2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in the zebrafish embryo: Local circulation failure in the dorsal midbrain is associated with increased apoptosis

Toxicological Sciences

Volumn 69, Issue 1, 2002, Pages 191-201

  Dong, Wu ^a   Teraoka, Hiroki ^a   Yamazaki, Koji ^a   Tsukiyama, Shusaku ^a   Imani, Sumiko ^a   Imagawa, Tomohiro ^b   Stegeman, John J ^c   Peterson, Richard E ^d   Hiraga, T ^a  

^a RAKUNO GAKUEN UNIVERSITY   (Japan)

^b TOTTORI UNIVERSITY   (Japan)

^c WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apoptosis; Aryl hydrocarbon receptor; Circulation failure; CYP1A; Cytochrome P4501A; Developmental toxicity; Dioxin; Endothelial cell; Mesencephalic vein; Midbrain; Oxidative stress; TCDD; Zebrafish embryo

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ACETYLCYSTEINE; ANTIOXIDANT; AROMATIC HYDROCARBON RECEPTOR; ASCORBIC ACID; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; BETA NAPHTHOFLAVONE; CASPASE INHIBITOR; CYTOCHROME P450; CYTOCHROME P450 1A1; ENZYME INHIBITOR; MESSENGER RNA; MICONAZOLE; PROADIFEN; WATER;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN BLOOD FLOW; BRAIN CIRCULATION; BRAIN PERFUSION; BRAIN VEIN; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; ENDOTHELIUM CELL; ENZYME INDUCTION; EXPOSURE; GENE EXPRESSION; HEAD; HEART; IMMUNOREACTIVITY; MESENCEPHALON; NONHUMAN; OXIDATIVE STRESS; TEMPERATURE; TRUNK; ZEBRA FISH;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CASPASES; CEREBROVASCULAR CIRCULATION; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 CYP1A2; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; ENVIRONMENTAL POLLUTANTS; ENZYME INHIBITORS; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; MESENCEPHALON; MICROSCOPY, IMMUNOELECTRON; TETRACHLORODIBENZODIOXIN; ZEBRAFISH;

ANIMALIA; DANIO; DANIO RERIO; VERTEBRATA;

EID: 0036737213     PISSN: 10966080     EISSN: None     Source Type: Journal    
DOI: 10.1093/toxsci/69.1.191     Document Type: Article

References (45)

1. Alsharif, N. Z., Lawson, T., and Stohs, S. J. (1994). Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin is mediated by the aryl hydrocarbon (Ah) receptor complex. Toxicology 92, 39-51.
2. Andreasen, E. A., Hahn, M. E., Heideman, W., Peterson, R. E., and Tanguay, R. L. (2002a). The zebrafish (Danio rerio) aryl hydrocarbon receptor Type 1 (zfAHR1) is a novel vertebrate receptor. Mol. Pharmacol. 62, 234-249.
3. Andreasen, E. A., Spitsbergen, J. M., Tanguay, R. L., Stegeman, J. J., Heideman, W., and Peterson, R. E. (2002b). Tissue-specific expression of AHR2, ARNT2, and CYP1A in zebrafish embryos and larvae: Effects of developmental stage and 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure. Toxicol. Sci. 68, 403-419.
4. Barth, K. A., and Wilson, S. W. (1995). Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768.
5. Belair, C. D., Peterson, R. E., and Heideman, W. (2001). Dioxin as a tool to study development: Disruption of erythropoiesis in the zebrafish. Dev. Dyn. 222, 581-594.
6. Calvert, G. M., Wall, D. K., Sweeney, M. H., and Fingerhut, M. A. (1998). Evaluation of cardiovascular outcomes among U.S. workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Environ. Health Perspect. 106, S635-643.
7. Cantrell, S. M., Joy-Schlezinger, J., Stegeman, J. J., Tillitt, D. E., and Hannink, M. (1998). Correlation of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced apoptotic cell death in the embryonic vasculature with embryotoxicity. Toxicol. Appl. Pharmacol. 148, 24-34.
8. Cantrell, S. M., Lutz, L. H., Tillitt, D. E., and Hannink, M. (1996). Embryo-toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): The embryonic vasculature is a physiological target for TCDD-induced DNA damage and apoptotic cell death in Medaka (Orizias latipes). Toxicol. Appl. Pharmacol. 141, 23-34.
9. Cook, P. M., Zabel, E. W., and Peterson, R. E. (1997). The TCDD Toxicity Equivalence Approach for Characterization of trout early life stage mortality risks associated with exposures to TCDD and related chemicals. In Chemically-Induced Alterations in the Functional Development and Reproduction of Fishes (R. M. Rolland, M. Gilberston, and R. E. Peterson, Eds.), pp. 9-27. SETAC Technical Publications Series.
10. Dong, W., Teraoka, H., Kondo, S., and Hiraga, T. (2001). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptosis in the dorsal midbrain of zebrafish embryos by activation of the arylhydrocarbon receptor. Neurosci. Lett. 303, 169-172.
11. Elonen, G. E., Spehar, R. L., Holcombe, G. W., Johnson, R. D., Fernandez, J. D., Erickson, R. J., Tietge, J. E., and Cook, P. M. (1998). Comparative toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to seven freshwater fish species during early life-stage development. Environ. Toxicol. Chem. 17, 472-483.
12. Flesch-Janys, D., Berger, J., Gurn, P., Manz, A., Nagel, S., Waltsgott, H., and Dwyer, J. H. (1995). Exposure to polychlorinated dioxins and furans (PCDD/F) and mortality in a cohort of workers from an herbicide-producing plant in Hamburg, Germany. Am. J. Epidemiol. 142, 1165-1175.
13. Gasiewicz, T. A., and Rucci, G. (1991). Alpha-naphthoflavone acts as an antagonist of 2,3,7,8-tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor. Mol. Pharmacol. 40, 607-612.
14. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
15. Guiney, P. D., Smolowitz, R. M., Peterson, R. E., and Stegeman, J. J. (1997). Correlation of 2,3,7,8-tetrachlorodibenzo-p-dioxin induction of cytochrome P4501A in vascular endothelium with toxicity in early life stages of lake trout. Toxicol. Appl. Pharmacol. 143, 256-273.
16. Guiney, P. D., Walker, M. K., Spitsbergen, J. M., and Peterson, R. E. (2000). Hemodynamic dysfunction and cytochrome P4501A mRNA expression induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin during embryonic stages of lake trout development. Toxicol. Appl. Pharmacol. 168, 1-14.
17. Hahn, M. E. (2001). Dioxin toxicology and aryl hydrocarbon receptor: Insights from fish and other non-traditional models. Mar. Biotechnol. 3, S224-238.
18. Hanneman, W. H., Legare, M. E., Barhoumi, R., Burghardt, R. C., Safe, S., and Tiffany-Castiglioni, E. (1996). Stimulation of calcium uptake in cultured rat hippocampal neurons by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicology 112, 19-28.
19. Hassoun, E. A., Li, F., Abushaban A., and Stohs, S. J. (2001). Production of superoxide anion, lipid peroxidation, and DNA damage in the hepatic and brain tissues of rats after subchronic exposure to mixtures of TCDD and its congeners. J. Appl. Toxicol. 21, 211-219.
20. Hassoun, E. A., Wilt, S. C., Devito, M. J., Van Birgelen, A., Alsharif, N. Z., Birnbaum, L. S., and Stohs, S. J. (1998). Induction of oxidative stress in brain tissues of mice after subchronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci. 42, 23-27.
21. Henry, T. R., Spitsbergen, J. M., Hornung, M. W., Abnet, C. C., and Peterson, R. E. (1997). Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 142, 56-68.
22. Hornung, M. W., Spitsbergen, J. M., and Peterson, R. E. (1999). 2,3,7,8-Tetrachlorodibenzo-p-dioxin alters cardiovascular and craniofacial development and function in sac fry of rainbow trout (Oncorhynchus mykiss). Toxicol. Sci. 47, 40-51.
23. Imagawa, T., Hashimoto, Y., Kon, Y., and Sugimura, M. (1991). Immunoglobulin containing cells in the head kidney of carp (Cyprinus carpio L.) after bovine serum albumin injection. Fish Shellfish Immunol. 1, 173-185.
24. Isogai, S., Horiguchi, M., and Weinstein, B. M. (2001). The vascular anatomy of the developing zebrafish: An atlas of embryonic and early larval development. Dev. Biol. 230, 278-301.
25. Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972). Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257.
26. Lahvis, G. P., Lindell, S. L., Thomas, R. S., McCuskey, R. S., Murphy, C., Glover, E., Bentz, M., Southard, J., and Bradfield, C. A. (2000). Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 97, 10442-10447.
27. Nitatori, T., Sato, N., Waguri, S., Karasawa, Y., Araki, H., Shibanai, K., Kominami, E., and Uchiyama, Y. (1995). Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15, 1001-1011.
28. Park, S. S., Miller, H., Klotz, A. V., Kloepper-Sams, P. J., Stegeman, J. J., and Gelboin, H. V. (1986). Monoclonal antibodies to liver microsomal cytochrome P-450E of the marine fish Stenotomus chrysops (scup): Cross reactivity with 3-methylcholanthrene induced rat cytochrome P-450. Arch. Biochem. Biophys. 249, 339-350.
29. Rowlands, J. C., and Gustafsson, J. A. (1997). Aryl hydrocarbon receptor-mediated signal transduction. Crit. Rev. Toxicol. 27, 109-134.
30. Schlezinger, J. J., Keller, J., Verbrugge, L. A., and Stegeman, J. J. (2000). 3,3′,4,4′-Tetrachlorobiphenyl oxidation in fish, bird, and reptile species: Relationship to cytochrome P450 1A inactivation and reactive oxygen production. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 125, 273-286.
31. Schlezinger, J. J., White, R. D., and Stegeman, J. J. (1999). Oxidative inactivation of cytochrome P450 1A (CYP1A) stimulated by 3,3′,4,4′-tetrachlorobiphenyl: Production of reactive oxygen by vertebrate CYP1As. Mol. Pharmacol. 56, 588-597.
32. Slim, R., Toborek, M., Robertson, L. W., Lehmler, H. J., and Hennig, B. (2000). Cellular glutathione status modulates polychlorinated biphenyl-induced stress response and apoptosis in vascular endothelial cells. Toxicol. Appl. Pharmacol. 166, 36-42.
33. Smolowitz, R. M., Hahn, M. E., and Stegeman, J. J. (1991). Immunohistochemical localization of cytochrome P-450IA1 induced by 3,3′,4,4′-tetrachlorobiphenyl and by 2,3,7,8-tetrachlorodibenzofuran in liver and extrahepatic tissues of the teleost Stenotomus chrysops (scrup). Drug Metab. Dispos. 19, 113-123.
34. Spitsbergen, J. M., Walker, M. K., Olson, J. R., and Peterson, R. E. (1990). Pathologic alterations in early life stages of lake trout, Salvelinus namaycush, exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin as fertilized eggs. Aqua. Toxicol. 19, 41-72.
35. Stegeman, J. J., Hahn, M. E., Weisbrod, R., Woodin, B. R., Joy, J. S., Najibi, S., and Cohen, R. A. (1995). Induction of cytochrome P4501A1 by aryl hydrocarbon receptor agonists in porcine aorta endothelial cells in culture and cytochrome P4501A1 activity in intact cells. Mol. Pharmacol. 47, 296-306.
36. Stegeman, J. J., Miller, M. R., and Hinton, D. E. (1989). Cytochrome P450IA1 induction and localization in endothelium of vertebrate (teleost) heart. Mol. Pharmacol. 36, 723-729.
37. Tanguay, R. L., Abnet, C. C., Heideman, W., and Peterson, R. E. (1999). Cloning and characterization of the zebrafish (Danio rerio) aryl hydrocarbon receptor. Biochim. Biophys. Acta 1444, 35-48.
38. Tassaneeyakul, W., Birkett, D. J., Veronese, M. E., McManus, M. E., Tukey, R. H., Quattrochi, L. C., Gelboin, H. V., and Miners, J. O. (1993). Specificity of substrate and inhibitor probes for human cytochromes P450 1A1 and 1A2. J. Pharmacol. Exp. Ther. 265, 401-407.
39. Teraoka, H., Dong, W., Ogawa, S., Tsukiyama, S., Okuhara, Y., Niiyama, M., Ueno, N., Peterson, R. E., and Hiraga, T. (2002). 2,3,7,8-Tetrachloro-dibenzo-p-dioxin toxicity in the zebrafish embryo: Altered regional blood flow and impaired lower jaw development. Toxicol. Sci. 65, 192-199.
40. Toborek, M., Barger, S. W., Mattson, M. P., Espandiari, P., Robertson, L.W., and Hennig, B. (1995). Exposure to polychlorinated biphenyls causes endothelial cell dysfunction. J. Biochem. Toxicol. 10, 219-226.
41. Toomey, B. H., Bello, S., Hahn, M. E., Cantrell, S., Wright, P., Tillitt, D. E., and Di Giulio, R. T. (2001). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces apoptotic cell death and cytochrome P4501A expression in developing Fundulus heteroclitus embryos. Aquat. Toxicol. 53, 127-138.
42. Walker, M. K., and Peterson, R. E. (1994). Aquatic toxicity of dioxins and related chemicals. In Dioxins and Health. (A. Schecter, Ed.), pp. 347-387. Plenum, New York.
43. Walker, M. K., Spitsbergen, J. M., Olson, J. R., and Peterson, R. E. (1991). 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) toxicity during early life-stage development of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 48, 875-883.
44. Wang, W.-D., Chen, Y.-M., and Hu, C.-H. (1998). Detection of Ah receptor and Ah receptor nuclear translocator mRNAs in the oocytes and developing embryos of zebrafish (Danio rerio). Fish Physiol. Biochem. 18, 49-57.
45. Westerfield, M. (1995). The Zebrafish Book. University of Oregon Press, Eugene, OR.