Cadmium exposure and the epigenome: Exposure-associated patterns of DNA methylation in leukocytes from mother-baby pairs

Epigenetics

Volumn 9, Issue 2, 2014, Pages 212-221

  Sanders, Alison P ^a,h   Smeester, Lisa ^a   Rojas, Daniel ^b   DeBussycher, Tristan ^c   Wu, Michael C ^d   Wright, Fred A ^d   Zhou, Yi Hui ^d   Laine, Jessica E ^d   Rager, Julia E ^a   Swamy, Geeta K ^e   Ashley Koch, Allison ^f   Miranda, Marie Lynn ^g   Fry, Rebecca C ^a,b  

^a University of North Carolina   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d The University of North Carolina at Chapel Hill   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cadmium; Cigarette smoke; Cord blood; Epigenetics; Heavy metal; Maternal blood; Methylation; Pregnancy

Indexed keywords

5 METHYLCYTOSINE; CADMIUM; CADMIUM ASSOCIATED GENE; COTININE; COTININE ASSOCIATED GENE; DNA; MATERNAL DNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CIGARETTE SMOKE; HEAVY METAL;

APOPTOSIS; ARTICLE; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; FEMALE; FETUS; GENE ONTOLOGY; GENETIC REGULATION; HEAVY METAL POISONING; HUMAN; LEUKOCYTE; MATERNAL BLOOD; METHYLATED CPG ISLAND RECOVERY ASSAY; NEWBORN; POLYMERASE CHAIN REACTION; PREGNANCY; PRENATAL EXPOSURE; PROMOTER REGION; BLOOD; ENVIRONMENTAL EXPOSURE; FETOMATERNAL TRANSFUSION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; HUMAN GENOME; MALE; METABOLISM; METHYLATION; POLLUTANT; UMBILICAL CORD BLOOD;

CADMIUM; CIGARETTE SMOKE; CORD BLOOD; EPIGENETICS; HEAVY METAL; MATERNAL BLOOD; METHYLATION; PREGNANCY;

5-METHYLCYTOSINE; CADMIUM; COTININE; CPG ISLANDS; DNA METHYLATION; ENVIRONMENTAL POLLUTANTS; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; INFANT, NEWBORN; LEUKOCYTES; MALE; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; PREGNANCY; PROMOTER REGIONS, GENETIC;

EID: 84892580935     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.26798     Document Type: Article

References (65)

1. ATSDR. Priority List of Hazardous Substances. Online at: http://wwwatsdrcdcgov/spl/ 2011.
2. ATSDR. Toxicological Profile for Cadmium. Atlanta, GA: Centers for Diseaes Control, 2008.
3. Arita A, Costa M. Epigenetics in metal carcinogenesis: nickel, arsenic, chromium and cadmium. Metallomics 2009; 1:222-8; PMID:20461219; http://dx.doi. org/10.1039/b903049b
4. Waalkes MP. Cadmium carcinogenesis in review. J Inorg Biochem 2000; 79:241-4; PMID:10830873; http://dx.doi.org/10.1016/S0162-0134(00)00009-X
5. IARC. Volume 58. Cadmium. 1993:119-238
6. Fréry N, Nessmann C, Girard F, Lafond J, Moreau T, Blot P, Lellouch J, Huel G. Environmental exposure to cadmium and human birthweight. Toxicology 1993; 79:109-18; PMID:8497864; http://dx.doi. org/10.1016/0300-483X(93)90124-B
7. Lin CM, Doyle P, Wang DL, Hwang YH, Chen PC. Does prenatal cadmium exposure affect fetal and child growth? Occup Environ Med 2011; 68:641-6; PMID:21186202; http://dx.doi.org/10.1136/ oem.2010.059758
8. Nishijo M, Tawara K, Honda R, Nakagawa H, Tanebe K, Saito S. Relationship between newborn size and mother's blood cadmium levels, Toyama, Japan. Arch Environ Health 2004; 59:22-5; PMID:16053205; http://dx.doi.org/10.3200/AEOH.59.1.22-25
9. Salpietro CD, Gangemi S, Minciullo PL, Briuglia S, Merlino MV, Stelitano A, Cristani M, Trombetta D, Saija A. Cadmium concentration in maternal and cord blood and infant birth weight: a study on healthy non-smoking women. J Perinat Med 2002; 30:395-9; PMID:12442603; http://dx.doi.org/10.1515/ JPM.2002.061
10. Ronco AM, Arguello G, Muñoz L, Gras N, Llanos M. Metals content in placentas from moderate cigarette consumers: correlation with newborn birth weight. Biometals 2005; 18:233-41; PMID:15984568; http://dx.doi.org/10.1007/s10534-005-0583-2
11. Llanos MN, Ronco AM. Fetal growth restriction is related to placental levels of cadmium, lead and arsenic but not with antioxidant activities. Reprod Toxicol 2009; 27:88-92; PMID:19103280; http:// dx.doi.org/10.1016/j.reprotox.2008.11.057
12. Tian LL, Zhao YC, Wang XC, Gu JL, Sun ZJ, Zhang YL, Wang JX. Effects of gestational cadmium exposure on pregnancy outcome and development in the offspring at age 4.5 years. Biol Trace Elem Res 2009; 132:51-9; PMID:19404590; http://dx.doi. org/10.1007/s12011-009-8391-0
13. Shirai S, Suzuki Y, Yoshinaga J, Mizumoto Y. Maternal exposure to low-level heavy metals during pregnancy and birth size. J Environ Sci Health A Tox Hazard Subst Environ Eng 2010; 45:1468-74; PMID:20694885; http://dx.doi.org/10.1080/10934 529.2010.500942
14. Bonithon-Kopp C, Huel G, Moreau T, Wendling R. Prenatal exposure to lead and cadmium and psychomotor development of the child at 6 years. Neurobehav Toxicol Teratol 1986; 8:307-10; PMID:3736760
15. Heyn H, Li N, Ferreira HJ, Moran S, Pisano DG, Gomez A, Diez J, Sanchez-Mut JV, Setien F, Carmona FJ, et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A 2012; 109:10522-7; PMID:22689993; http://dx.doi. org/10.1073/pnas.1120658109
16. Woodruff TJ, Zota AR, Schwartz JM. Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ Health Perspect 2011; 119:878-85; PMID:21233055; http://dx.doi. org/10.1289/ehp.1002727
17. Järup L, Akesson A. Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 2009; 238:201-8; PMID:19409405; http://dx.doi.org/10.1016/j.taap.2009.04.020
18. Yu XD, Yan CH, Shen XM, Tian Y, Cao LL, Yu XG, Zhao L, Liu JX. Prenatal exposure to multiple toxic heavy metals and neonatal neurobehavioral development in Shanghai, China. Neurotoxicol Teratol 2011; 33:437-43; PMID:21664460; http:// dx.doi.org/10.1016/j.ntt.2011.05.010
19. Godfrey K, Walker-Bone K, Robinson S, Taylor P, Shore S, Wheeler T, Cooper C. Neonatal bone mass: influence of parental birthweight, maternal smoking, body composition, and activity during pregnancy. J Bone Miner Res 2001; 16:1694-703; PMID:11547840; http://dx.doi.org/10.1359/ jbmr.2001.16.9.1694
20. Klebanoff MA, Levine RJ, Clemens JD, DerSimonian R, Wilkins DG. Serum cotinine concentration and self-reported smoking during pregnancy. Am J Epidemiol 1998; 148:259-62; PMID:9690362; ht tp: //dx. doi.org/10.1093/oxfordjournals.aje. a009633
21. Jarvis MJ, Russell MA, Benowitz NL, Feyerabend C. Elimination of cotinine from body fluids: implications for noninvasive measurement of tobacco smoke exposure. Am J Public Health 1988; 78:696-8; PMID:3369603; http://dx.doi.org/10.2105/ AJPH.78.6.696
22. Takiguchi M, Achanzar WE, Qu W, Li GY, Waalkes MP. Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp Cell Res 2003; 286:355-65; PMID:12749863; http://dx.doi.org/10.1016/ S0014-4827(03)00062-4
23. Wilson AG. Epigenetic regulation of gene expression in the inflammatory response and relevance to common diseases. J Periodontol 2008; 79(Suppl):1514-9; PMID:18673005; http://dx.doi. org/10.1902/jop.2008.080172
24. Martinez-Zamudio R, Ha HC. Environmental epigenetics in metal exposure. Epigenetics 2011; 6:820-7; PMID:21610324; http://dx.doi. org/10.4161/epi.6.7.16250
25. Benbrahim-Tallaa L, Waterland RA, Dill AL, Webber MM, Waalkes MP. Tumor suppressor gene inactivation during cadmium-induced malignant transformation of human prostate cells correlates with overexpression of de novo DNA methyltransferase. Environ Health Perspect 2007; 115:1454-9; PMID:17938735
26. Huang DJ, Zhang YM, Qi YM, Chen C, Ji WH. Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol Lett 2008; 179:43-7; PMID:18482805; http:// dx.doi.org/10.1016/j.toxlet.2008.03.018
27. Benbrahim-Tallaa L, Tokar EJ, Diwan BA, Dill AL, Coppin JF, Waalkes MP. Cadmium malignantly transforms normal human breast epithelial cells into a basal-like phenotype. Environ Health Perspect 2009; 117:1847-52; PMID:20049202; http://dx.doi. org/10.1289/ehp.0900999
28. Doi T, Puri P, McCann A, Bannigan J, Thompson J. Epigenetic effect of cadmium on global de novo DNA hypomethylation in the cadmium-induced ventral body wall defect (VBWD) in the chick model. Toxicol Sci 2011; 120:475-80; PMID:21278052; http://dx.doi.org/10.1093/toxsci/kfr022
29. Jiang GF, Xu L, Song SZ, Zhu CC, Wu Q, Zhang L, Wu L. Effects of long-term low-dose cadmium exposure on genomic DNA methylation in human embryo lung fibroblast cells. Toxicology 2008; 244:49-55; PMID:18077075; http://dx.doi. org/10.1016/j.tox.2007.10.028
30. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 2009; 180:462-7; PMID:19498054; http://dx.doi.org/10.1164/ rccm.200901-0135OC
31. Suter M, Ma J, Harris AS, Patterson L, Brown KA, Shope C, Showalter L, Abramovici A, Aagaard-Tillery KM. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics 2011; 6:1284-94; PMID:21937876; http://dx.doi.org/10.4161/ epi.6.11.17819
32. Joubert BR, Håberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK, Huang Z, Hoyo C, Midttun Ø, Cupul-Uicab LA, et al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect 2012; 120:1425-31; PMID:22851337
33. Smeester L, Rager JE, Bailey KA, Guan XJ, Smith N, García-Vargas G, Del Razo LM, Drobná Z, Kelkar H, Stýblo M, et al. Epigenetic changes in individuals with arsenicosis. Chem Res Toxicol 2011; 24:165-7; PMID:21291286; http://dx.doi.org/10.1021/ tx1004419
34. Bailey KA, Wu MC, Ward WO, Smeester L, Rager JE, García-Vargas G, Del Razo LM, Drobná Z, Stýblo M, Fry RC. Arsenic and the epigenome: interindividual differences in arsenic metabolism related to distinct patterns of DNA methylation. J Biochem Mol Toxicol 2013; 27:106-15; PMID:23315758; http://dx.doi. org/10.1002/jbt.21462
35. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012; 13:86; PMID:22568884; http://dx.doi.org/10.1186/1471-2105-13-86
36. Bollati V, Baccarelli A. Environmental epigenetics. Heredity (Edinb) 2010; 105:105-12; PMID:20179736; http://dx.doi.org/10.1038/ hdy.2010.2
37. Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003; 192:95-117; PMID:14580780; http://dx.doi.org/10.1016/ S0300-483X(03)00305-6
38. Lih CJ, Wei W, Cohen SN. Txr1: a transcriptional regulator of thrombospondin-1 that modulates cellular sensitivity to taxanes. Genes Dev 2006; 20:2082-95; PMID:16847352; http://dx.doi. org/10.1101/gad.1441306
39. Benton MA, Rager JE, Smeester L, Fry RC. Comparative genomic analyses identify common molecular pathways modulated upon exposure to low doses of arsenic and cadmium. BMC Genomics 2011; 12:173; PMID:21457566; http://dx.doi. org/10.1186/1471-2164-12-173
40. Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 2000; 59:95-104; PMID:10605938; http://dx.doi.org/10.1016/S0006-2952(99)00301-9
41. Shin HJ, Park KK, Lee BH, Moon CK, Lee MO. Identification of genes that are induced after cadmium exposure by suppression subtractive hybridization. Toxicology 2003; 191:121-31; PMID:12965115; http://dx.doi.org/10.1016/S0300-483X(03)00210-5
42. Robinson JF, Yu XZ, Moreira EG, Hong SW, Faustman EM. Arsenic-and cadmium-induced toxicogenomic response in mouse embryos undergoing neurulation. Toxicol Appl Pharmacol 2011; 250:117-29; PMID:20883709; http://dx.doi. org/10.1016/j.taap.2010.09.018
43. Robinson JF, Yu X, Hong S, Griffith WC, Beyer R, Kim E, Faustman EM. Cadmium-induced differential toxicogenomic response in resistant and sensitive mouse strains undergoing neurulation. Toxicol Sci 2009; 107:206-19; PMID:18974090; http://dx.doi.org/10.1093/toxsci/kfn221
44. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, Nemes A, Temper V, Razin A, Cedar H. Sp1 elements protect a CpG island from de novo methylation. Nature 1994; 371:435-8; PMID:8090226; http://dx.doi. org/10.1038/371435a0
45. Macleod D, Charlton J, Mullins J, Bird AP. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev 1994; 8:2282-92; PMID:7958895; http://dx.doi. org/10.1101/gad.8.19.2282
46. Lienert F, Wirbelauer C, Som I, Dean A, Mohn F, Schübeler D. Identification of genetic elements that autonomously determine DNA methylation states. Nat Genet 2011; 43:1091-7; PMID:21964573; http://dx.doi.org/10.1038/ng.946
47. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Schöler A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D, et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 2011; 480:490-5; PMID:22170606
48. Selvaraj A, Balamurugan K, Yepiskoposyan H, Zhou H, Egli D, Georgiev O, Thiele DJ, Schaffner W. Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev 2005; 19:891-6; PMID:15833915; http://dx.doi. org/10.1101/gad.1301805
49. Andrews GK. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 2001; 14:223-37; PMID:11831458; http://dx.doi. org/10.1023/A:1012932712483
50. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 2008; 22:746-55; PMID:18347094; http:// dx.doi.org/10.1101/gad.1642408
51. Merrill BJ, Gat U, DasGupta R, Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev 2001; 15:1688-705; PMID:11445543; http://dx.doi.org/10.1101/ gad.891401
52. Winger Q, Huang J, Auman HJ, Lewandoski M, Williams T. Analysis of transcription factor AP-2 expression and function during mouse preimplantation development. Biol Reprod 2006; 75:324-33; PMID:16672719; http://dx.doi. org/10.1095/biolreprod.106.052407
53. Nelson TJ, Balza R Jr., Xiao Q, Misra RP. SRFdependent gene expression in isolated cardiomyocytes: regulation of genes involved in cardiac hypertrophy. J Mol Cell Cardiol 2005; 39:479-89; PMID:15950986; http://dx.doi.org/10.1016/j.yjmcc.2005.05.004
54. Anglim PP, Alonzo TA, Laird-Offringa IA. DNA methylation-based biomarkers for early detection of non-small cell lung cancer: an update. Mol Cancer 2008; 7:81; PMID:18947422; http://dx.doi. org/10.1186/1476-4598-7-81
55. Sinnaeve PR, Donahue MP, Grass P, Seo D, Vonderscher J, Chibout SD, Kraus WE, Sketch M Jr., Nelson C, Ginsburg GS, et al. Gene expression patterns in peripheral blood correlate with the extent of coronary artery disease. PLoS One 2009; 4:e7037; PMID:19750006; http://dx.doi.org/10.1371/ journal.pone.0007037
56. Deaton AM, Webb S, Kerr AR, Illingworth RS, Guy J, Andrews R, Bird A. Cell type-specific DNA methylation at intragenic CpG islands in the immune system. Genome Res 2011; 21:1074-86; PMID:21628449; http://dx.doi.org/10.1101/ gr.118703.110
57. Pilsner JR, Hu H, Ettinger A, Sánchez BN, Wright RO, Cantonwine D, Lazarus A, Lamadrid-Figueroa H, Mercado-García A, Téllez-Rojo MM, et al. Influence of prenatal lead exposure on genomic methylation of cord blood DNA. Environ Health Perspect 2009; 117:1466-71; PMID:19750115
58. Perera F, Tang WY, Herbstman J, Tang DL, Levin L, Miller R, Ho SM. 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:e4488; PMID:19221603; http://dx.doi.org/10.1371/journal. pone.0004488
59. Miranda ML, Edwards S, Maxson PJ. Mercury levels in an urban pregnant population in Durham County, North Carolina. Int J Environ Res Public Health 2011; 8:698-712; PMID:21556174; http://dx.doi. org/10.3390/ijerph8030698
60. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 2003; 31:e15; PMID:12582260; http://dx.doi.org/10.1093/nar/ gng015
61. Davies MN, Volta M, Pidsley R, Lunnon K, Dixit A, Lovestone S, Coarfa C, Harris RA, Milosavljevic A, Troakes C, et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol 2012; 13:R43; PMID:22703893; http://dx.doi. org/10.1186/gb-2012-13-6-r43
62. Psychiatric Epigenetics Data KCL. http:// epigenetics.iop.kcl.ac.uk/brain%5D.
63. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, Johnson BE, Hong C, Nielsen C, Zhao Y, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010; 466:253-7; PMID:20613842; http:// dx.doi.org/10.1038/nature09165
64. Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ. The UCSC Table Browser data retrieval tool. Nucleic Acids Res 2004; 32(Database issue):D493-6; PMID:14681465; http://dx.doi.org/10.1093/nar/gkh103
65. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009; 37(Web Server issue):W202-8; PMID:19458158; http://dx.doi. org/10.1093/nar/gkp335