Identification and gene expression analysis of three GnRH genes in female Atlantic cod during puberty provides insight into GnRH variant gene loss in fish

General and Comparative Endocrinology

Volumn 172, Issue 3, 2011, Pages 458-467

  Hildahl, Jon ^a   Sandvik, Guro K ^b   Edvardsen, Rolf B ^c   Fagernes, Cathrine ^b   Norberg, Birgitta ^c   Haug, Trude M ^b   Weltzien, Finn Arne ^a,b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Pre pro GnRH; Pseudogene; QPCR; Synteny cloning; Teleost

Indexed keywords

GONADORELIN;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; ATLANTIC COD; BRAIN; CONTROLLED STUDY; DNA LIBRARY; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOSS; GENETIC VARIABILITY; GMGNRH1 GENE; GMGNRH2 GENE; GMGNRH3 GENE; HYPOPHYSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PSEUDOGENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEXUAL DEVELOPMENT; SEXUAL MATURATION; SPAWNING; UNINDEXED SEQUENCE;

EID: 79957800245     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.04.010     Document Type: Article

References (64)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Adelman J.P., Mason A.J., Hayflick J.S., Seeburg P.H. Isolation of the gene and hypothalamic cDNA for the common precursor of gonadotropin-releasing hormone and prolactin release-inhibiting factor in human and rat. Proc. Natl. Acad. Sci. USA 1986, 83:179-183.
3. Alok D., Kumar R.S., Trant J.M., Zohar Y. Recombinant perciform GnRH-R activates different signaling pathways in fish and mammalian heterologous cell lines. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 129:375-380.
4. 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. 2001, 129:551-558.
5. Baertsch R., Diekhans M., Kent W.J., Haussler D., Brosius J. Retrocopy contributions to the evolution of the human genome. BMC Genomics 2008, 9:466.
6. Bogerd J., Diepenbroek W.B., Hund E., van Oosterhout O.F., Teves A.C., Leurs R., Blomenrohr M. Two gonadotropin-releasing hormone receptors in the African catfish: no differences in ligand selectivity, but differences in tissue distribution. Endocrinology 2002, 143:4673-4682.
7. Canosa L.F., Stacey N., Peter R.E. Changes in brain mRNA levels of gonadotropin-releasing hormone, pituitary adenylate cyclase activating polypeptide, and somatostatin during ovulatory luteinizing hormone and growth hormone surges in goldfish. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R1815-R1821.
8. 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 2000, 141:505-512.
9. Chang J.P., Johnson J.D., Sawisky G.R., Grey C.L., Mitchell G., Booth M., Volk M.M., Parks S.K., Thompson E., Goss G.G., Klausen C., Habibi H.R. Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. Gen. Comp. Endocrinol. 2009, 161:42-52.
10. Counis R., Laverriere J.N., Garrel G., Bleux C., Cohen-Tannoudji J., Lerrant Y., Kottler M.L., Magre S. Gonadotropin-releasing hormone and the control of gonadotrope function. Reprod. Nutr. Dev. 2005, 45:243-254.
11. D'Errico I., Gadaleta G., Saccone C. Pseudogenes in metazoa: origin and features. Brief. Funct. Genomic. Proteomic. 2004, 3:157-167.
12. Davie A., Porter M.J.R., Bromage N.R., Migaud H. The role of seasonally altering photoperiod in regulating physiology in Atlantic cod (Gadus morhua). Part I. Sexual maturation. Can. J. Fish Aquat. Sci. 2007, 64:84-97.
13. Drummond A., Strimmer K. PAL: an object-oriented programming library for molecular evolution and phylogenetics. Bioinformatics 2001, 17:662-663.
14. Fernald R.D., White R.B. Gonadotropin-releasing hormone genes: phylogeny, structure, and functions. Front. Neuroendocrinol. 1999, 20:224-240.
15. Flanagan C.A., Chen C.C., Coetsee M., Mamputha S., Whitlock K.E., Bredenkamp N., Grosenick L., Fernald R.D., Illing N. Expression, structure, function, and evolution of gonadotropin-releasing hormone (GnRH) receptors GnRH-R1SHS and GnRH-R2PEY in the teleost, Astatotilapia burtoni. Endocrinology 2007, 148:5060-5071.
16. Garber A.F., Fordham S.E., Symonds J.E., Trippel E.A., Berlinsky D.L. Hormonal induction of ovulation and spermiation in Atlantic cod (Gadus morhua). Aquaculture 2009, 296:179-183.
17. 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 sea bass (Dicentrarchus labrax). J. Comp. Neurol. 2001, 429:144-155.
18. 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. 2002, 446:95-113.
19. Guilgur L.G., Strussmann C.A., Somoza G.M. mRNA expression of GnRH variants and receptors in the brain, pituitary and ovaries of pejerrey (Odontesthes bonariensis) in relation to the reproductive status. Fish Physiol. Biochem. 2009, 35:157-166.
20. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
21. Hansen T., Karlsen O., Taranger G.L., Hemre G.I., Holm J.C., Kjesbu O.S. Growth, gonadal development and spawning time of Atlantic cod (Gadus morhua) reared under different photoperiods. Aquaculture 2001, 203:51-67.
22. Holland M.C., Hassin S., Zohar Y. Seasonal fluctuations in pituitary levels of the three forms of gonadotropin-releasing hormone in striped bass, Morone saxatilis (Teleostei), during juvenile and pubertal development. J. Endocrinol. 2001, 169:527-538.
23. 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 1999, 96:2526-2531.
24. Johansen S.D., Coucheron D.H., Andreassen M., Karlsen B.O., Furmanek T., Jorgensen T.E., Emblem A., Breines R., Nordeide J.T., Moum T., Nederbragt A.J., Stenseth N.C., Jakobsen K.S. Large-scale sequence analyses of Atlantic cod. Nat. Biotechnol. 2009, 25:263-271.
25. Kah O., Lethimonier C., Somoza G., Guilgur L.G., Vaillant C., Lareyre J.J. GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen. Comp. Endocrinol. 2007, 153:346-364.
26. Kakizawa S., Kaneko T., Hirano T. Effects of hypothalamic factors on somatolactin secretion from the organ-cultured pituitary of rainbow trout. Gen. Comp Endocrinol. 1997, 105:71-78.
27. 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.
28. Kawai T., Oka Y., Eisthen H. The role of the terminal nerve and GnRH in olfactory system neuromodulation. Zool. Sci. 2009, 26:669-680.
29. Klausen C., Chang J.P., Habibi H.R. Time- and dose-related effects of gonadotropin-releasing hormone on growth hormone and gonadotropin subunit gene expression in the goldfish pituitary. Can. J. Physiol. Pharmacol. 2002, 80:915-924.
30. Kuo M.W., Lou S.W., Postlethwait J., Chung B.C. Chromosomal organization, evolutionary relationship, and expression of zebrafish GnRH family members. J. Biomed. Sci. 2005, 12:629-639.
31. Lethimonier C., Madigou T., Munoz-Cueto J.A., Lareyre J.J., Kah O. Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen. Comp. Endocrinol. 2004, 135:1-16.
32. Li C., Lu G., Orti G. Optimal data partitioning and a test case for ray-finned fishes (Actinopterygii) based on ten nuclear loci. Syst. Biol. 2008, 57:519-539.
33. Marchant T.A., Chang J.P., Nahorniak C.S., Peter R.E. Evidence that gonadotropin-releasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 1989, 124:2509-2518.
34. Matsuda K., Nakamura K., Shimakura S., Miura T., Kageyama H., Uchiyama M., Shioda S., Ando H. Inhibitory effect of chicken gonadotropin-releasing hormone II on food intake in the goldfish, Carassius auratus. Horm. Behav. 2008, 54:83-89.
35. Mittelholzer C., Andersson E., Taranger G.L., Consten D., Hirai T., Senthilkumaran B., Nagahama Y., Norberg B. Molecular characterization and quantification of the gonadotropin receptors FSH-R and LH-R from Atlantic cod (Gadus morhua). Gen. Comp. Endocrinol. 2009, 160:47-58.
36. Mittelholzer C., Andersson E., Taranger G.L., Karlsen O., Norberg B. Quantification of gonadotropin subunits GPalpha, FSHbeta, and LHbeta mRNA expression from Atlantic cod (Gadus morhua) throughout a reproductive cycle. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2009, 153:288-295.
37. 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. 1982, 107:820-827.
38. Morgan K., Millar R.P. Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species. Gen. Comp. Endocrinol. 2004, 139:191-197.
39. Morgan K., Sellar R., Pawson A.J., Lu Z.L., Millar R.P. Bovine and ovine gonadotropin-releasing hormone (GnRH)-II ligand precursors and type II GnRH receptor genes are functionally inactivated. Endocrinology 2006, 147:5041-5051.
40. Nelson J.S. Fishes of the World 1994, Wiley, New York. third ed.
41. 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.
42. Ogawa S., Akiyama G., Kato S., Soga T., Sakuma Y., Parhar I.S. Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids. Neurosci. Lett. 2006, 403:201-205.
43. Okubo K., Nagahama Y. Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol. (Oxf.) 2008, 193:3-15.
44. 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 2001, 142:4729-4739.
45. 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 2001, 142:1737-1743.
46. Seeburg P.H., Adelman J.P. Characterization of cDNA for precursor of human luteinizing hormone releasing hormone. Nature 1984, 311:666-668.
47. Seeburg P.H., Mason A.J., Stewart T.A., Nikolics K. The mammalian GnRH gene and its pivotal role in reproduction. Recent Prog. Horm. Res. 1987, 43:69-98.
48. Servili A., Lethimonier C., Lareyre J.J., Lopez-Olmeda J.F., Sanchez-Vazquez F.J., Kah O., Munoz-Cueto J.A. The highly conserved gonadotropin-releasing hormone-2 form acts as a melatonin-releasing factor in the pineal of a teleost fish, the European sea bass Dicentrarchus labrax. Endocrinology 2010, 151:2265-2275.
49. Shahjahan M., Hamabata T., Motohashi E., Doi H., Ando H. Differential expression of three types of gonadotropin-releasing hormone genes during the spawning season in grass puffer, Takifugu niphobles. Gen. Comp. Endocrinol. 2010, 167:153-163.
50. Sherwood N., Eiden L., Brownstein M., Spiess J., Rivier J., Vale W. Characterization of a teleost gonadotropin-releasing hormone. Proc. Natl. Acad. Sci. USA 1983, 80:2794-2798.
51. Stewart A.J., Katz A.A., Millar R.P., Morgan K. Retention and silencing of prepro-GnRH-II and type II GnRH receptor genes in mammals. Neuroendocrinology 2009, 90:416-432.
52. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., Hodges E., Anger M., Sachidanandam R., Schultz R.M., Hannon G.J. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.
53. Taranger G.L., Aardal L., Hansen T., Kjesbu O.S. Continuous light delays sexual maturation and increases growth of Atlantic cod (Gadus morhua L.) in sea cages. ICES J. Mar. Sci. 2006, 63:365-375.
54. Taranger G.L., Carrillo M., Schulz R.W., Fontaine P., Zanuy S., Felip A., Weltzien F.A., Dufour S., Karlsen O., Norberg B., Andersson E., Hansen T. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 2010, 165:483-515.
55. Temple J.L., Millar R.P., Rissman E.F. An evolutionarily conserved form of gonadotropin-releasing hormone coordinates energy and reproductive behavior. Endocrinology 2003, 144:13-19.
56. Volkoff H., Peter R.E. Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen. Comp. Endocrinol. 1999, 116:347-355.
57. Volkoff H., Xu M.Y., MacDonald E., Hoskins L. Aspects of the hormonal regulation of appetite in fish with emphasis on goldfish, Atlantic cod and winter flounder: notes on actions and responses to nutritional, environmental and reproductive changes. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 153:8-12.
58. Weber G.M., Powell J.F., Park M., Fischer W.H., Craig A.G., Rivier J.E., Nanakorn U., Parhar I.S., Ngamvongchon S., Grau E.G., Sherwood N.M. Evidence that gonadotropin-releasing hormone (GnRH) functions as a prolactin-releasing factor in a teleost fish (Oreochromis mossambicus) and primary structures for three native GnRH molecules. J. Endocrinol. 1997, 155:121-132.
59. Weltzien F.A., Andersson E., Andersen O., Shalchian-Tabrizi K., Norberg B. The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2004, 137:447-477.
60. Weltzien F.A., Pasqualini C., Vernier P., Dufour S. A quantitative real-time RT-PCR assay for European eel tyrosine hydroxylase. Gen. Comp. Endocrinol. 2005, 142:134-142.
61. 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 1998, 95:305-309.
62. Yamamoto N., Oka Y., Kawashima S. Lesions of gonadotropin-releasing hormone-immunoreactive terminal nerve cells: effects on the reproductive behavior of male dwarf gouramis. Neuroendocrinology 1997, 65:403-412.
63. Zohar Y., Elizur A., Sherwood N.M., Powell J.F., Rivier J.E., Zmora N. Gonadotropin-releasing activities of the three native forms of gonadotropin-releasing hormone present in the brain of gilthead seabream, Sparus aurata. Gen. Comp. Endocrinol. 1995, 97:289-299.
64. Y. Zohar, J.A. Munoz-Cueto, A. Elizur, O. Kah, Neuroendocrinology of reproduction in teleost fish, Gen. Comp. Endocrinol., 2009.