AHR2-mediated transcriptomic responses underlying the synergistic cardiac developmental toxicity of PAHs

Toxicological Sciences

Volumn 143, Issue 2, 2015, Pages 469-481

  Jayasundara, Nishad ^a   Van Tiem Garner, Lindsey ^a,c   Meyer, Joel N ^a   Erwin, Kyle N ^b   Di Giulio, Richard T ^a  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Cardno Entrix   (United States)

Author keywords

Aryl hydrocarbon receptor; Cardiac development; Cardiotoxicity; Polycyclic aromatic hydrocarbons; Transcriptomics; Zebrafish

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; AROMATIC HYDROCARBON RECEPTOR 2; BENZO[A]PYRENE; DIMETHYL SULFOXIDE; FLUORANTHENE; POLYCYCLIC AROMATIC HYDROCARBON DERIVATIVE; UNCLASSIFIED DRUG; AHR2 PROTEIN, ZEBRAFISH; CALCIUM; FLUORENE DERIVATIVE; TRANSCRIPTOME; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CARDIOTOXICITY; CONTROLLED STUDY; DEVELOPMENTAL TOXICITY; EMBRYO; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART FUNCTION; HEART RATE; MICROARRAY ANALYSIS; MUSCLE CONTRACTION; NERVE CELL DIFFERENTIATION; NONHUMAN; PROTEIN SYNTHESIS; RNA EXTRACTION; TRANSCRIPTOMICS; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; CHEMICALLY INDUCED; CONGENITAL HEART MALFORMATION; DRUG EFFECTS; DRUG POTENTIATION; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENETICS; HEART; METABOLISM;

DANIO RERIO;

ANIMALS; BENZO(A)PYRENE; CALCIUM; CARDIOTOXICITY; DRUG SYNERGISM; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FLUORENES; HEART; HEART DEFECTS, CONGENITAL; RECEPTORS, ARYL HYDROCARBON; TRANSCRIPTOME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84924680662     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu245     Document Type: Article

References (40)

1. Alexeyenko, A., Wassenberg, D. M., Lobenhofer, E. K., Yen, J., Linney, E., Sonnhammer, E. L. L., and Meyer, J. N. (2010). Dynamic zebrafish interactome reveals transcriptional mechanisms of dioxin toxicity. PLoS One 5, e10465.
2. Billiard, S. M., Timme-Laragy, A. R., Wassenberg, D. M., Cockman, C., and Di Giulio, R. T. (2006). The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol. Sci. 92, 526-536.
3. Burns, C. G., and MacRae, C. A. (2006). Purification of hearts from zebrafish embryos. Biotechniques 40, 274-278.
4. Camarata, T., Krcmery, J., Snyder, D., Park, S., Topczewski, J., and Simon, H. G. (2010). Pdlim7 (LMP4) regulation of Tbx5 specifies zebrafish heart atrio-ventricular boundary and valve formation. Dev. Biol. 337, 233-245.
5. Cantrell, S. M., Lutz, L. H., Tillitt, D. E., and Hannink, M. (1996). Embryotoxicity 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.
6. Carney, S. A., Chen, J., Burns, C. G., Xiong, K. M., Peterson, R. E., and Heideman, W. (2006). Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish. Mol. Pharmacol. 70, 549-561.
7. Clark, B. W., Matson, C. W., Jung, D., and Di Giulio, R. T. (2010). AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat. Toxicol. 99, 232-240.
8. Dolmetsch, R. E., Xu, K., and Lewis, R. S. (1998). Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-966.
9. Dong, W., Teraoka, H., Tsujimoto, Y., Stegeman, J. J., and Hiraga, T. (2004). Role of aryl hydrocarbon receptor in mesencephalic circulation failure and apoptosis in zebrafish embryos exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 77, 109-116.
10. Driever, W., and Rangini, Z. (1993). Characterization of a cell line derived from zebrafish (Brachydanio rerio) embryos. In vitro Cell Dev. Biol. Anim. 29, 749-754.
11. Frey, N., McKinsey, T. A., and Olson, E. N. (2000). Decoding calcium signals involved in cardiac growth and function. Nat. Med. 6, 1221-1227.
12. Garner, L. V., and Di Giulio, R. T. (2012) Glutathione transferase pi class 2 (GSTp2) protects against the cardiac deformities caused by exposure to PAHs but not PCB-126 in zebrafish embryos. Comp. Biochem. Physiol. C 155, 573-579.
13. Handley-Goldstone, H. M., Grow, M. W., and Stegeman, J. J. (2005). Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol. Sci. 85, 683-693.
14. Hoffer, A., Chang, C. Y., and Puga, A. (1996). Dioxin induces transcription of fos and jun genes by Ah receptor-dependent and -independent pathways. Toxicol. Appl. Pharmacol. 141, 238-247.
15. Huang, C. J., Tu, C. T., Hsiao, C. D., Hsieh, F. J., and Tsai, H. J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
16. Incardona, J. P., Collier, T. K., and Scholz, N. L. (2004). Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 196, 191-205.
17. Incardona, J. P., Carls, M. G., Teraoka, H., Sloan, C. A., Collier, T. K., and Scholz, N. L. (2005). Aryl hydrocarbon receptorindependent toxicity of weathered crude oil during fish development. Environ. Health Persp. 113, 1755-1762.
18. Incardona, J. P., Linbo, T. L., and Scholz, N. L. (2011). Cardiac toxicity of 5-ring polycyclic aromatic hydrocarbons is differentially dependent on the aryl hydrocarbon receptor 2 isoform during zebrafish development. Toxicol. Appl. Pharmacol. 257, 242-249.
19. Kawaguchi, M., Hager, H. A., Wada, A., Koyama, T., Chang, M. S. and Bader, D. M. (2008). Identification of a novel intracellular interaction domain essential for Bves function. PLoS One 3, e2261.
20. Kuwasako, K., Shimekake, Y., Masuda, M., Nakahara, K., Yoshida, T., Kitaura, M., Kitamura, K., Eto, T., and Sakata, T. (2000). Visualization of the calcitonin receptor-like receptor and its receptor activity-modifying proteins during internalization and recycling. J. Biol. Chem. 275, 29602-29609.
21. Lanham, K. E., Plavicki, J., Peterson, R. E., and Heideman, W. (2014). Cardiac myocyte-specific AHR activation phenocopies TCDD-induced toxicity in zebrafish. Toxicol. Sci. 141, 141-154.
22. Matson, C. W., Clark, B. W., Jenny, M. J., Fleming, C. R., Hahn, M. E., and Di Giulio, R. T. (2008). Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquat. Toxicol. 87, 289-295.
23. Metzger, J. M., and Westfall, M. V. (2004). Covalent and noncovalent modification of thin filament action: the essential role of troponin in cardiac muscle regulation. Circ. Res. 94, 146-158.
24. Mounho, B. J., Davila, D. R., and Burchiel, S. W. (1997). Characterization of intracellular calcium responses produced by polycyclic aromatic hydrocarbons in surface marker-defined human peripheral blood mononuclear cells. Toxicol. Appl. Pharmacol. 145, 323-330.
25. Mounho, B. J., and Burchiel, S. W. (1998). Alterations in human B cell calcium homeostasis by polycyclic aromatic hydrocarbons: possible associations with cytochrome P450 metabolism and increased protein tyrosine phosphorylation. Toxicol. Appl. Pharmacol. 149, 80-89.
26. Neilson, A. H. (1998). PAHs and Related Compounds-Biology. Springer, Berlin, Germany.
27. Nebert, D. W., Dalton, T. P., Okey, A. B., and Gonzalez, F. J. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 279, 23847-23850.
28. Nusslein-Volhard, C., and Dahm, R. (2002). Zebrafish. A Practical Approach. Oxford University Press, Oxford.
29. Prasch, A. L., Teraoka, H., Carney, S. A., Dong, W., Hiraga, T., Stegeman, J. J., Heideman, W., and Peterson, R. E. (2003) Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzop-dioxin developmental toxicity in zebrafish. Toxicol. Sci. 76, 138-150.
30. Rivkees, S. A., and Wendler, C. C. (2012). Regulation of cardiovascular development by adenosine and adenosine-mediated embryo protection. Thromb. Vasc. Biol. 32, 851-885.
31. Romero, D. L., Mounho, B. J., Lauer, F. T., Born, J. L., and Burchiel, S. W. (1997) Depletion of glutathione by benzo(a)pyrene metabolites, ionomycin, thapsigargin, and phorbol myristate in human peripheral blood mononuclear cells. Toxicol. Appl. Pharmacol. 144, 62-69.
32. Schmitt, J. P., Debold, E. P., Ahmad, F., Armstrong, A., Frederico, A., Conner, D. A., Mende, U., Lohse, M. J., Warshaw, D., Seidman, C. E., et al. (2006). Cardiac myosin missense mutations cause dilated cardiomyopathy in mouse models and depress molecular motor function. Proc. Natl Acad. Sci. U. S. A. 103, 14525-14530.
33. Söllner, C., Burghammer, M., Busch-Nentwich, E., Berger, J., Schwarz, H., Riekel, C., and Nicolson, T. (2003). Control of crystal size and lattice formation by starmaker in otolith biomineralization. Science 302, 282-286.
34. Timme-Laragy, A. R., Cockman, C. J., Matson, C. W., and Di Giulio, R. T. (2007). Synergistic induction of AHR regulated genes in developmental toxicity from co-exposure to two model PAHs in zebrafish. Aquat. Toxicol. 85, 241-250.
35. Timme-Laragy, A. R., Van Tiem, L. A., Linney, E. A., and Di Giulio, R. T. (2009). Antioxidant responses and NRF2 in synergistic developmental toxicity of PAHs in zebrafish. Toxicol. Sci. 109, 217-227.
36. Uno, S., Dalton, T. P., Sinclair, P. R., Gorman, N., Wang, B., Smith, A. G., Miller, M. L., Shertzer, H. G., and Nebert, D. W. (2004). Cyp1a1(-/-) male mice: protection against high-dose TCDDinduced lethality and wasting syndrome, and resistance to intrahepatocyte lipid accumulation and uroporphyria. Toxicol. Appl. Pharmacol. 196, 410-421.
37. Van Tiem, L. A., and Di Giulio, R. T. (2011). AHR2 knockdown prevents PAH-mediated cardiac toxicity and XRE- and ARE-associated gene induction in zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 254, 280-287.
38. Wassenberg, D. M., and Di Giulio, R. T. (2004). Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor Agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ. Health Perspect. 112, 1658-1664.
39. Whitehead, A., Triant, D. A., Champlin, D., and Nacci, D. (2010). Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Mol. Ecol. 19, 5186-5203.
40. Zheng, Q., and Zhao, Y. (2007). The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein-protein interaction. Biol. Cell. 99, 489-502.