Assessment of toxicity and genotoxicity of low doses of 5-fluorouracil in zebrafish (Danio rerio) two-generation study

Water Research

Volumn 77, Issue , 2015, Pages 201-212

  Kovács, Róbert ^a   Csenki, Zsolt ^a   Bakos, Katalin ^a   Urbányi, Béla ^a   Horváth, Ákos ^a   Garaj Vrhovac, Vera ^b   Gajski, Goran ^b   Gerić, Marko ^b   Negreira, Noelia ^c   López de Alda, Miren ^c   Barceló, Damià ^c,d   Heath, Ester ^e   Kosjek, Tina ^e   Žegura, Bojana ^f   Novak, Matjaž ^e,f,g   Zajc, Irena ^f   Baebler, Špela ^f   Rotter, Ana ^f   Ramšak, Živa ^f   Filipič, Metka ^f  

^a SZENT ISTVÁN UNIVERSITY   (Hungary)

^b INSTITUTE FOR MEDICAL RESEARCH AND OCCUPATIONAL HEALTH   (Croatia)

^c INSTITUTE OF ENVIRONMENTAL ASSESSMENT AND WATER RESEARCH   (Spain)

^d UNIVERSITY OF GIRONA   (Spain)

^e JO EF STEFAN INSTITUTE   (Slovenia)

^f NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

^g Ecological Engineering Institute IEI   (Slovenia)

Author keywords

5 Fluorouracil; Anticancer drugs; Chronic exposure; Danio rerio; Genotoxic; Toxicogenomic

Indexed keywords

AQUATIC ECOSYSTEMS; BLOOD; DISEASES; DRUG DOSAGE; FISH; ONCOGENIC VIRUSES; POPULATION STATISTICS; TOXICITY;

5-FLUOROURACIL; ANTICANCER DRUG; CHRONIC EXPOSURE; DANIO RERIO; DNA DAMAGES; DOSE-DEPENDENT; GENOTOXIC; TOXICOGENOMICS; ZEBRAFISH; ZEBRAFISH DANIO RERIO;

GENES;

FLUOROURACIL; ANTINEOPLASTIC ANTIMETABOLITE; WATER POLLUTANT;

CONCENTRATION (COMPOSITION); CYPRINID; DOSE-RESPONSE RELATIONSHIP; DRUG; GENOMICS; GENOTOXICITY; GROWTH RATE; HISTOPATHOLOGY; POLLUTION EFFECT; POLLUTION EXPOSURE; SURVIVAL; TOXICITY TEST;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD CELL; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; ENVIRONMENTAL EXPOSURE; FEMALE; FERTILIZATION; GENE EXPRESSION; GENOME; GENOTOXICITY; GILL; GONAD; HATCHING; HISTOPATHOLOGY; LIVER TOXICITY; LONG TERM EXPOSURE; MALE; MICRONUCLEUS; NEPHROTOXICITY; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; REPRODUCTION; SURVIVAL; TOXICITY TESTING; TRANSCRIPTOMICS; UPREGULATION; ZEBRA FISH; ANIMAL; COMET ASSAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; KIDNEY; LIVER; PATHOLOGY; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; BLOOD CELLS; COMET ASSAY; DNA DAMAGE; FLUOROURACIL; GENE EXPRESSION PROFILING; GILLS; GONADS; KIDNEY; LIVER; REPRODUCTION; TOXICITY TESTS, CHRONIC; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84927587469     PISSN: 00431354     EISSN: 18792448     Source Type: Journal    
DOI: 10.1016/j.watres.2015.03.025     Document Type: Article

References (54)

1. Adhikary S., Eilers M. Transcriptional regulation and transformation by MYC proteins. Nature Reviews. Mol. Cell. Biol. 2005, 6:635-645.
2. Amatruda J.F., Zon L.I. Dissecting hematopoiesis and disease using the zebrafish. Dev. Biol. 1999, 216:1-15.
3. Anderson S.L., Wild G.C. Linking genotoxic responses and reproductive success in ecotoxicology. Environ. Health Perspect. 1994, 102:9-12.
4. Besse J.P., Latour J.F., Garric J. Anticancer drugs in surface waters. What can we say about the occurrence and environmental significance of cytotoxic, cytostatic and endocrine therapy drugs?. Environ. Int. 2012, 39:73-86.
5. Bolognesi C., Cirillo S. Genotoxicity biomarkers in aquatic bioindicators. Curr. Zool. 2014, 60:273-284.
6. Bolognesi C., Hayashi M. Micronucleus assay in aquatic animals. Mutagenesis 2011, 26:205-213.
7. Bonassi S., El-Zein R., Bolognesi C., Fenech M. Micronuclei frequency in peripheral blood lymphocytes and cancer risk: evidence from human studies. Mutagenesis 2011, 26:93-100.
8. Brezovsek P., Elersek T., Filipic M. Toxicities of four anti-neoplastic drugs and their binary mixtures tested on the green alga Pseudokirchneriella subcapitata and the cyanobacterium Synechococcus leopoliensis. Water Res. 2014, 52:168-177.
9. Choudhury R.C., Misra S., Jagdale M.B., Palo A.K. S-phase dependent cytogenetic toxicity of 5-fluorouracil in bone marrow cells of mice. J. Exp. Clin. Cancer Res. 2001, 20:57-62.
10. Devaux A., Fiat L., Gillet C., Bony S. Reproduction impairment following paternal genotoxin exposure in brown trout (Salmo trutta) and Arctic charr (Salvelinus alpinus). Aquat. Toxicol. 2013, 101:405-411.
11. DeYoung D.J., Bantle J.A., Hull M.A., Burks S.L. Differences in sensitivity to developmental toxicants as seen in Xenopus and Pimephales embryos. Bull. Environ. Contam. Toxicol. 1996, 56:143-150.
12. Diekmann M., Hultsch V., Nagel R. On the relevance of genotoxicity for fish populations I: effects of a model genotoxicant on zebrafish (Danio rerio) in a complete life-cycle test. Aquat. Toxicol. 2004, 68:13-26.
13. Diekmann M., Waldmann P., Schnurstein A., Grummt T., Braunbeck T., Nagel R. On the relevance of genotoxicity for fish populations II: genotoxic effects in zebrafish (Danio rerio) exposed to 4-nitroquinoline-1-oxide in a complete life-cycle test. Aquat. Toxicol. 2004, 68:27-37.
14. Edgar R., Domrachev M., Lash A.E. Gene expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002, 30:207-210.
15. El-Sayyad H.I., Ismail M.F., Shalaby F.M., Abou-El-Magd R.F., Gaur R.L., Fernando A., Raj M.H.G., Ouhtit A. Histopathological effects of cisplatin, doxorubicin and 5-flurouracil (5-FU) on the liver of male albino rats. Int. J. Biol. Sci. 2009, 5:466-473.
16. European Medicines Agency Guidelines on the Environmental Risk Assessment of Medicinal Products for Human Use 2006, European Chemical Agency, Doc ref. EMEA/CHMP/SWP/4447/00.
17. Fassbender C., Braunbeck T. Reproductive and genotoxic effects in zebrafish after chronic exposure to methyl methanesulfonate in a multigeneration study. Ecotoxicology 2013, 22:825-837.
18. Frenzilli G., Nigro M., Lyons B.P. The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat. Res. Rev. Mutat. Res. 2009, 681:80-92.
19. Girardot F., Monnier V., Tricoire H. Genome wide analysis of common and specific stress responses in adult Drosophila melanogaster. BMC Genomics 2004, 5:16.
20. Grisolia C.K., Cordeiro C.M.T. Variability in micronucleus induction with different mutagens applied to several species of fish. Genet. Mol. Biol. 2000, 23:235-239.
21. Hernando M.D., Mezcua M., Fernandez-Alba A.R., Barcelo D. Environmental risk assessment of pharmaceutical residues in wastewater effluents, surface waters and sediments. Talanta 2006, 69:334-342.
22. Huber W., von Heydebreck A., Sültmann H., Poustka A., Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 2002, 18(1):S96-S104.
23. Johnson A.C., Jurgens M.D., Williams R.J., Kummerer K., Kortenkamp A., Sumpter J.P. Do cytotoxic chemotherapy drugs discharged into rivers pose a risk to the environment and human health? an overview and UK case study. J. Hydrol. 2008, 348:167-175.
24. Knežević A.H., Dikić D., Lisičić D., Kopjar N., Oršolić N., Karabeg S., Benković V. Synergistic effects of irinotecan and flavonoids on Ehrlich ascites tumour-bearing mice. Basic Clin. Pharmacol. Toxicol. 2011, 109:343-349.
25. Kosjek T., Heath E. Occurrence, fate and determination of cytostatic pharmaceuticals in the environment. Trends Anal. Chem. 2011, 30(7):1065-1087.
26. Kosjek T., Perko S., Žigon D.A., Heath E. Fluorouracil in the environment: analysis, occurrence, degradation and transformation. J. Chromatogr. A 2013, 1290:62-72.
27. Kumar S., Aninat C., Michaux G.G., Morel F. Anticancer drug 5-fluorouracil induces reproductive and developmental defects in Caenorhabditis elegans. Reprod. Toxicol. 2010, 29:415-420.
28. Lau C., Andersen M.E., Crawford-Brown D.J., Kavlock R.J., Kimmel C.A., Knudsen T.B., Muneoka K., Rogers J.M., Setzer R.W., Smith G., Tyl R. Evaluation of biologically based dose-response modeling for developmental toxicity: a workshop report. Regul. Toxicol. Pharmacol. 2000, 31:190-199.
29. Lenz K., Mahnik S.N., Weissenbacher N., Mader R.M., Krenn P., Hann S., Koellensperger G., Uhl M., Knasmuller S., Ferk F., Bursch W., Fuerhacker M. Monitoring, removal and risk assessment of cytostatic drugs in hospital wastewater. Water Sci. Technol. 2007, 56:141-149.
30. Lin A.Y., Lin Y.C., Lee W.N. Prevalence and sunlight photolysis of controlled and chemotherapeutic drugs in aqueous environments. Environ. Pollut. 2014, 187:170-181.
31. Loeb L.A., Bielas J.H., Beckman R.A. Cancers exhibit a mutator phenotype: clinical implications. Cancer Res. 2008, 68:3551-3557.
32. Longley D.B., Harkin D.P., Johnston P.G. 5-Fluorouracil: mechanisms of action and clinical strategies. Nat. Rev. Cancer 2003, 3:330-338.
33. Lorge E., Thybaud V., Aardema M.J., Oliver J., Wakata A., Lorenzon G., Marzin D. SFTG international collaborative study on in-vitro micronucleus test - I. General conditions and overall conclusions of the study. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2006, 607:13-36.
34. Macdonald J.S. Toxicity of 5-fluorouracil 1999, vol. 13:33-34. Oncology, New York.
35. Meyer N., Penn L.Z. MYC - Timeline reflecting on 25 years with MYC. Nat. Rev. Cancer 2008, 8:976-990.
36. Myers M.S., Johnson L.L., Collier T.K. Establishing the causal relationship between polycyclic aromatic hydrocarbon (PAH) exposure and hepatic neoplasms and neoplasia-related liver lesions in English sole (Pleuronectes vetulus). Hum. Ecol. Risk Assess. 2003, 9:67-94.
37. Negreira N., Mastroianni N., Lăłpez de Alda M., Barcelăł D. Multianalyte determination of 24 cytostatics and metabolites by liquid chromatography-electrospray-tandem mass spectrometry and study of their stability and optimum storage conditions in aqueous solution. Talanta 2013, 116:290-299.
38. Ohuchida A., Furukawa A., Yoshida J., Watanabe M., Aruga F., Miwa Y., Shinkawa K., Kinae N. Micronucleus assays on 5-fluorouracil and 6-mercaptopurine with mouse peripheral-blood reticulocytes. Mutat. Res. 1992, 278(2-3):139-143.
39. Oka H., Ikeda K., Yoshimura H., Ohuchida A., Honma M. Relationship between p53 status and 5-fluorouracil sensitivity in 3 cell lines. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2006, 606:52-60.
40. Parrella A., Lavorgna M., Criscuolo E., Russo C., Fiumano V., Isidori M. Acute and chronic toxicity of six anticancer drugs on rotifers and crustaceans. Chemosphere 2014, 115:59-66.
41. Pinkney A.E., Harshbarger J.C., Karouna-Renier N.K., Jenko K., Balk L., Skarphéinsdóttir H., Liewenborg B., Rutter M.A. Tumor prevalence and biomarkers of genotoxicity in brown bullhead (Ameiurus nebulosus) in Chesapeake bay tributaries. Sci. Total Environ. 2011, 410-411:248-257.
42. Reinardy H.C., Dharamshi J., Jha A.N., Henry T.B. Changes in expression profiles of genes associated with DNA repair following induction of DNA damage in larval zebrafish Danio rerio. Mutagenesis 2013, 28:601-608.
43. Schuetz J.D., Wallace H.J., Diasio R.B. 5-Fluorouracil incorporation into DNA of CF-1 mouse bone-marrow cells as a possible mechanism of toxicity. Cancer Res. 1984, 44:1358-1363.
44. Singh N.P., McCoy M., Tice R., Schneider E. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 1988, 175:184-191.
45. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor, Statistics for Biology and Health 2005, 397-420. Springer-Verlag. R. Gentleman, V.J. Carey, W. Huber, R.A. Irizarry, S. Dudoit (Eds.).
46. Straub J.O. Combined environmental risk assessment for 5-fluorouracil and capecitabine in Europe. Integr. Environ. Assess. Manag. 2010, 6:540-566.
47. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15545-15550.
48. Tice R.R., Agurell E., Anderson D., Burlinson B., Hartmann A., Kobayashi H., Miyamae Y., Rojas E., Ryu J.C., Sasaki Y.F. Single cell gel/comet assay: guidelines for in-vitro and in-vivo genetic toxicology testing. Environ. Mol. Mutagen. 2000, 35:206-221.
49. Ud-Daula A., Pfister G., Schramm K.W. 5-Fluorouracil accumulation in green microalgae and its biogenetic transfer into ciliate protozoan. Bull. Environ. Contam. Toxicol. 2012, 88(4):548-554.
50. van Kuilenburq A.B.P., Maring J.G. Evaluation of 5-fluorouracil pharmacokinetic models and therapeutic drug monitoring in cancer patients. Pharmacogenomics 2013, 14:799-811.
51. Vasquez M.Z. Recommendations for safety testing with the invivo comet assay. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2012, 747:142-156.
52. Williams T.D., Mirbahai L., Chipman J.K. The toxicological application of transcriptomics and epigenomics in zebrafish and other teleosts. Brief. Funct. Genomics 2014, 13:157-171.
53. Zhou C., Wang Q., Wang Z., Chang Y. Comparison of three-colour flow cytometry and slide-based microscopy for the scoring of micronucleated reticulocytes in rat bone-marrow and peripheral blood. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 2013, 758:12-17.
54. Zuniga-Gonzalez G.M., Torres-Bugarin O., Zamora-Perez A.L., Gomez-Meda B.C., Ramos-Ibarra M.L., Gallegos-Arreola P., Flores-Garcia A., Lopez-Uribe A. Induction of micronucleated erythrocytes in mouse peripheral blood after cutaneous application of 5-fluorouracil. Arch. Med. Res. 2003, 34:141-144.