Functional significance of GnRH and kisspeptin, and their cognate receptors in teleost reproduction

Frontiers in Endocrinology

Volumn 4, Issue MAR, 2013, Pages

  Gopurappilly, Renjitha ^a,b   Ogawa, Satoshi ^a   Parhar, Ishwar S ^a  

^a MONASH UNIVERSITY MALAYSIA   (Malaysia)

^b Manipal Academy of Higher Education   (India)

Author keywords

GnRH receptor; GPR54 ; Kisspeptin receptor; Reproduction; Teleost fish

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; GONADORELIN RECEPTOR; GONADORELIN RECEPTOR 1; GONADORELIN RECEPTOR 2; GONADORELIN RECEPTOR 3; KISSPEPTIN; KISSPEPTIN RECEPTOR 1; KISSPEPTIN RECEPTOR 2; NEUROPEPTIDE Y; SUBSTANCE P; UNCLASSIFIED DRUG;

GENE EXPRESSION; HUMAN; HYPOPHYSIS GONAD SYSTEM; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PUBERTY; RECEPTOR DOWN REGULATION; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; TELEOST;

EID: 84884186618     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2013.00024     Document Type: Review

References (132)

1. Akazome, Y., Kanda, S., Okubo, K., and Oka, Y. (2010). Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. J. Fish Biol. 76, 161-182.
2. Alok, D., Hassin, S., Sampath, K. R., Trant, J. M., Yu, K., and Zohar, Y. (2000). Characterization of a pituitary GnRH-receptor from a perciform fish, Morone saxatilis: functional expression in a fish cell line. Mol. Cell. Endocrinol. 168, 65-75.
3. Ando, H., Hew, C. L., and Urano, A. (2001). Signal transduction pathways and transcription factors involved in the gonadotropin-releasing hormone-stimulated gonadotropin subunit gene expression. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129, 525-532.
4. Ankley, G. T., and Johnson, R. D. (2004). Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. ILAR J. 45, 469-483.
5. Attwood, T. K. (2001). A compendium of specific motifs for diagnosing GPCR subtypes. Trends Pharmacol. Sci. 22, 162-165.
6. Batten, T. F. C., and Ingleton, P. M. (1987). "The structure and function of the hypothalamus and pituitary gland," in Fundamentals of Comparative Vertebrate Endocrinology, eds I. Chester-Jones, P. M. Ingleton, and J. G. Phillips (New York: Plenum Press), 285-409.
7. Biran, J., Ben-Dor, S., and Levavi-Sivan, B. (2008). Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol. Reprod. 79, 776-786.
8. Biran, J., Palevitch, O., Ben-Dor, S., and Levavi-Sivan, B. (2012). Neurokinin Bs and neurokinin B receptors in zebrafish-potential role in controlling fish reproduction. Proc. Natl. Acad. Sci. U.S.A. 109, 10269-10274.
9. Bjarnadottir, T. K., Schioth, H. B., and Fredriksson, R. (2005). The phylogenetic relationship of the glutamate and pheromone G-protein-coupled receptors in different vertebrate species. Ann. N. Y. Acad. Sci. 1040, 230-233.
10. Chandroo, K. P., Duncan, I. J. H., and Moccia, R. D. (2004). Can fish suffer? Perspectives on sentience, pain, fear and stress. Appl. Anim. Behav. Sci. 86, 225-250.
11. Chen, C. C., and Fernald, R. D. (2006). Distributions of two gonadotropin-releasing hormone receptor types in a cichlid fish suggest functional specialization. J. Comp. Neurol. 495, 314-323.
12. Chen, C. C., and Fernald, R. D. (2008). GnRH and GnRH receptors: distribution, function and evolution. J. Fish Biol. 73, 1099-1120.
13. Cheung, T. C., and Hearn, J. P. (2002). Molecular cloning and tissue expression of the gonadotropin-releasing hormone receptor in the tammar wallaby (Macropus eugenii). Reprod. Fertil. Dev. 14, 157-164.
14. Clarkson, J., and Herbison, A. E. (2006). Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin -releasing hormone neurons. Endocrinology 147, 5817-5825.
15. Corodimas, K. P., Rosenblatt, J. S., and Morrell, J. I. (1992). The habenular complex mediates hormonal stimulation of maternal behavior in rats. Behav. Neurosci. 106, 853-865.
16. d'Anglemont de Tassigny, X., and Colledge, W. H. (2010). The role of kisspeptin signaling in reproduction. Physiology (Bethesda) 25, 207-217.
17. e Roux, N., Genin, E., Carel, J. C., Matsuda, F., Chaussain, J. L., and Milgrom, E. (2003). Hypogonadotropic hypogonadism due to loss of function of the KiSS1- derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U.S.A. 100, 10972-10976.
18. Dungan, H. M., Clifton, D. K., and Steiner, R. A. (2006). Minireview: kisspeptin neurons as central processors in the regulation of gonadotropin-releasing hormone secretion. Endocrinology 147, 1154-1158.
19. Elizur, A. (2009). The KiSS1/GPR54 system in fish. Peptides 30, 164-170.
20. Felip, A., Zanuy, S., Pineda, R., Pinilla, L., Carrillo, M., Tena-Sempere, M., et al. (2009). 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, 61-71.
21. Ferguson, S. S. (2001). Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol. Rev. 53, 1-24.
22. Filby, A. L., Aerle, R. V., Duitman, J., and Tyler, C. R. (2008). The kisspeptin/gonadotropin-releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod. 78, 278-289.
23. Forfar, R., and Lu, Z.-L. (2011). Role of the transmembrane domain 4/extracellular loop 2 junction of the human gonadotropin-releasing hormone receptor in ligand binding and receptor conformational selection. J. Biol. Chem. 286, 34617-34626.
24. Gonzalez-Martinez, D., Madigou, T., Mananos, E., Cerda-Reverter, J. M., Zanuy, S., Kah, O., et al. (2004). Cloning and expression of gonadotropin-releasing hormone receptor in the brain and pituitary of the European sea bass: an in situ hybridization study. Biol. Reprod. 70, 1380-1391.
25. Grone, B. P., Carpenter, R. E., Lee, M., Maruska, K. P., and Fernald, R. D. (2012). Food deprivation explains effects of mouthbrooding on ovaries and steroid hormones, but not brain neuropeptide and receptor mRNAs, in an African cichlid fish. Horm. Behav. 62, 18-26.
26. Grone, B. P., Maruska, K. P., Korzan, W. J., and Fernald, R. D. (2010). Social status regulates kisspeptin receptor mRNA in the brain of Astatotilapia burtoni. Gen. Comp. Endocrinol. 169, 98-107.
27. Gur, G., Bonfil, D., Safarian, H., Naor, Z., and Yaron, Z. (2002). GnRH signaling pathways regulate differentially the tilapia gonadotropin subunit genes. Mol. Cell. Endocrinol. 189, 125-134.
28. Gutiérrez-Pascual, E., Martínez-Fuentes, A. J., Pinilla, L., Tena-Sempere, M., Malagón, M. M., and Castaño, J. P. (2007). Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion. J. Neuroendocrinol. 19, 521-530.
29. Han, S. K., Gottsch, M. L., Lee, K. J., Popa, S. M., Smith, J. T., Jakawich, S. K., et al. (2005). Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J. Neurosci. 25, 11349-11356.
30. Hanchate, N. K., Parkash, J., Bellefontaine, N., Mazur, D., Colledge, W. H., d'Anglemont de Tassigny, X., et al. (2012). Kisspeptin-GPR54 signaling in mouse NOsynthesizing neurons participates in the hypothalamic control of ovulation. J. Neurosci. 32, 932-945.
31. Hapgood, J. P., Sadie, H., Van Biljon, W., and Ronacher, K. (2005). Regulation of expression of mammalian gonadotropin-releasing hormone receptor genes. J. Neuroendocrinol. 17, 619-638.
32. Heitman, L. H., and Ijzerman, A. P. (2008). G protein-coupled receptors of the hypothalamic-pituitary-gonadal axis: a case for Gnrh, LH, FSH, and GPR54 receptor ligands. Med. Res. Rev. 28, 975-1011.
33. Herbison, A. E., d'Anglemont de Tassigny, X., Doran, J., and Colledge, W. H. (2010). Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons. Endocrinology 151, 312-321.
34. Hildahl, J., Taranger, G. L., Norberg, B., Haug, T. M., and Weltzien, F.-A. (2013). Differential regulation of GnRH ligand and receptor genes in the brain and pituitary of Atlantic cod exposed to different photoperiod. Gen. Comp. Endocrinol. 180, 7-14.
35. Illing, N., Troskie, B. E., Nahorniak, C. S., Hapgood, J. P., Peter, R. E., and Millar, R. P. (1999). Two gonadotropin-releasing hormone receptor subtypes with distinct ligand selectivity and differential distribution in brain and pituitary in the goldfish (Carassius auratus). Proc. Natl. Acad. Sci. U.S.A. 96, 2526-2531.
36. Irwig, M. S., Fraley, G. S., Smith, J. T., Acohido, B. V., Popa, S. M., Cunningham, M. J., et al. (2004). Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80, 264-272.
37. Jodo, A., Ando, H., and Urano, A. (2003). Five different types of putative GnRH receptor gene are expressed in the brain of masu salmon (Oncorhynchus masou). Zool. Sci. 20, 1117-1125.
38. Kadokawa, H., Matsui, M., Hayashi, K., Matsunaga, N., Kawashima, C., Shimizu, T., et al. (2008a). Peripheral administration of kisspeptin-10 increases plasma concentrations of GH as well as LH in prepubertal Holstein heifers. J. Endocrinol. 196, 331-334.
39. Kadokawa, H., Suzuki, S., and Hashizume, T. (2008b). Kisspeptin-10 stimulates the secretion of growth hormone and prolactin directly from cultured bovine anterior pituitary cells. Anim. Reprod. Sci. 105, 404-408.
40. Kah, O., Breton, B., and Dulka, J. G. (1986). A reinvestigation of the Gn-RH (gonadotropin-releasing hormone) systems in the goldfish brain using antibodies to salmon Gn-RH. Cell Tissue Res. 244, 327-337.
41. Kaiser, U. B., and Kuohung, W. (2005). KiSS-1 and GPR54 as new players in gonadotropin regulation and puberty. Endocrine 26, 277-284.
42. 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.
43. Karges, B., Karges, W., and De Roux, N. (2003). Clinical and molecular genetics of the human GnRH receptor. Hum. Reprod. Update 9, 523-530.
44. Khalil, M. H., Silverman, A.-J., and Silver, R. (2003). Mast cells in the rat brain synthesize gonadotropin-releasing hormone. J. Neurobiol. 56, 113-124.
45. Kim, D.-K., Cho, E. B., Moon, M. J., Park, S., Hwang, J.-I., Kah, O., et al. (2011). Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes. Gen. Comp. Endocrinol. 170, 68-78.
46. Kitahashi, T., Ogawa, S., and Parhar, I. S. (2009). Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150, 821-831.
47. Klemm, W. R. (2004). Habenular and interpeduncularis nuclei: shared components in multiple-function networks. Med. Sci. Monit. 10, RA261-RA273.
48. Kochman, K. (2012). Evolution of gonadotropin-releasing hormone (GnRH) structure and its receptor. J. Anim. Feed Sci. 21, 3-30.
49. Kotani, M., Detheux, M., Vandenbogaerde, A., Communi, D., Vanderwinden, J. M., 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.
50. Krsmanovic, L. Z., Mores, N., Navarro, C. E., Arora, K. K., and Catt, K. J. (2003). An agonist-induced switch in G protein coupling of the gonadotropin-releasing hormone receptor regulates pulsatile neuropeptide secretion. Proc. Natl. Acad. Sci. U.S.A. 100, 2969-2974.
51. Lee, D. K., Nguyen, T., O'Neill, G. P., Cheng, R., Liu, Y., Howard, A. D., et al. (1999). Discovery of a receptor related to the galanin receptors. FEBS Lett. 446, 103- 107.
52. Lee, Y. R., Tsunekawa, K., Moon, M. J., Um, H. N., Hwang, J. I., Osugi, T., et al. (2009). Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150, 2837-2846.
53. Lethimonier, C., Madigou, T., Munoz-Cueto, J. A., Lareyre, J. J., and Kah, O. (2004). Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen. Comp. Endocrinol. 135, 1-16.
54. Levavi-Sivan, B., and Avitan, A. (2005). Sequence analysis, endocrine regulation, and signal transduction of GnRH receptors in teleost fish. Gen. Comp. Endocrinol. 142, 67-73.
55. Levavi-Sivan, B., Safarian, H., Rosenfeld, H., Elizur, A., and Avitan, A. (2004). Regulation of gonadotropin-releasing hormone (GnRH)-receptor gene expression in tilapia: effect of GnRH and dopamine. Biol. Reprod. 70, 1545-1551.
56. 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.
57. Liu, F., Usui, I., Evans, L. G., Austin, D. A., Mellon, P. L., Olefsky, J. M., et al. (2002). Involvement of both Gq/11 and Gs proteins in gonadotropin-releasing hormone receptor-mediated signaling in L??T2 Cells. J. Biol. Chem. 277, 32099-32108.
58. Madigou, T., Mananos-Sanchez, E., Hulshof, S., Anglade, I., Zanuy, S., and Kah, O. (2000). Cloning, tissue distribution, and central expression of the gonadotropinreleasing hormone receptor in the rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 63, 1857-1866.
59. Marinissen, M. J., and Gutkind, J. S. (2001). G-protein-coupled receptors and signaling networks: emerging paradigms. Trends Pharmacol. Sci. 22, 368-376.
60. Martinez-Chavez, C. C., Minghetti, M., and Migaud, H. (2008). GPR54 and rGnRH I gene expression during the onset of puberty in Nile tilapia. Gen. Comp. Endocrinol. 156, 224-233.
61. Matthews-Felton, T., Corodimas, K. P., Rosenblatt, J. S., and Morrell, J. I. (1995). Lateral habenula neurons are necessary for the hormonal onset of maternal behavior and for the display of postpartum estrus in naturally parturient female rats. Behav. Neurosci. 109, 1172-1188.
62. McArdle, C. A., Franklin, J., Green, L., and Hislop, J. N. (2002). Signalling, cycling and desensitisation of gonadotropin-releasing hormone receptors. J. Endocrinol. 173, 1-11.
63. Mechaly, A. S., Vinas, J., Murphy, C., Reith, M., and Piferrer, F. (2010). 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, 78-89.
64. Mechaly, A. S., Vinas, J., and 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). Biol. Reprod. 80, 60-69.
65. Mechaly, A. S., Vinas, J., and 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. Mol. Cell. Endocrinol. 339, 14-24.
66. Messager, S., Chatzidaki, E. E., Ma, D., Hendrick, A. G., Zahn, D., Dixon, J., et al. (2005). Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U.S.A. 102, 1761-1766.
67. Metpally, R. P., and Sowdhamini, R. (2005). Genome wide survey of G protein-coupled receptors in Tetraodon nigroviridis. BMC Evol. Biol. 5:41. doi:10.1186/1471- 2148-5-41
68. Millar, R. P. (2003). GnRH II and type II GnRH receptors. Trends Endocrinol. Metab. 14, 35-43.
69. Millar, R. P., Lu, Z. L., Pawson, A. J., Flanagan, C. A., Morgan, K., and Maudsley, S. R. (2004). Gonadotropin-releasing hormone receptors. Endocr. Rev. 25, 235- 275.
70. Millar, R. P., and Newton, C. L. (2010). The year in G protein-coupled receptor research. Mol. Endocrinol. 24, 261-274.
71. Mitani, Y., Kanda, S., Akazome, Y., Zempo, B., and Oka, Y. (2010). Hypothalamic Kiss1 but not Kiss2 neurons are involved in estrogen feedback in medaka (Oryzias latipes). Endocrinology 151, 1751-1759.
72. Miyamoto, K., Hasegawa, Y., Nomura, M., Igarashi, M., Kangawa, K., and Matsuo, H. (1984). Identification of the second gonadotropin-releasing hormone in chicken hypothalamus: evidence that gonadotropin secretion is probably controlled by two distinct gonadotropin-releasing hormones in avian species. Proc. Natl. Acad. Sci. U.S.A. 81, 3874-3878.
73. Modianos, D. T., Hitt, J. C., and Flexman, J. (1974). Habenular lesions produce decrements in feminine, but not masculine, sexual behavior in rats. Behav. Biol. 10, 75-87.
74. Mohamed, J. S., Benninghoff, A. D., Holt, G. J., and Khan, I. A. (2007). Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia. J. Mol. Endocrinol. 38, 235-244.
75. Mollusk, A., Nematode, A. A., Echinoderm, G., Hemichordate, G., Mollusk, G., Arthropod, A. C. R., et al. (2011). "GnRHR superfamily: vertebrates and invertebrates," in Handbook of Neuroendocrinology, eds G. Fink, D. W. Pfaff, and J. Levine (Amsterdam/Boston: Elsevier/Academic Press), 81.
76. Moncaut, N., Somoza, G., Power, D. M., and Canario, A. V. (2005). Five gonadotropin-releasing hormone receptors in a teleost fish: isolation, tissue distribution and phylogenetic relationships. J. Mol. Endocrinol. 34, 767-779.
77. Mousa, S. A., and Mousa, M. A. (2006). Involvement of corticotropin-releasing factor and adrenocorticotropic hormone in the ovarian maturation, seawater acclimation, and induced spawning of Liza ramada. Gen. Comp. Endocrinol. 146, 167-179.
78. Neckers, L. M., Schwartz, J., Wyatt, R. J., and Speciale, S. G. (1979). Substance P afferents from the habenula innervate the dorsal raphe nucleus. Exp. Brain Res. 37, 619-623.
79. Neill, J. D. (2002). Minireview: GnRH and GnRH receptor genes in the human genome. Endocrinology 143, 737-743.
80. Nocillado, J. N., Biran, J., Lee, Y. Y., Levavi-Sivan, B., Mechaly, A. S., Zohar, Y., et al. (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. Mol. Cell. Endocrinol. 362, 211-220.
81. Nocillado, J. N., Levavi-Sivan, B., Carrick, F., and Elizur, A. (2007). 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. 150, 278-287.
82. Oakley, A. E., Clifton, D. K., and Steiner, R. A. (2009). Kisspeptin signaling in the brain. Endocr. Rev. 30, 713-743.
83. Ogawa, S., Kitahashi, T., Ng, K. W., and Parhar, I. S. (2010). "Autocrine regulation of kiss1 in the habenula of the zebrafish," in Proceedings of the 7th International Congress of Neuroendocrinology, abstr., Rouen, P2-P20.
84. Ogawa, S., Ng, K. W., Ramadasan, P. N., Nathan, F. M., and Parhar, I. S. (2012a). Habenular Kiss1 neurons modulate the serotonergic system in the brain of zebrafish. Endocrinology 153, 2398-2407.
85. Ogawa, S., Ramadasan, P. N., Goschorska, M., Anantharajah, A., We Ng, K., and Parhar, I. S. (2012b). Cloning and expression of tachykinins and their association with kisspeptins in the brains of zebrafish. J. Comp. Neurol. 520, 2991-3012.
86. Ogawa, S., and Parhar, I. S. (2013). Anatomy of the kisspeptin systems in teleosts. Gen. Comp. Endocrinol. 181, 169-174.
87. Oka, Y. (2009). Three types of gonadotropin-releasing hormone neurones and steroid-sensitive sexually dimorphic kisspeptin neurones in teleosts. J. Neuroendocrinol. 21, 334-338.
88. Okubo, K., Ishii, S., Ishida, J., Mitani, H., Naruse, K., Kondo, M., et al. (2003). A novel third gonadotropin-releasing hormone receptor in the medaka Oryzias latipes: evolutionary and functional implications. Gene 314, 121-131.
89. Okubo, K., and Nagahama, Y. (2008). Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol. (Oxf.) 193, 3-15.
90. Okubo, K., Nagata, S., Ko, R., Kataoka, H., Yoshiura, Y., Mitani, H., et al. (2001). Identification and characterization of two distinct GnRH receptor subtypes in a teleost, the medaka Oryzias latipes. Endocrinology 142, 4729-4739.
91. Okubo, K., Suetake, H., Usami, T., and Aida, K. (2000). Molecular cloning and tissue-specific expression of a gonadotrophin-releasing hormone receptor in the Japanese eel. Gen. Comp. Endocrinol. 119, 181-192.
92. Parhar, I. S. (2002). Cell migration and evolutionary significance of GnRH subtypes. Prog. Brain Res. 141, 3-17.
93. Parhar, I. S., Ogawa, S., and Sakuma, Y. (2004). 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.
94. Parhar, I. S., Ogawa, S., and Sakuma, Y. (2005a). Three GnRH receptor types in laser-captured single cells of the cichlid pituitary display cellular and functional heterogeneity. Proc. Natl. Acad. Sci. U.S.A. 102, 2204-2209.
95. Parhar, I. S., Soga, T., Ogawa, S., Ogawa, S., Pfaff, D. W., and Sakuma, Y. (2005b). Nonmammalian gonadotropin-releasing hormone molecules in the brain of promoter transgenic rats. Proc. Natl. Acad. Sci. U.S.A. 102, 5880-5885.
96. Parhar, I. S., Soga, T., Sakuma, Y., and Millar, R. P. (2002). Spatio-temporal expression of gonadotropin-releasing hormone receptor subtypes in gonadotropes, somatotropes and lactotropes in the cichlid fish. J. Neuroendocrinol. 14, 657-665.
97. Pasquier, J., Lafont, A. G., Leprince, J., Vaudry, H., Rousseau, K., and 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.
98. Qin, F., Wang, L., Wang, X., Liu, S., Xu, P., Wang, H., et al. (2013). Bisphenol A affects gene expression of gonadotropin-releasing hormones and type I GnRH receptors in brains of adult rare minnow Gobiocypris rarus. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 157, 192-202.
99. Ramaswamy, S., Guerriero, K. A., Gibbs, R. B., and Plant, T. M. (2008). 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 149, 4387-4395.
100. Robison, R. R., White, R. B., Illing, N., Troskie, B. E., Morley, M., Millar, R. P., et al. (2001). Gonadotropin-releasing hormone receptor in the teleost Haplochromis burtoni: structure, location, and function. Endocrinology 142, 1737-1743.
101. Roch, G. J., Busby, E. R., and Sherwood, N. M. (2011). Evolution of GnRH: diving deeper. Gen. Comp. Endocrinol. 171, 1-16.
102. Rønnekleiv, O. K., Bosch, M. A., and Zhang, C. (2010). Regulation of endogenous conductances in GnRH neurons by estrogens. Brain Res. 1364, 25-34.
103. Sealfon, S. C., Weinstein, H., and Millar, R. P. (1997). Molecular mechanisms of ligand interaction with the gonadotropin-releasing hormone receptor. Endocr. Rev. 18, 180-205.
104. 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.
105. Seminara, S. B., Messager, S., Chatzidaki, E. E., Thresher, R. R., Acierno, J. S. Jr., Shagoury, J. K., et al. (2003). The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 349, 1614-1627.
106. Servili, A., Le Page, Y., Leprince, J., Caraty, A., Escobar, S., Parhar, I. S., et al. (2011). Organization of two independent kisspeptin systems derived from evolutionaryancient kiss genes in the brain of zebrafish. Endocrinology 152, 1527-1540.
107. Shahjahan, M., Motohashi, E., Doi, H., and Ando, H. (2010). Elevation of Kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season. Gen. Comp. Endocrinol. 169, 48-57.
108. Sherwood, N. (1987). The GnRH family of peptides. Trends Neurosci. 10, 129-132.
109. Sherwood, N. M., Lovejoy, D. A., and Coe, I. R. (1993). Origin of mammalian gonadotropin-releasing hormones. Endocr. Rev. 14, 241-254.
110. Shi, Y., Zhang, Y., Li, S., Liu, Q., Lu, D., Liu, M., et al. (2010). Molecular identification of the Kiss2/Kiss1ra system and its potential function during 17alphamethyltestosterone- induced sex reversal in the orange-spotted grouper, Epinephelus coioides. Biol. Reprod. 83, 63-74.
111. Shoichet, B. K., and Kobilka, B. K. (2012). Structure-based drug screening for G-protein-coupled receptors. Trends Pharmacol. Sci. 33, 268-272.
112. Smith, Y., Parent, A., Kerkérian, L., and Pelletier, G. (1985). Distribution of neuropeptide Y immunoreactivity in the basal forebrain and upper brainstem of the squirrel monkey (Saimiri sciureus). J. Comp. Neurol. 236, 71-89.
113. Soga, T., Ogawa, S., Millar, R. P., Sakuma, Y., and Parhar, I. S. (2005). Localization of the three GnRH types and GnRH receptors in the brain of a cichlid fish: insights into their neuroendocrine and neuromodulator functions. J. Comp. Neurol. 487, 28-41.
114. Teitelbaum, P., and Epstein, A. N. (1962). The lateral hypothalamic syndrome: recovery of feeding and drinking after lateral hypothalamic lesions. Psychol. Rev. 69, 74-90.
115. Tena-Sempere, M., Felip, A., Gomez, A., Zanuy, S., and Carrillo, M. (2012). Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from nonmammalian vertebrates. Gen. Comp. Endocrinol. 175, 234-243.
116. Tensen, C., Okuzawa, K., Blomenrohr, M., Rebers, F., Leurs, R., Bogerd, J., et al. (1997). Distinct efficacies for two endogenous ligands on a single cognate gonadoliberin receptor. Eur. J. Biochem. 243, 134-140.
117. Tostivint, H. (2011). Evolution of the gonadotropin-releasing hormone (GnRH) gene family in relation to vertebrate tetraploidizations. Gen. Comp. Endocrinol. 170, 575-581.
118. Troskie, B., Illing, N., Rumbak, E., Sun, Y. M., Hapgood, J., Sealfon, S., et al. (1998). Identification of three putative GnRH receptor subtypes in vertebrates. Gen. Comp. Endocrinol. 112, 296-302.
119. Tsai, P. S. (2006). Gonadotropin-releasing hormone in invertebrates: structure, function, and evolution. Gen. Comp. Endocrinol. 148, 48-53.
120. Tsutsumi, M., Zhou, W., Millar, R. P., Mellon, P. L., Roberts, J. L., Flanagan, C. A., et al. (1992). Cloning and functional expression of a mouse gonadotropinreleasing hormone receptor. Mol. Endocrinol. 6, 1163-1169.
121. Um, H. N., Han, J. M., Hwang, J. I., Hong, S. I., Vaudry, H., and Seong, J. Y. (2010). Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann. N. Y. Acad. Sci. 1200, 67-74.
122. van Aerle, R., Kille, P., Lange, A., and Tyler, C. R. (2008). Evidence for the existence of a functional Kiss1/Kiss1 receptor pathway in fish. Peptides 29, 57-64.
123. Villani, L., Guarnieri, T., Salsi, U., and Bollini, D. (1991). Substance P in the habenulo-interpeduncular system of the goldfish. Brain Res. Bull. 26, 225-228.
124. Volkoff, H., Canosa, L. F., Unniappan, S., Cerda-Reverter, J. M., Bernier, N. J., Kelly, S. P., et al. (2005). Neuropeptides and the control of food intake in fish. Gen. Comp. Endocrinol. 142, 3-19.
125. Volkoff, H., and Peter, R. E. (1999). Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen. Comp. Endocrinol. 116, 347-355.
126. Weltzien, F. A., Andersson, E., Andersen, O., Shalchian-Tabrizi, K., and Norberg, B. (2004). The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp. Biochem. Physiol. A Mol Integr. Physiol. 137, 447-477.
127. White, R. B., and Fernald, R. D. (1998). Genomic structure and expression sites of three gonadotropin-releasing hormone genes in one species. Gen. Comp. Endocrinol. 112, 17-25.
128. Yang, B., Jiang, Q., Chan, T., Ko, W. K., and Wong, A. O. (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.
129. Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Elizur, A., and Levavi-Sivan, B. (2003). Regulation of fish gonadotropins. Int. Rev. Cytol. 225, 131-185.
130. Zhao, H., and Rusak, B. (2005). Circadian firing-rate rhythms and light responses of rat habenular nucleus neurons in vivo and in vitro. Neuroscience 132, 519-528.
131. Zmora, N., Stubblefield, J., Zulperi, Z., Biran, J., Levavi-Sivan, B., Muñoz-Cueto, J.-A., 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.
132. Zohar, Y., Munoz-Cueto, J. A., Elizur, A., and Kah, O. (2010). Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 165, 438-455.