Temporal expression of hepatic estrogen receptor 1, vitellogenin1 and vitellogenin2 in European silver eels

General and Comparative Endocrinology

Volumn 166, Issue 1, 2010, Pages 1-11

  Palstra, Arjan P ^a,b   Schnabel, Denhi ^a,c   Nieveen, Maaike C ^a   Spaink, Herman P ^a   van den Thillart, Guido E E J M ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF BARCELONA   (Spain)

^c INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

17 Estradiol; Anguilla anguilla Linnaeus; Dopaminergic inhibition; Eel reproduction; Estrogen receptor 2; Gonadotropin; Lipid deposition; Maturation; Pituitary extract; Puberty; Quantitative RT PCR; Silvering

Indexed keywords

CALCIUM; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FAT DROPLET; GONADOTROPIN; UNCLASSIFIED DRUG; VITELLOGENIN; VITELLOGENIN1; VITELLOGENIN2;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM BLOOD LEVEL; CONTROLLED STUDY; DEVELOPMENTAL STAGE; GENE EXPRESSION; GONAD DEVELOPMENT; LIPID STORAGE; LIVER CELL; LIVER DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; ORGANOGENESIS; PRIORITY JOURNAL; VITELLOGENESIS;

EID: 77349089938     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2009.09.006     Document Type: Article

References (68)

1. Adachi S., Ijiri S., Kazeto Y., Yamauchi K. Oogenesis in the Japanese eel, Anguilla japonica. Eel Biology 2003, 502-518. Springer, Heidelberg. K. Aida, K. Tsukamoto, K. Yamauchi (Eds.).
2. Aubry E., Cagnon C., Lalanne Y., Mouches C. Assessment of young yellow European eel Anguilla anguilla L. exposure to a CYP1A1 inducer by the quantification of increase in hepatic CYP1A1 mRNA using real-time RT-PCR. J. Fish Biol. 2007, 71:470-477.
3. Babin P.J., Carnevali O., Lubzens E., Schneider W.J. Molecular aspects of oocyte vitellogenesis in fish. The Fish Oocyte: From Basic Studies to Biotechnological Applications 2007, 39-76. Springer, Heidelberg. P.J. Babin, J. Cerda, E. Lubzens (Eds.).
4. Bardet P.-L., Horard B., Robinson-Rechavi M., Laudet V., Vanacker J.-M. Characterization of oestrogen receptors in zebrafish (Danio rerio). J. Mol. Endocrinol. 2002, 28:153-163.
5. Bezdenezhnykh V.A., Prokhorcik G.A., Petrikov A.M., Petukov V.B., Plyuta M.V. Obtaining the larvae of European eel Anguilla anguilla L. (Pisces, Anguillidae), under experimental conditions. Dokl. Akad. Nauk. SSSR 1983, 268:1264-1266.
6. Bezdenezhnykh V.A., Prokhorcik G.A. Period of oocyte maturation and assessment of egg quality of eel, Anguilla anguilla (Anguillidae), under stimulation of maturation with gonadotropic hormones. Vopr. Ikhtiol. 1984, 5:814-821.
7. Boëtius J., Boëtius L. Experimental maturation of female silver eels, Anguilla anguilla. Estimates of fecundity and energy reserves for migration and spawning. Dana 1980, 1:1-28.
8. Burzawa-Gerard E., Dumas-Vidal A. Effects of 17-beta-estradiol and carp gonadotropin on vitellogenesis in normal and hypophysectomised European silver female eel (Anguilla anguilla L.) employing a homologous radioimmunoassay for vitellogenin. Gen. Comp. Endocrinol. 1991, 84:264-276.
9. Campbell B., Dickey J., Beckman B., Young G., Pierce A., Fukada H., Swanson P. Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin. Biol. Reprod. 2006, 75:34-44.
10. Chang X.T., Kobayashi T., Todo T., Ikeuchi T., Yoshiura Y., Kajiura-Kobayashi H., Morrey C., Nagahama Y. Molecular cloning of estrogen receptors alpha and beta in the ovary of a teleost fish, the tilapia (Oreochromis niloticus). Zool. Sci. 1999, 16:653-658.
11. Choi C.Y., Habibi H.R. Molecular cloning of estrogen receptor α and expression pattern of estrogen receptor subtypes in male and female goldfish. Mol. Cell. Endocrinol. 2003, 204:169-177.
12. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
13. de Jonge H.W., de Bakker M.A.G., Verbeek F.J., Weijs W. Embedding of large specimens in glycol methacrylate: prerequisites for multi-signal detection and high-resolution imaging. Microsc. Res. Tech. 2005, 66:25-30.
14. Dufour S., Delerve-Le Belle N., Fontaine Y.A. Effects of steroid hormones on pituitary immunoreactive gonadotropin in European freshwater eel, Anguilla anguilla L. Gen. Comp. Endocrinol. 1983, 52:190-197.
15. Dufour S., Lopez E., Le Menn F., Le Belle N., Baloche S., Fontaine Y.A. 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.
16. Durif C., Dufour S., Elie P. The silvering process of the eel: a new classification from the yellow resident stage to the silver migrating stage. J. Fish Biol. 2005, 66:1-19.
17. Durif C.M.F., Dufour S., Elie P. Impact of silvering stage, age, body size and condition on the reproductive potential of the European eel. Mar. Ecol. Prog. Ser. 2006, 327:171-181.
18. Endo T., Todo T., Lokman P.M., Ijiri S., Adachi S., Yamauchi K. In vitro induction of oil droplet accumulation into previtellogenic oocytes of Japanese eel, Anguilla japonica. Cybium 2008, 32:239-240.
19. Filby A.L., Tyler C.R. Molecular characterization of estrogen receptors 1, 2a and 2b and their tissue and ontogenetic expression in fathead minnow (Pimephales promelas). Biol. Reprod. 2005, 73:648-662.
20. Fontaine M., Bertrand E., Lopez E., Callamand O. Sur la maturation des organes genitaux de l'anguille femelle (Anguilla anguilla L.) et l'émission spontanée des oeufs en aquarium. C. R. Acad. Sci. 1964, 259:2907-2910.
21. Hawkins M.B., Thornton J.W., Crews D., Skipper J.K., Dotte A., Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc. Natl. Acad. Sci. USA 2000, 97:10751-10756.
22. Kagawa H. Artificial induction of oocyte maturation and ovulation. Eel Biology 2003, 403-414. Springer, Heidelberg. K. Aida, K. Tsukamoto, K. Yamauchi (Eds.).
23. Kagawa H., Tanaka H., Ohta H., Unuma T., Nomura K. The first success of glass eel production in the world: basic biology on fish reproduction advances new applied technology in aquaculture. Fish Physiol. Biochem. 2005, 31:193-199.
24. Kazeto Y., Ijiri S., Adachi S., Yamauchi K. Cloning and characterization of a cDNA encoding cholesterol side-chain cleavage cytochrome P450 (CYP11A1): tissue distribution and changes in the transcript abundance in ovarian tissue of Japanese eel, Anguilla japonica, during artificially induced sexual development. J. Steroid Biochem. 2006, 99:121-128.
25. Larsson P., Hamrin S., Okla L. Fat content as a factor inducing migratory behaviour in the eel (Anguilla anguilla L.) to the Sargasso Sea. Naturwissenschaften 1990, 77:488-490.
26. Leaños-Castañeda O., Van Der Kraak G. Functional characterization of estrogen receptor subtypes, ERα and ERβ, mediating vitellogenin production in the liver of rainbow trout. Toxicol. Appl. Pharm. 2007, 224:116-125.
27. Lokman P.M., Young G. Induced spawning and early ontogeny of New Zealand freshwater eels (Anguilla dieffenbachi and A. australis). N. Z. J. Mar. Freshwater Res. 2000, 34:135-145.
28. Lokman P.M., George K.A.N., Divers S.L., Algie M., Young G. 11-Ketotestosterone and IGF-I increase the size of previtellogenic oocytes from shortfinned eel, Anguilla australis, in vitro. Reproduction 2007, 133:955-967.
29. Menuet A., Anglade I., Flouriot G., Pakdel F., Kah O. Tissue-specific expression of two structurally different estrogen receptor alpha isoforms along the female reproductive axis of an oviparous species, the rainbow trout. Biol. Reprod. 2001, 65:1548-1557.
30. Menuet A., Pellegrini E., Anglade I., Blaise O., Laudet V., Kah O., Pakdel F. Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol. Reprod. 2002, 66:1881-1892.
31. Menuet A., Le Page Y., Torres O., Kern L., Kah O., Pakdel F. Analysis of the estrogen regulation of the zebrafish estrogen receptor (ER) reveals distinct effects of ERalpha, ERbeta1 and ERbeta2. J. Mol. Endocrinol. 2004, 32:975-986.
32. Munoz-Cueto J.A., Burzawa-Gerard E., Kah O., Valotaire Y., Pakdel F. Cloning and sequencing of the gilthead sea bream estrogen receptor cDNA. DNA Seq. 1999, 10:75-84.
33. Muriach B., Cerdá-Reverter J.M., Gómez A., Zanuy S., Carrillo M. Molecular characterization and central distribution of the estradiol receptor alpha (ERα) in the sea bass (Dicentrarchus labrax). J. Chem. Neuroanat. 2008, 35:33-48.
34. Nagler J.J., Cavileer T., Sullivan J., Cyr D.G., Rexroad C. The complete nuclear estrogen receptor family in the rainbow trout: discovery of the novel ERα2 and both ERβ isoforms. Gene 2007, 392:164-173.
35. Olivereau M., Olivereau J. Effect of estradiol-17 beta on the cytology of the liver, gonads and pituitary, and on plasma electrolytes in the female freshwater eel. Cell Tissue Res. 1979, 199:431-454.
36. Pakdel F., Metivier R., Flouriot G., Valotaire Y. Two estrogen receptor (ER) isoforms with different estrogen dependencies are generated from the trout ER gene. Endocrinology 2000, 141:571-580.
37. Pankhurst N.W. Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla L. J. Fish Biol. 1982, 21:127-140.
38. Palstra A.P., Cohen E.G.H., Niemantsverdriet P.R.W., van Ginneken V.J.T., van den Thillart G.E.E.J.M. Artificial maturation and reproduction of European silver eel: development of oocytes during final maturation. Aquaculture 2005, 249:533-547.
39. Palstra A., Curiel D., Fekkes M., de Bakker M., Székely C., van Ginneken V., van den Thillart G. Swimming stimulates oocyte development in European eel (Anguilla anguilla L.). Aquaculture 2007, 270:321-332.
40. Palstra A., van Ginneken V., van den Thillart G. Effects of swimming on silvering and maturation. Spawning Migration of European Eel. Estimation of the Reproductive Success of Silver Eels 2009, 229-251. Springer, Heidelberg. G. van den Thillart, S. Dufour, C. Rankin (Eds.).
41. Palstra A., van den Thillart G. Artificial maturation and reproduction of European eel. Spawning Migration of European Eel. Estimation of the Reproductive Success of Silver Eels 2009, 309-331. Springer, Heidelberg. G. van den Thillart, S. Dufour, C. Rankin (Eds.).
42. Pãtino R., Xia Z., Gale W., Wu C., Maule A.G., Chang X. Novel transcripts of the estrogen receptor α gene in channel catfish. Gen. Comp. Endocrinol. 2000, 120:314-325.
43. Pãtino R., Sullivan C.V. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol. Biochem. 2002, 26:57-70.
44. Pedersen B.H. Fertilisation of eggs, rate of embryonic development and hatching following induced maturation of the European eel Anguilla anguilla. Aquaculture 2004, 237:461-473.
45. Perazzolo L.M., Coward K., Davail B., Normand E., Tyler C.R., Pakdel F., Schneider W.J., Le Menn F. Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biol. Reprod. 1999, 60:1057-1068.
46. Pérez, L., Peñaranda, D.S., Gallego, V., Dufour, S., Palstra, A., van den Thillart, G., Jover, M., Asturiano, J.F., 2008. Temperature effect during the hormonal induced maturation in European eel females. World Aquaculture Society, May 19-23, Busan, Korea.
47. Pierron F., Baudrimont M., Bossy A., Bourdineaud J.P., Brethes D., Elie P., Massabau J.C. Impairment of lipid storage by cadmium in the European eel (Anguilla anguilla). Aquat. Toxicol. 2007, 81:304-311.
48. Rogers S.A., Llewellyn L., Wigham T., Sweeney G.E. Cloning of the Atlantic salmon (Salmo salar) estrogen receptor-alpha gene. Comp. Biochem. Physiol. B 2000, 125:379-385.
49. Sabo-Attwood T., Kroll K.J., Denslow N.D. Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol. Mol. Cell. Endocrinol. 2004, 218:107-118.
50. Salas-Vidal E., Meijer A.H., Cheng X., Spaink H.P. Genomic annotation and expression analysis of the zebrafish Rho small GTPase family during development and bacterial infection. Genomics 2005, 86:25-37.
51. Sato N., Kawazoe I., Suzuki Y., Aida K. Induction of vitellogenesis. Eel Biology 2003, 387-399. Springer, Heidelberg. K. Aida, K. Tsukamoto, K. Yamauchi (Eds.).
52. Sato N., Kawazoe I., Suzuki Y., Aida K. Effects of temperature on vitellogenesis in Japanese Anguilla japonica. Fish. Sci. 2006, 72:961-966.
53. 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.
54. Socorro S., Power D.M., Olsson P.-E., Canario A.V.M. Two estrogen receptors expressed in the teleost fish, Sparus aurata: cDNA cloning, characterization and tissue distribution. J. Endocrinol. 2000, 166:293-306.
55. Sorensen P.W., Winn H.E. The induction of maturation and ovulation in American eels, Anguilla rostrata (LeSueur), and the relevance of chemical and visual cues to male spawning behavior. J. Fish Biol. 1984, 25:261-268.
56. Svedäng H., Wickström H. Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development. J. Fish Biol. 1997, 50:475-486.
57. Todd P.R. Morphometric changes, gonad histology, and fecundity estimates in migrating New Zealand freshwater eels (Anguilla spp.). N. Z. J. Mar. Freshwater Res. 1981, 15:155-170.
58. Todo T., Adachi S., Yamauchi K. Molecular cloning and characterization of Japanese eel estrogen receptor cDNA. Moll. Cell. Endocrinol. 1996, 119:37-45.
59. Tyler C.R., Sumpter J.P. Oocyte growth and development in teleosts. Rev. Fish Biol. Fish. 1996, 6:287-318.
60. van Ginneken V., Durif C., Dufour S., Sbaihi M., Boot R., Noorlander K., Doornbos J., Murk A.J., van den Thillart G. Endocrine profiles during silvering of the European eel (Anguilla anguilla L.) living in saltwater. Anim. Biol. 2007, 57:453-465.
61. van Ginneken V., Dufour S., Sbaihi M., Balm P., Noorlander K., de Bakker M., Doornbos J., Palstra A., Antonissen E., Mayer I., van den Thillart G. Does a 5500-km swim trial stimulate early sexual maturation in the European eel (Anguilla anguilla L.)?. Comp. Biochem. Physiol. A 2007, 147:1095-1103.
62. Verslycke T., Vandenbergh G.F., Versonnen B., Arijs K., Janssen C.R. Induction of vitellogenesis in 17α-ethinylestradiol-exposed rainbow trout (Oncorhynchus mykiss): a method comparison. Comp. Biochem. Physiol. C 2002, 132:483-492.
63. Versonnen B.J., Goemans G., Belpaire C., Janssen C.R. Vitellogenin content in European eel (Anguilla anguilla) in Flanders. Belgium Environ. Pollut. 2004, 128:363-371.
64. Vidal B., Pasqualini C., Le Belle N., Claire M., Holland H., 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.
65. Wallace R.A., Selman K. Cellular dynamic aspects of oocyte growth in teleosts. Am. Zool. 1981, 21:325-343.
66. Yamamoto K., Yamauchi K. Sexual maturation of Japanese eel and production of eel larvae in the aquarium. Nature 1974, 251:381.
67. Yamamoto K., Omori M., Yamauchi K. Oogenesis of the Japanese eel. Bull. Jpn. Soc. Sci. Fish. 1974, 40:9-15.
68. Yamauchi K., Nakamura M., Takahashi H., Takano K. Cultivation of larvae of Japanese eel. Nature 1976, 263:412.