Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish

Molecular Pharmacology

Volumn 70, Issue 2, 2006, Pages 549-561

  Carney, Sara A ^a   Chen, Jing ^a   Burns, C Geoffrey ^b   Xiong, Kong M ^a   Peterson, Richard E ^a   Heideman, Warren ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARDIOTOXICITY; CONTROLLED STUDY; FERTILIZATION; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; HEART DEVELOPMENT; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART STROKE VOLUME; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL CIRCULATION; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; UNINDEXED SEQUENCE; XENOBIOTIC METABOLISM; ZEBRA FISH;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; FEMALE; GENE EXPRESSION PROFILING; HEART; MALE; MYOCARDIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, ARYL HYDROCARBON; RESEARCH DESIGN; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION, GENETIC; XENOBIOTICS; ZEBRAFISH;

EID: 33746238115     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.025304     Document Type: Article

References (62)

1. Antkiewicz DS, Burns CG, Carney SA, Peterson RE, and Heideman W (2005) Heart malformation is an early response to TCDD in embryonic zebrafish. Toxicol Sci 84:368-377.
2. Bailis JM and Forsburg SL (2004) MCM proteins: DNA damage, mutagenesis and repair. Curr Opin Genet Dev 14:17-21.
3. Belair CD, Peterson RE, and Heideman W (2001) Disruption of erythropoiesis by dioxin in the zebrafish. Dev Dyn 222:581-594.
4. Brunstrom B and Lund J (1988) Differences between chick and turkey embryos in sensitivity to 3,3′,4,4′-tetrachloro-biphenyl and in concentration/affinity of the hepatic receptor for 2,3,7,8-tetrachlorodibenzo-p- dioxin. Comp Biochem Physiol C 91:507-512.
5. Bunger MK, Moran SM, Glover E, Thomae TL, Lahvis GP, Lin BC, and Bradfield CA (2003) Resistance to 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity and abnormal liver development in mice carrying a mutation in the nuclear localization sequence of the aryl hydrocarbon receptor. J Biol Chem 278:17767-17774.
6. Burns CG and MacRae CA (2006) Purification of hearts from zebrafish embryos [published erratum appears in Biotechniques 40:596, 2006]. Biotechniques 40:274, 276, 278.
7. Canga L, Levi R, and Rifkind AB (1988) Heart as a target organ in 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity: decreased beta-adrenergic responsiveness and evidence of increased intracellular calcium. Proc Natl Acad Sci USA 85:905-909.
8. Canga L, Paroli L, Blanck TJ, Silver RB, and Rifkind AB (1993) 2,3,7,8-Tetrachlorodibenzo-p-dioxin increases cardiac myocyte intracellular calcium and progressively impairs ventricular contractile responses to isoproterenol and to calcium in chick embryo hearts. Mol Pharmacol 44:1142-1151.
9. Carney SA, Peterson RE, and Heideman W (2004) 2,3,7,8-Tetrachlorodibenzo- p-dioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1A-independent mechanism in zebrafish. Mol Pharmacol 66:512-521.
10. Chambers DJ (2003) Mechanisms and alternative methods of achieving cardiac arrest. Ann Thorac Surg 75:S661-S666.
11. Cheung MO, Gilbert EF, and Peterson RE (1981) Cardiovascular teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the chick embryo. Toxicol Appl Pharmacol 61:197-204.
12. Coucelo J, Joachim N, and Coucelo J (2000) Calculation of volumes and systolic indices of heart ventricle from Halobatrachus didactylus: echocardiographic non-invasive method. J Exp Zool 286:585-595.
13. Dong W, Teraoka H, Tsujimoto Y, Stegeman JJ, 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.
14. Dong W, Teraoka H, Yamazaki K, Tsukiyama S, Imani S, Imagawa T, Stegeman JJ, Peterson RE, and Hiraga T (2002) 2,3,7,8-Tetrachlorodibenzo-p-dioxin toxicity in the zebrafish embryo: local circulation failure in the dorsal midbrain is associated with increased apoptosis. Toxicol Sci 69:191-201.
15. Ebert AM, Hume GL, Warren KS, Cook NP, Burns CG, Mohideen MA, Siegal G, Yelon D, Fishman MC, and Garrity DM (2005) Calcium extrusion is critical for cardiac morphogenesis and rhythm in embryonic zebrafish hearts. Proc Natl Acad Sci USA 102:17705-17710.
16. Eisen MB, Spellman PT, Brown PO, and Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868.
17. Elonen GE, Sphear RL, Holcombe GW, and Johnson RD (1998) Comparative toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to seven freshwater species during early life-stage development. Environ Toxicol Chem 17:472-483.
18. Fernandez-Salguero PM, Hilbert DM, Rudikoff S, Ward JM, and Gonzalez FJ (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140:173-179.
19. Fernandez-Salguero PM, Ward JM, Sundberg JP, and Gonzalez FJ (1997) Lesions of aryl-hydrocarbon receptor-deficient mice. Vet Pathol 34:605-614.
20. Fisher MT, Nagarkatti M, and Nagarkatti PS (2004) Combined screening of thymocytes using apoptosis-specific cDNA array and promoter analysis yields novel gene targets mediating TCDD-induced toxicity. Toxicol Sci 78:116-124.
21. Frueh FW, Hayashibara KC, Brown PO, and Whitlock JP Jr (2001) Use of cDNA microarrays to analyze dioxin-induced changes in human liver gene expression. Toxicol Lett 122:189-203.
22. Grandori C, Cowley SM, James LP, and Eisenman RN (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu Rev Cell Dev Biol 16:653-699.
23. Guiney PD, Walker MK, Spitsbergen JM, and Peterson RE (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.
24. Hahn ME (2003) Evolutionary and physiological perspectives on Ah receptor function and dioxin toxicity, in Dioxins and Health (Schecter A GT ed) pp 559-602, John Wiley and Sons, Hoboken, NJ.
25. Handley-Goldstone HM, Grow MW, and Stegeman JJ (2005) Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol Sci 85:683-693.
26. Hanlon PR, Zheng W, Ko AY, and Jefcoate CR (2005) Identification of novel TCDD-regulated genes by microarray analysis. Toxicol Appl Pharmacol 202:215-228.
27. Helder T (1980) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on early life stages of the pike (Esox lucius, L.). Sci Total Environ 14:183-193.
28. Helder T (1981) Effects of 2,3,7,8-tetrachlorodibenzo-dioxin (TCDD) on early life stages of rainbow trout (Salmo gairdneri, Richardson). Toxicology 19:101-112.
29. Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, and Peterson RE (1997) Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish (Danio rerio). Toxicol Appl Pharmacol 142:56-68.
30. Hornung MW, Spitsbergen JM, and Peterson RE (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.
31. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, and Gharib M (2003) Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature (Lond) 42:172-177.
32. Hu N, Sedmera D, Yost HJ, and Clark EB (2000) Structure and function of the developing zebrafish heart. Anat Rec 260:148-157.
33. Ivnitski I, Elmaoued R, and Walker MK (2001) 2,3,7,8-Tetrachlorodibenzo- p-dioxin (TCDD) inhibition of coronary development is preceded by a decrease in myocyte proliferation and an increase in cardiac apoptosis. Teratol 64:201-212.
34. Jin B, Kim G, Park DW, and Ryu DY (2004) Microarray analysis of gene regulation in the Hepa1c1c7 cell line following exposure to the DNA methylation inhibitor 5-aza-2′-deoxycytidine and 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol In Vitro 18:659-664.
35. Lahvis G, Lindell S, Thomas R, McCuskey R, Murphy C, Glover E, Bentz M, Southard J, and Bradfield C (2000) Portosystemic shunting and persistent fetal vascular structures in aryl hydrocarbon receptor-deficient mice. Proc Natl Acad Sci USA 97:10442-10447.
36. Lin TM, Ko K, Moore RW, Buchanan DL, Cooke PS, and Peterson RE (2001) Role of the aryl hydrocarbon receptor in the development of control and 2,3,7,8-tetrachlorodibenzo-p-dioxin-exposed male mice. J Toxicol Environ Health 64:327-342.
37. Lund AK, Goens MB, Kanagy NL, and Walker MK (2003) Cardiac hypertrophy in aryl hydrocarbon receptor null mice is correlated with elevated angiotensin II, endothelin-1, and mean arterial blood pressure. Toxicol Appl Pharmacol 193:177-187.
38. Mably JD, Mohideen MA, Burns CG, Chen JN, and Fishman MC (2003) heart of glass regulates the concentric growth of the heart in zebrafish. Curr Biol 13:2138-2147.
39. Martinez JM, Afshari CA, Bushel PR, Masuda A, Takahashi T, and Walker NJ (2002) Differential toxicogenomic responses to 2,3,7,8-tetrachlorodibenzo-p- dioxin in malignant and nonmalignant human airway epithelial cells. Toxicol Sci 69:409-423.
40. Nolte T, Kaufmann W, Schorsch F, Soames T, and Weber E (2005) Standardized assessment of cell proliferation: the approach of the RITA-CEPA working group. Exp Toxicol Pathol 57:91-103.
41. Prasch AL, Teraoka H, Carney SA, Dong W, Hiraga T, Stegeman JJ, Heideman W, and Peterson RE (2003) Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol Sci 76:138-150.
42. Puga A, Barnes SJ, Dalton TP, Chang C, Knudsen ES, and Maier MA (2000a) Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 275:2943-2950.
43. Puga A, Maier A, and Medvedovic M (2000b) The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem Pharmacol 60:1129-1142.
44. Rifkind AB, Sassa S, Reyes J, and Muschick H (1985) Polychlorinated aromatic hydrocarbon lethality, mixed-function oxidase induction, and uroporphyrinogen decarboxylase inhibition in the chick embryo: dissociation of dose-response relationships. Toxicol Appl Pharmacol 78:268-279.
45. Rowlands JC and Gustafsson JA (1997) Aryl hydrocarbon receptor-mediated signal transduction. Crit Rev Toxicol 27:109-134.
46. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374-378.
47. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I, et al. (1989) Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 2:358-367.
48. Schmidt JV and Bradfield CA (1996) Ah receptor signaling pathways. Annu Rev Cell Dev Biol 12:55-89.
49. Schmidt JV, Su GH, Reddy JK, Simon MC, and Bradfield CA (1996) Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci USA 93:6731-6736.
50. Sommer RJ, Hume AJ, Ciak JM, Vannostrand JJ, Friggens M, and Walker MK (2005) Early developmental 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure decreases chick embryo heart chronotropic response to isoproterenol but not to agents affecting signals downstream of the beta-adrenergic receptor. Toxicol Sci 83:363-371.
51. Spitsbergen JM, Walker MK, Olson JR, and Peterson RE (1991) Pathologic alterations in early life stages of lake trout, Salvelinus namaycush, exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin as fertilized eggs. Aquat Toxicol 19:41-72.
52. Teraoka H, Dong W, Ogawa S, Tsukiyama S, Okuhara Y, Niiyama M, Ueno N, Peterson RE, and Hiraga T (2002) 2,3,7,8-Tetrachlorodibenzo-p-dioxin toxicity in the zebrafish embryo: altered regional blood flow and impaired lower jaw development. Toxicol Sci 65:192-199.
53. Thackaberry EA, Bedrick EJ, Goens MB, Danielson L, Lund AK, Gabaldon D, Smith SM, and Walker MK (2003) Insulin regulation in AhR-null mice: embryonic cardiac enlargement, neonatal macrosomia, and altered insulin regulation and response in pregnant and aging AhR-null females. Toxicol Sci 76:407-417.
54. Thackaberry EA, Gabaldon DM, Walker MK, and Smith SM (2002) Aryl hydrocarbon receptor null mice develop cardiac hypertrophy and increased hypoxia-inducible factor-1alpha in the absence of cardiac hypoxia. Cardiovasc Toxicol 2:263-274.
55. Thackaberry EA, Jiang Z, Johnson CD, Ramos KS, and Walker MK (2005a) Toxicogenomic profile of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the murine fetal heart: modulation of cell cycle and extracellular matrix genes. Toxicol Sci 88:231-241.
56. Thackaberry EA, Nunez BA, Ivnitski-Steele ID, Friggins M, and Walker MK (2005b) Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on murine heart development: alteration in fetal and postnatal cardiac growth, and postnatal cardiac chronotropy. Toxicol Sci 88:242-249.
57. Vezina CM, Walker NJ, and Olson JR (2004) Subchronic exposure to TCDD, PeCDF, PCB126, and PCB153: effect on hepatic gene expression. Environ Health Perspect 112:1636-1644.
58. Walisser JA, Bunger MK, Glover E, and Bradfield CA (2004) Gestational exposure of Ahr and Arnt hypomorphs to dioxin rescues vascular development. Proc Natl Acad Sci USA 101:16677-16682.
59. Walker MK and Catron TF (2000) Characterization of cardiotoxicity induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin and related chemicals during early chick embryo development. Toxicol Appl Pharmacol 167:210-221.
60. Walker MK, Pollenz RS, and Smith SM (1997) Expression of the aryl hydrocarbon receptor (AhR) and AhR nuclear translocator during chick cardiogenesis is consistent with 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced heart defects. Toxicol Appl Pharmacol 143:407-419.
61. Wisk JD and Cooper KR (1990) The stage specific toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in embryos of the Japanese medaka (Oryzias latipes). Environ Toxicol Chem 9:1159-1169.
62. Xia X, Cheng A, Akinmade D, and Hamburger AW (2003) The N-terminal 24 amino acids of the p55 gamma regulatory subunit of phosphoinositide 3-kinase binds Rb and induces cell cycle arrest. Mol Cell Biol 23:1717-1725.