Developmental profiles and expression of the DNA methyltransferase genes in the fathead minnow (Pimephales promelas) following exposure to di-2-ethylhexyl phthalate

详细信息    查看全文

• 作者：Richard K. Wood ; Emma Crowley ; Christopher J. Martyniuk
• 关键词：Phthalates ; Toxicology ; Survival ; DNA methylation
• 刊名：Fish Physiology and Biochemistry
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：42
• 期：1
• 页码：7-18
• 全文大小：458 KB
• 参考文献：Aluru N, Kuo E, Helfrich LW, Karchner SI, Linney EA, Pais JE, Franks DG (2015) Developmental exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin alters DNA methyltransferase (dnmt) expression in zebrafish (Danio rerio). Toxicol Appl Pharmacol 284:142–151CrossRef PubMed
  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-β oestradiol. Environ Int 34(3):310–317CrossRef PubMed
  Ankley GT, Villeneuve DL (2006) The fathead minnow in aquatic toxicology: past, present and future. Aquat Toxicol 78:91–102CrossRef PubMed
  Beauchesne I, Barnabe S, Cooper DG, Nicell JA (2008) Plasticizers and related toxic degradation products in wastewater sludges. Water Sci Technol 57:367–374CrossRef PubMed
  Campos C, Valente LMP, Fernandes JMO (2012) Molecular evolution of zebrafish dnmt3 genes and thermal plasticity of their expression during embryonic development. Gene 500:93–100CrossRef PubMed
  Canadian Council of Ministers of the Environment (1999) Canadian water quality guidelines for the protection of aquatic life: Phthalate esters—DEHP, DBP and DOP Canadian environmental quality guidelines, 1999, Canadian Council of Ministers of the Environment, Winnipeg. http://​ceqg-rcqe.​ccme.​ca/​download/​en/​206
  Chikae M, Hatano Y, Ikeda R, Morita Y, Hasan Q, Tamiya E (2004a) Effects of bis(2-ethylhexyl) phthalate and benzo[a]pyrene on the embryos of Japanese medaka (Oryzias latipes). Environ Toxicol Pharmacol 16:141–145CrossRef PubMed
  Chikae M, Ikeda R, Hatano Y, Hasan Q, Morita Y, Tamiya E (2004b) Effects of bis(2-ethylhexyl) phthalate, gamma-hexachlorocyclohexane, and 17-beta-estradiol on the fry stage of medaka (Oryzias latipes). Environ Toxicol Pharmacol 18:9–12CrossRef PubMed
  Chishti YZ, Feswick A, Martyniuk CJ (2014) Progesterone increases ex vivo testosterone production and decreases the expression of progestin receptors and steroidogenic enzymes in the fathead minnow (Pimephales promelas) ovary. Gen Comp Endocrinol 199:16–25CrossRef PubMed
  Crisp TM, Clegg ED, Cooper RL, Wood WP, Anderson DG, Baetke KP, Hoffman JL, Morrow MS, Rodier DJ, Schaeffer JE, Touart LW, Zeeman MG, Dargnat C, Blanchard M, Chevreuil M, Teil MJ (2009) Occurrence of phthalate ester in the Seine River estuary (France). Hydrol Process 23:1192–1201CrossRef
  DeFoe DL, Holcombe GW, Hammermeister DE, Biesinger KE (1990) Solubility and toxicity of eight phthalate esters to four aquatic organisms. Environ Toxicol Chem 9:623–636CrossRef
  Devlin EW, Brammer JD, Puycar RL, McKim, JM (1996) Prehatching development of the fathead minnow Pimephales promelas Rafinesque. EPA/600/R-96/079
  Fang X, Corrales J, Thornton C, Scheffler BE, Willett KL (2013) Global and gene specific DNA methylation changes during zebrafish development. Comp Biochem Physiol B: Biochem Mol Biol 166(1):99–108CrossRef
  Fernandes JMO, Mommens M, Hagen Ø, Babiak I, Solberg C (2008) Selection of suitable reference genes for real-time PCR studies of Atlantic halibut development. Comp Biochem Physiol B 150(1):23–32CrossRef PubMed
  Hermann A, Gowher H, Jeltsch A (2004) Biochemistry and biology of mammalian DNA methyltransferases. Cell Mol Life Sci 61:2571–2587CrossRef PubMed
  Jeltsch A (2002) Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chem Bio Chem 3:274–293CrossRef PubMed
  Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070CrossRef PubMed
  Kang SC, Lee BM (2005) DNA methylation of estrogen receptor alpha gene by phthalates. J Toxicol Environ Health A 68:1995–2003CrossRef PubMed
  Keil R, Salemme K, Forrest B, Neibauer J, Logsdon M (2011) Differential presence of anthropogenic compounds dissolved in the marine waters of Puget Sound, WA and Barkley Sound, BC. Mar Pollut Bull 62:2404–2411CrossRef PubMed
  Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310CrossRef PubMed
  Latham T, Gilbert N, Ramsahoye B (2008) DNA methylation in mouse embryonic stem cells and development. Cell Tissue Res 331:31–55CrossRef PubMed
  Lee YW, Broday L, Costa M (1998) Effects of nickel on DNA methyltransferase activity and genomic DNA methylation levels. Mutat Res 415(3):213–218CrossRef PubMed
  Licchesi JC, Kelly WG, Panning B (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39:615–651CrossRef
  Liu Y, Yuan C, Chen S, Zheng Y, Zhang Y, Goa J, Wang Z (2014) Global and cyp19a1a gene specific DNA methylation in gonads of adult rare minnow Gobiocypris rarus under bisphenol A exposure. Aquat Toxicol 156:10–16CrossRef PubMed
  MacKay AB, Aizeddin AM, McGowan RA, Krone PH (2007) Immunological detection of changes in genomic DNA methylation during early zebrafish development. Genome 50:778–785CrossRef PubMed
  Mankidy R, Wiseman S, Ma H, Giesy JP (2013) Biological impact of phthalates. Toxicol Lett 217:50–58CrossRef PubMed
  Martinez-Arguelles DB, Culty M, Zirkin BR, Papadopolous V (2009) In utero exposure to di-2-(ethylhexyl) phthalate decreases mineralocorticoid receptor expression in the adult testis. Endocrinology 150:5575–5585PubMedCentral CrossRef PubMed
  McCurley AT, Callard GV (2008) Characterization of housekeeping genes in zebrafish: male–female differences and effects of tissue type, developmental stage and chemical treatment. BMC Mol Bio 9:102CrossRef
  Mhanni AA, McGowan RA (2004) Global changes in genomic methylation levels during early development of the zebrafish embryo. Dev Genes Evol 214:412–417CrossRef PubMed
  Mirbahai L, Chipman JK (2014) Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposure. Mutat Res Genet Toxicol Environ Mutagen 764–765:10–17CrossRef PubMed
  Norman A, Borjeson H, David F, Tiempont B, Norrgren L (2007) Studies of uptake, elimination, and late effects in Atlantic salmon (Salmo salar) dietary exposed to di-2-ethylhexyl phthalate (DEHP) during early life. Arch Environ Contam Toxicol 52:235–242CrossRef PubMed
  Olsvik PA, Williams TD, Tung HS, Mirbahai L, Sanden M, Skjaerven KH, Ellingsen S (2014) Impacts of TCDD and MeHg on DNA methylation in zebrafish (Danio rerio) across two generations. Comp Biochem Physiol C: Toxicol Pharmacol 165:17–27
  Øvergård AC, Nerland AH, Patel S (2010) Evaluation of potential reference genes for real time RT-PCR studies in Atlantic halibut (Hippoglossus Hippoglossus L.); during development, in tissues of healthy and NNV-injected fish, and in anterior kidney leucocytes. BMC Mol Biol 11:36PubMedCentral CrossRef PubMed
  Rai K, Nadauld LD, Chidester S, Manos EJ, James SR, Karpf AR, Cairs BR, Jones DA (2006) Zebra fish dnmt1 and suv39h1 regulate organ-specific terminal differentiation during development. Mol Cell Biol 26:7077–7085PubMedCentral CrossRef PubMed
  Rajesh P, Balasubramanian K (2014) Phthalate exposure in utero causes epigenetic changes and impairs insulin signalling. J Endocrinol 223:47–66CrossRef PubMed
  Razin A (1998) CpG methylation, chromatin structure and gene silencing—a three-way connection. EMBO J 17:4905–4908PubMedCentral CrossRef PubMed
  Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447:425–432CrossRef PubMed
  Rizwana R, Hahn PJ (1999) CpG methylation reduces genomic instability. J Cell Sci 112:4513–4519PubMed
  Schaedlich K, Schmidt JS, Kwong WY, Sinclair KD, Kurz R, Jahnke HG, Fischer B (2015) Impact of di-ethylhexylphthalate exposure on metabolic programming in P19 ECC-derived cardiomyocytes. J Appl Toxicol 35:861–869. doi:10.​1002/​jat.​3085 CrossRef PubMed
  Seritrakul P, Gross JM (2013) Expression of the de novo DNA methyltransferases (dnmt3–dnmt8) during zebrafish lens development. Dev Dyn 243:350–356CrossRef PubMed
  Shimoda N, Yamakoshi K, Miyake A, Takeda H (2005) Identification of a gene required for de novo DNA methylation of the zebrafish no tail gene. Dev Dyn 233:1509–1516CrossRef PubMed
  Smith THL, Collins TM, McGowan RA (2011) Expression of the dnmt3 genes in zebrafish development: similarity to Dnmt3a and Dnmt3b. Dev Genes Evol 220:347–353CrossRef PubMed
  Stein R, Razin A, Cedar H (1982) In vitro methylation of the hamster adenine phosphoribosyltransferase gene inhibits its expression in mouse L cells. Proc Natl Acad Sci USA 79:3418–3422PubMedCentral CrossRef PubMed
  Sun Y, Guo Z, Iku S, Saito T, Kurasaki M (2013) Diethyl phthalate enhances expression of SIRT1 and DNMT3a during apoptosis in PC12 cells. J Appl Toxicol 33:1484–1492CrossRef PubMed
  Tweedie S, Charlton J, Clark V, Bird A (1997) Methylation of genomes and genes at the invertebrate-vertebrate boundary. Mol Cell Biol 17:1469–1475PubMedCentral CrossRef PubMed
  United States Environmental Protection Agency (1996) Prehatching development of the Fathead Minnow Rafinesque Office Res Dev Washington, DC
  Untergrasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40(15):e115CrossRef
  Vandegehuchte MB, Janssen CR (2011) Epigenetics and its implications for ecotoxicology. Ecotoxicology 20:607–624CrossRef PubMed
  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):93–98CrossRef PubMed
  Wang X, Yang Y, Zhang L, Ma Y, Han J, Yang L, Zhou B (2013) Endocrine disruption by di-(2-ethylhexyl) phthalate in Chinese rare minnow. Environ Toxicol Chem 32:1846–1854CrossRef PubMed
  Wilkinson LS, Davies W, Isles AR (2007) Genomic imprinting effects on brain development and function. Nat Rev Neurosci 8:832–843CrossRef PubMed
  Williams TD, Mirbahai L, Chipman JK (2014) The toxicological application of transcriptomics and epigenomics in zebrafish and other teleosts. Brief Funct Genomics 13:157–171CrossRef PubMed
  Wood RK, Seidel JS, Martyniuk CJ (2015) Transcripts involved in steroid biosynthesis and steroid receptor signaling are expressed early in development in the fathead minnow (Pimephales promelas). Comp Biochem Physiol B: Biochem Mol Biol 182:64–72CrossRef
  Wu S, Zhu J, Li Y, Lin T, Gan L, Yuan X, Xiong J, Liu X, Xu M, Zhao D, Ma C, Li X, Wei G (2010) Dynamic epigenetic changes involved in testicular toxicity induced by di-2-(ethylhexyl) phthalate in mice. Basic Clin Pharmacol Toxicol 106:118–123CrossRef PubMed
  Ye T, Kang M, Huang Q, Fang C, Chen Y, Shen H, Dong S (2014) Exposure to DEHP and MEHP from hatching to adulthood causes reproductive dysfunction and endocrine disruption in marine medaka (Oryzias melastigma). Aquat Toxicol 146:115–126CrossRef PubMed
  Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335–340CrossRef PubMed
  Zanotelli VR, Neuhauss SC, Ehrengruber MU (2010) Long-term exposure to bis(2-ethylhexyl)phthalate (DEHP) inhibits growth of guppy fish (Poecilia reticulata). J Appl Toxicol 30:29–33CrossRef PubMed
  
• 作者单位：Richard K. Wood (1)
  Emma Crowley (1)
  Christopher J. Martyniuk (1) (2)
  
  1. Department of Biology, Canadian Rivers Institute, University of New Brunswick, Saint John, NB, E2L 4L5, Canada
  2. Department of Physiological Sciences, Center for Environmental and Human Toxicology, University of Florida Genetics Institute, University of Florida, Gainesville, FL, 32611, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Hydrobiology
  Animal Physiology
  Animal Anatomy, Morphology and Histology
  Animal Biochemistry
  Zoology
  
• 出版者：Springer Netherlands
• ISSN：1573-5168

文摘

DNA methylation is an epigenetic regulator of gene expression, and this process has been shown to be disrupted by environmental contaminants. Di-2-(ethylhexyl) phthalate (DEHP) and related phthalate esters have been shown to affect development in early life stages of fish and can alter genomic methylation patterns in vertebrates. The objectives of this study were the following: (1) Describe the expression patterns of the DNA methyltransferase (dnmt) genes during early fathead minnow (FHM) development. These genes are critical for methylation and imprinting during development. (2) Determine the effects of DEHP on the development of FHM larvae [1 and 14 days post-hatch (dph)]. (3) Determine the effect of DEHP on dnmt expression and global methylation status in larval FHM. FHMs were first collected over a developmental time course [1, 3, 5, 6, and 14 days post-fertilization (dpf)] to investigate the expression patterns of five dnmt isoforms. The expression of dnmt1 and dnmt7 was relatively high in embryos at 1 dpf but was variable in expression, and these transcripts were later expressed at a lower level (>3 dpf); dnmt3 was significantly higher in embryos at 1 dpf compared to those at 3 dpf. Dnmt6 showed more of a constitutive pattern of expression during the first 2 weeks of development, and the mRNA levels of dnmt8 were higher in embryos at 5 and 6 dpf compared to those at 1 and 3 dpf, corresponding to the hatching period of the embryos. A waterborne exposure to three concentrations of DEHP (1, 10 and 100 µg/L) was conducted on 1-day FHM embryos for 24 h and on larval fish for 2 weeks, ending at 14 dpf. DEHP did not negatively affect survival, hatch rate, or the expression of dnmt isoforms in FHMs. There were no differences in global cytosine methylation following DEHP treatments in 14 dpf larvae, suggesting that environmentally relevant levels of DEHP may not affect global methylation at this stage of FHM development. However, additional targeted methylome studies are required to determine whether specific gene promoters are differently methylated following exposure to DEHP. This study offers new insight into the roles of the dnmt enzymes during FHM development. Keywords Phthalates Toxicology Survival DNA methylation