Kisspeptin and seasonal control of reproduction in male European sea bass (Dicentrarchus labrax)

General and Comparative Endocrinology

Volumn 179, Issue 3, 2012, Pages 384-399

  Migaud, H ^a   Ismail, R ^a   Cowan, M ^a   Davie, A ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

Author keywords

Brain; Dicentrarchus labrax; GnRH; Kisspeptin; Reproduction; Sea bass

Indexed keywords

11 OXOTESTOSTERONE; FOLLITROPIN BETA SUBUNIT; KISSPEPTIN; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; TESTOSTERONE; GONADORELIN;

ADULT; ANIMAL REPRODUCTIVE PROCEDURES; ANIMAL TISSUE; ARTICLE; CGNRHII GENE; CIRCANNUAL RHYTHM; CONTROLLED STUDY; CORRELATIONAL STUDY; EUROPEAN SEA BASS; FSH BETA GENE; GENE; GENE EXPRESSION; GENETIC CONSERVATION; GONAD DEVELOPMENT; HISTOLOGY; HORMONE DETERMINATION; HYPOPHYSIS GONAD SYSTEM; KISS1 GENE; KISS2 GENE; KISSR4 GENE; LH BETA GENE; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SBGNRH GENE; SEASONAL VARIATION; SEQUENCE ANALYSIS; SGNRH GENE; SPAWNING; SPERMATOGENESIS; VALIDATION PROCESS; ANIMAL; BASS; METABOLISM; PHYSIOLOGY; SEASON;

ANIMALS; BASS; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; MALE; REPRODUCTION; SEASONS;

EID: 84867747722     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.07.033     Document Type: Article

References (94)

1. Y. Akazome, S. Kanda, K. Okubo, Y. Oka, Functional and evolutionary insights into vertebrate Kisspeptin system from studies of fish brain, J. Fish Biol. 76 (2010) 161-182.
2. M. Amano, K. Okubo, T. Yamanome, H. Yamada, K. Aida, K. Yamamori, Changes in brain GnRH mRNA and pituitary GnRH peptide during testicular maturation in barfin flounder, Comp. Biochem. Physiol. (B) 138 (2004) 435-443.
3. I. Begtashi, L. Rodriguez, G. Moles, S. Zanuy, M. Carrillo, Long-term exposure to continuous light inhibits precocity in juvenile male European sea bass (Dicentrarchus labrax), Morphol. aspects Aquacult. 241 (2004) 539-559.
4. J. Biran, S. Ben-Dor, B. Levavi-Sivan, Molecular identification and functional characterization of the Kisspeptin/Kisspeptin receptor system in lower vertebrates, Biol. Repro. 79 (2008) 776-786.
5. M. Carrillo, S. Zanuy, A. Felip, M.J. Bayarri, G. Moles, A. Gomez, Hormonal and environmental control of puberty in perciform fish: the case of sea bass, Ann. NY Acad. Sci. 1163 (2009) 49-59.
6. J. Cerdà, F. Chauvigne, M.J. Agulleiro, E. Marin, S. Halm, G. Gonzalo Martínez- Rodríguez, F. Prat, Molecular cloning of senegalese sole (Solea senegalensis) follicle-stimulating hormone and luteinizing hormone subunits and expression pattern during spermatogenesis, Gen. Comp. Endocrinol. 156 (2008) 470-481.
7. J. Clarkson, S.-K. Han, X. Liu, K. Lee, A.E. Herbison, Neurobiological mechanisms underlying Kisspeptin activation of gonadotropin-releasing hormone (GnRH) neurons at puberty, Mol. Cell. Endocrinol. 324 (2010) 45-50.
8. P.M. Collins, D.F. O'Neill, B.R. Barron, R.K. Moore, N.M. Sherwood, Gonadotropin-releasing hormone content in the brain and pituitary of male and female grass rockfish (Sebastes rastrelliger) in relation to seasonal changes in reproductive status, Biol. Repro. 65 (2001) 173-179.
9. N. de Roux, E. Genin, J.C. Carel, F. Matsuda, J.L. Chaussin, E. Milgrom, Hypogonadotropic hypogonadism due to loss of function of the Kiss1- derived peptide receptor GPR54, Proc. Nat. Acad. Sci. (USA). 100 (2003) 10972-10976.
10. W.S. Dhillo, O.B. Chaudhri, M. Patterson, E.L. Thompson, K.G. Murphy, M.K. Badman, B.M. McGowan, V. Amber, S. Patel, M.A. Ghatei, S.R. Bloom, Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males, J. Clin. Endocrinol. Metabol. 90 (2005) 6609-6615.
11. A. Elizur, The Kiss1/GPR54 system in fish, Peptides 30 (2009) 164-170.
12. S. Escobar, A. Servili, A. Felip, F. Espigares, A. Gómez, S. Zanuy, M. Carrillo, O. Kah, Neuroanatomical characterization of the Kisspeptin systems in the brain of European sea bass (D. labrax), in: 25th Conference of European Comparative Endocrinologists, Pècs, Hungary, 2010, pp. 90.
13. K.M. Estrada, C.M. Clay, S. Pompolo, J.T. Smith, I.J. Clarke, Elevated Kiss1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for Kisspeptin in oestrogen-positive feedback, J. Neuroendocrinol. 18 (2006) 806-809.
14. A. Felip, S. Zanuy, R. Pineda, L. Pinilla, M. Carrillo, M. Tena-Sempere, A. Gomez, Evidence for two distinct Kiss genes in non-placental vertebrates that encode Kisspeptins with different gonadotropin-releasing activities in fish and mammals, Mol. Cell. Endocrinol. 312 (2009) 61-71.
15. J. Felsenstein, Confidence limits on phylogenies: a approach using the bootstrap, Mole. Biol. Evol. 39 (1985) 783-791.
16. A.L. Filby, R. van Aerle, J. Duitman, C.R. Tyler, The Kisspeptin/Gonadotropinreleasing hormone pathway and molecular signaling of puberty in fish, Biol. Repro. 78 (2008) 278-289.
17. M.A. Fornies, J.M. Castellano, E. Mananos, L.A. Sorbera, Y. Zohar, S. Zanuy, Relative potency of the forms of GnRH and their analogs on LH-secretion in sea bass Dicentrarchus labrax, J. Fish Biol. 63 (2002) 73-89.
18. A. Fostier, R. Billard, B. Breton, M. Legendre, S. Marlot, Plasma 11- oxotestosterone and gonadotropin during the beginning of spermiation in rainbow trout (Salmo gairdneri R.), Gen. Comp. Endocrinol. 46 (1982) 428-434.
19. S. Funes, J.A. Hedrick, G. Vassileva, L. Markowitz, S. Abbondanzo, A. Golovko, S. Yang, F.J. Monsma, E.L. Gustafson, The Kiss1 receptor GPR54 is essential for the development of the murine reproductive system, Biochem. Biophys. Res. Commu. 312 (2003) 1357-1363.
20. D. Gonzalez-Martinez, N. Zamora, I. Anglade, T. Madigou, S. Zanuy, J.A. Munoz- Cueto, Y. Zohar, A. Elizur, O. Kah, Differential expression of the three different prepro-GnRH (gonadotropin-releasing hormone) messengers in the brain of the European sea bas (Dicentrarchus labrax), J. Comp. Neurol. 429 (2001) 144- 155.
21. D. González-Martínez, N. Zmora, E. Mañanos, D. Saligaut, S. Zanuy, Y. Zohar, A. Elizur, O. Kah, J.A. Muñoz-Cueto, Immunohistochemical localization of three different prepro GnRHs in the brain and pituitary of the European sea bass (Dicentrarchus labrax) using antibodies to the corresponding GnRH-associated peptides, J. Comp. Neurol. 446 (2002) 95-113.
22. D. Gonzalez-Martinez, N. Zamora, S. Zanuy, C. Sarasquete, A. Elizur, O. Kah, J.A. Munoz-Cueto, Developmental expression of three different prepro-GnRH messengers in the brain of the European sea bass Dincentrarchus labrax, J. Chem. Neuroanat. 23 (2002) 255-267.
23. D. González-Martínez, T. Madigou, E. Mañanós, J.M. Cerdá-Reverter, S. Zanuy, O. Kah, J.A. Muñoz-Cueto, Cloning and expression of gonadotropin-releasing hormone receptor in the brain and pituitary of the European sea bass: an in situ hybridization study, Biol. Repro. 70 (2004) 1380-1391.
24. D. Gonzalez-Martinez, T. Madigou, E. Mananos, J.M. Cerda-Reveter, S. Zanuy, O. Kah, J.A. Munoz-Cueto, Cloning and expression of the gonadotropin-releasing hormone receptor in the brain and pituitary of the European sea bass: an in situ hybridization study, Biol. Repro. 70 (2004) 1380-1391.
25. M.L. Gottsch, M.J. Canningham, J.T. Smith, S.M. Popa, B.V. Acohido, W.F. Crowley, S.B. Seminara, D.K. Clifton, R.A. Steiner, A role for kisspeptins in the regulation of gonadotropin secretion in the mouse, Gen. Comp. Endocrinol. 145 (2004) 4073-4077.
26. S.L. Gray, B.A. Adams, C.M. Warby, K.R. Schalburg, N. Sherwood, Transcripion and translation of salmon Gonadotropin -releasing hormone genes in brain and gonads of sexually maturing Rainbow trout (Oncorhynchus mykiss), Biol. Repro. 67 (2002) 1621-1627.
27. S. Han, M.L. Gottsch, K. Lee, S.M. Popa, J.T. Smith, S.K. Jakawich, D.K. Clifton, R.A. Steiner, A.E. Herbison, Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty, J. Neuroendocrinol. 25 (2005) 11349-11356.
28. M.S. Irwig, G.S. Fraley, J.T. Smith, B.V. Acohido, S.M. Popa, M.J. Cunningham, M.L. Gottsch, D.K. Clifton, R.A. Steiner, Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of Kiss1 mRNA in the male rat, J. Neuroendocrinol. 80 (2004) 264-272.
29. O. Kah, C. Lethimonier, G. Somoza, L.G. Guilgur, C. Vaillant, J.J. Lareyre, GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective, Gen. Comp. Endocrinol. 153 (2007) 346-364.
30. S. Kanda, Y. Akazome, T. Matsunaga, N. Yamamoto, S. Yamada, H. Tsukamura, K. Maeda, Y. Oka, Identification of Kiss1 product kisspeptin and steroidsensitive sexually dimorphic kisspeptin neurons in medaka Oryzias latipes, Gen. Comp. Endocrinol. 149 (2008) 2467-2476.
31. S. Kanda, T. Karigo, Y. Oka, Steroid sensitive kiss2 neurones in the goldfish: evolutionary insights into the duplicate kisspeptin gene-expressing neurones, J. Neuroendocrinol. (In press, http://dx.doi.org/10.1111/j.1365-2826.2012. 02296.x).
32. A.S. Kauffman, A. Wills, R.P. Millar, E.F. Rissman, Evidence that the type-2 Gonadotrophin-releasing hormone (GnRH) receptor mediates the behavioural effects of GnRH-II on feeding and reproduction in musk shrews, J. Neuroendocrinol. 17 (2005) 489-497.
33. A.S. Kauffmann, Coming of age in the kisspeptin era: sex differences, development and puberty, Mol. Cell. Endocrinol. 324 (2010) 51-63.
34. A.S. Kauffmann, D.K. Clifton, R.A. Steiner, Emerging ideas about kisspeptin GPR54 signaling in the neuroendocrine regulation of reproduction, Trends Neurosci. 30 (2007) 504-511.
35. D.Y. Kim, E.B. Cho, M.J. Moon, S. Park, J.I. Hwang, O. Kah, S.S. Sower, H. Vaudry, J.Y. Seong, Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes, Gen. Comp. Endocrinol. 170 (2011) 68-78.
36. D.-K. Kim, E.B. Cho, M.J. Moon, S. Park, J.-I. Hwang, J.-L. Do Rego, H. Vaudry, J.Y. Seong, Molecular coevolution of neuropeptides Gonadotropin-releasing hormone and Kiss peptin with their Cognate G protein-coupled receptors., Frontier Neurosci. 6 (2012), http://dx.doi.org/10.3389/fnins.2012.00003.
37. T. Kitahashi, S. Ogawa, I.S. Parhar, Cloning and expression of Kiss2 in the zebrafish and medaka, Gen. Comp. Endocrinol. 150 (2009) 821-831.
38. J.H. Lee, M.E. Miele, D.J. Hicks, K.K. Phillips, J.M. Trent, B.E. Weissman, D.R. Welch, Kiss1, a novel human malignant melanoma metastasissuppressorgene, J. Nat. Cancer Inst. 88 (1996) 1731-1737.
39. D.K. Lee, T. Nguyen, G.P. O'Neill, R. Cheng, Y. Liu, A.D. Howard, N. Coulombe, C.P. Tan, A. Tang-Nguyen, S.R. George, B.F. O'Dowd, Discovery of a receptor related to the galanin receptors, (FEBS) Lett. 446 (1999) 103-107.
40. Y.R. Lee, K. Tsunekawa, M.J. Moon, H.N. Um, J.I. Hwang, T. Osugi, N. Otaki, Y. Sunakawa, K. Kim, H. Vaudry, H.B. Kwon, J.Y. Seong, K. Tsutsui, Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates, Gen. Comp. Endocrinol. 150 (2009) 2837-2846.
41. S. Li, Y. Zhang, Y. Liu, X. Huang, W. Huang, D. Lu, P. Zhu, Y. Shi, C. Cheng, X. Liu, H. Lin, Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish Carassius auratus, J. Endocrinol. 201 (2009) 407-418.
42. E. Mananos, S. Zanuy, M. Carrillo, Photoperiodic manipulations of the reproductive cycle of sea bass (Dicentrarchus labrax) and their effects on gonadal development and plasma 17b-estradiol and vitellogenin, Fish physiol. Biochem. 16 (1997) 211-222.
43. T. Maniatis, Mechanism of alternative pre-mRNA splicing, Anim. Repro. Sci. 251 (1991) 33-34.
44. C.C. Martinez-Chavez, M. Minghetti, H. Migaud, GPR54 and rGnRH I gene expression during the onset of puberty in Nile tilapia, Gen. Comp. Endocrinol. 156 (2008) 224-233.
45. J. Mateos, E. Mananos, G. Martinez-Rodriguez, M. Carrillo, M. Querat, S. Zanuy, Molecular characterization of sea bass gonadotropin subunits(a, FSHb and LHb) and their expression during the reproductive cycle, Gen. Comp. Endocrinol. 13 (2003) 216-232.
46. H. Matsui, Y. Takatsu, S. Kumano, H. Matsumoto, T. Ohtaki, Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat, Biochem. Biophys. Res. Commu. 320 (2004) 383-388.
47. A.S. Mechaly, J. Vinas, F. Piferrer, Identification of two isoforms of the Kisspeptin-1 receptor (Kiss1r) generated by alternative splicing in a modern teleost, the Senegalese Sole (Solea senegalensis), Biol. Repro. 80 (2009) 60-69.
48. A.S. Mechaly, J. Vinas, C. Murphy, M. Reith, F. Piferrer, Gene structure of the kiss1 receptor-2 (kiss1r-2) in the Atlantic halibut: insights into the evolution and regulation of kiss1r genes, Mol. Cell. Endocrinol. 317 (2010) 78-89.
49. S. Messager, E.E. Chatzidaki, D. Ma, A.G. Hendrick, D. Zahn, J. Dixon, R.R. Thresher, I. Malinge, D. Lomet, M.B.L. Carlton, W.H. Colledge, A. Caraty, S.A. Aparicio, Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54, Proc. Nat. Acad. Sci. (USA). 102 (2005) 1761-1766.
50. H. Migaud, A. Davie, J.F. Taylor, Current knowledge on the photoneuroendocrime regulation of reproduction in temperate fish species, J. Fish Biol. 76 (2010) 27-68.
51. R.P. Millar, GnRHs and GnRH receptors, Anim. Repro. Sci. 88 (2005) 5-28.
52. L.A. Miranda, C.A. Strussmann, L.G. Guilgur, P.H. Strobl-Mazzula, G.M. Somoza, Cloning of FSH-b, LH-b and glycoprotein hormone a subunits in pejerrey Odontesthes bonariensis (Valenciennes): expression profile and relationship with GnRH expression and plasma sex steroid levels in male fish, J. Fish Biol. 71 (2007) 1571-1589.
53. Y. Mitani, S. Kanda, Y. Akazome, B. Zempo, Y. Oka, Hypothalamic kiss1 but not kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes), Gen. Comp. Endocrinol. 151 (2010) 1751-1759.
54. K. Mitter, G. Kotoulas, A. Magoulas, V. Mulero, P. Sepulcre, A. Figuease, B. Novoa, E. Sarropoulou, Evaluation of candidated reference genes for QPCR during ontogenesis and of immune-relevant tissues of European seabass (Dicentrarchus labrax), Comp. Biochem. Physiol. (B) 153 (2009) 340-347.
55. J.Sh. Mohamed, A.D. Benninghoff, G.J. Holt, I.A. Han, Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia, J. Mole. Endocrinol. 38 (2007) 235-244.
56. G. Moles, M. Carrillo, E. Mananos, C.C. Mylonas, S. Zanuy, Temporal profile of brain and pituitary GnRHs, GnRH-R and gonadotropin mRNA expression and content during early development in European sea bass Dicentrarchus labrax L., Gen. Comp. Endocrinol. 150 (2007) 75-86.
57. A.I. Muir, L. Chamberlain, N.A. Elshourbagy, D. Michalovich, D.J. Moore, A. Calamari, P.G. Szekeres, H.M. Sarau, J.K. Chambers, P. Murdock, K. Steplewski, U. Shabon, J.E. Miller, S.E. Middleton, J.G. Darker, C.G. Larminie, S. Wilson, D.J. Bergsma, P. Emson, R. Faull, K.L. Philpott, D.C. Harrison, AXOR12, a novel human G protein-coupled receptor, activated by the peptide Kiss1, J.Biol. Chem. 276 (2001) 28969-28975.
58. M. Nabissi, L. Soverchia, A. Polzonetti-Magni, H. Habibi, Differential splicing of three Gonadotropin-releasing hormone transcripts in the ovary of sea bream (Sparus aurata), Biol. Repro. 62 (2000) 1329-1337.
59. V.M. Navarro, J.M. Castellano, R. Fernandez-Fernandez, S. Tovar, J. Roa, A. Mayen, R. Nougueiras, M.J. Vazquez, M.L. Barreiro, P. Magni, E. Aguilar, C. Dieguez, L. Inilla, M. Tena-Sempere, Characterization of the potent luteinizing hormone-releasing activity of Kiss1 peptide, the natural ligand of GPR54, Gen. Comp. Endocrinol. 146 (2005) 156-163.
60. J.M. Navas, E. Man? anos, M. Thrush, J. Romos, S. Zanuy, M. Carrillo, Y. Zohar, N. Bromage, Effect of dietary lipid composition on vitellogenin, 17b-estradiol and gonadotropin plasma levels and spawning performance in captive sea bass (Dicentrarchus labrax), Morphol. aspects Aquacult. 165 (1998) 65-79.
61. J.N. Nocillado, B. Levavi-Sivan, F. Carrick, A. Elizur, Temporal expression of Gprotein- coupled receptor 54 (GPR54), gonadotropin-releasing hormones (GnRH) and dopamine receptor D2 (drd2) in pubertal female grey mullet Mugil cephalus, Gen. Comp. Endocrinol. 150 (2007) 278-287.
62. K. Okuzawa, K. Gen, M. Bruysters, J. Bogerd, Y. Gothilf, Y. Zohar, H. Kagawa, Seasonal variation of the three native gonadotropin-releasing hormone messenger ribonucleic acids levels in the brain of female red sea bream, Gen. Comp. Endocrinol. 130 (2003) 324-332.
63. N.W. Pankhurst, M.J.R. Porter, Cold and dark or warm and light: variations on the theme of environmental control of reproduction, Fish physiol. Biochem. 28 (2003) 385-389.
64. I.S. Parhar, S. Ogawa, Y. Sakuma, Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G Proteincoupled receptor (GPR54) during maturation in cichlid fish, Gen. Comp. Endocrinol. 145 (2004) 3613-3618.
65. M.G. Pawson, G.D. Pickett, The annual pattern of condition and maturity in bass (Dicentrarachus labrax L.) in waters around the UK, J. Mar. Biol. Assoc. UK. 76 (1996) 107-126.
66. F. Prat, S. Zanuy, M. Carrillo, A. Mones, A. Fostier, Seasonal changes in plasma levels of gonadal steroids of sea bass Dicentrarchus labrax L, Gen. Comp. Endocrinol. 78 (1990) 361-373.
67. L. Rodriguez, M. Carrillo, L.A. Sorbera, M.A. Soubrier, E. Mananos, M.C.H. Holland, Y. Zohar, S. Zanuy, Pituitary levels of three forms of GnRH in the male European sea bass (Dicentrarchus labrax, L.) during sex differentiation and first spawning season, Gen. Comp. Endocrinol. 120 (2000) 67-74.
68. N. Saitou, M. Nei, The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mole. Biol. Evol. 4 (1987) 406-425.
69. R.W. Schulz, L.R. Franca, J.J. Lareyre, F. LeGac, H. Chiarini-Garcia, R.H. Nobrega, T. Miura, Spermatogenesis in fish, Gen. Comp. Endocrinol. 3 (2010) 390-411.
70. S. Selvaraj, H. Kitano, Y. Fujinaga, H. Ohga, M. Yoneda, A. Yamaguchi, A. Shimizu, M. Matsuyama, 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, Gen. Comp. Endocrinol. 169 (2010) 28-38.
71. S. Selvaraja, H. Kitanoa, M. Amanob, M. Nyujia, K. Kanekoa, A. Yamaguchia, M. Matsuyamaa, Molecular characterization and expression profiles of three GnRH forms in the brain and pituitary of adult chub mackerel (Scomber japonicus) maintained in captivity, Morphol. aspects Aquacult. 356-357 (2012) 200-210.
72. S.B. Seminara, S. Messager, E.E. Chatzidaki, R.R. Thresher, J.S. Acierno Jr., J.K. Shagoury, Y. Bo-Abbas, W. Kuohung, K.M. Schwinof, A.G. Hendrick, D. Zahn, J. Dixon, U.B. Kaiser, S.A. Slaugenhaupt, J.F. Gusella, S. O'Rahilly, M.B.L. Carlton, W.F. Crowley, S.A. Aparicio, W.H. Colledge, The GPR54 gene as a regulator of puberty, New England J. Med. 349 (2003) 1614-1627.
73. A. Servili, C. Lethimonier, J. Lareyre, J.F. Olmeda, F.J. Sánchez-Vázquez, O. Kah, J.A. Munoz-Cueto, The highly conserved Gonadotropin-releasing hormone-2 form acts as a Melatonin-Releasing factor in the pineal of teleost fish, the European sea bass Dicentrarchus labrax, J. Neuroendocrinol. 15 (2010) 2265- 2275.
74. A. Servili, Y. Le Page, J. Leprince, A. Caraty, S. Escobar, I.S. Parhar, J.Y. Seong, H. Vaudry, O. Kah, Organisation of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish, Gen. Comp. Endocrinol. 1 (2011) 1527-1540.
75. M.D. Shahjahan, E. Motohashi, H. Doi, H. Ando, Elevation of Kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season, Gen. Comp. Endocrinol. 169 (2010) 48-57.
76. M.D. Shahjahan, T. Hamabata, E. Motohashi, H. Doi, H. Ando, Differential expression of three types of gonadotropin-releasing hormone genes during the spawning season in grass puffer Takifugu niphobles, Gen. Comp. Endocrinol. 167 (2010) 153-163.
77. Y. Shimizu, J. Tomikawa, K. Hirano, Y. Nanikawa, Y. Akazome, S. Kanda, Y. Kazeto, K. Okuzawa, Y. Uenoyama, S. Ohkura, H. Tsukamura, K. Maeda, K. Gen, Y. Oka, N. Yamamoto, Central distribution of kiss2 neurons and peri-pubertal changes in their expression in the brain of male and female red seabream Pagrus major, Gen. Comp. Endocrinol. 175 (2012) 432-442.
78. T. Shiraishi, S.D. Ketkar, H. Kitano, M. Nyuji, A. Yamaguchi, M. Matsuyama, Time course of final oocyte maturation and ovulation in chub mackerel Scomber japonicus induced by hCG and GnRHa, Fisheries Sci. 74 (2008) 764- 769.
79. J.T. Smith, H.M. Dungan, E.A. Stoll, M.L. Gottsch, R.E. Braun, S.M. Eacker, D.K. Clifton, R.A. Steiner, Differential regulation of Kiss1 mRNA expression by sex steroids in the brain of the male mouse, Gen. Comp. Endocrinol. 146 (2005) 2976-2984.
80. J.T. Smith, A. Rao, A. Pereira, A. Caraty, R.P. Millar, I.J. Clarke, Kisspeptin is present in ovine hypophysial portal blood but does not increase during the preovulatory luteinizing hormone surge: evidence that gonadotropes are not direct targets of kisspeptin in vivo, Gen. Comp. Endocrinol. 149 (2008) 1951- 1959.
81. K. Tamura, M. Nei, S. Kumar, Prospects for inferring very large phylogenies by using the neighbor-joining method, Proc. Nat. Acad. Sci. (USA). 101 (2004) 11030-11035.
82. K. Tamura, J. Dudley, M. Nei, S. Kumar, MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4, Mole. Biol. Evol. 24 (2007) 1596- 1599.
83. M. Tena-Sempere, A. Felip, A. Gomez, S. Zanuy, M. Carrillo, Comparative insights of the kisspeptin/kisspeptin receptor system: Lessons from nonmammalian vertebrates, Gen. Comp. Endocrinol. 175 (2012) 234-243.
84. J.D. Thompson, F. Plewniak, J.C. Thierry, O. Poch, DbClustal: rapid and reliable global multiple alignments of protein sequences detected by database searches, Nucleic Acids Res. 24 (2000) 1596-1599.
85. S. Uzbekova, F. Ferriere, Y. Guiguen, T. Bailhache, B. Breton, J. Lareyre, Stagedevelopment and alternative splicing of sGnRH messengers in rainbow trout testis during spermatogenesis, Mole. Reprod. Develop. 59 (2001) 1-10.
86. S. Uzbekova, J. Lareyre, T. Madigou, B. Davail, B. Jalabert, B. Breton, Expression of prepro-GnRH and GnRH receptor messengers in rainbow trout ovary depends on the stage of ovarian follicular development, Mole. Reprod. Develop. 62 (2002) 47-56.
87. R. van Aerle, P. Kille, A. Lange, C.R. Tyler, Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish, Peptides 29 (2008) 57-64.
88. B. Vidal, C. Pasqualini, N. Le Belle, M.C.H. Holland, M. Sbaihi, P. Vernier, Y. Zohar, S. Dufour, Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: a neuroendocrine lock for the onset of puberty, Biol. Repro. 71 (2004) 1491-1500.
89. F.A. Weltzien, E. Andersson, Ø. Andersen, K. Shalchian-Tabrizi, B. Norberg, The brain-pituitary-gonad axis in male teleost, with special emphasis on flatfish Pleuronectiformes, Comp. Biochem. Physiol. A 137 (2004) 447-477.
90. B.Q. Yang, T. Jiang, W.K. Ko Chan, A.O. Wong, Goldfish kisspeptin: molecular cloning, tissue distribution of transcript expression, and stimulatory effects on prolactin, growth hormone and luteinizing hormone secretion and gene expression via direct actions at the pituitary level, Gen. Comp. Endocrinol. 165 (2010) 60-71.
91. N. Zmora, D. González-Martínez, J.A. Muñoz-Cueto, T. Madigou, E. Mañanos- Sanchez, S.Z. Doste, Y. Zohar, O. Kah, A. Elizur, The GnRH system in the European sea bass Dicentrarchus labrax, J. Endocrinol. 172 (2002) 105-116.
92. N. Zmora, J. Stubblefield, Z. Zulperi, U. Klenke, Y. Zohar, Kisspeptin photoperiodic/ gonadal steroid relationships in the brain of two perciforms, the striped and hybrid basses, Ind J.Sci. Technol. 4 (2011) 10-11.
93. N. Zmora, J. Stubblefield, Z. Zulperi, J. Biran, B. Levavi-Sivan, J.A. Muñoz-Cueto, Y. Zohar, Differential and gonad stage-dependent roles of Kisspeptin1 and Kisspeptin2 in reproduction in the modern Teleosts, Morone species. Biol. Reprod. (In press, http://dx.doi.org/10.1095/biolreprod.111.097667).
94. Y. Zohar, J.A. Munoz-Cueto, A. Elizur, O. Kah, Neuroendocrinology of reproduction in teleost fish, Gen. Comp. Endocrinol. 165 (2010) 438-455.