Review: Evolution of GnIH and related peptides structure and function in the chordates

Frontiers in Neuroscience

Volumn , Issue 8 JUL, 2014, Pages

  Osugi, Tomohiro ^a,b   Ubuka, Takayoshi ^a   Tsutsui, Kazuyoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b SUNTORY INSTITUTE FOR BIOORGANIC RESEARCH   (Japan)

Author keywords

Amphioxus; Chordates; Evolution; Gonadotropin inhibitory hormone (GnIH); Lamprey; Reproduction; RF amide peptides

Indexed keywords

CYCLIC AMP; GONADORELIN; GONADOTROPIN; GONADOTROPIN ANTAGONIST; AMIDE; GONADOTROPIN BETA; GONADOTROPIN INHIBITORY HORMONE; GONADOTROPIN RELEASING HORMONE III; HYPOTHALAMUS HORMONE; MESSENGER RNA; NEUROPEPTIDE; POLYPEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BIRD; BRAIN; BRANCHIOSTOMA; CARBOXY TERMINAL SEQUENCE; CHORDATA; GOLDFISH; HORMONE SYNTHESIS; HYPOTHALAMUS; IN VITRO STUDY; LAMPREY; NONHUMAN; ORYZIAS; PROTEIN FUNCTION; PROTEIN STRUCTURE; QUAIL; REPRODUCTION; REVIEW; GENE EXPRESSION; GENETIC VARIABILITY; GONADOTROPIN RELEASE; HORMONE ACTION; HORMONE STRUCTURE; HUMAN; MOLECULAR EVOLUTION; NERVE FIBER; PETROMYZON; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SPECIES COMPARISON; SPECIES DIVERSITY;

EID: 84905907540     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00255     Document Type: Review

References (75)

1. Amano, M., Moriyama, S., Iigo, M., Kitamura, S., Amiya, N., Yamamori, K., Ukena, K., and Tsutsui, K. (2006). Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon. J. Endocrinol. 188, 417-423.
2. Bédécarrats, G. Y., McFarlane, H., Maddineni, S. R., and Ramachandran, R. (2009). Gonadotropin-inhibitory hormone receptor signaling and its impact on reproduction in chickens. Gen. Comp. Endocrinol. 163, 7-11.
3. Bentley, G. E., Jensen, J. P., Kaur, G. J., Wacker, D. W., Tsutsui, K., and Wingfield, J.C. (2006). Rapid inhibition of female sexual behavior by gonadotropin-inhibitory hormone (GnIH). Horm. Behav. 49, 550-555.
4. Burgus, R., Butcher, M., Amoss, M., Ling, N., Monahan, M., Rivier, J., Fellows, R., Blackwell, R., Vale, W., and Guillemin, R. (1972). Primary structure of the ovine hypothalamic luteinizing hormone-releasing factor (LRF). Proc. Natl. Acad. Sci. USA 69, 278-282.
5. Chartrel, N., Dujardin, C., Leprince, J., Desrues, L., Tonon, M. C., Cellier, E., Cosette, P., Jouenne, T., Simonnet, G., and Vaudry, H. (2002). Isolation, characterization, and distribution of a novel neuropeptide, Rana RFamide (R-RFa), in the brain of the European green frog Rana esculenta. J. Comp. Neurol. 448, 111-127.
6. Chowdhury, V. S., Ubuka, T., Osugi, T., Shimura, T., and Tsutsui, K. (2011). Identification, localization and expression of LPXRFamide peptides, and melatonin-dependent induction of their precursor mRNA in the newt brain. J. Endocrinol. 209, 211-220.
7. Clarke, I. J., Sari, I. P., Qi, Y., Smith, J. T., Parkington, H. C., Ubuka, T., Iqbal, J., Li, Q., Tilbrook, A., Morgan, K., Pawson, A. J., Tsutsui, K., Millar, R. P., and Bentley, G. E. (2008). Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 149, 5811-5821.
8. Dockray, G. J., Reeve Jr., J. R., Shively, J., Gayton, R. J., and Barnard, C. S. (1983). A novel active pentapeptide from chicken brain identified by antibodies to FMRFamide. Nature 305, 328-330.
9. Ducret, E., Anderson, G. M., and Herbison, A. E. (2009). RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology 150, 2799-2804.
10. Felip, A., Zanuy, S., Pineda, R., Pinilla, L., Carrillo, M., Tena-Sempere, M., and Gómez, A. (2009). Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol. Cell. Endocrinol. 312, 61-71.
11. Greenberg, M. J., and Price, D. A. (1992). Relationships among the FMRFamide-like peptides. Prog. Brain Res. 92, 25-37.
12. Fukusumi, S., Habata, Y., Yoshida, H., Iijima, N., Kawamata, Y., Hosoya, M., Fujii, R., Hinuma, S., Kitada, C., Shintani, Y., Suenaga, M., Onda, H., Nishimura, O., Tanaka, M., Ibata, Y., and Fujino, M. (2001). Characteristics and distribution of endogenous RFamide-related peptide-1. Biochim. Biophys. Acta. 1540, 221-232.
13. Hinuma, S., Shintani, Y., Fukusumi, S., Iijima, N., Matsumoto, Y., Hosoya, M., Fujii, R., Watanabe, T., Kikuchi, K., Terao, Y., Yano, T., Yamamoto, T., Kawamata, Y., Habata, Y., Asada, M., Kitada, C., Kurokawa, T., Onda, H., Nishimura, O., Tanaka, M., Ibata, Y., and Fujino, M. (2000). New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat. Cell Biol. 2, 703-708.
14. Ikemoto, T., and Park M. K. (2005). Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. J. Reprod. Dev. 51, 359-377.
15. Johnson, M. A., Tsutsui, K., and Fraley, G. S. (2007). Rat RFamide-related peptide-3 stimulates GH secretion, inhibits LH secretion, and has variable effects on sex behavior in the adult male rat. Horm. Behav. 51, 171-180.
16. Kadokawa, H., Shibata, M., Tanaka, Y., Kojima, T., Matsumoto, K., Oshima, K., and Yamamoto, N. (2009). Bovine C-terminal octapeptide of RFamide-related peptide-3 suppresses luteinizing hormone (LH) secretion from the pituitary as well as pulsatile LH secretion in bovines. Domest. Anim. Endocrinol. 36, 219-224.
17. King, J. A., and Millar, R. P. (1982). Structure of chicken hypothalamic luteinizing hormone-releasing hormone. I. Structural determination on partially purified material. J. Biol. Chem. 257, 10722-10728.
18. Koda, A., Ukena, K., Teranishi, H., Ohta, S., Yamamoto, K., Kikuyama, S., and Tsutsui K. (2002). A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology 143, 411-419.
19. Kriegsfeld, L. J., Mei, D. F., Bentley, G. E., Ubuka, T., Mason, A. O., Inoue, K., Ukena, K., Tsutsui, K., and Silver, R. (2006). Identification and characterization of a gonadotropin-inhibitory system in the brains of mammals. Proc. Natl. Acad. Sci. USA 103, 2410-2415.
20. 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., and Tsutsui K. (2009) Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology, 150:2837-2846.
21. Li, X., Su, J., Fang, R., Zheng, L., Lei, R., Wang, X., Lei, Z., Jin, M., Jiao, Y., Hou, Y., Guo, T., and Ma, Z. (2013). The effects of RFRP-3, the mammalian ortholog of GnIH, on the female pig reproductive axis in vitro. Mol. Cell. Endocrinol. 372, 65-72.
22. Matsuo, H., Baba, Y., Nair, R. M., Arimura, A., and Schally, A. V. (1971). Structure of the porcine LH- and FSH-releasing hormone. I. The proposed amino acid sequence. Biochem. Biophys. Res. Commun. 43, 1334-1339.
23. Miyamoto, K., Hasegawa, Y., Minegishi, T., Nomura, M., Takahashi, Y., Igarashi, M., Kangawa, K., and Matsuo, H. (1982). Isolation and characterization of chicken hypothalamic luteinizing hormone-releasing hormone. Biochem. Biophys. Res. Commun. 107, 820-827.
24. 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. USA 81, 3874-3878.
25. Mount, S. M. (1982). A catalogue of splice junction sequences. Nucleic Acids Res. 10, 459-472.
26. Moussavi, M., Wlasichuk, M., Chang, J. P., and Habibi, H. R. (2012). Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish. Mol. Cell. Endocrinol. 350, 53-60.
27. Moussavi, M., Wlasichuk, M., Chang, J. P., and Habibi, H. R. (2013). Seasonal effect of gonadotrophin inhibitory hormone on gonadotrophin-releasing hormone-induced gonadotroph functions in the goldfish pituitary. J. Neuroendocrinol. 25, 506-516.
28. Murakami, M., Matsuzaki, T., Iwasa, T., Yasui, T., Irahara, M., Osugi, T., and Tsutsui, K. (2008). Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J. Endocrinol. 199, 105-112.
29. Osugi, T., Okamura, T., Son, Y. L., Ohkubo, M., Ubuka, T., Henmi, Y., and Tsutsui K. Evolutionary origin of GnIH and NPFF in chordates: Insights from novel amphioxus RFamide peptides. PLoS ONE, 9: e100962.
30. Osugi, T., Daukss, D., Gazda, K., Ubuka, T., Kosugi, T., Nozaki, M., Sower, S. A., and Tsutsui, K. (2012). Evolutionary origin of the structure and function of gonadotropin-inhibitory hormone: insights from lampreys. Endocrinology 153, 2362-2374.
31. Osugi, T., Uchida, K., Nozaki, M., and Tsutsui, K. (2011). Characterization of novel RFamide peptides in the central nervous system of the brown hagfish: isolation, localization, and functional analysis. Endocrinology 152, 4252-4264.
32. Osugi, T., Ukena, K., Bentley, G. E., O'Brien, S., Moore, I. T., Wingfield, J. C., and Tsutsui, K. (2004). Gonadotropin-inhibitory hormone in Gambel's white-crowned sparrow (Zonotrichia leucophrys gambelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J. Endocrinol. 182, 33-42.
33. Osugi, T., Ukena, K., Sower, S. A., Kawauchi, H., and Tsutsui, K. (2006). Evolutionary origin and divergence of PQRFamide peptides and LPXRFamide peptides in the RFamide peptide family. Insights from novel lamprey RFamide peptides. FEBS J. 273, 1731-1743.
34. Pasquier, J., Lafont, A. G., Tostivint, H., Vaudry, H., Rousseau, K., and Dufour, S. (2012). Comparative evolutionary histories of kisspeptins and kisspeptin receptors in vertebrates reveal both parallel and divergent features. Front. Endocrinol. (Lausanne) 3, 173.
35. Price, D. A., and Greenberg, M. J. (1977). Structure of a molluscan cardioexcitatory neuropeptide. Science 197, 670-671.
36. Qi, X., Zhou, W., Li, S., Lu, D., Yi, S., Xie, R., Liu, X., Zhang, Y., and Lin, H. (2013). Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus. Mol. Cell. Endocrinol. 366, 9-20.
37. Rizwan, M. Z., Poling, M. C., Corr, M., Cornes, P. A., Augustine, R. A., Quennell, J. H., Kauffman, A. S., and Anderson, G. M. (2012). RFamide-related peptide-3 receptor gene expression in GnRH and kisspeptin neurons and GnRH-dependent mechanism of action. Endocrinology 153, 3770-3779.
38. Sari, I. P., Rao, A., Smith, J. T., Tilbrook, A. J., and Clarke, I. J. (2009). Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology150, 5549-5556.
39. Satake, H., Hisada, M., Kawada, T., Minakata, H., Ukena, K., and Tsutsui, K. (2001). Characterization of a cDNA encoding a novel avian hypothalamic neuropeptide exerting an inhibitory effect on gonadotropin release. Biochem. J. 354, 379-385.
40. Sawada, K., Ukena, K., Kikuyama, S., and Tsutsui, K. (2002a). Identification of a cDNA encoding a novel amphibian growth hormone-releasing peptide and localization of its transcript. J. Endocrinol. 174, 395-402.
41. Sawada, K., Ukena, K., Satake, H., Iwakoshi, E., Minakata, H., and Tsutsui, K. (2002b). Novel fish hypothalamic neuropeptide. Eur. J. Biochem. 269, 6000-6008.
42. Shahjahan, M., Ikegami, T., Osugi, T., Ukena, K., Doi, H., Hattori, A., Tsutsui, K., and Ando, H. (2011). Synchronised expressions of LPXRFamide peptide and its receptor genes: seasonal, diurnal and circadian changes during spawning period in grass puffer. J. Neuroendocrinol. 23, 39-51.
43. Sherwood, N. M., Sower, S. A., Marshak, D. R., Fraser, B. A., and Brownstein. M. J. (1986). Primary structure of gonadotropin-releasing hormone in lamprey brain. J. Biol. Chem. 15, 4812-4819.
44. Shimizu, M., and Bédécarrats, G. Y. (2010). Activation of the chicken gonadotropin-inhibitory hormone receptor reduces gonadotropin releasing hormone receptor signaling. Gen. Comp. Endocrinol. 167, 331-337.
45. Smith, J. T., Coolen, L. M., Kriegsfeld, L. J., Sari, I. P., Jaafarzadehshirazi, M. R., Maltby, M., Bateman, K., Goodman, R. L., Tilbrook, A. J., Ubuka, T., Bentley, G. E., Clarke, I. J., and Lehman, M. N. (2008). Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149, 5770-5782.
46. Son, Y. L., Ubuka, T., Millar, R. P., Kanasaki, H., and Tsutsui, K. (2012). Gonadotropin-inhibitory hormone inhibits GnRH-induced gonadotropin subunit gene transcriptions by inhibiting AC/cAMP/PKA-dependent ERK pathway in LßT2 cells. Endocrinology 153, 2332-2343.
47. St. John, J. A., Braun, E. L., Isberg, S. R., Miles, L. G., Chong, A. Y., Gongora, J., Dalzell, P., Moran, C., Bed'hom, B., Abzhanov, A., Burgess, S. C., Cooksey, A. M., Castoe, T. A., Crawford, N. G., Densmore, L. D., Drew, J. C., Edwards, S. V., Faircloth, B. C., Fujita, M. K., Greenwold, M. J., Hoffmann, F. G., Howard, J. M., Iguchi, T., Janes, D. E., Khan, S. Y., Kohno, S., de Koning, A. J., Lance, S. L., McCarthy, F. M., McCormack, J. E., Merchant, M. E., Peterson, D. G., Pollock, D. D., Pourmand, N., Raney, B. J., Roessler, K. A., Sanford, J. R., Sawyer, R. H., Schmidt, C. J., Triplett, E. W., Tuberville, T. D., Venegas-Anaya, M., Howard, J. T., Jarvis, E. D., Guillette, L. J. Jr., Glenn, T.C., Green, R. E., and Ray, D. A. (2012). Sequencing three crocodilian genomes to illuminate the evolution of archosaurs and amniotes. Genome Biol. 13, 415.
48. Thorson, J. F., Prezotto, L. D., Cardoso, R. C., Sharpton, S. M., Edwards, J. F., Welsh, T. H. Jr., Riggs, P. K., Caraty, A., Amstalden, M., Williams, G. L. (2014). Hypothalamic distribution, adenohypophyseal receptor expression, and ligand functionality of RFamide-related peptide 3 in the mare during the breeding and nonbreeding seasons. Biol. Reprod. 90, 28.
49. Tobari, Y., Iijima, N., Tsunekawa, K., Osugi, T., Okanoya, K., Tsutsui, K., and Ozawa, H. (2010). Identification of gonadotropin-inhibitory hormone in the zebra finch (Taeniopygia guttata): Peptide isolation, cDNA cloning and brain distribution. Peptides 31, 816-826.
50. Tsutsui, K., Saigoh, E., Ukena, K., Teranishi, H., Fujisawa, Y., Kikuchi, M., Ishii, S., and Sharp, P. J. (2000). A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem. Biophys. Res. Commun. 275, 661-667.
51. Tsutsui, K., and Ukena, K. (2006). Review: Hypothalamic LPXRF-amide peptides in vertebrates: identification, localization and hypophysiotropic activity. Peptides 27, 1121-1129.
52. Tsutsui, K., Ubuka, T., Yin, H., Osugi, T., Ukena, K., Bentley, G. E., Ciccone, N., Inoue, K., Chowdhury, V. S., Sharp, P. J., and Wingfield, J. C. (2006). Review: Mode of action and functional significance of avian gonadotropin-inhibitory hormone (GnIH). J. Exp. Zool. 305A, 801-806.
53. Tsutsui, K., Bentley, G. E., Ubuka, T., Saigoh, E., Yin, H., Osugi, T., Inoue, K., Chowdhury, V. S., Ukena, K., Ciccone, N., Sharp, P. J., and Wingfield, J. C. (2007). Review: The general and comparative biology of gonadotropin-inhibitory hormone (GnIH). Gen. Comp. Endocrinol. 153, 365-370.
54. Tsutsui, K. (2009). Review: A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): Biosynthesis, mode of action and functional significance. Prog. Neurobiol. 88, 76-88.
55. Tsutsui, K., Bentley, G. E., Bedecarrats, G. T., Osugi, T., Ubuka, T., and Kriegsfeld, L.J. (2010a). Review: Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front. Neuroendocrinol. 31, 284-295.
56. Tsutsui, K., Bentley, G. E., Kriegsfeld, L. J., Osugi, T., Seong, J. Y., and Vaudry, H. (2010b). Review: Discovery and evolutionary history of gonadotrophin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J. Neuroendocrinol. 22, 716-727.
57. Tsutsui, K., and Ubuka, T. (2012). Gonadotropin-inhibitory hormone, in: Kastin, A.J., Vaudry, H. (Eds.), Handbook of biologically active peptides. Academic Press, London, pp. 802-811.
58. Tsutsui, K., Ubuka, T., Bentley, G. E., and Kriegsfeld, L. J. (2012). Review: Gonadotropin-inhibitory hormone (GnIH): discovery, progress and prospect. Gen. Comp. Endocrinol. 177, 305-314.
59. Tsutsui, K., Ubuka, T., Bentley, G. E., and Kriegsfeld, L. J. (2013). Review: Regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front. Neurosci. 7, 60.
60. Ubuka, T., Kim, S., Huang, Y. C., Reid, J., Jiang, J., Osugi, T., Chowdhury, V. S., Tsutsui, K, and Bentley, G. E. (2008). Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology 149, 268-278.
61. Ubuka, T., Haraguchi, S., Tobari, Y., Narihiro, M., Ishikawa, K., Hayashi, T., Harada, N., and Tsutsui, K. (2014). Hypothalamic inhibition of socio-sexual behaviour by increasing neuroestrogen synthesis. Nat. Commun. 5, 3061.
62. Ubuka, T., Inoue, K., Fukuda, Y., Mizuno, T., Ukena, K., Kriegsfeld, L. J., and Tsutsui K. (2012a). Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 153, 373-385.
63. Ubuka, T. Lai, H., Kitani, M., Suzuuchi, A., Pham, V., Cadigan, P. A., Wang, A., Chowdhury, V. S., Tsutsui, K., and Bentley, G. E. (2009a). Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J. Comp. Neurol. 517, 841-855.
64. Ubuka, T., Morgan, K., Pawson, A. J., Osugi, T., Chowdhury, V. S., Minakata, H., Tsutsui, K., Millar, R. P., and Bentley, G. E. (2009b). Identification of human GnIH homologs, RFRP-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS ONE 4, e8400.
65. Ubuka, T., Mukai, M., Wolfe, J., Beverly, R., Clegg, S., Wang, A., Hsia, S., Li, M., Krause, J. S., Mizuno, T., Fukuda, Y., Tsutsui, K., Bentley, G. E., and Wingfield, J. C. (2012b). RNA interference of gonadotropin-inhibitory hormone gene induces arousal in songbirds. PLoS One 7, e30202.
66. Ubuka, T., Son, Y. L., Bentley, G. E., Millar, R. P., and Tsutsui, K. (2013a). Review: Gonadotropin-inhibitory hormone (GnIH), GnIH receptor and cell signaling. Gen. Comp. Endocrinol. 190, 10-17.
67. Ubuka, T., Mizuno, T., Fukuda, Y., Bentley, G. E., Wingfield, J. C., and Tsutsui, K. (2013b). RNA interference of gonadotropin-inhibitory hormone gene induces aggressive and sexual behaviors in birds. Gen. Comp. Endocrinol. 181, 179-186.
68. Ubuka, T., Ukena, K., Sharp, P. J., Bentley, G. E., and Tsutsui, K. (2006). Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 147, 1187-1194.
69. Ukena, K., Iwakoshi, E., Minakata, H., and Tsutsui, K. (2002). A novel rat hypothalamic RFamide-related peptide identified by immunoaffinity chromatography and mass spectrometry. FEBS Lett. 512, 255-258.
70. Ukena, K., Koda, A., Yamamoto, K., Kobayashi, T., Iwakoshi-Ukena, E., Minakata, H., Kikuyama, S., and Tsutsui, K. (2003). Novel neuropeptides related to frog growth hormone-releasing peptide: isolation, sequence, and functional analysis. Endocrinology 144, 3879-3884.
71. Ukena. K., and Tsutsui, K. (2005). A new member of the hypothalamic RF-amide peptide family, LPXRF-amide peptides: structure, localization, and function. Mass Spectrom. Rev. 24, 469-486.
72. Venkatesh, B., Kirkness, E. F., Loh, Y. H., Halpern, A. L., Lee, A. P., Johnson, J., Dandona, N., Viswanathan, L. D., Tay, A., Venter, J. C., Strausberg, R. L., and Brenner, S. (2007). Survey sequencing and comparative analysis of the elephant shark (Callorhinchus milii) genome. PLoS Biol. 5, e101.
73. Yin, H., Ukena, K., Ubuka, T., and Tsutsui, K. (2005). A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. J. Endocrinol. 184, 257-266.
74. Yoshida, H., Habata, Y., Hosoya, M., Kawamata, Y., Kitada, C., and Hinuma, S. (2003). Molecular properties of endogenous RFamide-related peptide-3 and its interaction with receptors. Biochim. Biophys. Acta. 1593, 151-157.
75. Zhang, Y., Li, S., Liu, Y., Lu, D., Chen, H., Huang, X., Liu, X., Meng, Z., Lin, H., and Cheng, C. H. (2010). Structural diversity of the GnIH/GnIH receptor system in teleost: its involvement in early development and the negative control of LH release. Peptides 31, 1034-1043.