Environmental factors affecting thyroid function of wild sea bass (Dicentrarchus labrax) from European coasts

[en] Thyroid functional status of wild fish in relation with the contamination of their environment deserves further investigation. We here applied a multi-level approach of thyroid function assessment in 87 wild sea bass collected near several estuaries: namely the Scheldt, the Seine, the Loire, the Charente and the Gironde. Thyroxine (T4) and triiodothyronine (T3) concentrations in muscle were analyzed by radioimmunoassay. The activity of hepatic enzymes involved in extrathyroidal pathways of thyroid hormone metabolism, viz. deiodination, glucuronidation and sulfatation were analyzed. Last, follicle diameter and epithelial cell heights were measured. We observed changes that are predicted to lead to an increased conversion of T4–T3 and lowered thyroid hormone excretion. The changes in the metabolic pathways of thyroid hormones can be interpreted as a pathway to maintain thyroid hormone homeostasis. From all compounds tested, the higher chlorinated PCBs seemed to be the most implicated in this perturbation.

Research center :

MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège

Disciplines :

Aquatic sciences & oceanology

Author, co-author :

Schnitzler, Joseph ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie

Klaren, Peter

Bouquegneau, Jean-Marie ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie

Das, Krishna ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Océanologie

Language :

English

Title :

Environmental factors affecting thyroid function of wild sea bass (Dicentrarchus labrax) from European coasts

Publication date :

2012

Journal title :

Chemosphere

ISSN :

0045-6535

eISSN :

1879-1298

Publisher :

Elsevier Science, Oxford, United Kingdom

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

FRIA - Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture [BE]

Available on ORBi :

since 26 October 2011

Statistics

Number of views

172 (33 by ULiège)

Number of downloads

427 (11 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Adams B.A., Cyr D.G., Eales J.G. Thyroid hormone deiodination in tissues of American plaice, hippoglossoides platessoides: characterization and short-term responses to polychlorinated biphenyls (PCBs) 77 and 126. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 2000, 127:367-378.
Aldegunde M., Soengas J., Ruibal C., Andres M. Effects of chronic exposure to gamma-HCH (lindane) on brain serotonergic and gabaergic systems, and serum cortisol and thyroxine levels of rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 1999, 20:325-330.
Bernier N.J., Flik G., Klaren P.H.M. Regulation and Contribution of the Corticotropic, Melanotropic and Thyrotropic Axes to the Stress Response in Fishes. Fish Physiology 2009, 235-311. Academic Press, (Chapter 6). D.N.J. Bernier DGVDKDAPF, J.B. Dr. Colin, D. Colin (Eds.).
Besselink H., vanBeusekom S., Roex E., Vethaak A., Koeman J., Brouwer A. Low hepatic 7-ethoxyresorufin-O-deethylase (EROD) activity and minor alterations in retinoid and thyroid hormone levels in flounder (Platichthys flesus) exposed to the polychlorinated biphenyl (PCB) mixture, Clophen A50. Environ. Pollut. 1996, 92:267-274.
Blanton M.L., Specker J.L. The Hypothalamic-Pituitary-Thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit. Rev. Toxicol. 2007, 37:97-115.
Boas M., Feldt-Rasmussen U., Skakkebaek N.E., Main K.M. Environmental chemicals and thyroid function. Eur. J. Endocrinol. 2006, 154:599-611.
Brouwer A., Morse D.C., Lans M.C., Schuur A.G., Murk A.J., Klasson-Wehler E., Bergman A., Visser T.J. Interactions of Persistent Environmental Organohalogens with the Thyroid Hormone System: Mechanisms and Possible Consequences for Animal and Human Health 1998, Princeton Scientific Publ. Inc., pp. 59-84.
Brown S.B., Adams B.A., Cyr D.G., Eales J.G. Contaminant effects on the teleost fish thyroid. Environ. Toxicol. Chem. 2004, 23:1680-1701.
Brucker-Davis F. Effects of environmental synthetic chemicals on thyroid function. Thyroid 1998, 8:827-856.
de Jesus E.G.T., Hirano T. Changes in whole body concentrations of cortisol, thyroid hormones, and sex steroids during early development of the chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 1992, 85:55-61.
Eales J.G., Brown S.B. Measurement and regulation of thyroidal status in teleost fish. Rev. Fish Biol. Fisheries 1993, 3:299-347.
Fok P., Eales J., Brown S. Determination of 3,5,3'-Triiodo-L-thyronine (T3) levels in tissues of rainbow trout (Salmo gairdneri) and the effect of low ambient pH and aluminium. Fish Physiol. Biochem. 1990, 8:281-290.
Funkenstein B., Bowman C.J., Denslow N.D., Cardinali M., Carnevali O. Contrasting effects of estrogen on transthyretin and vitellogenin expression in males of the marine fish, Sparus aurata. Mol. Cell. Endocrinol. 2000, 167:33-41.
Howdeshell K. A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect. 2002, 110:337-348.
Ishihara A., Sawatsubashi S., Yamauchi K. Endocrine disrupting chemicals: interference of thyroid hormone binding to transthyretins and to thyroid hormone receptors. Mol. Cell. Endocrinol. 2003, 199:105-117.
Janz D.M. Gross Functional Anatomy: Endocrine System. The Handbook of Experimental Animals - Laboratory Fish 2000, 189-217. Academic Press, London, UK. G.K. Ostrander (Ed.).
Kashiwagi K., Furuno N., Kitamura S., Ohta S., Sugihara K., Utsumi K., Hanada H., Taniguchi K., Suzuki K., Kashiwagi A. Disruption of thyroid hormone function by environmental pollutants. J. Health Sci. 2009, 55:147-160.
Klaren P.H.M., Haasdijk R., Metz J.R., Nitsch L.M.C., Darras V.M., Van der Geyten S., Flik G. Characterization of an iodothyronine 5'-deiodinase in gilthead seabream (Sparus auratus) that is inhibited by dithiothreitol. Endocrinology 2005, 146:5621-5630.
Kumar R., Ijiri S., Kight K., Swanson P., Dittman A., Alok D. Cloning and functional expression of a thyrotropin receptor from the gonads of a vertebrate (bony fish): potential thyroid-independent role for thyrotropin in reproduction. Mol. Cell. Endocrinol. 2000, 167:1-9.
Lans M., Spiertz C., Brouwer A., Koeman J. Different competition of thyroxine-binding to transthyretin and thyroxine-binding globulin by hydroxy-PCBs, PCDDs and PCDFs. Eur. J. Pharmacol. Environ. Toxicol. Pharmacol. Sect. 1994, 270:129-136.
Leatherland J.F. Field observation on reproductive and developmental dysfunction in introduced and native salmonids from the great lakes. Histochem. J. 1993, 19:737-751.
Leatherland J.F., Down N.E. Tumours and related lesions of the endocrine system of bony and cartilaginous fishes. Fish Fish. 2001, 2:59-77.
Leatherland J.F., Lin L., Down N.E., Donaldson E.M. Thyroid hormone content of eggs and early developmental stages of three stocks of goitred coho salmon (Oncorhynchus kisutch) from the great lakes of north America, and a comparison with a stock from British Columbia. Can. J. Fish. Aquat. Sci. 1989, 46:2146-2152.
Leatherland J.F., Lin T.H., Down N.E., Donaldson E.M. Thyroid hormone content of eggs and early development stages of five Oncorhynchus species. Can. J. Fish. Aquat. Sci. 1989, 46:2140-2145.
Leatherland J.F., Sonstegard R.A. Lowering of serum thyroxine and triiodothyronine levels in yearling coho salmon by dietary mirex and PCBs. J. Fish. Res. Board Can. 1978, 35:1285-1289.
Leatherland J.F., Sonstegard R.A. Effect of dietary polychlorinated biphenyls (PCBs) or mirex in combination with food deprivation and testosterone administration on serum thyroid hormone concentration and bioaccumulation of organochlorines in rainbow trout, Salmo gairdneri. J. Fish. Dis. 1980, 3:115-124.
Leroy K., Thomas P., Khan I. Thyroid hormone status of Atlantic croaker exposed to Aroclor 1254 and selected PCB congeners. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 2006, 144:263-271.
Lewis M.A., Scott G.I., Bearden D.W., Quarles R.L., Moore J., Strozier E.D., Sivertsen S.K., Dias A.R., Sanders M. Fish tissue quality in near-coastal areas of the gulf of Mexico receiving point source discharges. Sci. Total Environ. 2002, 284:249-261.
Loizeau V. A steady-state model of PCB bioaccumulation in the sea bass (Dicentrarchus labrax) food web from the Seine estuary, France. Estuaries 2001, 24:1074-1087.
Marino M., McCluskey R.T. Role of thyroglobulin endocytic pathways in the control of thyroid hormone release. Am. J. Physiol. Cell Physiol. 2000, 279:C1295-1306.
Morse D.C., Wehler E.K., Wesseling W., Koeman J.H., Brouwer A. Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254). Toxicol. Appl. Pharmacol. 1996, 136:269-279.
Naso B., Perrone D., Ferrante M.C., Bilancione M., Lucisano A. Persistent organic pollutants in edible marine species from the gulf of Naples, southern Italy. Sci. Total Environ. 2005, 343:83-95.
Pandey A., George K., Mohamed M. Effect of DDT on the thyroid gland of the mullet Liza parsia. J. Mar. Biol. Assoc. India 1995, 37:287-290.
Parker S., Specker J. Salinity and temperature effects on whole-animal thyroid-hormone levels in larval and juvenile stripped bass, Morone Saxatilis. Fish Physiol. Biochem. 1990, 8:507-514.
Power D.M., Llewellyn L., Faustino M., Nowell M.A., Björnsson B.T., Einarsdottir I.E., Canario A.V.M., Sweeney G.E. Thyroid hormones in growth and development of fish. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2001, 130:447-459.
Raine J. Assessment of thyroid function in adult medaka (Oryzias latipes) and juvenile rainbow trout (Oncorhynchus mykiss) using immunostaining methods. J. Exp. Zool. 2001, 290:366-378.
Rolland R. A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. J. Wildl. Dis. 2000, 36:615-635.
Schnitzler J.G., Koutrakis E., Siebert U., Thomé J.P., Das K. Effects of persistent organic pollutants on the thyroid function of the European sea bass (Dicentrarchus labrax) from the Aegean sea, is it an endocrine disruption?. Mar. Pollut. Bull. 2008, 56:1755-1764.
Schnitzler J.G., Thomé J.P., Lepage M., Das K. Organochlorine pesticides and polychlorinated biphenyl residues in wild sea bass (Dicentrarchus labrax) off European estuaries. Sci. Total Environ. 2011, 409:3680-3686.
Schuur A.G., Bergman å., Brouwer A., Visser T.J. Effects of pentachlorophenol and hydroxylated polychlorinated biphenyls on thyroid hormone conjugation in a rat and a human hepatoma cell line. Toxicol. In Vitro 1999, 13:417-425.
Shukla L., Pandey A.K. Restitution of thyroid activity in the DDT exposed<i>Sarotherodon Massambicus</i>: A histological and histochemical profile. Water Air Soil Pollut. 1986, 27:225-236.
Tagawa M., Hirano T. Presence of thyroxine in eggs and changes in its content during early development of chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol. 1987, 68:129-135.
Tagawa M., Miwa S., Inui Y., Dejesus E., Hirano T. Changes in thyroid-hormone concentrations during early development and metamorphosis of the flounder, Paralichthys olivaceus. Zool. Sci. 1990, 7:93-96.
Tagawa M., Tanaka M., Matsumoto S., Hirano T. Thyroid-hormones in eggs of various freshwater, marine and diadromous teleosts and their changes during egg development. Fish Physiol. Biochem. 1990, 8:515-520.
van der Heide S., Visser T., Everts M., Klaren P. Metabolism of thyroid hormones in cultured cardiac fibroblasts of neonatal rats. J. Endocrinol. 2002, 174:111-119.
Visser T.J., Kaptein E., Vantoor H., Vanraaij J., Vandenberg K.J., Joe C.T.T., Vanengelen J.G.M., Brouwer A. Glucuronidation of thyroid-hormone in rat-liver - effects of in-vivo treatment with microsomal-enzyme inducers and in-vitro assay conditions. Endocrinology 1993, 133:2177-2186.
Weber G.M., Okimoto D.K., Richman N.H., Grau E.G. Patterns of thyroxine and triiodothyronine in serum and follicle-bound oocytes of the tilapia, Oreochromis mossambicus, during oogenesis. Gen. Comp. Endocrinol. 1992, 85:392-404.
Wester P., Canton J. Histopathology of P. reticulata (Guppy) and Oryzias latipes (Medaka) in toxicity testing of some environmental contaminants. Aquat. Toxicol. 1988, 12:323-344.
Yadav A., Singh T. Pesticide induced changes in peripheral thyroid hormone levels during different reproductive phases in Heteropneustes fossilis. Ecotoxicol. Environ. Saf. 1987, 13:97-103.
Yamano K. The role of thyroid hormone in fish development with reference to aquaculture. JARQ 2005, 39:161-168.
Yamano K., Tagawa M., de Jesus E.G.T., Hirano T., Miwa S., Inui Y. Changes in whole body concentrations of thyroid hormones and cortisol in metamorphosing conger eel. J. Comp. Physiol. B 1991, 161:371-375.
Yoshiura Y., Sohn Y., Munakata A., Kobayashi M., Aida K. Molecular cloning of the cDNA encoding the beta subunit of thyrotropin and regulation of its gene expression by thyroid hormones in the goldfish, Carassius auratus. Fish Physiol. Biochem. 1999, 21:201-210.
Zoeller R.T., Tan S.T., Tyl R.W. General background on the Hypothalamic-Pituitary-Thyroid (HPT) axis. Crit. Rev. Toxicol. 2007, 37:11-53.