Peripheral administration of kiss1 pentadecapeptide induces gonadal development in sexually immature adult scombroid fish

Zoological Science

Volumn 30, Issue 6, 2013, Pages 446-454

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

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Kiss1 15; Kiss2 12; kisspeptins; spermiation; vitellogenic onset

Indexed keywords

KISSPEPTIN; MESSENGER RNA; SEX HORMONE;

ANIMAL; ARTICLE; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PERCIFORMES; SEXUAL MATURATION;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADAL STEROID HORMONES; KISSPEPTINS; MALE; PERCIFORMES; RNA, MESSENGER; SEXUAL MATURATION;

RASTRELLIGER; SCOMBER JAPONICUS; TELEOSTEI;

EID: 84878530071     PISSN: 02890003     EISSN: None     Source Type: Journal    
DOI: 10.2108/zsj.30.446     Document Type: Article

References (71)

1. Ansel L, Bentsen AH, Ancel C, Bolborea M, Klosen P, Mikkelsen JD, et al. (2011) Peripheral kisspeptin reverses short photoperiodinduced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction 142: 417-425
2. Beck BH, Fuller SA, Peatman E, McEntire ME, Darwish A, Freeman DW (2012) Chronic exogenous kisspeptin administration accelerates gonadal development in basses of the genus Morone. Comp Biochem Physiol Part A 162: 265-273
3. Biran J, Ben-Dor S, Levavi-Sivan B (2008) Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol Reprod 79: 776-786
4. Bustin S, Benes V, Garson J, Hellemans J, Huggett J, Kubista M, et al. (2009) The MIQE guidelines: minimal information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622
5. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, et al. (2007) Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 148: 5258-5267
6. Caraty A, Decourt C, Briant C, Beltramo M (2012) Kisspeptins and the reproductive axis: potential applications to manage reproduction in farm animals. Domest Anim Endocrinol 43: 95-102
7. D'Anglemont de Tassigny X, Colledge WH (2010) The role of kisspeptin signaling in reproduction. Physiology (Bethesda) 25: 207-217
8. 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. Proc Natl Acad Sci USA 100: 10972-10976
9. Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364
10. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, et al. (2007) Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 92: 3958-3966
11. Elizur A, Nocillado JN, Biran J, Sivan B, Zohar Y (2011) Advancement of the onset of puberty in seriola lalandi by chronic treatment with kiss peptides. Indian J Sci Technol 4: 274-275
12. Escobar S, Felip A, Gueguen MM, Zanuy S, Carrillo M, Kah O, et al. (2012) Expression of kisspeptins in the brain and pituitary of the european sea bass (Dicentrarchus labrax). J Comp Neurol DOI:10.1002/cne.23211
13. Felip A, Zanuy S, Pineda R, Pinilla L, Carrillo M, Tena-Sempere M, et al. (2009) Evidence for two distinct KiSS genes in nonplacental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol Cell Endocrinol 312: 61-71
14. Filby AL, van Aerle R, Duitman JW, Tyler CR (2008) The kisspeptin/ gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol Reprod 78: 278-289
15. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, et al. (2004) A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145: 4073-4077
16. Grone BP, Maruska KP, Korzan WJ, Fernald RD (2010) Social status regulates kisspeptin receptor mRNA in the brain of Astatotilapia burtoni. Gen Comp Endocrinol 169: 98-107
17. Kanda S, Akazome Y, Matsunaga T, Yamamoto N, Yamada S, Tsukamura H, et al. (2008) Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 149: 2467-2476
18. Kim DK, Cho EB, Moon MJ, Park S, Hwang JI, Rego JLD, et al. (2012) Molecular coevolution of neuropeptides gonadotropinreleasing hormone and kisspeptin with their cognate G proteincoupled receptors. Front Neurosci 6: 1-8
19. Kitahashi T, Ogawa S, Parhar IS (2009) Cloning and expression of kiss2 in the Zebrafish and Medaka. Endocrinology 150: 821-831
20. Knobil E (1992) Remembrance: the discovery of the hypothalamic gonadotropin-releasing hormone pulse generator and of its physiological significance. Endocrinology 131: 1005-1006
21. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, et al. (2001) The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 276: 34631-34636
22. Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 62: 1-16
23. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, et al. (1996) KiSS-1, a novel human malignant melanoma metastasis-suppressor gene. J Natl Cancer Inst 88: 1731-1737
24. Lee JY, Moon JS, Eu YJ, Lee CW, Yang ST, Lee SK, et al. (2009a) Molecular interaction between kisspeptin decapeptide analogs and a lipid membrane. Arch Biochem Biophys 485: 109-114
25. Lee YR, Tsunekawa K, Moon MJ, Um HN, Hwang JI, Osugi T, et al. (2009b) Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150: 2837-2846
26. Li S, Zhang Y, Liu Y, Huang X, Huang W, Lu D, et al. (2009) Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J Endocrinol 201: 407-418
27. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T (2004) Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 320: 383-388
28. Matsuyama M, Takeuchi H, Kashiwagi M, Hirose K, Kagawa H (1995) Induced gonadal development and spawning of immature red seabream Pagrus major with LHRH-a administration in different ways during winter season. Fish Sci 61: 472-477
29. Matsuyama M, Shiraishi T, Sundaray JK, Rahman MA, Ohta K, Yamaguchi A (2005) Steroidogenesis in ovarian follicles of chub mackerel, Scomber japonicus. Zool Sci 22: 101-110
30. Mendiola D, Yamashita Y, Matsuyama M, Alvarez P, Tanaka M (2008) Scomber japonicus, H. is a better candidate species for juvenile production activities than Scomber scombrus. L. Aqua Res 39: 1122-1127
31. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, et al. (2001) AXOR12, a novel human G proteincoupled receptor, activated by the peptide KiSS-1. J Biol Chem 276: 28969-28975
32. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Dev Growth Differ S1: S195-S219
33. Navarro VM, Fernandez-Fernandez R, Castellano JM, Roa J, Mayen A, Barreiro ML, et al. (2004) Advanced vaginal opening and precocious activation of the reproductive axis by KiSS-1 peptide, the endogenous ligand of GPR54. J Physiol 561: 379-386
34. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, et al. (2005) Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 146: 1689-1697
35. Nocillado JN, Biran J, Lee YY, Levavi-Sivan B, Mechaly AS, Zohar Y, et al. (2012a) 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 362: 211-220
36. Nocillado JN, Mechaly AS, Elizur A (2012b) In silico analysis of the regulatory region of the Yellowtail Kingfish and Zebrafish Kiss and Kiss receptor genes. Fish Physiol Biochem DOI:10.1007/ s10695-012-9642-0
37. Nyuji M, Shiraishi T, Selvaraj S, In VV, Kitano H, Yamaguchi A, et al. (2011) Immunoreactive changes in pituitary FSH and LH cells during seasonal reproductive and spawning cycles of female chub mackerel Scomber japonicus. Fish Sci 77: 731-739
38. Nyuji M, Selvaraj S, Kitano H, Ohga H, Yoneda M, Shimizu A, et al. (2012a) Changes in the expression of pituitary gonadotropin subunits during reproductive cycle of multiple spawning female chub mackerel Scomber japonicus. Fish Physiol Biochem 38: 883-897
39. Nyuji M, Selvaraj S, Kitano H, Shiraishi T, Yamaguchi A, Shimizu A, et al. (2012b) 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 29: 623-629
40. Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocr Rev 30: 713-743
41. Ohga H, Kaneko K, Shimizu A, Kitano H, Selvaraj S, Nyuji M, et al. (2012a) Steroidogenic and maturation-inducing potency of native gonadotropic hormones in female chub mackerel, Scomber japonicus. Reprod Biol Endocrinol 10: 71
42. Ohga H, Selvaraj S, Fujinaga Y, Kitano H, Nyuji M, Yamaguchi A, et al. (2012b) Identification and seasonal expression variations of two subtypes of kisspeptin receptors in a scombroid fish, chub mackerel. In. Program Abstracts of the 2nd World Conference on Kisspeptin signaling in the brain, Japan 2012, p 138
43. Ohta K, Hirano M, Mine T, Mizutani H, Yamaguchi A, Matsuyama M (2008) Body color change and serum steroid hormone levels throughout the process of sex change in the adult wrasse, Pseudolabrus sieboldi. Mar Biol 153: 843-852
44. Ohta K, Sakai M, Sundaray JK, Kitano T, Takeda T, Yamaguchi A, et al. (2012) Bidirectional sex change induced by sex steroid implantation in the hermaphrodite fish, Pseudolabrus sieboldi. J Exp Zool 9999A: 1-9
45. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, et al. (2001) Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 411: 613-617
46. Okubo K, Nagahama Y (2008) Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol 193: 3-15
47. Orsini MJ, 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. J Med Chem 50: 462-471
48. Parhar I, Ogawa S, Kitahashi T (2012) RFamide peptides as mediators in environmental control of GnRH neurons. Prog Neurobiol 98: 176-196
49. Parhar IS, Ogawa S, Sakuma Y (2003) 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 145: 3613-3618
50. Pasquier J, Lafont AG, Leprince J, Vaudry H, Rousseau, Dufour S (2011) First evidence for a direct inhibitory effect of kisspeptins on LH expression in the eel, Anguilla anguilla. Gen Comp Endocrinol 173: 216-225
51. Pineda R, Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, Ruiz-Pino F, et al. (2010) Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 151: 722-730
52. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M (2012) Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 92: 1235-1316
53. Sébert ME, Lomet D, Ben Saïd S, Monget P, Briant C, Scaramuzzi RJ, et al. (2010) Insights into the mechanism by which kisspeptin stimulates a preovulatory LH surge and ovulation in seasonally acyclic ewes: Potential role of estradiol Domest Anim Endocrinol 38: 289-298
54. Selvaraj S, Kitano H, Fujinaga Y, Amano M, Takahashi A, Shimizu A, et al. (2009) Immunological characterization and distribution of three GnRH forms in the brain and pituitary gland of chub mackerel (S. japonicus). Zool Sci 26: 828-839
55. Selvaraj S, Kitano H, Fujinaga Y, Ohga H, Yoneda M, Yamaguchi A, et al. (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. Gen Comp Endocrinol 169: 28-38
56. Selvaraj S, Kitano H, Amano M, Ohga H, Yoneda M, Yamaguchi A, et al. (2012a) Increased expression of kisspeptin and GnRH forms in the brain of scombroid fish during final ovarian maturation and ovulation. Reprod Biol Endocrinol 10: 64
57. Selvaraj S, Kitano H, Amano M, Nyuji M, Kaneko K, Yamaguchi A, et al. (2012b) Molecular characterization and expression profiles of three GnRH forms in the brain and pituitary of adult chub mackerel (Scomber japonicus) maintained in captivity. Aquaculture 356/357: 200-210
58. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, et al. (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349: 1614-1627
59. Servili A, Le Page Y, Leprince J, Caraty A, Escobar S, Parhar IS, et al. (2011) Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 152: 1527-1540
60. Shiraishi T, Ketkar SD, Kitano H, Nyuji M, Yamaguchi A, Matsuyama M (2008a) Time course of final oocyte maturation and ovulation in chub mackerel Scomber japonicus induced by hCG and GnRHa. Fish Sci 74: 764-769
61. Shiraishi T, Okamoto K, Yoneda M, Sakai T, Ohshimo S, Onoe S, et al. (2008b) Age validat-ion, growth and annual reproductive cycle of chub Scomber japonicus off the waters of northern Kyushu and in the East China Sea. Fish Sci 74: 947-954
62. Smith JT, Saleh SN, Clarke IJ (2009) Seasonal and cyclical change in the luteinizing hormone response to kisspeptin in the ewe Neuroendocrinology 90: 283-291
63. Tena-Sempere M, Felip A, Gómez A, Zanuy S, Carillo M (2012) Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen Comp Endocrinol 175: 234-243
64. Tomita K, Niida A, Oishi S, Ohno H, Cluzeau J, Navenot JM, et al. (2006) Structure-activity relationship study on small peptidic GPR54 agonists. Bioorg Med Chem 14: 7595-7603
65. Tovar S, Vazquez MJ, Navarro VM, Fernandez-Fernandez R, Castellano JM, Vigo E, et al. (2006) Effects of single or repeated intravenous administration of kisspeptin upon dynamic LH secretion in conscious male rats. Endocrinology 147: 2696-2704
66. 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
67. Yang B, Jiang Q, Chan T, Ko KWW, Wong AOL (2010) 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: 60-71
68. Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B (2003) Regulation of fish gonadotropins. Int Rev Cytol 225: 131-185
69. Zmora N, Stubblefield J, Zulperi Z, Biran J, Levavi-Sivan B, Muñoz-Cueto JA, et al. (2012) Differential and gonad stage-dependent roles of kisspeptin1 and kisspeptin2 in reproduction in the modern teleosts Morone species. Biol Reprod 86: 177
70. Zohar Y, Mylonas CC (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture 197: 99-136
71. Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O (2010) Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 165: 438-455