Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: A neuroendocrine lock for the onset of puberty

Biology of Reproduction

Volumn 71, Issue 5, 2004, Pages 1491-1500

  Vidal, Bernadette ^a   Pasqualini, Catherine ^b   Le Belle, Nadine ^a   Holland, M Claire H ^c   Sbaihi, Miskal ^a   Vernier, Philippe ^b   Zohar, Yonathan ^c   Dufour, Sylvie ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b CNRS   (France)

^c UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

Author keywords

Dopamine; Gonadotropin releasing hormone; Luteinizing hormone; Neuroendocrinology; Puberty

Indexed keywords

DOPAMINE; ESTRADIOL; GONADORELIN; LUTEINIZING HORMONE; PIMOZIDE; TESTOSTERONE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EEL; FEMALE; HORMONAL REGULATION; IMMUNOCYTOCHEMISTRY; LUTEINIZING HORMONE RELEASE; NEUROENDOCRINOLOGY; NONHUMAN; PRIORITY JOURNAL; PUBERTY; SEXUAL MATURATION;

ANIMALS; BIOMETRY; BODY WEIGHT; BRAIN; DOPAMINE; DOPAMINE ANTAGONISTS; EELS; ENDOCRINE GLANDS; FEMALE; GASTROINTESTINAL TRACT; GENITALIA; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; LIVER; LUTEINIZING HORMONE; NEUROSECRETORY SYSTEMS; ORGAN SIZE; OVARY; PIMOZIDE; PITUITARY GLAND; PUBERTY; TESTOSTERONE; TYROSINE 3-MONOOXYGENASE;

ANGUILLA ANGUILLA; ANGUILLIFORMES; ANIMALIA; MORONE SAXATILIS; PISCES; TELEOSTEI; VERTEBRATA;

EID: 6344233636     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.030627     Document Type: Article

References (64)

1. Huang YS, Rousseau K, Le Belle N, Vidal B, Burzawa-Gérard E, Marchelidon J, Dufour S. Insulin-like growth factor stimulates gonadotrophin production from eel pituitary cells: a possible metabolic signal for induction of puberty. J Endocrinol 1998; 159:43-52.
2. Huang YS, Rousseau K, Sbaihi M, Le Belle N, Schmilz M, Dufour S. Cortisol selectively stimulates pituitary gonadotropin β-subunit in a primitive teleost, Anguilla anguilla. Endocrinology 1999; 140:1228-1235.
3. Lauder GV, Liem KE Patterns of diversity and evolution in ray-finned fishes. In: Northcutt RC, David RE (eds.), Fish Neurobiology, 1st ed. Ann Arbor, MI: University of Michigan Press; 1983:2-24.
4. Stone R. Freshwater eels are slip-sliding away. Science 2003; 302:221-222.
5. Dufour S, Burzawa-Gérard E, Le Belle N, Sbaihi M, Vidal B. Reproductive endocrinology of the European eel, Anguilla anguilla. In: Aida K, Tsukamoto K, Yamauchi K (eds.), Eel Biology. Tokyo: Springer Verlag; 2003:373-383.
6. Fontaine M. Sur la maturation complète des organes génitaux de l'anguille mâle et l'émission spontanée de ses produits sexuels. C R Acad Sci Paris 1936; 202:1312-1315.
7. Fontaine M, Bertrand E, Lopez E, Callamand O. Sur la maturation des organes génitaux de l'anguille femelle (Anguilla anguilla L.) et l'émission spontanée des oeufs en aquarium. C R Acad Sci Paris 1964; 259:822-824.
8. Dufour S, Delerue-Le Belle N, Fontaine YA. Effects of steroid hormones on pituitary immunoreactive gonadotropin in European freshwater eel, Anguilla anguilla L. Gen Comp Endocrinol 1983; 52:190-197.
9. Goos HJ. Steroid feedback on pituitary gonadotropin secretion. In: Idler DR, Crim LW, Walsh J (eds.), Proceedings of the Third International Symposium on Reproductive Physiology of Fish. St. John's University, St. John, NS, Canada: Fish Symposium; 1987:16-20.
10. Dufour S, Lopez E, Le Menn F, Le Belle N, Baloche S, Fontaine YA. Stimulation of gonadotropin release and of ovarian development, by the administration of a gonadoliberin agonist and of dopamine antagonists, in female silver eel pretreated with estradiol. Gen Comp Endocrinol 1988; 70:20-30.
11. Peter RE, Chang JP, Nahorniak CS, Omeljaniuk RJ, Sokolowska M, Shih SH, Billard R. Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Prog Horm Res 1986; 42:513-548.
12. Peter RE, Paulencu CR. Involvement of the preoptic region in the gonadotropin release-inhibition in the goldfish. Neuroendocrinology 1980; 31:133-141.
13. Kah O, Dulka JG, Dubourg P, Thibault J, Peter RE. Neuroanatomical substrate for the inhibition of gonadotrophin secretion in goldfish: existence of a dopaminergic preopticohypophyseal pathway. Neuroendocrinology 1987; 45:451-458.
14. Linard B, Anglade I, Corio M, Navas JM, Pakdel F, Saligaut C, Kah O. Estrogen receptors are expressed in a subset of tyrosine hydroxylase-positive neurons of the anterior preoptic region in the rainbow trout. Neuroendocrinology 1996; 63:156-165.
15. Peter RE, Lin HR, Van Der Kraak G. Induced ovulation and spawning of cultured freshwater fish in China: advances in application of GnRH analogues and dopamine antagonists. Aquaculture 1988; 74:1-10.
16. 2 receptors in the dopaminergic inhibition of gonadotropin release in the African catfish, Clarias gariepinus. Aquaculture 1988; 72:369-378.
17. Van der Kraak G, Donaldson EM, Chang JP. Dopamine involvement in the regulation of gonadotropin secretion in coho salmon. Can J Zool 1986; 64:1245-1248.
18. Yaron Z, Gur G, Melamed P, Rosenfeld H, Elizur A, Levavi-Sivan B. Regulation offish gonadotropins. Int Rev Cytol 2003; 225:131-185.
19. Zohar Y, Harel M, Hassin S, Tandler A. Broodstock management and manipulation of spawning in the gilthead seabream, Spams aurata. In: Bromage N, Roberts RJ (eds.), Broodstock Management and Egg and Larval Quality. London: Blackwell Scientific Press; 1995:94-117.
20. Copeland PA, Thomas P. Control of gonadotropin release in the Atlantic croaker (Micropogonias undulatus): evidence for lack of dopaminergic inhibition. Gen Comp Endocrinol 1989; 74:474-483.
21. Marcano D, Guerrero HY, Gago N, Cardillo E, Requena M, Ruiz L. Monoamine metabolism in the hypothalamus of the juvenile teleost fish, Chaetodipterus faber. In: Goetz FW, Thomas P (eds.), Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish. University of Texas, Austin, TX: Fish Symposium; 1995;95:64-66.
22. Holland MC, Hassin S, Zohar Y. Effects of long-term testosterone, gonadotropin-releasing hormone agonist, and pimozide treatments on gonadotropin 11 levels and ovarian development in juvenile female striped bass (Morone saxatilis). Biol Reprod 1998; 59;1153-1162.
23. Kumakura N, Okuzawa K, Gen K, Kagawa H. Effects of gonadotropin-releasing hormone agonist and dopamine antagonist on hypothalamus-pituitary-gonadal axis of prepubertal female red seabream (Pagrus major). Gen Comp Endocrinol 2003; 131:264-273.
24. Linard B, Bennani S, Saligaut C. Involvement of estradiol in a catecholamine inhibitory tone of gonadotropin release in rainbow trout (Oncorhyncus mykiss). Gen Comp Endocrinol 1995; 99:192-196.
25. Saligaut C, Linard B, Breton B, Anglade I, Bailhache T, Kah O, Jego P. Brain aminergic systems in salmonids and other teleosts in relation to steroid feedback and gonadotropin release. Aquaculture 1999; 177:13-20.
26. Crim L. Hormonal manipulation of fish seasonal reproductive cycles. In: Scott AP, Sumpter JP, Kime DE, Rolfe MS (eds.), Reproductive Physiology of Fish. Sheffield, UK: Fish Symposium; 1991:43-47.
27. Benita S, Benoit JP, Puisieux F, Thies C. Characterization of drug-loaded poly(D,L-lactide) microspheres. J Pharm Sci 1984; 73:1721-1724.
28. Mylonas CC, Tabata Y, Langer R, Zohar Y. Preparation and evaluation of polyanhydride microspheres containing gonadotropin-releasing hormone (GnRH), for inducing ovulation and spermiation in fish. J Controlled Release 1995; 35:25-34.
29. Gabe M. Techniques Histologiques. Paris: Masson & Cie; 1968.
30. Dufour S, Delerue-Le Belle N, Fontaine YA. Development of a heterologous radioimmunoassay for eel (Anguilla anguilla) gonadotropin. Gen Comp Endocrinol 1983; 49:404-413.
31. Burzawa-Gérard E, Nath P, Baloche S, Peyon P. ELISA (enzyme-linked immunosorbent assay) for vitellogenin and vitellus in the eel (Anguilla anguilla) and in the Indian major carp (Labeo rohita). In: Scott AP, Sumpter JP, Kime DE, Rolfe MS (eds.), Reproductive Physiology of Fish. University of East Anglia, Sheffield, UK: Fish Symposium; 1991:319.
32. Boularand S, Faucon-Biguet NF, Vidal B, Veron M, Mallet J, Vincent JD, Dufour S, Vernier P. Tyrosine hydroxylase in the European eel (Anguilla anguilla): cDNA cloning, brain distribution, and phylogenetic analysis. J Neurochem 1998; 71:460-470.
33. Ohta H, Kagawa H, Tanaka H, Okuzawa K, Iinuma N, Hirose K. Artificial induction of maturation and fertilization in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 1997; 17:163-169.
34. Leloup-Hatey J, Hardy A, Nahoul K, Quérat B, Zohar Y. Influence of a gonadotrophic treatment upon the ovarian steroidogenesis in European silver eel. In: Reproduction in Fish: Basic and Applied Aspects in Endocrinology and Genetics. Paris: INRA; 1988:127-130.
35. Huang YS, Schmitz M, Le Belle N, Chang CF, Querat B, Dufour S. Androgens stimulate gonadotropin-II β subunit in eel pituitary cells in vitro. Mol Cell Endocrinol 1997; 131:157-166.
36. Pankhurst NW, Sorensen PW. Degeneration of the alimentary tract in sexually maturing European Anguilla anguilla (L.) and American eels Anguilla rostrata (LeSueur). Can J Zool 1984; 62:1143-1149.
37. Hassin S, Holland MCH, Zohar Y. Early maturity in the male striped bass: FSH and LH gene expression and their regulation by GnRHa and testosterone. Biol Reprod 2000; 63:1691-1697.
38. Crim LW, Evans DM. Influence of testosterone and/or luteinizing-hormone releasing hormone analogue on precocious sexual development in the juvenile rainbow trout. Biol Reprod 1983; 29:137-142.
39. Burzawa-Gerard E, Dumas-Vidal A. Effects of 17β-estradiol and carp gonadotropin on vitellogenesis in normal and hypophysectomized European silver female eel (Anguilla anguilla L.) employing a homologous radioimmunoassay for vitellogenin. Gen Comp Endocrinol 1991; 84:264-276.
40. Vétillard 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.
41. Trudeau VL, Lin HR, Peter RE. Testosterone potentiates the serum gonadotropin response to gonadotropin-releasing hormone in the common carp (Cyprinus carpio) and Chinese loach (Paramisgurnus dabryanus). Can J Zool 1991; 96:2480-2484.
42. Lo A, Chang JP. In vitro application of testosterone potentiates gonadotropin-releasing hormone-stimulated gonadotropin-II secretion from cultured goldfish pituitary cells. Gen Comp Endocrinol 1998; 111:334-346.
43. Lo A, Chang JP. In vitro action of testosterone in potentiating gonadotropin-releasing hormone-stimulated gonadotropin-H secretion in goldfish pituitary cells: involvement of protein kinase C, calcium, and testosterone metabolites. Gen Comp Endocrinol 1998; 111:318-333.
44. Goos H, Schulz R. Gonadal steroid hormones drive puberty in fish. In: Kawashima S, Kikuyama S (eds.), Advances in Comparative Endocrinology. Bologna, Italy: Monduzzi Editore; 1997:1429-1433.
45. Lokman PM, Rohr DH, Davie PS, Young G. The physiology of silvering in anguillid eels: androgens and control of metamorphosis from the yellow to silver stage. In: Aida K, Tsukamoto K, Yamauchi K (eds.), Eel Biology. Tokyo: Springer Verlag; 2003:331-349.
46. Lin H-R, Zhang ML, Zhang SM, Van Der Kraak G, Peter RE. Stimulation of pituitary gonadotropin and ovarian development by chronic administration of testosterone in female Japanese silver eel, Anguilla japonica. Aquaculture 1991; 96:87-95.
47. Jeng SR, Chen GR, Lai JY, Huang YS, Dufour S, Chang CF. Regulation of pituitary gonadotropin II and growth hormone content by sex steroids and pituitary extract in the aquacultured Japanese eel, Anguilla japonica. Aquaculture 2002; 209:319-332.
48. Chang JP, Yu KL, Wong AO, Peter RE. Differential actions of dopamine receptor subtypes on gonadotropin and growth hormone release in vitro in goldfish. Neuroendocrinology 1990; 51:664-674.
49. De Leeuw R, Van't Veer C, Goos HJ, Van Oordt PG. The dopaminergic regulation of gonadotropin-releasing hormone receptor binding in the pituitary of the African catfish, Clarias gariepinus. Gen Comp Endocrinol 1988; 72:408-415.
50. De Leeuw R, Habibi HR, Nahorniak CS, Peter RE. Dopaminergic regulation of pituitary gonadotropin-releasing hormone receptor activity in the goldfish (Carassius auratus). J Endocrinol 1989; 121:239-247.
51. Yu KL, Peter RE. Dopaminergic regulation of brain gonadotropin-releasing hormone in male goldfish during spawning behavior. Neuroendocrinology 1990; 52:276-283.
52. Peter RE, Trudeau V, Sloley BD, Peng C, Nahorniak CS. Actions of catecholamines, peptides and sex steroids in regulation of gonadotropin-II in the goldfish. In: Scott AR Sumpter JP, Kime DE, MS Rolfe (eds.), Reproductive Physiology of Fish. University of East Anglia, Sheffield, UK: Fish Symposium; 1991:30-34.
53. Roberts BL, Meredith GE, Maslam S. Immunocytochemical analysis of the dopamine system in the brain and spinal cord of the European eel, Anguilla anguilla. Anat Embryol 1989; 180:401-412.
54. Olivereau M., Nagahama Y. Immunocytochemical study of eel and trout gonadotrophs. Gen Comp Endocrinol 1982; 46:365-366.
55. Montera M, Vidal B, King JA, 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 1994; 7:227-241.
56. Sotowska-Brochocka J, Martynska L, Licht P. Dopaminergic inhibition of gonadotropic release in hibernating frogs, Rana temporaria. Gen Comp Endocrinol 1994; 93:192-196.
57. El Halawani ME, Burke WH. Brain monoamine metabolism of turkey hens in various stages of their reproductive cycle. Biol Reprod 1976; 15:254-259.
58. Sharp PJ, Talbot RT, Macnamee MC. Evidence for the involvement of dopamine and 5-hydroxytryptamine in the regulation of the preovulatory release of luteinizing hormone in the domestic hen. Gen Comp Endocrinol 1989; 76:205-213.
59. Brango CW, Whisnant CS, Goodman R. A role of catecholaminergic neurons in the suppression of pulsatile luteinizing hormone secretion in the prepubertal ewe lamb. Neuroendocrinology 1990; 52:448-454.
60. Thiéry JC, Gayrard V, Le Corre S, Viguié C, Martin GB, Chemineau P, Malpaux B. Dopaminergic control of LH secretion by the A15 nucleus in anestrous ewes. J Reprod Fertil 1995; 49:285-296.
61. 2-like dopaminergic receptors in the median eminence during the establishment of long-day inhibition of LH secretion in the ewe. J Endocrinol 1999; 163:243-254.
62. Dailey RA, Tsou RC, Tindall GT, Neill JD. Direct hypophysial inhibition of luteinizing hormone release by dopamine in the rabbit. Life Sci 1978; 22:1491-1498.
63. Huseman CA, Kugler JA, Schneider IG. Mechanism of dopaminergic suppression of gonadotropin secretion in men. J Clin Endocrinol Metab 1980; 51:209-214.
64. Chen YN, Fan HF, Hsieh SL, Kuo CM. Physiological involvement of DA in ovarian development of the freshwater giant prawn, Macro-brachium rosenbergii. Aquaculture 2003; 228:383-395.