DNA methylation changes in the placenta are associated with fetal manganese exposure

Reproductive Toxicology

Volumn 57, Issue , 2015, Pages 43-49

  Maccani, Jennifer Z J ^a   Koestler, Devin C ^b   Houseman, E Andrés ^c   Armstrong, David A ^e   Marsit, Carmen J ^d,e   Kelsey, Karl T ^f,g  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d Department of Community and Family Medicine ^*  (United States)

^e DARTMOUTH MEDICAL SCHOOL   (United States)

^f BROWN UNIVERSITY   (United States)

^g BROWN UNIVERSITY   (United States)

Author keywords

Epigenetics; In utero; LOC284276; Manganese; Methylation; Placenta; Pregnancy

Indexed keywords

MANGANESE;

ADULT; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; FETUS; FETUS GROWTH; GENE LOCUS; GENETIC ASSOCIATION; HUMAN; HUMAN TISSUE; INFANT; LOW BIRTH WEIGHT; MALE; NERVE CELL DIFFERENTIATION; PLACENTA; PRENATAL EXPOSURE; TUMOR GENE; BIRTH WEIGHT; CHEMISTRY; FETOMATERNAL TRANSFUSION; GENETIC EPIGENESIS; MATERNAL EXPOSURE; NAIL; NEWBORN; PREGNANCY; YOUNG ADULT;

ADULT; BIRTH WEIGHT; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; INFANT, NEWBORN; MALE; MANGANESE; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; NAILS; PLACENTA; PREGNANCY; YOUNG ADULT;

EID: 84939563991     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2015.05.002     Document Type: Article

References (84)

1. Dandrea J., Wilson V., Gopalakrishnan G., Heasman L., Budge H., Stephenson T., et al. Maternal nutritional manipulation of placental growth and glucose transporter 1 (GLUT-1) abundance in sheep. Reproduction 2001, 122(5):793-800.
2. Desai M., Hales C.N. Role of fetal and infant growth in programming metabolism in later life. Biol Rev Camb Philos Soc 1997, 72(2):329-348.
3. Mattison D.R. Environmental exposures and development. Curr Opin Pediatr 2010, 22(2):208-218.
4. Maccani J.Z.J., Koestler D.C., Houseman E.A., Marsit C.J., Kelsey K.T. Smoking-related changes to placental DNA methylation at the RUNX3 gene are associated with gestational age. Epigenomics 2013, 5(6):619-630.
5. Novakovic B., Ryan J., Pereira N., Boughton B., Craig J.M., Saffery R. Postnatal stability, tissue, and time specific effects of AHRR methylation change in response to maternal smoking in pregnancy. Epigenetics 2014, 9(3):377-386.
6. Wilhelm-Benartzi C.S., Houseman E.A., Maccani M.A., Poage G.M., Koestler D.C., Langevin S.M., et al. In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect 2012, 120(2):296-302.
7. Suter M., Abramovici A., Showalter L., Hu M., Shope C.D., Varner M., et al. In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism: Clin Exp 2010, 59(10):1481-1490.
8. Suter M., Ma J., Harris A., Patterson L., Brown K.A., Shope C., et al. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics 2011, 6(11):1284-1294. (official journal of the DNA Methylation Society).
9. Nielsen F.H. How should dietary guidance be given for mineral elements with beneficial actions or suspected of being essential?. J Nutr 1996, 126(9 Suppl):2377S-2385S.
10. Pennington J.A., Young B.E. Total diet study nutritional elements, 1982-1989. J Am Diet Assoc 1991, 91(2):179-183.
11. Antonova M.V. Effect of different amounts of manganese in the daily food ration on the growth and development of the progeny of white rats. Vopr Pitan 1978, 1:65-68.
12. Wozniak A., Kujawa A., Senczuk-Przybylowska M., Kulza M., Gawecki W., Szybiak B., et al. Physiological metals in the serum, hair and nails of patients with head and neck cancer. Przegl Lek 2012, 69(10):785-797.
13. Karimi G., Shahar S., Homayouni N., Rajikan R., Abu Bakar N.F., Othman M.S. Association between trace element and heavy metal levels in hair and nail with prostate cancer. Asian Pac J Cancer Prev 2012, 13(9):4249-4253.
14. Zota A.R., Ettinger A.S., Bouchard M., Amarasiriwardena C.J., Schwartz J., Hu H., et al. Maternal blood manganese levels and infant birth weight. Epidemiology 2009, 20(3):367-373.
15. Mistry H.D., Williams P.J. The importance of antioxidant micronutrients in pregnancy. Oxid Med Cell Longevity 2011, 2011:841749.
16. Misselwitz B., Muhler A., Weinmann H.J. A toxicologic risk for using manganese complexes? A literature survey of existing data through several medical specialties. Invest Radiol 1995, 30(10):611-620.
17. Takser L., Mergler D., Hellier G., Sahuquillo J., Huel G. Manganese, monoamine metabolite levels at birth, and child psychomotor development. Neurotoxicology 2003, 24(4-5):667-674.
18. Miller R.K., Mattison D.R., Panigel M., Ceckler T., Bryant R., Thomford P. Kinetic assessment of manganese using magnetic resonance imaging in the dually perfused human placenta in vitro. Environ Health Perspect 1987, 74:81-91.
19. Cantone L., Nordio F., Hou L., Apostoli P., Bonzini M., Tarantini L., et al. Inhalable metal-rich air particles and histone H3K4 dimethylation and H3K9 acetylation in a cross-sectional study of steel workers. Environ Health Perspect 2011, 119(7):964-969.
20. Goodrich J.M., Basu N., Franzblau A., Dolinoy D.C. Mercury biomarkers and DNA methylation among Michigan dental professionals. Environ Mol Mutagen 2013, 54(3):195-203.
21. Baccarelli A., Bollati V. Epigenetics and environmental chemicals. Curr Opin Pediatr 2009, 21(2):243-251.
22. Wang L., Shiraki A., Itahashi M., Akane H., Abe H., Mitsumori K., et al. Aberration in epigenetic gene regulation in hippocampal neurogenesis by developmental exposure to manganese chloride in mice. Toxicol Sci 2013, 136(1):154-165.
23. Hu H., Shine J., Wright R.O. The challenge posed to children's health by mixtures of toxic waste: the Tar Creek superfund site as a case-study. Pediatr Clin North Am 2007, 54(1):155-175.
24. Delves H.T., Clayton B.E., Bicknell J. Concentration of trace metals in the blood of children. Br J Prev Soc Med 1973, 27(2):100-107.
25. Joselow M.M., Tobias E., Koehler R., Coleman S., Bogden J., Gause D. Manganese pollution in the city environment and its relationship to traffic density. Am J Public Health 1978, 68(6):557-560.
26. Zielhuis R.L., del Castilho P., Herber R.F., Wibowo A.A. Levels of lead and other metals in human blood: suggestive relationships, determining factors. Environ Health Perspect 1978, 25:103-109.
27. Claus Henn B., Ettinger A.S., Schwartz J., Tellez-Rojo M.M., Lamadrid-Figueroa H., Hernandez-Avila M., et al. Early postnatal blood manganese levels and children's neurodevelopment. Epidemiology 2010, 21(4):433-439.
28. Roels H.A., Bowler R.M., Kim Y., Claus Henn B., Mergler D., Hoet P., et al. Manganese exposure and cognitive deficits: a growing concern for manganese neurotoxicity. Neurotoxicology 2012, 33(4):872-880.
29. Ericson J.E., Crinella F.M., Clarke-Stewart K.A., Allhusen V.D., Chan T., Robertson R.T. Prenatal manganese levels linked to childhood behavioral disinhibition. Neurotoxicol Teratol 2007, 29(2):181-187.
30. Bunin G.R., Li Y., Ganguly A., Meadows A.T., Tseng M. Parental nutrient intake and risk of retinoblastoma resulting from new germline RB1 mutation. Cancer Causes Control: CCC 2013, 24(2):343-355.
31. Illumina Illumina HumanMethylation450 BeadChip Kit 2013, Available 〈http://www.illumina.com/products/methylation_450_beadchip_kits.ilmn〉 [accessed 2013 Mar 7 2013].
32. Lesseur C., Gilbert-Diamond D., Andrew A.S., Ekstrom R.M., Li Z., Kelsey K.T., et al. A case-control study of polymorphisms in xenobiotic and arsenic metabolism genes and arsenic-related bladder cancer in New Hampshire. Toxicol Lett 2012, 210(1):100-106.
33. Karagas M.R., Andrew A.S., Nelson H.H., Li Z., Punshon T., Schned A., et al. SLC39A2 and FSIP1 polymorphisms as potential modifiers of arsenic-related bladder cancer. Hum Genet 2012, 131(3):453-461.
34. Banister C.E., Koestler D.C., Maccani M.A., Padbury J.F., Houseman E.A., Marsit C.J. Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics 2011, 6(7):920-927. (official journal of the DNA Methylation Society).
35. Koestler D.C., Avissar-Whiting M., Houseman E.A., Karagas M.R., Marsit C.J. Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic in utero. Environ Health Perspect 2013, 121(8):971-977.
36. Marsit C.J., Houseman E.A., Christensen B.C., Gagne L., Wrensch M.R., Nelson H.H., et al. Identification of methylated genes associated with aggressive bladder cancer. PLoS ONE 2010, 5(8):e12334.
37. Blair J.D., Langlois S., McFadden D.E., Robinson W.P. Overlapping DNA methylation profile between placentas with trisomy 16 and early-onset preeclampsia. Placenta 2014, 35(3):216-222.
38. Kuan P.F., Wang S., Zhou X., Chu H. A statistical framework for Illumina DNA methylation arrays. Bioinformatics 2010, 26(22):2849-2855.
39. Johnson W.E., Li C., Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007, 8(1):118-127.
40. Westfall P.H., Young S.S. Resampling-based multiple testing: examples and methods for P-value adjustment 1993, Wiley, New York, NY.
41. Dunn O.J. Multiple comparisons among means. JASA 1961, 56(293):52-64.
42. Goullé J.P., Saussereau E., Mahieu L., Bouige D., Groenwont S., Guerbet M., et al. Application of inductively coupled plasma mass spectrometry multielement analysis in fingernail and toenail as a biomarker of metal exposure. J Anal Toxicol 2009, 33:92-98.
43. Spigoni G., Gedressi C., Mallamaci A. Regulation of Emx2 expression by antisense transcripts in murine cortico-cerebral precursors. PLoS ONE 2010, 5(1):e8658.
44. Leachman N.T., Brellier F., Ferralli J., Chiquet-Ehrismann R., Tucker R.P. ATAD2B is a phylogenetically conserved nuclear protein expressed during neuronal differentiation and tumorigenesis. Dev Growth Differ 2010, 52(9):747-755.
45. Alves dos Santos M.T., Smidt M.P. En1 and Wnt signaling in midbrain dopaminergic neuronal development. Neural Dev 2011, 6:23.
46. Bassols J., Prats-Puig A., Vazquez-Ruiz M., Garcia-Gonzalez M.M., Martinez-Pascual M., Avelli P., et al. Placental FTO expression relates to fetal growth. Int J Obes (Lond) 2010, 34(9):1365-1370.
47. Vigeh M., Yokoyama K., Ramezanzadeh F., Dahaghin M., Fakhriazad E., Seyedaghamiri Z., et al. Blood manganese concentrations and intrauterine growth restriction. Reprod Toxicol 2008, 25(2):219-223.
48. Guan H., Wang M., Li X., Piao F., Li Q., Xu L., et al. Manganese concentrations in maternal and umbilical cord blood: related to birth size and environmental factors. Eur J Public Health 2014, 24(1):150-157.
49. Barrett T., Wilhite S.E., Ledoux P., Evangelista C., Kim I.F., Tomashevsky M., et al. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res 2013, 41(Jan (Database issue)):D991-D995.
50. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003, 4(5):P3.
51. Aston C., Jiang L., Sokolov B.P. Transcriptional profiling reveals evidence for signaling and oligodendroglial abnormalities in the temporal cortex from patients with major depressive disorder. Mol Psychiatry 2005, 10(3):309-322.
52. Anitha A., Nakamura K., Yamada K., Suda S., Thanseem I., Tsujii M., et al. Genetic analyses of roundabout (ROBO) axon guidance receptors in autism. Am J Med Genet, B: Neuropsychiatr Genet 2008, 147B(7):1019-1027. (the official publication of the International Society of Psychiatric Genetics).
53. Araki T., Milbrandt J. ZNRF proteins constitute a family of presynaptic E3 ubiquitin ligases. J Neurosci 2003, 23(28):9385-9394. (the official journal of the Society for Neuroscience).
54. Aston C., Jiang L., Sokolov B.P. Microarray analysis of postmortem temporal cortex from patients with schizophrenia. J Neurosci Res 2004, 77(6):858-866.
55. Bani-Yaghoub M., Felker J.M., Sans C., Naus C.C. The effects of bone morphogenetic protein 2 and 4 (BMP2 and BMP4) on gap junctions during neurodevelopment. Exp Neurol 2000, 162(1):13-26.
56. Bao X., Nishimura S., Mikami T., Yamada S., Itoh N., Sugahara K. Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of l-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities. J Biol Chem 2004, 279(11):9765-9776.
57. Bohm J., Buck A., Borozdin W., Mannan A.U., Matysiak-Scholze U., Adham I., et al. Sall1, sall2, and sall4 are required for neural tube closure in mice. Am J Pathol 2008, 173(5):1455-1463.
58. Carroll K., Gomez C., Shapiro L. Tubby proteins: the plot thickens. Nat Rev Mol Cell Biol 2004, 5(1):55-63.
59. Christensen R., de la Torre-Ubieta L., Bonni A., Colon-Ramos D.A. A conserved PTEN/FOXO pathway regulates neuronal morphology during C. elegans development. Development 2011, 138(23):5257-5267.
60. Dai X., Jiang W., Zhang Q., Xu L., Geng P., Zhuang S., et al. Requirement for integrin-linked kinase in neural crest migration and differentiation and outflow tract morphogenesis. BMC Biol 2013, 11:107.
61. de Vries P.J., Howe C.J. The tuberous sclerosis complex proteins-a GRIPP on cognition and neurodevelopment. Trends Mol Med 2007, 13(8):319-326.
62. Fukumoto K., Morita T., Mayanagi T., Tanokashira D., Yoshida T., Sakai A., et al. Detrimental effects of glucocorticoids on neuronal migration during brain development. Mol Psychiatry 2009, 14(12):1119-1131.
63. Gaufo G.O., Thomas K.R., Capecchi M.R. Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 2003, 130(21):5191-5201.
64. Grady R.M., Merlie J.P., Sanes J.R. Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 1997, 136(4):871-882.
65. Yang T., Kersigo J., Jahan I., Pan N., Fritzsch B. The molecular basis of making spiral ganglion neurons and connecting them to hair cells of the organ of Corti. Hear Res 2011, 278(1-2):21-33.
66. St John J.A., Key B. EphB2 and two of its ligands have dynamic protein expression patterns in the developing olfactory system. Brain Res Dev Brain Res 2001, 126(1):43-56.
67. Griswold A.J., Ma D., Cukier H.N., Nations L.D., Schmidt M.A., Chung R.H., et al. Evaluation of copy number variations reveals novel candidate genes in autism spectrum disorder-associated pathways. Hum Mol Genet 2012, 21(15):3513-3523.
68. Laurin N., Lee J., Ickowicz A., Pathare T., Malone M., Tannock R., et al. Association study for genes at chromosome 5p13-q11 in attention deficit hyperactivity disorder. Am J Med Genet, B: Neuropsychiatr Genet 2008, 147B(5):600-605. (the official publication of the International Society of Psychiatric Genetics).
69. Kowalska A., Midro A.T., Janik P., Gogol A., Sluzewski W., Rajewski A. Searching for Tourette's syndrome gene. Part 2. Patient's genome variability. Postepy Hig Med Dosw (Online) 2012, 66:89-95.
70. Hosak L. New findings in the genetics of schizophrenia. World J Psychiatry 2013, 3(3):57-61.
71. Bian J.T., Zhao H.L., Zhang Z.X., Bi X.H., Zhang J.W. Association of NAD(P)H:quinone oxidoreductase 1 polymorphism and Alzheimer's disease in Chinese. J Mol Neurosci 2008, 34(3):235-240.
72. Gant J.C., Blalock E.M., Chen K.C., Kadish I., Porter N.M., Norris C.M., et al. FK506-binding protein 1b/12.6: A key to aging-related hippocampal Ca dysregulation?. Eur J Pharmacol 2014, 739:74-82.
73. Brooks W.S., Helton E.S., Banerjee S., Venable M., Johnson L., Schoeb T.R., et al. G2E3 is a dual function ubiquitin ligase required for early embryonic development. J Biol Chem 2008, 283(32):22304-22315.
74. Schwindinger W.F., Reese K.J., Lawler A.M., Gearhart J.D., Levine M.A. Targeted disruption of Gnas in embryonic stem cells. Endocrinology 1997, 138(10):4058-4063.
75. Campioni M., Severino A., Manente L., Tuduce I.L., Toldo S., Caraglia M., et al. The serine protease HtrA1 specifically interacts and degrades the tuberous sclerosis complex 2 protein. Mol Cancer Res: MCR 2010, 8(9):1248-1260.
76. Clark D.E., Smith S.K., Licence D., Evans A.L., Charnock-Jones D.S. Comparison of expression patterns for placenta growth factor, vascular endothelial growth factor (VEGF), VEGF-B and VEGF-C in the human placenta throughout gestation. J Endocrinol 1998, 159(3):459-467.
77. Gellhaus A., Schmidt M., Dunk C., Lye S.J., Kimmig R., Winterhager E. Decreased expression of the angiogenic regulators CYR61 (CCN1) and NOV (CCN3) in human placenta is associated with pre-eclampsia. Mol Hum Reprod 2006, 12(6):389-399.
78. Hemberger M., Nozaki T., Winterhager E., Yamamoto H., Nakagama H., Kamada N., et al. Parp1-deficiency induces differentiation of ES cells into trophoblast derivatives. Dev Biol 2003, 257(2):371-381.
79. Westerman B.A., Chhatta A., Poutsma A., van Vegchel T., Oudejans C.B. NEUROD1 acts in vitro as an upstream regulator of NEUROD2 in trophoblast cells. Biochim Biophys Acta 2004, 1676(1):96-103.
80. Bromer C., Marsit C.J., Armstrong D.A., Padbury J.F., Lester B. Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Dev Psychobiol 2013, 55(7):673-683.
81. Lesseur C., Paquette A.G., Marsit C.J. Epigenetic regulation of infant neurobehavioral outcomes. Med Epigenet 2014, 2(2):71-79.
82. Marsit C.J. Influence of environmental exposure on human epigenetic regulation. J Exp Biol 2015, 218(Pt 1):71-79.
83. Sanders A.P., Smeester L., Rojas D., DeBussycher T., Wu M.C., Wright F.A., et al. Cadmium exposure and the epigenome: exposure-associated patterns of DNA methylation in leukocytes from mother-baby pairs. Epigenetics 2014, 9(2):212-221.
84. Feldmann A., Ivanek R., Murr R., Gaidatzis D., Burger L., Schübeler D. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet 2013, 9(12):e1003994.