Maternal smoking and DNA methylation abnormalities in children at early developmental stages


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The paper analyzes the results of current studies of the role of DNA methylation during human embryonic development and the effects of tobacco smoke from maternal smoking on the epigenetic status of a developing child. The molecular mechanisms mediating the association between maternal smoking and its effects on the development and health of the offspring, especially its long-term effects that manifest throughout his/her life are the object of active research in medicine and biology. Human genomics studies in recent years have shown that one of these mechanisms may be the epigenetic regulation of gene activity, namely, stable tobacco smoke-induced alterations in this system can cause concomitant smoking-related developmental and health problems. Active smoking is an important risk factor for morbidity and premature mortality, while maternal smoking during pregnancy has a double effect: firstly, it adversely affects women’s health and secondly, it leads to irreparable fetal developmental disorders and affects the health and development of the newborn and the quality of his/her subsequent life.

Full Text

Restricted Access

About the authors

Veronika V. Odintsova

National Medical Research Center of Obstetrics, Gynecology, and Perinatology named after Academician V.I. Kulakov; VU University; Saint Petersburg State University; Central Research Institute for Public Health Organization and Informatization, Ministry of Health of Russia

Email: veronika.od@gmail.com
PhD in Medicine, PhD researcher, Department of Biological Psychology; advisor

Alsu F. Saifitdinova

Saint Petersburg State University; International Center for Reproductive Medicine

Email: saifitdinova@mail.ru
Director of the Research Recourse Center “Chromas Core Facility”; Deputy Head of the Laboratory of Assisted Reproductive Technologies

Oxana Yu. Naumova

N.I. Vavilov Institute of General Genetics, Russian Academy of Sciences; University of Houston

Email: oksana.yu.naumova@gmail.com
PhD, Senior Researcher

References

  1. Fagerström К. The epidemiology of smoking: health consequences and benefits of cessation. Drugs. 2002; 62(Suppl. 2): 1-9.
  2. Lambers D.S., Clark K.E. The maternal and fetal physiologic effects of nicotine. Semin. Perinatol. 1996; 20(2): 115-26.
  3. Neuman A., Hohmann C., Orsini N., Pershagen G., Eller E., Kjaer H.F. et al.; ENRIECO Consortium. Maternal smoking in pregnancy and asthma in preschool children: a pooled analysis of eight birth cohorts. Am. J. Respir. Crit. Care Med. 2012; 186(10): 1037-43.
  4. Roza S.J., Verbürg B.O., Jaddoe V.W., Hofman A., Mackenbach J.P., Steegers E.A. et al. Effects of maternal smoking in pregnancy on prenatal brain development. The Generation R Study. Eur. J. Neurosci. 2007; 25(3): 611-7.
  5. Janssen B.G., Gyselaers W., Byun H.M., Roels H.A., Cuypers A., Baccarelli A.A., Nawrot T.S. Placental mitochondrial DNA and CYP1A1 gene methylation as molecular signatures for tobacco smoke exposure in pregnant women and the relevance for birth weight. J. Transl. Med. 2017; 15(1): 5.
  6. Banik A., Kandilya D., Ramya S., Stünkel W., Seng Chong Y., Dheen S.T. Maternal factors that induce epigenetic changes contribute to neurological disorders in offspring. Genes (Basel). 2017; 8(6). pii: E150.
  7. van Otterdijk S.D., Binder A.M., Michels K.B. Locus-specific DNA methylation in the placenta is associated with levels of pro-inflammatory proteins in cord blood and they are both independently affected by maternal smoking during pregnancy. Epigenetics. 2017; 12(10): 875-85.
  8. Meberg A., Sande H., Foss O.P., Stenwig J.T. Smoking during pregnancy--effects on the fetus and on thiocyanate levels in mother and baby. Acta Paediatr. Scand. 1979; 68(4): 547-52.
  9. Dolinoy D.C., Weidman J.R., Jirtle R.L. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod. Toxicol. 2007; 23(3): 297-307.
  10. Razin A. CpG methylation, chromatin structure and gene silencing-a three-way connection. EMBO J. 1998; 17(17): 4905-8.
  11. Escamilla-Del-Arenal M., DaRocha S.T., Heard E. Evolutionary diversity and developmental regulation of X-chromosome inactivation. Hum. Genet. 2011; 130(2): 307-27.
  12. Fazzari M.J., Greally J.M. Epigenomics: beyond CpG islands. Nat. Rev. Genet. 2004; 5(6): 446-55.
  13. Eckhardt F., Lewin J., Cortese R., Rakyan V.K., Attwood J., Burger M. et al. DNA methylation profiling of human chromosomes 6, 20 and 22. Nat. Genet. 2006; 38(12): 1378-85.
  14. Okano M., Bell D. W, Haber D.A., Li E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 1999; 99(3): 247-57.
  15. Ramchandani S., Bhattacharya S.K., Cervoni N., Szyf M. DNA methylation is a reversible biological signal. Proc. Natl. Acad. Sci. USA. 1999; 96(11): 6107-12.
  16. Efimova O.A., Pendina A.A., Tikhonov A.V., Fedorova I.D., Krapivin M.I., Chiryaeva O.G., Shilnikova E.M., Bogdanova M.A., Kogan I.Y., Kuznetzova T.V., Gzgzyan A.M., Ailamazyan E.K., Baranov V.S. Chromosome hydroxymethylation patterns in human zygotes and cleavage-stage embryos. Reproduction. 2015; 149(3): 223-33.
  17. Wu H., D’Alessio A.C., Ito S., Xia K., Wang Z., Cui K. et al. Dual functions ofTet1 in transcriptional regulation in mouse embryonic stem cells. Nature. 2011; 473(7347): 389-93.
  18. Meaney M.J., Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci. 2005; 7(2): 103-23.
  19. Naumova O.Y., Hein S., Suderman M., Barbot B., Lee M., Raefski A. et al. Epigenetic patterns modulate the connection between developmental dynamics of parenting and offspring psychosocial adjustment. Child Dev. 2016; 87(1): 98-110.
  20. Calvanese V., Lara E., Kahn A., Fraga M.F. The role of epigenetics in aging and age-related diseases. Aging Res. Rev. 2009; 8(4): 268-76.
  21. Landgrave-Gomez J., Mercado-Gomez O., Guevara-Guzmân R. Epigenetic mechanisms in neurological and neurodegenerative diseases. Front. Cell. Neurosci. 2015; 9: 58.
  22. Robertson K.D. DNA methylation and human disease. Nat. Rev. Genet. 2005; 6(8): 597-610.
  23. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007; 8(4): 253-62.
  24. Rakyan V.K., Down T.A., Balding D.J., Beck S. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet. 2011; 12(8): 529-41.
  25. Chavez L., Jozefczuk J., Grimm C., Dietrich J., Timmermann B., Lehrach H. et al. Computational analysis of genome-wide DNA methylation during the differentiation of human embryonic stem cells along the endodermal lineage. Genome Res. 2010; 20(10): 1441-50.
  26. Haaf T. Methylation dynamics in the early mammalian embryo: implications of genome reprogramming defects for development. Curr. Top. Microbiol. Immunol. 2006; 310: 13-22.
  27. Dean W. DNA methylation and demethylation: a pathway to gametogenesis and development. Mol.Reprod. Dev. 2014; 81(2): 113-25.
  28. Reik W., Surani M.A. Germline and pluripotent stem cells. Cold Spring Harb. Perspect. Biol. 2015; 7(11). pii: a019422.
  29. Breton C.V, Byun H.M., Wenten M., Pan F., Yang A., Gillil F.D. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am. J. Respir. Crit. Care Med. 2009; 180(5): 462-7.
  30. Joubert B.R., Hâberg S.E., Nilsen R.M., Wang X., Vollset S.E., Murphy S.K. et al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ. Health Perspect. 2012; 120(10): 1425-31.
  31. Tehranifar P., Wu H.C., McDonald J.A., Jasmine F., Santella R.M., Gurvich I. et al. Maternal cigarette smoking during pregnancy and offspring DNA methylation in midlife. Epigenetics. 2018; 13(2): 129-34.
  32. Rzehak P., Saffery R., Reischl E., Covic M., Wahl S., Grote V. et al.; European Childhood Obesity Trial Study Group. Maternal smoking during pregnancy and DNA-methylation in children at age 5.5 years: epigenome-wide-analysis in the European Childhood Obesity Project (CHOP)-study. PLoS One. 2016; 11(5): e0155554.
  33. Sengupta S.M., Smith A.K., Grizenko N., Joober R. Locus-specific DNA methylation changes and phenotypic variability in children with attention-deficit hyperactivity disorder. Psychiatry Res. 2017; 256: 298-304.
  34. Shorey-Kendrick L.E., McEvoy C.T., Ferguson B., Burchard J., Park B.S., Gao L. et al. Vitamin C prevents offspring DNA methylation changes associated with maternal smoking in pregnancy. Am. J. Respir. Crit. Care Med. 2017; 196(6): 745-55.
  35. Rotroff D.M., Joubert B.R., Marvel S.W., Hâberg S.E., Wu M.C., Nilsen R.M. et al. Maternal smoking impacts key biological pathways in newborns through epigenetic modification in utero. BMC Genomics. 2016; 17(1): 976.
  36. Morales E., Vilahur N., Salas L.A., Motta V., Fernandez M.F., Murcia M. et al. Genome-wide DNA methylation study in human placenta identifies novel loci associated with maternal smoking during pregnancy. Int. J. Epidemiol. 2016; 45(5): 1644-55.
  37. Suter M., Ma J., Harris A., Patterson L., Brown K.A., Shope C. Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics. 2011; 6(11): 1284-94.
  38. Joubert B.R., Felix J.F., Yousefi P., Bakulski K.M., Just A.C., Breton C. et al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis. Am. J. Hum. Genet. 2016; 98(4): 680-96.
  39. Richmond R.C., Simpkin A.J., Woodward G., Gaunt T.R., Lyttleton O., McArdle W.L. 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(8): 2201-17.
  40. Markunas C.A., Xu Z., Harlid S., Wade P.A., Lie R.T., Taylor J.A., Wilcox A.J. Identification of DNA methylation changes in newborns related to maternal smoking during pregnancy. Environ. Health Perspect. 2014; 122(10): 1147-53.
  41. Meyer K.F., Verkaik-Schäkel R.N., Timens W, KobzikL., Plösch T., Hylkema M.N. The fetal programming effect of prenatal smoking on Igflr and Igfl methylation is organ- and sex-specific. Epigenetics. 2017; 12(12): 1076-91.
  42. Chatterton Z., Hartley B.J., Seok M.H., Mendelev N., Chen S., Milekic M. et al. In utero exposure to maternal smoking is associated with DNA methylation alterations and reduced neuronal content in the developing fetal brain. Epigenetics Chromatin. 2017; 10: 4.
  43. Fa S., Larsen T.V., Bilde K., Daugaard T.F., Ernst E.H., Olesen R.H. et al. Assessment of global DNA methylation in the first trimester fetal tissues exposed to maternal cigarette smoking. Clin. Epigenetics. 2016; 8: 128.
  44. Fa S., Larsen T.V., Bilde K., Daugaard T.F., Emst E.H., Lykke-Hartmann К. et al. Changes in first trimester fetal CYP1A1 and AHRR DNA methylation and mRNA expression in response to exposure to maternal cigarette smoking. Environ. Toxicol. Pharmacol. 2017; 57: 19-27.
  45. Peters I., Vaske B., Albrecht K., Kuczyk M.A., Jonas If., Serth J. Adiposity and age are statistically related to enhanced RASSF1A tumor suppressor gene promoter methylation in normal autopsy kidney tissue. Cancer Epidemiol. Biomarkers Prev. 2007; 16(12): 2526-32.
  46. Satta R., Maloku E., Zhubi A., Pibiri E, Hajos M., Costa E., Guidotti A. Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proc. Natl. Acad. Sei. USA 2008; 105(42): 16356-61.
  47. Mann B.S., Johnson J.R., Cohen M.H., Justice R., Pazdur R. FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist. 2007; 12(10): 1247-52.
  48. Mikaelsson M.A., Miller C.A. The path to epigenetic treatment of memory disorders. Neurobiol. Learn. Mem. 2011; 96(1): 13-8.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies