Transcriptomic assessment of resistance to effects of an aryl hydrocarbon receptor (AHR) agonist in embryos of Atlantic killifish (Fundulus heteroclitus) from a marine Superfund site

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Oleksiak, Marjorie F ^a   Karchner, Sibel I ^b   Jenny, Matthew J ^b,c   Franks, Diana G ^b   Mark Welch, David B ^d   Hahn, Mark E ^b  

^a UNIVERSITY OF MIAMI   (United States)

^b WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

^c UNIVERSITY OF ALABAMA   (United States)

^d MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A; 3,4,5,3',4'-PENTACHLOROBIPHENYL; POLYCHLORINATED BIPHENYL; UNSPECIFIC MONOOXYGENASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYP1A GENE; CYPRINODONTIFORMES; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; FUNDULUS HETEROCLITUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORK; LARVAL DEVELOPMENT; MICROARRAY ANALYSIS; NONHUMAN; PYROSEQUENCING; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; UNITED STATES; ANIMAL; ANIMAL EMBRYO; BIOSYNTHESIS; DNA MICROARRAY; DRUG EFFECT; DRUG POTENTIATION; DRUG RESISTANCE; ENZYME INDUCTION; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; LARVA; METABOLISM; PRENATAL DEVELOPMENT; SEA; SEQUENCE ANALYSIS; TIME;

FUNDULUS HETEROCLITUS;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; DRUG RESISTANCE; EMBRYO, NONMAMMALIAN; ENZYME INDUCTION; FUNDULIDAE; GENE EXPRESSION PROFILING; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LARVA; OCEANS AND SEAS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYCHLORINATED BIPHENYLS; RECEPTORS, ARYL HYDROCARBON; SEQUENCE ANALYSIS, RNA; TIME FACTORS;

EID: 79956285594     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-263     Document Type: Article

References (77)

1. Darwin CR. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life 1859, London: John Murray, 1.
2. Schlötterer C. Towards a molecular characterization of adaptation in local populations. Curr Opin Genet Dev 2002, 12:683-687. 10.1016/S0959-437X(02)00349-0, 12433582.
3. Schulte PM. Environmental adaptations as windows on molecular evolution. Comp Biochem Physiol B Biochem Mol Biol 2001, 128:597-611. 10.1016/S1096-4959(00)00357-2, 11250554.
4. Powers DA, Schulte PM. Evolutionary adaptations of gene structure and expression in natural populations in relation to a changing environment: a multidisciplinary approach to address the million-year saga of a small fish. J Exper Zool 1998, 282:71-94.
5. Burnett KG, Bain LJ, Baldwin WS, Callard GV, Cohen S, Di Giulio RT, Evans DH, Gómez-Chiarri M, Hahn ME, Hoover CA, et al. Fundulus as the premier teleost model in environmental biology: Opportunities for new insights using genomics. Comp Biochem Physiol D 2007, 2:257-286.
6. Wirgin I, Waldman JR. Resistance to contaminants in North American fish populations. Mutat Res 2004, 552:73-100.
7. van Veld PA, Nacci DE. Chapter 13. Toxicity Resistance. The Toxicology of Fishes 2007, Taylor & Francis, Di Giulio RT, Hinton DE.
8. Nacci DE, Champlin D, Jayaraman S. Adaptation of the estuarine fish Fundulus heteroclitus (Atlantic killifish) to polychlorinated biphenyls (PCBs). Estuaries and Coasts 2010, 33:853-864.
9. Prince R, Cooper KR. Comparisons of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus: I. TCDD toxicity. Environ Toxicol Chem 1995, 14:579-587.
10. Prince R, Cooper KR. Comparisons of the effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on chemically impacted and nonimpacted subpopulations of Fundulus heteroclitus: II. Metabolic considerations. Environ Toxicol Chem 1995, 14:589-595.
11. Van Veld PA, Westbrook DJ. Evidence for depression of cytochrome P4501A in a population of chemically resistant mummichog (Fundulus heteroclitus). Environ Sci 1995, 3:221-234.
12. Ownby DR, Newman MC, Mulvey M, Vogelbein WK, Unger MA, Arzayus LF. Fish (Fundulus heteroclitus) populations with different exposure histories differ in tolerance of creosote-contaminated sediments. Environ Toxicol Chem 2002, 21:1897-1902.
13. Meyer JN, Nacci DE, Di Giulio RT. Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol Sci 2002, 68:69-81. 10.1093/toxsci/68.1.69, 12075112.
14. Nacci D, Coiro L, Champlin D, Jayaraman S, McKinney R, Gleason T, Munns WR, Specker JL, Cooper K. Adaptation of wild populatons of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Mar Biol 1999, 134:9-17.
15. Bello SM, Franks DG, Stegeman JJ, Hahn ME. 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. 10.1093/toxsci/60.1.77, 11222875.
16. Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S. Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 2002, 21:1525-1532.
17. Okey AB. An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI. Toxicol Sci 2007, 98:5-38. 10.1093/toxsci/kfm096, 17569696.
18. Ma Q. Xenobiotic-activated receptors: from transcription to drug metabolism to disease. Chem Res Toxicol 2008, 21:1651-1671. 10.1021/tx800156s, 18707139.
19. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH. The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 2008, 18:207-250. 2583464, 18540824.
20. Powell WH, Bright R, Bello SM, Hahn ME. 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. 10.1093/toxsci/57.2.229, 11006353.
21. Bello SM. Characterization of resistance to halogenated aromatic hydrocarbons in a population of Fundulus heteroclitus from a marine superfund site. Ph.D. Thesis 1999, Woods Hole Oceanographic Institution/Massachusetts Institute of Technology.
22. Williams LM, Oleksiak MF. Signatures of selection in natural populations adapted to chronic pollution. BMC Evol Biol 2008, 8:282. 10.1186/1471-2148-8-282, 2570689, 18847479.
23. Williams LM, Ma X, Boyko AR, Bustamante CD, Oleksiak MF. SNP identification, verification, and utility for population genetics in a non-model genus. BMC Genet 2010, 11:32. 2874759, 20433726.
24. Aluru N, Karchner SI, Hahn ME. Role of DNA methylation of AHR1 and AHR2 promoters in differential sensitivity to PCBs in Atlantic Killifish, Fundulus heteroclitus. Aquat Toxicol 2011, 101:288-294. 10.1016/j.aquatox.2010.10.010, 21111492.
25. Hahn ME, Karchner SI, Franks DG, Evans BR, Nacci D, Champlin D, Cohen S. Mechanism of PCB- and Dioxin-Resistance in Fish in the Hudson River Estuary: Role of Receptor Polymorphisms. Final Report, Hudson River Foundation Grant 004/02A 2005, http://www.hudsonriver.org/ls/
26. Carney SA, Peterson RE, Heideman W. 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 2004, 66:512-521.
27. Wassenberg DM, Di Giulio RT. Synergistic embryotoxicity of polycyclic aromatic hydrocarbon aryl hydrocarbon receptor agonists with cytochrome P4501A inhibitors in Fundulus heteroclitus. Environ Health Persp 2004, 112:1658-1664.
28. Billiard SM, Timme-Laragy AR, Wassenberg DM, Cockman C, Di Giulio RT. The role of the aryl hydrocarbon receptor pathway in mediating synergistic developmental toxicity of polycyclic aromatic hydrocarbons to zebrafish. Toxicol Sci 2006, 92:526-536. 10.1093/toxsci/kfl011, 16687390.
29. Billiard SM, Meyer JN, Wassenberg DM, Hodson PV, Di Giulio RT. Nonadditive effects of PAHs on Early Vertebrate Development: mechanisms and implications for risk assessment. Toxicol Sci 2008, 105:5-23. 10.1093/toxsci/kfm303, 2734299, 18156145.
30. Matson CW, Clark BW, Jenny MJ, Fleming CR, Hahn ME, Di Giulio RT. Development of the morpholino gene knockdown technique in Fundulus heteroclitus: a tool for studying molecular mechanisms in an established environmental model. Aquat Toxicol 2008, 87:289-295. 10.1016/j.aquatox.2008.02.010, 2413436, 18378331.
31. Oleksiak MF, Kolell KJ, Crawford DL. Utility of natural populations for microarray analyses: Isolation of genes necessary for functional genomic studies. Mar Biotechnol 2001, 3:S203-S211. 10.1007/s10126-001-0043-0, 14961317.
32. Oleksiak MF, Churchill GA, Crawford DL. Variation in gene expression within and among natural populations. Nat Genet 2002, 32:261-266. 10.1038/ng983, 12219088.
33. Fisher MA, Oleksiak MF. Convergence and divergence in gene expression among natural populations exposed to pollution. BMC Genomics 2007, 8:108. 10.1186/1471-2164-8-108, 1868758, 17459166.
34. Oleksiak MF. Changes in gene expression due to chronic exposure to environmental pollutants. Aquat Toxicol 2008, 90:161-171. 10.1016/j.aquatox.2008.08.010, 2584160, 18929415.
35. Bozinovic B, Oleksiak MF. Embryonic gene expression among pollutant resistant and sensitive Fundulus heteroclitus populations. Aquat Toxicol 2010, 98:221-229. 10.1016/j.aquatox.2010.02.022, 20363516.
36. Shanklin DR. Studies on the Fundulus chorion. J Cell Comp Physiol 1959, 53:1-11. 10.1002/jcp.1030530102, 14445474.
37. Oleksiak MF, Roach JL, Crawford DL. Natural variation in cardiac metabolism and gene expression in Fundulus heteroclitus. Nat Genet 2005, 37:67-72. 1447534, 15568023.
38. Scott CP, Williams DA, Crawford DL. The effect of genetic and environmental variation on metabolic gene expression. Mol Ecol 2009, 18:2832-2843. 10.1111/j.1365-294X.2009.04235.x, 2705469, 19500250.
39. Scott CP, VanWye J, McDonald MD, Crawford DL. Technical analysis of cDNA microarrays. PLoS One 2009, 4:e4486. 10.1371/journal.pone.0004486, 2637424, 19221589.
40. Whitehead A, Crawford DL. Neutral and adaptive variation in gene expression. Proc Natl Acad Sci USA 2006, 103:5425-5430. 10.1073/pnas.0507648103, 1414633, 16567645.
41. Bozinovic G, Sit TL, Hinton DE, Oleksiak MF. Gene expression throughout a vertebrate's embryogenesis. BMC Genomics 2011, 12:132. 10.1186/1471-2164-12-132, 3062618, 21356103.
42. Kerr MK, Churchill GA. Experimental design for gene expression microarrays. Biostatistics 2001, 2:183-201. 10.1093/biostatistics/2.2.183, 12933549.
43. Kerr MK, Churchill GA. Statistical design and the analysis of gene expression microarray data. Genet Res 2001, 77:123-128.
44. Altman NS, Hua J. Extending the loop design for two-channel microarray experiments. Genet Res 2006, 88:153-163. 10.1017/S0016672307008476, 17371610.
45. http://www.jmp.com/software/genomics/
46. Wu H, Kerr K, Cui X, Churchill G. "MAANOVA: a software package for the analysis of spotted cDNA microarray experiments". The Analysis of Gene Expression Data: Methods and Software 2003,
47. Jin W, Riley RM, Wolfinger RD, White KP, Passador-Gurgel G, Gibson G. The contributions of sex, genotype and age to transcriptional variance in Drosophila melanogaster. Nat Genet 2001, 29:389-395. 10.1038/ng766, 11726925.
48. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS. Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 2001, 8:625-637. 10.1089/106652701753307520, 11747616.
49. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 1995, 57:289-3000.
50. Storey JD, Tibshirani R. Estimating false discovery rates under dependence, with applications to DNA microarrays. 2001, Technical Report 2001-28, Department of Statistics, Stanford University.
51. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci USA 2003, 100:9440-9445. 10.1073/pnas.1530509100, 170937, 12883005.
52. Cluster 3.0. , http://bonsai.hgc.jp/~mdehoon/software/cluster/software.htm
53. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics 2004, 20:1453-1454. 10.1093/bioinformatics/bth078, 14871861.
54. Matlab. , http://www.mathworks.com/
55. GraphViz. , http://www.graphviz.org/
56. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380. 1464427, 16056220.
57. BlastStation. , http://www.blaststation.com/en/index.html
58. Cap3. , http://pbil.univ-lyon1.fr/cap3.php
59. Henry TR, Spitsbergen JM, Hornung MW, Abnet CC, Peterson RE. Early life stage toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in Zebrafish (Danio rerio). Toxicology and Applied Pharmacology 1997, 142:56-68. 10.1006/taap.1996.8024, 9007034.
60. Jönsson ME, Jenny MJ, Woodin BR, Hahn ME, Stegeman JJ. 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 3,3',4,4',5-pentachlorobiphenyl or 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Sci 2007, 100:180-193. 10.1093/toxsci/kfm207, 17686920.
61. Carlson EA, Roy NK, Wirgin. Microarray analysis of polychlorinated biphenyl mixture-induced changes in gene expression among Atlantic tomcod populations displaying differential sensitivity to halogenated aromatic hydrocarbons. Environ Toxicol Chem 2009, 28:759-771. 10.1897/08-195R.1, 19391682.
62. Moffat ID, Boutros PC, Chen H, Okey AB, Pohjanvirta R. Aryl hydrocarbon receptor (AHR)-regulated transcriptomic changes in rats sensitive or resistant to major dioxin toxicities. BMC Genomics 2010, 11:263. 10.1186/1471-2164-11-263, 2881023, 20420666.
63. Franc MA, Moffat ID, Boutros PC, Tuomisto JT, Tuomisto J, Pohjanvirta R, Okey AB. Patterns of dioxin-altered mRNA expression in livers of dioxin-sensitive versus dioxin-resistant rats. Arch Toxicol 2008, 82:809-830. 10.1007/s00204-008-0303-0, 18465118.
64. Boutros PC, Yao CQ, Watson JD, Wu AH, Moffat ID, Prokopec SD, Smith AB, Okey AB, Pohjanvirta R. Hepatic Transcriptomic Responses to TCDD in Dioxin-Sensitive and Dioxin-Resistant Rats During the Onset of Toxicity, Toxicology and Applied Pharmacology. Toxicol Appl Pharmacol 2011, 251:119-129. 10.1016/j.taap.2010.12.010, 21215274.
65. Whitlock JP. Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol 1999, 39:103-125. 10.1146/annurev.pharmtox.39.1.103, 10331078.
66. Karchner SI, Franks DG, Powell WH, Hahn ME. Regulatory interactions among three members of the vertebrate aryl hydrocarbon receptor family: AHR repressor, AHR1, and AHR2. J Biol Chem 2002, 277:6949-6959. 10.1074/jbc.M110779200, 11742002.
67. Tijet N, Boutros PC, Moffat ID, Okey AB, Tuomisto J, Pohjanvirta R. Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol Pharmacol 2006, 69:140-153.
68. Whitehead A, Triant DA, Champlin D, Nacci D. Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Molec Ecol 2010, 19:5186-5203.
69. Poland A, Glover E. Genetic expression of aryl hydrocarbon hydroxylase by 2,3,7,8-tetrachlorodibenzo-p-dioxin: evidence for a receptor mutation in genetically non-responsive mice. Molec Pharmacol 1975, 11:389-398.
70. Poland A, Palen D, Glover E. Analysis of the four alleles of the murine aryl hydrocarbon receptor. Molec Pharmacol 1994, 46:915-921.
71. Powell WH, Morrison HG, Weil EJ, Karchner SI, Sogin ML, Stegeman JJ, Hahn ME. Cloning and analysis of the CYP1A promoter from the Atlantic killifish (Fundulus heteroclitus). Mar Environ Res 2004, 58:119-124. 10.1016/j.marenvres.2004.03.005, 15178023.
72. Hahn ME, Karchner SI, Shapiro MA, Perera SA. Molecular evolution of two vertebrate aryl hydrocarbon (dioxin) receptors (AHR1 and AHR2) and the PAS family. Proc Nat'l Acad Sci USA 1997, 94:13743-13748. 10.1073/pnas.94.25.13743, 21241125.
73. Karchner SI, Powell WH, Hahn ME. Identification and functional characterization of two highly divergent aryl hydrocarbon receptors (AHR1 and AHR2) in the teleost Fundulus heteroclitus. Evidence for a novel subfamily of ligand-binding basic helix-loop-helix Per-ARNT-Sim (bHLH-PAS) factors. J Biol Chem 1999, 274:33814-33824. 10.1074/jbc.274.47.33814, 10559277.
74. Clark BW, Matson CW, Jung D, Di Giulio RT. AHR2 mediates cardiac teratogenesis of polycyclic aromatic hydrocarbons and PCB-126 in Atlantic killifish (Fundulus heteroclitus). Aquat Toxicol 2010, 99:232-240. 10.1016/j.aquatox.2010.05.004, 20605646.
75. Wirgin I, Roy NK, Loftus M, Chambers RC, Franks DG, Hahn ME. Mechanistic Basis of Resistance to PCBs in Atlantic Tomcod from the Hudson River. Science 2011, 331:1322-1325. 10.1126/science.1197296, 21330491.
76. Meyer JN, Wassenberg DM, Karchner SI, Hahn ME, DiGiulio RT. Expression and inducibility of aryl hydrocarbon receptor (AHR) pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant exposure histories. Environ Toxicol Chem 2003, 22:2337-2343. 10.1897/02-495, 14551997.
77. Hahn ME, Karchner SI, Franks DG, Merson RR. Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus). Pharmacogenetics 2004, 14:131-143. 10.1097/00008571-200402000-00007, 15077014.