Endocrine evidence that silvering, a secondary metamorphosis in the eel, is a pubertal rather than a metamorphic event

Neuroendocrinology

Volumn 82, Issue 3-4, 2005, Pages 221-232

  Aroua, Salima ^a   Schmitz, Monika ^b   Baloche, Sylvie ^a   Vidal, Bernadette ^a   Rousseau, Karine ^a   Dufour, Sylvie ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Fish; Gonadal steroids; Gonadotropins; Growth hormone; Metamorphosis; Puberty; Silvering; Thyrotropin

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; FOLLITROPIN; GROWTH HORMONE; HYPOPHYSIS HORMONE; LUTEINIZING HORMONE; MESSENGER RNA; SEX HORMONE; TESTOSTERONE; THYROTROPIN; THYROXINE; VITELLOGENIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMETRY; COLOR; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DIGESTIVE SYSTEM; EEL; FEMALE; GONAD; HORMONAL REGULATION; HYPOPHYSIS FUNCTION; HYPOPHYSIS GONAD SYSTEM; HYPOPHYSIS THYROID SYSTEM; LIFE CYCLE; METAMORPHOSIS; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; SILVERING; STEROIDOGENESIS;

ANIMALS; EELS; ESTRADIOL; FEMALE; FOLLICLE STIMULATING HORMONE; GROWTH HORMONE; IMMUNOBLOTTING; IMMUNOENZYME TECHNIQUES; LUTEINIZING HORMONE; METAMORPHOSIS, BIOLOGICAL; PITUITARY GLAND; SEXUAL MATURATION; TESTOSTERONE; THYROID GLAND; THYROTROPIN; THYROXINE; VITELLOGENINS;

EID: 33646495959     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000092642     Document Type: Article

References (58)

1. Gudernatsch JF: Feeding experiments on tadpoles: the influence of specific organs given as food on growth and differentiation: a contribution to the knowledge of organs of internal secretion. Wilhelm Roux' Arch Entwi Mech Org 1912;35:457-483.
2. Power DM, Llewellyn L, Faustino M, Nowell MA, Björnsson B Th, Einarsdottir IE, Canario AVM, Sweeney GE: Thyroid hormones in growth and development of fish. Comp Biochem Physiol 2001;130C:447-459.
3. Schreiber AM: Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective. Comp Biochem Physiol 2001;129B: 587-595.
4. Inui Y, Miwa S: Thyroid hormone induces metamorphosis of flounder larvae. Gen Comp Endocrinol 1985;60:450-454.
5. Miwa S, Inui Y: Effects of various doses of thyroxine and triiodothyronine on the metamorphosis of flounder (Paralichthys olivaceus). Gen Comp Endocrinol 1987;67:356-363.
6. de Jesus EG, Hirano T, Inui Y: Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. Gen Comp Endocrinol 1991;82:369-376.
7. Yamano K, Tagawa M, De Jesus EG, Hirano T, Miwa S, Inui Y: Changes in whole body concentrations of thyroid hormones and cortisol in metamorphosing conger eel. J Comp Physiol 1991;161B: 371-375.
8. Tata JR: Amphibian metamorphosis as a model for studying the developmental action of thyroid hormone. Biochimie 1999;81:359-366.
9. Hayes TB: Amphibian metamorphosis: an historical perspective. Am Zool 1997;37:121-124.
10. Fontaine M: Physiological mechanisms in the migration of marine and amphihaline fish; in Russell FS, Younge M (eds): Advances in Marine Biology. New York, Academic Press, 1975, vol 13, pp 241-355.
11. Barron MG: Endocrine control of smoltification in anadromous salmonids. J Endocrinol 1986;108:313-319.
12. Hoar W: The physiology of smolting salmonids; in Hoar W, Randall D (eds): Fish Physiology. San Diego, Academic Press, 1988, vol XI, pp 275-343.
13. Boeuf G: Salmonid smolting: a pre-adaptation to the oceanic environment; in Rankin JF, Frank B (eds): Fish Ecophysiology. London, Chapman & Hall, 1993, pp 105-135.
14. Björnsson BT: The biology of salmon growth hormone: from daylight to dominance. Fish Physiol Biochem 1997;17:9-24.
15. Bertin L: Larves et metamorphoses; in Grassé P (ed): Traité de Zoologie. Paris, Masson, 1958, XIII, 3, pp 1813-1834.
16. Tesch FW: The eel. Biology and Management of Anguillid Eels. London, Chapman & Hall, 1977.
17. Wald G: Metamorphosis: an overview; in Gilbert LI, Frieden E (eds): Metamorphosis, a Problem in Developmental Biology, ed 2. New York, Plenum Press, 1981, pp 1-39.
18. Lecomte-Finiger R: Métamorphose de l'anguille jaune en anguille argentée (Anguilla anguilla L.) et sa migration catadrome. Ann Biol 1990;29:183-194.
19. Fontaine Y-A: L'argenture de l'anguille: metamorphose, anticipation, adaptation. Bull Fr Pêche Piscicult 1994;335:171-185.
20. Pankhurst NW: Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). J Fish Biol 1982;21:127-140.
21. Beatty DD: Visual pigments in the American eel Anguilla rostrata. Vision Res 1975;15:771-776.
22. Wood P, Partridge JC: Opsin substitution induced in retinal rods of the eel (Anguilla anguilla L.): a model for G-protein-linked receptors. Proc R Soc Lond [B] 1993;254:227-232.
23. Thompson AJ, Sargent JR: Changes in the levels of chloride cells and (Na-K) dependant ATPase in the gills of yellow and silver eels adapting to seawater. J Exp Zool 1978;200:33-40.
24. Egginton S: Metamorphosis of the American eel, Anguilla rostrata LeSueur. I. Changes in metabolism of skeletal muscle. J Exp Zool 1986;237:173-184.
25. Lokman PM, Vermeulen GJ, Lambert JGD, Young G: Gonad histology and plasma steroid profiles in wild New Zealand freshwater eels (Anguilla dieffenbachii and A. australis) before and at the onset of the natural spawning migration. I. Females. Fish Physiol Biochem 1998;19:325-338.
26. Sbaihi M, Fouchereau-Peron M, Meunier F, Elie P, Mayer I, Burzawa-Gérard E, Vidal B, Dufour S: Reproductive biology of the conger eel from the south coast of Brittany, France and comparison with the European eel. J Fish Biol 2001;59:302-318.
27. Cottrill RA, McKinley RS, van der Kraak G, Dutil J-D, Reid KB, McGrath KJ: Plasma non-esterified fatty acid profiles and 17β-oestradiol levels of juvenile immature and maturing adult American eels in the St Lawrence River. J Fish Biol 2001;59:364-379.
28. Han Y-S, Liao I-C, Tzeng W-N, Huang Y-S, Yu J Y-L: Serum estradiol-17β and testosterone levels during silvering in wild Japanese eel Anguilla japonica. Comp Biochem Physiol 2003;136B: 913-920.
29. 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, 2003, pp 373-383.
30. Romeo RD: Puberty: a period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol 2003;15:1185-1192.
31. 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.
32. Rousseau K, Le Belle N, Sbaihi M, Marchelidon J, Schmitz M, Dufour S: Evidence for a negative feedback in the control of eel growth hormone by thyroid hormones. J Endocrinol 2002;175:605-613.
33. Vidal B, Pasqualini C, Le Belle N, Holland NCH, Sbaihi M, Vernier P, Zohar Y, Dufour S: Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: a neuroendocrine lock for the onset of puberty. Biol Reprod 2004;71:1491-1500.
34. Dufour S, Delerue-Le Belle N, Fontaine Y-A: Development of a heterologous radioimmunoassay for eel (Anguilla anguilla) gonadotropin. Gen Comp Endocrinol 1983;49:404-413.
35. Marchelidon J, Schmitz M, Houdebine LM, Vidal B, Le Belle N, Dufour S: Development of a radioimmunoassay for European eel growth hormone and application to the study of silvering and experimental fasting. Gen Comp Endocrinol 1996;102:360-369.
36. Leloup J, de Luze A: Prolactine et hormones thyroidiennes chez l'anguille, Anguilla anguilla. Cr Acad Fr 1980;291:87-90.
37. Burzawa-Gérard 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.
38. Huang Y-S, Schmitz M, Le Belle N, Chang CF, Quérat B, Dufour S: Androgens stimulate gonadotropin-II β-subunit in eel pituitary cells in vitro. Mol Cell Endocrinol 1997;131:157-166.
39. Schmitz M, Aroua S, Vidal B, Le Belle N, Elie P, Dufour S: Differential regulation of luteinizing hormone and follicle-stimulating hormone expression during ovarian development and under sexual steroid feedback in the European eel. Neuroendocrinology 2005;81:107-119.
40. Quérat B, Moumni M, Jutisz M, Fontaine YA, Counis R: Molecular cloning and sequence analysis of the cDNA for the putative β subunit of the type-II gonadotrophin from the European eel. J Mol Endocrinol 1990;4:257-264.
41. Quérat B, Jutisz M, Fontaine YA, Counis R: Cloning and sequence analysis of the cDNA for the pituitary glycoprotein hormone α-subunit of the European eel. Mol Cell Endocrinol 1990;71:253-259.
42. Pradet-Balade B, Schmitz M, Salmon C, Dufour S, Quérat B: Down-regulation of TSH subunit mRNA levels by thyroid hormones in the European eel. Gen Comp Endocrinol 1997;108:191-198.
43. Durif C, Dufour S, Elie P: The silvering process of the Eruopean eel: a new classification from the yellow resident stage to the silver migrating stage. J Fish Biol 2005;66:1-19.
44. 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.
45. Marchelidon J, Le Belle N, Hardy A, Vidal B, Sbaihi M, Burzawa-Gérard E, Schmitz M, Dufour S: Etude des variations de paramètres anatomiques et endocriniens chez l'anguille européenne (Anguilla anguilla) femelle, sédentaire et d'avalaison: application à la caractérisation du stade argenté. Bull Fr Pêche Piscicult 1999;355:349-368.
46. Quérat B, Hardy A, Leloup-Hatey J: Niveaux plasmatiques, vitesses de clairance métabolique, et vitesses de secretion de la testosterone et de l'oestradiol-17β chez l'anguille (Anguilla anguilla L.) argentée. Gen Comp Endocrinol 1985;59:482-493.
47. Han Y-S, Liao I-C, Huang Y-S, Tzeng W-N, Yu J Y-L: Profiles of PGH-α, GTH I-β, and GTH II-β transcript levels at different ovarian stages in the wild female Japanese eel, Anguilla japonica. Gen Comp Endocrinol 2003;133:8-16.
48. Yoshiura Y, Suetake H, Aida K: Duality of gonadotropin in a primitive teleost, Japanese eel (Anguilla japonica). Gen Comp Endocrinol 1999;114:121-131.
49. Nagae M, Todo T, Gen K, Kato Y, Young G, Adachi S, Yamauchi K: Molecular cloning of the cDNAs encoding pituitary glycoprotein hormone α- and gonadotropin IIβ subunits of the Japanese eel, Anguilla japonica, and increase in their mRNAs during ovarian development induced by injection of chum salmon pituitary homogenate. J Mol Endocrinol 1996;16:171-181.
50. Suetake H, Okubo K, Sato N, Yoshiura Y, Suzuki Y, Aida K: Differential expression of two gonadotropin (GTH) β subunit genes during ovarian maturation induced by repeated injection of salmon GTH in the Japanese eel Anguilla japonica. Fish Sci 2002;68:290-298.
51. Nagae M, Adachi S, Yamauchi K: Changes in transcription of pituitary glycoprotein hormone α and gonadotropin IIβ subunits during ovarian development induced by repeated injections of salmon pituitary homogenate in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 1996;17:179-186.
52. Saito K, Mokman PM, Young G, Ozaki Y, Matsubara H, Okumura H, Kazeto Y, Yoshiura Y, Aida K, Adachi S, Yamauchi K: Follicle-stimulating hormone β, luteinizing hormone β and glycoprotein hormone α subunit mRNA levels in artificially maturing Japanese eel Anguilla japonica and naturally maturing New Zealand longfinned eel Anguilla dieffenbachii. Fish Sci 2003;69:146-153.
53. Han Y-S, Liao I-C, Tzeng W-N, Yu J Y-L: Cloning of the cDNA for thyroid stimulating hormone β subunit and changes in activity of the pituitary-thyroid axis during silvering of the Japanese eel, Anguilla japonica. J Mol Endocrinol 2004;32:179-194.
54. Rohr DH, Lokman PM, Davie PS, Young G: 11-ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla rostrata (Le Sueur). J Fish Biol 2001;32:297-307.
55. Boëtius I, Larsen LO: Effects of testosterone on eye size and spermiation in silver eels, Anguilla anguilla. Gen Comp Endocrinol 1991;82:238.
56. Pankhurst NW, Sorensen PW: Degeneration of the alimentary tract in sexually maturing European Anguilla anguilla (L.) and American eels Anguilla rostrata (Le Sueur). Can J Zool 1984;62:1143-1149.
57. Olivereau M, Olivereau J: Effects of 17 α-methyltestosterone on the skin and gonads of freshwater male silver eels. Gen Comp Endocrinol 1985;57:64-71.
58. Wright ML, Cykowski LG, Lundrigan L, Hemond KL, Kochan DM, Faszewski EE, Anuszewski CM: Anterior pituitary and adrenal cortical hormones accelerate or inhibit tadpole hindlimb growth and development depending on stage of spontaneous development or thyroxine concentration in induced metamorphosis. J Exp Zool 1994;270:175-188.