-85. doi:10.1042/0264-6021:3540379
25. Ikemoto T, Park MK. Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. J Reprod Dev (2005) 51:359-77. doi:10.1262/jrd.16087
26. Osugi T, Ukena K, Bentley GE, O'Brien S, Moore IT, Wingfield JC, et al. Gonadotropin-inhibitory hormone in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J Endocrinol (2004) 182:33-42. doi:10.1677/joe.0.1820033
27. Bentley GE, Jensen JP, Kaur GJ, Wacker DW, Tsutsui K, Wingfield JC. Rapid inhibition of female sexual behavior by gonadotropin-inhibitory hormone (GnIH). Horm Behav (2006) 49:550-5. doi:10.1016/j.yhbeh.2005.12.005
28. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, Osugi T, et al. Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology (2008) 149:268-78. doi:10.1210/en.2007-0983
29. Tobari Y, Iijima N, Tsunekawa K, Osugi T, Okanoya K, Tsutsui K, et al. Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): peptide isolation, cDNA cloning and brain distribution. Peptides (2010) 31:816-26. doi:10.1016/j.peptides.2010.01.015
30. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, 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. doi:10.1371/journal.pone.0008400
31. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA, et al. Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol (2009) 517:841-55. doi:10.1002/cne.22191
32. Bentley GE, Tsutsui K, Kriegsfeld LJ. Recent studies of gonadotropin-inhibitory hormone (GnIH) in the mammalian hypothalamus, pituitary and gonads. Brain Res (2010) 1364:62-71. doi:10.1016/j.brainres.2010.10.001
33. Smith JT, Shahab M, Pereira A, Pau K-YF, Clarke IJ. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biol Reprod (2010) 83:568-77. doi:10.1095/biolreprod.110.085407
34. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, et al. Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci U S A (2006) 103:2410-5. doi:10.1073/pnas.0511003103
35. Poling MC, Quennell JH, Anderson GM, Kauffman AS. Kisspeptin neurones do not directly signal to RFRP-3 neurones but RFRP-3 may directly modulate a subset of hypothalamic kisspeptin cells in mice. J Neuroendocrinol (2013) 25:876-86. doi:10.1111/jne.12084
36. Hinuma S, Shintani Y, Fukusumi S, Iijima N, Matsumoto Y, Hosoya M, et al. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat Cell Biol (2000) 2:703-8. doi:10.1038/35036326
37. Ukena K, Iwakoshi E, Minakata H, Tsutsui K. A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett (2002) 512:255-8. doi:10.1016/S0014-5793(02)02275-5
38. 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) 51:171-80. doi:10.1016/j.yhbeh.2006.09.009
39. Rizwan M, Harbid A, Inglis M, Quennell J, Anderson G. Evidence that hypothalamic RFamide related peptide-3 neurones are not leptin-responsive in mice and rats. J Neuroendocrinol (2014) 26:247-57. doi:10.1111/jne.12140
40. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, et al. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology (2012) 153:373-85. doi:10.1210/en.2011-1110
41. Fukusumi S, Habata Y, Yoshida H, Iijima N, Kawamata Y, Hosoya M, et al. Characteristics and distribution of endogenous RFamide-related peptide-1. Biochim Biophys Acta (2001) 1540:221-32. doi:10.1016/S0167-4889(01)00135-5
42. Yoshida H, Habata Y, Hosoya M, Kawamata Y, Kitada C, Hinuma S. Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim Biophys Acta (2003) 1593:151-7. doi:10.1016/S0167-4889(02)00389-0
43. Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC, Ubuka T, 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) 149:5811-21. doi:10.1210/en.2008-0575
44. Dardente H, Birnie M, Lincoln GA, Hazlerigg DG. RFamide-Related peptide and its cognate receptor in the sheep: cDNA cloning, mRNA distribution in the hypothalamus and the effect of photoperiod. J Neuroendocrinol (2008) 20:1252-9. doi:10.1111/j.1365-2826.2008.01784.x
45. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, et al. 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 (2008) 149:5770-82. doi:10.1210/en.2008-0581
46. Qi Y, Oldfield BJ, Clarke IJ. Projections of RFamide-related peptide-3 neurones in the ovine hypothalamus, with special reference to regions regulating energy balance and reproduction. J Neuroendocrinol (2009) 21:690-7. doi:10.1111/j.1365-2826.2009.01886.x
47. Li X, Su J, Lei Z, Zhao Y, Jin M, Fang R, et al. Gonadotropin-inhibitory hormone (GnIH) and its receptor in the female pig: cDNA cloning, expression in tissues and expression pattern in the reproductive axis during the estrous cycle. Peptides (2012) 36:176-85. doi:10.1016/j.peptides.2012.05.008
48. Amano M, Moriyama S, Iigo M, Kitamura S, Amiya N, Yamamori K, et al. Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon. J Endocrinol (2006) 188:417-23. doi:10.1677/joe.1.06494
49. Murakami M, Matsuzaki T, Iwasa T, Yasui T, Irahara M, Osugi T, et al. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J Endocrinol (2008) 199:105-12. doi:10.1677/JOE-08-0197
50. Kadokawa H, Shibata M, Tanaka Y, Kojima T, Matsumoto K, Oshima K, 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) 36:219-24. doi:10.1016/j.domaniend.2009.02.001
51. Ubuka T, McGuire NL, Calisi RM, Perfito N, Bentley GE. The control of reproductive physiology and behavior by gonadotropin-inhibitory hormone. Integr Comp Biol (2008) 48:560-9. doi:10.1093/icb/icn019
52. Tsutsui K, Ubuka T, Bentley GE, Kriegsfeld LJ. Gonadotropin-inhibitory hormone (GnIH): discovery, progress and prospect. Gen Comp Endocrinol (2012) 177:305-14. doi:10.1016/j.ygcen.2012.02.013
53. Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H. Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol (2010) 22:716-27. doi:10.1111/j.1365-2826.2010.02018.x
54. Qi X, Zhou W, Li S, Lu D, Yi S, Xie R, et al. Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus. Mol Cell Endocrinol (2013) 366:9-20. doi:10.1016/j.mce.2012.11.001
55. Qi X, Zhou W, Lu D, Wang Q, Zhang H, Li S, et al. Sexual dimorphism of steroidogenesis regulated by GnIH in the goldfish, Carassius auratus. Biol Reprod (2013) 88(89):81-7. doi:10.1095/biolreprod.112.105114
56. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun (2014) 5:3657. doi:10.1038/ncomms4657
57. Klein SL, Strausberg RL, Wagner L, Pontius J, Clifton SW, Richardson P. Genetic and genomic tools for Xenopus research: the NIH Xenopus initiative. Dev Dyn (2002) 225:384-91. doi:10.1002/dvdy.10174
58. Vonk FJ, Casewell NR, Henkel CV, Heimberg AM, Jansen HJ, McCleary RJ, et al. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc Natl Acad Sci U S A (2013) 110:20651-6. doi:10.1073/pnas.1314702110
59. Yin H, Ukena K, Ubuka T, Tsutsui K. A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. J Endocrinol (2005) 184:257-66. doi:10.1677/joe.1.05926
60. Maddineni SR, Ocón-Grove OM, Krzysik-Walker SM, Hendricks GL, Ramachandran R. Gonadotropin-inhibitory hormone (GnIH) receptor gene is expressed in the chicken ovary: potential role of GnIH in follicular maturation. Reproduction (2008) 135:267-74. doi:10.1530/REP-07-0369
61. Shimizu M, Bédécarrats GY. Activation of the chicken gonadotropin-inhibitory hormone receptor reduces gonadotropin releasing hormone receptor signaling. Gen Comp Endocrinol (2010) 167:331-7. doi:10.1016/j.ygcen.2010.03.029
62. Vassilatis DK, Hohmann JG, Zeng H, Li F, Ranchalis JE, Mortrud MT, et al. The G protein-coupled receptor repertoires of human and mouse. Proc Natl Acad Sci U S A (2003) 100:4903-8. doi:10.1073/pnas.0230374100
63. Soga T, Wong DW, Clarke IJ, Parhar IS. Citalopram (antidepressant) administration causes sexual dysfunction in male mice through RF-amide related peptide in the dorsomedial hypothalamus. Neuropharmacology (2010) 59:77-85. doi:10.1016/j.neuropharm.2010.03.018
64. Gibson EM, Humber SA, Jain S, Williams WP III, Zhao S, Bentley GE, et al. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology (2008) 149:4958-69. doi:10.1210/en.2008-0316
65. Zhao S, Zhu E, Yang C, Bentley GE, Tsutsui K, Kriegsfeld LJ. RFamide-related peptide and messenger ribonucleic acid expression in mammalian testis: association with the spermatogenic cycle. Endocrinology (2010) 151:617-27. doi:10.1210/en.2009-0978
66. Moussavi M, Wlasichuk M, Chang JP, Habibi HR. Seasonal effect of gonadotrophin inhibitory hormone on gonadotrophin-releasing hormone-induced gonadotroph functions in the goldfish pituitary. J Neuroendocrinol (2013) 25:506-16. doi:10.1111/jne.12024
67. Bonini JA, Jones KA, Adham N, Forray C, Artymyshyn R, Durkin MM, et al. Identification and characterization of two G protein-coupled receptors for neuropeptide FF. J Biol Chem (2000) 275:39324-31. doi:10.1074/jbc. M004385200
68. Liu Q, Guan X-M, Martin WJ, McDonald TP, Clements MK, Jiang Q, et al. Identification and characterization of novel mammalian neuropeptide FF-like peptides that attenuate morphine-induced antinociception. J Biol Chem (2001) 276:36961-9. doi:10.1074/jbc. M105308200
69. Ubuka T, Son YL, Bentley GE, Millar RP, Tsutsui K. Gonadotropin-inhibitory hormone (GnIH), GnIH receptor and cell signaling. Gen Comp Endocrinol (2013) 190:10-7. doi:10.1016/j.ygcen.2013.02.030
70. Gouarderes C, Mazarguil H, Mollereau C, Chartrel N, Leprince J, Vaudry H, et al. Functional differences between NPFF1 and NPFF2 receptor coupling: high intrinsic activities of RFamide-related peptides on stimulation of [35S]GTPgammaS binding. Neuropharmacology (2007) 52:376-86. doi:10.1016/j.neuropharm.2006.07.034
71. Tsutsui K, Ukena K. Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity. Peptides (2006) 27:1121-9. doi:10.1016/j.peptides.2005.06.036
72. Biswas S, Jadhao AG, Pinelli C, Palande NV, Tsutsui K. GnIH and GnRH expressions in the central nervous system and pituitary of Indian major carp, Labeo rohita during ontogeny: an immunocytochemical study. Gen Comp Endocrinol (2014). doi:10.1016/j.ygcen.2014.06.005
73. Stewart AJ, Katz AA, Millar RP, Morgan K. Retention and silencing of prepro-GnRH-II and type II GnRH receptor genes in mammals. Neuroendocrinology (2009) 90:416-32. doi:10.1159/000233303
74. Ekström P, van Veen T. Central connections of the pineal organ in the three-spined stickleback, Gasterosteus aculeatus L (Teleostei). Cell Tissue Res (1983) 232:141-55. doi:10.1007/BF00222380
75. Ekström P, van Veen T. Pineal neural connections with the brain in two teleosts, the crucian carp and the European eel. J Pineal Res (1984) 1:245-61. doi:10.1111/j.1600-079X.1984.tb00216.x
76. Puzdrowski RL, Northcutt RG. Central projections of the pineal complex in the silver lamprey Ichthyomyzon unicuspis. Cell Tissue Res (1989) 255:269-74. doi:10.1007/BF00224108
77. Kawano E, Takahata Y, Oishi T, Ukena K, Tsutsui K, Tamotsu S. Neural interaction of gonadotropin-regulating hormone immunoreactive neurons and the suprachiasmatic nucleus with the paraventricular organ in the Japanese grass lizard (Takydromus tachydromoides). Zoolog Sci (2006) 23:277-87. doi:10.2108/zsj.23.277
78. 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. doi:10.1046/j.1365-2826.2003.01062.x
79. Ukena K, Ubuka T, Tsutsui K. Distribution of a novel avian gonadotropin-inhibitory hormone in the quail brain. Cell Tissue Res (2003) 312:73-9. doi:10.1007/s00441-003-0700-x
80. Small TW, Sharp PJ, Bentley GE, Millar RP, Tsutsui K, Mura E, et al. Photoperiod-independent hypothalamic regulation of luteinizing hormone secretion in a free-living sonoran desert bird, the rufous-winged sparrow (Aimophila carpalis). Brain Behav Evol (2008) 71:127-42. doi:10.1159/000111459
81. Soga T, Kitahashi T, Clarke IJ, Parhar IS. Gonadotropin-inhibitory hormone promoter-driven enhanced green fluorescent protein expression decreases during aging in female rats. Endocrinology (2014) 155:1944-55. doi:10.1210/en.2013-1786
82. Smith JT, Ross Young I, Veldhuis JD, Clarke IJ. Gonadotropin-inhibitory hormone (GnIH) secretion into the ovine hypophyseal portal system. Endocrinology (2012) 153:3368-75. doi:10.1210/en.2012-1088
83. 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 (2009) 150:1413-20. doi:10.1210/en.2008-1287
84. Iwasa T, Matsuzaki T, Murakami M, Kinouchi R, Osugi T, Gereltsetseg G, et al. Developmental changes in the mammalian gonadotropin-inhibitory hormone (GnIH) ortholog RFamide-related peptide (RFRP) and its cognate receptor GPR147 in the rat hypothalamus. Int J Dev Neurosci (2012) 30:31-7. doi:10.1016/j.ijdevneu.2011.10.003
85. Ubuka T, Son YL, Tobari Y, Narihiro M, Bentley GE, Kriegsfeld LJ, et al. Central and direct regulation of testicular activity by gonadotropin-inhibitory hormone and its receptor. Front Endocrinol (Lausanne) (2014) 5:8. doi:10.3389/fendo.2014.00008
86. Tsutsui K, Bentley GE, Bedecarrats G, Osugi T, Ubuka T, Kriegsfeld LJ. Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrinol (2010) 31:284-95. doi:10.1016/j.yfrne.2010.03.001
87. Singh P, Krishna A, Sridaran R, Tsutsui K. Changes in GnRH I, bradykinin and their receptors and GnIH in the ovary of Calotes versicolor during reproductive cycle. Gen Comp Endocrinol (2008) 159:158-69. doi:10.1016/j.ygcen.2008.08.016
88. McGuire NL, Bentley GE. A functional neuropeptide system in vertebrate gonads: gonadotropin-inhibitory hormone and its receptor in testes of field-caught house sparrow (Passer domesticus). Gen Comp Endocrinol (2010) 166:565-72. doi:10.1016/j.ygcen.2010.01.010
89. McGuire NL, Kangas K, Bentley GE. Effects of melatonin on peripheral reproductive function: regulation of testicular GnIH and testosterone. Endocrinology (2011) 152:3461-70. doi:10.1210/en.2011-1053
90. Singh P, Krishna A, Sridaran R, Tsutsui K. Immunohistochemical localization of GnRH and RFamide-related peptide-3 in the ovaries of mice during the estrous cycle. J Mol Histol (2011) 42:371-81. doi:10.1007/s10735-011-9340-8
91. Oishi H, Klausen C, Bentley GE, Osugi T, Tsutsui K, Gilks CB, et al. The human gonadotropin-inhibitory hormone ortholog RFamide-related peptide-3 suppresses gonadotropin-induced progesterone production in human granulosa cells. Endocrinology (2012) 153:3435-45. doi:10.1210/en.2012-1066
92. Anjum S, Tsutsui K. Inhibitory roles of the mammalian GnIH ortholog RFRP-3 in testicular activities in adult mice. J Endocrinol (2014) 223(1):79-91. doi:10.1530/JOE-14-0333
93. Singh P, Krishna A, Tsutsui K. Effects of gonadotropin-inhibitory hormone on folliculogenesis and steroidogenesis of cyclic mice. Fertil Steril (2011) 95:1397-404. doi:10.1016/j.fertnstert.2010.03.052
94. Poling MC, Kim J, Dhamija S, Kauffman AS. Development, sex steroid regulation, and phenotypic characterization of RFamide-related peptide (Rfrp) gene expression and RFamide receptors in the mouse hypothalamus. Endocrinology (2012) 153:1827-40. doi:10.1210/en.2011-2049
95. Rizwan MZ, Poling MC, Corr M, Cornes PA, Augustine RA, Quennell JH, et al. RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology (2012) 153:3770-9. doi:10.1210/en.2012-1133
96. Soga T, Dalpatadu S, Wong D, Parhar I. Neonatal dexamethasone exposure down-regulates GnRH expression through the GnIH pathway in female mice. Neuroscience (2012) 218:56-64. doi:10.1016/j.neuroscience.2012.05.023
97. Umatani C, Abe H, Oka Y. Neuropeptide RFRP inhibits the pacemaker activity of terminal nerve GnRH neurons. J Neurophysiol (2013) 109:2354-63. doi:10.1152/jn.00712.2012
98. Fu L-Y, van den Pol AN. Kisspeptin directly excites anorexigenic proopiomelanocortin neurons but inhibits orexigenic neuropeptide Y cells by an indirect synaptic mechanism. J Neurosci (2010) 30:10205-19. doi:10.1523/JNEUROSCI.2098-10.2010
99. 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 (2009) 587:1401-11. doi:10.1113/jphysiol.2008.166447
100. Moussavi M, Wlasichuk M, Chang JP, Habibi HR. Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish. Mol Cell Endocrinol (2012) 350:53-60. doi:10.1016/j.mce.2011.11.020
101. Ubuka T, Ukena K, Sharp PJ, Bentley GE, Tsutsui K. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology (2006) 147:1187-94. doi:10.1210/en.2005-1178
102. Ciccone N, Dunn I, Boswell T, Tsutsui K, Ubuka T, Ukena K, et al. Gonadotrophin inhibitory hormone depresses gonadotrophin a and follicle-stimulating hormone ß subunit expression in the pituitary of the domestic chicken. J Neuroendocrinol (2004) 16:999-1006. doi:10.1111/j.1365-2826.2005.01260.x
103. Tachibana T, Sato M, Takahashi H, Ukena K, Tsutsui K, Furuse M. Gonadotropin-inhibiting hormone stimulates feeding behavior in chicks. Brain Res (2005) 1050:94-100. doi:10.1016/j.brainres.2005.05.035
104. Deviche P, Small T, Sharp P, Tsutsui K. Control of luteinizing hormone and testosterone secretion in a flexibly breeding male passerine, the rufous-winged sparrow, Aimophila carpalis. Gen Comp Endocrinol (2006) 149:226-35. doi:10.1016/j.ygcen.2006.06.004
105. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3 (RFRP-3), a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone (GnRH) neuron firing in the mouse. Endocrinology (2009) 150(6):2799-804. doi:10.1210/en.2008-1623
106. Kaewwongse M, Takayanagi Y, Onaka T. Effects of RFamide-related peptide (RFRP)-1 and RFRP-3 on oxytocin release and anxiety-related behaviour in rats. J Neuroendocrinol (2011) 23:20-7. doi:10.1111/j.1365-2826.2010.02077.x
107. 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 (2009) 150:5549-56. doi:10.1210/en.2009-0775
108. Pineda R, Garcia-Galiano D, Sanchez-Garrido MA, Romero M, Ruiz-Pino F, Aguilar E, et al. 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 (2010) 299:E39-46. doi:10.1152/ajpendo.00108.2010
109. Calisi RM. An integrative overview of the role of gonadotropin-inhibitory hormone in behavior: applying Tinbergen's four questions. Gen Comp Endocrinol (2014) 203:95-105. doi:10.1016/j.ygcen.2014.03.028
110. Ubuka T, Haraguchi S, Tobari Y, Narihiro M, Ishikawa K, Hayashi T, et al. Hypothalamic inhibition of socio-sexual behaviour by increasing neuroestrogen synthesis. Nat Commun (2014) 5:3061. doi:10.1038/ncomms4061
111. Black MP, Balthazart J, Baillien M, Grober MS. Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli. Proc Biol Sci (2005) 272:2435-40. doi:10.1098/rspb.2005.3210
112. Hallgren SL, Linderoth M, Olsén KH. Inhibition of cytochrome p450 brain aromatase reduces two male specific sexual behaviours in the male Endler guppy (Poecilia reticulata). Gen Comp Endocrinol (2006) 147:323-8. doi:10.1016/j.ygcen.2006.02.005
113. Huffman LS, O'Connell LA, Hofmann HA. Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiol Behav (2013) 11(2-113):77-83. doi:10.1016/j.physbeh.2013.02.004
114. Calisi RM, Díaz-Muñoz SL, Wingfield JC, Bentley GE. Social and breeding status are associated with the expression of GnIH. Genes Brain Behav (2011) 10:557-64. doi:10.1111/j.1601-183X.2011.00693.x
115. Ubuka T, Mizuno T, Fukuda Y, Bentley GE, Wingfield JC, Tsutsui K. RNA interference of gonadotropin-inhibitory hormone gene induces aggressive and sexual behaviors in birds. Gen Comp Endocrinol (2013) 181:179-86. doi:10.1016/j.ygcen.2012.09.010
116. Clarke IJ, Smith JT, Henry BA, Oldfield BJ, Stefanidis A, Millar RP, et al. Gonadotropin-inhibitory hormone is a hypothalamic peptide that provides a molecular switch between reproduction and feeding. Neuroendocrinology (2012) 95:305-16. doi:10.1159/000332822
117. Piekarski DJ, Zhao S, Jennings KJ, Iwasa T, Legan SJ, Mikkelsen JD, et al. Gonadotropin-inhibitory hormone reduces sexual motivation but not lordosis behavior in female Syrian hamsters (Mesocricetus auratus). Horm Behav (2013) 64:501-10. doi:10.1016/j.yhbeh.2013.06.006
118. Tsutsui K, Ubuka T, Yin H, Osugi T, Ukena K, Bentley GE, et al. Mode of action and functional significance of avian gonadotropin-inhibitory hormone (GnIH): a review. J Exp Zool A Comp Exp Biol (2006) 305:801-6. doi:10.1002/jez.a.305
119. Molnar C, Kallo I, Liposits Z, Hrabovszky E. Estradiol down-regulates RF-amide-related peptide (RFRP) expression in the mouse hypothalamus. Endocrinology (2011) 152:1684-90. doi:10.1210/en.2010-1418
120. Greives TJ, Kriegsfeld LJ, Bentley GE, Tsutsui K, Demas GE. Recent advances in reproductive neuroendocrinology: a role for RFamide peptides in seasonal reproduction? Proc Biol Sci (2008) 275:1943-51. doi:10.1098/rspb.2008.0433
121. Smith J. The role of kisspeptin and gonadotropin inhibitory hormone in the seasonal regulation of reproduction in sheep. Domest Anim Endocrinol (2012) 43:75-84. doi:10.1016/j.domaniend.2011.11.003
122. Tsutsui K, Ubuka T, Bentley GE, Kriegsfeld LJ. Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front Neurosci (2013) 7:60. doi:10.3389/fnins.2013.00060
123. Chowdhury VS, Ubuka T, Tsutsui K. Review: melatonin stimulates the synthesis and release of gonadotropin-inhibitory hormone in birds. Gen Comp Endocrinol (2013) 181:175-8. doi:10.1016/j.ygcen.2012.08.005
124. Bromage N, Porter M, Randall C. The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture (2001) 197:63-98. doi:10.1016/S0044-8486(01)00583-X
125. Falcón J, Migaud H, Muñoz-Cueto JA, Carrillo M. Current knowledge on the melatonin system in teleost fish. Gen Comp Endocrinol (2010) 165:469-82. doi:10.1016/j.ygcen.2009.04.026
126. Perfito N, Zann R, Ubuka T, Bentley G, Hau M. Potential roles for GNIH and GNRH-II in reproductive axis regulation of an opportunistically breeding songbird. Gen Comp Endocrinol (2011) 173:20-6. doi:10.1016/j.ygcen.2011.04.016
127. Ubuka T, Bentley GE, Ukena K, Wingfield JC, Tsutsui K. Melatonin induces the expression of gonadotropin-inhibitory hormone in the avian brain. Proc Natl Acad Sci U S A (2005) 102:3052-7. doi:10.1073/pnas.0403840102
128. 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) 151:271-80. doi:10.1210/en.2009-0908
129. Wang G, Harpole CE, Paulose J, Cassone VM. The role of the pineal gland in the photoperiodic control of bird song frequency and repertoire in the house sparrow, Passer domesticus. Horm Behav (2014) 65:372-9. doi:10.1016/j.yhbeh.2014.02.008
130. Greives TJ, Kingma SA, Beltrami G, Hau M. Melatonin delays clutch initiation in a wild songbird. Biol Lett (2012) 8:330-2. doi:10.1098/rsbl.2011.1100
131. Bentley GE, Van't Hof TJ, Ball GF. Seasonal neuroplasticity in the songbird telencephalon: a role for melatonin. Proc Natl Acad Sci U S A (1999) 96:4674-9. doi:10.1073/pnas.96.8.4674
132. Revel FG, Saboureau M, Pevet P, Simonneaux V, Mikkelsen JD. RFamide-related peptide gene is a melatonin-driven photoperiodic gene. Endocrinology (2008) 149:902-12. doi:10.1210/en.2007-0848
133. 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 U S A (2009) 106:11324-9. doi:10.1073/pnas.0901176106
134. Son YL, Ubuka T, Narihiro M, Fukuda Y, Hasunuma I, Yamamoto K, et al. Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology (2014) 155:1817-26. doi:10.1210/en.2013-2076
135. Messeguer X, Escudero R, Farré D, Núñez O, Martinez J, Albà MM. PROMO: detection of known transcription regulatory elements using species- tailored searches. Bioinformatics (2002) 18:333-4. doi:10.1093/bioinformatics/18.2.333
136. Farré D, Roset R, Huerta M, Adsuara JE, Roselló L, Albà MM, et al. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res (2003) 31:3651-3. doi:10.1093/nar/gkg605
137. 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 (2008) 157:283-7. doi:10.1016/j.ygcen.2008.05.010
138. Gingerich S, Wang X, Lee P, Dhillon S, Chalmers J, Koletar M, et al. The generation of an array of clonal, immortalized cell models from the rat hypothalamus: analysis of melatonin effects on kisspeptin and gonadotropin-inhibitory hormone neurons. Neuroscience (2009) 162:1134-40. doi:10.1016/j.neuroscience.2009.05.026
139. Gojska NM, Belsham DD. Glucocorticoid receptor-mediated regulation of Rfrp (GnIH) and Gpr147 (GnIH-R) synthesis in immortalized hypothalamic neurons. Mol Cell Endocrinol (2014) 384:23-31. doi:10.1016/j.mce.2013.12.015
140. Kime DE. A strategy for assessing the effects of xenobiotics on fish reproduction. Sci Total Environ (1999) 225:3-11. doi:10.1016/S0048-9697(98)00328-3
141. Peter RE, Yu KL, Marchant TA, Rosenblum PM. Direct neural regulation of the teleost adenohypophysis. J Exp Zool (1990) 256:84-9. doi:10.1002/jez.1402560415