A panel of biological tests reveals developmental effects of pharmaceutical pollutants on late stage zebrafish embryos.

[en] Standard toxicological assays using the zebrafish model system evaluate lethality and teratogenicity upon exposure during the first two days after fertilization. We tested the biological effects of several widely used drugs on zebrafish by acute treatment for 24hours starting at late embryonic stages, between 48 and 72hours post-fertilization. For 4 out of 6 compounds, we observed a higher sensitivity of late stage zebrafish embryos for general toxicity (lethality) compared to younger embryos. Morphological defects such as edema, body curvature, delayed growth, decreased heart rate and locomotion were observed for each of the compounds tested, often at sublethal concentrations. Gene expression studies on a set of four selected genes revealed a specific regulatory pattern for the different compounds tested. Our results allow us to compare various toxicological endpoints and may contribute to the design of a rational high throughput approach using the zebrafish model.

Research Center/Unit :

AFFISH-RC - Applied and Fundamental FISH Research Center - ULiège
Giga-Development and Stem Cells - ULiège

Disciplines :

Biochemistry, biophysics & molecular biology
Environmental sciences & ecology

Author, co-author :

Pruvot, Benoist ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Quiroz O' Donova, Yobhana ; Université de Liège - ULiège > SYST -- ACC -- AD ULg

Voncken, Audrey ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Jeanray, Nathalie ; Université de Liège - ULiège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Systèmes et modélisation

PIOT, Amandine ; Centre Hospitalier Universitaire de Liège - CHU > Chimie médicale

Martial, Joseph ; Université de Liège - ULiège > Département des sciences de la vie > Département des sciences de la vie

Muller, Marc ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire

Language :

English

Title :

A panel of biological tests reveals developmental effects of pharmaceutical pollutants on late stage zebrafish embryos.

Publication date :

2012

Journal title :

Reproductive Toxicology

ISSN :

0890-6238

eISSN :

1873-1708

Publisher :

Elsevier, Netherlands

Pages :

in press

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 26 October 2012

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Bibliography

Molina G., Vogt A., Bakan A., Dai W., Queiroz de Oliveira P., Znosko W., et al. Zebrafish chemical screening reveals an inhibitor of Dusp6 that expands cardiac cell lineages. Nature Chemical Biology 2009, 5:680.
Brittijn S.A., Duivesteijn S.J., Belmamoune M., Bertens L.F., Bitter W., de Bruijn J.D., et al. Zebrafish development and regeneration: new tools for biomedical research. International Journal of Developmental Biology 2009, 53:835.
Froehlicher M., Liedtke A., Groh K.J., Neuhauss S.C., Segner H., Zebrafish Eggen R.I. (Danio rerio) neuromast: promising biological endpoint linking developmental and toxicological studies. Aquatic Toxicology 2009, 95:307.
Irons T.D., MacPhail R.C., Hunter D.L., Padilla S. Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicology and Teratology 2009, 32:84.
Pruvot B., Jacquel A., Droin N., Auberger P., Bouscary D., Tamburini J., et al. Leukemic cell xenograft in zebrafish embryo for investigating drug efficacy. Haematologica 2011, 96:612.
Langenau D.M., Keefe M.D., Storer N.Y., Guyon J.R., Kutok J.L., Le X., et al. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes and Development 2007, 21:1382.
Zhuravleva J., Solary E., Chluba J., Bastie J.N., Delva L. A role for the transcription intermediary factor 2 in zebrafish myelopoiesis. Experimental Hematology 2008, 36:559.
Campbell W.A., Yang H., Zetterberg H., Baulac S., Sears J.A., Liu T., et al. Zebrafish lacking Alzheimer presenilin enhancer 2 (Pen-2) demonstrate excessive p53-dependent apoptosis and neuronal loss. Journal of Neurochemistry 2006, 96:1423.
Xia W. Exploring Alzheimer's disease in zebrafish. Journal of Alzheimer's Disease 2010, 20:981.
Teraoka H., Dong W., Hiraga T. Zebrafish as a novel experimental model for developmental toxicology. Congenital Anomalies (Kyoto) 2003, 43:123.
Spitsbergen J.M., Kent M.L. The state of the art of the zebrafish model for toxicology and toxicologic pathology research - advantages and current limitations. Toxicologic Pathology 2003, 31(Suppl.):62.
Nagel R., Dar T. The embryo test with the zebrafish Danio rerio - a general model in ecotoxicology and toxicology. Altex-Alternativen Zu Tierexperimenten 2002, 19:38.
Embry M.R., Belanger S.E., Braunbeck T.A., Galay-Burgos M., Halder M., Hinton D.E., et al. The fish embryo toxicity test as an animal alternative method in hazard and risk assessment and scientific research. Aquatic Toxicology 2010, 97:79.
Halling-Sorensen B., Nors Nielsen S., Lanzky P.F., Ingerslev F., Holten Lutzhoft H.C., Jorgensen S.E. Occurrence, fate and effects of pharmaceutical substances in the environment - a review. Chemosphere 1998, 36:357.
Santos L.H., Araujo A.N., Fachini A., Pena A., Delerue-Matos C., Montenegro M.C. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. Journal of Hazardous Materials 2010, 175:45.
Ferrari B., Paxeus N., Lo Giudice R., Pollio A., Garric J. Ecotoxicological impact of pharmaceuticals found in treated wastewaters: study of carbamazepine, clofibric acid, and diclofenac. Ecotoxicology and Environment Safety 2003, 55:359.
Gibs J., Stackelberg P.E., Furlong E.T., Meyer M., Zaugg S.D., Lippincott R.L. Persistence of pharmaceuticals and other organic compounds in chlorinated drinking water as a function of time. Science of the Total Environment 2007, 373:240.
Khetan S.K., Collins T.J. Human pharmaceuticals in the aquatic environment: a challenge to green chemistry. Chemical Reviews 2007, 107:2319.
Mompelat S., Le Bot B., Thomas O. Occurrence and fate of pharmaceutical products and by-products, from resource to drinking water. Environment International 2009, 35:803.
Gould T.D., Manji H.K. The Wnt signaling pathway in bipolar disorder. Neuroscientist 2002, 8:497.
Feng H.L., Leng Y., Ma C.H., Zhang J., Ren M., Chuang D.M. Combined lithium and valproate treatment delays disease onset, reduces neurological deficits and prolongs survival in an amyotrophic lateral sclerosis mouse model. Neuroscience 2008, 155:567.
Westerfield M. THE ZEBRAFISH BOOK, 5th edition: a guide for the laboratory use of zebrafish (Danio rerio) 2007, University of Oregon Press, Eugene.
Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Developmental Dynamics 1995, 203:253.
Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 2001, 29:2002.
Steel R.G.D., Torrie J.H. Analysis of covariance. Principles and procedures of statistics: a biometrical approach 1996, 401. McGraw-Hill, New York, ISBN: 9780070610286. 3rd ed.
Li X., Jia S., Wang S., Wang Y., Meng A. Mta3-NuRD complex is a master regulator for initiation of primitive hematopoiesis in vertebrate embryos. Blood 2009, 114:5464.
Farooq M., Sulochana K.N., Pan X., To J., Sheng D., Gong Z., et al. Histone deacetylase 3 (hdac3) is specifically required for liver development in zebrafish. Developmental Biology 2008, 317:336.
Gurvich N., Berman M.G., Wittner B.S., Gentleman R.C., Klein P.S., Green J.B. Association of valproate-induced teratogenesis with histone deacetylase inhibition in vivo. FASEB Journal 2005, 19:1166.
Isenberg J.S., Jia Y., Field L., Ridnour L.A., Sparatore A., Del Soldato P., et al. Modulation of angiogenesis by dithiolethione-modified NSAIDs and valproic acid. British Journal of Pharmacology 2007, 151:63.
Selderslaghs I.W., Van Rompay A.R., De Coen W., Witters H.E. Development of a screening assay to identify teratogenic and embryotoxic chemicals using the zebrafish embryo. Reproductive Toxicology 2009, 28:308.
van den Brandhof E.J., Montforts M. Fish embryo toxicity of carbamazepine, diclofenac and metoprolol. Ecotoxicology and Environment Safety 2010, 73:1862.
Nassef M., Matsumoto S., Seki M., Khalil F., Kang I.J., Shimasaki Y., et al. Acute effects of triclosan, diclofenac and carbamazepine on feeding performance of Japanese medaka fish (Oryzias latipes). Chemosphere 2010, 80:1095.
Berridge M.J., Downes C.P., Hanley M.R. Neural and developmental actions of lithium: a unifying hypothesis. Cell 1989, 59:411.
Maslanski J.A., Leshko L., Busa W.B. Lithium-sensitive production of inositol phosphates during amphibian embryonic mesoderm induction. Science 1992, 256:243.
Stachel S.E., Grunwald D.J., Myers P.Z. Lithium perturbation and goosecoid expression identify a dorsal specification pathway in the pregastrula zebrafish. Development 1993, 117:1261.
Rana N., Moond M., Marthi A., Bapatla S., Sarvepalli T., Chatti K., et al. Caffeine-induced effects on heart rate in zebrafish embryos and possible mechanisms of action: an effective system for experiments in chemical biology. Zebrafish 2010, 7:69.
Chen Y.H., Huang Y.H., Wen C.C., Wang Y.H., Chen W.L., Chen L.C., et al. Movement disorder and neuromuscular change in zebrafish embryos after exposure to caffeine. Neurotoxicology and Teratology 2008, 30:440.
Kennedy M.D., Galloway A.V., Dickau L.J., Hudson M.K. The cumulative effect of coffee and a mental stress task on heart rate, blood pressure, and mental alertness is similar in caffeine-naive and caffeine-habituated females. Nutrition Research 2008, 28:609.
McClaran S.R., Wetter T.J. Low doses of caffeine reduce heart rate during submaximal cycle ergometry. Journal of the International Society of Sports Nutrition 2007, 4:11.
Bichler A., Swenson A., Harris M.A. A combination of caffeine and taurine has no effect on short term memory but induces changes in heart rate and mean arterial blood pressure. Amino Acids 2006, 31:471.
Turley K.R., Gerst J.W. Effects of caffeine on physiological responses to exercise in young boys and girls. Medicine and Science in Sports and Exercise 2006, 38:520.
Chakraborty C., Hsu C.H., Wen Z.H., Lin C.S., Agoramoorthy G. Effect of caffeine, norfloxacin and nimesulide on heartbeat and VEGF expression of zebrafish larvae. Journal of Environment biology 2011, 32:179.
Egan R.J., Bergner C.L., Hart P.C., Cachat J.M., Canavello P.R., Elegante M.F., et al. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behavioural Brain Research 2009, 205:38.
Wong K., Elegante M., Bartels B., Elkhayat S., Tien D., Roy S., et al. Analyzing habituation responses to novelty in zebrafish (Danio rerio). Behavioural Brain Research 2010, 208:450.
Zhdanova I.V., Wang S.Y., Leclair O.U., Danilova N.P. Melatonin promotes sleep-like state in zebrafish. Brain Research 2001, 903:263.
Renier C., Faraco J.H., Bourgin P., Motley T., Bonaventure P., Rosa F., et al. Genomic and functional conservation of sedative-hypnotic targets in the zebrafish. Pharmacogenetics and Genomics 2007, 17:237.
Rihel J., Prober D.A., Arvanites A., Lam K., Zimmerman S., Jang S., et al. Zebrafish behavioral profiling links drugs to biological targets and rest/wake regulation. Science 2010, 327:348.
Selderslaghs I.W., Hooyberghs J., De Coen W., Witters H.E. Locomotor activity in zebrafish embryos: a new method to assess developmental neurotoxicity. Neurotoxicology and Teratology 2010, 32:460.
Scholz S., Fischer S., Gundel U., Kuster E., Luckenbach T., Voelker D. The zebrafish embryo model in environmental risk assessment - applications beyond acute toxicity testing. Environmental Science and Pollution Research International 2008, 15:394.
Yang L., Kemadjou J.R., Zinsmeister C., Bauer M., Legradi J., Muller F., et al. Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biology 2007, 8:R227.
Ankley G.T., Bencic D.C., Breen M.S., Collette T.W., Conolly R.B., Denslow N.D., et al. Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquatic Toxicology 2009, 92:168.
Rahman Q., Abidi P., Afaq F., Schiffmann D., Mossman B.T., Kamp D.W., et al. Glutathione redox system in oxidative lung injury. Critical Reviews in Toxicology 1999, 29:543.
Saito M., Sato K., Kunisaki N., Kimura S. Characterization of a rainbow trout matrix metalloproteinase capable of degrading type I collagen. European Journal of Biochemistry 2000, 267:6943.
Ortega N., Behonick D., Stickens D., Werb Z. How proteases regulate bone morphogenesis. Annals of the New York Academy of Sciences 2003, 995:109.
Zhang Y., Bai X.T., Zhu K.Y., Jin Y., Deng M., Le H.Y., et al. In vivo interstitial migration of primitive macrophages mediated by JNK-matrix metalloproteinase 13 signaling in response to acute injury. Journal of Immunology 2008, 181:2155.
Setsuie R., Wada K. The functions of UCH-L1 and its relation to neurodegenerative diseases. Neurochemistry International 2007, 51:105.
Day I.N., Thompson R.J. UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Progress in Neurobiology 2010, 90:327.
Zhang X., Heng X., Li T., Li L., Yang D., Du Y., et al. Long-term treatment with lithium alleviates memory deficits and reduces amyloid-beta production in an aged Alzheimer's disease transgenic mouse model. Journal of Alzheimer's Disease 2011, 24:739.
Henn K., Braunbeck T. Dechorionation as a tool to improve the fish embryo toxicity test (FET) with the zebrafish (Danio rerio). Comparative Biochemistry and Physiology. Part C: Toxicology and Pharmacology 2011, 153:91.