The antidepressant drug Carbamazepine induces differential transcriptome expression in the brain of Atlantic salmon, Salmo salar

Aquatic Toxicology

Volumn 151, Issue , 2014, Pages 114-123

  Hampel, M ^a,b   Bron, J E ^a   Taggart, J B ^a   Leaver, M J ^a  

^a UNIVERSITY OF STIRLING   (United Kingdom)

^b INSTITUTO DE CIENCIAS MARINAS DE ANDALUCÍA   (Spain)

Author keywords

Atlantic salmon; Carbamazepine; CDNA; Functional enrichment and network analysis; Pituitary hormones; Transcriptome expression

Indexed keywords

ALPHA6 INTEGRIN; CARBAMAZEPINE; COMPLEMENTARY DNA; GROWTH HORMONE; HYPOPHYSIS HORMONE; MESSENGER RNA; PROLACTIN; SOMATOLACTIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

BIOACCUMULATION; BRAIN; DRUG; ENVIRONMENTAL EFFECT; GENE EXPRESSION; HORMONE; NETWORK ANALYSIS; PHYSIOLOGY; RNA; SALMONID; SUBLETHAL EFFECT; TOXICITY;

ADAPTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; AQUATIC ENVIRONMENT; ARTICLE; ATLANTIC SALMON; BINDING AND RELATED PHENOMENA; BIOINFORMATICS; CHROMATIN BINDING; COMPARATIVE STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EFFLUENT; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT; EXTRACELLULAR MATRIX; FOCAL ADHESION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; HEME SYNTHESIS; HORMONE ACTION; HOSPITAL WASTE; JUVENILE ANIMAL; LIMIT OF DETECTION; MALE; MOLECULAR INTERACTION; NEGATIVE FEEDBACK; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; UPREGULATION; WATER POLLUTION;

SALMO SALAR;

ATLANTIC SALMON; CARBAMAZEPINE; CDNA; FUNCTIONAL ENRICHMENT AND NETWORK ANALYSIS; PITUITARY HORMONES; TRANSCRIPTOME EXPRESSION;

ANIMALS; BRAIN; CARBAMAZEPINE; GENE EXPRESSION PROFILING; SALMO SALAR; TRANSCRIPTOME; WATER POLLUTANTS, CHEMICAL;

EID: 84899488354     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.12.018     Document Type: Article

References (86)

1. Ágústsson T., Sundell K., Sakamoto T., Ando M., Björnsson B.T. Pituitary gene expression of somatolactin, prolactin, and growth hormone during Atlantic salmon parr-smolt transformation. Aquaculture 2003, 222:229-238.
2. Ambrosio A.F., Soares-da-Silva P., Carvalho C.M., Carvalho A.P. Mechanisms of action of Carbamazepine and its derivatives, oxcarbazepine, BIA 2-093, and BIA 2-024. Neurochem. Res. 2002, 27(1-2):121-130.
3. Ashton D., Hilton M., Thomas K.V. Investigating the environmental transport of human pharmaceuticals to streams in the United Kingdom. Sci. Total Environ. 2004, 333:167-184.
4. Auperin B., Rentier-Delrue F., Martial J.A., Prunet P. Regulation of gill prolactin receptors in tilapia (Oreochromis mossambicus) after a change in salinity or hypophysectomy. J. Endocrinol. 1995, 145:213-220.
5. Avella M., Schreck C.B., Prunet P. Plasma prolactin and cortisol concentrations of stressed coho salmon Oncorhynchus kisutch, in fresh water or salt water. Gen. Comp. Endocrinol. 1991, 81:21-27.
6. Bendz D., Paxéus N.A., Ginn T.R., Loge F.J. Occurrence and fate of pharmaceutically active compounds in the environment, a case study: Höje River in Sweden. J. Hazard. Mater. 2005, 122:195-204.
7. Beutler A.S., Li S., Nicol R., Walsh M.J. Carbamazepine is an inhibitor of histone deacetylases. Life Sci. 2005, 76:3107-3115.
8. Brazma A., Hingamp P., Quackenbush J., Sherlock G., Spellman P., et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat. Genet. 2001, 29(4):365-371.
9. Buser H.R., Mullere M.D., Theobald N. Occurrence of the pharmaceutical clofibric acid and the herbicide mecoprop in various Swiss Lakes and in the North Sea. Environ. Sci. Technol. 1998, 32:188-192.
10. Chen G., Pan B., Hawver D.B., Wright C.B., Potter W.Z., Manji H.K. Attenuation of cyclic AMP production by carbamazepine. J. Neurochem. 1996, 67:2079-2086.
11. Crane M., Watts C., Boucard T. Chronic aquatic environmental risks from exposure to human pharmaceuticals. Sci. Total Environ. 2006, 367:23-41.
12. Danielson P.B. The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr. Drug Metab. 2002, 3(6):561-597.
13. Disler P.B., Blekkenhorst G.H., Fates L., Moore M.R., Straughan J. S. Afr. Med. J. 1982, 61:656.
14. Dufau M.L., Liao M., Zhang Y. Participation of signaling pathways in the derepression of luteinizing hormone receptor transcription. Mol. Cell. Endocrinol. 2010, 314(2):221-227.
15. Eckey M., Moehren U., Baniahmad A. Gene silencing by the thyroid hormone receptor. Mol. Cell. Endocrinol. 2003, 213:13-22.
16. Directive, 2004/27/EC of the European Parliament and of the Council of 31 March 2004 amending Directive 2001/83/EC on the Community code relating to medicinal products for human use. Article 1. Published March 31, 2004.
17. Elonen G.E., Spehar R.L., Holcombe G.W., Johnson R.D., Fernandez J.D., Erickson R.J., Tietge J.E., Cook P.M. Comparative toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to seven freshwater fish species during early life-stage development. Environ. Toxicol. Chem. 1998, 17:472-483.
18. Fukamachi S., Yada T., Meyer A., Kinoshita M. Effects of constitutive expression of somatolactin alpha on skin pigmentation in medaka. Gene 2009, 442(1-2):81-87.
19. Fukamachi S., Sugimoto M., Mitani H., Shima A. Somatolactin selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10661-10666.
20. Gómez M.J., Martínez Bueno M.J., Lacorte S., Fernández-Alba A.R., Agüera A. Pilot survey monitoring pharmaceuticals and related compounds in a sewage treatment plant located on the Mediterranean coast. Chemosphere 2007, 66:993-1002.
21. Hagenaars A., Knapen D., Meyer I.J., van der Ven K., Hoff P., De Coen W. Toxicity evaluation of perfluorooctane sulfonate (PFOS) in the liver of common carp (Cyprinus carpio). Aquat. Toxicol. 2008, 88(3):155-163.
22. Hampel M., Alonso E., Aparicio I., Bron J.E., Santos J.L., Taggart J.B., Leaver M.J. Potential physiological effects of pharmaceutical compounds in Atlantic salmon (Salmo salar), implied by transcriptomic analysis. Env. Sci. Pollut. Res. 2010, 17(4):917-923.
23. Hansson M.C., Hahn M.E. Functional properties of the four Atlantic salmon (Salmo salar) aryl hydrocarbon receptor type 2 (AHR2) isoforms. Aquat. Toxicol. 2008, 86:121-130.
24. Heckert L.L. Structure and Regulation of the FSH Receptor Gene. Sertoli Cell Biol 2005, 281-299.
25. Hintermann E., Quaranta V. Epithelial cell motility on laminin-5: regulation by matrix assembly, proteolysis, integrins and erbB receptors. Matrix Biol. 2004, 23(2):75-85.
26. Hobara T., Uchida S., Otsuki K., Matsubara T., Funato H., Matsuo K., Suetsugi M., Watanabe Y. Altered gene expression of histone deacetylases in mood disorder patients. J. Psychiat. Res. 2010, 44(5):263-270.
27. Jamers A., van der Ven K., Moens L., Robbens J., Potters G., Guisez Y., Blust R., De Coen W. Effect of copper exposure on gene expression profiles in Chlamydomonas reinhardtii based on microarray analysis. Aquat. Toxicol. 2006, 80(3):249-260.
28. Jensen J.B., Mørk A. Altered protein phosphorylation in the rat brain following chronic lithium and Carbamazepine treatments. Eur. Neuropsychopharm. 1997, 7(3):173-179.
29. Jones K.A. (1996) Summation of basic endocrine data. Handbook of Endocrinology 1996, 1-42. CRC Press, New York, NY. 2nd ed. G.H. Gass, H.M. Kaplan (Eds.).
30. Jordal A.E.O., Torstensen B.E., Tsoi S., Tocher D.R., Lall S.P., Douglas S.E. Dietary rapeseed oil affects the expression of genes involved in hepatic lipid metabolism in Atlantic salmon (Salmo salar L.). J. Nutr. 2005, 135:2355-2361.
31. Jørgensen S.M., Afanasyev S., Krasnov A. Gene expression analyses in Atlantic salmon challenged with infectious salmon anemia virus reveal differences between individuals with early intermediate and late mortality. BMC Genomics 2008, 9:179-185.
32. Kanehisa M., Goto S., Kawashima S., Nakaya A. The KEGG databases at GenomeNet. Nucleic Acids Res. 2002, 30(1):42-46.
33. Kaneko T. Cell biology of somatolactin. Int. Rev. Cytol. 1996, 169:1-24.
34. Kakizawa S., Kaneko T., Hirano T. Elevation of plasma somatolactin concentrations during acidosis in rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 1996, 199:1043-1051.
35. Kaplan B.H. Synthesis of heme. Hematology 1977, 287-294. McGraw-Hill, New York. 2nd ed. W.J. Williams, E. Beutler, A.J. Erslev, R. Wayne (Eds.).
36. Kolpin D.W., Furlong E.T., Meyer M.T., Thurman E.M., Zaugg S.D., Barber L.B., Buxton H.T. Pharmaceuticals, hormones, and other organic wastewater contaminants in US streams 1999-2000: a national reconnaissance. Environ. Sci. Technol. 2002, 36:1202-1211.
37. Koumanova B. 2006 Fate of chemicals in the aquatic environment. NATO Security through Science Series 2006, 93-103.
38. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
39. Kümmerer K. Pharmaceuticals in the environment Emission of pharmaceuticals, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources-a review. Chemosphere 2001, 45:957-969.
40. Kümmerer Pharmaceuticals in the Environment. Annu. Rev. Environ. Resour. 2010, 35:57-75.
41. Leaver M.J., Villeneuve L.A.N., Obach A., Jensen L., Bron J.E., Tocher D.R., Taggart J.B. Functional genomics reveals increases in cholesterol biosynthetic genes and highly unsaturated fatty acid biosynthesis after dietary substitution of fish oil with vegetable oils in Atlantic salmon (Salmo salar). BMC Genomics 2008, 9:299-314.
42. Leaver M.J., Diab A., Boukouvala E., Williams T.D., Chipman J.K., Moffat C.F., Robinson C.D., George S.G. Hepatic gene expression in flounder chronically exposed to multiply polluted estuarine sediment Absence of classical exposure 'biomarker' signals and induction of inflammatory, innate immune and apoptotic pathways. Aquat. Toxicol. 2010, 96:234-245.
43. Lee H.J., Rao J.S., Rapoport S.I., Bazinet R.P. Antimanic therapies target brain arachidonic acid signaling Lessons learned about the regulation of brain fatty acid metabolism. Prostaglandins Leukot. Essent. Fatty Acid 2007, 77:239-246.
44. Lin A.Y., Yu T., Lin C. Pharmaceutical contamination in residential, industrial, and agricultural waste streams risk to aqueous environments in Taiwan. Chemosphere 2008, 74:131-141.
45. López-Rodas G., Brosch G., Georgieva E.I., Sendra R., Franco L., Loidl P. Histone deacetylase: a key enzyme for the binding of regulatory proteins to chromatin. FEBS Lett. 1993, 317(3):175-180.
46. Manzon L.A. The role of prolactin in fish osmoregulation: a review. Gen. Compar. Endocrinol. 2002, 125(2):291-310.
47. Martin S.A.M., Taggart J.B., Seear P.J., Bron J.E., Talbot R., Teale A.J., Sweeney G.E., Hoyheim B., Houlihan D.F., Tocher D.R., Zou J., Secombes C.J. Interferon type I and type II responses in an Atlantic salmon (Salmo salar) SHK-1 cell line using the salmon TRAITS/SGP microarray. Physiol. Genomics 2007, 32:33-44.
48. Martin-Diaz L., Franzellitti S., Buratti S., Valbonesi P., Capuzzoc A., Fabbri E. Effects of environmental concentrations of the antiepilectic drug carbamazepine on biomarkers and cAMP-mediated cell signaling in the mussel Mytilus galloprovincialis. Aquat. Toxicol. 2009, 94:177-185.
49. 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. Aquat. Toxicol. 2007, 84:38-49.
50. McAlexander M.B., Yu-Lee L.Y. Prolactin activation of IRF-1 transcription involves changes in histone acetylation. FEBS Lett. 2001, 488(1-2):91-94.
51. Melamed P. Histone deacetylases and repression of the gonadotropin genes. Trends Endocrin. Met. 2008, 19(1):25-31.
52. Montezinho L.P., Mork A., Duarte C.B., Penschuck S., Geraldes C.F., Castro M.M. Effects of mood stabilizers on the inhibition of adenylate cyclase via dopamine D(2)-like receptors. Bipolar Disord. 2007, 9:290-297.
53. Nelson D.R., Kamataki T., Waxman D.J., Guengerich F.P., Estabrook R.W., Feyereisen R., et al. The P450 superfamily: update on new sequences, gene mapping, accession numbers, early trivial names of enzymes, and nomenclature. DNA Cell Biol. 1993, 12(1):1-51.
54. OECD Guideline for Testing of Chemicals 203: Fish, Acute Toxicity Test (Updated Guideline, adopted 17th July 1992) and 204 Fish, Prolonged Toxicity Test: 14-Day Study (Original Guideline, adopted 4th April 1984).
55. O'Keeffe A.M., Hubert S., Voisin M., Houeix B., Cotter D., Cairns M.T. Somatolactin mRNA expression during the parr-smolt transformation in hatchery-reared Atlantic salmon Salmo salar smolts. J. Fish Biol. 2008, 73(2):436-443.
56. Palmer G.C., Jones D.J., Medina M.A., Stavinoha W.B. Anticonvulsant drug actions on in vitro and in vivo levels of cyclic AMP in the mouse brain. Epilepsia 1979, 20:95-104.
57. Palmer G.C. Interactions of antiepileptic drugs on adenylate cyclase and phosphodiesterase in rat and mouse cerebrum. Exp. Neural. 1979, 63:322-335.
58. Pérez-Martín J.M., Fernández-Freire P., Labrador V., Hazen M.J. Carbamazepine induces mitotic arrest in mammalian Vero cells. Mutat. Res. Fundament. Mol. 2008, 637(1-2):124-133.
59. Pinero D.J., Connor J.R. Iron in the brain: an important contributor in normal and diseased states. Neuroscientist 2000, 6:435-453.
60. Raffin-Sanson M.L., de Keyzer Y., Bertagna X. Proopiomelanocortin a polypeptide precursor with multiple functions: from physiology to pathological conditions. Eur. J. Endocrinol. 2003, 149:79-90.
61. Rand-Weaver M., Pottingere T.G., Sumpter J.P. Plasma somatolactin concentrations in salmonids fish are elevated by stress. J. Endocrinol. 1993, 138:509-515.
62. Rao J.S., Bazinet R.P., Rapoport S.I., Lee H.-J. Chronic administration of carbamazepine down-regulates AP-2 DNA-binding activity and AP-2α protein expression in rat frontal cortex. Biol. Psychiat. 2007, 61(2):154-161.
63. Rouault T. 2001 systemic iron metabolism: a review of basic concepts and implications for brain iron metabolism. Pediatr. Neurol. 2001, 25:130-137.
64. Sakamoto T., McCormick S.D. Prolactin and growth hormone in fish osmoregulation. Gen. Comp. Endocr. 2006, 147(1):24-30.
65. Santos J.L., Aparicio I., Alonso E., Callejón M. Simultaneous determination of pharmaceutically active compounds in wastewater samples by solid phase extraction and high-performance liquid chromatography with diode array and fluorescence detectors. Anal. Chim. Acta 2005, 550:116-122.
66. Shahbazian M.D., Grunstein M. Functions of site-specific histone acetylation and deacetylation. Annu. Rev. Biochem. 2007, 76:75-100.
67. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
68. Slater G.S.C., Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinform. 2005, 6:31-42.
69. Taggart J.B., Bron J.E., Martin S.A.M., Seear P.J., Høyheim B., Talbot R., Villeneuve L., Sweeney G.E., Houlihan D.F., Secombes C.J., Tocher D.R., Teale A.J. A description of the origins, design and performance of the TRAITS/SGP Atlantic salmon (Salmo salar L.) cDNA microarray. J. Fish Biol. 2008, 72(9):2071-2094.
70. Ternes T.A. Occurrence of pharmaceuticals in German sewage treatment plants and rivers. Water Res. 1998, 32:3245-3260.
71. Ternes T.A., Stumpf M., Mueller J., Haberer K., Wilken R.-D., Servos M. Behavior and occurrence of estrogens in municipal sewage treatment plants-I. investigations in Germany, Canada and Brazil. Sci. Total Environ. 1999, 225:81-90.
72. Thusher V., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Nat. Acad. Sci. U. S. A. 2001, 98:5116-5121.
73. Tsiftsoglou A.S., Tsamadou A.I., Papadopoulou L.C. Heme as key regulator of major mammalian cellular functions molecular, cellular, and pharmacological aspects. Pharmacol. Therapeut. 2006, 111:327-345.
74. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R., Lee D.H., Peterson Myers J., Shioda T., Soto A.M., vom Saal F.S., Welshons W.V., Zoeller R.T. Regulatory decisions on endocrine disrupting chemicals should be based on the principles of endocrinology. Reprod. Toxicol. 2013, 38:1-15.
75. van der Ven K., Keil D., Moens L.N., van Hummelen P., van Remortel P., Maras M., De Coen W. Effects of the antidepressant mianserin in zebrafish: molecular markers of endocrine disruption. Chemosphere 2006, 65(10):1836-1845.
76. Vega-Rubin de Celis S., Rojas P., Gomez-Requeni P., Albalat A., Gutierrez J., Medale F., Kaushik S.J., Navarro I., Perez-Sanchez J. Nutritional assessment of somatolactin function in gilthead sea bream (Sparus aurata): concurrent changes in somatotropic axis and pancreatic hormones. Comp. Biochem. Physiol. 2004, 138:533-542.
77. von Schalburg K.R., Rise M.L., Cooper G.A., Brown G.D., Gibbs A.R., Nelson C.C., Davidson W.S., Koop B.F. Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 2005, 15(6):126-137.
78. von Schalburg K.R., Cooper G.A., Leong J., Robb A., Lieph R., Rise M.L., Davidson W.S., Koop B.F. Expansion of the genomics research on Atlantic salmon Salmo salar L project (GRASP) microarray tools. J. Fish Biol. 2008, 72:2051-2070.
79. Walker M.K., Peterson R.E. Potencies of polychlorinated dibenzo-p-dioxin, dibenzofuran, and biphenyl congeners relative to 2,3,7,8-tetrachlodibenzo-p-dioxin for producing early life stage mortality in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol. 1991, 21:219-238.
80. Walker M.K., Spitsbergen J.M., Olson J.R., Peterson R.E. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) toxicity during early life stage development of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 1991, 48:875-883.
81. Walker M.K., Cook P.M., Butterworth B.C., Zabel E.W., Peterson R.E. Potency of a complex mixture of polychloronated dibenzo-p-dioxin dibenzofuran, and biphenyl congeners compared to 2,3,7,8-tetrachlorodibenzo-p-dioxin in causing fish early life stage mortality. Fundament. Appl. Toxicol. 1996, 30:178-186.
82. Weber G.M., Grau E.G. Changes in serum concentrations and pituitary content of the two prolactins and growth hormone during the reproductive cycle in female tilapia Oreochromis mossambicus, compared with changes during fasting. Compar. Biochem. Physiol. 1999, 124:323-335.
83. Weissman C. The metabolic response to stress: an overview and update. Anesthesiology 1990, 73:308-327.
84. Wynne J.W., O'Sullivan M.G., Cook M.T., Stone G., Nowak B.F., Lovell D.R., Elliott N.G. Transcriptome analyses of Amoebic gill disease-affected Atlantic Salmon (Salmo salar) tissues reveal localized host gene suppression. Mar. Biotechnol. 2008, 10:388-403.
85. Ye W., Zhang L. Heme deficiency causes apoptosis but does not increase ROS generation in HeLa cells. Biochem. Biophys. Res. Commun. 2004, 319(4):1065-1071.
86. Zhu X., Wang J., Ju B.-G., Rosenfeld M.G. Signaling and epigenetic regulation of pituitary development. Curr. Opin. Cell Biol. 2007, 19(6):605-611.