Role of DNA methylation of AHR1 and AHR2 promoters in differential sensitivity to PCBs in Atlantic Killifish, Fundulus heteroclitus

Aquatic Toxicology

Volumn 101, Issue 1, 2011, Pages 288-294

  Aluru, Neelakanteswar ^a   Karchner, Sibel I ^a   Hahn, Mark E ^a  

^a WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

DNA methylation; Epigenetics; Killifish

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; AROMATIC HYDROCARBON RECEPTOR 1; AROMATIC HYDROCARBON RECEPTOR 2; BISULFITE; CYTOCHROME P450 1A; DNA; MESSENGER RNA; POLYCHLORINATED BIPHENYL; UNCLASSIFIED DRUG;

DNA; GENE EXPRESSION; METHYLATION; PCB; POLLUTION EXPOSURE;

ANIMAL CELL; ARTICLE; ATLANTIC KILLFISH; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; ENZYME INDUCTION; FISH; GENE EXPRESSION; GENETIC RESISTANCE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASE SEQUENCE; CPG ISLANDS; DNA METHYLATION; DNA PRIMERS; FUNDULIDAE; MASSACHUSETTS; MOLECULAR SEQUENCE DATA; POLYCHLORINATED BIPHENYLS; PROMOTER REGIONS, GENETIC; RECEPTORS, ARYL HYDROCARBON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; WATER POLLUTANTS, CHEMICAL;

MASSACHUSETTS; NEW BEDFORD HARBOR; UNITED STATES;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

EID: 78649908355     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2010.10.010     Document Type: Article

References (39)

1. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308:1466-1469.
2. Arzuaga X., Calcaño W., Elskus A. The DNA de-methylating agent 5-azacytidine does not restore CYP1A induction in PCB resistant Newark Bay killifish (Fundulus heteroclitus). Mar. Environ. Res. 2004, 58:517-520.
3. Bello S.M., Franks D.G., Stegeman J.J., Hahn M.E. Acquired resistance to aryl hydrocarbon receptor agonists in a population of Fundulus heteroclitus from a marine superfund site: in vivo and in vitro studies on the induction of xenobiotic metabolizing enzymes. Toxicol. Sci. 2001, 60:77-91.
4. Burnett K.G., Bain L.J., Baldwin W.S., Callard G.V., Cohen S., Di Giulio R.T., Evans D.H., Gómez-Chiarri M., Hahn M.E., Hoover C.A., Karchner S.I., Katoh F., Maclatchy D.L., Marshall W.S., Meyer J.N., Nacci D.E., Oleksiak M.F., Rees B.B., Singer T.D., Stegeman J.J., Towle D.W., Van Veld P.A., Vogelbein W.K., Whitehead A., Winn R.N., Crawford D.L. Fundulus as the premier teleost model in environmental biology: opportunities for new insights using genomics. Comp. Biochem. Physiol. D Genomics Proteomics 2007, 2:257-286.
5. Clark B.W., Matson C.W., Jung D., Di Giulio R.T. AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat. Toxicol. 2010, 99:232-240.
6. Cooper D.N., Gerber-Huber S., Nardelli D., Schubiger J.L., Wahli W. The distribution of the dinucleotide CpG and cytosine methylation in the vitellogenin family. J. Mol. Evol. 1987, 25:107-115.
7. Cooper D.N., Krawczak M. Cytosine methylation and the fate of CpG dinucleotides in vertebrate genomes. Hum. Genet. 1989, 83:181-188.
8. Elskus A.A., Monosson E., McElroy A.E., Stegeman J.J., Woltering D.S. Altered CYP1A expression in Fundulus heteroclitus adults and larvae: a sign of pollutant resistance?. Aquat. Toxicol. 1999, 45:99-113.
9. Feinberg A.P. Phenotypic plasticity and the epigenetics of human disease. Nature 2007, 447:433-440.
10. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J. Mol. Biol. 1987, 196:261-282.
11. Hahn M.E. Mechanisms of innate and acquired resistance to dioxin-like compounds. Rev. Toxicol. 1998, 2:395-443.
12. Hahn, M.E., Karchner, S.I., Franks, D.G., Evans, B.R., Nacci, D., Champlin, D., Cohen, S., 2005. Mechanism of PCB- and dioxin-resistance in fish in the Hudson River estuary: role of receptor polymorphisms. Hudson River Foundation Grant 004/02A report. p. 33. http://www.hudsonriver.org/ls/.
13. Hahn M.E., Karchner S.I., Franks D.G., Merson R.R. Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics 2004, 14:131-143.
14. Hahn M.E., Karchner S.I., Shapiro M.A., Perera S.A. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13743-13748.
15. Hankinson O. The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 1995, 35:307-340.
16. Karchner S.I., Franks D.G., Powell W.H., Hahn M.E. Regulatory interactions among three members of the vertebrates aryl hydrocarbon receptor family: AHR repressor AHR1 and AHR2. J. Biol. Chem. 2002, 277:6949-6959.
17. Karchner S.I., Powell W.H., Hahn M.E. Structural and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. Evidence for a novel class of ligand-binding basis helix-loop-helix Per-ARNT-Sim(bHLH-PAS) factors. J. Biol. Chem. 1999, 274:33814-33824.
18. Lake J.L., McKinney R., Lake C.A., Osterman F.A., Heltshe J. Comparisons of patterns of polychlorinated biphenyl congeners in water, sediment, and indigenous organisms from New Bedford Harbor, Massachusetts. Arch. Environ. Contam. Toxicol. 1995, 29:207-220.
19. Merson R.R., Karchner S.I., Hahn M.E. Interaction of fish aryl hydrocarbon receptor paralogs (AHR1 and AHR2) with the retinoblastoma protein. Aquat. Toxicol. 2009, 94:47-55.
20. Meyer J.N., Nacci D.E., Di Giulio R.T. Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol. Sci. 2002, 68:69-81.
21. Mulero-Navarro S., Carvajal-Gonzalez J.M., Herranz M., Ballestar E., Fraga M.F., Ropero S., Esteller M., Fernandez-Salguero P.M. The dioxin receptor is silenced by promoter hypermethylation in human acute lymphoblastic leukemia through inhibition of Sp1 binding. Carcinogenesis 2006, 27:1099-1104.
22. Nacci D., Coiro L., Champlin D., Jayaraman S., McKinney R., Gleason T., Munns W.R., Specker J.L., Cooper K. Adaptation of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar. Biol. 1999, 134:9-17.
23. Nacci D., Coiro L., Champlin D., Jayaraman S., McKinney R. Predicting the occurrence of genetic adaptation to dioxin-like compounds in populations of the estuarine fish Fundulus heteroclitus. Environ. Toxicol. Chem. 2002, 21:1525-1532.
24. Nacci D.E., Champlin D., Jayaraman S. Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuar. Coast. 2010, 33:853-864.
25. Oleksiak, M.F., Karchner, S.I., Jenny, M.J., Franks, D.G., Hahn, M.E., 2010. Transcriptomic assessment of resistance to effects of an aryl hydrocarbon receptor agonist in embryos of Atlantic Killifish (Fundulus heteroclitus) from a Marine Superfund Site. (in preparation).
26. Powell W.H., Bright R., Bello S.M., Hahn M.E. Developmental and tissue-specific expression of AHR1, AHR2, and ARNT2 in dioxin-sensitive and -resistant populations of the marine fish Fundulus heteroclitus. Toxicol. Sci. 2000, 57:229-239.
27. Razin A., Riggs A.D. DNA methylation and gene function. Science 1980, 210:604-610.
28. Schulte P.M., Glemet H.C., Fiebig A.A., Powers D.A. Adaptive variation in lactate dehydrogenase-B gene expression: Role of a stress-responsive regulatory element. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:6597-6602.
29. Selker E.V., Stevens J.N. DNA methylation at asymmetric sites is associated with numerous transition mutations. Proc. Natl. Acad. Sci. U.S.A. 1985, 82:8114-8118.
30. Takai D., Jones P. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3740-3745.
31. Timme-Laragy A.R., Meyer J.N., Waterland R.A., Di Giulio R.T. Analysis of CpG methylation in the killifish CYP1A promoter. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2005, 141:406-411.
32. Van Veld P.A., Nacci D. Chemical tolerance: acclimation and adaptations to chemical stress. The Toxicology of Fishes 2008, 597-644. Taylor and Francis, Washington, DC. R.T. Di Guilio, D.E. Hinton (Eds.).
33. Van Veld P.A., Westbrook D.J. Evidence for depression of cytochrome P4501A in a population of chemically resistant mummichog (Fundulus heteroclitus). Environ. Sci. 1995, 3:221-234.
34. Weis J.S., Smith G., Zhou T., Santiago-Bass C., Weis P. Effects of contaminants on behavior: Biochemical mechanisms and ecological consequences. BioScience 2001, 51:209-217.
35. Whitehead A., Triant D.A., Champlin D., Nacci D. Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Mol Ecol. 2010, 10.1111/j.1365-294X.2010.04829.x.
36. Williams L.M., Oleksiak M.F. Signatures of selection in natural populations adapted to chronic pollution. BMC Evol. Biol. 2008, 8:282.
37. Williams L.M., Ma X., Boyko A.R., Bustamante C.D., Oleksiak M.F. SNP identification, verification, and utility for population genetics in a non-model genus. BMC Genet. 2010, 11:32.
38. Wills L.P., Matson C.W., Landon C.D., Di Giullio R.T. Characterization of the recalcitrant CYP1 phenotype found in Atlantic killifish (Fundulus heteroclitus) inhabiting a Superfund site on the Elizabeth River, VA. Aquat. Toxicol. 2010, 99:33-41.
39. Wirgin I., Waldman J.R. Resistance to contaminants in North American fish populations. Mutat. Res. 2004, 552:73-100.