Dithiocarbamates are teratogenic to developing zebrafish through inhibition of lysyl oxidase activity

Toxicology and Applied Pharmacology

Volumn 244, Issue 2, 2010, Pages 156-161

  van Boxtel, Antonius L ^a   Kamstra, Jorke H ^a   Fluitsma, Donna M ^b   Legler, Juliette ^a  

^a INSTITUTE FOR ENVIRONMENTAL STUDIES   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Developmental toxicity; Dithiocarbamate; Inhibition; Lysyl oxidase; Pesticide; Teratogenic; Zebrafish

Indexed keywords

DITHIOCARBAMIC ACID; PROTEIN LOXL1; PROTEIN LOXL5; PROTEIN LYSINE 6 OXIDASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONGENITAL MALFORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME INHIBITION; EX VIVO STUDY; NONHUMAN; NOTOCHORD; NUCLEOTIDE SEQUENCE; SENSITIZATION; TERATOGENICITY; ZEBRA FISH;

ABNORMALITIES, DRUG-INDUCED; ANIMALS; ENZYME INHIBITORS; GENE KNOCKDOWN TECHNIQUES; PROTEIN-LYSINE 6-OXIDASE; TERATOGENS; THIOCARBAMATES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 77950034488     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.12.028     Document Type: Article

References (31)

1. Anderson C., Bartlett S.J., Gansner J.M., Wilson D., He L., Gitlin J.D., Kelsh R.N., Dowden J. Chemical genetics suggests a critical role for lysyl oxidase in zebrafish notochord morphogenesis. Mol. Biosyst. 2007, 3:51-59.
2. Caldas E.D., Miranda M.C., Conceicao M.H., de Souza L.C. Dithiocarbamates residues in Brazilian food and the potential risk for consumers. Food Chem. Toxicol. 2004, 42:1877-1883.
3. Cole D.C., Carpio F., Julian J., Leon N. Assessment of peripheral nerve function in an Ecuadorian rural population exposed to pesticides. J. Toxicol. Environ. Health A 1998, 55:77-91.
4. European commission. Monitoring of Pesticide Residues in Products of Plant Origin in the European Union, Norway, Iceland and Liechtenstein, (2003). Accessed 2009. URL: http://ec.europa.eu/food/fvo/specialreports/pesticide_residues/report_2001_en.pdf.
5. Fitsanakis V.A., Amarnath V., Moore J.T., Montine K.S., Zhang J., Montine T.J. Catalysis of catechol oxidation by metal-dithiocarbamate complexes in pesticides. Free Radic. Biol. Med. 2002, 33:1714-1723.
6. Furuta S., Ortiz F., Sun X.Z., Wu H.H., Mason A., Momand J. Copper uptake is required for pyrrolidine dithiocarbamate-mediated oxidation and protein level increase of p53 in cells. Biochem. J. 2002, 365:639-648.
7. Gansner J.M., Gitlin J.D. Essential role for the alpha 1 chain of type VIII collagen in zebrafish notochord formation. Dev. Dyn. 2008, 237(12):3715-3726.
8. Gansner J.M., Mendelsohn B.A., Hultman K.A., Johnson S.L., Gitlin J.D. Essential role of lysyl oxidases in notochord development. Dev. Biol. 2007, 307:202-213.
9. Guven K., Deveci E., Akba O., Onen A., de P.D. The accumulation and histological effects of organometallic fungicides Propineb and Maneb in the kidneys of fetus and female rats during pregnancy. Toxicol. Lett. 1998, 99:91-98.
10. Haendel M.A., Tilton F., Bailey G.S., Tanguay R.L. Developmental toxicity of the dithiocarbamate pesticide sodium metam in zebrafish. Toxicol. Sci. 2004, 81:390-400.
11. Heikkila R.E., Cabbat F.S., Cohen G. In vivo inhibition of superoxide dismutase in mice by diethyldithiocarbamate. J. Biol. Chem. 1976, 251:2182-2185.
12. Lucero H.A., Kagan H.M. Lysyl oxidase: an oxidative enzyme and effector of cell function. Cell Mol. Life Sci. 2006, 63:2304-2316.
13. Maki J.M. Lysyl oxidases in mammalian development and certain pathological conditions. Histol. Histopathol. 2009, 24:651-660.
14. Nagel R. DarT: The embryo test with the Zebrafish Danio rerio-a general model in ecotoxicology and toxicology. ALTEX 2002, 19(Suppl. 1):38-48.
15. Nasevicius A., Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 2000, 26:216-220.
16. Palamakumbura A.H., Trackman P.C. A fluorometric assay for detection of lysyl oxidase enzyme activity in biological samples. Anal. Biochem. 2002, 300:245-251.
17. Parsons M.J., Pollard S.M., Saúde L., Feldman B., Coutinho P., Hirst E.M., Stemple D.L. Zebrafish mutants identify an essential role for laminins in notochord formation. Development 2002, 129(13):3137-3146.
18. Rath N.C., Huff W.E., Huff G.R., Kannan L. Induction of tibial dyschondroplasia by carbamate and thiocarbamate pesticides. Avian Dis. 2007, 51:590-593.
19. Reynaud C., Baas D., Gleyzal C., Le Guellec D., Sommer P. Morpholino knockdown of lysyl oxidase impairs zebrafish development, and reflects some aspects of copper metabolism disorders. Matrix Biol. 2008, 27(6):547-560.
20. Robens J.F. Teratologic studies of carbaryl, diazinon, norea, disulfiram, and thiram in small laboratory animals. Toxicol. Appl. Pharmacol. 1969, 15:152-163.
21. Robu M.E., Larson J.D., Nasevicius A., Beiraghi S., Brenner C., Farber S.A., Ekker S.C. p53 activation by knockdown technologies. PLoS Genet. 2007, 3:e78.
22. Roll R. Teratologic studies with Thiram (TMTD) on two strains of mice. Arch. Toxikol. 1971, 27:173-186.
23. Simsa S., Hasdai A., Dan H., Ornan E.M. Induction of tibial dyschondroplasia in turkeys by tetramethylthiuram disulfide (thiram). Poult. Sci. 2007, 86:1766-1771.
24. Stemple D.L. Structure and function of the notochord: an essential organ for chordate development. Development 2005, 132:2503-2512.
25. Tang S.S., Trackman P.C., Kagan H.M. Reaction of aortic lysyl oxidase with beta-aminopropionitrile. J. Biol. Chem. 1983, 258:4331-4338.
26. Teraoka H., Urakawa S., Nanba S., Nagai Y., Dong W., Imagawa T., Tanguay R.L., Svoboda K., Handley-Goldstone H.M., Stegeman J.J., Hiraga T. Muscular contractions in the zebrafish embryo are necessary to reveal thiuram-induced notochord distortions. Toxicol. Appl. Pharmacol. 2006, 212:24-34.
27. Tilton F., La Du J.K., Vue M., Alzarban N., Tanguay R.L. Dithiocarbamates have a common toxic effect on zebrafish body axis formation. Toxicol. Appl. Pharmacol. 2006, 216:55-68.
28. van Boxtel A.L., Kamstra J.H., Cenijn P.H., Pieterse B., Wagner J.M., Antink M., Krab K., van der B.B., Marsh G., Brouwer A., Legler J. Microarray analysis reveals a mechanism of phenolic polybrominated diphenylether toxicity in zebrafish. Environ. Sci. Technol. 2008, 42:1773-1779.
29. Viguet-Carrin S., Garnero P., Delmas P.D. The role of collagen in bone strength. Osteoporos. Int. 2006, 17:319-336.
30. World Health Organization. Dithiocarbamates pesticides, ethylenethiourea, and propylenethiourea: a general introduction (2008). Accessed 2009. URL: http://www.wpro.who.int/NR/rdonlyres/ED05F324-B487-4B7F-A240-16DBA39AD994/0/Environmentalhealthcriteria78dithiocarbamatepesticidesethelynethioureaandpropylenethioureaageneralintroduction.pdf.
31. Yan Y.L., Hatta K., Riggleman B., Postlethwait J.H. Expression of a type II collagen gene in the zebrafish embryonic axis. Dev. Dyn. 1995, 203:363-376.