Longitudinal analysis of DNA methylation associated with birth weight and gestational age

Human Molecular Genetics

Volumn 24, Issue 13, 2015, Pages 3752-3763

  Simpkin, Andrew J ^a   Suderman, Matthew ^a   Gaunt, Tom R ^a   Lyttleton, Oliver ^a   McArdle, Wendy L ^a   Ring, Susan M ^a   Tilling, Kate ^a   Davey Smith, George ^a   Relton, Caroline L ^a,b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ARTICLE; BIRTH; BIRTH WEIGHT; BLOOD; BONE DENSITY; CHILD; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENTAL GENE; DNA METHYLATION; FEMALE; GENE; GENE LOCUS; GESTATIONAL AGE; HUMAN; LONGITUDINAL STUDY; MALE; NFIX GENE; PHENOTYPE; PRIORITY JOURNAL; UMBILICAL CORD BLOOD; FETUS BLOOD; GENETICS; METABOLISM;

NFIX PROTEIN, HUMAN; NUCLEAR FACTOR I;

ADOLESCENT; BIRTH WEIGHT; CHILD; CPG ISLANDS; DNA METHYLATION; FEMALE; FETAL BLOOD; GESTATIONAL AGE; HUMANS; LONGITUDINAL STUDIES; MALE; NFI TRANSCRIPTION FACTORS;

EID: 84936748049     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv119     Document Type: Article

References (68)

1. Irving, R.J., Belton, N.R., Elton, R.A. and Walker, B.R. (2000) Adult cardiovascular risk factors in premature babies. The Lancet, 355, 2135-2136.
2. Behrman, R.E. and Butler, A.S. (2007) Preterm Birth: Causes, Consequences, and Prevention. National Academies Press, Washington DC, USA.
3. Aarnoudse-Moens, C.S.H., Weisglas-Kuperus, N., van Goudoever, J.B. and Oosterlaan, J. (2009) Meta-analysis of neurobehavioral outcomes in very preterm and/or very low birth weight children. Pediatrics, 124, 717-728.
4. Kwinta, P. and Pietrzyk, J.J. (2010) Preterm birth and respiratory disease in later life. Expert Rev. Respir. Med., 4, 593-604.
5. Schroeder, J.W., Conneely, K.N., Cubells, J.C., Kilaru, V., Newport, D.J., Knight, B.T., Stowe, Z.N., Brennan, P.A., Krushkal, J., Tylavsky, F.A. et al. (2011) NeonatalDNA methylation patterns associate with gestational age. Epigenetics, 6, 1498-1504.
6. Lee, H., Jaffe, A.E., Feinberg, J.I., Tryggvadottir, R., Brown, S., Montano, C., Aryee, M.J., Irizarry, R.A., Herbstman, J., Witter, F.R. et al. (2012) DNA methylation shows genome-wide association of NFIX, RAPGEF2 and MSRB3 with gestational age at birth. Int. J. Epidemiol., 41, 188-199.
7. Parets, S.E., Conneely, K.N., Kilaru, V., Fortunato, S.J., Syed, T. A., Saade, G., Smith, A.K. and Menon, R. (2013) Fetal DNA methylation associates with early spontaneous preterm birth and gestational age. PLoS ONE, 8, e67489.
8. Engel, S.M., Joubert, B.R., Wu, M.C., Olshan, A.F., Håberg, S.E., Ueland, P.M., Nystad, W., Nilsen, R.M., Vollset, S.E., Peddada, S.D. et al. (2014) Neonatal genome-wide methylation patterns in relation to birthweight in the Norwegian Mother and Child Cohort. Am. J. Epidemiol., 179, 834-842.
9. Gluckman, P.D., Hanson, M.A., Cooper, C. and Thornburg, K.L. (2008) Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med., 359, 61-73.
10. Gluckman, P.D., Hanson, M.A., Buklijas, T., Low, F.M. and Beedle, A.S. (2009) Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat. Rev. Endocr., 5, 401-408.
11. Heijmans, B.T., Tobi, E.W., Stein, A.D., Putter, H., Blauw, G.J., Susser, E.S., Slagboom, P.E. and Lumey, L. (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl. Acad. Sci., 105, 17046-17049.
12. Kahn, H.S., Graff, M., Stein, A.D. and Lumey, L. (2009) A fingerprint marker from early gestation associated with diabetes in middle age: the Dutch Hunger Winter Families Study. Int. J. Epidemiol., 38, 101-109.
13. Tobi, E.W., Lumey, L., Talens, R.P., Kremer, D., Putter, H., Stein, A.D., Slagboom, P.E. and Heijmans, B.T. (2009) DNA methylation differences after exposure to prenatal famine are common and timing-and sex-specific. Hum. Mol. Genet., 18, 4046-4053.
14. Whitson, R.H., Tsark, W., Huang, T.H. and Itakura, K. (2003) Neonatal mortality and leanness in mice lacking the ARID transcription factor Mrf-2. Biochem. Biophys. Res. Commun., 312, 997-1004.
15. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638.
16. Griffin, C.S., Simpson, P.J., Wilson, C.R. and Thacker, J. (2000) Mammalian recombination-repair genes XRCC2 and XRCC3 promote correct chromosome segregation. Nat. Cell Biol., 2, 757-761.
17. Tan, Q., Frost, M., Heijmans, B.T., von Bornemann Hjelmborg, J., Tobi, E.W., Christensen, K. and Christiansen, L. (2014) Epigenetic signature of birth weight discordance in adult twins. BMC Genomics, 15, 1062.
18. Novakovic, B., Yuen, R.K., Gordon, L., Penaherrera, M.S., Sharkey, A., Moffett, A., Craig, J.M., Robinson, W.P. and Saffery, R. (2011) Evidence for widespread changes in promoter methylation profile in human placenta in response to increasing gestational age and environmental/stochastic factors. BMC Genomics, 12, 529.
19. Cruickshank, M.N., Oshlack, A., Theda, C., Davis, P.G., Martino, D., Sheehan, P., Dai, Y., Saffery, R., Doyle, L.W. and Craig, J.M. (2013) Analysis of epigenetic changes in survivors of preterm birth reveals the effect of gestational age and evidence for a long term legacy. Genome Med., 5, 96.
20. Jaenisch, R. and Bird, A. (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet., 33, 245-254.
21. Migliore, L. and Coppedè, F. (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat. Res.-Fund. Mol. Mech. M., 667, 82-97.
22. Feil, R. and Fraga, M.F. (2012) Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Gen., 13, 97-109.
23. Wong, C., Caspi, A., Williams, B., Craig, I.W., Houts, R., Ambler, A., Moffitt, T.E. and Mill, J. (2010) A longitudinal study of epigenetic variation in twins. Epigenetics, 5, 516-526.
24. Wang, D., Liu, X., Zhou, Y., Xie, H., Hong, X., Tsai, H.-J., Wang, G., Liu, R. and Wang, X. (2012) Individual variation and longitudinal pattern of genome-wide DNA methylation from birth to the first two years of life. Epigenetics, 7, 594-605.
25. Madrigano, J., Baccarelli, A., Mittleman, M.A., Sparrow, D., Vokonas, P.S., Tarantini, L. and Schwartz, J. (2012) Aging and epigenetics. Epigenetics, 7, 63-70.
26. Alisch, R.S., Barwick, B.G., Chopra, P., Myrick, L.K., Satten, G. A., Conneely, K.N. and Warren, S.T. (2012) Age-associated DNA methylation in pediatric populations. Genome Res., 22, 623-632.
27. Bell, J.T., Tsai, P.-C., Yang, T.-P., Pidsley, R., Nisbet, J., Glass, D., Mangino, M., Zhai, G., Zhang, F., Valdes, A. et al. (2012) Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet., 8, e1002629.
28. Heyn, H., Li, N., Ferreira, H.J., Moran, S., Pisano, D.G., Gomez, A., Diez, J., Sanchez-Mut, J.V., Setien, F., Carmona, F.J. et al. (2012) Distinct DNA methylomes of newborns and centenarians. Proc. Natl. Acad. Sci., 109, 10522-10527.
29. Johansson, Å., Enroth, S. and Gyllensten, U. (2013) Continuous aging of the human DNA methylome throughout the human lifespan. PLoS ONE, 8, e67378.
30. Florath, I., Butterbach, K., Müller, H., Bewerunge-Hudler, M. and Brenner, H. (2013) Cross-sectional and longitudinal changes in DNA methylation with age: an epigenome-wide analysis revealing over 60 novel age-associated CpG sites. Hum. Mol. Genet., 23, 1186-1201.
31. Herbstman, J.B., Wang, S., Perera, F.P., Lederman, S.A., Vishnevetsky, J., Rundle, A.G., Hoepner, L.A., Qu, L. and Tang, D. (2013) Predictors and consequences of global DNA methylation in cord blood and at three years. PLoS ONE, 8, e72824.
32. Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S., Klotzle, B., Bibikova, M., Fan, J.-B., Gao, Y. et al. (2013) Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol. Cell, 49, 359-367.
33. Martino, D., Loke, Y.J., Gordon, L., Ollikainen, M., Cruickshank, M.N., Saffery, R. and Craig, J.M. (2013) Longitudinal, genome-scale analysis of DNA methylation in twins from birth to 18 months of age reveals rapid epigenetic change in early life and pair-specific effects of discordance. Genome Biol., 14, R42.
34. Martino, D., Maksimovic, J., Joo, J.-H., Prescott, S. and Saffery, R. (2012) Genome-scale profiling reveals a subset of genes regulated by DNA methylation that program somatic T-cell phenotypes in humans. Genes Immun., 13, 388-398.
35. Dedeurwaerder, S., Defrance, M., Calonne, E., Denis, H., Sotiriou, C. and Fuks, F. (2011) Evaluation of the Infinium Methylation 450 K technology. Epigenomics, 3, 771-784.
36. Houseman, E.A., Molitor, J. and Marsit, C.J. (2014) Referencefree cell mixture adjustments in analysis ofDNA methylation data. Bioinformatics, 30, 1431-1439.
37. Magnus, P., Irgens, L.M., Haug, K., Nystad, W., Skjærven, R. and Stoltenberg, C. (2006) Cohort profile: the Norwegian mother and child cohort study (MoBa). Int. J. Epidemiol., 35, 1146-1150.
38. Lee, K., Richmond, R., Hu, P., French, L., Shin, J., Bourdon, C., Reischl, E., Waldenberger, M., Zeilinger, S., Gaunt, T. et al. (2014) Prenatal exposure to maternal cigarette smoking and DNA methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ. Health Perspect, 123, 193-199.
39. Richmond, R.C., Simpkin, A.J., Woodward, G., Gaunt, T.R., Lyttleton, O., McArdle, W.L., Ring, S.M., Smith, A.D., Timpson, N. J., Tilling, K. et al. (2014) Prenatal exposure tomaternal smoking and offspring DNA methylation across the lifecourse: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Hum. Mol. Genet., 24, 2201-2217.
40. Sharp, G., Lawlor, D., Richmond, R., Fraser, A., Simpkin, A., Suderman, M., Shihab, H., Lyttleton, O., McArdle, W., Ring, S. et al. (2015) Maternal pre-pregnancy BMI and gestational weight gain, offspring DNA methylation and later offspring adiposity: findings from the Avon Longitudinal Study of Parents and Children. Int. J. Epidemiol., doi: 10.1093/ije/dyv042.
41. Shields, J.D., Kourtis, I.C., Tomei, A.A., Roberts, J.M. and Swartz, M.A. (2010) Induction of lymphoid-like stroma and immune escape by tumors that express the chemokine CCL21. Science, 328, 749-752.
42. Harvey, N.C., Lillycrop, K.A., Garratt, E., Sheppard, A., McLean, C., Burdge, G., Slater-Jefferies, J., Rodford, J., Crozier, S., Inskip, H. et al. (2012) Evaluation of methylation status of the eNOS promoter at birth in relation to childhood bone mineral content. Calcif. Tissue Int., 90, 120-127.
43. Åkerlund, M. (2002) Involvement of oxytocin and vasopressin in the pathophysiology of preterm labor and primary dysmenorrhea. Prog. Brain Res., 139, 359-365.
44. Salomonis, N., Cotte, N., Zambon, A.C., Pollard, K.S., Vranizan, K., Doniger, S.W., Dolganov, G. and Conklin, B.R. (2005) Identifying genetic networks underlying myometrial transition to labor. Genome Biol., 6, R12.
45. Stadtman, E.R., Van Remmen, H., Richardson, A., Wehr, N.B. and Levine, R.L. (2005) Methionine oxidation and aging. Biochim. Biophys. Acta, 1703, 135-140.
46. Shringarpure, R. and Davies, K.J. (2002) Protein turnover by the proteasome in aging and disease. Free Radic. Biol. Med., 32, 1084-1089.
47. Van Engelen, E., Breeveld-Dwarkasing, V., Taverne, M., Everts, M., Van der Weijden, G. and Rutten, V. (2008) MMP-2 expression precedes the final ripening process of the bovine cervix. Mol. Reprod. Dev., 75, 1669-1677.
48. Lufkin, T., Lohnes, D., Mark, M., Dierich, A., Gorry, P., Gaub, M.-P., LeMeur, M. and Chambon, P. (1993) High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc. Natl. Acad. Sci., 90, 7225-7229.
49. Messina, G., Biressi, S., Monteverde, S., Magli, A., Cassano, M., Perani, L., Roncaglia, E., Tagliafico, E., Starnes, L., Campbell, C. E. et al. (2010) Nfix regulates fetal-specific transcription in developing skeletal muscle. Cell, 140, 554-566.
50. Randall, T.D., Carragher, D.M. and Rangel-Moreno, J. (2008) Development of secondary lymphoid organs. Annu. Rev. Immunol., 26, 627.
51. Trainor, P.A. and Krumlauf, R. (2000) Patterning the cranial neural crest: Hinbrain segmentation and hox gene plasticity. Nat. Rev. Neurosci. 1, 116-124.
52. Durbán, M., Harezlak, J., Wand, M. and Carroll, R. (2005) Simple fitting of subject-specific curves for longitudinal data. Stat. Med., 24, 1153-1167.
53. Fraser, A., Macdonald-Wallis, C., Tilling, K., Boyd, A., Golding, J., Smith, G.D., Henderson, J., Macleod, J., Molloy, L., Ness, A. et al. (2013) Cohort profile: the Avon Longitudinal Study of Parents and Children: ALSPAC mothers cohort. Int. J. Epidemiol., 42, 97-110.
54. Touleimat, N. and Tost, J. (2012) Complete pipeline for Infinium ® Human Methylation 450 K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics, 4, 325-341.
55. Barfield, R.T., Kilaru, V., Smith, A.K. and Conneely, K.N. (2012) CpGassoc: an R function for analysis of DNA methylation microarray data. Bioinformatics, 28, 1280-1281.
56. Du, P., Zhang, X., Huang, C.-C., Jafari, N., Kibbe, W.A., Hou, L. and Lin, S.M. (2010) Comparison of Beta-value and M-value methods for quantifying methylation levels by microarray analysis. BMC Bioinformatics, 11, 587.
57. Teschendorff, A.E., Zhuang, J. and Widschwendter, M. (2011) Independent surrogate variable analysis to deconvolve confounding factors in large-scale microarray profiling studies. Bioinformatics, 27, 1496-1505.
58. Laird, N.M. and Ware, J.H. (1982) Random-effects models for longitudinal data. Biometrics, 38, 963-974.
59. Goldstein, H. (1986) Multilevel mixed linear-model analysis using iterative generalized least-squares. Biometrika, 73, 43-56.
60. Lawlor, D.A., Davey Smith, G. and Ebrahim, S. (2003) Association between leg length and offspring birthweight: partial explanation for the trans-generational association between birthweight and cardiovascular disease: findings from the BritishWomen's Heart and Health Study. Paediatr. Perinat. Epidemiol., 17, 148-155.
61. Lawlor, D.A., Ebrahim, S. and Smith, G.D. (2005) Association of birth weight with adult lung function: findings from the British Women's Heart and Health Study and a meta-analysis. Thorax, 60, 851-858.
62. Sørensen, H.T., Sabroe, S., Rothman, K.J., Gillman, M., Steffensen, F.H., Fischer, P. and Serensen, T.I. (1999) Birth weight and length as predictors for adult height. Am. J. Epidemiol., 149, 726-729.
63. Eide, M.G., Øyen, N., Skjærven, R., Nilsen, S.T., Bjerkedal, T. and Tell, G.S. (2005) Size at birth and gestational age as predictors of adult height and weight. Epidemiology, 16, 175-181.
64. Yarbrough, D., Barrett-Connor, E. and Morton, D. (2000) Birth weight as a predictor of adult bone mass in postmenopausal women: the Rancho Bernardo Study. Osteoporos. Int., 11, 626-630.
65. Singhal, A., Wells, J., Cole, T.J., Fewtrell, M. and Lucas, A. (2003) Programming of lean body mass: a link between birthweight, obesity, and cardiovascular disease? Am. J. Clin. Nutr., 77, 726-730.
66. Hamed, H., Purdie, D., Ramsden, C., Carmichael, B., Steel, S. and Howey, S. (1993) Influence of birth weight on adult bone mineral density. Osteoporos. Int., 3, 1-2.
67. Barker, M., Robinson, S., Osmond, C. and Barker, D. (1997) Birth weight and body fat distribution in adolescent girls. Arch. Dis. Child., 77, 381-383.
68. Matte, T.D., Bresnahan, M., Begg, M.D. and Susser, E. (2001) Influence of variation in birth weight within normal range and within sibships on IQ at age 7 years: cohort study. BMJ, 323, 310-314.