Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish

General and Comparative Endocrinology

Volumn 135, Issue 1, 2004, Pages 1-16

  Lethimonier, Christèle ^a   Madigou, Thierry ^a   Muñoz Cueto, José Antonio ^b   Lareyre, Jean Jacques ^c   Kah, Olivier ^a  

^a CNRS   (France)

^b UNIVERSITY OF CÁDIZ   (Spain)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Genome analysis; GnRH; GnRH receptors; Hypothalamus; Pituitary; Reproduction; Teleost

Indexed keywords

GONADORELIN; GONADORELIN RECEPTOR; LIGAND; RECEPTOR SUBTYPE;

AMINO ACID SEQUENCE; BRAIN; COMPARATIVE STUDY; GENETIC CODE; GENETIC ORGANIZATION; GENOME ANALYSIS; HORMONE ACTION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SHORT SURVEY; SPECIES COMPARISON; TELEOST; TISSUE DISTRIBUTION; VERTEBRATE;

EID: 0344393413     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2003.10.007     Document Type: Short Survey

References (83)

1. Adams B.A., Vickers E.D., Warby C., Park M., Fischer W.H., Grey Craig A., Rivier J.E., Sherwood N.M. Three forms of gonadotropin-releasing hormone, including a novel form, in a basal salmonid, Coregonus clupeaformis. Biol. Reprod. 67:2002;232-239.
2. Adams B.A., Tello J.A., Erchegyi J., Warby C., Hong D.J., Akinsanya K.O., Mackie G.O., Vale W., Rivier J.E., Sherwood N.M. Six novel gonadotropin- releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology. 144:2003;1907-1919.
3. Alok D., Hassin S., Sampath K.R., Trant J.M., Yu K., Zohar Y. Characterization of a pituitary GnRH-receptor from a perciform fish, Morone saxatilis: functional expression in a fish cell line. Mol. Cell. Endocrinol. 168:2000;65-75.
4. Amano M., Oka Y., Aida K., Okumoto N., Kawashima S., Hasegawa Y. Immunocytochemical demonstration of salmon GnRH and chicken GnRH-II in the brain of masu salmon, Oncorhynchus masou. J. Comp. Neurol. 314:1991;587-597.
5. Amano M., Oka Y., Yamanome T., Okuzawa K., Yamamori K. Three GnRH systems in the brain and pituitary of a pleuronectiform fish, the barfin flounder Verasper moseri. Cell Tissue Res. 309:2002;323-329.
6. Anctil M. Evidence for gonadotropin-releasing hormone-like peptides in a cnidarian nervous system. Gen. Comp. Endocrinol. 119:2000;317-328.
7. Andersson E., Fjelldal P.G., Klenke U., Vikingstad E., Taranger G.L., Zohar Y., Stefansson S.O. Three forms of GnRH in the brain and pituitary of the turbot, Scophthalmus maximus: immunological characterization and seasonal variation. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 129:2001;551-558.
8. Aparicio S., Chapman J., Stupka E., Putnam N., Chia J.M., Dehal P., Christoffels A., Rash S., Hoon S., Smit A., Gelpke M.D., Roach J., Oh T., Ho I.Y., Wong M., Detter C., Verhoef F., Predki P., Tay A., Lucas S., Richardson P., Smith S.F., Clark M.S., Edwards Y.J., Doggett N., Zharkikh A., Tavtigian S.V., Pruss D., Barnstead M., Evans C., Baden H., Powell J., Glusman G., Rowen L., Hood L., Tan Y.H., Elgar G., Hawkins T., Venkatesh B., Rokhsar D., Brenner S. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science. 297:2002;1301-1310.
9. Bailey G.S., Poulter R.T., Stockwell P.A. Gene duplication in tetraploid fish: model for gene silencing at unlinked duplicated loci. Proc. Natl. Acad. Sci. USA. 75:1978;5575-5579.
10. Blomenröhr M., Bogerd J., Leurs R., Goos H. Differences in structure-function relations between nonmammalian and mammalian GnRH receptors: what we have learnt from the African catfish GnRH receptor. Endocrinology. 141:2002;87-93.
11. Bogerd J., Li K.W., Janssen-Dommerholt C., Goos H. Two gonadotropin-releasing hormones from African catfish (Clarias gariepinus). Biochem. Biophys. Res. Commun. 187:1992;127-134.
12. Bogerd J., Diepenbroek W.B., Hund E., van O.F., Teves A.C., Leurs R., Blomenröhr M. Two gonadotropin-releasing hormone receptors in the African catfish: no differences in ligand selectivity, but differences in tissue distribution. Endocrinology. 143:2002;4673-4682.
13. Breton B., Jalabert B., Billard R., Weil C. In vitro stimulation of the release of pituitary gonadotropic hormone by a hypothalamic factor in the carp Cyprinus carpio LCR. Acad. Sci. D. 273:1971;2591-2594.
14. Carolsfeld J., Powell J.F., Park M., Fischer W.H., Craig A.G., Chang J.P., Rivier J.E., Sherwood N.M. Primary structure and function of three gonadotropin-releasing hormones, including a novel form, from an ancient teleost, herring. Endocrinology. 141:2000;505-512.
15. Chow M.M., Kight K.E., Gothilf Y., Alok D., Stubblefield J., Zohar Y. Multiple GnRHs present in a teleost species are encoded by separate genes: analysis of the sbGnRH and cGnRH-II genes from the striped bass, Morone saxatilis. J. Mol. Endocrinol. 21:1998;277-289.
16. Dubois E.A., Zandbergen M.A., Peute J., Bogerd J., Goos H.J. Development of three distinct GnRH neuron populations expressing two different GnRH forms in the brain of the African catfish (Clarias gariepinus). J. Comp. Neurol. 437:2001;308-320.
17. Dubois E.A., Zandbergen M.A., Peute J., Goos H.J. Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates. Brain Res. Bull. 57:2002;413-418.
18. Fredriksson R., Lagerström M.C., Lundin L.-G., Schiöth H.B. The G-protein coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon, groups, and fingerprints. Mol. Pharmacol. 63:2003;1256-1272.
19. Gonzalez-Martinez D., Madigou T., Zmora N., Anglade I., Zanuy S., Zohar Y., Elizur A., Munoz-Cueto J.A., Kah O. Differential expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the european bass (Dicentrarchus labrax). J. Comp. Neurol. 429:2001;144-155.
20. Gonzalez-Martinez D., Zmora N., Mananos E., Saligaut D., Zanuy S., Zohar Y., Elizur A., Kah O., Munoz-Cueto J.A. 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.
21. Gonzalez-Martinez D., Zmora N., Zanuy S., Sarasquete C., Elizur A., Kah O., Munoz-Cueto J.A. Developmental expression of three different prepro-GnRH (gonadotrophin-releasing hormone) messengers in the brain of the European sea bass (Dicentrarchus labrax). J. Chem. Neuroanat. 23:2002;255-267.
22. Gonzalez-Martinez, D., Madigou, T., Mananos, E., Zanuy, S., Kah, O., Munoz-Cueto, J.A., 2002c. GnRH receptor mRNA expression in the brain and pituitary of the sea bass (Dicentrarchus labrax). Proceedings of the 21st conference of European and Comparative Endocrinologists, Bonn (Germany), pp. 39-45.
23. Gothilf Y., Munoz-Cueto J.A., Sagrillo C.A., Selmanoff M., Chen T.T., Kah O., Elizur A., Zohar Y. Three forms of gonadotropin-releasing hormone in a perciform fish (Sparus aurata): complementary deoxyribonucleic acid characterization and brain localization. Biol. Reprod. 55:1996;636-645.
24. Habibi H.R., Peter R.E., Sokolowska M., Rivier J.E., Vale W.W. Characterization of gonadotropin-releasing hormone (GnRH) binding to pituitary receptors in goldfish (Carassius auratus). Biol. Reprod. 36:1987;844-853.
25. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp. 41:2002;95-98.
26. Illing N., Troskie B.E., Nahorniak C.S., Hapgood J.P., Peter R.E., Millar R.P. 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. USA. 96:1999;2526-2531.
27. Iwakoshi E., Takuwa-Kuroda K., Fujisawa Y., Hisada M., Ukena K., Tsutsui K., Minakata H. Isolation and characterization of a GnRH-like peptide from Octopus vulgaris. Biochem. Biophys. Res. Commun. 291:2002;1187-1193.
28. Jimenez-Linan M., Rubin B.S., King J.C. Examination of guinea pig luteinizing hormone-releasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain. Endocrinology. 138:1997;4123-4130.
29. Kah O., Breton B., Dulka J.G., Nunez-Rodriguez J., Peter R.E., Corrigan A., Rivier J.E., Vale W.W. A reinvestigation of the Gn-RH (gonadotrophin- releasing hormone) systems in the goldfish brain using antibodies to salmon Gn-RH. Cell Tissue Res. 244:1986;327-337.
30. Kim M.H., Oka Y., Amano M., Kobayashi M., Okuzawa K., Hasegawa Y., Kawashima S., Suzuki Y., Aida K. Immunocytochemical localization of sGnRH and cGnRH-II in the brain of goldfish, Carassius auratus. J. Comp. Neurol. 356:1995;72-82.
31. King J.A., Dufour S., Fontaine Y.A., Millar R.P. Chromatographic and immunological evidence for mammalian GnRH and chicken GnRH II in eel (Anguilla anguilla) brain and pituitary. Peptides. 11:1990;507-514.
32. Klausen C., Chang J.P., Habibi H.R. Multiplicity of gonadotropin- releasing hormone signaling: a comparative perspective. Prog. Brain Res. 141:2002;111-128.
33. Lepretre E., Anglade I., Williot P., Vandesande F., Tramu G., Kah O. Comparative distribution of mammalian GnRH (gonadotrophin-releasing hormone) and chicken GnRH-II in the brain of the immature Siberian sturgeon (Acipenser baeri). J. Comp. Neurol. 337:1993;568-583.
34. Li W.H. Rate of gene silencing at duplicate loci: a theoretical study and interpretation of data from tetraploid fishes. Genetics. 95:1980;237-258.
35. Lin X.W., Peter R.E. Cloning and expression pattern of a second [His5Trp7Tyr8]gonadotropin-releasing hormone (chicken GnRH-H-II) mRNA in goldfish: evidence for two distinct genes. Gen. Comp. Endocrinol. 107:1997;262-272.
36. Lin X., Janovick J.A., Brothers S., Blomenrohr M., Bogerd J., Conn P.M. Addition of catfish gonadotropin-releasing hormone (GnRH) receptor intracellular carboxyl-terminal tail to rat GnRH receptor alters receptor expression and regulation. Mol. Endocrinol. 12:1998;161-171.
37. Lovejoy D.A., Fischer W.H., Ngamvongchon S., Craig A.G., Nahorniak C.S., Peter R.E., Rivier J.E., Sherwood N.M. Distinct sequence of gonadotropin- releasing hormone (GnRH) in dogfish brain provides insight into GnRH evolution. Proc. Natl. Acad. Sci. USA. 89:1992;6373-6377.
38. Lynch M., Conery J.S. The evolutionary fate and consequences of duplicate genes. Science. 290:2000;1151-1155.
39. Madigou T., Mananos-Sanchez E., Hulshof S., Anglade I., Zanuy S., Kah O. Cloning, tissue distribution, and central expression of the gonadotropin- releasing hormone receptor in the rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 63:2000;1857-1866.
40. Madigou T., Uzbekova S., Lareyre J.J., Kah O. Two messenger RNA isoforms of the gonadotrophin-releasing hormone receptor, generated by alternative splicing and/or promoter usage, are differentially expressed in rainbow trout gonads during gametogenesis. Mol. Reprod. Dev. 63:2002;151-160.
41. Matsuo H., Baba Y., Nair R.M., Arimura A., Schally A.V. Structure of the porcine LH- and FSH-releasing hormone I. The proposed amino acid sequence. Biochem. Biophys. Res. Commun. 43:1971;1334-1339.
42. Millar R.P. GnRH II and type II GnRH receptors. Trends Endocrinol. Metab. 14:2002;35-43.
43. Miyamoto K., Hasegawa Y., Minegishi T., Nomura M., Takahashi Y., Igarashi M., Kangawa K., Matsuo H. Isolation and characterization of chicken hypothalamic luteinizing hormone-releasing hormone. Biochem. Biophys. Res. Commun. 107:1982;820-827.
44. Miyamoto K., Hasegawa Y., Nomura M., Igarashi M., Kangawa K., Matsuo H. 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. 81:1984;3874-3878.
45. Montaner A.D., Park M.K., Fischer W.H., Craig A.G., Chang J.P., Somoza G.M., Rivier J.E., Sherwood N.M. Primary structure of a novel gonadotropin-releasing hormone in the brain of a teleost, Pejerrey. Endocrinology. 142:2001;1453-1460.
46. Montero M., Vidal B., King J.A., Tramu G., Vandesande F., Dufour S., Kah O. Immunocytochemical localization of mammalian GnRH (gonadotropin-releasing hormone) and chicken GnRH-II in the brain of the European silver eel (Anguilla anguilla L.). J. Chem. Neuroanat. 7:1994;227-241.
47. Neill J.D. GnRH and GnRH receptor genes in the human genome. Endocrinology. 143:2002;737-743.
48. Ngamvongchon S., Sherwood N.M., Warby C.M., Rivier J.E. Gonadotropin-releasing hormone from thai catfish: chromatographic and physiological studies. Gen. Comp. Endocrinol. 87:1992;266-274.
49. Ohno S. Evolution by Gene Duplication. 1970;Springer-Verlag, Heidelberg, Germany.
50. Oka Y. Physiology and release activity of GnRH neurons. Prog. Brain Res. 141:2002;259-281.
51. Oka Y., Matsushima T. Gonadotropin-releasing hormone (GnRH)- immunoreactive terminal nerve cells have intrinsic rhythmicity and project widely in the brain. J. Neurosci. 13:1993;2161-2176.
52. Okubo K., Amano M., Yoshiura Y., Suetake H., Aida K. A novel form of gonadotropin-releasing hormone in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 276:2000;298-303.
53. Okubo K., Suetake H., Usami T., Aida K. Molecular cloning and tissue-specific expression of a gonadotropin-releasing hormone receptor in the Japanese eel. Gen. Comp. Endocrinol. 119:2000;181-192.
54. Okubo K., Aida K. Gonadotropin-releasing hormones (GnRHs) in a primitive teleost, the arowana: phylogenetic evidence that three paralogous lineages of GnRH occurred prior to the emergence of teleosts. Gen. Comp. Endocrinol. 124:2001;125-133.
55. Okubo K., Nagata S., Ko R., Kataoka H., Yoshiura Y., Mitani H., Kondo M., Naruse K., Shima A., Aida K. Identification and characterization of two distinct GnRH receptor subtypes in a teleost, the medaka Oryzias latipes. Endocrinology. 142:2001;4729-4739.
56. Okubo K., Mitani H., Naruse K., Kondo M., Shima A., Tanaka M., Asakawa S., Shimizu N., Yoshiura Y., Aida K. Structural characterization of GnRH loci in the medaka genome. Gene. 293:2002;181-189.
57. Okuzawa K., Amano M., Kobayashi M., Aida K., Hanyu I., Hasegawa Y., Miyamoto K. Differences in salmon GnRH and chicken GnRH-II contents in discrete brain areas of male and female rainbow trout according to age and stage of maturity. Gen. Comp. Endocrinol. 80:1990;116-126.
58. O'neill D.F., Powell J.F., Standen E.M., Youson J.H., Warby C.M., Sherwood N.M. Gonadotropin-releasing hormone (GnRH) in ancient teleosts, the bonytongue fishes: putative origin of salmon GnRH. Gen. Comp. Endocrinol. 112:1998;415-425.
59. Parhar I.S. Cell migration and evolutionary significance of GnRH subtypes. Prog. Brain Res. 141:2002;3-17.
60. Parhar I.S., Soga T., Sakuma Y., Millar R.P. Spatio-temporal expression of gonadotropin-releasing hormone receptor subtypes in gonadotropes, somatotropes and lactotropes in the cichlid fish. J. Neuroendocrinol. 14:2002;657-665.
61. Pati D., Habibi H.R. Involvement of protein kinase C and arachidonic acid pathways in the gonadotropin-releasing hormone regulation of oocyte meiosis and follicular steroidogenesis in the goldfish ovary. Biol. Reprod. 66:2002;813-822.
62. Peter R.E., Prasada Rao P.D., Baby S.M., Illing N., Millar R.P. Differential brain distribution of gonadotropin-releasing hormone receptors in the goldfish. Gen. Comp. Endocrinol. 132:2003;399-408.
63. Powell J.F., Zohar Y., Elizur A., Park M., Fischer W.H., Craig A.G., Rivier J.E., Lovejoy D.A., Sherwood N.M. Three forms of gonadotropin-releasing hormone characterized from brains of one species. Proc. Natl. Acad. Sci. USA. 91:1994;12081-12085.
64. Powell J.F., Krueckl S.L., Collins P.M., Sherwood N.M. Molecular forms of GnRH in three model fishes: rockfish, medaka and zebrafish. J. Endocrinol. 150:1996;17-23.
65. Powell J.F., Standen E.M., Carolsfeld J., Borella M.I., Gazola R., Fischer W.H., Park M., Craig A.G., Warby C.M., Rivier J.E., Val-Sella M.V., Sherwood N.M. Primary structure of three forms of gonadotropin-releasing hormone (GnRH) from the pacu brain. Regul. Pept. 68:1997;189-195.
66. Robinson-Rechavi M., Laudet V. Evolutionary rates of duplicate genes in fish and mammals. Mol. Biol. Evol. 18:2001;681-683.
67. Robison R.R., White R.B., Illing N., Troskie B.E., Morley M., Millar R.P., Fernald R.D. gonadotropin-releasing hormone receptor in the teleost Haplochromis burtoni: structure, location, and function. Endocrinology. 142:2001;1737-1743.
68. Senthilkumaran B., Okuzawa K., Gen K., Ookura T., Kagawa H. Distribution and seasonal variations in levels of three native GnRHs in the brain and pituitary of perciform fish. J. Neuroendocrinol. 11:1999;181-186.
69. Sherwood N., Eiden L., Brownstein M., Spiess J., Rivier J., Vale W. Characterization of a teleost gonadotropin-releasing hormone. Proc. Natl. Acad. Sci. USA. 80:1983;2794-2798.
70. Sherwood N.M., Doroshov S., Lance V. Gonadotropin-releasing hormone (GnRH) in bony fish that are phylogenetically ancient: reedfish (Calamoichthys calabaricus), sturgeon (Acipenser transmontanus), and alligator gar (Lepisosteus spatula). Gen. Comp. Endocrinol. 84:1991;44-57.
71. Somoza G.M., Lescheid D.W., Miranda L.A., Lo Nostro F.L., Magliulo-Cepriano L., Montaner A.D., Schreibman M.P., Rivier J.E., Sherwood N.M. Expression of pejerrey gonadotropin-releasing hormone in three orders of fish. Biol. Reprod. 67:2002;1864-1871.
72. Sower S.A., Chiang Y.C., Lovas S., Conlon J.M. Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinology. 132:1993;1125-1131.
73. Taylor J.S., Van de Peer Y., Meyer A. Revisiting recent challenges to the ancient fish-specific genome duplication hypothesis. Curr. Biol. 11:2001;R1005-R1008.
74. Tensen C., Okuzawa K., Blomenrohr M., Rebers F., Leurs R., Bogerd J., Schulz R., Goos H. Distinct efficacies for two endogenous ligands on a single cognate gonadoliberin receptor. Eur. J. Biochem. 243:1997;134-140.
75. Wang L., Bogerd J., Choi H.S., Seong J.Y., Soh J.M., Chun S.Y., Blomenrohr M., Troskie B.E., Millar R.P., Yu W.H., McCann S.M., Kwon H.B. Three distinct types of GnRH receptor characterized in the bullfrog. Proc. Natl. Acad. Sci. USA. 98:2001;361-366.
76. White R.B., Fernald R.D. Ontogeny of gonadotropin-releasing hormone (GnRH) gene expression reveals a distinct origin for GnRH-containing neurons in the midbrain. Gen. Comp. Endocrinol. 112:1998;322-329.
77. White R.B., Eisen J.A., Kasten T.L., Fernald R.D. Second gene for gonadotropin-releasing hormone in humans. Proc. Natl. Acad. Sci. USA. 95:1998;305-309.
78. White S.A., Kasten T.L., Bond C.T., Adelman J.P., Fernald R.D. Three gonadotropin-releasing hormone genes in one organism suggest novel roles for an ancient peptide. Proc. Natl. Acad. Sci. USA. 92:1995;8363-8367.
79. Yoo M.S., Kang H.M., Choi H.S., Kim J.W., Troskie B.E., Millar R.P., Kwon H.B. Molecular cloning, distribution and pharmacological characterization of a novel gonadotropin-releasing hormone ([Trp8] GnRH) in frog brain. Mol. Cell. Endocrinol. 164:2000;197-204.
80. Yu K.L., Sherwood N.M., Peter R.E. Differential distribution of two molecular forms of gonadotropin-releasing hormone in discrete brain areas of goldfish (Carassius auratus). Peptides. 9:1988;625-630.
81. Zandbergen M.A., Kah O., Bogerd J., Peute J., Goos H.J. Expression and distribution of two gonadotropin-releasing hormones in the catfish brain. Neuroendocrinology. 62:1995;571-578.
82. Zmora N., Gonzalez-Martinez D., Munoz-Cueto J.A., Madigou T., Mananos-Sanchez E., Zanuy S., Zohar Y., Kah O., Elizur A. The GnRH system in the European sea bass (Dicentrarchus labrax). J. Endocrinol. 172:2002;105-116.
83. Zohar Y., Mylonas C.C. Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture. 197:2001;99-136.