Epigenetics and its implications for ecotoxicology

Ecotoxicology

Volumn 20, Issue 3, 2011, Pages 607-624

  Vandegehuchte, Michiel B ^a   Janssen, Colin R ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

DNA methylation; Environmental toxicology; Invertebrates; Transgenerational effects

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; ARSENIC; AZACITIDINE; CADMIUM; DNA METHYLTRANSFERASE; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; FUNGICIDE; HISTONE; LEAD; NANOMATERIAL; NICKEL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; UNTRANSLATED RNA; VINCLOZOLIN; ZINC;

DNA; ECOTOXICOLOGY; ENDOCRINE DISRUPTOR; ENVIRONMENTAL IMPACT; FUNGICIDE; GENE EXPRESSION; INVERTEBRATE; METHYLATION; ORGANIC POLLUTANT; RODENT;

AIR POLLUTION; CARCINOGENIC ACTIVITY; DNA METHYLATION; DNA MODIFICATION; DNA STRAND BREAKAGE; ECOTOXICOLOGY; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL IMPACT ASSESSMENT; EPIGENETICS; EVOLUTIONARY ADAPTATION; GENE SILENCING; GENOTOXICITY; HISTONE MODIFICATION; NONHUMAN; PHENOTYPE; PLESIOMORPHY; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; TRANSGENICS;

ANIMALS; AZACITIDINE; CLADOCERA; ECOTOXICOLOGY; ENVIRONMENTAL POLLUTANTS; EPIGENESIS, GENETIC; FISHES; FUNGICIDES, INDUSTRIAL; RATS; RISK ASSESSMENT;

CLADOCERA; INVERTEBRATA; MAMMALIA; RATTUS; RODENTIA;

EID: 79955850831     PISSN: 09639292     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10646-011-0634-0     Document Type: Review

References (136)

1. Aagaard-Tillery KM, Grove K, Bishop J, Ke XR, Fu Q, McKnight R, Lane RH (2008) Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol 41(1-2):91-102. doi: 10.1677/jme-08-0025
2. Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant 121(3):472-480 (Pubitemid 38927697)
3. Allis CD, Jenuwein T, Reinberg D (2007) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
4. Aniagu SO, Williams TD, Allen Y, Katsiadaki I, Chipman JK (2008) Global genomic methylation levels in the liver and gonads of the three-spine stickleback (Gasterosteus aculeatus) after exposure to hexabromocyclododecane and 17-[beta] oestradiol. Environ Int 34(3):310-317
5. Anway MD, Skinner MK (2008) Transgenerational effects of the endocrine disruptor vinclozolin on the prostate transcriptome and adult onset disease. Prostate 68(5):517-529 (Pubitemid 351500212)
6. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308(5727):1466-1469 (Pubitemid 40791300)
7. Anway MD, Leathers C, Skinner MK (2006) Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology 147(12):5515-5523. doi:10.1210/en.2006-0640 (Pubitemid 44833467)
8. Anway MD, Rekow SS, Skinner MK (2008) Transgenerational epigenetic programming of the embryonic testis transcriptome. Genomics 91(1):30-40 (Pubitemid 350298395)
9. Baccarelli A, Bollati V (2009) Epigenetics and environmental chemicals. Curr Opin Pediatr 21(2):243-251. doi:10.1097/MOP. 0b013e32832925cc
10. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz J (2009) Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 179(7):572-578. doi: 10.1164/rccm.200807-1097OC
11. Backdahl L, Herberth M, Wilson G, Tate P, Campos LS, Cortese R, Eckhardt F, Beck S (2009) Gene body methylation of the dimethylarginine dimethylamino-hydrolase 2 (Ddah2) gene is an epigenetic biomarker for neural stem cell differentiation. Epigenetics 4(4):248-254
12. Bartova E, Krejci J, Harnicarova A, Galiova G, Kozubek S (2008) Histone modifications and nuclear architecture: a review. J Histochem Cytochem 56(8):711-721. doi:10.1369/jhc.2008.951251 (Pubitemid 351991084)
13. Baun A, Hartmann NB, Grieger K, Kusk KO (2008) Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17(5):387-395. doi:10.1007/s10646-008- 0208-y
14. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A (2009) An operational definition of epigenetics. Genes Dev 23(7):781-783. doi:10.1101/gad.1787609
15. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16(1):6-21
16. Bocock PN, Aagaard-Tillery KM (2009) Animal models of epigenetic inheritance. Semin Reprod Med 27(5):369-379. doi:10.1055/s-0029-1237425
17. Bollati V, Baccarelli A (2010) Environmental epigenetics. Heredity 105(1):105-112. doi:10.1038/hdy.2010.2
18. Bonduriansky R, Day T (2009) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst 40:103-125. doi:10.1146/annurev.ecolsys. 39.110707.173441
19. Bongiorni S, Cintio O, Prantera G (1999) The relationship between DNA methylation and chromosome imprinting in the coccid planococcus citri. Genetics 151(4):1471-1478 (Pubitemid 29177556)
20. Bossdorf O, Richards CL, Pigliucci M (2008) Epigenetics for ecologists. Ecol Lett 11(2):106-115. doi:10.1111/j.1461-0248.2007.01130.x
21. Boyko A, Blevins T, Yao YL, Golubov A, Bilichak A, Ilnytskyy Y, Hollander J, Meins F, Kovalchuk I (2010) Transgenerational adaptation of arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS ONE 5(3). doi: 10.1371/journal.pone.0009514
22. Bromer JG, Wu J, Zhou Y, Taylor HS (2009) Hypermethylation of homeobox A10 by in utero diethylstilbestrol exposure: an epigenetic mechanism for altered developmental programming. Endocrinology 150(7):3376-3382. doi:10.1210/en.2009- 0071
23. Brown KH, Schultz IR, Nagler JJ (2009) Lack of a heritable reproductive defect in the offspring of male rainbow trout exposed to the environmental estrogen 17[alpha]-ethynylestradiol. Aquat Toxicol 91(1):71-74
24. Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA (2007) Dietary protein restriction of pregnant rats in the F-0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F-1 and F-2 generations. Br J Nutr 97(3):435-439. doi:10.1017/s0007114507352392 (Pubitemid 46662031)
25. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136(4):642-655
26. Chang H-S, Anway MD, Rekow SS, Skinner MK (2006) Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination. Endocrinology 147(12):5524-5541. doi:10.1210/en.2006-0987
27. Chang H-S, Anway MD, Rekow SS, Skinner MK (2009) Transgenerational epigenetic imprinting of the male germline by endocrine disruptor exposure during gonadal sex determination (Retraction of vol 147, p. 5524, 2006). Endocrinology 150(6):2976
28. Choi AO, Brown SE, Szyf M, Maysinger D (2008) Quantum dot-induced epigenetic and genotoxic changes in human breast cancer cells. J Mol Med 86(3):291-302. doi:10.1007/s00109-007-0274-2 (Pubitemid 351311423)
29. Choudhuri S, Cui Y, Klaassen CD (2010) Molecular targets of epigenetic regulation and effectors of environmental influences. Toxicol Appl Pharmacol 245:378-393
30. Collier J (2009) Epigenetic regulation of the bacterial cell cycle. Curr Opin Microbiol 12(6):722-729. doi:10.1016/j.mib.2009.08.005
31. Costa M, Davidson TL, Chen H, Ke Q, Zhang P, Yan Y, Huang C, Kluz T (2005) Nickel carcinogenesis: epigenetics and hypoxia signaling. Mutat Res 592(1-2):79-88 (Pubitemid 41714046)
32. Counts JL, Sarmiento JI, Harbison ML, Downing JC, McClain RM, Goodman JI (1996) Cell proliferation and global methylation status changes in mouse liver after phenobarbital and/or cholinedevoid, methionine-deficient diet administration. Carcinogenesis 17(6):1251-1257. doi:10.1093/carcin/17.6.1251 (Pubitemid 26196336)
33. Cropley JE, Suter CM, Beckman KB, Martin DIK (2006) Germ-line epigenetic modification of the murine A(vy) allele by nutritional supplementation. Proc Natl Acad Sci USA 103(46):17308-17312. doi:10.1073/pnas.0607090103 (Pubitemid 44788965)
34. Cui P, Zhang L, Lin Q, Ding F, Xin C, Fang X, Hu S, Yu J (2010) A novel mechanism of epigenetic regulation: nucleosome-space occupancy. Biochem Biophys Res Commun 391(1):884-889
35. Dalkvist T, Topping CJ, Forbes VE (2009) Population-level impacts of pesticide-induced chronic effects on individuals depend more on ecology than toxicology. Ecotoxicol Environ Saf 72(6):1663-1672
36. Day JK, Bauer AM, desBordes C, Zhuang Y, Kim BE, Newton LG, Nehra V, Forsee KM, MacDonald RS, Besch-Williford C, Huang THM, Lubahn DB (2002) Genistein alters methylation patterns in mice. J Nutr 132(8):2419S-2423S
37. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL (2006) Maternal genistein alters coat color and protects Avy mouse offspring from obesty by modifying the fetal epigenome. Environ Health Perspect 114(4):567-572
38. Field LM (2000) Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer). Biochem J 349:863-868
39. Field LM, Lyko F, Mandrioli M, Prantera G (2004) DNA methylation in insects. Insect Mol Biol 13(2):109-115 (Pubitemid 38522240)
40. Foret S, Kucharski R, Pittelkow Y, Lockett G, Maleszka R (2009) Epigenetic regulation of the honey bee transcriptome: unravelling the nature of methylated genes. BMC Genom 10(1):472
41. Fuks F (2005) DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev 15(5):490-495
42. 2 nanoparticles induce global genomic hypomethylation in HaCaT cells. Biochem Biophys Res Commun 397(3):397-400
43. Goodman JI, Augustine KA, Cunnningham ML, Dixon D, Dragan YP, Falls JG, Rasoulpour RJ, Sills RC, Storer RD, Wolf DC, Pettit SD (2010) What do we need to know prior to thinking about incorporating an epigenetic evaluation into safety assessments?(2). Toxicol Sci 116(2):375-381. doi:10.1093/toxsci/kfq133
44. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci 105(44):17046-17049. doi:10.1073/pnas.0806560105
45. Henckel A, Nakabayashi K, Sanz LA, Feil R, Hata K, Arnaud P (2009) Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum Mol Genet 18(18):3375-3383. doi:10.1093/hmg/ ddp277
46. Herrera CM, Bazaga P (2010) Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis. New Phytol 187(3):867-876. doi:10.1111/j.1469-8137.2010.03298.x
47. Ho DH, Burggren WW (2010) Epigenetics and transgenerational transfer: a physiological perspective. J Exp Biol 213(1):3-16. doi:10.1242/jeb.019752
48. Holliday R (1994) Epigenetics: an overview. Dev Genet 15(6):453-457
49. Huang Z, Chen Y, Zhao Y, Zuo Z, Chen M, Wang C (2005) Antioxidant responses in Meretrix meretrix exposed to environmentally relevant doses of tributyltin. Environ Toxicol Pharmacol 20(1):107-111 (Pubitemid 40615365)
50. Huang D, Zhang Y, Qi Y, Chen C, Ji W (2008) Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of Cadmium-stimulated K562 cell proliferation. Toxicol Lett 179(1):43-47
51. Inawaka K, Kawabe M, Takahashi S, Doi Y, Tomigahara Y, Tarui H, Abe J, Kawamura S, Shirai T (2009) Maternal exposure to antiandrogenic compounds, vinclozolin, flutamide and procymidone, has no effects on spermatogenesis and DNA methylation in male rats of subsequent generations. Toxicol Appl Pharmacol 237(2):178-187
52. Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mechanisms and implications for the study of heredity and evolution. Q Rev Biol 84(2):131-176
53. Jeltsch A, Nellen W, Lyko F (2006) Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 31(6):306-308 (Pubitemid 43922415)
54. Jensen TJ, Novak P, Wnek SM, Gandolfi AJ, Futscher BW (2009) Arsenicals produce stable progressive changes in DNA methylation patterns that are linked to malignant transformation of immortalized urothelial cells. Toxicol Appl Pharmacol 241(2): 221-229
55. Jernström B, Funk M, Frank H, Mannervik B, Seidel A (1996) CARCINOGENESIS: Glutathione S-transferase A1-1-catalysed conjugation of bay and fjord region diol epoxides of polycyclic aromatic hydrocarbons with glutathione. Carcinogenesis 17(7):1491-1498. doi:10.1093/carcin/17.7.1491 (Pubitemid 26242656)
56. Jiang GF, Xu L, Song SZ, Zhu CC, Wu Q, Zhang L (2008) Effects of long-term low-dose cadmium exposure on genomic DNA methylation in human embryo lung fibroblast cells. Toxicology 244:49-55. doi:10.1016/j.tox.2007.10.028 (Pubitemid 50013239)
57. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. Plos Genet 5(6). doi:e100053010.1371/journal.pgen. 1000530
58. Jurkowski TP, Meusburger M, Phalke S, Helm M, Nellen W, Reuter G, Jeltsch A (2008) Human DNMT2 methylates tRNAAsp molecules using a DNA methyltransferase-like catalytic mechanism. RNA 14(8):1663-1670. doi:10.1261/rna.970408
59. Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871):1827-1830. doi:10.1126/science.1153069 (Pubitemid 351451590)
60. Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, Jonak C, Hauser MT, Luschnig C (2010) Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in arabidopsis. Mol Plant 3(3):594-602. doi: 10.1093/mp/ssq014
61. LeBaron MJ, Rasoulpour RJ, Klapacz J, Ellis-Hutchings RG, Hollnagel HM, Gollapudi BB (2010) Epigenetics and chemical safety assessment. Mutat Res/Rev Mutat Res 705:83-95
62. Lee YW, Broday L, Costa M (1998) Effects of nickel on DNA methyltransferase activity and genomic DNA methylation levels. Mutat Res 415:213-218 (Pubitemid 28352258)
63. Lee DH, Jacobs DR, Porta M (2009) Hypothesis: a unifying mechanism for nutrition and chemicals as lifelong modulators of DNA hypomethylation. Environ Health Perspect 117(12): 1799-1802. doi:10.1289/ehp.0900741
64. Legler J (2010) Epigenetics: an emerging field in environmental toxicology. Integr Environ Assess Manage 6(2):314-315
65. Lennartsson A, Ekwall K (2009) Histone modification patterns and epigenetic codes. Biochimica et Biophysica Acta (BBA) - General Subjects 1790(9):863-868
66. Li S, Hansman R, Newbold R, Davis B, McLachlan JA, Barrett JC (2003) Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol Carcinog 38(2):78-84 (Pubitemid 37255143)
67. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC (2005) Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr 135(6):1382-1386 (Pubitemid 40799599)
68. Lippman Z, Martienssen R (2004) The role of RNA interference in heterochromatic silencing. Nature 431(7006):364-370 (Pubitemid 39265677)
69. Lyko F (2001) DNA methylation learns to fly. Trends Genet 17(4):169-172
70. MacKay AB, Mhanni AA, McGowan RA, Krone PH (2007) Immunological detection of changes in genomic DNA methylation during early zebrafish development. Genome 50(8):778-785. doi:10.1139/g07-055 (Pubitemid 350033236)
71. Majid S, Dar AA, Shahryari V, Hirata H, Ahmad A, Saini S, Tanaka Y, Dahiya AV, Dahiya R (2010) Genistein reverses hypermethylation and induces active histone modifications in tumor suppressor gene B-Cell translocation gene 3 in prostate cancer. Cancer 116(1):66-76
72. Marsit CJ, Eddy K, Kelsey KT (2006) MicroRNA responses to cellular stress. Cancer Res 66(22):10843-10848. doi:10.1158/0008-5472.can-06-1894 (Pubitemid 44876980)
73. Martienssen R (2008) Great leap forward? Transposable elements, small interfering RNA and adaptive Lamarckian evolution. New Phytol 179(3):570-572. doi:10.1111/j.1469-8137.2008.02567.x
74. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G, Benes V, Jeltsch A, Gannon F, Salbert G (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452(7183):45-50 (Pubitemid 351355084)
75. Morgan HD, Sutherland HGE, Martin DIK, Whitelaw E (1999) Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23(3):314-318 (Pubitemid 29526429)
76. Morgan AJ, Kille P, Sturzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41(4):1085-1096
77. Nan XS, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998) Transcriptional repression by the methyl- CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393(6683):386-389 (Pubitemid 28269714)
78. Newbold RR, Padilla-Banks E, Jefferson WN (2006) Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147(6):S11-S17 (Pubitemid 43764585)
79. Nilsson EE, Anway MD, Stanfield J, Skinner MK (2008) Transgenerational epigenetic effects of the endocrine disruptor vinclozolin on pregnancies and female adult onset disease. Reproduction 135(5):713-721. doi:10.1530/rep-07-0542 (Pubitemid 351676454)
80. Ou X, Long L, Zhang Y, Xue Y, Liu J, Lin X, Liu B (2009) Spaceflight induces both transient and heritable alterations in DNA methylation and gene expression in rice (Oryza sativa L.). Mutat Res 662(1-2):44-53
81. Pilsner JR, Hu H, Ettinger A, Sanchez BN, Wright RO, Cantonwine D, Lazarus A, Lamadrid-Figueroa H, Mercado-Garcia A, Tellez- Rojo MM, Hernandez-Avila M (2009) Influence of prenatal lead exposure on genomic methylation of cord blood DNA. Environ Health Perspect 117(9):1466-1471. doi:10.1289/ehp.0800497
82. Pilsner JR, Lazarus AL, Nam DH, Letcher RJ, Sonne C, Dietz R, Basu N (2010) Mercury-associated DNA hypomethylation in polar bear brains via the LUminometric Methylation Assay: a sensitive method to study epigenetics in wildlife. Mol Ecol 19(2):307-314. doi:10.1111/j.1365-294X.2009.04452.x
83. Pruss D, Hayes JJ, Wolffe AP (1995) Histone and DNA contributions to nucleosome structure. In: Wolffe AP (ed) The nucleus, volume 1: the nucleosome. pp 3-29
84. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KVK, Whitelaw E (2003) Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission. Proc Natl Acad Scies 100(5):2538-2543. doi:10.1073/pnas.0436776100 (Pubitemid 36297534)
85. Riggs AD, Martienssen RA, Russo VEA (1996) Introduction. In: Russo VEA, Martienssen RA, Riggs AD (eds) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, pp 1-4
86. Ropero S, Esteller M (2009) Epigenetics and cancer: DNA methylation. In: Esteller M (ed) Epigenetics in biology and medicine. CRC Press, Boca Raton, FL
87. Rosenfeld CS (2010) Animal models to study environmental epigenetics. Biol Reprod 82(3):473-488. doi:10.1095/biolreprod.109.080952
88. Ross SA (2009) Nutrition, epigenetics, and cancer. In: Choi S-W, Friso S (eds) Nutrients and epigenetics. CRC Press, Boca Raton, FL
89. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC (2008) Global DNA hypomethylation is associated with high serum-persistent organic pollutants in greenlandic Inuit. Environ Health Perspect 116(11):1547-1552. doi:10.1289/ehp.11338
90. Schaefer M, Lyko F (2007) DNA methylation with a sting: an active DNA methylation system in the honeybee. Bioessays 29(3):208-211. doi:10.1002/bies.20548 (Pubitemid 46384159)
91. Schneider S, Kaufmann W, Buesen R, van Ravenzwaay B (2008) Vinclozolin - the lack of a transgenerational effect after oral maternal exposure during organogenesis. Reprod Toxicol 25(3): 352-360
92. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G (2007) Genome regulation by polycomb and trithorax proteins. Cell 128(4):735-745 (Pubitemid 46273581)
93. Shugart LR (1990) 5-Methyl deoxycytidine content of DNA from bluegill sunfish (Lepomis macrochirus) exposed to benzo[a]pyrene. Environ Toxicol Chem 9(2):205-208
94. Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrin Met 21(4):214-222
95. Soares J, Coimbra AM, Reis-Henriques MA, Monteiro NM, Vieira MN, Oliveira JMA, Guedes-Dias P, Fontaínhas-Fernandes A, Parra SS, Carvalho AP, Castro LFC, Santos MM (2009) Disruption of zebrafish (Danio rerio) embryonic development after full life-cycle parental exposure to low levels of ethinylestradiol. Aquat Toxicol 95(4):330-338
96. Stouder C, Paoloni-Giacobino A (2010) Transgenerational effects of the endocrine disruptor vinclozolin on the methylation pattern of imprinted genes in the mouse sperm. Reproduction 139(2):373-379. doi:10.1530/rep-09-0340
97. Stromqvist M, Tooke N, Brunstrom B (2010) DNA methylation levels in the 50 flanking region of the vitellogenin I gene in liver and brain of adult zebrafish (Danio rerio)-sex and tissue differences and effects of 17 alpha-ethinylestradiol exposure. Aquat Toxicol 98(3):275-281. doi:10.1016/j.aquatox.2010.02.023
98. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9(6):465-476. doi:10.1038/nrg2341 (Pubitemid 351693975)
99. Suzuki MM, Kerr ARW, De Sousa D, Bird A (2007) CpG methylation is targeted to transcription units in an invertebrate genome. Genome Res 17(5):625-631. doi:10.1101/gr.6163007 (Pubitemid 46715513)
100. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324(5929):930-935. doi:10.1126/science.1170116
101. Takiguchi M, Achanzar WE, Qu W, Li G, Waalkes MP (2003) Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp Cell Res 286:355-365 (Pubitemid 36566447)
102. Tarantini L, Bonzini M, Apostoli P, Pegoraro V, Bollati V, Marinelli B, Cantone L, Rizzo G, Hou L, Schwartz J, Bertazzi PA, Baccarelli A (2009) Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environ Health Perspect 117(2):217-222
103. Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M, Ciaudo C, Cruaud C, Poulain J, Berdasco M, Fraga MF, Voinnet O, Wincker P, Esteller M, Colot V (2009) A role for RNAi in the selective correction of DNA methylation defects. Science 323(5921):1600-1604. doi:10.1126/science.1165313
104. The Nasonia Genome Working Group (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327(5963):343-348. doi:10.1126/science.1178028
105. Tweedie S, Charlton J, Clark V, Bird A (1997) Methylation of genomes and genes at the invertebrate-vertebrate boundary. Mol Cell Biol 17(3):1469-1475 (Pubitemid 27097376)
106. Tweedie S, Ng HH, Barlow AL, Turner BM, Hendrich B, Bird A (1999) Vestiges of a DNA methylation system in Drosophila melanogaster? Nat Genet 23(4):389-390
107. Vandegehuchte MB, Kyndt T, Vanholme B, Haegeman A, Gheysen G, Janssen CR (2009a) Occurrence of DNA methylation in Daphnia magna and influence of multigeneration Cd exposure. Environ Int 35:700-706
108. Vandegehuchte MB, Lemière F, Janssen CR (2009b) Quantitative DNA-methylation in Daphnia magna and effects of multigeneration Zn exposure. Comp Biochem Phys C 150(3):343-348
109. Vandegehuchte MB, De Coninck D, Vandenbrouck T, De Coen WM, Janssen CR (2010a) Gene transcription profiles, global DNA methylation and potential transgenerational epigenetic effects related to Zn exposure history in Daphnia magna. Environ Pollut 158:3323-3329
110. Vandegehuchte MB, Lemière F, Vanhaecke L, Vanden Berghe W, Janssen CR (2010b) Direct and transgenerational impact on Daphnia magna of chemicals with a known effect on DNA methylation. Comp Biochem Physiol C 151:278-285
111. Vandegehuchte MB, Vandenbrouck T, Coninck DD, De Coen WM, Janssen CR (2010c) Can metal stress induce transferable changes in gene transcription in Daphnia magna? Aquat Toxicol 97(3):188-195
112. Verhoeven K, Jansen J, van Dijk P, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108-1118
113. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F (2006) The polycomb group protein EZH2 directly controls DNA methylation. Nature 439(7078):871-874. doi:10.1038/nature04431 (Pubitemid 43255707)
114. Waddington CH (1939) Introduction to modern genetics. Allen and Unwin, London
115. Wang Y, Leung FCC (2008) GC content increased at CpG flanking positions of fish genes compared with sea squirt orthologs as a mechanism for reducing impact of DNA methylation. PLoS ONE 3(11):e3612
116. Wang Y, Jorda M, Jones PL, Maleszka R, Ling X, Robertson HM, Mizzen CA, Peinado MA, Robinson GE (2006) Functional CpG methylation system in a social insect. Science 314(5799):645-647 (Pubitemid 44646387)
117. Wang Y, Wang C, Zhang J, Chen Y, Zuo Z (2009) DNA hypomethylation induced by tributyltin, triphenyltin, and a mixture of these in sebastiscus marmoratus liver. Aquat Toxicol 95(2):93-98
118. Wassenegger M (2005) The role of the RNAi machinery in heterochromatin formation. Cell 122(1):13-16
119. Waterland RA, Jirtle RL (2003) Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol 23(15):5293-5300 (Pubitemid 36950884)
120. Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG (2006) Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 44(9):401-406 (Pubitemid 44454044)
121. Waterland RA, Travisano M, Tahiliani KG (2007) Diet-induced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J 21(12):3380-3385. doi:10.1096/fj.07-8229com (Pubitemid 47565556)
122. Watson RE, Goodman JI (2002) Effects of phenobarbital on DNA methylation in GC-rich regions of hepatic DNA from mice that exhibit different levels of susceptibility to liver tumorigenesis. Toxicol Sci 68(1):51-58. doi:10.1093/toxsci/68.1.51 (Pubitemid 34785229)
123. Watters E (2006) DNA is not destiny. Discover Nov:32-37, 95
124. Weaver ICG, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7(8):847-854 (Pubitemid 38989508)
125. Wu J, Basha MR, Brock B, Cox DP, Cardozo-Pelaez F, McPherson CA, Harry J, Rice DC, Maloney B, Chen D, Lahiri DK, Zawia NH (2008) Alzheimer's disease (AD)-like pathology in aged monkeys after infantile exposure to environmental metal lead (Pb): Evidence for a developmental origin and environmental link for AD. J Neurosci 28(1):3-9. doi:10.1523/jneurosci.4405-07.2008
126. Wu SD, Zhu J, Li YS, Lin T, Gan LQ, Yuan XG, Xiong J, Liu X, Xu MD, Zhao D, Ma C, Li XL, Wei GH (2010) Dynamic epigenetic changes involved in testicular toxicity induced by di-2-(ethylhexyl) phthalate in mice. Basic Clin Pharmacol Toxicol 106(2):118-123. doi:10.1111/j.1742-7843.2009.00483.x
127. Yakovlev IA, Asante DKA, Fossdal CG, Junttila O, Johnsen ø (2011) Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Sci 180(1):132-139
128. Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schboten FJ, Berndt ML, Pogribny IF, Koturbash I, Williams A, Douglas GR, Kovalchuk O (2008) Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci U S A 105(2):605-610. doi: 10.1073/pnas.0705896105
129. Youngson N, Whitelaw E (2008) Transgenerational epigenetic effects. Annu Rev Genom Hum Genet 9(1):233-257
130. Yu Z (2008) Non-coding RNAs in gene regulation. In: Tost J (ed) Epigenetics. Caister Academic Press, Norfolk, UK, pp 171-186
131. Zhang X (2008) The epigenetic landscape of plants. Science 320(5875):489-492. doi:10.1126/science.1153996
132. Zhao CQ, Young MR, Diwan BA, Coogan TP, Waalkes MP (1997) Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci U S A 94(20):10907-10912 (Pubitemid 27430834)
133. Zhou XW, Zhu GN, Jilisa M, Sun JH (2001) Influence of Cu, Zn, Pb, Cd and their heavy metalion mixture on the DNA methylation level of the fish (Carassius auratus). China Environ Sci 21(6): 549-552 (Pubitemid 34028684)
134. Zhou X, Li Q, Arita A, Sun H, Costa M (2009) Effects of nickel, chromate, and arsenite on histone 3 lysine methylation. Toxicol Appl Pharmacol 236(1):78-84
135. Zilberman D (2008) The evolving functions of DNA methylation. Curr Opin Plant Biol 11:554-559
136. Zilberman D, Henikoff S (2005) Epigenetic inheritance in Arabidopsis: selective silence. Curr Opin Genet Dev 15(5):557-562 (Pubitemid 41262413)