Dithiocarbamates induce craniofacial abnormalities and downregulate sox9a during zebrafish development

Toxicological Sciences

Volumn 117, Issue 1, 2010, Pages 209-217

  van boxtel, Antonius Leonardus ^a   Pieterse, Bart ^b   Cenijn, Peter ^a   Kamstra, Jorke Harmen ^a   Brouwer, Abraham ^b   van wieringen, Wessel ^c,d   de Boer, Jacob ^a   Legler, Juliette ^a  

^a INSTITUTE FOR ENVIRONMENTAL STUDIES   (Netherlands)

^b BIODETECTION SYSTEMS B V   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

Craniofacial; Dithiocarbamate; Microarray; Sox9a; TGF 1; Zebrafish

Indexed keywords

DIETHYLDITHIOCARBAMIC ACID; DISULFIRAM; METAMITRON; THIRAM; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CONNECTIVE TISSUE; CRANIOFACIAL MALFORMATION; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE IDENTIFICATION; MICROARRAY ANALYSIS; NONHUMAN; SIGNAL TRANSDUCTION; TERATOGENESIS; ZEBRA FISH;

ANIMALS; BASE SEQUENCE; CRANIOFACIAL ABNORMALITIES; DNA PRIMERS; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOX9 TRANSCRIPTION FACTOR; TERATOGENS; THIOCARBAMATES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 77955861744     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq169     Document Type: Article

References (38)

1. Anderson, C., Bartlett, S. J., Gansner, J. M., Wilson, D., He, L., Gitlin, J. D., Kelsh, R. N., and Dowden, J. (2007). Chemical genetics suggests a critical role for lysyl oxidase in zebrafish notochord morphogenesis. Mol. Biosyst. 3, 51-59.
2. Atsawasuwan, P., Mochida, Y., Katafuchi, M., Kaku, M., Fong, K. S., Csiszar, K., and Yamauchi, M. (2008). Lysyl oxidase binds transforming growth factor-beta and regulates its signaling via amine oxidase activity. J. Biol. Chem. 283, 34229-34240.
3. Begemann, G., Schilling, T. F., Rauch, G. J., Geisler, R., and Ingham, P. W. (2001). The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128, 3081-3094.
4. Chiang, E. F., Pai, C. I., Wyatt, M., Yan, Y. L., Postlethwait, J., and Chung, B. (2001). Two sox9 genes on duplicated zebrafish chromosomes: expression of similar transcription activators in distinct sites. Dev. Biol. 231, 149-163.
5. European Commission. (2002). Monitoring of Pesticide Residues in Products of Plant Origin in the European Union, Norway, Iceland and Liechtenstein. European Commission, Brussels, Belgium. Available at: http://ec.europa.eu /food/fvo/specialreports/pesticide_residues/report_2001_en.pdf. Accessed December 2009.
6. Gansner, J. M., Mendelsohn, B. A., Hultman, K. A., Johnson, S. L., and Gitlin, J. D. (2007). Essential role of lysyl oxidases in notochord development. Dev. Biol. 307, 202-213.
7. Goldring, M. B., Tsuchimochi, K., and Ijiri, K. (2006). The control of chondrogenesis. J. Cell Biochem. 97, 33-44.
8. Haendel, M. A., Tilton, F., Bailey, G. S., and Tanguay, R. L. (2004). Developmental toxicity of the dithiocarbamate pesticide sodium metam in zebrafish. Toxicol. Sci. 81, 390-400.
9. Janssens, K., ten, D. P., Janssens, S., and Van, H. W. (2005). Transforming growth factor-beta1 to the bone. Endocr. Rev. 26, 743-774.
10. Kopinke, D., Sasine, J., Swift, J., Stephens, W. Z., and Piotrowski, T. (2006). Retinoic acid is required for endodermal pouch morphogenesis and not for pharyngeal endoderm specification. Dev. Dyn. 235, 2695-2709.
11. Korhonen, A., Hemminki, K., and Vainio, H. (1983). Embryotoxicity of industrial chemicals on the chicken embryo: dithiocarbamates. Teratog. Carcinog. Mutagen. 3, 163-175.
12. Lang, M. R., Lapierre, L. A., Frotscher, M., Goldenring, J. R., and Knapik, E. W. (2006). Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat. Genet. 38, 1198-1203.
13. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W., et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
14. Maki, J. M. (2009). Lysyl oxidases in mammalian development and certain pathological conditions. Histol. Histopathol. 24, 651-660.
15. Nagel, R. (2002). DarT: the embryo test with the Zebrafish Danio rerio-a general model in ecotoxicology and toxicology. ALTEX 19(Suppl. 1), 38-48.
16. Rath, N. C., Huff, W. E., Huff, G. R., and Kannan, L. (2007). Induction of tibial dyschondroplasia by carbamate and thiocarbamate pesticides. Avian Dis. 51, 590-593.
17. Reynaud, C., Baas, D., Gleyzal, C., Le Guellec, D., and Sommer, P. (2008). Morpholino knockdown of lysyl oxidase impairs zebrafish development, and reflects some aspects of copper metabolism disorders. Matrix Biol. 27, 547-560.
18. Robens, J. F. (1969). Teratologic studies of carbaryl, diazinon, norea, disulfiram, and thiram in small laboratory animals. Toxicol. Appl. Pharmacol. 15, 152-163.
19. Roll, R. (1971). Teratologic studies with Thiram (TMTD) on two strains of mice. Arch. Toxikol. 27, 173-186.
20. Simsa, S., Hasdai, A., Dan, H., and Ornan, E. M. (2007). Induction of tibial dyschondroplasia in turkeys by tetramethylthiuram disulfide (thiram). Poult. Sci. 86, 1766-1771.
21. Stemple, D. L. (2005). Structure and function of the notochord: an essential organ for chordate development. Development 132, 2503-2512.
22. Stratford, T., Horton, C., and Maden, M. (1996). Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr. Biol. 6, 1124-1133.
23. Teraoka, H., Urakawa, S., Nanba, S., Nagai, Y., Dong, W., Imagawa, T., Tanguay, R. L., Svoboda, K., Handley-Goldstone, H. M., Stegeman, J. J., et al. (2006). Muscular contractions in the zebrafish embryo are necessary to reveal thiuram-induced notochord distortions. Toxicol. Appl. Pharmacol. 212, 24-34.
24. Thisse, C., Thisse, B., Schilling, T. F., and Postlethwait, J. H. (1993). Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119, 1203-1215.
25. Tilton, F., La Du, J. K., and Tanguay, R. L. (2008). Sulfhydryl systems are a critical factor in the zebrafish developmental toxicity of the dithiocarbamate sodium metam (NaM). Aquat. Toxicol. 90, 121-127.
26. Tilton, F., La Du, J. K., Vue, M., Alzarban, N., and Tanguay, R. L. (2006). Dithiocarbamates have a common toxic effect on zebrafish body axis formation. Toxicol. Appl. Pharmacol. 216, 55-68.
27. Tilton, F., and Tanguay, R. L. (2008). Exposure to sodium metam during zebrafish somitogenesis results in early transcriptional indicators of the ensuing neuronal and muscular dysfunction. Toxicol. Sci. 106, 103-112.
28. Vallari, R. C., and Pietruszko, R. (1982). Human aldehyde dehydrogenase: mechanism of inhibition of disulfiram. Science 216, 637-639.
29. 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., et al. (2008). Microarray analysis reveals a mechanism of phenolic polybrominated diphenylether toxicity in zebrafish. Environ. Sci. Technol. 42, 1773-1779.
30. van Boxtel, A. L., Kamstra, J. H., Fluitsma, D. M., and Legler, J. (2010). Dithiocarbamates are teratogenic to developing zebrafish through inhibition of lysyl oxidase activity. Toxicol. Appl. Pharmacol. 244, 156-161.
31. Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F. D., Keutel, J., and Hustert, E. (1994). Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120.
32. Walker, M. B., and Kimmel, C. B. (2007). A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 82, 23-28.
33. Westerfield, M. (2000). The Zebrafish Book. University of Oregon Press, Eugene, OR.
34. Eugene, OR. Whitmore, D., Foulkes, N. S., and Sassone-Corsi, P. (2000). Light acts directly on organs and cells in culture to set the vertebrate circadian clock. Nature 404, 87-91.
35. Woods, A., Wang, G., and Beier, F. (2007). Regulation of chondrocyte differentiation by the actin cytoskeleton and adhesive interactions. J. Cell Physiol. 213, 1-8.
36. World Health Organization (WHO). (1988). Dithiocarbamates Pesticides, Ethylenethiourea, and Propylenethiourea: A General Introduction. International Program on Chemical Safety, Geneva, Switzerland. Available at: http://www .inchem.org/documents/ehc/ehc/ehc78.htm. Accessed December 2009.
37. Yan, Y. L., Hatta, K., Riggleman, B., and Postlethwait, J. H. (1995). Expression of a type II collagen gene in the zebrafish embryonic axis. Dev. Dyn. 203, 363-376.
38. Yan, Y. L., Miller, C. T., Nissen, R. M., Singer, A., Liu, D., Kirn, A., Draper, B., Willoughby, J., Morcos, P. A., Amsterdam, A., et al. (2002). A zebrafish sox9 gene required for cartilage morphogenesis. Development 129, 5065-5079.