Aberrant 5′-CpG methylation of cord blood TNFα associated with maternal exposure to polybrominated diphenyl ethers

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Dao, Tyna ^a   Hong, Xiumei ^a   Wang, Xiaobin ^a   Tang, Wan Yee ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; INTERLEUKIN 1BETA; POLYBROMINATED DIPHENYL ETHER; TUMOR NECROSIS FACTOR ALPHA; DIPHENYL ETHER DERIVATIVE; TNF PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ADULT; AGE; ARTICLE; BLOOD LEVEL; BODY MASS; CHILD HEALTH; COHORT ANALYSIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EDUCATIONAL STATUS; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE; GENDER; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MALE; MATERNAL AGE; MATERNAL BLOOD; PARITY; PREMATURE LABOR; PROMOTER REGION; SMOKING; TNF ALPHA GENE; UMBILICAL CORD BLOOD; BLOOD; CHEMISTRY; DRUG EFFECTS; EPIDEMIOLOGY; FETUS BLOOD; GENETIC EPIGENESIS; GENETICS; MATERNAL EXPOSURE; NEWBORN; PREGNANCY; PREGNANCY OUTCOME;

ADULT; COHORT EFFECT; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL BLOOD; HALOGENATED DIPHENYL ETHERS; HUMANS; INFANT, NEWBORN; MALE; MATERNAL EXPOSURE; PREGNANCY; PREGNANCY OUTCOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84947226174     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138815     Document Type: Article

References (65)

1. Woods R, Vallero RO, Golub MS, Suarez JK, Ta TA, Yasui DH, et al. Long-lived epigenetic interactions between perinatal PBDE exposure and Mecp2308 mutation. Human molecular genetics. 2012; 21 (11):2399-411. doi: 10.1093/hmg/dds046 PMID: 22343140
2. Costa LG, de Laat R, Tagliaferri S, Pellacani CA mechanistic view of polybrominated diphenyl ether (PBDE) developmental neurotoxicity. Toxicology letters. 2014; 230(2):282-94. doi: 10.1016/j.toxlet.2013.11.011 PMID: 24270005
3. Ta TA, Koenig CM, Golub MS, Pessah IN, Qi L, Aronov PA, et al. Bioaccumulation and behavioral effects of 2, 2', 4, 4'-tetrabromodiphenyl ether (BDE-47) in perinatally exposed mice. Neurotoxicology and teratology. 2011; 33(3):393-404. doi: 10.1016/j.ntt.2011.02.003 PMID: 21334437
4. Abdallah MA, Harrad S. Polybrominated diphenyl ethers in UK human milk: implications for infant exposure and relationship to external exposure. Environment international. 2014; 63:130-6. doi: 10.1016/j.envint.2013.11.009 PMID: 24291653
5. Koenig CM, Lango J, Pessah IN, Berman RF. Maternal transfer of BDE-47 to offspring and neurobeha-vioral development in C57BL/6J mice. Neurotoxicology and teratology. 2012; 34(6):571-80. doi: 10.1016/j.ntt.2012.09.005 PMID: 23022914
6. Geyer HJ, Schramm K, Darnerud PO, Aune M, Feicht EA, Fried KW, et al. Terminal elimination half-lives of the brominated flame retardants TBBPA, HBCD, and lower brominated PBDEs in humans. Organohalogen Compounds. 2004; 66:3820-5.
7. USEPA. An Exposure Assessment of Polybrominated Diphenyl Ethers. Washington, DC 2010.
8. Koh TW, Chih-Cheng Chen S, Chang-Chien GP, Lin DY, Chen FA, Chao HR. Breast-milk levels of polybrominated diphenyl etherflame retardants in relation to women's age and pre-pregnant body mass index. Int J Hyg Environ Health. 2010; 213(1):59-65. doi: 10.1016/j.ijheh.2009.09.004 PMID: 19781992
9. Costa LG, Giordano G. Developmental neurotoxicity of polybrominated diphenyl ether (PBDE) flame retardants. Neurotoxicology. 2007; 28(6):1047-67. PMID: 17904639
10. Suvorov A, Girard S, Lachapelle S, Abdelouahab N, Sebire G, Takser L. Perinatal exposure to low-dose BDE-47, an emergent environmental contaminant, causes hyperactivity in rat offspring. Neonatology. 2009; 95(3):203-9. doi: 10.1159/000155651 PMID: 18799892
11. Suvorov A, Takser L. Delayed response in the rat frontal lobe transcriptome to perinatal exposure to the flame retardant BDE-47. Journal of applied toxicology: JAT. 2011; 31(5):477-83. doi: 10.1002/jat.1667 PMID: 21394737
12. Herbstman JB, Sjodin A, Kurzon M, Lederman SA, Jones RS, Rauh V, et al. Prenatal exposure to PBDEs and neurodevelopment. Environmental health perspectives. 2010; 118(5):712-9. doi: 10.1289/ehp.0901340 PMID: 20056561
13. Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG, Johnson C, et al. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environmental health perspectives. 2013; 121(2):257-62. doi: 10.1289/ehp.1205597 PMID: 23154064
14. Martin PA, Mayne GJ, Bursian FS, Tomy G, Palace V, Pekarik C, et al. Immunotoxicity of the commercial polybrominated diphenyl ether mixture DE-71 in ranch mink (Mustela vison). Environ Toxicol Chem. 2007; 26(5):988-97. PMID: 17521147
15. Suvorov A, Bissonnette C, Takser L, Langlois MF. Does 2, 2', 4, 4'-tetrabromodiphenyl ether interact directly with thyroid receptor? Journal of applied toxicology: JAT. 2011; 31(2):179-84. doi: 10.1002/jat.1580 PMID: 20737425
16. Hales CN, Barker DJ, Clark PM, Cox LJ, Fall C, Osmond C, et al. Fetal and infant growth and impaired glucose tolerance at age 64. BMJ (Clinical researched). 1991; 303(6809):1019-22.
17. Barker DJ, Osmond C, Simmonds SJ, Wield GA. The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. BMJ (Clinical research ed). 1993; 306 (6875):422-6.
18. Tang WY, Ho SM. Epigenetic reprogramming and imprinting in origins of disease. Reviews in endocrine & metabolic disorders. 2007; 8(2):173-82.
19. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nature reviews Genetics. 2007; 8(4):253-62. PMID: 17363974
20. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS. Developmental exposure to estradiol and bisphe-nol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer research. 2006; 66(11):5624-32. PMID: 16740699
21. Tang WY, Levin L, Talaska G, Cheung YY, Herbstman J, Tang D, et al. Maternal exposure to polycyclic aromatic hydrocarbons and 5'-CpG methylation of interferon-gamma in cord white blood cells. Environmental health perspectives. 2012; 120(8):1195-200. doi: 10.1289/ehp.1103744 PMID: 22562770
22. Tang WY, Newbold R, Mardilovich K, Jefferson W, Cheng RY, Medvedovic M, et al. Persistent hypo-methylation in the promoter of nucleosomal binding protein 1 (Nsbp1) correlates with overexpression of Nsbp1 in mouse uteri neonatally exposed to diethylstilbestrol or genistein. Endocrinology. 2008; 149 (12):5922-31. doi: 10.1210/en.2008-0682 PMID: 18669593
23. Perera F, Tang WY, Herbstman J, Tang D, Levin L, Miller R, et al. Relation of DNA methylation of 5'-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PloS one. 2009; 4(2):e4488. doi: 10.1371/journal.pone.0004488 PMID: 19221603
24. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012; 13(7):484-92. doi: 10.1038/nrg3230 PMID: 22641018
25. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. Global DNA hypo-methylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environmental health perspectives. 2008; 116(11):1547-52. doi: 10.1289/ehp.11338 PMID: 19057709
26. Huen K, Yousefi P, Bradman A, Yan L, Harley KG, Kogut K, et al. Effects of age, sex, and persistent organic pollutants on DNA methylation in children. Environmental and molecular mutagenesis. 2014; 55(3):209-22. doi: 10.1002/em.21845 PMID: 24375655
27. Byun HM, Benachour N, Zalko D, Frisardi MC, Colicino E, Takser L, Baccarelli AA. Epigenetic effects of low perinatal doses of flame retardant BDE-47 on mitochondrial and nuclear genes in rat offspring. Toxicology. 2015; 328:152-159. doi: 10.1016/j.tox.2014.12.019 PMID: 25533936
28. Du P, Li Z, Du L, Zhang H, Zhou Y, Sun W, Xiao X, He Y, Sun B, Yu Y, Chen DThe effects of PBDE-209 exposure during pregnancy on placental ET-1 and eNOS expression and the birth weight of offspring. Int J Dev Neurosci. 2015 Mar 27.
29. Liu X, Zhan H, Zeng X, Zhang C, Chen D. The PBDE-209 exposure during pregnancy and lactation impairs immune function in rats. Mediators of inflammation. 2012; 2012:692467. doi: 10.1155/2012/692467 PMID: 22619485
30. Viviani B, Boraso M, Marchetti N, Marinovich M. Perspectives on neuroinflammation and excitotoxicity: a neurotoxic conspiracy? Neurotoxicology. 2014; 43:10-20. doi: 10.1016/j.neuro.2014.03.004 PMID: 24662010
31. Evans HL. Markers of neurotoxicity: from behaviorto autoantibodies against brain proteins. Clin Chem. 1995; 41(12 Pt 2):1874-81. PMID: 7497648
32. Galic MA, Riazi K, Pittman QJ. Cytokines and brain excitability. Front Neuroendocrinol. 2012; 33 (1):116-25. doi: 10.1016/j.yfrne.2011.12.002 PMID: 22214786
33. Hong X, Wang X. Early life precursors, epigenetics, and the development of food allergy. Seminars in immunopathology. 2012; 34(5):655-69. doi: 10.1007/s00281-012-0323-y PMID: 22777545
34. Wang D, Liu X, Zhou Y, Xie H, Hong X, Tsai HJ, et al. Individual variation and longitudinal pattern of genome-wide DNA methylation from birth to the first two years of life. Epigenetics: official journal of the DNA Methylation Society. 2012; 7(6):594-605.
35. Wang X, Zuckerman B, Pearson C, Kaufman G, Chen C, Wang G, et al. Maternal cigarette smoking, metabolic gene polymorphism, and infant birth weight. Jama. 2002; 287(2):195-202. PMID: 11779261
36. Liu X, Wang G, Hong X, Tsai HJ, Liu R, Zhang S, et al. Associations between gene polymorphisms in fatty acid metabolism pathway and preterm delivery in a US urban black population. Human genetics. 2012; 131(3):341-51. doi: 10.1007/s00439-011-1079-5 PMID: 21847588
37. Sjodin A, McGahee EE3rd, Focant JF, Jones RS, Lapeza CR, Zhang Y, et al. Semiautomated high-throughput extraction and cleanup method for the measurement of polybrominated diphenyl ethers and polybrominated and polychlorinated biphenyls in breast milk. Anal Chem. 2004; 76(15):4508-14. PMID: 15283595
38. Matoba N, Yu Y, Mestan K, Pearson C, Ortiz K, Porta N, et al. Differential patterns of 27 cord blood immune biomarkers across gestational age. Pediatrics. 2009; 123(5):1320-8. doi: 10.1542/peds.2008-1222 PMID: 19403498
39. Sullivan KE, Reddy AB, Dietzmann K, Suriano AR, Kocieda VP, Stewart M, et al. Epigenetic regulation of tumor necrosis factor alpha. Molecular and cellular biology. 2007; 27(14):5147-60. PMID: 17515611
40. Liu X, Chen Q, Tsai HJ, Wang G, Hong X, Zhou Y, et al. Maternal preconception body mass index and offspring cord blood DNA methylation: exploration of early life origins of disease. Environmental and molecular mutagenesis. 2014; 55(3):223-30. doi: 10.1002/em.21827 PMID: 24243566
41. Golikova EA, Lopatnikova JA, Kovalevskaya-Kucheryavenko TV, Nepomnyashih VM, Sennikov SV. Levels of TNF, TNF autoantibodies and soluble TNF receptors in patients with bronchial asthma. The Journal of asthma: official journal of the Association for the Care of Asthma. 2013; 50(7):705-11.
42. Blandizzi C, Gionchetti P, Armuzzi A, Caporali R, Chimenti S, Cimaz R, et al. The role of tumour necrosis factor in the pathogenesis of immune-mediated diseases. International journal of immunopathology and pharmacology. 2014; 27(1 Suppl):1-10. PMID: 24774503
43. Nasiri R, Amirzargar AA, Movahedi M, Hirbod-Mobarakeh A, Farhadi E, Behniafard N, et al. Single-nucleotide polymorphisms of TNFA and IL1 in allergic rhinitis. Journal of investigational allergology & clinical immunology. 2013; 23(7):455-61.
44. Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature. 2013; 494(7437):361-5. doi: 10.1038/nature11824 PMID: 23376950
45. Goldfeld AE, Tsai E, Kincaid R, Belshaw PJ, Schrieber SL, Strominger JL, et al. Calcineurin mediates human tumor necrosis factor alpha gene induction in stimulated T and B cells. The Journal of experimental medicine. 1994; 180(2):763-8. PMID: 8046352
46. El Gazzar M, Yoza BK, Chen X, Hu J, Hawkins GA, McCall CE. G9a and HP1 couple histone and DNA methylation to TNFalpha transcription silencing during endotoxin tolerance. The Journal of biological chemistry. 2008; 283(47):32198-208. doi: 10.1074/jbc.M803446200 PMID: 18809684
47. Barthel R, Tsytsykova AV, Barczak AK, Tsai EY, Dascher CC, Brenner MB, et al. Regulation of tumor necrosis factor alpha gene expression by mycobacteria involves the assembly of a unique enhanceo-some dependent on the coactivator proteins CBP/p300. Molecular and cellular biology. 2003; 23 (2):526-33. PMID: 12509451
48. Li Y, Reddy MA, Miao F, Shanmugam N, Yee JK, Hawkins D, et al. Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes. Relevance to diabetes and inflammation. The Journal of biological chemistry. 2008; 283(39):26771-81. doi: 10.1074/jbc.M802800200 PMID: 18650421
49. Ranjbar S, Rajsbaum R, Goldfeld AE. Transactivator of transcription from HIV type 1 subtype E selectively inhibits TNF gene expression via interference with chromatin remodeling of the TNF locus. Journal of immunology (Baltimore, Md: 1950). 2006; 176(7):4182-90.
50. Tsytsykova AV, Falvo JV, Schmidt-Supprian M, Courtois G, Thanos D, Goldfeld AE. Post-induction, stimulus-specific regulation of tumor necrosis factor mRNA expression. The Journal of biological chemistry. 2007; 282(16):11629-38. PMID: 17303559
51. Li Z, Chao TC, Chang KY, Lin N, Patil VS, Shimizu C, et al. The long noncoding RNATHRIL regulates TNFalpha expression through its interaction with hn RNPL. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111(3):1002-7. doi: 10.1073/pnas.1313768111 PMID: 24371310
52. Tsytsykova AV, Rajsbaum R, Falvo JV, Ligeiro F, Neely SR, Goldfeld AE. Activation-dependent intrachromosomal interactions formed by the TNF gene promoter and two distal enhancers. Proceedings of the National Academy of Sciences of the United States of America. 2007; 104(43):16850-5. PMID: 17940009
53. Sullivan KE, Suriano A, Dietzmann K, Lin J, Goldman D, Petri MA. The TNFalpha locus is altered in monocytes from patients with systemic lupus erythematosus. Clinical immunology. 2007; 123(1):74-81. PMID: 17276734
54. Hermsdorff HH, Mansego ML, Campion J, Milagro FI, Zulet MA, Martinez JA. TNF-alpha promoter methylation in peripheral white blood cells: relationship with circulating TNFalpha, truncal fat and n-6 PUFA intake in young women. Cytokine. 2013; 64(1):265-71. doi: 10.1016/j.cyto.2013.05.028 PMID: 23796695
55. Falvo JV, Jasenosky LD, Kruidenier L, Goldfeld AE. Epigenetic control of cytokine gene expression: regulation of the TNF/LT locus and T helper cell differentiation. Advances in immunology. 2013; 118:37-128. doi: 10.1016/B978-0-12-407708-9.00002-9 PMID: 23683942
56. Almasry SM, Eldomiaty MA, Elfayomy AK, Habib FA. Expression pattern of tumor necrosis factor alpha in placentae of idiopathic fetal growth restriction. Journal of molecular histology. 2012; 43(3):253-61. doi: 10.1007/s10735-012-9410-6 PMID: 22461198
57. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HHetal. DNAmeth-ylation arrays as surrogate measures of cell mixture distribution. BMC bioinformatics. 2012; 13:86 doi: 10.1186/1471-2105-13-86 PMID: 22568884
58. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan Betal. Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. Hum Mol Genet. 2012; 21(2):371-83. doi: 10.1093/hmg/ddr472 PMID: 21994764
59. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén SE, Greco Detal. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoSOne. 2012; 7(7):e41361. doi: 10.1371/journal.pone.0041361 PMID: 22848472
60. Singh AK, Kashyap MP. An Overview on Human Umbilical Cord Blood Stem Cell-Based Alternative In Vitro Models for Developmental Neurotoxicity Assessment. Mol Neurobiol. 2015. [Epub ahead of print].
61. Stock W, Hoffman R.White blood cells 1: non-malignant disorders. Lancet. 2000. 355:1351-57. PMID: 10776761
62. Sanders JM, Lebetkin EH, Chen LJ, Burka LT. Disposition of 2, 2', 4, 4', 5, 5'-hexabromodiphenyl ether (BDE153) and its interaction with other polybrominated diphenyl ethers (PBDEs) in rodents. Xenobio-tica. 2006; 36(9):824-37. PMID: 16971346
63. Staskal DF, Diliberto JJ, DeVito MJ, Birnbaum LS. Toxicokinetics of BDE 47 infemale mice: effect of dose, route of exposure, and time. Toxicological sciences: an official journal of the Society of Toxicology. 2005; 83(2):215-23.
64. Staskal DF, Hakk H, Bauer D, Diliberto JJ, Birnbaum LS. Toxicokinetics of polybrominated diphenyl ether congeners 47, 99, 100, and 153 in mice. Toxicological sciences: an official journal of the Society of Toxicology. 2006; 94(1):28-37.
65. Emond C, Sanders JM, Wikoff D, Birnbaum LS. Proposed mechanistic description of dose-dependent BDE-47 urinary elimination in mice using a physiologically based pharmacokinetic model. Toxicology and applied pharmacology. 2013; 273(2):335-44. doi: 10.1016/j.taap.2013.09.007 PMID: 24055880