Subcutaneous administration of Kiss1 pentadecapeptide accelerates spermatogenesis in prepubertal male chub mackerel (Scomber japonicus)

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 166, Issue 2, 2013, Pages 228-236

  Selvaraj, Sethu ^a   Ohga, Hirofumi ^a   Nyuji, Mitsuo ^a   Kitano, Hajime ^a   Nagano, Naoki ^a   Yamaguchi, Akihiko ^a   Matsuyama, Michiya ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

GnRHa; Kiss1 15; Kiss2 12; Kisspeptins; Spermatogenesis

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; GONADORELIN; KISSPEPTIN; KISSPEPTIN[1-15]; KISSPEPTIN[2-12]; LUTEINIZING HORMONE BETA SUBUNIT; RECOMBINANT FOLLITROPIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FISH; GENE EXPRESSION PROFILING; GERM CELL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PREPUBERTY; SCOMBER JAPONICUS; SEXUAL MATURATION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TELENCEPHALON; TESTIS;

EID: 84880254595     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.06.007     Document Type: Article

References (94)

1. Adachi H., Kodama R., Ohga H., Nyuji M., Selvaraj S., Yamamoto M., Ikeda A., Kato K., Yamamoto S., Yamaguchi A., Matsuyama M. Temporal expression of kisspeptins, kisspeptin receptors, GnRHs and GtHs during the pubertal process of chub mackerel, Scomber japonicus. Abstract book of 10th AFAF, CAA4 2013, April 30-May 4, Yeosu, Korea 2013, 544.
2. Alvarado M.N., Carrillo M., Felip A. Expression of kisspeptins and their receptors, gnrh1/gnrhr-II-1a and gonadotropin genes in the brain of adult male and female European seabass during different gonadal stages. Gen. Comp. Endocrinol. 2013, 187:104-116.
3. Amer M.A., Miura T., Miura C., Yamauchi K. Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol. Reprod. 2001, 65:1057-1066.
4. Beck B.H., Fuller S.A., Peatman E., McEntire M.E., Darwish A., Freeman D.W. Chronic exogenous kisspeptin administration accelerates gonadal development in basses of the genus Morone. Comp. Biochem. Physiol. A 2012, 162:265-273.
5. Biran J., Ben-Dor S., Levavi-Sivan B. Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol. Reprod. 2008, 79:776-786.
6. Bustin S., Benes V., Garson J., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M., Shipley G., Vandesompele J., Wittwer C. The MIQE guidelines: minimal information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
7. Caraty A., Smith J.T., Lomet D., Ben Said S., Morrissey A., Cognie J., Doughton B., Baril G., Briant C., Clarke I.J. Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 2007, 148:5258-5267.
8. Caraty A., Decourt C., Briant C., Beltramo M. Kisspeptins and the reproductive axis: potential applications to manage reproduction in farm animals. Domest. Anim. Endocrinol. 2012, 43:95-102.
9. Chianese R., Ciaramella V., Fasano S., Pierantoni R., Meccariello R. Kisspeptin receptor, GPR54, as a candidate for the regulation of testicular activity in the frog Rana esculenta. Biol. Reprod. 2013, 88:73.
10. D'Anglemont de Tassigny X., Colledge W.H. The role of kisspeptin signaling in reproduction. Physiology (Bethesda) 2010, 25:207-217.
11. Elizur A., Nocillado J.N., Biran J., Sivan B., Zohar Y. Advancement of the onset of puberty in Seriola lalandi by chronic treatment with kiss peptides. Indian J. Sci. Technol. 2011, 4:274-275.
12. Escobar S., Felip A., Gueguen M.M., Zanuy S., Carrillo M., Kah O., Servilli A. Expression of kisspeptins in the brain and pituitary of the European sea bass (Dicentrarchus labrax). J. Comp. Neurol. 2012, 10.1002/cne.23211.
13. Ezzat A.A., Saito H., Sawada T., Yaegashi T., Yamashita T., Hirata T.I., Sawai K., Hashizume T. Characteristics of the stimulatory effect of kisspeptin-10 on the secretion of luteinizing hormone, follicle-stimulating hormone and growth hormone in prepubertal male and female cattle. J. Reprod. Dev. 2009, 55:650-654.
14. Felip A., Zanuy S., Muriach B., Cerda-Reverter J.M., Carrillo M. Reduction of sexual maturation in male Dicentrarchus labrax by continuous light both before and during gametogenesis. Aquaculture 2008, 275:347-355.
15. Felip A., Zanuy S., Pineda R., Pinilla L., Carrillo M., Tena-Sempere M., Gómez A. 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. 2009, 312:61-71.
16. Filby A.L., van Aerle R., Duitman J.W., Tyler C.R. The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod. 2008, 78:278-289.
17. Gines R., Afonso J.M., Arguello A., Zamorano M.J., Lopez J.L. Growth in adult gilthead sea bream (Sparus aurata L.) as a result of interference in sexual maturation by different photoperiod regimes. Aquacult. Res. 2003, 34:73-83.
18. Gottsch M.L., Cunningham M.J., Smith J.T., Popa S.M., Acohido B.V., Crowley W.F., Seminara S., Clifton D.K., Steiner R.A. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004, 145:4073-4077.
19. Grone B.P., Maruska K.P., Korzan W.J., Fernald R.D. Social status regulates kisspeptin receptor mRNA in the brain of Astatotilapia burtoni. Gen. Comp. Endocrinol. 2010, 169:98-107.
20. Kanda S., Akazome Y., Matsunaga T., Yamamoto N., Yamada S., Tsukamura H., Maeda K., Oka Y. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 2008, 149:2467-2476.
21. Kanda S., Karigo T., Oka Y. Steroid sensitive kiss2 neurones in the goldfish: evolutionary insights into the duplicate kisspeptin gene-expressing neurons. J. Neuroendocrinol. 2012, 24:897-906.
22. Karlsen O., Norberg B., Kjesbu O.S., Taranger G.L. Effects of photoperiod and exercise on growth, liver size, and age at puberty in farmed Atlantic cod (Gadus morhua L.). ICES J. Mar. Sci. 2006, 63:355-364.
23. Kim D.K., Cho E.B., Moon M.J., Park S., Hwang J.I., Rego J.L.D., Vaudry H., Seong J.Y. Molecular coevolution of neuropeptides gonadotropin-releasing hormone and kisspeptin with their cognate G protein-coupled receptors. Front. Neurosci. 2012, 6:1-8.
24. Kitahashi T., Ogawa S., Parhar I.S. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 2009, 150:821-831.
25. Kotani M., Detheux M., Vandenbogaerde A., Communi D., Vanderwinden J.M., Le Poul E., Brézillon S., Tyldesley R., Suarez-Huerta N., Vandeput F., Blanpain C., Schiffmann S.N., Vassart G., Parmentier M. The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol. Chem. 2001, 276:34631-34636.
26. Kuohung W., Kaiser U.B. GPR54 and KiSS-1: role in the regulation of puberty and reproduction. Rev. Endocr. Metab. Disord. 2006, 7:257-263.
27. Larionov A., Krause A., Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005, 62:1-16.
28. Lee J.H., Miele M.E., Hicks D.J., Phillips K.K., Trent J.M., Weissman B.E., Welch D.R. KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J. Natl. Cancer Inst. 1996, 88:1731-1737.
29. Lee J.Y., Moon J.S., Eu Y.J., Lee C.W., Yang S.T., Lee S.K., Jung H.H., Kim H.H., Rhim H., Seong J.Y., Kim J.I. Molecular interaction between kisspeptin decapeptide analogs and a lipid membrane. Arch. Biochem. Biophys. 2009, 485:109-114.
30. Lee Y.R., Tsunekawa K., Moon M.J., Um H.N., Hwang J.I., Osugi T., Otaki N., Sunakawa Y., Kim K., Vaudry H., Kwon H.B., Seong J.Y., Tsutsui K. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 2009, 150:2837-2846.
31. Lents C.A., Heidorn N.L., Barb C.R., Ford J.J. Central and peripheral administration of kisspeptin activates gonadotropin but not somatotropin secretion in prepubertal gilts. Reproduction 2008, 135:879-887.
32. Levavi-Sivan B., Bogerd J., Mananos E.L., Gomez A., Lareyre J.J. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 2010, 165:412-437.
33. Li S., Zhang Y., Liu Y., Huang X., Huang W., Lu D., Zhu P., Shi Y., Cheng C.H., Liu X., Lin H. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J. Endocrinol. 2009, 201:407-418.
34. Matsui H., Takatsu Y., Kumano S., Matsumoto H., Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem. Biophys. Res. Commun. 2004, 320:383-388.
35. Matsuyama M., Shiraishi T., Sundaray J.K., Rahman M.A., Ohta K., Yamaguchi A. Steroidogenesis in ovarian follicles of chub mackerel, Scomber japonicus. Zool. Sci. 2005, 22:101-110.
36. McClure C.A., Hammell K.L., Moore M., Dohoo I.R., Burnley H. Risk factors for early sexual maturation in Atlantic salmon in seawater farms in New Brunswick and Nova Scotia, Canada. Aquaculture 2007, 272:370-379.
37. Mendiola D., Yamashita Y., Matsuyama M., Alvarez P., Tanaka M. Scomber japonicus, H. is a better candidate species for juvenile production activities than Scomber scombrus. L. Aquac. Res. 2008, 39:1122-1127.
38. Messager S., Chatzidaki E.E., Ma D., Hendrick A.G., Zahn D., Dixon J., Thresher R.R., Malinge I., Lomet D., Carlton M.B.L., Colledge W.H., Caraty A., Aparicio S.A. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:1761-1766.
39. Miura T., Yamauchi K., Takahashi H., Nagahama Y. The role of hormones in the acquisition of sperm motility in salmonid fish. J. Exp. Zool. 1992, 261:359-363.
40. Miura T., Miura C., Ohta T., Nader M.R., Todo T., Yamauchi K. Estradiol-17beta stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Commun. 1999, 264:230-234.
41. Muir A.I., Chamberlain L., Elshourbagy N.A., Michalovich D., Moore D.J., Calamari A., Szekeres P.G., Sarau H.M., Chambers J.K., Murdock P., Steplewski K., Shabon U., Miller J.E., Middleton S.E., Darker J.G., Larminie C.G., Wilson S., Bergsma D.J., Emson P., Faull R., Philpott K.L., Harrison D.C. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J. Biol. Chem. 2001, 276:28969-28975.
42. Murata S., Yamamoto S., Ishibashi R., Oka Y., Yoneshima H., Kato K., Miyashita S., Kumai H. Egg development and growth of larval and juvenile cultured chub mackerel Scomber japonicus (Perciformes: Scombridae) in a captive spawning experiment. Aquat. Sci. 2005, 53(3):319-324.
43. Nagahama Y., Yamashita M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, S1:S195-S219.
44. Navarro V.M., Fernandez-Fernandez R., Castellano J.M., Roa J., Mayen A., Barreiro M.L., Gaytan F., Aguilar E., Pinilla L., Dieguez C., Tena-Sempere M. Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J. Physiol. 2004, 561:379-386.
45. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Barreiro M.L., Casanueva F.F., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005, 146:1689-1697.
46. Navarro V.M., Castellano J.M., García-Galiano D., Tena-Sempere M. Neuroendocrine factors in the initiation of puberty: the emergent role of kisspeptin. Rev. Endocr. Metab. Disord. 2007, 8:11-20.
47. Nestor C.C., Briscoe A.M., Davis S.M., Valent M., Goodman R.L., Hileman S.M. Evidence of a role for kisspeptin and neurokinin B in puberty of female sheep. Endocrinology 2012, 153:2756-2765.
48. Nocillado J.N., Levavi-Sivan B., Carrick F., Elizur A. Temporal expression of G-protein-coupled receptor 54 (GPR54), gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female grey mullet, Mugil cephalus. Gen. Comp. Endocrinol. 2007, 150:278-287.
49. Nocillado J.N., Biran J., Lee Y.Y., Levavi-Sivan B., Mechaly A.S., Zohar Y., Elizur A. The Kiss2 receptor (Kiss2r) gene in southern bluefin tuna, Thunnus maccoyii and in yellowtail kingfish, Seriola lalandi - functional analysis and isolation of transcript variants. Mol. Cell. Endocrinol. 2012, 362:211-220.
50. Nocillado J.N., Mechaly A.S., Elizur A. In silico analysis of the regulatory region of the yellowtail kingfish and zebrafish Kiss and Kiss receptor genes. Fish Physiol. Biochem. 2012, 10.1007/s10695-012-9642-0.
51. Nyuji M., Shiraishi T., Selvaraj S., In V.V., Kitano H., Yamaguchi A., Matsuyama M. Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus. Fish. Sci. 2011, 77:731-739.
52. Nyuji M., Selvaraj S., Kitano H., Ohga H., Yoneda M., Shimizu A., Kaneko K., Yamaguchi A., Matsuyama M. Changes in the expression of pituitary gonadotropin subunits during reproductive cycle of multiple spawning female chub mackerel Scomber japonicus. Fish Physiol. Biochem. 2012, 38:883-897.
53. Nyuji M., Selvaraj S., Kitano H., Shiraishi T., Yamaguchi A., Shimizu A., Matsuyama M. Immunoreactivity of gonadotrophs (FSH and LH Cells) and gonadotropin subunit gene expression in the male chub mackerel Scomber japonicus pituitary during reproductive cycle. Zool. Sci. 2012, 29:623-629.
54. Oakley A.E., Clifton D.K., Steiner R.A. Kisspeptin signaling in the brain. Endocr. Rev. 2009, 30:713-743.
55. Ohga H., Kaneko K., Shimizu A., Kitano H., Selvaraj S., Nyuji M., Adachi H., Yamaguchi A., Matsuyama M. Steroidogenic and maturation-inducing potency of native gonadotropic hormones in female chub mackerel, Scomber japonicus. Reprod. Biol. Endocrinol. 2012, 10:71.
56. Ohga H., Selvaraj S., Fujinaga Y., Kitano H., Nyuji M., Yamaguchi A., Matsuyama M. Identification and seasonal expression variations of two subtypes of kisspeptin receptors in a scombroid fish, chub mackerel. Program Abstracts of the 2nd World Conference on kisspeptin signaling in the brain, Japan 2012 2012, 138.
57. Ohga H., Selvaraj S., Adachi H., Imanaga Y., Nyuji M., Kitano H., Yamaguchi A., Matsuyama M. Functional analysis of kisspeptin peptides using an intracerebroventricular administration method in adult chub mackerel (Scomber japonicus). Abstract book of 10th AFAF, CAA4 2013, April 30-May 4, Yeosu, Korea 2013, 265.
58. Ohta K., Hirano M., Mine T., Mizutani H., Yamaguchi A., Matsuyama M. Body color change and serum steroid hormone levels throughout the process of sex change in the adult wrasse, Pseudolabrus sieboldi. Mar. Biol. 2008, 153:843-852.
59. Ohta K., Sakai M., Sundaray J.K., Kitano T., Takeda T., Yamaguchi A., Matsuyama M. Bidirectional sex change induced by sex steroid implantation in the hermaphrodite fish, Pseudolabrus sieboldi. J. Exp. Zool. 2012, 9999A:1-9.
60. Ohtaki T., Shintani Y., Honda S., Matsumoto H., Hori A., Kanehashi K., Terao Y., Kumano S., Takatsu Y., Masuda Y., Ishibashi Y., Watanabe T., Asada M., Yamada T., Suenaga M., Kitada C., Usuki S., Kurokawa T., Onda H., Nishimura O., Fujino M. Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001, 411:613-617.
61. Okamura H., Yamamura T., Wakabayashi Y. Kisspeptin as a master player in the central control of reproduction in mammals: an overview of kisspeptin research in domestic animals. Anim. Sci. J. 2013, 10.1111/asj.12056.
62. Okubo K., Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol. 2008, 193:3-15.
63. Okuzawa K. Puberty in teleosts. Fish Physiol. Biochem. 2002, 26:31-41.
64. Orsini M.J., Klein M.A., Beavers M.P., Connolly P.J., Middleton S.A., Mayo K.H. Metastin (KiSS-1) mimetics identified from peptide structure-activity relationship-derived pharmacophores and directed small molecule database screening. J. Med. Chem. 2007, 50:462-471.
65. Parhar I.S., 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, 145:3613-3618.
66. Parhar I.S., Ogawa S., Kitahashi T. RFamide peptides as mediators in environmental control of GnRH neurons. Prog. Neurobiol. 2012, 98:176-196.
67. Pinilla L., Aguilar E., Dieguez C., Millar R.P., Tena-Sempere M. Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol. Rev. 2012, 92:1235-1316.
68. Redmond J.S., Macedo G.G., Velez I.C., Caraty A., Williams G.L., Amstalden M. Kisspeptin activates the hypothalamic-adenohypophyseal-gonadal axis in prepubertal ewe lambs. Reproduction 2011, 141:541-548.
69. Saito H., Sawada T., Yaegashi T., Goto Y., Jin J., Sawai K., Hashizume T. Kisspeptin-10 stimulates the release of luteinizing hormone and testosterone in pre- and postpubertal male goats. Anim. Sci. J. 2012, 83:487-492.
70. Sam A.H., Dhillo W.S. Kisspeptin: a critical regulator of puberty and reproductive function. Curr. Drug Targets 2010, 11:971-977.
71. Schulz R.W., de França L.R., Lareyre J.J., Le Gac F., Chiarini-Garcia H., Nobrega R.H., Miura T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010, 165(3):390-411.
72. Scott A.P., Witthames P.R., Vermeirssen E.L.M., Carolsfeld J. Prolonged-release gonadotropin-releasing hormone analogue implants enhance oocyte final maturation and ovulation, and increase plasma concentrations of sulphated C21 steroids in North Sea plaice. J. Fish Biol. 1999, 55:316-328.
73. Selvaraj S., Kitano H., Fujinaga Y., Amano M., Takahashi A., Shimizu A., Yamaguchi A., Matsuyama M. Immunological characterization and distribution of three GnRH forms in the brain and pituitary gland of chub mackerel (S. japonicus). Zool. Sci. 2009, 26:828-839.
74. Selvaraj S., Kitano H., Fujinaga Y., Ohga H., Yoneda M., Yamaguchi A., Matsuyama M. 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. 2010, 169:28-38.
75. Selvaraj S., Kitano H., Amano M., Nyuji M., Kaneko K., Yamaguchi A., Matsuyama M. Molecular characterization and expression profiles of three GnRH forms in the brain and pituitary of adult chub mackerel (Scomber japonicus) maintained in captivity. Aquaculture 2012, 356(357):200-210.
76. Selvaraj S., Kitano H., Amano M., Ohga H., Yoneda M., Yamaguchi A., Matsuyama M. Increased expression of kisspeptin and GnRH forms in the brain of scombroid fish during final ovarian maturation and ovulation. Reprod. Biol. Endocrinol. 2012, 10:64.
77. Selvaraj S., Ohga H., Kitano H., Nyuji M., Yamaguchi A., Matsuyama M. Peripheral administration of Kiss1 pentadecapeptide induces gonadal development in sexually immature adult scombroid fish. Zool. Sci. 2013, 30(6):446-454.
78. Servili A., Le Page Y., Leprince J., Caraty A., Escobar S., Parhar I.S., Seong J.Y., Vaudry H., Kah O. Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 2011, 152:1527-1540.
79. Shewmon L.N., Godwin J.R., Murashige R.S., Daniels H.V. Environmental manipulation of growth and sexual maturation in yellow perch, Perca flavescens. J. World Aquacult. Soc. 2007, 38:383-394.
80. Shimizu Y., Tomikawa J., Hirano K., Nanikawa Y., Akazome Y., Kanda S., Kazeto Y., Okuzawa K., Uenoyama Y., Ohkura S., Tsukamura H., Maeda K.I., Gen K., Oka Y., Yamamoto N. 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. 2012, 175:432-442.
81. Shiraishi T., Ohta K., Yamaguchi A., Yoda M., Chuda H., Matsuyama M. Reproductive parameters of the chub mackerel Scomber japonicus estimated from human chorionic gonadotropin induced final oocyte maturation and ovulation in captivity. Fish. Sci. 2005, 71:531-542.
82. Shiraishi T., Ketkar S.D., Kitano H., Nyuji M., Yamaguchi A., Matsuyama M. Time course of final oocyte maturation and ovulation in chub mackerel Scomber japonicus induced by hCG and GnRHa. Fish. Sci. 2008, 74:764-769.
83. Sundaray J.K., Ohta K., Yamaguchi A., Suzuki K., Matsuyama M. Diurnal rhythm of steroid biosynthesis in the testis of terminal phase male of protogynous wrasse, Pseudolabrus sieboldi, a daily spawner. Fish Physiol. Biochem. 2003, 28:193-195.
84. Tena-Sempere M., Felip A., Gómez A., Zanuy S., Carillo M. Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen. Comp. Endocrinol. 2012, 175:234-243.
85. Tomita K., Niida A., Oishi S., Ohno H., Cluzeau J., Navenot J.M., Wang Z.X., Peiper S.C., Fujii N. Structure-activity relationship study on small peptidic GPR54 agonists. Bioorg. Med. Chem. 2006, 14:7595-7603.
86. Tovar S., Vazquez M.J., Navarro V.M., Fernandez-Fernandez R., Castellano J.M., Vigo E., Roa J., Casanueva F.F., Aguilar E., Pinilla L., Dieguez C., Tena-Sempere M. Effects of single or repeated intravenous administration of kisspeptin upon dynamic LH secretion in conscious male rats. Endocrinology 2006, 147:2696-2704.
87. Ueda H., Kambegawa A., Nagahama Y. Involvement of gonadotrophin and steroid hormones in spermiation in the amago salmon, Oncorhynchus rhodurus, and goldfish, Carassius auratus. Gen. Comp. Endocrinol. 1985, 59:24-30.
88. Van Aerle R., Kille P., Lange A., Tyler C.R. Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 2008, 29:57-64.
89. Watanabe A., Endo G., Kashiwadate A., Ohkawa K., Onitake K. Estradiol-17β stimulates proliferation of type A spermatagonia independently of the inhibition of spermatogenesis in the medaka fish. J. Reprod. Dev. 2000, 46:69-70.
90. Weltzien F.-A., Karlsen O., Norberg B. Growth patterns and plasma levels of testoterone, 11-ketotestosterone, and IGF-1 in male Atlantic halibut (Hippoglossus hippoglossus) from juvenile stages throughout sexual development. Fish Physiol. Biochem. 2003, 28:227-228.
91. Yang B., Jiang Q., Chan T., Ko K.W.W., Wong A.O.L. 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. 2010, 165:60-71.
92. Yueh W.S., Chang C.F. 17a,20b,21-trihydroxy-4-pregnen-3-one and 17a,20b-dihydroxy-4-pregnen-3-one stimulated spermiation in protandrous black porgy, Acanthopagrus schlegeli. Fish Physiol. Biochem. 1997, 17:187-193.
93. Zmora N., Stubblefield J., Zulperi Z., Biran J., Levavi-Sivan B., Muñoz-Cueto J.A., Zohar Y. Differential and gonad stage-dependent roles of kisspeptin1 and kisspeptin2 in reproduction in the modern teleosts Morone species. Biol. Reprod. 2012, 86:177.
94. Zohar Y., Muñoz-Cueto J.A., Elizur A., Kah O. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 2010, 165:438-455.