Regulation of salmon gonadotrophin-releasing hormone gene expression by sex steroids in rainbow trout brain

Journal of Neuroendocrinology

Volumn 18, Issue 6, 2006, Pages 445-453

  Vetillard, A ^a   Ferriere, F ^b   Jego, P ^b   Bailhache, T ^b  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

mRNA; Rainbow trout; Sex steroids; sGnRH; Teleost

Indexed keywords

ANDROSTANOLONE; ESTRADIOL; GONADORELIN; MESSENGER RNA; SEX HORMONE; TESTOSTERONE;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; FEEDBACK SYSTEM; FEMALE; FOREBRAIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HORMONE ACTION; HORMONE DETERMINATION; HYPOPHYSIS GONAD SYSTEM; IMMATURITY; IN SITU HYBRIDIZATION; IN VIVO STUDY; NONHUMAN; OOCYTE MATURATION; OVARIECTOMY; OVARY CYCLE; OVULATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAINBOW TROUT; SALMON; TELEOST; TRIPLOIDY; VITELLOGENESIS;

ANIMALS; DIHYDROTESTOSTERONE; ESTROGENS; FEEDBACK, BIOCHEMICAL; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADAL STEROID HORMONES; GONADOTROPIN-RELEASING HORMONE; NEURONS; ONCORHYNCHUS MYKISS; OVARIECTOMY; PROSENCEPHALON; REPRODUCTION; TESTOSTERONE;

EID: 33646349727     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2006.01432.x     Document Type: Article

References (57)

1. Breton B, Weil C, Jalabert B, Billard R. Reciprocal activity of hypothalamic factors of rams (Ovis aries) and of teleostean fishes on the secretion in vitro of gonadotropic hormones c-HG and LH, respectively, by carp and ram hypophyses. C R Acad Sci Paris D 1972; 274: 2530-2533.
2. Yu KL, Kobayashi M, Peter RE. Effects of ovariectomy and steroid replacement on gonadotropin-releasing hormone immunoreactivities in discrete brain areas of goldfish. Second International Symposium on Fish Endocrinology, Saint Malo. Amsterdam: Kugler Publications BV, 1992: 25.
3. Dufour S, Fontaine YA, Kerdelhue B. Increase in brain and pituitary radioimmunoassayable gonadotropin releasing hormone (GnRH) in the European silver eel treated with sexual steroid or human chorionic gonadotropin. Neuropeptides 1985; 6: 495-502.
4. Goos HJ, de Leeuw R, Cook H, van Oordt PG. Gonadotropic hormone-releasing hormone (GnRH) bioactivity in the brain of the immature rainbow trout, Salmo gairdneri: The effect of testosterone. Gen Comp Endocrinol 1986; 64: 80-84.
5. Schreibman MP, Margolis-Nunno H, Halpern-Sebold LR, Goos HJ, Perlman PW. The influence of androgen administration on the structure and function of the brain-pituitary-gonad axis of sexually immature platyfish, Xiphophorus maculatus. Cell Tissue Res 1986; 245: 519-524.
6. Trudeau VL, Peter RE, Sloley BD. Testosterone and estradiol potentiate the serum gonadotropin response to gonadotropin-releasing hormone in goldfish. Biol Reprod 1991; 44: 951-960.
7. Trudeau VL, Sloley BD, Wong AO, Peter RE. Interactions of gonadal steroids with brain dopamine and gonadotropin-releasing hormone in the control of gonadotropin-II secretion in the goldfish. Gen Comp Endocrinol 1993; 89: 39-50.
8. Montero M, Le Belle N, King JA, Millar RP, Dufour S. Differential regulation of the two forms of gonadotropin-releasing hormone (mGnRH and cGnRH-II) by sex steroids in the European female silver eel (Anguilla anguilla). Neuroendocrinology 1995; 61: 525-535.
9. Dubois EA, Zandbergen MA, Peute J, Goos HJ. Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates. Brain Res Bull 2002; 57: 413-418.
10. Lethimonier C, Madigou T, Munoz-Cueto JA, Lareyre JJ, Kah O. Evolutionary aspects of GnRHs, GnRH neuronal systems and GnRH receptors in teleost fish. Gen Comp Endocrinol 2004; 135: 1-16.
11. Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H. Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci Res 1998; 31: 31-38.
12. Gonzalez-Martinez D, Madigou T, Zmora N, Anglade I, Zanuy S, Zohar Y, Elizur A, Munoz-Cueto JA, 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.
13. Parhar IS, Soga T, Sakuma Y. Thyroid hormone and estrogen regulate brain region-specific messenger ribonucleic acids encoding three gonadotropin-releasing hormone genes in sexually immature male fish, Oreochromis niloticus. Endocrinology 2000; 141: 1618-1626.
14. Soga T, Sakuma Y, Parhar IS. Testosterone differentially regulates expression of GnRH messenger RNAs in the terminal nerve, preoptic and midbrain of male tilapia. Brain Res Mol Brain Res 1998; 60: 13-20.
15. Soma KK, Francis RC, Wingfield JC, Fernald RD. Androgen regulation of hypothalamic neurons containing gonadotropin-releasing hormone in a cichlid fish: Integration with social cues. Horm Behav 1996; 30: 216-226.
16. 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 2001; 124: 125-133.
17. Parhar IS, Soga T, Sakuma Y. In situ hybridization for two differentially expressed GnRH genes following estrogen and triiodothyronine treatment in the brains of juvenile tilapia (cichlid). Neurosci Lett 1996; 218: 135-138.
18. Parhar IS, Soga T, Sakuma Y. Quantitative in situ hybridization of three gonadotropin-releasing hormone-encoding mRNAs in castrated and progesterone-treated male tilapia. Gen Comp Endocrinol 1998; 112: 406-414.
19. Zandbergen MA, Kah O, Bogerd J, Peute J, Goos HJ. Expression and distribution of two gonadotropin-releasing hormones in the catfish brain. Neuroendocrinology 1995; 62: 571-578.
20. 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 1991; 314: 587-597.
21. 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 1990; 80: 116-126.
22. Sherwood NM, Harvey B, Brownstein MJ, Eiden LE. Gonadotropin-releasing hormone (Gn-RH) in striped mullet (Mugil cephalus), milkfish (Chanos chanos), and rainbow trout (Salmo gairdneri): Comparison with salmon Gn-RH. Gen Comp Endocrinol 1984; 55: 174-181.
23. Bailhache T, Arazam A, Klungland H, Alestrom P, Breton B, Jego P. Localization of salmon gonadotropin-releasing hormone mRNA and peptide in the brain of Atlantic salmon and rainbow trout. J Comp Neurol 1994; 347: 444-454.
24. Navas JM, Anglade I, Bailhache T, Pakdel F, Breton B, Jego P, Kah O. Do gonadotrophin-releasing hormone neurons express estrogen receptors in the rainbow trout? A double immunohistochemical study. J Comp Neurol 1995; 363: 461-474.
25. Amano M, Hyodo S, Urano A, Okumoto N, Kitamura S, Ikuta K, Suzuki Y, Aida K. Activation of salmon gonadotropin-releasing hormone synthesis by 17 alpha-methyltestosterone administration in yearling masu salmon, Oncorhynchus masou. Gen Comp Endocrinol 1994; 95: 374-380.
26. Breton B, Sambroni E. Steroid activation of the brain-pituitary complex gonadotropic function in the triploid rainbow trout Oncorhynchus mykiss. Gen Comp Endocrinol 1996; 101: 155-164.
27. Ashihara M, Suzuki M, Kubokawa K, Yoshiura Y, Kobayashi M, Urano A, Aida K. Two differing precursor genes for the salmon-type gonadotropin-releasing hormone exist in salmonids. J Mol Endocrinol 1995; 15: 1-9.
28. Li WH. Evolution of duplicate genes and pseudogenes. In: Nei M Kohen R, eds. Evolution of Genes and Proteins. Sunderland, MA: Sinauer Associates, 1983: 14-37.
29. Ohno S, Wolf U, Atkin NB. Evolution from fish to mammals by gene duplication. Hereditas 1968; 59: 169-187.
30. Hiraoka S, Suzuki M, Yanagisawa T, Iwata M, Urano A. Divergence of gene expression in neurohypophysial hormone precursors among salmonids. Gen Comp Endocrinol 1993; 92: 292-301.
31. Von Schalburg KR, Sherwood NM. Regulation and expression of gonadotropin-releasing hormone gene differs in brain and gonads in rainbow trout. Endocrinology 1999; 140: 3012-3024.
32. Ferriere F, Uzbekova S, Breton B, Jego P, Bailhache T. Two different messenger RNAs for salmon gonadotropin-releasing hormone are expressed in rainbow trout (Oncorhynchus mykiss). Brain Gen Comp Endocrinol 2001; 124: 321-332.
33. Thorgaard GH. Chromosome set manipulation and sex control in fish. In: Hoar WS Randall DJ, Donaldson EM, eds. Fish Physiology, Vol. 9. New York, NY: Academic Press, 1983: 405-434.
34. Atteke C, Vetillard A, Fostier A, Garnier DH, Jego P, Bailhache T. Effects of progesterone and estradiol on the reproductive axis in immature diploid and triploid rainbow trout. Comp Biochem Physiol a Mol Integr Physiol 2003; 134: 693-705.
35. Saligaut C, Garnier DH, Bennani S, Salbert G, Bailhache T, Jego P. Effects of estradiol on brain aminergic turnover of the female rainbow trout (Oncorhynchus mykiss) at the beginning of vitellogenesis. Gen Comp Endocrinol 1992; 88: 209-216.
36. Vetillard A, Atteke C, Saligaut C, Jego P, Bailhache T. Differential regulation of tyrosine hydroxylase and estradiol receptor expression in the rainbow trout brain. Mol Cell Endocrinol 2003; 199: 37-47.
37. Uzbekova S, Chyb J, Ferriere F, Bailhache T, Prunet P, Alestrom P, Breton B. Transgenic rainbow trout expressed sGnRH-antisense RNA under the control of sGnRH promoter of Atlantic salmon. J Mol Endocrinol 2000; 25: 337-350.
38. Vetillard A, Bailhache T. Cadmium: An endocrine disrupter that affects gene expression in the liver and brain of juvenile rainbow trout. Biol Reprod 2005; 72: 119-126.
39. Connor W, Mezquita J, Winkfein RJ, States JC, Dixon GH. Organization of the histone genes in the rainbow trout (Salmo gairdnerii). J Mol Evol 1984; 20: 227-235.
40. Von Schalburg KR, Harrower WL, Sherwood NM. Regulation and expression of gonadotropin-releasing hormone in salmon embryo and gonad. Mol Cell Endocrinol 1999; 157: 41-54.
41. Onuma T, Higa M, Ando H, Ban M, Urano A. Elevation of gene expression for salmon gonadotropin-releasing hormone in discrete brain loci of prespawning chum salmon during upstream migration. J Neurobiol 2005; 63: 126-145.
42. Davies B, Bromage N, Swanson P. The brain-pituitary-gonadal axis of female rainbow trout Oncorhynchus mykiss: Effects of photoperiod manipulation1. Gen Comp Endocrinol 1999; 115: 155-166.
43. Breton B, Motin A, Billard R, Kah O, Geoffre S, Precigoux G. Immunoreactive gonadotropin-releasing hormone-like material in the brain and the pituitary gland during the periovulatory period in the brown trout (Salmo trutta L.): Relationships with the plasma and pituitary gonadotropin. Gen Comp Endocrinol 1986; 61: 109-119.
44. Gomez JM, Weil C, Ollitrault M, Le Bail PY, Breton B, Le Gac F. Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen Comp Endocrinol 1999; 113: 413-428.
45. Dickey JT, Swanson P. Effects of sex steroids on gonadotropin (FSH and LH) regulation in coho salmon (Oncorhynchus kisutch). J Mol Endocrinol 1998; 21: 291-306.
46. Breton B, Govoroun M, Mikolajczyk T. GTH I and GTH II secretion profiles during the reproductive cycle in female rainbow trout: Relationship with pituitary responsiveness to GnRH-A stimulation. Gen Comp Endocrinol 1998; 111: 38-50.
47. Amano M, Ashihara M, Yoshiura Y, Kitamura S, Ikuta K, Aida K. Two differing salmon GnRH precursor mRNAs are co-expressed in the brain of sockeye salmon. Cell Tissue Res 1998; 292: 267-273.
48. Amano M, Ikuta K, Kitamura S, Aida K. The maturation of the salmon GnRH system and its regulation by gonadal steroids in masu salmon. Fish Physiol Biochem 1997; 17: 63-70.
49. Pakdel F, Le Guellec C, Vaillant C, Le Roux MG, Valotaire Y. Identification and estrogen induction of two estrogen receptors (ER) messenger ribonucleic acids in the rainbow trout liver: Sequence homology with other ERs. Mol Endocrinol 1989; 3: 44-51.
50. Takeo J, Yamashita S. Two distinct isoforms of cDNA encoding rainbow trout androgen receptors. J Biol Chem 1999; 274: 5674-5680.
51. Anglade I, Pakdel F, Bailhache T, Petit F, Salbert G, Jego P, Valotaire Y, Kah O. Distribution of estrogen receptor-immunoreactive cells in the brain of the rainbow trout (Oncorhynchus mykiss). J Neuroendocrinol 1994; 6: 573-583.
52. Salbert G, Bonnec G, Le Goff P, Boujard D, Valotaire Y, Jego P. Localization of the estradiol receptor mRNA in the forebrain of the rainbow trout. Mol Cell Endocrinol 1991; 76: 173-180.
53. Buchanan CD, Mahesh VB, Brann DW. Estrogen-astrocyte-luteinizing hormone-releasing hormone signaling: A role for transforming growth factor-beta (1). Biol Reprod 2000; 62: 1710-1721.
54. Takeo J, Yamashita S. Rainbow trout androgen receptor-alpha fails to distinguish between any of the natural androgens tested in transactivation assay, not just 11-ketotestosterone and testosterone. Gen Comp Endocrinol 2000; 117: 200-206.
55. Higa M, Kitahashi T, Sasaki Y, Okada H, Ando H. Distinct promoter sequences of two precursor genes for salmon gonadotropin-releasing hormone in masu salmon. J Mol Endocrinol 1997; 19: 149-161.
56. Klungland H, Andersen O, Kisen G, Alestrom P, Tora L. Estrogen receptor binds to the salmon GnRH gene in a region with long palindromic sequences. Mol Cell Endocrinol 1993; 95: 147-154.
57. Lincoln R, Scott A. Sexual maturation in triploid rainbow trout, Salmo gairdneri Richardson. J Fish Biol 1984; 25: 385-392.