Quality control and statistical modeling for environmental epigenetics: A study on in Utero lead exposure and DNA methylation at birth

Epigenetics

Volumn 10, Issue 1, 2015, Pages 19-30

  Goodrich, Jaclyn M ^a   Sánchez, Brisa N ^a   Dolinoy, Dana C ^a   Zhang, Zhenzhen ^a   Hernández Ávila, Mauricio ^b   Hu, Howard ^c   Peterson, Karen E ^a,d,e   Téllez Rojo, Martha M ^b  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF MICHIGAN   (United States)

^e HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

DNA methylation; Environmental exposure; Lead; Pyrosequencing; Quality control; Statistical methods

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; BIOLOGICAL MARKER; CPG OLIGODEOXYNUCLEOTIDE; SOMATOMEDIN B; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; HSD11B2 PROTEIN, HUMAN; IGF2 PROTEIN, HUMAN;

ANTHROPOMETRY; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; CONTROLLED STUDY; DNA EXTRACTION; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE; FOOD FREQUENCY QUESTIONNAIRE; GENE; GENETIC ANALYSIS; GESTATIONAL AGE; H19 GENE; HUMAN; INTERVIEW; LINE 1 GENE; MALE; MEASUREMENT ACCURACY; MEASUREMENT PRECISION; PATELLA; PERFORMANCE; PYROSEQUENCING; QUALITY CONTROL; REGRESSION ANALYSIS; RELIABILITY; SENSITIVITY ANALYSIS; SEX; SIMULATION; STATISTICAL MODEL; TIBIA; UMBILICAL CORD BLOOD; ADULT; BIOLOGICAL MODEL; GENETIC EPIGENESIS; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; LEAD POISONING; LONG INTERSPERSED REPEAT; MATERNAL EXPOSURE; NEWBORN; PREGNANCY; PRENATAL EXPOSURE;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ADULT; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENE-ENVIRONMENT INTERACTION; HUMANS; INFANT, NEWBORN; INSULIN-LIKE GROWTH FACTOR II; LEAD POISONING; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MATERNAL EXPOSURE; MODELS, GENETIC; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84924364200     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/15592294.2014.989077     Document Type: Article

References (67)

1. Weinhouse C, Anderson OS, Jones TR, Kim J, Liberman SA, Nahar MS, Rozek LS, Jirtle RL, Dolinoy DC. An expression microarray approach for the identification of metastable epialleles in the mouse genome. Epigenetics 2011; 6:1105-13; PMID:21829099; http://dx.doi.org/10.4161/epi.6.9.17103
2. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci U S A 2007; 104:13056-61; PMID:17670942; http://dx.doi.org/10.1073/pnas.0703739104
3. Dolinoy DC, Weidman JR, Waterland RA, Jirtle RL. Maternal genistein alters coat color and protects avy mouse offspring from obesity by modifying the fetal epigenome. Environ Health Perspect 2006; 114:567-72; PMID:16581547; http://dx.doi.org/10.1289/ehp.8700
4. Anderson OS, Nahar MS, Faulk C, Jones TR, Liao C, Kannan K, Weinhouse C, Rozek LS, Dolinoy DC. Epigenetic responses following maternal dietary exposure to physiologically relevant levels of bisphenol A. Environ Mol Mutagen 2012; 53:334-42; PMID:22467340; http://dx.doi.org/10.1002/em.21692
5. Huen K, Yousefi P, Bradman A, Yan L, Harley KG, Kogut K, Eskenazi B, Holland N. Effects of age, sex, and persistent organic pollutants on DNA methylation in children. Environ Mol Mutagen 2014; 55:209-22; PMID:24375655; http://dx.doi.org/10.1002/em.21845
6. Joubert BR, Haberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK, Huang Z, Hoyo C, Midttun O, 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; http://dx.doi.org/10.1289/ehp.1205412
7. Kippler M, Engstrom K, Mlakar SJ, Bottai M, Ahmed S, Hossain MB, Raqib R, Vahter M, Broberg K. Sexspecific effects of early life cadmium exposure on DNA methylation and implications for birth weight. Epigenetics 2013; 8:494-503; PMID:23644563; http://dx.doi.org/10.4161/epi.24401
8. Koestler DC, Avissar-Whiting M, Houseman EA, Karagas MR, Marsit CJ. Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic. Environ Health Perspect 2013; 121:971-77; PMID:23757598
9. Murphy SK, Adigun A, Huang Z, Overcash F, Wang F, Jirtle RL, Schildkraut JM, Murtha AP, Iversen ES, Hoyo C. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene 2011; 494:36-43; PMID:22202639; http://dx.doi.org/10.1016/j.gene.2011.11.062
10. Rager JE, Bailey KA, Smeester L, Miller SK, Parker JS, Laine JE, Drobn_a Z, Currier J, Douillet C, Olshan AF, et al. Prenatal arsenic exposure and the epigenome: Altered microRNAs associated with innate and adaptive immune signaling in newborn cord blood. Environ Mol Mutagen 2014; 55:196-208; PMID:24327377; http://dx.doi.org/10.1002/em.21842
11. Faulk C, Barks A, Liu K, Goodrich JM, Dolinoy DC. Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice. Epigenomics 2013; 5:487-500; PMID:24059796; http://dx.doi.org/10.2217/epi.13.49
12. Dosunmu R, Alashwal H, Zawia NH. Genome-wide expression and methylation profiling in the aged rodent brain due to early-life pb exposure and its relevance to aging. Mech Ageing Dev 2012; 133:435-443; PMID:22613225; http://dx.doi.org/10.1016/j.mad.2012.05.003
13. Hanna CW, Bloom MS, Robinson WP, Kim D, Parsons PJ, Vom Saal FS, Taylor JA, Steuerwald AJ, Fujimoto VY. DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF. Hum Reprod 2012; 27:1401-10; PMID:22381621; http://dx.doi.org/10.1093/humrep/des038
14. Kovatsi L, Georgiou E, Ioannou A, Haitoglou C, Tzimagiorgis G, Tsoukali H, Kouidou S. p16 promoter methylation in Pb2C-exposed individuals. Clin Toxicol (Phila) 2010; 48:124-8; PMID:20199129
15. Pilsner JR, Hu H, Ettinger A, Sanchez BN, Wright RO, Cantonwine D, Lazarus A, Lamadrid-Figueroa H, Mercado-Garcia A, Tellez-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; http://dx.doi.org/10.1289/ehp.0800497
16. Li C, Yang X, Xu M, Zhang J, Sun N. Epigenetic marker (LINE-1 promoter) methylation level was associated with occupational lead exposure. Clin Toxicol (Phila) 2013; 51:225-29; PMID:13528182; http://dx.doi.org/10.3109/15563650.2013.782410
17. Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L, Park SK, Hu H, Sparrow D, Vokonas P, Baccarelli A. Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ Health Perspect 2010; 118:790-5; PMID:20064768; http://dx.doi.org/10.1289/ehp.0901429
18. Bogdanovic O, Veenstra GJ. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 2009; 118:549-65; PMID:19506892; http://dx.doi.org/10.1007/s00412-009-0221-9
19. Razin A, Cedar H. DNA methylation and gene expression. Microbiol Rev 1991; 55:451-8; PMID:1943996
20. Umer M, Herceg Z. Deciphering the epigenetic code: an overview of DNA methylation analysis methods. Antioxid Redox Signal 2013; 18:1972-86; PMID:23121567; http://dx.doi.org/10.1089/ars.2012.4923
21. Tost J, Gut IG. DNA methylation analysis by pyrosequencing. Nature Protocols 2007; 2:2265-75; PMID:17853883; http://dx.doi.org/10.1038/nprot.2007.314
22. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, Cantor CR, Field JK, van den Boom D. Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci U S A 2005; 102:15785-90; PMID:16243968; http://dx.doi.org/10.1073/pnas.0507816102
23. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci U S A 1996; 93:9821-6; PMID:8790415; http://dx.doi.org/10.1073/pnas.93.18.9821
24. Marabita F, Almgren M, Lindholm ME, Ruhrmann S, Fagerstrom-Billai F, Jagodic M, Sundberg CJ, Ekstrom TJ, Teschendorff AE, Tegner J, et al. An evaluation of analysis pipelines for DNA methylation profiling using the illumina HumanMethylation450 BeadChip platform. Epigenetics 2013; 8:333-46; PMID:23422812; http://dx.doi.org/10.4161/epi.24008
25. Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, Beck S. A beta-mixture quantile normalization method for correcting probe design bias in illumina infinium 450 k DNA methylation data. Bioinformatics 2013; 29:189-96; PMID:23175756; http://dx.doi.org/10.1093/bioinformatics/bts680
26. Morris TJ, Butcher LM, Feber A, Teschendorff AE, Chakravarthy AR, Wojdacz TK, Beck S. ChAMP: 450k chip analysis methylation pipeline. Bioinformatics 2014; 30:428-30; PMID:24336642; http://dx.doi.org/10.1093/bioinformatics/btt684
27. Pidsley R, Y Wong CC, Volta M, Lunnon K, Mill J, Schalkwyk LC. A data-driven approach to preprocessing illumina 450K methylation array data. BMC Genomics 2013; 14:293; PMID:23631413; http://dx.doi.org/10.1186/1471-2164-14-293
28. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 2009; 55:611-22; PMID:19246619; http://dx.doi.org/10.1373/clinchem.2008.112797
29. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 2007; 8:R19; PMID:17291332
30. DeRoo LA, Bolick SCE, Xu Z, Umbach DM, Shore D, Weinberg CR, Sandler DP, Taylor JA. Global DNA methylation and one-carbon metabolism gene polymorphisms and the risk of breast cancer in the sister study. Carcinogenesis 2014; 35:333-8; PMID:24130171; http://dx.doi.org/10.1093/carcin/bgt342
31. Hu H, Aro A, Rotnitzky A. Bone lead measured by Xray fluorescence: epidemiologic methods. Environ Health Perspect 1995; 103 Suppl 1:105-10; PMID:7621788; http://dx.doi.org/10.1289/ehp.95103s1105
32. Lamadrid-Figueroa H, Tellez-Rojo MM, Angeles G, Hernandez-Avila M, Hu H. Bias correction by use of errors-in-variables regression models in studies with KX-ray fluorescence bone lead measurements. Environ Res 2011; 111:17-20; PMID:21092947; http://dx.doi.org/10.1016/j.envres.2010.10.011
33. Fitzmaurice GM, Laird NM, Ware JH. Applied Longitudinal Analysis. 2nd ed. Hoboken, New Jersey: John Wiley & Sons, Inc 2011.
34. Hernandez-Avila M, Smith D, Meneses F, Sanin LH, Hu H. The influence of bone and blood lead on plasma lead levels in environmentally exposed adults. Environ Health Perspect 1998; 106:473-77; PMID:9681974; http://dx.doi.org/10.1289/ehp.98106473
35. Hernandez-Avila M, Peterson KE, Gonzalez-Cossio T, Sanin LH, Aro A, Schnaas L, Hu H. Effect of maternal bone lead on length and head circumference of newborns and 1-month-old infants. Arch Environ Health 2002; 57:482-88; PMID:12641193; http://dx.doi.org/10.1080/00039890209601441
36. Gonzalez-Cossio T, Peterson KE, Sanin LH, Fishbein E, Palazuelos E, Aro A, Hernandez-Avila M, Hu H. Decrease in birth weight in relation to maternal bone-lead burden. Pediatrics 1997; 100:856-62; PMID:9346987; http://dx.doi.org/10.1542/peds.100.5.856
37. Xie X, Ding G, Cui C, Chen L, Gao Y, Zhou Y, Shi R, Tian Y. The effects of low-level prenatal lead exposure on birth outcomes. Environ Pollut 2013; 175:30-4; PMID:23321271; http://dx.doi.org/10.1016/j.envpol.2012.12.013
38. Sanin LH, Gonzalez-Cossio T, Romieu I, Peterson KE, Ruiz S, Palazuelos E, Hernandez-Avila M, Hu H. Effect of maternal lead burden on infant weight and weight gain at one month of age among breastfed infants. Pediatrics 2001; 107:1016-23; PMID:11331680; http://dx.doi.org/10.1542/peds.107.5.1016
39. Afeiche M, Peterson KE, Sanchez BN, Cantonwine D, Lamadrid-Figueroa H, Schnaas L, Ettinger AS, Hernandez- Avila M, Hu H, Tellez-Rojo MM. Prenatal lead exposure and weight of 0- to 5-year-old children in mexico city. Environ Health Perspect 2011; 119:1436-41; PMID:21715242; http://dx.doi.org/10.1289/ehp.1003184
40. Wong HL, Byun HM, Kwan JM, Campan M, Ingles SA, Laird PW, Yang AS. Rapid and quantitative method of allele-specific DNA methylation analysis. BioTechniques 2006; 41:734-9; PMID:17191619; http://dx.doi.org/10.2144/000112305
41. Hughes S, Jones JL. The use of multiple displacement amplified DNA as a control for methylation specific PCR, pyrosequencing, bisulfite sequencing and methylation-sensitive restriction enzyme PCR. BMC Mol Biol 2007; 8:91; PMID:17939862; http://dx.doi.org/10.1186/1471-2199-8-91
42. Warnecke PM, Stirzaker C, Melki JR, Millar DS, Paul CL, Clark SJ. Detection and measurement of PCR bias in quantitative methylation analysis of bisulphitetreated DNA. Nucleic Acids Res 1997; 25:4422-6; PMID:9336479; http://dx.doi.org/10.1093/nar/25.21.4422
43. Turker MS. The establishment and maintenance of DNA methylation patterns in mouse somatic cells. Semin Cancer Biol 1999; 9:329-37; PMID:10547341
44. Weaver IC, Diorio J, Seckl JR, Szyf M, Meaney MJ. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: Characterization of intracellular mediators and potential genomic target sites. Ann N Y Acad Sci 2004; 1024:182-212; PMID:15265782; http://dx.doi.org/10.1196/annals.1321.099
45. Byun HM, Motta V, Panni T, Bertazzi PA, Apostoli P, Hou L, Baccarelli AA. Evolutionary age of repetitive element subfamilies and sensitivity of DNA methylation to airborne pollutants. Part Fibre Toxicol 2013; 10:28; PMID:23855992; http://dx.doi.org/10.1186/1743-8977-10-28
46. Virani S, Dolinoy DC, Halubai S, Jones TR, Domino SE, Rozek LS, Nahar MS, Padmanabhan V. Delivery type not associated with global methylation at birth. Clin Epigenetics 2012; 4:8; PMID:22682523; http://dx.doi.org/10.1186/1868-7083-4-8
47. Tarantini L, Bonzini M, Apostoli P, Pegoraro V, Bollati V, Marinelli B, Cantone L, Rizzo G, Hou L, Schwartz J, et al. Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environ Health Perspect 2009; 117:217-22; PMID:19270791; http://dx.doi.org/10.1289/ehp.11898
48. Vilahur N, Bustamante M, Byun HM, Fernandez MF, Santa Marina L, Basterrechea M, Ballester F, Murcia M, Tardon A, Fernandez-Somoano A, et al. Prenatal exposure to mixtures of xenoestrogens and repetitive element DNA methylation changes in human placenta. Environ Int 2014; 71:81-7; PMID:24980756; http://dx.doi.org/10.1016/j.envint.2014.06.006
49. Xu H, Wang F, Liu Y, Yu Y, Gelernter J, Zhang H. Sex-biased methylome and transcriptome in human prefrontal cortex. Hum Mol Genet 2014; 23:1260-70; PMID:24163133; http://dx.doi.org/10.1093/hmg/ddt516
50. Zhang FF, Cardarelli R, Carroll J, Fulda KG, Kaur M, Gonzalez K, Vishwanatha JK, Santella RM, Morabia A. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 2011; 6:623-629; PMID:21739720; http://dx.doi.org/10.4161/epi.6.5.15335
51. Goodrich JM, Basu N, Franzblau A, Dolinoy DC. Mercury biomarkers and DNA methylation among michigan dental professionals. Environ Mol Mutagen 2013; 54:195-203; PMID:23444121; http://dx.doi.org/10.1002/em.21763
52. Murphy SK, Adigun A, Huang Z, Overcash F, Wang F, Jirtle RL, Schildkraut JM, Murtha AP, Iversen ES, Hoyo C. Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene 2012; 494:36-43; PMID:22202639; http://dx.doi.org/10.1016/j.gene.2011.11.062
53. Dolinoy DC, Das R,Weidman JR, Jirtle RL. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr Res 2007; 61:30R-37R; PMID:17413847; http://dx.doi.org/10.1203/pdr.0b013e31804575f7
54. Waterland RA, Kellermayer R, Laritsky E, Rayco-Solon P, Harris RA, Travisano M, Zhang W, Torskaya MS, Zhang J, Shen L, et al. Season of conception in rural gambia affects DNA methylation at putative humanmetastable epialleles. PLoS Genet 2010; 6:e1001252; PMID:21203497; http://dx.doi.org/10.1371/journal.pgen.1001252
55. Harris RA, Nagy-Szakal D, Kellermayer R. Human metastable epiallele candidates link to common disorders. Epigenetics 2013; 8:157-63; PMID:23321599; http://dx.doi.org/10.4161/epi.23438
56. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 2008; 105:17046-9; PMID:18955703; http://dx.doi.org/10.1073/pnas.0806560105
57. Mai A, Altucci L. Epi-drugs to fight cancer: From chemistry to cancer treatment, the road ahead. Int J Biochem Cell Biol 2009; 41:199-213; PMID:18790076; http://dx.doi.org/10.1016/j.biocel.2008.08.020
58. Hernandez-Avila M, Romieu I, Parra S, Hernandez-Avila J, Madrigal H, Willett W. Validity and reproducibility of a food frequency questionnaire to assess dietary intake of women living in mexico city. Salud Publica Mex 1998; 40:133-40; PMID:9617194; http://dx.doi.org/10.1590/S0036-36341998000200005
59. Aro AC, Todd AC, Amarasiriwardena C, Hu H. Improvements in the calibration of 109Cd K x-ray fluorescence systems for measuring bone lead in vivo. Phys Med Biol 1994; 39:2263-71; PMID:15551552; http://dx.doi.org/10.1088/0031-9155/39/12/009
60. Hu H, Milder FL, Burger DE. The use of K X-ray fluorescence for measuring lead burden in epidemiological studies: High and low lead burdens and measurement uncertainty. Environ Health Perspect 1991; 94:107-10; PMID:1954919; http://dx.doi.org/10.2307/3431301
61. Hopkins MR, Ettinger AS, Hernandez-Avila M, Schwartz J, Tellez-Rojo MM, Lamadrid-Figueroa H, Bellinger D, Hu H, Wright RO. Variants in iron metabolism genes predict higher blood lead levels in young children. Environ Health Perspect 2008; 116:1261-6; PMID:18795173; http://dx.doi.org/10.1289/ehp.11233
62. Grunau C, Clark SJ, Rosenthal A. Bisulfite genomic sequencing: Systematic investigation of critical experimental parameters. Nucleic Acids Res 2001; 29:E65-5; PMID:11433041; http://dx.doi.org/10.1093/nar/29.13.e65
63. Seckl JR. Glucocorticoids, feto-placental 11 betahydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids 1997; 62:89-94; PMID:9029721
64. Lui JC, Finkielstain GP, Barnes KM, Baron J. An imprinted gene network that controls mammalian somatic growth is down-regulated during postnatal growth deceleration in multiple organs. Am J Physiol Regul Integr Comp Physiol 2008; 295:R189-96; PMID:18448610; http://dx.doi.org/10.1152/ajpregu.00182.2008
65. Hoyo C, Murtha AP, Schildkraut JM, Jirtle RL, Demark-Wahnefried W, Forman MR, Iversen ES, Kurtzberg J, Overcash F, Huang Z, et al. Methylation variation at IGF2 differentially methylated regions and maternal folic acid use before and during pregnancy. Epigenetics. 2011; 6:928-36; PMID:21636975; http://dx.doi.org/10.4161/epi.6.7.16263
66. Alikhani-Koopaei R, Fouladkou F, Frey F, Frey B. Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. J Clin Invest: 114(8):1146-57; PMID:15489962
67. National Institutes of Health (NIH) Office of Research on Women’s Health. Moving into the future with new dimensions and strategies: a vision for 2020 women’s health research. 2010; Report 10-7606.