Top

Published in:

Open Access 01-12-2004 | Research

17beta-estradiol induced vitellogenesis is inhibited by cortisol at the post-transcriptional level in Arctic char (Salvelinus alpinus)

Authors: Hakan Berg, Carina Modig, Per-Erik Olsson

Published in: Reproductive Biology and Endocrinology | Issue 1/2004

Abstract

This study was performed to investigate stress effects on the synthesis of egg yolk precursor, vitellogenin (Vtg) in Arctic char (Salvelinus alpinus). In particular the effect of cortisol (F) was determined since this stress hormone has been suggested to interfere with vitellogenesis and is upregulated during sexual maturation in teleosts. Arctic char Vtg was purified and polyclonal antibodies were produced in order to develop tools to study regulation of vitellogenesis. The Vtg antibodies were used to develop an enzyme-linked immunosorbent assay. The corresponding Vtg cDNA was cloned from a hepatic cDNA library in order to obtain DNA probes to measure Vtg mRNA expression. Analysis of plasma from juvenile Arctic char, of both sexes, exposed to different steroids showed that production of Vtg was induced in a dose dependent fashion by 17β-estradiol (E2), estrone and estriol. Apart from estrogens a high dose of F also upregulated Vtg. In addition, F, progesterone (P) and tamoxifen were tested to determine these compounds ability to modulate E2 induced Vtg synthesis at both the mRNA and protein level. Tamoxifen was found to inhibit E2 induced Vtg mRNA and protein upregulation. P did not alter the Vtg induction while F reduced the Vtg protein levels without affecting the Vtg mRNA levels. Furthermore the inhibition of Vtg protein was found to be dose dependent. Thus, the inhibitory effect of F on Vtg appears to be mediated at the post-transcriptional level.

Available only for authorised users

Lazier CB, MacKay ME: Vitellogenin gene expression in teleost fish. In Biochemistry and Molecular Biology of Fishes. Edited by: Hochachka PW, Mommsen TP. 1993, Elsevier, Amsterdam, NL, 2: 391-406.

Byrne BM, Gruber M, Ab G: The evolution of egg yolk proteins. Prog Biophys Mol Biol. 1989, 53: 33-69. 10.1016/0079-6107(89)90005-9.CrossRefPubMed

Shibata N, Yoshikuni M, Nagahama Y: Vitellogenin incorporation into Oocytes of Rainbow trout, Oncorhynchus mykiss, in Vitro: Effects of hormones on denuded oocytes. Develop Growth Differ. 1993, 35: 115-121.CrossRef

Ng TB, Idler DR: Yolk formation and differentiation in teleost fishes. In Fish Physiology, Reproduction: Part A: Endocrine tissues and hormones. Edited by: Hoar WS, Randall DJ, Donaldsson EM. 1983, Academic press, New York, USA, IX: 373-404.CrossRef

Carnevali O, Carletta R, Cambi A, Vita A, Bromage N: Yolk formation and degradation during oocyte maturation in seabream Sparus aurata: involvement of two lysosomal proteinases. Biol Reprod. 1999, 60: 140-6.CrossRefPubMed

Matsubara T, Ohkubo N, Andoh T, Sullivan CV, Hara A: Two forms of vitellogenin, yielding two distinct lipovitellins, play different roles during oocyte maturation and early development of barfin flounder, Verasper moseri, a marine teleost that spawns pelagic eggs. Develop Biol. 1999, 213: 18-32. 10.1006/dbio.1999.9365.CrossRefPubMed

Wahli W, Dawid IB, Ryffel GU, Weber R: Vitellogenesis and the vitellogenin gene family. Science. 1981, 212: 298-304.CrossRefPubMed

Montorzi M, Falchuk KH, Vallee BL: Xenopus laevis vitellogenin is a zinc protein. Biochem Biophys Res Commun. 1994, 200: 1407-1413. 10.1006/bbrc.1994.1607.CrossRefPubMed

Montorzi M, Falchuk KH, Vallee BL: Vitellogenin and lipovitellin: zinc proteins of Xenopus laevis oocytes. Biochemistry. 1995, 34: 10851-10858.CrossRefPubMed

10.

Falchuk KH, Montorzi M: Zinc physiology and biochemistry in oocytes and embryos. Biometals. 2001, 14: 385-395. 10.1023/A:1012994427351.CrossRefPubMed

11.

Falchuk KH: The molecular basis for the role of zinc in developmental biology. Mol Cell Biochem. 1998, 188: 41-48. 10.1023/A:1006808119862.CrossRefPubMed

12.

Wahli W: Evolution and expression of vitellogenin genes. Trends Genet. 1988, 4: 227-232. 10.1016/0168-9525(88)90155-2.CrossRefPubMed

13.

Chen JS, Sappington TW, Raikhel AS: Extensive sequence conservation among insect, nematode, and vertebrate vitellogenins reveals ancient common ancestry. J Mol Evol. 1997, 44: 440-451.CrossRefPubMed

14.

Wang H, Yan T, Tan JT, Gong Z: A zebrafish vitellogenin gene (vg3) encodes a novel vitellogenin without a phosvitin domain and may represent a primitive vertebrate vitellogenin gene. Gene. 2000, 256: 303-10. 10.1016/S0378-1119(00)00376-0.CrossRefPubMed

15.

Trichet V, Buisine N, Mouchel N, Moran P, Pendas AM, Le Pennec JP, Wolff J: Genomic analysis of the vitellogenin locus in rainbow trout (Oncorhynchus mykiss) reveals a complex history of gene amplification and retroposon activity. Mol Gen Genet. 2000, 263: 828-837. 10.1007/s004380000247.CrossRefPubMed

16.

Sundarara BI, Goswami SV, Lamba VJ: Role of testosterone, estradiol-17β and cortisol during vitellogenin synthesis in the catfish, Heteropneustes fossilis (Bloch). Gen Comp Endocrinol. 1982, 48: 390-397.CrossRef

17.

Campbell PM, Pottinger TG, Sumpter JP: Stress reduces the quality of gametes produced by rainbow trout. Biol Reprod. 1992, 47: 1140-1150.CrossRefPubMed

18.

Pelissero C, Flouriot G, Foucher JL, Bennetau B, Dunogues J, Le Gac F, Sumpter JP: Vitellogenin synthesis in cultured hepatocytes; an in vitro test for the estrogenic potency of chemicals. J Steroid Biochem Mol Biol. 1993, 44: 263-272. 10.1016/0960-0760(93)90086-C.CrossRefPubMed

19.

Lethimonier C, Flouriot G, Valotaire Y, Kah O, Ducouret B: Transcriptional interference between glucocorticoid receptor and estradiol receptor mediates the inhibitory effect of cortisol on fish vitellogenesis. Biol Reprod. 2000, 62: 1763-1771.CrossRefPubMed

20.

Aida K, Ngan P, Hibiya T: Physiological studies on gonadal maturation of fishes – Sexual difference in composition of plasma protein of Ayu in relation to gonadal maturation. Bull Jap Soc Sci Fish. 1973, 39: 1091-1106.CrossRef

21.

Mommsen TP, Walsh PJ: Vitellogenesis and oocyte assembly. In Fish physiology, Academic Press, Inc. XIA. The physiology of developing fish: Part A: Eggs and larvae. Edited by: Hoar WS, Randall DJ, Donaldsson EM. 1988, Academic press, New York, USA, 347-406.CrossRef

22.

Heppell SA, Denslow ND, Folmar LC, Sullivan CV: Universal assay of vitellogenin as a biomarker for environmental estrogens. Environ Health Perspect. 1995, 103: 9-15.PubMedCentralCrossRefPubMed

23.

Sumpter JP, Jobling S: Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect. 1995, 103: 173-178.PubMedCentralCrossRefPubMed

24.

Silversand C, Haux C: Isolation of turbot (Scophthalmus maximus) vitellogenin by high-performance anion-exchange chromatography. J Chromatogr. 1989, 478: 387-397. 10.1016/S0021-9673(01)84408-3.PubMed

25.

Laemmli U: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970, 227: 680-685.CrossRefPubMed

26.

Le Guellec K, Lawless K, Valotaire Y, Kress M, Tenniswood M: Vitellogenin gene expression in male rainbow trout (Salmo gairdneri). Gen Comp Endocrinol. 1988, 71: 359-371.CrossRefPubMed

27.

Chomczynski P, Sacchi N: Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987, 162: 156-159. 10.1006/abio.1987.9999.CrossRefPubMed

28.

Olsson P-E, Kling P, Petterson C, Silversand C: Interaction of cadmium and oestradiol-17 beta on metallothionein and vitellogenin synthesis in rainbow trout (Oncorhynchus mykiss). Biochem J. 1995, 307: 197-203.PubMedCentralCrossRefPubMed

29.

Silversand C, Hyllner SJ, Haux C: Isolation, Immunological detection, and Observations of the instability of Vitellogenin from four teleosts. Exp Zool. 1993, 267: 587-597.CrossRef

30.

Specker JL, Sullivan CV: Vitellogenesis in fishes: status and perspectives. In Perspectives in Endocrinology. Edited by: Davey KG, Peter RE, Tobe SS. 1994, National Research Council, Ottawa, Canada, 304-315.

31.

Chen T: Identification and characterisation of estrogen responsive gene products in the liver of rainbow trout. J Biochem Cell Biol. 1983, 61: 802-810.CrossRef

32.

Norberg B, Haux C: Induction, isolation and a characterization of the lipid content of plasma vitellogenin from two Salmo species: rainbow trout (Salmo gairdneri) and sea trout (Salmo trutta). Comp Biochem Physiol B. 1985, 81: 869-876. 10.1016/0305-0491(85)90081-1.CrossRefPubMed

33.

Johnsen H, Tveiten H, Willassen NP, Arnesen AM: Arctic charr (Salvelinus alpinus) vitellogenin: development and validation of an enzyme-linked immunosorbent assay. Comp Biochem Physiol B Biochem Mol Biol. 1989, 124: 355-362. 10.1016/S0305-0491(99)00132-7.CrossRef

34.

Buerano CC, Inaba K, Natividad FF, Morisawa M: Vitellogenins of Oreochromis niloticus: identification, isolation, and biochemical and immunochemical characterization. J Exp Zool. 1995, 273: 59-69.CrossRefPubMed

35.

Brion F, Nilsen BM, Eidem JK, Goksoyr A, Porcher JM: Development and validation of an enzyme-linked immunosorbent assay to measure vitellogenin in the zebrafish (Danio rerio). Environ Toxicol Chem. 2002, 21: 1699-1708.CrossRefPubMed

36.

Kuiper GJM, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S, Gustafsson J-Å: Comparison of the ligand binding specificity and transcriptional tissue distribution of estrogen receptors α and β. Endocrinology. 1997, 138: 863-870. 10.1210/en.138.3.863.PubMed

37.

Matthews J, Celius T, Halgren R, Zacharewski T: Differential estrogen receptor binding of estrogenic substances: a species comparison. J Steroid Biochem Mol Biol. 2000, 74: 223-234. 10.1016/S0960-0760(00)00126-6.CrossRefPubMed

38.

Berg AH, Westerlund L, Olsson P-E: Regulation of Arctic char (Salvelinus alpinus) egg shell proteins and vitellogenin during reproduction and in response to 17β-estradiol and cortisol. Gen Comp Endocrinol. 2003, 135: 276-285. 10.1016/j.ygcen.2003.10.004.CrossRef

39.

Olsson P-E, Haux C, Förlin L: Variations in hepatic metallothionein, zinc and copper levels during an annual reproductive cycle in rainbow trout, Salmo gairdneri. Fish Physiol Biochem. 1987, 3: 39-47.CrossRefPubMed

40.

Lethimonier C, Flouriot G, Kah O, Ducouret B: The glucocorticoid receptor represses the positive autoregulation of the trout estrogen receptor gene by preventing the enhancer effect of a C/EBPbeta-like protein. Endocrinology. 2002, 143: 2961-2974. 10.1210/en.143.8.2961.PubMed

41.

Marilley D, Robyr D, Schild-Poulter C, Wahli W: Regulation of the vitellogenin gene b1 promoter after transfer into hepatocytes in primary cultures. Mol Cell Endocrinol. 1998, 141: 79-93. 10.1016/S0303-7207(98)00090-2.CrossRefPubMed

42.

Carruth LL, Dores RM, Maldonado TA, Norris DO, Ruth T, Jones RE: Elevation of plasma cortisol during the spawning migration of landlocked kokanee salmon (Oncorhynchus nerka kennerlyi). Comp Biochem Physiol C Toxicol Pharmacol. 2000, 127: 123-131. 10.1016/S0742-8413(00)00140-7.PubMed

43.

Hyllner SJ, Andersson T, Haux C, Olsson P-E: Cortisol induction of metallothionein in primary culture of rainbow trout hepatocytes. J Cell Physiol. 1989, 139: 24-28.CrossRefPubMed

44.

Olsson P-E: Metallothionein gene expression and regulation in fish. In The Biochemistry and Molecular Biology of Fishes. Edited by: Hochachka PW, Mommsen TP. 1993, Molecular Biology Frontiers, 2: 259-278.

45.

Olsson P-E, Zafarullah M, Gedamu L: A role of metallothionein in zinc regulation after estradiol indcuction of vitellogenin synthesis in rainbow trout, Salmo gairdneri. Biochem J. 1989, 257: 555-560.PubMedCentralCrossRefPubMed

46.

Gerpe M, Kling P, Berg AH, Olsson P-E: Arctic char (Salvelinus alpinus) metallothionein: cDNA sequence, expression, and tissue-specific inhibition of cadmium-mediated metallothinein induction by 17β-estradiol, 4-OH-PCB30, and PCB 104. Environ Toxicol Chem. 2000, 19: 638-645.CrossRef

Title: 17beta-estradiol induced vitellogenesis is inhibited by cortisol at the post-transcriptional level in Arctic char (Salvelinus alpinus)
Authors: Hakan Berg
Carina Modig
Per-Erik Olsson
Publication date: 01-12-2004
Publisher: BioMed Central
Published in: Reproductive Biology and Endocrinology / Issue 1/2004
Electronic ISSN: 1477-7827
DOI: https://doi.org/10.1186/1477-7827-2-62

Keynote webinar | Spotlight on medication adherence

Springer Medicine

17beta-estradiol induced vitellogenesis is inhibited by cortisol at the post-transcriptional level in Arctic char (Salvelinus alpinus)

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2004

Human chorionic gonadotropin administration is associated with high pregnancy rates during ovarian stimulation and timed intercourse or intrauterine insemination

Reproductive Biology and Endocrinology – First year anniversary

Comparative aspects of trophoblast development and placentation

Leptin receptor in the chicken ovary: potential involvement in ovarian dysfunction of ad libitum-fed broiler breeder hens

Biology of primate relaxin: A paracrine signal in early pregnancy?

Methods to find out the expression of activated genes