Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

The aim of this study was to describe the time-course of estrogen-induced gene expression, corresponding plasma protein detection and histological alterations after cessation of octylphenol (OP) exposure of Cichlasoma dimerus, to test differential responses of biomarkers suitable for environmental monitoring. Male fish were exposed to a nominal concentration of 150μg/L OP for 28 days, and later transferred to OP-free water aquaria for 1, 3, 7, 14, 21 or 28 days. Blood and mucus samples were obtained in order to analyze vitellogenin (VTG) and zona pellucida (ZP) proteins by Western blot; liver samples were used for gene expression and to assess tissue damage and further recovery of all the analyzed endpoints. Partial sequences of C. dimerus VTG and Na +/K +-ATPase were obtained. Comparison with VTGs of several teleosts supports that the partial sequence obtained for C. dimerus belongs to VTGAb type. ZP and VTG expression was highly up-regulated by OP. Immunoreactive (ir-) bands of 62, 52 and 50kDa for ZP and 140, 103, 75 and 64kDa for VTG, were detected after 28 days of OP exposure in plasma and mucus samples. After transfer of treated fish to clean water, ZP ir-bands in plasma disappeared rapidly (day 3), while VTG ir-bands decreased gradually; no ir-bands were detected on day 28 of recovery. Similarly, ZPB transcripts abruptly returned to background levels (day 3), earlier than for ZPC (day 7) or VTG (day 14). Liver from OP treated fish showed tissue disarrangement, eccentric and euchromatic hepatocytes nuclei and intense perinuclear basophilia. After the recovery period, these changes were still evident though less pronounced, accounting for irreversibility of tissue damage or the requirement for a longer period of depuration. The present results confirm that for biochemical and molecular biomarkers, such as induction of female proteins in male fish exposed to OP, complete recovery is achieved after adequate time of depuration (28 days). Male ZPB expression reflects a recent exposure to estrogenic contaminants, while VTG may reveal past exposures. The combination of biomarkers with different temporal responses such as C. dimerus ZP and VTG provides a more comprehensive interpretation of pollution status. © 2012 Elsevier B.V.

Registro:

Documento: Artículo
Título:Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol
Autor:Genovese, G.; Regueira, M.; Piazza, Y.; Towle, D.W.; Maggese, M.C.; Lo Nostro, F.
Filiación:Laboratorio de Ecotoxicología Acuática, Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, C1428EHA, Argentina
Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Rivadavia 1917,, Buenos Aires, C1033AAJ, Argentina
Mount Desert Island Biological Laboratory, Salisbury Cove, 04672, ME, United States
Idioma: Inglés
Palabras clave:Cichlid; Gene expression; Octylphenol; Recovery; Vitellogenin; Zona pellucida proteins; adenosine triphosphatase (potassium sodium); estrogen; octylphenol; phenol derivative; unclassified drug; vitellogenin; biomarker; biomonitoring; cichlid; estrogenic compound; gene expression; histology; phenolic compound; pollution exposure; protein; animal experiment; animal tissue; article; cichlid; controlled study; environmental exposure; environmental monitoring; female; gene expression; liver cell; liver injury; male; nonhuman; nucleotide sequence; priority journal; protein expression; teleost; upregulation; water pollution; zona pellucida; Amino Acid Sequence; Animals; Cichlids; Egg Proteins; Endocrine Disruptors; Estradiol; Estrogens; Female; Gene Expression Regulation; Male; Membrane Glycoproteins; Molecular Sequence Data; Phenols; Phylogeny; Protein Isoforms; Protein Subunits; Receptors, Cell Surface; RNA, Messenger; Sodium-Potassium-Exchanging ATPase; Water Pollutants, Chemical; Cichlasoma; Cichlidae; Teleostei
Año:2012
Volumen:114-115
Página de inicio:1
Página de fin:13
DOI: http://dx.doi.org/10.1016/j.aquatox.2012.02.005
Título revista:Aquatic Toxicology
Título revista abreviado:Aquat. Toxicol.
ISSN:0166445X
CODEN:AQTOD
CAS:Egg Proteins; Endocrine Disruptors; Estradiol, 50-28-2; Estrogens; Membrane Glycoproteins; Phenols; Protein Isoforms; Protein Subunits; RNA, Messenger; Receptors, Cell Surface; Sodium-Potassium-Exchanging ATPase, 3.6.3.9; Water Pollutants, Chemical; octylphenol; zona pellucida glycoproteins
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0166445X_v114-115_n_p1_Genovese

Referencias:

  • Alonso, F., Cánepa, M., Guimarães Moreira, R., Pandolfi, M., Social and reproductive physiology and behavior of the Neotropical cichlid fish Cichlasoma dimerus under laboratory conditions (2011) Neotrop. Ichthyol., 9 (3), pp. 559-570
  • Andersen, L., Holbech, H., Gessbo, Å., Norrgren, L., Petersen, G.I., Effects of exposure to 17a-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio) (2003) Comp. Biochem. Physiol. C, 134, pp. 365-374
  • Arukwe, A., Kullman, S.W., Hinton, D.E., Differential biomarker gene and protein expressions in nonylphenol and estradiol-17β treated juvenile rainbow trout (Oncorhynchus mykiss) (2001) Comp. Biochem. Physiol. C, 129, pp. 1-10
  • Arukwe, A., Goksøyr, A., Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation: oogenetic, population, and evolutionary implications of endocrine disruption (2003) Comp. Hepatol., 2, p. 4
  • Arukwe, A., Røe, K., Molecular and cellular detection of expression of vitellogenin and zona radiata protein in liver and skin of juvenile salmon (Salmo salar) exposed to nonylphenol (2008) Cell Tissue Res., 331, pp. 701-712
  • Au, D.W.T., The application of histo-cytopathological biomarkers in marine pollution monitoring: a review (2004) Mar. Pollut., 48, pp. 817-834
  • Babin, P.J., Bogerd, J., Kooiman, F.P., Van Marrewijk, W.J.A., Van der Horst, D.J., Apolipophorin II/I, apolipoprotein B, vitellogenin, and microsomal triglyceride transfer protein genes are derived from a common ancestor (1999) J. Mol. Evol., 49, pp. 150-160
  • Babin, P.J., Carnevali, O., Lubzens, E., Schneider, W.J., Molecular aspects of oocyte vitellogenesis in fish (2007) The Fish Oocyte: From Basic Studies to Biotechnological Applications, pp. 39-76. , Springer, New York, P.J. Babin, J. Cerdà, E. Lubzens (Eds.)
  • Baker, M.E., Is vitellogenin an ancestor of apolipoprotein B-100 of human lowdensity lipoprotein and human lipoprotein lipase? (1988) Biochem. J., 255, pp. 1057-1060
  • Bangsgaard, K., Madsen, S.S., Korsgaard, B., Effect of waterborne exposure to 4-tert-octylphenol and 17β-estradiol on smoltification and downstream migration in Atlantic salmon, Salmo salar (2006) Aquat. Toxicol., 80, pp. 23-32
  • Beale, K.M., Towle, D.W., Jayasundara, N., Smith, C.M., Shields, J.D., Small, H.J., Greenwood, S.J., Anti-lipopolysaccharide factors in the American lobster Homarus americanus: molecular characterization and transcriptional response to Vibrio fluvialis challenge (2008) Comp. Biochem. Physiol.: Part D Genomics Proteomics, 3 (4), pp. 263-269
  • Blackburn, M.A., Kirby, S.J., Waldock, M.J., Concentrations of alkyphenol polyethoxylates entering UK estuaries (1999) Mar. Pollut. Bull., 38 (2), pp. 109-118
  • Bowman, C.J., Kroll, K.J., Hemmer, M.J., Folmar, L.C., Denslow, N.D., Estrogen-induced vitellogenin mRNA and protein in sheepshead minnow (Cyprinodon variegatus) (2000) Gen. Comp. Endocrinol., 120, pp. 300-313
  • Bustin, S.A., Benes, V., Nolan, T., Pfaffl, M.W., Quantitative real-time RT-PCR - a perspective (2005) J. Mol. Endocrinol., 34, pp. 597-601
  • Calabrese, E.J., Baldwin, L.A., Hormesis: U-shaped dose responses and their centrality in toxicology (2001) Trends Pharmacol. Sci., 22 (6), pp. 285-291
  • Casciotta, J.R., Almirón, A.E., Bechara, J., (2005), p. 244. , Peces del Iberá. Hábitat y Diversidad. Grafikar, La Plata, Argentina; UNDP, Fundación Ecos, UNLP-UNNECéspedes, R., Lacorte, S., Raldυa, D., Ginebreda, A., Barceló, D., Piña, B., Distribution of endocrine disruptors in the Llobregat River basin (Catalonia, NE Spain) (2005) Chemosphere, 61 (11), pp. 1710-1719
  • Craft, J.A., Brown, M., Dempsey, K., Francey, J., Kirby, M.F., Scott, A.P., Katsiadaki, I., Moffat, C.F., Kinetics of vitellogenin protein and mRNA induction and depuration in fish following laboratory and environmental exposure to oestrogens (2004) Mar. Environ. Res., 58, pp. 419-423
  • Da Cuña, R., Rey Vázquez, G., Piol, N., Verrengia Guerrero, N., Maggese, M.C., LoNostro, F., Assessment of the acute toxicity of the organochlorine pesticide endosulfan in Cichlasoma dimerus (Teleostei, Perciformes) (2011) Ecotoxicol. Environ. Saf., 74, pp. 1065-1073
  • Davis, R.A., Kern, F., Showalter, R., Sutherland, E., Sinensky, M., Simon, F.R., Alterations of hepatic Na +,K +-ATPase and bile flow by estrogen: effects on liver surface membrane lipid structure and function (1978) Proc. Natl. Acad. Sci. U.S.A., 75 (9), pp. 4130-4134
  • de Souza, F.S.J., Gomes, S.L., A P-type ATPase from the aquatic fungus Blastocladiella emersonii similar to animal Na, K-ATPases (1998) Biochim. Biophys. Acta, 1383, pp. 183-187
  • Feng, S.H., Leu, J.H., Yang, C.H., Fang, M.J., Huang, C.J., Hwang, P.P., Gene expression of Na +-K +-ATPase alpha 1 and alpha 3 subunits in gills of the teleost Oreochromis mossambicus, adapted to different environmental salinities (2002) Mar. Biotechnol. (NY), 4 (4), pp. 379-391
  • Fiedler, S., Foerster, M., Glaser, B., Zech, W., Alkylphenols in sediments of the Atlantic rainforest south-west of Sao Paulo, Brazil (2007) Chemosphere, 66, pp. 212-218
  • Finn, R.N., Kristoffersen, B.A., Vertebrate vitellogenin gene duplication in relation to the " 3R hypothesis": correlation to the pelagic egg and the oceanic radiation of teleosts (2007) PLoS ONE, 2 (1), pp. e169
  • Finn, R.N., Kolarevic, J., Kongshaug, H., Nilsen, F., Evolution and differential expression of a vertebrate vitellogenin gene cluster (2009) BMC Evol. Biol., 9, p. 2
  • Flouriot, G., Pakdel, F., Valotaire, Y., Transcriptional and post-transcriptional regulation of rainbow trout estrogen receptor and vitellogenin gene expression (1996) Mol. Cell. Endocrinol., 124, pp. 173-183
  • Fox, G.A., Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence basin (2001) Environ. Health Perspect., 109, pp. 853-861
  • Genovese, G., Regueira, M., Lo Nostro, F., Da Cuña, R., Maggese, C., Luquet, C., Towle, D., CDNA sequencing of vitelline envelope protein and gene expression in Cichlasoma dimerus (Teleostei, Perciformes) induced by xenoestrogens (2006) Bull. Mt. Desert Isl. Biol. Lab. Salisb. Cove Maine, 45, pp. 127-128
  • Genovese, G., Regueira, M., Lo Nostro, F., Maggese, C., Towle, D., Vitelline envelope proteins and vitellogenin gene expression in Cichlasoma dimerus (Teleostei, Perciformes) exposed to octylphenol (2007) Bull. Mt. Desert Isl. Biol. Lab. Salisb. Cove Maine, 46, pp. 161-162
  • Genovese, G., Maggesse, M.C., Towle, D., Differential induction of estrogen receptors in Cichlasoma dimerus (Teleostei Perciformes) exposed to octylphenol (2008) Bull. Mt. Desert Isl. Biol. Lab. Salisb. Cove Maine, 47, pp. 56-57
  • Genovese, G., Da Cuña, R., Towle, D.W., Maggese, M.C., Lo Nostro, F., Early expression of zona pellucida proteins under octylphenol exposure in Cichlasoma dimerus (Perciformes, Cichlidae) (2011) Aquat. Toxicol., 101 (1), pp. 175-185
  • Gronen, S., Denslow, N., Manning, S., Barnes, S., Barnes, D., Brouwer, M., Serum vitellogenin levels and reproductive impairment of male Japanese medaka (Oryzias latipes) exposed to 4-tert-octylphenol (1999) Environ. Health Perspect., 107 (5), pp. 385-390
  • Hemmer, M.J., Bowman, C.J., Hemmer, B.L., Friedman, S.D., Marcovich, D., Kroll, K.J., Denslow, N.D., Vitellogenin mRNA regulation and plasma clearance in male sheepshead minnows, (Cyprinodon variegatus) after cessation of exposure to 17β-estradiol and p-nonylphenol (2002) Aquat. Toxicol., 58, pp. 99-112
  • Hiramatsu, N., Hara, A., Hiramatsu, K., Fukada, H., Weber, G.M., Denslow, N.D., Sullivan, C.V., Vitellogenin-derived yolk proteins of white perch, Morone americana: purification, characterization, and vitellogenin-receptor binding (2002) Biol. Reprod., 67, pp. 655-667
  • Hiramatsu, N., Matsubara, T., Fujita, T., Sullivan, C.V., Hara, A., Multiple piscine vitellogenins: biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments (2006) Mar. Biol., 149, pp. 35-47
  • Iguchi, T., Watanabe, H., Katsu, Y., Developmental effects of estrogenic agents on mice, fish, and frogs: a mini-review (2001) Horm. Behav., 40, pp. 248-251
  • , p. 2008. , IRAM, Calidad ambiental, Calidad del agua. Determinación de la toxicidad letal aguda de sustancias en peces de agua dulce. Método semiestático. IRAM 29112Islinger, M., Willimski, D., Völkl, A., Braunbeck, T., Effects of 17a-ethinylestradiol on the expression of three estrogen-responsive genes and cellular ultrastructure of liver and testes in male zebrafish (2003) Aquat. Toxicol., 62, pp. 85-103
  • Izquierdo-Rico, M.J., Jiménez-Movilla, M., Llop, E., Pérez-Oliva, A.B., Ballesta, J., Gutiérrez-Gallego, R., Jiménez-Cervantes, C., Avilés, M., Hamster zona pellucida is formed by tour glycoproteins: ZP1, ZP2, ZP3, and ZP4 (2009) J. Proteome Res., 8, pp. 926-941
  • Jayasundara, N., Towle, D.W., Weihrauch, D., Spanings-Pierrot, C., Gill-specific transcriptional regulation of Na +/K +-ATPase α-subunit in the euryhaline shore crab Pachygrapsus marmoratus: sequence variants and promoter structure (2007) J. Exp. Biol., 210, pp. 2070-2081
  • Jin, Y., Wang, W., Sheng, G.D., Liu, W., Fu, Z., Hepatic and extrahepatic expression of estrogen-responsive genes in male adult zebrafish (Danio rerio) as biomarkers of short-term exposure to 17β-estradiol (2008) Environ. Monit. Assess., 146, pp. 105-111
  • Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685
  • Lee, K.-H., Finnigan-Bunick, C., Bahr, J., Bunick, D., Estrogen regulation of ion transporter messenger RNA levels in mouse efferent ductules are mediated differentially through estrogen receptor (ER) α and ERβ (2001) Biol. Reprod., 65, pp. 1534-1541
  • Lewis, S.K., Lech, J.J., Uptake, disposition, and persistence of nonylphenol in rainbow trout (1996) Xenobiotica, 26, pp. 813-819
  • Li, A., Sadasivam, M., Ding, J.L., Receptor-ligand interaction between vitellogenin receptor (VtgR) and vitellogenin (Vtg), implications on low density lipoprotein receptor and apolipoprotein B/E (2003) J. Biol. Chem., 31, pp. 2799-2806
  • Lowry, O.M., Rosenbrough, N.J., Farr, L., Randall, R.J., Protein measurement with the phenol reagent (1951) J. Biol. Chem., 193, pp. 265-275
  • Maltais, D., Roy, R.L., Purification and partial characterization of vitellogenin from shorthead redhorse (Moxostoma macrolepidotum) and copper redhorse (Moxostoma hubbsi) and detection in plasma and mucus with a heterologous antibody (2009) Fish. Physiol. Biochem., 35, pp. 241-254
  • Martyniuk, C.J., Gerrie, E.R., Popesku, J.T., Ekker, M., Trudeau, V.L., Microarray analysis in the zebrafish (Danio rerio) liver and telencephalon after exposure to low concentration of 17alpha-ethinylestradiol (2007) Aquat. Toxicol., 84, pp. 38-49
  • Matsubara, T., Ohkubo, N., Andoh, T., Sullivan, C.V., 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 (1999) Dev. Biol., 213 (1), pp. 18-32
  • Mendiola, J., Torres-Cantero, A.M., Moreno-Grau, J.M., Ten, J., Roca, M., Moreno-Grau, S., Bernabeu, R., Food intake and its relationship with semen quality: a case-control study (2009) Fertil. Steril., 91 (3), pp. 812-818
  • Meucci, V., Arukwe, A., Detection of vitellogenin and zona radiate protein expressions in surface mucus of immature juvenile Atlantic salmon (Salmo salar) exposed to waterborne nonylphenol (2005) Aquat. Toxicol., 73, pp. 1-10
  • Modig, C., Westerlund, L., Olsson, P.E., Oocyte zona pellucida proteins (2007) The Fish Oocyte, from Basic Studies to Biotechnological Applications, pp. 113-140. , Springer, Dordrecht, P.J. Babin, J. Cerdà, E. Lubzens (Eds.)
  • Moncaut, N., Lo Nostro, F.L., Maggese, M.C., Vitellogenin detection in surface mucus of the South American cichlid fish Cichlasoma dimerus (Heckel, 1840) induced by estradiol-17β. Effects on liver and gonads (2003) Aquat. Toxicol., 63, pp. 127-137
  • Moncaut, N., Trichet, V., Betz, A., Le Pennec, J.P., Wolff, J., Characterization of vitellogenin from rainbow trout (Oncorhynchus mykiss) (1996) Gene, 174, pp. 59-64
  • Nelson, J.S., (2006) Fishes of the World, p. 622. , Wiley & Sons, Inc., New Jersey, USA
  • NIH (National Institute of Health) (2011), p. 220. , Guide for the care and use of laboratory animals. 8th ed. National Academy Press, WashingtonPedersen, R.T., Hill, E.M., Tissue distribution and depuration of 4-tert-octylphenol residues in the cyprinid fish, Scardinius erythrophthalmus (2002) Environ. Sci. Technol., 36, pp. 3275-3283
  • Pedersen, K.H., Pedersen, S.N., Pedersen, K.L., Korsgaard, B., Bjerregaard, P., Estrogenic effect of dietary 4-tert-octylphenol in rainbow trout (Oncorhynchus mykiss) (2003) Aquat. Toxicol., 62, pp. 295-303
  • Piazza, Y., Pandolfi, M., Lo Nostro, F., Effect of the organochlorine pesticide endosulfan on GnRH and gonadotrope cell populations in fish larvae (2011) Arch. Environ. Contam. Toxicol., 61 (2), pp. 300-310
  • Pressley, T.A., Phylogenetic conservation of isoform-specific regions within alpha-subunit of Na(+)-K(+)-ATPase (1992) Am. J. Physiol. Cell Physiol., 262 (3), pp. C743-C751
  • Reading, B.J., Hiramatsu, N., Sawaguchi, S., Matsubara, T., Hara, A., Lively, M.O., Sullivan, C.V., Conserved and variant molecular and functional features of multiple egg yolk precursor proteins (vitellogenins) in white perch (Morone americana) and other teleosts (2009) Mar. Biotechnol., 11, pp. 169-187
  • Reite, O.B., Evensen, Ø., Inflammatory cells of teleostean fish: a review focusing on mast cells/eosinophilic granule cells and rodlet cells (2006) Fish Shellfish Immunol., 20, pp. 192-208
  • Rey Vázquez, G., Meijide, F.J., Da Cuña, R.H., Lo Nostro, F.L., Piazza, Y.G., Babay, P.A., Trudeau, V.L., Guerrero, G.A., Exposure to waterborne 4-tert-octylphenol induces vitellogenin synthesis and disrupts testis morphology in the South American freshwater fish Cichlasoma dimerus (Teleostei, Perciformes) (2009) Comp. Biochem. Physiol. C, 150, pp. 298-306
  • Ribeiro, V.M.A., Bazzoli, N., Maria, T.A., Santos, G.B., Ultrastructural changes in female hepatocytes during ovarian maturation of Steindachnerina insculpta (Pisces: Curimatidae) (2006) Braz. J. Biol., 66, pp. 957-962
  • Robinson, C.D., Brown, E., Craft, J.A., Davies, I.M., Moffat, C.F., Effects of prolonged exposure to 4-tert-octylphenol on toxicity and indices of oestrogenic exposure in the sand goby (Pomatoschistus minutes, Pallas) (2004) Mar. Environ. Res., 58, pp. 19-38
  • Romano, M., Rosanova, P., Anteo, C., Limatola, E., Vertebrate yolk proteins: a review (2004) Mol. Reprod. Dev., 69, pp. 109-116
  • Rudel, R.A., Melly, S.J., Geno, P.W., Sun, G., Brody, J.G., Identification of alkylphenols and other estrogenic phenolic compounds in wastewater, septage, and groundwater on Cape Cod, Massachussetts (1998) Environ. Sci. Technol., 32, pp. 861-869
  • Saradha, B., Mathur, P.P., Effect of environmental contaminants on male reproduction (2006) Environ. Toxicol. Pharmacol., 22, pp. 90-96
  • Sawaguchi, S., Koya, Y., Yoshizaki, N., Ohkubo, N., Andoh, T., Hiramatsu, N., Sullivan, C.V., Matsubara, T., Multiple vitellogenins (Vgs) in mosquitofish (Gambusia affinis): identification and characterization of three functional Vg genes and their circulating and yolk protein products (2005) Biol. Reprod., 72, pp. 1045-1060
  • Spargo, S.C., Hope, R.M., Evolution and nomenclature of the zona pellucida gene family (2003) Biol. Reprod., 68, pp. 358-362
  • Seki, M., Yokota, H., Maeda, M., Tadokoro, H., Kobayashi, K., Effects of 4-nonylphenol and 4-tert-octylphenol on sex differentiation and vitellogenin induction in medaka (Oryzias latipes) (2003) Environ. Toxicol. Chem., 22 (7), pp. 1507-1516
  • Suzuki-Yagawa, Y., Kawakami, K., Nagano, K., Housekeeping Na, K-ATPase α 1 subunit gene promoter is composed of multiple cis elements to which common and cell type-specific factors bind (1992) Mol. Cell. Biol., 12, pp. 4046-4055
  • Tingaud-Sequeira, A., Knoll-Gellida, A., André, M., Babin, P.J., Vitellogenin expression in white adipose tissue in female teleost fish (2011) Biol. Reprod., (12). , October
  • Van den Belt, K., Wester, P.W., van der Ven, L.T., Verheyen, R., Witters, H., Effects of ethynylestradiol on the reproductive physiology in zebrafish (Danio rerio): time dependency and reversibility (2002) Environ. Toxicol. Chem., 21, pp. 767-775
  • Westerlund, L., Hyllner, S.J., Schopen, A., Olsson, P.E., Expression of three vitelline envelope protein genes in arctic char (2001) Gen. Comp. Endocrinol., 122, pp. 78-87
  • White, R., Jobling, S., Hoare, S.A., Sumpter, J.P., Parker, M.G., Environmentally persistent alkylphenolic compounds are estrogenic (1994) Endocrinology, 135, pp. 175-182
  • Woods, M., Kumar, A., Barton, M., Woods, A., Kookana, R., Localisation of estrogen responsive genes in the liver and testis of Murray rainbowfish Melanotaenia fluviatilis exposed to 17β-estradiol (2009) Mol. Cell. Endocrinol., 303, pp. 57-66
  • Wu, R.S.S., Siu, W.H.L., Shin, P.K.S., Induction, adaptation and recovery of biological responses: Implications for environmental monitoring (2005) Mar. Pollut. Bull., 51 (8-12), pp. 623-634
  • Yadetie, F., Arukwe, A., Goksøyr, A., Male, R., Induction of hepatic estrogen receptor in juvenil Atlantic salmon in vivo by the environmental estrogen, 4-nonylphenol (1999) Sci. Tot. Environ., 233, pp. 201-210
  • Zha, J., Sun, L., Zhou, Y., Spear, P.A., Ma, M., Wang, Z., Assessment of 17a-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow (Gobiocypris rarus) (2008) Toxicol. Appl. Pharmacol., 226, pp. 298-308

Citas:

---------- APA ----------
Genovese, G., Regueira, M., Piazza, Y., Towle, D.W., Maggese, M.C. & Lo Nostro, F. (2012) . Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol. Aquatic Toxicology, 114-115, 1-13.
http://dx.doi.org/10.1016/j.aquatox.2012.02.005
---------- CHICAGO ----------
Genovese, G., Regueira, M., Piazza, Y., Towle, D.W., Maggese, M.C., Lo Nostro, F. "Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol" . Aquatic Toxicology 114-115 (2012) : 1-13.
http://dx.doi.org/10.1016/j.aquatox.2012.02.005
---------- MLA ----------
Genovese, G., Regueira, M., Piazza, Y., Towle, D.W., Maggese, M.C., Lo Nostro, F. "Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol" . Aquatic Toxicology, vol. 114-115, 2012, pp. 1-13.
http://dx.doi.org/10.1016/j.aquatox.2012.02.005
---------- VANCOUVER ----------
Genovese, G., Regueira, M., Piazza, Y., Towle, D.W., Maggese, M.C., Lo Nostro, F. Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol. Aquat. Toxicol. 2012;114-115:1-13.
http://dx.doi.org/10.1016/j.aquatox.2012.02.005