Breastfeeding effects on DNA methylation in the offspring: A systematic literature review

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Hartwig, Fernando Pires ^a,b   De Mola, Christian Loret ^a   Davies, Neil Martin ^b   Victora, Cesar Gomes ^a   Relton, Caroline L ^b  

^a FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; DNA; GLUCOSE TRANSPORTER 4; CDKN2A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 2C; SLC2A4 PROTEIN, HUMAN;

BREAST FEEDING; CDKN2A GENE; DNA METHYLATION; EPIGENETICS; GENE; GENETIC VARIABILITY; HUMAN; LEP GENE; NYP GENE; PROGENY; PROMOTER REGION; REVIEW; SLC2A4 GENE; SYSTEMATIC REVIEW; BREAST MILK; CHEMISTRY; FEMALE; GENETIC EPIGENESIS; GENETICS; INFANT; LONGITUDINAL STUDY; MALE; METABOLISM; PHYSIOLOGY;

BREAST FEEDING; CYCLIN-DEPENDENT KINASE INHIBITOR P18; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GLUCOSE TRANSPORTER TYPE 4; HUMANS; INFANT; LONGITUDINAL STUDIES; MALE; MILK, HUMAN;

EID: 85014489847     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0173070     Document Type: Review

References (79)

1. Victora CG, Bahl R, Barros AJ, Franca GV, Horton S, Krasevec J, et al. Breastfeeding in the 21st century: epidemiology, mechanisms, and lifelong effect. Lancet. 2016; 387:475-490. doi: 10.1016/S0140-6736(15)01024-7 PMID: 26869575
2. Relton CL, Hartwig FP, Davey Smith G. From stem cells to the law courts: DNA methylation, the forensic epigenome and the possibility of a biosocial archive. Int J Epidemiol. 2015; 44:1083-1093. doi: 10. 1093/ije/dyv198 PMID: 26424516
3. Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007; 61:5R-10R. doi: 10.1203/pdr.0b013e318045bedb PMID: 17413851
4. Gluckman PD, Hanson MA, Mitchell MD. Developmental origins of health and disease: reducing the burden of chronic disease in the next generation. Genome Med. 2010; 2:14. doi: 10.1186/gm135 PMID: 20236494
5. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007; 27:363-388. doi: 10.1146/annurev.nutr.27.061406.093705 PMID: 17465856
6. Han L, Su B, Li WH, Zhao Z. CpG island density and its correlations with genomic features in mammalian genomes. Genome Biol. 2008; 9:R79. doi: 10.1186/gb-2008-9-5-r79 PMID: 18477403
7. Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet. 2011; 12:529-541. doi: 10.1038/nrg3000 PMID: 21747404
8. Boddicker RL, Koltes JE, Fritz-Waters ER, Koesterke L, Weeks N, Yin T, et al. Genome-wide methylation profile following prenatal and postnatal dietary omega-3 fatty acid supplementation in pigs. Anim Genet. 2016.
9. Mischke M, Plosch T. More than just a gut instinct-the potential interplay between a baby's nutrition, its gut microbiome, and the epigenome. Am J Physiol Regul Integr Comp Physiol. 2013; 304:R1065-1069. doi: 10.1152/ajpregu.00551.2012 PMID: 23594611
10. Karlsson O, Rodosthenous RS, Jara C, Brennan KJ, Wright RO, Baccarelli AA, et al. Detection of long non-coding RNAs in human breastmilk extracellular vesicles: Implications for early child development. Epigenetics. 2016:0.
11. Alsaweed M, Hartmann PE, Geddes DT, Kakulas F. MicroRNAs in Breastmilk and the Lactating Breast: Potential Immunoprotectors and Developmental Regulators for the Infant and the Mother. Int J Environ Res Public Health. 2015; 12:13981-14020. doi: 10.3390/ijerph121113981 PMID: 26529003
12. Verduci E, Banderali G, Barberi S, Radaelli G, Lops A, Betti F, et al. Epigenetic effects of human breast milk. Nutrients. 2014; 6:1711-1724. doi: 10.3390/nu6041711 PMID: 24763114
13. Obermann-Borst SA, Eilers PH, Tobi EW, de Jong FH, Slagboom PE, Heijmans BT, et al. Duration of breastfeeding and gender are associated with methylation of the LEPTIN gene in very young children. Pediatr Res. 2013; 74:344-349. doi: 10.1038/pr.2013.95 PMID: 23884163
14. Stoger R. In vivo methylation patterns of the leptin promoter in human and mouse. Epigenetics. 2006; 1:155-162. PMID: 17965621
15. Rossnerova A, Tulupova E, Tabashidze N, Schmuczerova J, Dostal M, Rossner P Jr., et al. Factors affecting the 27K DNA methylation pattern in asthmatic and healthy children from locations with various environments. Mutat Res. 2013; 741-742:18-26. doi: 10.1016/j.mrfmmm.2013.02.003 PMID: 23458556
16. Soto-Ramirez N, Karmaus W, Ziyab A, Lockett G, Arshad S, Holloway J, et al (2013) The interaction of breastfeeding, DNA methylation, and genetic variants in chromosome 17q12 and the risk of asthma in girls at age 18 years. American Thoracic Society 2013 International Conference. Philadelphia, USA: American Journal of Respiratory and Critical Care Medicine. pp. A:3517.
17. Soto-Ramirez N, Arshad SH, Holloway JW, Zhang H, Schauberger E, Ewart S, et al. The interaction of genetic variants and DNA methylation of the interleukin-4 receptor gene increase the risk of asthma at age 18 years. Clin Epigenetics. 2013; 5:1. doi: 10.1186/1868-7083-5-1 PMID: 23286427
18. Tao MH, Marian C, Shields PG, Potischman N, Nie J, Krishnan SS, et al. Exposures in early life: associations with DNA promoter methylation in breast tumors. J Dev Orig Health Dis. 2013; 4:182-190. doi: 10.1017/S2040174412000694 PMID: 25054684
19. Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis. 2010; 31:27-36. doi: 10.1093/ carcin/bgp220 PMID: 19752007
20. Berdasco M, Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell. 2010; 19:698-711. doi: 10.1016/j.devcel.2010.10.005 PMID: 21074720
21. Cole SR, Platt RW, Schisterman EF, Chu H, Westreich D, Richardson D, et al. Illustrating bias due to conditioning on a collider. Int J Epidemiol. 2010; 39:417-420. doi: 10.1093/ije/dyp334 PMID: 19926667
22. Ng JW, Barrett LM, Wong A, Kuh D, Davey Smith G, Relton CL. The role of longitudinal cohort studies in epigenetic epidemiology: challenges and opportunities. Genome Biol. 2012; 13:246. doi: 10.1186/gb-2012-13-6-246 PMID: 22747597
23. Simpkin AJ, Hemani G, Suderman M, Gaunt TR, Lyttleton O, McArdle WL, et al. Prenatal and early life influences on epigenetic age in children: a study of mother-offspring pairs from two cohort studies. Hum Mol Genet. 2016; 25:191-201. doi: 10.1093/hmg/ddv456 PMID: 26546615
24. Relton CL, Gaunt T, McArdle W, Ho K, Duggirala A, Shihab H, et al. Data Resource Profile: Accessible Resource for Integrated Epigenomic Studies (ARIES). Int J Epidemiol. 2015; 44:1181-1190. doi: 10. 1093/ije/dyv072 PMID: 25991711
25. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013; 14:R115. doi: 10.1186/gb-2013-14-10-r115 PMID: 24138928
26. Jaffe AE, Irizarry RA. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014; 15:R31. doi: 10.1186/gb-2014-15-2-r31 PMID: 24495553
27. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013; 49:359-367. doi: 10.1016/j.molcel. 2012.10.016 PMID: 23177740
28. Mahmood S, Smiraglia DJ, Srinivasan M, Patel MS. Epigenetic changes in hypothalamic appetite regulatory genes may underlie the developmental programming for obesity in rat neonates subjected to a high-carbohydrate dietary modification. J Dev Orig Health Dis. 2013; 4:479-490. doi: 10.1017/ S2040174413000238 PMID: 24924227
29. Raychaudhuri N, Thamotharan S, Srinivasan M, Mahmood S, Patel MS, Devaskar SU. Postnatal exposure to a high-carbohydrate diet interferes epigenetically with thyroid hormone receptor induction of theadult male rat skeletal muscle glucose transporter isoform 4 expression. J Nutr Biochem. 2014; 25:1066-1076. doi: 10.1016/j.jnutbio.2014.05.011 PMID: 25086780
30. Ehrich M, Nelson MR, Stanssens P, Zabeau M, Liloglou T, Xinarianos G, et al. Quantitative highthroughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci U S A. 2005; 102:15785-15790. doi: 10.1073/pnas.0507816102 PMID: 16243968
31. Vadlamudi S, Hiremagalur BK, Tao L, Kalhan SC, Kalaria RN, Kaung HL, et al. Long-term effects on pancreatic function of feeding a HC formula to rats during the preweaning period. Am J Physiol. 1993; 265:E565-571. PMID: 8238331
32. Mitrani P, Srinivasan M, Dodds C, Patel MS. Role of the autonomic nervous system in the development of hyperinsulinemia by high-carbohydrate formula feeding to neonatal rats. Am J Physiol Endocrinol Metab. 2007; 292:E1069-1078. doi: 10.1152/ajpendo.00477.2006 PMID: 17164433
33. Srinivasan M, Mitrani P, Sadhanandan G, Dodds C, Shbeir-ElDika S, Thamotharan S, et al. A high-carbohydrate diet in the immediate postnatal life of rats induces adaptations predisposing to adult-onset obesity. J Endocrinol. 2008; 197:565-574. doi: 10.1677/JOE-08-0021 PMID: 18492820
34. Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol. 2008; 29:386-397. doi: 10.1016/j.yfrne.2008.03.003 PMID: 18462782
35. Champagne FA, Curley JP. Epigenetic mechanisms mediating the long-term effects of maternal care on development. Neurosci Biobehav Rev. 2009; 33:593-600. doi: 10.1016/j.neubiorev.2007.10.009PMID: 18430469
36. McGowan PO, Suderman M, Sasaki A, Huang TC, Hallett M, Meaney MJ, et al. Broad epigenetic signature of maternal care in the brain of adult rats. PLoS One. 2011; 6:e14739. doi: 10.1371/journal.pone.0014739 PMID: 21386994
37. Gudsnuk K, Champagne FA. Epigenetic influence of stress and the social environment. ILAR J. 2012; 53:279-288. doi: 10.1093/ilar.53.3-4.279 PMID: 23744967
38. Wagner JR, Busche S, Ge B, Kwan T, Pastinen T, Blanchette M. The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol. 2014; 15:R37. doi: 10.1186/gb-2014-15-2-r37 PMID: 24555846
39. Deng Y, Chan SS, Chang S. Telomere dysfunction and tumour suppression: the senescence connection. Nat Rev Cancer. 2008; 8:450-458. doi: 10.1038/nrc2393 PMID: 18500246
40. Tow J. Heal the mother, heal the baby: epigenetics, breastfeeding and the human microbiome. Breastfeed Rev. 2014; 22:7-9.
41. Joubert BR, Felix JF, Yousefi P, Bakulski KM, Just AC, Breton C, et al. DNA Methylation in Newborns and Maternal Smoking in Pregnancy: Genome-wide Consortium Meta-analysis. Am J Hum Genet. 2016; 98:680-696. doi: 10.1016/j.ajhg.2016.02.019 PMID: 27040690
42. Shrier I, Platt RW. Reducing bias through directed acyclic graphs. BMC Med Res Methodol. 2008; 8:70. doi: 10.1186/1471-2288-8-70 PMID: 18973665
43. Chor D, Lima CR. [Epidemiologic aspects of racial inequalities in health in Brazil]. Cad Saude Publica. 2005; 21:1586-1594. PMID: 16158166
44. Williams DR, Mohammed SA, Leavell J, Collins C. Race, socioeconomic status, and health: complexities, ongoing challenges, and research opportunities. Ann N Y Acad Sci. 2010; 1186:69-101. doi: 10. 1111/j.1749-6632.2009.05339.x PMID: 20201869
45. Quillian L. Segregation and Poverty Concentration: The Role of Three Segregations. Am Sociol Rev. 2012; 77:354-379. doi: 10.1177/0003122412447793 PMID: 24648570
46. Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, Korbel JO, et al. A global reference for human genetic variation. Nature. 2015; 526:68-74. doi: 10.1038/nature15393 PMID: 26432245
47. Paaby AB, Rockman MV. The many faces of pleiotropy. Trends Genet. 2013; 29:66-73. doi: 10.1016/j. tig.2012.10.010 PMID: 23140989
48. Jones JR, Kogan MD, Singh GK, Dee DL, Grummer-Strawn LM. Factors associated with exclusive breastfeeding in the United States. Pediatrics. 2011; 128:1117-1125. doi: 10.1542/peds.2011-0841PMID: 22123898
49. Michels KA, Mumford SL, Sundaram R, Bell EM, Bello SC, Yeung EH. Differences in infant feeding practices by mode of conception in a United States cohort. Fertil Steril. 2016; 105:1014-1022 e1011. doi: 10.1016/j.fertnstert.2015.12.043 PMID: 26773191
50. Kitano N, Nomura K, Kido M, Murakami K, Ohkubo T, Ueno M, et al. Combined effects of maternal age and parity on successful initiation of exclusive breastfeeding. Prev Med Rep. 2016; 3:121-126. doi: 10. 1016/j.pmedr.2015.12.010 PMID: 26844198
51. Oakley LL, Renfrew MJ, Kurinczuk JJ, Quigley MA. Factors associated with breastfeeding in England: an analysis by primary care trust. BMJ Open. 2013; 3.
52. Wojcicki JM. Maternal prepregnancy body mass index and initiation and duration of breastfeeding: a review of the literature. J Womens Health (Larchmt). 2011; 20:341-347.
53. Castillo H, Santos IS, Matijasevich A. Maternal pre-pregnancy BMI, gestational weight gain and breastfeeding. Eur J Clin Nutr. 2016; 70:431-436. doi: 10.1038/ejcn.2015.232 PMID: 26813940
54. Horta BL, Kramer MS, Platt RW. Maternal smoking and the risk of early weaning: a meta-analysis. Am J Public Health. 2001; 91:304-307. PMID: 11211645
55. Richmond RC, Simpkin AJ, Woodward G, Gaunt TR, Lyttleton O, McArdle WL, et al. Prenatal exposure to maternal smoking and offspring DNA methylation across the lifecourse: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Hum Mol Genet. 2015; 24:2201-2217. doi: 10.1093/ hmg/ddu739 PMID: 25552657
56. Engel SM, Joubert BR, Wu MC, Olshan AF, Haberg SE, Ueland PM, et al. Neonatal genome-wide methylation patterns in relation to birth weight in the Norwegian Mother and Child Cohort. Am J Epidemiol. 2014; 179:834-842. doi: 10.1093/aje/kwt433 PMID: 24561991
57. Adkins RM, Thomas F, Tylavsky FA, Krushkal J. Parental ages and levels of DNA methylation in the newborn are correlated. BMC Med Genet. 2011; 12:47. doi: 10.1186/1471-2350-12-47 PMID: 21453505
58. Markunas CA, Wilcox AJ, Xu Z, Joubert BR, Harlid S, Panduri V, et al. Maternal Age at Delivery Is Associated with an Epigenetic Signature in Both Newborns and Adults. PLoS One. 2016; 11:e0156361. doi: 10.1371/journal.pone.0156361 PMID: 27383059
59. Herbstman JB, Wang S, Perera FP, Lederman SA, Vishnevetsky J, Rundle AG, et al. Predictors and consequences of global DNA methylation in cord blood and at three years. PLoS One. 2013; 8:e72824. doi: 10.1371/journal.pone.0072824 PMID: 24023780
60. Sharp GC, Lawlor DA, Richmond RC, Fraser A, Simpkin A, Suderman M, et al. 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. 2015; 44:1288-1304. doi: 10. 1093/ije/dyv042 PMID: 25855720
61. Simpkin AJ, Suderman M, Gaunt TR, Lyttleton O, McArdle WL, Ring SM, et al. Longitudinal analysis of DNA methylation associated with birth weight and gestational age. Hum Mol Genet. 2015; 24:3752-3763. doi: 10.1093/hmg/ddv119 PMID: 25869828
62. Raisanen S, Gissler M, Kramer MR, Heinonen S. Influence of delivery characteristics and socioeconomic status on giving birth by caesarean section-a cross sectional study during 2000-2010 in Finland. BMC Pregnancy Childbirth. 2014; 14:120. doi: 10.1186/1471-2393-14-120 PMID: 24678806
63. Elshibly EM, Schmalisch G. The effect of maternal anthropometric characteristics and social factors on gestational age and birth weight in Sudanese newborn infants. BMC Public Health. 2008; 8:244. doi: 10. 1186/1471-2458-8-244 PMID: 18638377
64. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, et al. Maternal and child undernutrition: global and regional exposures and health consequences. Lancet. 2008; 371:243-260. doi: 10. 1016/S0140-6736(07)61690-0 PMID: 18207566
65. Ng SK, Cameron CM, Hills AP, McClure RJ, Scuffham PA. Socioeconomic disparities in prepregnancy BMI and impact on maternal and neonatal outcomes and postpartum weight retention: the EFHL longitudinal birth cohort study. BMC Pregnancy Childbirth. 2014; 14:314. doi: 10.1186/1471-2393-14-314PMID: 25201481
66. Walker SP, Wachs TD, Gardner JM, Lozoff B, Wasserman GA, Pollitt E, et al. Child development: risk factors for adverse outcomes in developing countries. Lancet. 2007; 369:145-157. doi: 10.1016/S0140-6736(07)60076-2 PMID: 17223478
67. Zetterstrom R. Breastfeeding and infant-mother interaction. Acta Paediatr Suppl. 1999; 88:1-6.
68. Fergusson DM, Woodward LJ. Breast feeding and later psychosocial adjustment. Paediatr Perinat Epidemiol. 1999; 13:144-157. PMID: 10214606
69. Byun HM, Siegmund KD, Pan F, Weisenberger DJ, Kanel G, Laird PW, et al. Epigenetic profiling of somatic tissues from human autopsy specimens identifies tissue- and individual-specific DNA methylation patterns. Hum Mol Genet. 2009; 18:4808-4817. doi: 10.1093/hmg/ddp445 PMID: 19776032
70. Ziller MJ, Gu H, Muller F, Donaghey J, Tsai LT, Kohlbacher O, et al. Charting a dynamic DNA methylation landscape of the human genome. Nature. 2013; 500:477-481. doi: 10.1038/nature12433 PMID: 23925113
71. Illingworth RS, Gruenewald-Schneider U, De Sousa D, Webb S, Merusi C, Kerr AR, et al. Inter-individual variability contrasts with regional homogeneity in the human brain DNA methylome. Nucleic Acids Res. 2015; 43:732-744. doi: 10.1093/nar/gku1305 PMID: 25572316
72. Relton CL, Davey Smith G. Epigenetic epidemiology of common complex disease: prospects for prediction, prevention, and treatment. PLoS Med. 2010; 7:e1000356. doi: 10.1371/journal.pmed.1000356PMID: 21048988
73. Heijmans BT, Mill J. Commentary: The seven plagues of epigenetic epidemiology. Int J Epidemiol. 2012; 41:74-78. doi: 10.1093/ije/dyr225 PMID: 22269254
74. Kramer MS, Aboud F, Mironova E, Vanilovich I, Platt RW, Matush L, et al. Breastfeeding and child cognitive development: new evidence from a large randomized trial. Arch Gen Psychiatry. 2008; 65:578-584. doi: 10.1001/archpsyc.65.5.578 PMID: 18458209
75. Brion MJ, Lawlor DA, Matijasevich A, Horta B, Anselmi L, Araujo CL, et al. What are the causal effects of breastfeeding on IQ, obesity and blood pressure? Evidence from comparing high-income with middle-income cohorts. Int J Epidemiol. 2011; 40:670-680. doi: 10.1093/ije/dyr020 PMID: 21349903
76. Horta BL, Loret de Mola C, Victora CG. Breastfeeding and intelligence: a systematic review and metaanalysis. Acta Paediatr. 2015; 104:14-19. doi: 10.1111/apa.13139 PMID: 26211556
77. Davies MN, Volta M, Pidsley R, Lunnon K, Dixit A, Lovestone S, et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol. 2012; 13:R43. doi: 10.1186/gb-2012-13-6-r43 PMID: 22703893
78. Walton E, Hass J, Liu J, Roffman JL, Bernardoni F, Roessner V, et al. Correspondence of DNA Methylation Between Blood and Brain Tissue and Its Application to Schizophrenia Research. Schizophr Bull. 2016; 42:406-414. doi: 10.1093/schbul/sbv074 PMID: 26056378
79. Hannon E, Lunnon K, Schalkwyk L, Mill J. Interindividual methylomic variation across blood, cortex, and cerebellum: implications for epigenetic studies of neurological and neuropsychiatric phenotypes. Epigenetics. 2015; 10:1024-1032. doi: 10.1080/15592294.2015.1100786 PMID: 26457534