Adult monozygotic twins discordant for intra-uterine growth have indistinguishable genome-wide DNA methylation profiles

Genome Biology

Volumn 14, Issue 5, 2013, Pages

  Souren, Nicole Y P ^a,b,c   Lutsik, Pavlo ^a   Gasparoni, Gilles ^a   Tierling, Sascha ^a   Gries, Jasmin ^a   Riemenschneider, Matthias ^d   Fryns, Jean Pierre ^e   Derom, Catherine ^e   Zeegers, Maurice P ^b,c,f   Walter, Jörn ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d SAARLAND UNIVERSITY   (Germany)

^e UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ADULT; ARTICLE; BIRTH WEIGHT; CELL COMPOSITION; CELL TYPE; COHORT ANALYSIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; FEMALE; GENE LOCUS; GENE SEQUENCE; HUMAN; HUMAN GENOME; MONOZYGOTIC TWINS; NUCLEOTIDE SEQUENCE; PRENATAL GROWTH; SALIVA; TWIN DISCORDANCE; CYTOLOGY; DNA SEQUENCE; GENETICS; HIGH THROUGHPUT SEQUENCING; MIDDLE AGED; MOLECULAR GENETICS; PROCEDURES; YOUNG ADULT;

ADULT; BIRTH WEIGHT; DNA METHYLATION; FEMALE; GENOME, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MIDDLE AGED; MOLECULAR SEQUENCE DATA; SALIVA; SEQUENCE ANALYSIS, DNA; TWINS, MONOZYGOTIC; YOUNG ADULT;

EID: 84878005371     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-5-r44     Document Type: Article

References (60)

1. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 2005, 85:571-633. 10.1152/physrev.00053.2003, 15788706.
2. Newsome CA, Shiell AW, Fall CH, Phillips DI, Shier R, Law CM. Is birth weight related to later glucose and insulin metabolism? A systematic review. Diabet Med 2003, 20:339-348. 10.1046/j.1464-5491.2003.00871.x, 12752481.
3. Barker DJ. Adult consequences of fetal growth restriction. Clin Obstet Gynecol 2006, 49:270-283. 10.1097/00003081-200606000-00009, 16721106.
4. Lindsay RS, Dabelea D, Roumain J, Hanson RL, Bennett PH, Knowler WC. Type 2 diabetes and low birth weight: the role of paternal inheritance in the association of low birth weight and diabetes. Diabetes 2000, 49:445-449. 10.2337/diabetes.49.3.445, 10868967.
5. Wannamethee SG, Lawlor DA, Whincup PH, Walker M, Ebrahim S, Davey-Smith G. Birthweight of offspring and paternal insulin resistance and paternal diabetes in late adulthood: cross sectional survey. Diabetologia 2004, 47:12-18. 10.1007/s00125-003-1270-x, 14647894.
6. Grunnet L, Vielwerth S, Vaag A, Poulsen P. Birth weight is nongenetically associated with glucose intolerance in elderly twins, independent of adult obesity. J Intern Med 2007, 262:96-103. 10.1111/j.1365-2796.2007.01793.x, 17598817.
7. Poulsen P, Vaag AA, Kyvik KO, Moller Jensen D, Beck-Nielsen H. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia 1997, 40:439-446. 10.1007/s001250050698, 9112021.
8. Bo S, Cavallo-Perin P, Scaglione L, Ciccone G, Pagano G. Low birthweight and metabolic abnormalities in twins with increased susceptibility to Type 2 diabetes mellitus. Diabet Med 2000, 17:365-370.
9. Monrad RN, Grunnet LG, Rasmussen EL, Malis C, Vaag A, Poulsen P. Age-dependent nongenetic influences of birth weight and adult body fat on insulin sensitivity in twins. J Clin Endocrinol Metab 2009, 94:2394-2399. 10.1210/jc.2008-1858, 19417034.
10. Iliadou A, Cnattingius S, Lichtenstein P. Low birthweight and type 2 diabetes: a study on 11 162 Swedish twins. Int J Epidemiol 2004, 33:948-953. 10.1093/ije/dyh117, 15166205.
11. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 2008, 359:61-73. 10.1056/NEJMra0708473, 18596274.
12. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev 2002, 16:6-21. 10.1101/gad.947102, 11782440.
13. Seki Y, Williams L, Vuguin PM, Charron MJ. Minireview: Epigenetic programming of diabetes and obesity: animal models. Endocrinology 2012, 153:1031-1038. 10.1210/en.2011-1805, 3281534, 22253432.
14. 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 USA 2008, 105:17046-17049. 10.1073/pnas.0806560105, 2579375, 18955703.
15. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, Slagboom PE, Heijmans BT. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet 2009, 18:4046-4053. 10.1093/hmg/ddp353, 2758137, 19656776.
16. Einstein F, Thompson RF, Bhagat TD, Fazzari MJ, Verma A, Barzilai N, Greally JM. Cytosine methylation dysregulation in neonates following intrauterine growth restriction. PLoS One 2010, 5:e8887. 10.1371/journal.pone.0008887, 2811176, 20126273.
17. Yaghootkar H, Freathy RM. Genetic origins of low birth weight. Curr Opin Clin Nutr Metab Care 2012, 15:258-264. 10.1097/MCO.0b013e328351f543, 22406741.
18. Meaburn EL, Schalkwyk LC, Mill J. Allele-specific methylation in the human genome: implications for genetic studies of complex disease. Epigenetics 2010, 5:578-582. 10.4161/epi.5.7.12960, 3052843, 20716955.
19. Derom CA, Vlietinck RF, Thiery EW, Leroy FO, Fryns JP, Derom RM. The East Flanders Prospective Twin Survey (EFPTS). Twin Res Hum Genet 2006, 9:733-738. 10.1375/twin.9.6.733, 17254399.
20. Kaminsky ZA, Tang T, Wang SC, Ptak C, Oh GH, Wong AH, Feldcamp LA, Virtanen C, Halfvarson J, Tysk C, McRae AF, Visscher PM, Montgomery GW, Martin NG, Petronis A. DNA methylation profiles in monozygotic and dizygotic twins. Nat Genet 2009, 41:240-245. 10.1038/ng.286, 19151718.
21. Lewi L, Gucciardo L, Van Mieghem T, de Koninck P, Beck V, Medek H, Van Schoubroeck D, Devlieger R, De Catte L, Deprest J. Monochorionic diamniotic twin pregnancies: natural history and risk stratification. Fetal Diagn Ther 2010, 27:121-133. 10.1159/000313300, 20413975.
22. Loos RJ, Beunen G, Fagard R, Derom C, Vlietinck R. The influence of zygosity and chorion type on fat distribution in young adult twins consequences for twin studies. Twin Res 2001, 4:356-364.
23. Aps JK, Van den Maagdenberg K, Delanghe JR, Martens LC. Flow cytometry as a new method to quantify the cellular content of human saliva and its relation to gingivitis. Clin Chim Acta 2002, 321:35-41. 10.1016/S0009-8981(02)00062-1, 12031590.
24. Thiede C, Prange-Krex G, Freiberg-Richter J, Bornhauser M, Ehninger G. Buccal swabs but not mouthwash samples can be used to obtain pretransplant DNA fingerprints from recipients of allogeneic bone marrow transplants. Bone Marrow Transplant 2000, 25:575-577.
25. Rakyan VK, Beyan H, Down TA, Hawa MI, Maslau S, Aden D, Daunay A, Busato F, Mein CA, Manfras B, Dias KR, Bell CG, Tost J, Boehm BO, Beck S, Leslie RD. Identification of type 1 diabetes-associated DNA methylation variable positions that precede disease diagnosis. PLoS Genet 2011, 7:e1002300. 10.1371/journal.pgen.1002300, 3183089, 21980303.
26. Vidovic A, Vidovic Juras D, Vucicevic Boras V, Lukac J, Grubisic-Ilic M, Rak D, Sabioncello A. Determination of leucocyte subsets in human saliva by flow cytometry. Arch Oral Biol 2012, 57:577-583. 10.1016/j.archoralbio.2011.10.015, 22118990.
27. Tierling S, Souren NY, Reither S, Zang KD, Meng-Hentschel J, Leitner D, Oehl-Jaschkowitz B, Walter J. DNA methylation studies on imprinted loci in a male monozygotic twin pair discordant for Beckwith-Wiedemann syndrome. Clin Genet 2011, 79:546-553. 10.1111/j.1399-0004.2010.01482.x, 20618351.
28. Weksberg R, Shuman C, Caluseriu O, Smith AC, Fei YL, Nishikawa J, Stockley TL, Best L, Chitayat D, Olney A, Ives E, Schneider A, Bestor TH, Li M, Sadowski P, Squire J. Discordant KCNQ1OT1 imprinting in sets of monozygotic twins discordant for Beckwith-Wiedemann syndrome. Hum Mol Genet 2002, 11:1317-1325. 10.1093/hmg/11.11.1317, 12019213.
29. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
30. Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet 2011, 12:529-541. 10.1038/nrg3000, 3508712, 21747404.
31. Bibikova M, Le J, Barnes B, Saedinia-Melnyk S, Zhou L, Shen R, Gunderson KL. Genome-wide DNA methylation profiling using Infinium(R) assay. Epigenomics 2009, 1:177-200. 10.2217/epi.09.14, 22122642.
32. Chen YA, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, Gallinger S, Hudson TJ, Weksberg R. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics 2013, 8:203-209. 10.4161/epi.23470, 3592906, 23314698.
33. Dedeurwaerder S, Defrance M, Calonne E, Denis H, Sotiriou C, Fuks F. Evaluation of the Infinium Methylation 450K technology. Epigenomics 2011, 3:771-784. 10.2217/epi.11.105, 22126295.
34. Fryer AA, Emes RD, Ismail KM, Haworth KE, Mein C, Carroll WD, Farrell WE. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics 2011, 6:86-94. 10.4161/epi.6.1.13392, 3052917, 20864804.
35. Turan N, Ghalwash MF, Katari S, Coutifaris C, Obradovic Z, Sapienza C. DNA methylation differences at growth related genes correlate with birth weight: a molecular signature linked to developmental origins of adult disease?. BMC Med Genomics 2012, 5:10. 10.1186/1755-8794-5-10, 3359247, 22498030.
36. Adkins RM, Tylavsky FA, Krushkal J. Newborn umbilical cord blood DNA methylation and gene expression levels exhibit limited association with birth weight. Chem Biodivers 2012, 9:888-899. 10.1002/cbdv.201100395, 22589090.
37. Banister CE, Koestler DC, Maccani MA, Padbury JF, Houseman EA, Marsit CJ. Infant growth restriction is associated with distinct patterns of DNA methylation in human placentas. Epigenetics 2011, 6:920-927. 10.4161/epi.6.7.16079, 3154432, 21758004.
38. Gordon L, Joo JE, Powell JE, Ollikainen M, Novakovic B, Li X, Andronikos R, Cruickshank MN, Conneely KN, Smith AK, Alisch RS, Morley R, Visscher PM, Craig JM, Saffery R. Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res 2012, 22:1395-1406. 10.1101/gr.136598.111, 3409253, 22800725.
39. Michels KB, Harris HR, Barault L. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS One 2011, 6:e25254. 10.1371/journal.pone.0025254, 3182185, 21980406.
40. Wilhelm-Benartzi CS, Houseman EA, Maccani MA, Poage GM, Koestler DC, Langevin SM, Gagne LA, Banister CE, Padbury JF, Marsit CJ. In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta. Environ Health Perspect 2012, 120:296-302. 3279448, 22005006.
41. Gielen M, Lindsey PJ, Derom C, Loos RJ, Souren NY, Paulussen AD, Zeegers MP, Derom R, Vlietinck R, Nijhuis JG. Twin-specific intrauterine 'growth' charts based on cross-sectional birthweight data. Twin Res Hum Genet 2008, 11:224-235. 10.1375/twin.11.2.224, 18361725.
42. Liu J, Morgan M, Hutchison K, Calhoun VD. A study of the influence of sex on genome wide methylation. PLoS One 2010, 5:e10028. 10.1371/journal.pone.0010028, 2850313, 20386599.
43. Souren NY, Tierling S, Fryns JP, Derom C, Walter J, Zeegers MP. DNA Methylation variability at growth-related imprints does not contribute to overweight in monozygotic twins discordant for BMI. Obesity (Silver Spring) 2011, 19:1519-1522.
44. Derom R, Derom C, Vlietinck R. Placentation. Multiple Pregnancy: Epidemiology, Gestation and Perinatal Outcome 1995, 113-128. New York: The Parthenon Publishing Group, Keith LG, Papiernik E, Keith DM, Luke B.
45. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, Delano D, Zhang L, Schroth GP, Gunderson KL, Fan JB, Shen R. High density DNA methylation array with single CpG site resolution. Genomics 2011, 98:288-295. 10.1016/j.ygeno.2011.07.007, 21839163.
46. Lutsik P, Feuerbach L, Arand J, Lengauer T, Walter J, Bock C. BiQ Analyzer HT: locus-specific analysis of DNA methylation by high-throughput bisulfite sequencing. Nucleic Acids Res 2011, 39:W551-556. 10.1093/nar/gkr312, 3125748, 21565797.
47. El-Maarri O, Herbiniaux U, Walter J, Oldenburg J. A rapid, quantitative, non-radioactive bisulfite-SNuPE- IP RP HPLC assay for methylation analysis at specific CpG sites. Nucleic Acids Res 2002, 30:e25. 10.1093/nar/30.6.e25, 101369, 11884644.
48. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H, Campan M, Noushmehr H, Bell CG, Maxwell AP, Savage DA, Mueller-Holzner E, Marth C, Kocjan G, Gayther SA, Jones A, Beck S, Wagner W, Laird PW, Jacobs IJ, Widschwendter M. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 2010, 20:440-446. 10.1101/gr.103606.109, 2847747, 20219944.
49. Essex MJ, Thomas Boyce W, Hertzman C, Lam LL, Armstrong JM, Neumann SM, Kobor MS. Epigenetic vestiges of early developmental adversity: childhood stress exposure and DNA methylation in adolescence. Child Dev 2013, 84:58-75. 10.1111/j.1467-8624.2011.01641.x, 21883162.
50. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.
51. Shieh G, Jan SL, Randles RH. Power and sample size determinations for the Wilcoxon signed-rank test. J Stat Comput Simulation 2007, 77:717-724.
52. Chai KH, McLoughlin DM, Chan TF, Chan HY, Lau KF. Genomic organization and promoter cloning of the human X11alpha gene APBA1. DNA Cell Biol 2012, 31:651-659. 10.1089/dna.2011.1447, 22136355.
53. Miaczynska M, Christoforidis S, Giner A, Shevchenko A, Uttenweiler-Joseph S, Habermann B, Wilm M, Parton RG, Zerial M. APPL proteins link Rab5 to nuclear signal transduction via an endosomal compartment. Cell 2004, 116:445-456. 10.1016/S0092-8674(04)00117-5, 15016378.
54. Schenck A, Goto-Silva L, Collinet C, Rhinn M, Giner A, Habermann B, Brand M, Zerial M. The endosomal protein Appl1 mediates Akt substrate specificity and cell survival in vertebrate development. Cell 2008, 133:486-497. 10.1016/j.cell.2008.02.044, 18455989.
55. Jiang S, Fang Q, Yu W, Zhang R, Hu C, Dong K, Bao Y, Wang C, Xiang K, Jia W. Genetic variations in APPL2 are associated with overweight and obesity in a Chinese population with normal glucose tolerance. BMC Med Genet 2012, 13:22. 3368742, 22462604.
56. Christiansen J, Kolte AM, Hansen TO, Nielsen FC. IGF2 mRNA-binding protein 2: biological function and putative role in type 2 diabetes. J Mol Endocrinol 2009, 43:187-195. 10.1677/JME-09-0016, 19429674.
57. Rapti A, Trangas T, Samiotaki M, Ioannidis P, Dimitriadis E, Meristoudis C, Veletza S, Courtis N. The structure of the 5'-untranslated region of mammalian poly(A) polymerase-alpha mRNA suggests a mechanism of translational regulation. Mol Cell Biochem 2010, 340:91-96. 10.1007/s11010-010-0405-x, 20174964.
58. Burwinkel B, Rootwelt T, Kvittingen EA, Chakraborty PK, Kilimann MW. Severe phenotype of phosphorylase kinase-deficient liver glycogenosis with mutations in the PHKG2 gene. Pediatr Res 2003, 54:834-839. 10.1203/01.PDR.0000088069.09275.10, 12930917.
59. Liu C, Lin JD. PGC-1 coactivators in the control of energy metabolism. Acta Biochim Biophys Sin (Shanghai) 2011, 43:248-257.
60. Komori T. Signaling networks in RUNX2-dependent bone development. J Cell Biochem 2011, 112:750-755. 10.1002/jcb.22994, 21328448.