Molecular evolution of GPCRs: Kisspeptin/kisspeptin receptors

Journal of Molecular Endocrinology

Volumn 52, Issue 3, 2014, Pages

  Pasquier, Jérémy ^a   Kamech, Nédia ^a   Lafont, Anne Gaëlle ^a   Vaudry, Hubert ^b   Rousseau, Karine ^a   Dufour, Sylvie ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b UNIVERSITY OF ROUEN   (France)

Author keywords

Evolution; Kisspeptin; Receptor; Vertebrates

Indexed keywords

ASPARAGINE; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; GALANIN RECEPTOR; KISSPEPTIN; METASTIN; NEUROPEPTIDE FF; PROLACTIN RELEASING FACTOR; KISS1R PROTEIN, HUMAN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; AMPHIBIA; ANOLIS CAROLINENSIS; AUTOSOME; BULLFROG; CARBOXY TERMINAL SEQUENCE; CARTILAGINOUS FISH; CELL SURFACE; CEPHALOCHORDATA; COELACANTH; CYCLOSTOME; ECHINODERM; EXON; GENE LOSS; GENE STRUCTURE; GENETIC VARIABILITY; GOLDFISH; HUMAN; HYPOGONADOTROPIC HYPOGONADISM; INTRACELLULAR SIGNALING; INTRON; MAMMAL; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR MODEL; MOLECULAR PHYLOGENY; MULTIGENE FAMILY; NONHUMAN; PELOPHYLAX ESCULENTUS; PHYLOGENY; PRIORITY JOURNAL; PUFFER FISH; REVIEW; SAUROPSID; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY; STICKLEBACK; STRUCTURE ACTIVITY RELATION; TELEOST; TRANSACTIVATION; VERTEBRATE; ANIMAL; EVOLUTION; GENE DUPLICATION; GENETICS; METASTASIS; NUCLEOTIDE SEQUENCE; PATHOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL EVOLUTION; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENETIC VARIATION; HUMANS; KISSPEPTINS; NEOPLASM METASTASIS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84901415254     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-13-0224     Document Type: Review

References (95)

1. van Aerle R., Kille P, Lange A & Tyler CR 2008 Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 29 57-64. (doi:10.1016/j.peptides.2007.10.018)
2. Akazome Y., Kanda S, Okubo K & Oka Y 2010 Functional and evolutionary insights into vertebrate kisspeptin systems fromstudies of fish brain. Journal of FishBiology76161-182. (doi:10.1111/j.1095-8649.2009.02496.x)
3. Arora K. K, Krsmanovic LZ, Mores N, O'Farrell H & Catt KJ 1998 Mediation of cyclic AMP signaling by the first intracellular loop of the gonadotropinreleasing hormone receptor. Journal of Biological Chemistry 273 25581-25586. (doi:10.1074/jbc.273.40.25581)
4. Asami T., Nishizawa N, Ishibashi Y, Nishibori K, Nakayama M, Horikoshi Y, Matsumoto S., Yamaguchi M, Matsumoto H, Tarui N et al. 2012 Serum stability of selected decapeptide agonists of KISS1R using pseudopeptides. Bioorganic & Medicinal Chemistry Letters 22 6391-6396. (doi:10.1016/j.bmcl.2012.08.069)
5. Baldwin J. M 1993 The probable arrangement of the helices in G proteincoupled receptors. EMBO Journal 12 1693-1703.
6. Becker J. A, Mirjolet JF, Bernard J, Burgeon E, Simons MJ, Vassart G, Parmentier M. & Libert F 2005 Activation of GPR54 promotes cell cycle arrest and apoptosis of human tumor cells through a specific transcriptional program not shared by other Gq-coupled receptors. Biochemical and Biophysical Research Communications 326 677-686. (doi:10.1016/j.bbrc.2004.11.094)
7. Bianco S. D, Vandepas L, Correa-Medina M, Gereben B, Mukherjee A, Kuohung W., Carroll R, Teles MG, Latronico AC & Kaiser UB 2011 KISS1R intracellular trafficking and degradation: effect of the Arg386Pro disease-associated mutation. Endocrinology 152 1616-1626. (doi:10.1210/en.2010-0903)
8. Biran J., Ben-Dor S & Levavi-Sivan B 2008 Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biology of Reproduction 79 776-786. (doi:10.1095/biolreprod.107.066266)
9. Bockaert J. & Pin JP 1999 Molecular tinkering of G protein-coupled receptors: an evolutionary success. EMBO Journal 18 1723-1729. (doi:10.1093/emboj/18.7.1723)
10. Bourne H. R 1997 How receptors talk to trimeric G proteins. Current Opinion in Cell Biology 9 134-142. (doi:10.1016/S0955-0674(97)80054-3)
11. Cartwright J. E &Williams PJ 2012 Altered placental expression of kisspeptin and its receptor in pre-eclampsia. Journal of Endocrinology 214 79-85. (doi:10.1530/JOE-12-0091)
12. Castaño J. P, Martínez-Fuentes AJ, Gutiérrez-Pascual E, Vaudry H, Tena-SempereM& Malagón MM 2009 Intracellular signaling pathways activated by kisspeptins through GPR54: do multiple signals underlie function diversity? Peptides 30 10-15. (doi:10.1016/j.peptides. 2008.07.025)
13. Castellano J. M, Navarro VM, Fernández-Fernández R, Castaño JP, Malagón M. M, Aguilar E, Dieguez C, Magni P, Pinilla L & Tena-Sempere M. 2006 Ontogeny and mechanisms of action for the stimulatory effect of kisspeptin on gonadotropin-releasing hormone system of the rat. Molecular and Cellular Endocrinology 257-258 75-83. (doi:10.1016/j.mce.2006.07.002)
14. Chevrier L., de Brevern A, Hernandez E, Leprince J, Vaudry H, Guedj AM & de Roux N. 2013 PRR repeats in the intracellular domain of KISS1R are important for its export to cell membrane. Molecular Endocrinology 27 1004-1014. (doi:10.1210/me.2012-1386)
15. Chianese R., Ciaramella V, Fasano S, Pierantoni R & Meccariello R 2013 Kisspeptin receptor, GPR54, as a candidate for the regulation of testicular activity in the frog Rana esculenta. Biology of Reproduction 88 73. (doi:10.1095/biolreprod.112.103515)
16. Choe H. K, Kim HD, Park SH, LeeHW, Park JY, Seong JY, Lightman SL, SonGH & Kim K 2013 Synchronous activation of gonadotropin-releasing hormone gene transcription and secretion by pulsatile kisspeptin stimulation. PNAS 110 5677-5682. (doi:10.1073/pnas.1213594110)
17. Clements M. K, McDonald TP, Wang R, Xie G, O'Dowd BF, George SR, Austin C. P & Liu Q 2001 FMRFamide-related neuropeptides are agonists of the orphan G-protein-coupled receptor GPR54. Biochemical and Biophysical Research Communications 284 1189-1193. (doi:10.1006/ bbrc.2001.5098)
18. Curtis A. E, Cooke JH, Baxter JE, Parkinson JR, Bataveljic A, Ghatei MA, Bloom S. R & Murphy KG 2010 A kisspeptin-10 analog with greater in vivo bioactivity than kisspeptin-10. American Journal of Physiology. Endocrinology and Metabolism 298 E296-E303. (doi:10.1152/ajpendo. 00426.2009)
19. Dungan Lemko H. M & Elias CF 2012 Kiss of the mutant mouse: how genetically altered mice advanced our understanding of kisspeptin's role in reproductive physiology. Endocrinology 153 5119-5129. (doi:10.1210/en.2012-1494)
20. Eipper B. A, Stoffers DA &Mains RE 1992 The biosynthesis of neuropeptides: peptide α-amidation. Annual Review of Neuroscience 15 57-85. (doi:10.1146/annurev.ne.15.030192.000421)
21. Evans B. J, Wang Z, Mobley L, Khosravi D, Fujii N, Navenot JM & Peiper SC 2008 Physical association of GPR54 C-terminal with protein phosphatase 2A. Biochemical and Biophysical Research Communications 377 1067-1071. (doi:10.1016/j.bbrc.2008.10.108)
22. Farrens D. L, Altenbach C, Yang K, Hubbell WL & Khorana HG 1996 Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274 768-770. (doi:10.1126/science. 274.5288.768)
23. Felip A., Zanuy S, Pineda R, Pinilla L, Carrillo M, Tena-SempereM&Gómez A 2009 Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Molecular and Cellular Endocrinology 312 61-71. (doi:10.1016/j.mce.2008.11.017)
24. Fukusumi S., Fujii R & Hinuma S 2006 Recent advances in mammalian RFamide peptides: the discovery and functional analyses of PrRP, RFRPs and QRFP. Peptides 27 1073-1086. (doi:10.1016/j.peptides.2005.06.031)
25. Funes S., Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S., Monsma FJ & Gustafson EL 2003 The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochemical and Biophysical Research Communications 312 1357-1363. (doi:10.1016/j.bbrc.2003.11.066)
26. Gopurappilly R., Ogawa S & Parhar IS 2013 Functional significance of GnRH and kisspeptin, and their cognate receptors in teleost reproduction. Frontiers in Endocrinology 4 24. (doi:10.3389/fendo.2013.00024).
27. Gutiérrez-Pascual E., Martínez-Fuentes A, Pinilla L, Tena-Sempere M, Malagón M. & Castaño J 2007 Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion. Journal of Neuroendocrinology 19 521-530. (doi:10.1111/j.1365-2826.2007.01558.x)
28. Gutiérrez-Pascual E., Leprince J, Martínez-Fuentes AJ, Ségalas-Milazzo I, Pineda R., Roa J, Duran-PradoM, Guilhaudis L, Desperrois E, Lebreton A et al. 2009 In vivo and in vitro structure-activity relationships and structural conformation of Kisspeptin-10-related peptides. Molecular Pharmacology 76 58-67. (doi:10.1124/mol.108.053751)
29. Hodne K., Weltzien FA, Oka Y & Okubo K 2013 Expression and putative function of kisspeptins and their receptors during early development in medaka. Endocrinology 154 3437-3446. (doi:10.1210/en.2013-1065)
30. Holland L. Z, Albalat R, Azumi K, Benito-Gutierrez E, Blow MJ, Bronner-F, Raser M, Brunet F, Butts T, Candiani S, Dishaw LJ et al. 2008 The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Research 18 1100-1111. (doi:10.1101/ gr.073676.107)
31. Hultqvist G., Ocampo Daza D, Larhammar D & Kilimann MW 2012 Evolution of the vertebrate paralemmin gene family: ancient origin of gene duplicates suggests distinct functions. PLoS ONE 7 e41850. (doi:10.1371/journal.pone.0041850)
32. Kim D. K, Cho EB, Moon MJ, Park S, Hwang JI, Do Rego JL, Vaudry H & Seong J. Y 2012 Molecular coevolution of neuropeptides gonadotropinreleasing hormone and kisspeptin with their cognate G proteincoupled receptors. Frontiers in Neuroscience 6 3. (doi:10.3889/fnins. 2012.00003)
33. Kitahashi T., Ogawa S & Parhar IS 2009 Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150 821-831. (doi:10.3389/ fnins.2012.00003)
34. Kotani M., DetheuxM, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E., Brezillon S, Tyldesley R, Suarez-HuertaN, Vandeput F et al. 2001 The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. Journal of Biological Chemistry 276 34631-34636. (doi:10.1074/jbc.M104847200)
35. Lee J. H, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE & Welch D. R 1996 KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. Journal of the National Cancer Institute 88 1731-1737. (doi:10.1093/jnci/88.23.1731)
36. Lee D. K, Nguyen T, O'Neill GP, Cheng R, Liu Y, Howard AD, Coulombe N, Tan C. P, Tang-Nguyen AT, George SR et al. 1999 Discovery of a receptor related to the galanin receptors. FEBS Letters 446 103-107. (doi:10.1016/S0014-5793(99)00009-5)
37. Lee J. Y, Moon JS, Eu YJ, Lee CW, Yang ST, Lee SK, Jung HH, Kim HH, Rhim H, Seong J. Y et al. 2009a Molecular interaction between kisspeptin decapeptide analogs and a lipid membrane. Archives of Biochemistry and Biophysics 485 109-114. (doi:10.1016/j.abb.2009.03.002)
38. Lee Y. R, Tsunekawa K, Moon MJ, Um HN, Hwang JI, Osugi T, Otaki N, Sunakawa Y., Kim K, Vaudry H et al. 2009b Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150 2837-2846. (doi:10.1210/en.2008-1679)
39. Li S., Zhang Y, Liu Y, Huang X, Huang W, Lu D, Zhu P, Shi Y, Cheng CH, Liu X. et al. 2009 Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). Journal of Endocrinology 201 407-418. (doi:10.1677/JOE-09-0016)
40. Li Y., Xiang Q, Zhang Q, Huang Y & Su Z 2012 Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides 37 207-215. (doi:10.1016/j.peptides.2012.07.001)
41. Liu Z., Ren C, JonesW, Chen P, Seminara SB, Chan YM, Smith NF, Covey JM, Wang J. & Chan KK 2013 LC-MS/MS quantification of a neuropeptide fragment kisspeptin-10 (NSC 741805) and characterization of its decomposition product and pharmacokinetics in rats. Journal of Chromatography. B. Analytical Technologies in the Biomedical and Life Sciences 926 1-8. (doi:10.1016/j.jchromb.2013.02.027)
42. Luque R. M, Córdoba-Chacón J, Gahete MD, Navarro VM, Tena-Sempere M, Kineman R. D & Castaño JP 2011 Kisspeptin regulates gonadotroph and somatotroph function in nonhuman primate pituitary via common and distinct signaling mechanisms. Endocrinology 152 957-966. (doi:10.1210/en.2010-1142)
43. Masui T. D, Doi R, Mori R, Toyoda E, Koizumi M, Kami K, Ito D, Peiper SC, Broach J.R, Oishi S et al. 2004 Metastin and its variant forms suppress migration of pancreatic cancer cells. Biochemical and Biophysical Research Communications 315 85-92. (doi:10.1016/j.bbrc.2004.01.021)
44. Mechaly A. S, Viñas J & Piferrer F 2009 Identification of two isoforms of the Kisspeptin-1 receptor (kiss1r) generated by alternative splicing in a modern teleost, the Senegalese sole (Solea senegalensis). Biology of Reproduction 80 60-69. (doi:10.1095/biolreprod.108.072173)
45. Mechaly A. S, Viñas J & Piferrer F 2011 Gene structure analysis of kisspeptin-2 (Kiss2) in the Senegalese sole (Solea senegalensis): characterization of two splice variants of Kiss2, and novel evidence for metabolic regulation of kisspeptin signaling in non-mammalian species. Molecular and Cellular Endocrinology 339 14-24. (doi:10.1016/j.mce.2011.03.004)
46. Michelsen K., Yuan H & Schwappach B 2005 Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. EMBO Reports 6 717-722. (doi:10.1038/ sj.embor.7400480)
47. Mirabeau O. & Joly JS 2013 Molecular evolution of peptidergic signaling systems in bilaterians. PNAS 110 E2028-E2037. (doi:10.1073/ pnas.1219956110)
48. Misu R., Oishi S, Setsuda S, Noguchi T, Kaneda M, Ohno H, Evans B, Navenot J. M, Peiper SC & Fujii N 2013 Characterization of the receptor binding residues of kisspeptins by positional scanning using peptide photoaffinity probes. Bioorganic & Medicinal Chemistry Letters 23 2628-2631. (doi:10.1016/j.bmcl.2013.02.098)
49. Moon J. S, Lee YR, Oh DY, Hwang JI, Lee JY, Kim JI, Vaudry H, Kwon HB & Seong J. Y 2009 Molecular cloning of the bullfrog kisspeptin receptor GPR54 with high sensitivity to Xenopus kisspeptin. Peptides 30 171-179. (doi:10.1016/j.peptides.2008.04.015)
50. Muir A. I, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A., Szekeres PG, Sarau HM, Chambers JK, Murdock P et al. 2001 AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. Journal of Biological Chemistry 276 28969-28975. (doi:10.1074/jbc.M102743200)
51. Nakatani Y., Takeda H, Kohara Y & Morishita S 2007 Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. GenomeResearch 171254-1265. (doi:10.1101/gr.6316407)
52. Niida A., Wang Z, Tomita K, Oishi S, Tamamura H, Otaka A, Navenot JM, Broach J. R, Peiper SC & Fujii N 2006 Design and synthesis of downsized metastin (45-54) analogs with maintenance of high GPR54 agonistic activity. Bioorganic & Medicinal Chemistry Letters 16 134-137. (doi:10.1016/j.bmcl.2005.09.054)
53. Nocillado J. N, Biran J, Lee YY, Levavi-Sivan B, Mechaly AS, Zohar Y & Elizur A. 2012 The Kiss2 receptor (Kiss2r) gene in Southern Bluefin Tuna, Thunnus maccoyii and in Yellowtail Kingfish, Seriola lalandi-functional analysis and isolation of transcript variants. Molecular and Cellular Endocrinology 362 211-220. (doi:10.1016/j.mce.2012.06.024)
54. Novaira H. J, Ng Y, Wolfe A & Radovick S 2009 Kisspeptin increases GnRH mRNA expression and secretion in GnRH secreting neuronal cell lines. Molecular and Cellular Endocrinology 311 126-134. (doi:10.1016/j.mce. 2009.06.011)
55. Ohga H., Fujinaga Y, Selvaraj S, Kitano H, Nyuji M, Yamaguchi A & Matsuyama M. 2013 Identification, characterization, and expression profiles of two subtypes of kisspeptin receptors in a scombroid fish (chub mackerel). General and Comparative Endocrinology 193C 130-140. (doi:10.1016/j.ygcen.2013.07.016)
56. Ohtaki T., Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S., Takatsu Y, Masuda Y et al. 2001 Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411 613-617. (doi:10.1038/35079135)
57. Onuma T. A & Duan C 2012 Duplicated Kiss1 receptor genes in zebrafish: distinct gene expression patterns, different ligand selectivity, and a novel nuclear isoform with transactivating activity. FASEB Journal 26 2941-2950. (doi:10.1096/fj.11-201095)
58. Orsini M. J, Klein MA, Beavers MP, Connolly PJ, Middleton SA & Mayo KH 2007 Metastin (KiSS-1) mimetics identified from peptide structure-activity relationship-derived pharmacophores and directed small molecule database screening. Journal of Medicinal Chemistry 50 462-471. (doi:10.1021/jm0609824)
59. Osugi T., Ohtaki N, Sunakawa Y, Son YL, Ohkubo M, Iigo M, Amano M & Tsutsui K. 2013 Molecular evolution of Kiss2 genes and peptides in vertebrates. Endocrinology 154 4270-4280. (doi:10.1210/en.2012-2267)
60. Palczewski K., Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Le Trong I., Teller DC, Okada T, Stenkamp RE et al. 2000 Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289 739-745. (doi:10.1126/science.289.5480.739)
61. Pasquier J., Lafont AG, Jeng SR, Morini M, Dirks R, van den Thillart G, Tomkiewicz J., Tostivint H, Chang CF, Rousseau K et al. 2012a Multiple kisspeptin receptors in early osteichthyans provide new insights into the evolution of this receptor family. PLoS ONE 7 e48931. (doi:10.1371/ journal.pone.0048931)
62. Pasquier J., Lafont AG, Tostivint H, Vaudry H, Rousseau K & Dufour S 2012b Comparative evolutionary histories of kisspeptins and kisspeptin receptors in vertebrates reveal both parallel and divergent features. Frontiers in Endocrinology 3 173. (doi:10.3389/fendo.2012.00173)
63. Pasquier J., Lafont A-G, Rousseau K, Querat B, Chemineau P & Dufour S 2014 Looking for the bird Kiss: evolutionary scenario in sauropsids. BMC Evolutionary Biology 14 30. (doi:10.1186/1471-2148-14-30)
64. Pellissier L. P, Barthet G, Gaven F, Cassier E, Trinquet E, Pin JP, Marin P, Dumuis A., Bockaert J, Banères JL et al. 2011 G protein activation by serotonin type 4 receptor dimers: evidence that turning on two protomers is more efficient. Journal of Biological Chemistry 286 9985-9997. (doi:10.1074/jbc.M110.201939)
65. Pinilla L., Aguilar E, Dieguez C, Millar RP& Tena-Sempere M 2012 Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiological Reviews 92 1235-1316. (doi:10.1152/physrev.00037.2010)
66. Price D. A & Greenberg MJ 1977a Purification and characterization of a cardioexcitatory neuropeptide from the central ganglia of a bivalve mollusc. Preparative Biochemistry 7 261-281. (doi:10.1080/ 00327487708061643)
67. Price D. A & Greenberg MJ 1977b Structure of a molluscan cardioexcitatory neuropeptide. Science 197 670-671. (doi:10.1126/science.877582)
68. Putnam N. H, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M., Shoguchi E, Terry A, Yu JK et al. 2008 The amphioxus genome and the evolution of the chordate karyotype. Nature 453 1064-1071. (doi:10.1038/nature06967)
69. Ringel M. D, Hardy E, Bernet VJ, Burch HB, Schuppert F, Burman KD & SajiM 2002 Metastin receptor is overexpressed in papillary thyroid cancer and activates MAP kinase in thyroid cancer cells. Journal of Clinical Endocrinology and Metabolism 87 2399. (doi:10.1210/jcem.87.5.8626)
70. Roa J., Aguilar E, Dieguez C, Pinilla L & Tena-Sempere M 2008 New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Frontiers in Neuroendocrinology 29 48-69. (doi:10.1016/j.yfrne.2007.07.002)
71. de Roux N., Genin E, Carel JC, Matsuda F, Chaussain JL & Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. PNAS 100 10972-10976. (doi:10. 1073/pnas.1834399100)
72. Roy A., Kucukural A & Zhang Y 2010 I-TASSER: a unified platform for automated protein structure and function prediction. Nature Protocols 5 725-738. (doi:10.1038/nprot.2010.5)
73. Saksela K. & Permi P 2012 SH3 domain ligand binding: what's the consensus and where's the specificity? FEBS Letters 586 2609-2614. (doi:10.1016/ j.febslet.2012.04.042)
74. Scheer A., Fanelli F, Costa T, De Benedetti PG & Cotecchia S 1996 Constitutively active mutants of the α1B-adrenergic receptor: role of highly conserved polar amino acids in receptor activation. EMBO Journal 15 3566-3578.
75. Selvaraj S., Kitano H, Fujinaga Y, Ohga H, Yoneda M, Yamaguchi A, Shimizu A. & Matsuyama M 2010 Molecular characterization, tissue distribution, and mRNA expression profiles of two Kiss genes in the adult male and female chub mackerel (Scomber japonicus) during different gonadal stages. General and Comparative Endocrinology 169 28-38. (doi:10.1016/j.ygcen.2010.07.011)
76. Seminara S. B, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Shagoury J. K, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG et al. 2003 The GPR54 gene as a regulator of puberty. New England Journal of Medicine 349 1614-1627. (doi:10.1056/NEJMoa035322)
77. Semple R. K, Achermann JC, Ellery J, Farooqi IS, Karet FE, Stanhope RG, O'rahilly S & Aparicio SA 2005 Two novel missense mutations in g protein-coupled receptor 54 in a patient with hypogonadotropic hypogonadism. Journal of Clinical Endocrinology and Metabolism 90 1849-1855. (doi:10.1210/jc.2004-1418)
78. Servili A., Le Page Y, Leprince J, Caraty A, Escobar S, Parhar IS, Seong JY, Vaudry H. & Kah O 2011 Organization of two independent kisspeptin systems delivered from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 152 1527-1540. (doi:10.1210/en.2010-0948)
79. Shi Y., Zhang Y, Li S, Liu Q, Lu D, Liu M, Meng Z, Cheng CH, Liu X & Lin H 2010 Molecular identification of the Kiss2/Kiss1ra system and its potential function during 17β-methyltestosterone-induced sex reversal in the orange-spotted grouper, Epinephelus coioides. Biology of Reproduction 83 63-74. (doi:10.1095/biolreprod.109.080044)
80. Stafford L. J, Xia C, Ma W, Cai Y & Liu M 2002 Identification and characterization of mouse metastasis-suppressor KiSS1 and its G-protein-coupled receptor. Cancer Research 62 5399-5404.
81. Stathatos N., Bourdeau I, Espinosa AV, Saji M, Vasko VV, Burman KD, Stratakis C. A & Ringel MD 2005 KiSS-1/G protein-coupled receptor 54 metastasis suppressor pathway increases myocyte-enriched calcineurin interacting protein 1 expression and chronically inhibits calcineurin activity. Journal of Clinical Endocrinology and Metabolism 90 5432-5440. (doi:10.1210/jc.2005-0963)
82. Teles M. G, Bianco SD, Brito VN, Trarbach EB, Kuohung W, Xu S, Seminara S. B, Mendonca BB, Kaiser UB & Latronico AC 2008 A GPR54-activating mutation in a patient with central precocious puberty. New England Journal of Medicine 358 709-715. (doi:10.1056/ NEJMoa073443)
83. Tena-Sempere M., Felip A, Gomez A, Zanuy S & Carrillo M 2012 Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. General and Comparative Endocrinology 175 234-243. (doi:10.1016/j.ygcen.2011.11.015)
84. Tenenbaum-Rakover Y., Commenges-Ducos M, Iovane A, Aumas C, Admoni O. & de Roux N 2007 Neuroendocrine phenotype analysis in five patients with isolated hypogonadotropic hypogonadism due to a L102P inactivating mutation of GPR54. Journal of Clinical Endocrinology and Metabolism 92 1137-1144. (doi:10.1210/jc.2006-2147)
85. Tomikawa J., Homma T, Tajima S, Shibata T, Inamoto Y, Takase K, Inoue N, Ohkura S., Uenoyama Y, Maeda K et al. 2010 Molecular characterization and estrogen regulation of hypothalamic KISS1 gene in the pig. Biology of Reproduction 82 313-319. (doi:10.1095/biolreprod.109.079863)
86. Tomikawa J., Uenoyama Y, OzawaM, Fukanuma T, Takase K, Goto T, Abe H, Ieda N., Minabe S, Deura C et al. 2012 Epigenetic regulation of Kiss1 gene expression mediating estrogen-positive feedback action in the mouse brain. PNAS 109 E1294-E1301. (doi:10.1073/pnas.1114245109)
87. Tomita K., Niida A, Oishi S, Ohno H, Cluzeau J, Navenot JM, Wang ZX, Peiper S. C & Fujii N 2006 Structure-activity relationship study on small peptidic GPR54 agonists. Bioorganic & Medicinal Chemistry 14 7595-7603. (doi:10.1016/j.bmc.2006.07.009)
88. Topaloglu A. K, Tello JA, Kotan LD, Ozbek MN, Yilmaz MB, Erdogan S, Gurbuz F., Temiz F, Millar RP & Yuksel B 2012 Inactivating KISS1 mutation and hypogonadotropic hypogonadism. New England Journal of Medicine 366 629-635. (doi:10.1056/NEJMoa1111184)
89. 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. Journal of Neuroendocrinology 22 716-727. (doi:10.1111/j.1365-2826.2010.02018.x)
90. Unger V. M, Hargrave PA, Baldwin JM & Schertler GF 1997 Arrangement of rhodopsin transmembrane α-helices. Nature 389 203-206. (doi:10.1038/38316)
91. Vilardaga J. P, Agnati LF, Fuxe K & Ciruela F 2010 G-protein-coupled receptor heteromer dynamics. Journal of Cell Science 123 4215-4220. (doi:10.1242/jcs.063354)
92. Wacker J. L, Feller DB, Tang XB, Defino MC, Namkung Y, Lyssand JS, Mhyre A. J, Tan X, Jensen JB & Hague C 2008 Disease-causing mutation in GPR54 reveals the importance of the second intracellular loop for class A G-protein-coupled receptor function. Journal of Biological Chemistry 283 31068-31078. (doi:10.1074/jbc.M805251200)
93. Wahab F., Quinton R & Seminara SB 2011 The kisspeptin signaling pathway and its role in human isolated GnRH deficiency. Molecular and Cellular Endocrinology 346 29-36. (doi:10.1016/j.mce.2011.05.043)
94. Witham E. A, Meadows JD, Hoffmann HM, Shojaei S, Coss D, Kauffman AS & Mellon P. L 2013 Kisspeptin regulates gonadotropin genes via immediate early gene induction in pituitary gonadotropes. Molecular Endocrinology 27 1283-1294. (doi:10.1210/me.2012-1405) ZmoraN, Stubblefield J, Zulperi Z, Biran J, Levavi-Sivan B, Muñoz-Cueto JA&
95. Zohar Y. 2012Differential and gonad stage-dependent roles of kisspeptin1 and kisspeptin2 in reproduction in the modern teleosts, Morone species. Biology of Reproduction 86 177. (doi:10.1095/biolreprod.111.097667)