Dynamic zebrafish interactome reveals transcriptional mechanisms of dioxin toxicity

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Alexeyenko, Andrey ^a,e   Wassenberg, Deena M ^b,f   Lobenhofer, Edward K ^c,g   Yen, Jerry ^b   Linney, Elwood ^b   Sonnhammer, Erik L L ^a   Meyer, Joel N ^d  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c Cogenics ^*  (United States)

^d DUKE UNIVERSITY   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

^f UNIVERSITY OF MINNESOTA   (United States)

^g AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYTOCHROME P450 1A; DIOXIN; IRON;

ANIMAL TISSUE; ARTICLE; CALCIUM METABOLISM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; GENE CONTROL; GENE EXPRESSION; GENETIC MARKER; GENETIC TRANSCRIPTION; IRON METABOLISM; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NONHUMAN; RETINA DEVELOPMENT; TOXICOGENETICS; ZEBRA FISH;

ANIMALS; DATABASES, GENETIC; DIOXINS; EUKARYOTA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GLYCOLYSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TERATOGENS; TRANSCRIPTION, GENETIC; ZEBRAFISH;

DANIO RERIO; EUKARYOTA; MAMMALIA;

EID: 77956508108     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010465     Document Type: Article

References (92)

1. Ivnitski I, Elmaoued R, 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. Teratology 64: 201-212.
2. Baccarelli A, Mocarelli P, Patterson DG, Jr., Bonzini M, Pesatori AC, et al. (2002) Immunologic effects of dioxin: new results from Seveso and comparison with other studies. Environ Health Perspect 110: 1169-1173.
3. Bock KW, Kohle C (2006) Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 72: 393-404.
4. Goldstone HM, Stegeman JJ (2006) Molecular mechanisms of 2,3,7,8-tetrachlorodibenzo-p-dioxin cardiovascular embryotoxicity. Drug Metab Rev 38: 261-289.
5. Karchner SI, Franks DG, Kennedy SW, Hahn ME (2006) The molecular basis for differential dioxin sensitivity in birds: role of the aryl hydrocarbon receptor. Proc Natl Acad Sci U S A 103: 6252-6257.
6. Knerr S, Schrenk D (2006) Carcinogenicity of 2,3,7,8-tetrachlorodibenzo-pdioxin in experimental models. Mol Nutr Food Res 50: 897-907.
7. Aragon AC, Kopf PG, Campen MJ, Huwe JK, Walker MK (2008) In utero and lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure: effects on fetal and adult cardiac gene expression and adult cardiac and renal morphology. Toxicol Sci 101: 321-330.
8. Augspurger TP, Tillitt DE, Bursian SJ, Fitzgerald SD, Hinton DE, et al. (2008) Embryo toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to the wood duck (Aix sponsa). Arch Environ Contam Toxicol 55: 659-669.
9. Humblet O, Birnbaum L, Rimm E, Mittleman MA, Hauser R (2008) Dioxins and cardiovascular disease mortality. Environ Health Perspect 116: 1443-1448.
10. Vezina CM, Lin TM, Peterson RE (2009) AHR signaling in prostate growth, morphogenesis, and disease. Biochem Pharmacol 77: 566-576.
11. Hahn ME (2001) Dioxin toxicology and the aryl hydrocarbon receptor: insights from fish and other non-traditional models. Mar Biotechnol (NY) 3: S224-238.
12. Carney SA, Prasch AL, Heideman W, Peterson RE (2006) Understanding dioxin developmental toxicity using the zebrafish model. Birth Defects Res A Clin Mol Teratol 76: 7-18.
13. Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, 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.
14. Cantrell SM, Joy-Schlezinger J, Stegeman JJ, Tillitt DE, 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.
15. Cantrell SM, Lutz LH, Tillitt DE, 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.
16. Hornung MW, Spitsbergen JM, 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.
17. Toomey BH, Bello S, Hahn ME, Cantrell S, Wright P, et al. (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.
18. Dong W, Teraoka H, Yamazaki K, Tsukiyama S, Imani S, et al. (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.
19. Prasch AL, Teraoka H, Carney SA, Dong W, Hiraga T, et al. (2003) Aryl hydrocarbon receptor 2 mediates 2,3,7,8-tetrachlorodibenzo-p-dioxin developmental toxicity in zebrafish. Toxicol Sci 76: 138-150.
20. Volz DC, Bencic DC, Hinton DE, Law JM, Kullman SW (2005) 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces organ- specific differential gene expression in male Japanese medaka (Oryzias latipes). Toxicol Sci 85: 572-584.
21. Antkiewicz DS, Peterson RE, Heideman W (2006) Blocking expression of AHR2 and ARNT1 in zebrafish larvae protects against cardiac toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 94: 175-182.
22. Xiong KM, Peterson RE, Heideman W (2008) Aryl hydrocarbon receptormediated down-regulation of sox9b causes jaw malformation in zebrafish embryos. Mol Pharmacol 74: 1544-1553.
23. Carney SA, Peterson RE, Heideman W (2004) 2,3,7,8-Tetrachlorodibenzo-pdioxin activation of the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator pathway causes developmental toxicity through a CYP1Aindependent mechanism in zebrafish. Mol Pharmacol 66: 512-521.
24. Handley-Goldstone HM, Grow MW, Stegeman JJ (2005) Cardiovascular gene expression profiles of dioxin exposure in zebrafish embryos. Toxicol Sci 85: 683-693.
25. Carney SA, Chen J, Burns CG, Xiong KM, Peterson RE, et al. (2006) Aryl hydrocarbon receptor activation produces heart-specific transcriptional and toxic responses in developing zebrafish. Mol Pharmacol 70: 549-561.
26. Yang L, Kemadjou JR, Zinsmeister C, Bauer M, Legradi J, et al. (2007) Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol 8: R227.
27. Chen J, Carney SA, Peterson RE, Heideman W (2008) Comparative genomics identifies genes mediating cardiotoxicity in the embryonic zebrafish heart. Physiol Genomics 33: 148-158.
28. Cusick ME, Klitgord N, Vidal M, Hill DE (2005) Interactome: gateway into systems biology. Hum Mol Genet 14 Spec No. 2: R171-181.
29. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2: 2366-2382.
30. Frueh FW, Hayashibara KC, Brown PO, Whitlock JP, Jr. (2001) Use of cDNA microarrays to analyze dioxin-induced changes in human liver gene expression. Toxicol Lett 122: 189-203.
31. Puga A, Maier A, Medvedovic M (2000) The transcriptional signature of dioxin in human hepatoma HepG2 cells. Biochem Pharmacol 60: 1129-1142.
32. Alexeyenko A, Sonnhammer EL (2009) Global networks of functional coupling in eukaryotes from comprehensive data integration. Genome Res 19: 1107-1116.
33. Berglund AC, Sjolund E, Ostlund G, Sonnhammer EL (2008) InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 36: D263-266.
34. Hulsen T, Huynen MA, de Vlieg J, Groenen PM (2006) Benchmarking ortholog identification methods using functional genomics data. Genome Biol 7: R31.
35. Sonnhammer EL, Koonin EV (2002) Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 18: 619-620.
36. Dehal P, Boore JL (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol 3: e314.
37. Antkiewicz DS, Burns CG, Carney SA, Peterson RE, Heideman W (2005) Heart malformation is an early response to TCDD in embryonic zebrafish. Toxicol Sci 84: 368-377.
38. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, et al. (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4: R28.
39. Zeeberg BR, Qin H, Narasimhan S, Sunshine M, Cao H, et al. (2005) High- Throughput GoMiner, an 'industrial-strength' integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics 6: 168.
40. Ideker T, Ozier O, Schwikowski B, Siegel AF (2002) Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 18 Suppl 1: S233-240.
41. Beyer A, Bandyopadhyay S, Ideker T (2007) Integrating physical and genetic maps: from genomes to interaction networks. Nat Rev Genet 8: 699-710.
42. Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37: 424-438.
43. Teraoka H, Dong W, Tsujimoto Y, Iwasa H, Endoh D, et al. (2003) Induction of cytochrome P450 1A is required for circulation failure and edema by 2,3,7,8-tetrachlorodibenzo-p-dioxin in zebrafish. Biochem Biophys Res Commun 304: 223-228.
44. Hodson PV, Qureshi K, Noble CA, Akhtar P, Brown RS (2007) Inhibition of CYP1A enzymes by alpha-naphthoflavone causes both synergism and antagonism of retene toxicity to rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 81: 275-285.
45. Wassenberg DM, Di Giulio RT (2004) Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ Health Perspect 112: 1658-1664.
46. Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT (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.
47. Billiard SM, Meyer JN, Wassenberg DM, Hodson PV, Di Giulio RT (2008) Non-additive effects of PAHs on early vertebrate development: mechanisms and implications for risk assessment. Toxicol Sci 105: 5-23.
48. Dragin N, Dalton TP, Miller ML, Shertzer HG, Nebert DW (2006) For dioxininduced birth defects, mouse or human CYP1A2 in maternal liver protects whereas mouse CYP1A1 and CYP1B1 are inconsequential. J Biol Chem 281: 18591-18600.
49. Uno S, Dalton TP, Sinclair PR, Gorman N, Wang B, et al. (2004) Cyp1a1(2/2) male mice: protection against high-dose TCDD-induced lethality and wasting syndrome, and resistance to intrahepatocyte lipid accumulation and uroporphyria. Toxicol Appl Pharmacol 196: 410-421.
50. Nebert DW, Karp CL (2008) Endogenous functions of the aryl hydrocarbon receptor (AHR): intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. J Biol Chem 283: 36061-36065.
51. Dragin N, Shi Z, Madan R, Karp CL, Sartor MA, et al. (2008) Phenotype of the Cyp1a1/1a2/1b12/2 triple-knockout mouse. Molecular Pharmacology 73: 1844-1856.
52. Rifkind AB (2006) CYP1A in TCDD toxicity and in physiology-with particular reference to CYP dependent arachidonic acid metabolism and other endogenous substrates. Drug Metab Rev 38: 291-335.
53. Pelclova D, Urban P, Preiss J, Lukas E, Fenclova Z, et al. (2006) Adverse health effects in humans exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Rev Environ Health 21: 119-138.
54. Sul D, Kim HS, Cho EK, Lee M, Kim HS, et al. (2009) 2,3,7,8-TCDD neurotoxicity in neuroblastoma cells is caused by increased oxidative stress, intracellular calcium levels, and tau phosphorylation. Toxicology 255: 65-71.
55. Urban P, Pelclova D, Lukas E, Kupka K, Preiss J, et al. (2007) Neurological and neurophysiological examinations on workers with chronic poisoning by 2,3,7,8-TCDD: follow-up 35 years after exposure. Eur J Neurol 14: 213-218.
56. Hill A, Howard CV, Strahle U, Cossins A (2003) Neurodevelopmental defects in zebrafish (Danio rerio) at environmentally relevant dioxin (TCDD) concentrations. Toxicol Sci 76: 392-399.
57. Blankenship AL, Hilscherova K, Nie M, Coady KK, Villalobos SA, et al. (2003) Mechanisms of TCDD-induced abnormalities and embryo lethality in white leghorn chickens. Comp Biochem Physiol C Toxicol Pharmacol 136: 47-62.
58. Carvalho PS, Tillitt DE (2004) 2,3,7,8-TCDD effects on visual structure and function in swim-up rainbow trout. Environ Sci Technol 38: 6300-6306.
59. Carvalho PS, Noltie DB, Tillitt DE (2004) Intra-strain dioxin sensitivity and morphometric effects in swim-up rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C Toxicol Pharmacol 137: 133-142.
60. Miettinen HM, Huuskonen H, Partanen AM, Miettinen P, Tuomisto JT, et al. (2004) Effects of epidermal growth factor receptor deficiency and 2,3,7,8-tetrachlorodibenzo-p-dioxin on fetal development in mice. Toxicol Lett 150: 285-291.
61. Yeager RL, Oleske DA, Millsap DS, Henshel DS (2006) Severe craniofacial malformations resulting from developmental exposure to dioxin. Reprod Toxicol 22: 811-812.
62. Puga A, Nebert DW, Carrier F (1992) Dioxin induces expression of c-fos and cjun proto-oncogenes and a large increase in transcription factor AP-1. DNA Cell Biol 11: 269-281.
63. Monteiro P, Gilot D, Le Ferrec E, Rauch C, Lagadic-Gossmann D, et al. (2008) Dioxin-mediated up-regulation of aryl hydrocarbon receptor target genes is dependent on the calcium/calmodulin/CaMKIalpha pathway. Mol Pharmacol 73: 769-777.
64. Dale YR, Eltom SE (2006) Calpain mediates the dioxin-induced activation and down-regulation of the aryl hydrocarbon receptor. Mol Pharmacol 70: 1481-1487.
65. Puga A, Ma C, Marlowe JL (2009) The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem Pharmacol 77: 713-722.
66. Davies R, Clothier B, Robinson SW, Edwards RE, Greaves P, et al. (2008) Essential role of the AH receptor in the dysfunction of heme metabolism induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Chem Res Toxicol 21: 330-340.
67. Lorenzen A, Kennedy SW, Bastien LJ, Hahn ME (1997) Halogenated aromatic hydrocarbon-mediated porphyrin accumulation and induction of cytochrome P4501A in chicken embryo hepatocytes. Biochem Pharmacol 53: 373-384.
68. Tittlemier SA, Kennedy SW, Hahn ME, Reddy CM, Norstrom RJ (2003) Naturally produced halogenated dimethyl bipyrroles bind to the aryl hydrocarbon receptor and induce cytochrome P4501A and porphyrin accumulation in chicken embryo hepatocytes. Environ Toxicol Chem 22: 1622-1631.
69. Belair CD, Peterson RE, Heideman W (2001) Disruption of erythropoiesis by dioxin in the zebrafish. Dev Dyn 222: 581-594.
70. Hahn ME, Chandran K (1996) Uroporphyrin accumulation associated with cytochrome P4501A induction in fish hepatoma cells exposed to aryl hydrocarbon receptor agonists, including 2,3,7,8-tetrachlorodibenzo-p-dioxin and planar chlorobiphenyls. Arch Biochem Biophys 329: 163-174.
71. Senft AP, Dalton TP, Nebert DW, Genter MB, Hutchinson RJ, et al. (2002) Dioxin increases reactive oxygen production in mouse liver mitochondria. Toxicol Appl Pharmacol 178: 15-21.
72. Shertzer HG, Clay CD, Genter MB, Chames MC, Schneider SN, et al. (2004) Uncoupling-mediated generation of reactive oxygen by halogenated aromatic hydrocarbons in mouse liver microsomes. Free Radic Biol Med 36: 618-631.
73. Biswas G, Srinivasan S, Anandatheerthavarada HK, Avadhani NG (2008) Dioxin-mediated tumor progression through activation of mitochondria-tonucleus stress signaling. Proc Natl Acad Sci U S A 105: 186-191.
74. Genter MB, Clay CD, Dalton TP, Dong H, Nebert DW, et al. (2006) Comparison of mouse hepatic mitochondrial versus microsomal cytochromes P450 following TCDD treatment. Biochem Biophys Res Commun 342: 1375-1381.
75. Park JY, Shigenaga MK, Ames BN (1996) Induction of cytochrome P4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin or indolo(3,2-b)carbazole is associated with oxidative DNA damage. Proc Natl Acad Sci U S A 93: 2322-2327.
76. Shertzer HG, Nebert DW, Puga A, Ary M, Sonntag D, et al. (1998) Dioxin causes a sustained oxidative stress response in the mouse. Biochem Biophys Res Commun 253: 44-48.
77. Nebert DW, Roe AL, Dieter MZ, Solis WA, Yang Y, et al. (2000) Role of the aromatic hydrocarbon receptor and [Ah] gene battery in the oxidative stress response, cell cycle control, and apoptosis. Biochem Pharmacol 59: 65-85.
78. Schlezinger JJ, Stegeman JJ (2001) Induction and suppression of cytochrome P450 1A by 3,39,4,49,5-pentachlorobiphenyl and its relationship to oxidative stress in the marine fish scup (Stenotomus chrysops). Aquat Toxicol 52: 101-115.
79. Schlezinger JJ, Struntz WD, Goldstone JV, Stegeman JJ (2006) Uncoupling of cytochrome P450 1A and stimulation of reactive oxygen species production by co-planar polychlorinated biphenyl congeners. Aquat Toxicol 77: 422-432.
80. Di Giulio RT, Meyer JN (2008) Reactive oxygen species and oxidative stress. In: Di Giulio RT, Hinton DE, eds. The Toxicology of Fishes. Washington, D.C.: Taylor and Francis. pp 273-324.
81. Nebert DW, Dalton TP, Okey AB, Gonzalez FJ (2004) Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J Biol Chem 279: 23847-23850.
82. Tijet N, Boutros PC, Moffat ID, Okey AB, Tuomisto J, et al. (2006) Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol Pharmacol 69: 140-153.
83. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH (2008) The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 18: 207-250.
84. Jonsson ME, Jenny MJ, Woodin BR, Hahn ME, Stegeman JJ (2007) Role of AHR2 in the expression of novel cytochrome P450 1 family genes, cell cycle genes, and morphological defects in developing zebra fish exposed to 3,39,4,49,5- pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 100: 180-193.
85. Mathew LK, Sengupta SS, Ladu J, Andreasen EA, Tanguay RL (2008) Crosstalk between AHR and Wnt signaling through R-Spondin1 impairs tissue regeneration in zebrafish. Faseb J 22: 3087-3096.
86. Andreasen EA, Mathew LK, Tanguay RL (2006) Regenerative growth is impacted by TCDD: gene expression analysis reveals extracellular matrix modulation. Toxicol Sci 92: 254-269.
87. Thackaberry EA, Jiang Z, Johnson CD, Ramos KS, Walker MK (2005) 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.
88. Keller JM, Meyer JN, Mattie M, Augspurger T, Rau M, et al. (1999/2000) Assessment of immunotoxicology in wild populations: Review and recommendations. Reviews in Toxicology 3: 167-212.
89. Birnbaum LS, Fenton SE (2003) Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 111: 389-394.
90. Driever W, Rangini Z (1993) Characterization of a cell line derived from zebrafish (Brachydanio rerio) embryos. In Vitro Cell Dev Biol Anim 29A: 749-754.
91. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449.
92. Huitson A (1966) The analysis of variance: Charles Griffin and company, Ltd.