The impact of first trimester phthalate and phenol exposure on IGF2/H19 genomic imprinting and birth outcomes

Environmental Research

Volumn 133, Issue , 2014, Pages 396-406

  LaRocca, Jessica ^a,c   Binder, Alexandra M ^b,c   McElrath, Thomas F ^c   Michels, Karin B ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Allele specific expression; Endocrine disruptors; Epidemiology; Imprinting; Methylation

Indexed keywords

ENDOCRINE DISRUPTOR; PHENOL; PHTHALIC ACID; RNA H19; SOMATOMEDIN B;

ALLELE; BIRTH RATE; ENDOCRINE DISRUPTOR; EPIDEMIOLOGY; GENE EXPRESSION; GENOMICS; METHYLATION; PHENOL; PHTHALATE; POLLUTION EXPOSURE;

ADULT; ALLELE; ARTICLE; BIRTH WEIGHT; CONTROLLED STUDY; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; FEMALE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; GENETIC VARIABILITY; GENOME IMPRINTING; HUMAN; INFANT; KIDNEY CONCENTRATING CAPACITY; MAJOR CLINICAL STUDY; MALE; MOLECULAR WEIGHT; PREGNANCY OUTCOME; PRENATAL CARE; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PYROSEQUENCING;

ALLELE-SPECIFIC EXPRESSION; ENDOCRINE DISRUPTORS; EPIDEMIOLOGY; IMPRINTING; METHYLATION;

ADULT; ALLELES; BIOLOGICAL MARKERS; COHORT STUDIES; DNA METHYLATION; ENDOCRINE DISRUPTORS; FEMALE; GENOMIC IMPRINTING; HUMANS; INFANT, NEWBORN; INSULIN-LIKE GROWTH FACTOR II; MALE; PHENOLS; PHTHALIC ACIDS; PLACENTA; PREGNANCY; PREGNANCY OUTCOME; PREGNANCY TRIMESTER, FIRST; RNA, LONG NONCODING;

EID: 84904982358     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2014.04.032     Document Type: Article

References (58)

1. Adibi J.J., Whyatt R.M., Williams P.L., Calafat A.M., Camann D., Herrick R., et al. Characterization of phthalate exposure among pregnant women assessed by repeat air and urine samples. Environ. Health Perspect. 2008, 116(4):467-473.
2. Anway M.D., Cupp A.S., Uzumcu M., Skinner M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308(5727):1466-1469.
3. Birnbaum L.S. State of the science of endocrine disruptors. Environ. Health Perspect. 2013, 121(4):A107.
4. Barker D.J. Maternal nutrition, fetal nutrition, and disease in later life. Nutrition 1997, 13(9):807-813.
5. Boeniger M.F., Lowry L.K., Rosenberg J. Interpretation of urine results used to assess chemical exposure with emphasis on creatinine adjustments: a review. Am. Ind. Hyg. Assoc. J. 1993, 54(10):615-627.
6. Becker K., Seiwert M., Angerer J., Heger W., Koch H.M., Nagorka R., et al. DEHP metabolites in urine of children and DEHP in house dust. Int. J. Hyg. Environ. Health 2004, 207(5):409-417.
7. Braun J.M., Smith K.W., Williams P.L., Calafat A.M., Berry K., Ehrlich S., et al. Variability of urinary phthalate metabolite and bisphenol A concentrations before and during pregnancy. Environ. Health Perspect. 2012, 120(5):739-745.
8. Braun J.M., Kalkbrenner A.E., Calafat A.M., Bernert J.T., Ye X., Silva M.J., et al. Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ. Health Perspect. 2011, 119(1):131-137.
9. Calafat A.M., Ye X., Wong L.Y., Reidy J.A., Needham L.L. Urinary concentrations of triclosan in the U.S. population: 2003-2004. Environ. Health Perspect. 2008, 116(3):303-307.
10. Calafat A.M., Wong L.Y., Ye X., Reidy J.A., Needham L.L. Concentrations of the sunscreen agent benzophenone-3 in residents of the United States: National Health and Nutrition Examination Survey 2003-2004. Environ. Health Perspect. 2008, 116(7):893-897.
11. CDC. Fourth national report on human exposure to environmental chemicals, updated tables. Available at: (accessed 01.02.12). http://www.cdc.gov/exposurereport/pdf/.
12. Constancia M., Hemberger M., Hughes J., Dean W., Ferguson-Smith A., Fundele R., et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002, 417(6892):945-948.
13. Chao H.H., Zhang X.F., Chen B., Pan B., Zhang L.J., Li L., et al. Bisphenol A exposure modifies methylation of imprinted genes in mouse oocytes via the estrogen receptor signaling pathway. Histochem. Cell Biol. 2012, 137(2):249-259.
14. DeChiara T.M., Efstratiadis A., Robertson E.J. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 1990, 345(6270):78-80.
15. Eubig P.A., Aguiar A., Schantz S.L. Lead and PCBs as risk factors for attention deficit/hyperactivity disorder. Environ. Health Perspect. 2010, 118(12):1654-1667.
16. Frederiksen H., Jorgensen N., Andersson A.M. Correlations between phthalate metabolites in urine, serum, and seminal plasma from young Danish men determined by isotope dilution liquid chromatography-tandem mass spectrometry. J. Anal. Toxicol. 2010, 34(7):400-410.
17. Gabory A., Ripoche M.A., Yoshimizu T., Dandolo L. The H19 gene: regulation and function of a non-coding RNA. Cytogenet. Genome Res. 2006, 113(1-4):188-193.
18. Gabory A., Jammes H., Dandolo L. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 2010, 32(6):473-480.
19. Hauser R., Calafat A.M. Phthalates and human health. Occup. Environ. Med. 2005, 62(11):806-818.
20. Haycock P.C., Ramsay M. Exposure of mouse embryos to ethanol during preimplantation development: effect on DNA methylation in the H19 imprinting control region. Biol. Reprod. 2009, 81(4):618-627.
21. Hornung R.W., Reed L.D. Estimation of average concentrations in the presence of nondetectable values. Appl. Occup. Environ. Hyg. 1990, 5:46-51.
22. Irvin E.A., Calafat A.M., Silva M.J., Aguilar-Villalobos M., Needham L.L., Hall D.B., et al. An estimate of phthalate exposure among pregnant women living in Trujillo, Peru. Chemosphere 2010, 80(11):1301-1307.
23. Jansson T., Powell T.L. Role of the placenta in fetal programming: underlying mechanisms and potential interventional approaches. Clin. Sci. (Lond) 2007, 113(1):1-13.
24. Koch H.M., Calafat A.M. Human body burdens of chemicals used in plastic manufacture. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364(1526):2063-2078.
25. Koch H.M., Preuss R., Angerer J. Di(2-ethylhexyl)phthalate (DEHP): human metabolism and internal exposure-- an update and latest results. Int. J. Androl. 2006, 29(1):155-165. (discussion 181-155).
26. Kundakovic M., Gudsnuk K., Franks B., Madrid J., Miller R.L., Perera F.P., et al. Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proc. Natl. Acad. Sci. USA 2013, 110(24):9956-9961.
27. Kim J.H., Rozek L.S., Soliman A.S., Sartor M.A., Hablas A., Seifeldin I.A., et al. Bisphenol A-associated epigenomic changes in prepubescent girls: a cross-sectional study in Gharbiah, Egypt. Environ. Health: A Glob. Access Sci. Source 2013, 12:33.
28. Lovekamp-Swan T., Davis B.J. Mechanisms of phthalate ester toxicity in the female reproductive system. Environ. Health Perspect. 2003, 111(2):139-145.
29. Markham J.A., Koenig J.I. Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology (Berl.) 2011, 214(1):89-106.
30. Michels K.B., Harris H.R., Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS One 2011, 6:9.
31. McElrath T.F., Lim K.H., Pare E., Rich-Edwards J., Pucci D., Troisi R., et al. Longitudinal evaluation of predictive value for preeclampsia of circulating angiogenic factors through pregnancy. Am. J. Obstet. Gynecol. 2012, 207(5):407e401-407e407.
32. Meeker J.D., Sathyanarayana S., Swan S.H. Phthalates and other additives in plastics: human exposure and associated health outcomes. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2009, 364(1526):2097-2113.
33. Meeker J.D., Hu H., Cantonwine D.E., Lamadrid-Figueroa H., Calafat A.M., Ettinger A.S., et al. Urinary phthalate metabolites in relation to preterm birth in Mexico city. Environ. Health Perspect. 2009, 117(10):1587-1592.
34. Meeker J.D., Calafat A.M., Hauser R. Urinary phthalate metabolites and their biotransformation products: predictors and temporal variability among men and women. J. Expo. Sci. Environ. Epidemiol. 2012, 22(4):376-385.
35. Meeker J.D., Cantonwine D.E., Rivera-Gonzalez L.O., Ferguson K.K., Mukherjee B., Calafat A.M., et al. Distribution, variability, and predictors of urinary concentrations of phenols and parabens among pregnant women in Puerto Rico. Environ. Sci. Technol. 2013, 47(7):3439-3447.
36. Nomura Y., Lambertini L., Rialdi A., Lee M., Mystal E.Y., Grabie M., et al. Global methylation in the placenta and umbilical cord blood from pregnancies with maternal gestational diabetes, preeclampsia, and obesity. Reprod. Sci 2014, 21(1):131-137.
37. Peck J.D., Sweeney A.M., Symanski E., Gardiner J., Silva M.J., Calafat A.M., et al. Intra- and inter-individual variability of urinary phthalate metabolite concentrations in Hmong women of reproductive age. J. Expo. Sci. Environ. Epidemiol. 2010, 20(1):90-100.
38. Philippat C., Wolff M.S., Calafat A.M., Ye X., Bausell R., Meadows M., et al. Prenatal exposure to environmental phenols: concentrations in amniotic fluid and variability in urinary concentrations during pregnancy. Environ. Health Perspect 2013.
39. Roseboom T.J., Painter R.C., van Abeelen A.F., Veenendaal M.V., de Rooij S.R. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 2011, 70(2):141-145.
40. Reik W., Walter J. Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2001, 2(1):21-32.
41. Rancourt R.C., Harris H.R., Michels K.B. Methylation levels at imprinting control regions are not altered with ovulation induction or in vitro fertilization in a birth cohort. Hum. Reprod. 2012, 27(7):2208-2216.
42. Rancourt R.C., Harris H.R., Barault L., Michels K.B. The prevalence of loss of imprinting of H19 and IGF2 at birth. FASEB J 2013, 27(8):3335-3343.
43. Rastogi S.C., Schouten A., de Kruijf N., Weijland J.W. Contents of methyl-, ethyl-, propyl-, butyl- and benzylparaben in cosmetic products. Contact Dermati. 1995, 32(1):28-30.
44. 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.
45. Silva M.J., Preau J.L., Needham L.L., Calafat A.M. Cross validation and ruggedness testing of analytical methods used for the quantification of urinary phthalate metabolites. J. Chromatogr. B. Anal. Technol. Biomed. Life Sci. 2008, 873(2):180-186.
46. Schulz L.C. The Dutch Hunger Winter and the developmental origins of health and disease. Proc. Natl. Acad. Sci. USA 2010, 107(39):16757-16758.
47. Susiarjo M., Sasson I., Mesaros C., Bartolomei M.S. Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet. 2013, 9(4):e1003401.
48. Shin H.S., Seo J.H., Jeong S.H., Park S.W., Park Y., Son S.W., et al. Exposure of pregnant mice to chlorpyrifos-methyl alters embryonic H19 gene methylation patterns. Environ. Toxicol 2012.
49. Smith K.W., Braun J.M., Williams P.L., Ehrlich S., Correia K.F., Calafat A.M., et al. Predictors and variability of urinary paraben concentrations in men and women, including before and during pregnancy. Environ. Health Perspect. 2012, 120(11):1538-1543.
50. Teass A.B.R., DeBord D. Application of biological monitoring methods. NIOSH Manual of Analytical Method 1998, National Institute for Occupational Safety and Health Division of Physical Sciences and Engineering, Cincinnati. P. Eller (Ed.).
51. Tefre de Renzy-Martin K., Frederiksen H., Christensen J., Boye Kyhl H., Andersson A.M., Husby S., et al. Current exposure of 200 pregnant Danish women to phthalates, parabens and phenols. Reproduction 2013.
52. Waterland R.A., Dolinoy D.C., Lin J.R., Smith C.A., Shi X., Tahiliani K.G. Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis 2006, 44(9):401-406.
53. Williams J. Williams Obstetrics 2005, McGraw-Hill, New York.
54. 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.
55. Weaver J.R., Sarkisian G., Krapp C., Mager J., Mann M.R., Bartolomei M.S. Domain-specific response of imprinted genes to reduced DNMT1. Mol. Cell. Biol. 2010, 30(16):3916-3928.
56. Ye X., Kuklenyik Z., Needham L.L., Calafat A.M. Automated on-line column-switching HPLC-MS/MS method with peak focusing for the determination of nine environmental phenols in urine. Anal. Chem. 2005, 77(16):5407-5413.
57. Ye X., Bishop A.M., Reidy J.A., Needham L.L., Calafat A.M. Parabens as urinary biomarkers of exposure in humans. Environ. Health Perspect. 2006, 114(12):1843-1846.
58. Yang B., Wagner J., Damaschke N., Yao T., Wuerzberger-Davis S.M., Lee M.H., et al. A novel pathway links oxidative stress to loss of insulin growth factor-2 (IGF2) imprinting through NF-kappaB activation. PloS One 2014, 9(2):e88052.