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Beijer, K., Jönsson, M., Shaik, S., Behrens, D., Brunström, B. & Brandt, I. (2018). Azoles additively inhibit cytochrome P450 1 (EROD) and 19 (aromatase) in rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology, 198, 73-81
Open this publication in new window or tab >>Azoles additively inhibit cytochrome P450 1 (EROD) and 19 (aromatase) in rainbow trout (Oncorhynchus mykiss)
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2018 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 198, p. 73-81Article in journal (Refereed) Published
Abstract [en]

Antifungal azoles are widely used in medicine, agriculture, and material protection and several antifungal azoles have been found in environmental samples. Although these compounds were designed to inhibit fungal enzymes such as lanosterol-14-demethylase (cytochrome P450 (CYP) 51), it is well established that the inhibitory actions of azoles are not specific for fungal CYP isozymes.

We refined a gill filament assay to determine the inhibition of CYP1, measured as reduced 7-ethoxyresorufin-O-deethylase (EROD) activity, in rainbow trout (Oncorhynchus mykiss) gill tissue ex vivo. The advantage of this method is that both induction and inhibition of EROD are performed ex vivo. Among thirteen azoles studied, the five that caused the strongest inhibition of gill EROD activity at a concentration of 5 μM were selected for concentration–response assessment. These compounds (bifonazole, clotrimazole, imazalil, miconazole, and prochloraz) showed IC50 values ranging from 0.1 to 1.5 μM. CYP19 (aromatase) inhibition was measured using microsomes from rainbow trout brains. Concentration-response curves for CYP19 inhibition were determined for letrozole, bifonazole, clotrimazole, imazalil, miconazole and prochloraz, which gave IC50 values ranging from 0.02 to 3.3 μM. It was further found that mixtures of the five most potent azoles reduced both CYP1 and 19 catalytic activity in an additive fashion (IC50 = 0.7 μM and 0.6 μM, in the respective assay). Bifonazole (IC50 = 0.1 μM) is not previously known to inhibit CYP1 activity.

The additive inhibition of CYP1 and CYP19 catalytic activity is an important finding of the present study. We conclude that this additive action of azoles could mediate adverse impacts on CYP regulated physiological functions in environmentally exposed fish.

Keywords
Azole fungicide, EROD activity, cytochrome P450 (CYP), CYP1A, CYP19, aromatase, pharmaceutical, contaminant, chemical, fish, rainbow trout, gill, EROD aktivitet, cytokrom P450 (CYP), CYP1A, CYP19, aromatase, läkemedel, azol, fungicid, kemikalier, förorening, fisk, regnbågslax, gäle
National Category
Other Biological Topics
Research subject
Biology with specialization in Environmental Toxicology
Identifiers
urn:nbn:se:uu:diva-249010 (URN)10.1016/j.aquatox.2018.02.016 (DOI)000430630100008 ()
Funder
Mistra - The Swedish Foundation for Strategic Environmental Research
Available from: 2015-04-15 Created: 2015-04-10 Last updated: 2018-08-07Bibliographically approved
Mattsson, A. & Brunström, B. (2017). Effects of selective and combined activation of estrogen receptor α and β on reproductive organ development and sexual behaviour in Japanese quail (Coturnix japonica). PLoS ONE, 12(7), Article ID e0180548.
Open this publication in new window or tab >>Effects of selective and combined activation of estrogen receptor α and β on reproductive organ development and sexual behaviour in Japanese quail (Coturnix japonica)
2017 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 12, no 7, article id e0180548Article in journal (Refereed) Published
Abstract [en]

Excess estrogen exposure of avian embryos perturbs reproductive organ development in both sexes and demasculinizes the reproductive behaviors of adult males. We have previously shown that these characteristic effects on the reproductive organs also can be induced by exposure of Japanese quail (Coturnix japonica) embryos to selective agonists of estrogen receptor alpha (ER alpha). In contrast, the male copulatory behavior is only weakly affected by developmental exposure to an ERa agonist. To further elucidate the respective roles of ER alpha and ER beta in estrogen-induced disruption of sexual differentiation, we exposed Japanese quail embryos in ovo to the selective ER alpha agonist 16 alpha-lactone-estradiol (16 alpha LE2), the selective ER beta agonist WAY-200070, or both substances in combination. The ERa agonist feminized the testes in male embryos and reduced cloacal gland size in adult males. Furthermore, anomalous retention and malformations of the Mullerian ducts/oviducts were seen in embryos and juveniles of both sexes. The ER beta agonist did not induce any of these effects and did not influence the action of the ERa agonist. Male copulatory behavior was not affected by embryonic exposure to either the ER alpha-or the ER beta-selective agonist but was slightly suppressed by treatment with the two compounds combined. Our results suggest that the reproductive organs become sexually differentiated consequent to activation of ER alpha by endogenous estrogens; excessive activation of ER alpha, but not ER beta, during embryonic development may disrupt this process. Our results also suggest that the demasculinizing effect of estrogens on male copulatory behavior is only partly mediated by ER alpha and ER beta, and may rather involve other estrogen-responsive pathways.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2017
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-331244 (URN)10.1371/journal.pone.0180548 (DOI)000405268500063 ()28671963 (PubMedID)
Funder
Swedish Research Council Formas, 2016-20128 99
Available from: 2017-10-19 Created: 2017-10-19 Last updated: 2017-11-29Bibliographically approved
Beijer, K., Björlenius, B., Shaik, S., Lindberg, R. H., Brunström, B. & Brandt, I. (2017). Removal of pharmaceuticals and unspecified contaminants in sewage treatment effluents by activated carbon filtration and ozonation: Evaluation using biomarker responses and chemical analysis. Chemosphere, 176, 342-351
Open this publication in new window or tab >>Removal of pharmaceuticals and unspecified contaminants in sewage treatment effluents by activated carbon filtration and ozonation: Evaluation using biomarker responses and chemical analysis
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2017 (English)In: Chemosphere, ISSN 0045-6535, E-ISSN 1879-1298, Vol. 176, p. 342-351Article in journal (Refereed) Published
Abstract [en]

Traces of active pharmaceutical ingredients (APIs) and other chemicals are demonstrated in effluents from sewage treatment plants (STPs) and they may affect quality of surface water and eventually drinking water. Treatment of effluents with granular activated carbon (GAC) or ozone to improve removal of APIs and other contaminants was evaluated at two Swedish STPs, Kappala and Uppsala (88 and 103 APIs analyzed). Biomarker responses in rainbow trout exposed to regular and additionally treated effluents were determined. GAC and ozone treatment removed 87-95% of the total concentrations of APIs detected. In Kappala, GAC removed 20 and ozonation (7 g O-3/m(3)) 21 of 24 APIs detected in regular effluent. In Uppsala, GAC removed 25 and ozonation (5.4 g O-3/m(3)) 15 of 25 APIs detected in effluent. GAC and ozonation also reduced biomarker responses caused by unidentified pollutants in STP effluent water. Elevated ethoxyresorufin-O-deethylase (EROD) activity in gills was observed in fish exposed to effluent in both STPs. Gene expression analysis carried out in Kappala showed increased concentrations of cytochrome P450 (CYP1A5 and CYP1C3) transcripts in gills and of CYP1As in liver of fish exposed to effluent. In fish exposed to GAC- or ozone-treated effluent water, gill EROD activity and expression of CYP1As and CYP1C3 in gills and liver were generally equal to or below levels in fish held in tap water. The joint application of chemical analysis and sensitive biomarkers proved useful for evaluating contaminant removal in STPs with new technologies.

Keywords
Wastewater, Activated carbon, Ozonation, Pharmaceuticals, Biomarkers, Rainbow trout
National Category
Environmental Sciences Environmental Biotechnology
Identifiers
urn:nbn:se:uu:diva-322509 (URN)10.1016/j.chemosphere.2017.02.127 (DOI)000399849300039 ()28273541 (PubMedID)
Funder
Mistra - The Swedish Foundation for Strategic Environmental Research
Note

De 2 första författarna delar förstaförfattarskapet.

Available from: 2017-05-30 Created: 2017-05-30 Last updated: 2017-05-30Bibliographically approved
Jönsson, M. E., Mattsson, A., Shaik, S. & Brunström, B. (2016). Toxicity and cytochrome P450 1A mRNA induction by 6-formylindolo[3,2-b]carbazole (FICZ) in chicken and Japanese quail embryos. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 179, 125-136
Open this publication in new window or tab >>Toxicity and cytochrome P450 1A mRNA induction by 6-formylindolo[3,2-b]carbazole (FICZ) in chicken and Japanese quail embryos
2016 (English)In: Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, ISSN 1532-0456, E-ISSN 1878-1659, Vol. 179, p. 125-136Article in journal (Refereed) Published
Abstract [en]

The tryptophan derivative formylindolo[3,2-b]carbazole (FICZ) binds with high ligand affinity to the aryl hydrocarbon receptor (AHR) and is readily degraded by AHR-regulated cytochrome P450 family 1 (CYP1) enzymes. Whether in vivo exposure to FICZ can result in toxic effects has not been examined and the main objective of this study was to determine if FICZ is embryotoxic in birds. We examined toxicity and CYP1 mRNA induction of FICZ in embryos from chicken (Gallus domesticus) and Japanese quail (Coturnix japonica) exposed to FICZ (2200 jag kg(-1)) by yolk and air sac injections. FICZ caused liver toxicity, embryo mortality, and CYP1A4 and CYP1A5 induction in both species with similar potency. This is in stark contrast to the very large difference in sensitivity of these species to halogenated AHR agonists. We also exposed chicken embryos to a low dose of FICZ (4 mu g kg(-1)) in combination with a CYP inhibitor, ketoconazole (KCZ). The mixture of FICZ and KCZ was lethal while FICZ alone had no effect at 4 mu g kg(-1). Furthermore, mixed exposure to FICZ and KCZ caused stronger and more long-lasting hepatic CYP1A4 induction than exposure to each compound alone. These findings indicate reduced biotransformation of FICZ by co-treatment with KCZ as a cause for the enhanced effects although additive AHR activation is also possible. To conclude, FICZ is toxic to bird embryos and it seems reasonable that the toxicity by FICZ involves AHR activation. However, the molecular targets and biological events leading to hepatic damage and mortality are unknown.

Keywords
Formylindolo[3, 2-b]carbazole (FICZ), Cytochrome P450 1 (CYP1), Chicken, Japanese quail, Embryo toxicity, Liver necrosis
National Category
Ecology Pharmacology and Toxicology
Identifiers
urn:nbn:se:uu:diva-274425 (URN)10.1016/j.cbpc.2015.09.014 (DOI)000366873300016 ()26456929 (PubMedID)
Funder
Swedish Research Council Formas, 216-2008-1249Carl Tryggers foundation , CTS 12:227
Available from: 2016-01-21 Created: 2016-01-21 Last updated: 2018-01-10Bibliographically approved
Agerstrand, M., Berg, C., Bjorlenius, B., Breitholtz, M., Brunström, B., Fick, J., . . . Ruden, C. (2015). Improving Environmental Risk Assessment of Human Pharmaceuticals. Environmental Science and Technology, 49(9), 5336-5345
Open this publication in new window or tab >>Improving Environmental Risk Assessment of Human Pharmaceuticals
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2015 (English)In: Environmental Science and Technology, ISSN 0013-936X, E-ISSN 1520-5851, Vol. 49, no 9, p. 5336-5345Article in journal (Refereed) Published
Abstract [en]

This paper presents 10 recommendations for improving the European Medicines Agency's guidance for environmental risk assessment of human pharmaceutical products. The recommendations are based on up-to-date, available science in combination with experiences from other chemical frameworks such as the REACH-legislation for industrial chemicals. The recommendations concern: expanding the scope of the current guideline; requirements to assess the risk for development of antibiotic resistance; jointly performed assessments; refinement of the test proposal; mixture toxicity assessments on active pharmaceutical ingredients with similar modes of action; use of all available ecotoxicity studies; mandatory reviews; increased transparency; inclusion of emission data from production; and a risk management option. We believe that implementation of our recommendations would strengthen the protection of the environment and be beneficial to society. Legislation and guidance documents need to be updated at regular intervals in order to incorporate new knowledge from the scientific community. This is particularly important for regulatory documents concerning pharmaceuticals in the environment since this is a research field that has been growing substantially in the last decades.

National Category
Environmental Sciences Pharmacology and Toxicology
Identifiers
urn:nbn:se:uu:diva-256532 (URN)10.1021/acs.est.5b00302 (DOI)000354155800012 ()25844810 (PubMedID)
Available from: 2015-06-26 Created: 2015-06-24 Last updated: 2018-01-11Bibliographically approved
Mattsson, A., Kärrman, A., Pinto, R. & Brunström, B. (2015). Metabolic Profiling of Chicken Embryos Exposed to Perfluorooctanoic Acid ( PFOA) and Agonists to Peroxisome Proliferator-Activated Receptors. PLoS ONE, 10(12), Article ID e0143780.
Open this publication in new window or tab >>Metabolic Profiling of Chicken Embryos Exposed to Perfluorooctanoic Acid ( PFOA) and Agonists to Peroxisome Proliferator-Activated Receptors
2015 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 10, no 12, article id e0143780Article in journal (Refereed) Published
Abstract [en]

Untargeted metabolic profiling of body fluids in experimental animals and humans exposed to chemicals may reveal early signs of toxicity and indicate toxicity pathways. Avian embryos develop separately from their mothers, which gives unique possibilities to study effects of chemicals during embryo development with minimal confounding factors from the mother. In this study we explored blood plasma and allantoic fluid from chicken embryos as matrices for revealing metabolic changes caused by exposure to chemicals during embryonic development. Embryos were exposed via egg injection on day 7 to the environmental pollutant perfluorooctanoic acid (PFOA), and effects on the metabolic profile on day 12 were compared with those caused by GW7647 and rosiglitazone, which are selective agonists to peroxisome-proliferator activated receptor a (PPAR alpha) and PPAR gamma, respectively. Analysis of the metabolite concentrations from allantoic fluid by Orthogonal Partial Least Squares Discriminant Analysis (OPLS-DA) showed clear separation between the embryos exposed to GW7647, rosiglitazone, and vehicle control, respectively. In blood plasma only GW7647 caused a significant effect on the metabolic profile. PFOA induced embryo mortality and increased relative liver weight at the highest dose. Sublethal doses of PFOA did not significantly affect the metabolic profile in either matrix, although single metabolites appeared to be altered. Neonatal mortality by PFOA in the mouse has been suggested to be mediated via activation of PPAR alpha. However, we found no similarity in the metabolite profile of chicken embryos exposed to PFOA with those of embryos exposed to PPAR agonists. This indicates that PFOA does not activate PPAR pathways in our model at concentrations in eggs and embryos well above those found in wild birds. The present study suggests that allantoic fluid and plasma from chicken embryos are useful and complementary matrices for exploring effects on the metabolic profile resulting from chemical exposure during embryonic development.

National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-272138 (URN)10.1371/journal.pone.0143780 (DOI)000365891600050 ()
Funder
Swedish Research Council Formas, 216-2012-899
Available from: 2016-01-12 Created: 2016-01-12 Last updated: 2017-11-30Bibliographically approved
Uebbing, S., Konzer, A., Xu, L., Backström, N., Brunström, B., Bergquist, J. & Ellegren, H. (2015). Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken. Molecular biology and evolution, 32(10), 2716-2725
Open this publication in new window or tab >>Quantitative Mass Spectrometry Reveals Partial Translational Regulation for Dosage Compensation in Chicken
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2015 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 10, p. 2716-2725Article in journal (Refereed) Published
Abstract [en]

There is increasing evidence that dosage compensation is not a ubiquitous feature following sex chromosome evolution, especially not in organisms where females are the heterogametic sex, like in birds. Even when it occurs, compensation can be incomplete and limited to dosage-sensitive genes. However, previous work has mainly studied transcriptional regulation of sex-linked genes, which may not reflect expression at the protein level. Here, we used liquid chromatography–tandem mass spectrometry to detect and quantify expressed levels of more than 2,400 proteins in ten different tissues of male and female chicken embryos. For comparison, transcriptome sequencing was performed in the same individuals, five of each sex. The proteomic analysis revealed that dosage compensation was incomplete, with a mean male-to-female (M:F) expression ratio of Z-linked genes of 1.32 across tissues, similar to that at the RNA level (1.29). The mean Z chromosome-to-autosome expression ratio was close to 1 in males and lower than 1 in females, consistent with partly reduced Z chromosome expression in females. Although our results exclude a general mechanism for chromosome-wide dosage compensation at translation, 30% of all proteins encoded from Z-linked genes showed a significant change in the M:F ratio compared with the corresponding ratio at the RNA level. This resulted in a pattern where some genes showed balanced expression between sexes and some close to 2-fold higher expression in males. This suggests that proteomic analyses will be necessary to reveal a more complete picture of gene regulation and sex chromosome evolution.

Keywords
sex chromosome evolution, dosage compensation, chicken, proteomics, mass spectrometry
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-258796 (URN)10.1093/molbev/msv147 (DOI)000361987100019 ()26108680 (PubMedID)
Funder
Swedish Research Council, 2010-5650, 2013-8271, 2011-4423EU, European Research Council, AdG 249976Knut and Alice Wallenberg Foundation
Available from: 2015-07-20 Created: 2015-07-20 Last updated: 2018-02-22Bibliographically approved
Svensson, J., Fick, J., Brandt, I. & Brunström, B. (2014). Environmental concentrations of an androgenic progestin disrupts the seasonal breeding cycle in male three-spined stickleback (Gasterosteus aculeatus). Aquatic Toxicology, 147, 84-91
Open this publication in new window or tab >>Environmental concentrations of an androgenic progestin disrupts the seasonal breeding cycle in male three-spined stickleback (Gasterosteus aculeatus)
2014 (English)In: Aquatic Toxicology, ISSN 0166-445X, E-ISSN 1879-1514, Vol. 147, p. 84-91Article in journal (Refereed) Published
Abstract [en]

Synthetic steroid hormones from contraceptive pharmaceuticals have become global aquatic contaminants. Progestins, the synthetic analogs to progesterone, are receiving increasing attention as contaminants and have been shown to impair reproduction in fish and amphibians at low ng L-1 concentrations. Certain progestins, such as levonorgestrel have androgenic properties and seem to be several orders of magnitude more potent in terms of reproductive impairment in fish than non-androgenic progestins and progestagens. We recently reported that levonorgestrel has strong androgenic effects in female three-spined sticklebacks (Gasterosteus aculeatus), including induction of the normally male-specific glue protein spiggin and suppression of vitellogenesis. In light of this we investigated if exposure to levonorgestrel could disrupt the highly androgen-dependent seasonal reproductive cycle in male sticklebacks. Male sticklebacks that were in the final stage of a breeding period were exposed to various concentrations of levonorgestrel for six weeks in winter conditions in terms of light and temperature, after which reproductive status was evaluated from gross morphology, histology and key gene transcript levels. During the experimental period the controls had transitioned from full breeding condition into the non-breeding state, including regression of secondary sex characteristics, cessation of spiggin production in the kidney, and resumption of spermatogenesis in the testes. This is ascribed to the natural drop in plasma androgen levels after breeding. However, in the groups concurrently exposed to levonorgestrel, transition to the non-breeding condition was dose-dependently inhibited. Our results show that levonorgestrel can disrupt the seasonal breeding cycle in male sticklebacks. The fitness costs of such an effect could be detrimental to natural stickleback populations. Some effects occurred at a levonorgestrel concentration of 6.5 ng L-1, well within the range of levonorgestrel levels in surface waters and may therefore occur in progestin-contaminated waters. Furthermore, the effects by levonorgestrel in the present study were likely mediated mainly by its androgenic activity, and the low concentration at which they occurred makes levonorgestrel one of the most potent androgenic contaminants known.

Keywords
Levonorgestrel, Progestins, Three-spined stickleback, Androgen, Reproductive cycle
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-221976 (URN)10.1016/j.aquatox.2013.12.013 (DOI)000331856600011 ()
Available from: 2014-04-08 Created: 2014-04-07 Last updated: 2017-12-05Bibliographically approved
Jönsson, M., Shaik, S., Rannug, A. & Brunström, B. (2013). Developmental effects of 6-formyl-indolo[3,2-b]carbazole in birds. In: Toxicology Letters: . Paper presented at Society of Toxicology, 52nd Annual Meeting and ToxExpo, March 10–14, 2013, San Antonio, Texas, USA (pp. 68). UK: Oxford University Press
Open this publication in new window or tab >>Developmental effects of 6-formyl-indolo[3,2-b]carbazole in birds
2013 (English)In: Toxicology Letters, UK: Oxford University Press, 2013, p. 68-Conference paper, Poster (with or without abstract) (Refereed)
Place, publisher, year, edition, pages
UK: Oxford University Press, 2013
National Category
Developmental Biology
Identifiers
urn:nbn:se:uu:diva-215099 (URN)
Conference
Society of Toxicology, 52nd Annual Meeting and ToxExpo, March 10–14, 2013, San Antonio, Texas, USA
Available from: 2014-01-10 Created: 2014-01-10 Last updated: 2014-01-10Bibliographically approved
Beijer, K., Gao, K., Jönsson, M. E., Larsson, D. G., Brunström, B. & Brandt, I. (2013). Effluent from drug manufacturing affects cytochrome P450 1 regulation and function in fish. Chemosphere, 90(3), 1149-1157
Open this publication in new window or tab >>Effluent from drug manufacturing affects cytochrome P450 1 regulation and function in fish
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2013 (English)In: Chemosphere, ISSN 0045-6535, E-ISSN 1879-1298, Vol. 90, no 3, p. 1149-1157Article in journal (Refereed) Published
Abstract [en]

We have previously reported very high concentrations of pharmaceuticals in the effluent from a treatment plant receiving wastewater from about 90 bulk drug manufacturers near Hyderabad, India. The main objective of the present study was to examine how high dilutions of this effluent affect mRNA expression of cytochrome P450 (CYP) 1 family genes and ethoxyresorufin O-deethylase (EROD) activity in exposed wildlife, using the three-spined stickleback (Gasterosteus aculeatus) as a model. In gill filaments exposed to diluted effluent ex vivo, EROD activity was strongly inhibited in a concentration-dependent manner. In a subsequent in vivo study, groups of fish were exposed (24. h) to three concentrations of effluent, 0.8%, 1.6% or 3.2%. In this experiment, EROD in gills was induced 27-, 52- or 60-fold, respectively. Accordingly, CYP1A mRNA was markedly up-regulated in gill, liver and brain of fish exposed to all three effluent concentrations. Expression of mRNA for CYP1B1 and CYP1C1 was induced in gills at all concentrations while effects on these genes in liver and brain were weak or absent. The results of a time course study suggested that most CYP1-inducing substances in the effluent were readily metabolised or excreted, because the induced EROD activity and mRNA expression decreased when the fish were transferred to clean water. Considering that CYP1 enzymes play important roles in biotransformation of endogenous and foreign compounds, the observed dual effect of the effluent on CYP1 catalytic activity and mRNA expression suggests that multiple physiological functions could be affected in exposed wildlife.

Keywords
CYP1, EROD, Gills, Pharmaceuticals, Three-spined stickleback, Treated wastewater, Drug products, Effluent treatment, Fish, Gene expression, Wastewater treatment, Effluents, cytochrome P450, cytochrome P450 1, cytochrome P450 1A, cytochrome P450 1B1, cytochrome P450 1C1, cytochrome P450 1C2, ethoxyresorufin deethylase, industrial effluent, messenger RNA, tap water, unclassified drug, biotransformation, concentration (composition), drug, ecological modeling, effluent, enzyme activity, manufacturing, metabolism, pollution exposure, teleost, wastewater, water treatment, animal experiment, animal tissue, article, brain, controlled study, enzyme induction, enzyme inhibition, female, Gasterosteus aculeatus, gene, genetic transcription, gill, liver, mortality, nonhuman, spiggin gene, upregulation, vitellogenin gene, waste water treatment plant, Andhra Pradesh, Hyderabad [Andhra Pradesh], India
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-192012 (URN)10.1016/j.chemosphere.2012.09.023 (DOI)000312978700035 ()
Note

De två första författarna delar förstaförfattarskapet.

Available from: 2013-01-24 Created: 2013-01-15 Last updated: 2017-12-06Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-4590-1211

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