The role of choline in epigenetic programming of somatic and mental health during fetal development and prevention of obstetric complications

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Abstract

The metabolism of choline and its metabolites plays one of the key roles in embryogenesis: phosphatidylcholine is a component of the cell membrane, acetylcholine plays the role of a neurotransmitter, betaine is involved in the metabolism of homocysteine, and dimethylglycine is involved in the processes of mitochondrial respiration. Choline deficiency can cause liver, kidney, pancreatic dysfunction and cognitive impairment. It has been shown that an increase in the choline content in the diet of pregnant women leads to an increase in the cognitive abilities of offspring, which is associated with the normalization of DNA methylation processes. It has been found that only 1 out of 11 pregnant women receives the required amount of choline from food, so an additional 550 mg of choline daily is recommended for pregnant women.

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About the authors

Natalya I. Tapilskaya

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology

Author for correspondence.
Email: tapnatalia@mail.ru
ORCID iD: 0000-0001-5309-0087
SPIN-code: 3605-0473
ResearcherId: A-7504-2016

Dr. Sci. (Med.), Professor, Head of the Department of Reproduction

Russian Federation, St. Petersburg

T. S. Zhernakova

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology

Email: tapnatalia@mail.ru
ORCID iD: 0000-0002-5131-4363
Russian Federation, St. Petersburg

O. N. Bespalova

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology

Email: tapnatalia@mail.ru
ORCID iD: 0000-0002-6542-5953
SPIN-code: 4732-8089
ResearcherId: D-3880-2018
Russian Federation, St. Petersburg

Yu. R. Ryzhov

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology

Email: tapnatalia@mail.ru
ORCID iD: 0000-0002-5073-8279
SPIN-code: 8320-1234
ResearcherId: HZK-6150-2023
Russian Federation, St. Petersburg

R. I. Glushakov

S. M. Kirov Military Medical Academy

Email: tapnatalia@mail.ru
ORCID iD: 0000-0002-0161-5977
Russian Federation, St. Petersburg

References

  1. Geldenhuys W.J., Allen D.D. The blood-brain barrier choline transporter. Cent Nerv Syst Agents Med Chem. 2012;12(2):95–9. doi: 10.2174/187152412800792670.
  2. Wallace T.C., Blusztajn J.K., Caudill M.A., et al. Choline: The Neurocognitive Essential Nutrient of Interest to Obstetricians and Gynecologists. J Diet Suppl. 2020;17(6):733–52. doi: 10.1080/19390211.2019.1639875.
  3. Nakamura A., Suzuki Y., Umegaki H., et al. Dietary restriction of choline reduces hippocampal acetylcholine release in rats: in vivo microdialysis study. Brain Res Bull. 2001;56(6):593–97. doi: 10.1016/s0361-9230(01)00732-8.
  4. Cam B., Sagdilek E., Yildirim N., Savci V. Cytidine 5’-diphosphocholine differentially affects hemostatic parameters in diverse conditions in rats: an investigation via thromboelastography. Shock. 2015;43(4):387–94. doi: 10.1097/SHK.0000000000000301.
  5. Bye L.J., Finol-Urdaneta R.K., Tae H.S., Adams D.J. Nicotinic acetylcholine receptors: Key targets for attenuating neurodegenerative diseases. Int J Biochem Cell Biol. 2023;157:106387. doi: 10.1016/j.biocel.2023.106387.
  6. Mechawar N., Cozzari C., Descarries L. Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J Comp Neurol. 2000;428(2):305–18. doi: 10.1002/1096-9861(20001211)428:2<305:: aid-cne9>3.0.co;2-y.
  7. Smiley J.F., Subramanian M., Mesulam M.M. Monoaminergic-cholinergic interactions in the primate basal forebrain. Neuroscience. 1999;93(3):817–29. doi: 10.1016/s0306-4522(99)00116-5.
  8. Bruel-Jungerman E., Lucassen P.J., Francis F. Cholinergic influences on cortical development and adult neurogenesis. Behav Brain Res. 2011;221(2):379–88. doi: 10.1016/j.bbr.2011.01.021.
  9. McCann J.C., Hudes M., Ames B.N. An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring. Neurosci Biobehav Rev. 2006;30(5):696–712. doi: 10.1016/j.neubiorev.2005.12.003.
  10. Cheng Q., Yakel J.L. The effect of α7 nicotinic receptor activation on glutamatergic transmission in the hippocampus. Biochem Pharmacol. 2015;97(4):439–44. doi: 10.1016/j.bcp.2015.07.015.
  11. Valentine G., Sofuoglu M. Cognitive Effects of Nicotine: Recent Progress. Curr Neuropharmacol. 2018;16(4):403–14. doi: 10.2174/1570159X15666171103152136.
  12. Srivareerat M., Tran T.T., Salim S., et al. Chronic nicotine restores normal Aβ levels and prevents short-term memory and E-LTP impairment in Aβ rat model of Alzheimer’s disease. Neurobiol Aging. 2011;32(5):834–44. doi: 10.1016/j.neurobiolaging.2009.04.015.
  13. Nery A.A., Magdesian M.H., Trujillo C.A., et al. Rescue of amyloid-Beta-induced inhibition of nicotinic acetylcholine receptors by a peptide homologous to the nicotine binding domain of the alpha 7 subtype. PLoS One. 2013;8(7):e67194. doi: 10.1371/journal.pone.0067194.
  14. Marrs T.C., Maynard R.L. Neurotranmission systems as targets for toxicants: a review. Cell Biol Toxicol. 2013;29(6):381–96. doi: 10.1007/s10565-013-9259-9.
  15. Yanai J., Ben-Shaanan T.L., Haimovitch H., et al. Mechanism-based approaches for the reversal of drug neurobehavioral teratogenicity. Ann N Y Acad Sci. 2006;1074:659–71. doi: 10.1196/annals.1369.066.
  16. Steingart R.A., Abu-Roumi M., Newman M.E., et al. Neurobehavioral damage to cholinergic systems caused by prenatal exposure to heroin or phenobarbital: cellular mechanisms and the reversal of deficits by neural grafts. Brain Res Dev Brain Res. 2000;122(2):125–33. doi: 10.1016/s0165-3806(00)00063-8.
  17. Du J., Zhang P., Luo J., et al. Dietary betaine prevents obesity through gut microbiota-drived microRNA-378a family. Gut Microbes. 2021;13(1):1–19. doi: 10.1080/19490976.2020.1862612.
  18. Ismaeel A. Effects of Betaine Supplementation on Muscle Strength and Power: A Systematic Review. J Strength Cond Res. 2017;31(8):2338–46. doi: 10.1519/JSC.0000000000001959.
  19. Hsieh C.P., Chen H., Chan M.H., et al. N,N-dimethylglycine prevents toluene-induced impairment in recognition memory and synaptic plasticity in mice. Toxicology. 2020;446:152613. doi: 10.1016/j.tox.2020.152613.
  20. Imbard A., Benoist J.F., Blom H.J. Neural tube defects, folic acid and methylation. Int J Environ Res Public Health. 2013;10(9):4352–89. doi: 10.3390/ijerph10094352.
  21. Clare C.E., Brassington A.H., Kwong W.Y., Sinclair K.D. One-Carbon Metabolism: Linking Nutritional Biochemistry to Epigenetic Programming of Long-Term Development. Annu Rev Anim Biosci. 2019;7:263–87. doi: 10.1146/annurev-animal-020518-115206.
  22. Ding Y., Li J., Liu S., et al. DNA hypomethylation of inflammation-associated genes in adipose tissue of female mice after multigenerational high fat diet feeding. Int J Obes (Lond). 2014;38(2):198–204. doi: 10.1038/ijo.2013.98.
  23. Liu H.Y., Liu S.M., Zhang Y.Z. Maternal Folic Acid Supplementation Mediates Offspring Health via DNA Methylation. Reprod Sci. 2020;27(4):963–76. doi: 10.1007/s43032-020-00161-2.
  24. Caudill M.A. Pre- and postnatal health: evidence of increased choline needs. J Am Diet Assoc. 2010;110(8):1198–206. doi: 10.1016/j.jada.2010.05.009.
  25. Derbyshire E., Obeid R. Choline, Neurological Development and Brain Function: A Systematic Review Focusing on the First 1000 Days. Nutrients. 2020;12(6):1731. doi: 10.3390/nu12061731.
  26. Fisher M.C., Zeisel S.H., Mar M.H., Sadler T.W. Inhibitors of choline uptake and metabolism cause developmental abnormalities in neurulating mouse embryos. Teratology. 2001;64(2):114–22. doi: 10.1002/tera.1053.
  27. Signore C., Ueland P.M., Troendle J., Mills JL. Choline concentrations in human maternal and cord blood and intelligence at 5 y of age. Am J Clin Nutr. 2008;87(4):896–902. doi: 10.1093/ajcn/87.4.896.
  28. Wallace T.C., Fulgoni V.L. Usual Choline Intakes Are Associated with Egg and Protein Food Consumption in the United States. Nutrients. 2017;9(8):839. doi: 10.3390/nu9080839.
  29. AMA Wire AMA Backs Global Health Experts in Calling Infertility a Disease. [(accessed on 10 June 2019)]. Available online: https://wire.ama-assn.org/ama-news/ama-backs-global-health-experts-calling-infertility- disease
  30. Bekdash R.A. Early Life Nutrition and Mental Health: The Role of DNA Methylation. Nutrients. 2021;13(9):3111. doi: 10.3390/nu13093111.
  31. Fisher M.C., Zeisel S.H., Mar M.H., Sadler T.W. Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. FASEB J. 2002;16(6):619–21. doi: 10.1096/fj.01-0564fje.
  32. Niculescu M.D., Zeisel S.H. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr. 2002;132(8 Suppl):2333S–5S. doi: 10.1093/jn/132.8.2333S.
  33. Ash J.A., Velazquez R., Kelley C.M., et al. Maternal choline supplementation improves spatial mapping and increases basal forebrain cholinergic neuron number and size in aged Ts65Dn mice. Neurobiol Dis. 2014;70:32–42. doi: 10.1016/j.nbd.2014.06.001.
  34. Mehedint M.G., Craciunescu C.N., Zeisel S.H. Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus. Proc Natl Acad Sci U S A. 2010;107(29):12834–39. doi: 10.1073/pnas.0914328107.
  35. Wu B.T., Dyer R.A., King D.J., et al. Early second trimester maternal plasma choline and betaine are related to measures of early cognitive development in term infants. PLoS One. 2012;7(8):e43448. doi: 10.1371/journal.pone.0043448.
  36. Borge T.C., Aase H., Brantsæter A.L., Biele G. The importance of maternal diet quality during pregnancy on cognitive and behavioural outcomes in children: a systematic review and meta-analysis. BMJ Open. 2017;7(9):e016777. doi: 10.1136/bmjopen-2017-016777.
  37. Caudill M.A., Strupp B.J., Muscalu L., et al. Maternal choline supplementation during the third trimester of pregnancy improves infant information processing speed: a randomized, double-blind, controlled feeding study. FASEB J. 2018;32(4):2172–80. doi: 10.1096/fj.201700692RR.
  38. Bahnfleth C.L., Strupp B.J., Caudill M.A., Canfield R.L. Prenatal choline supplementation improves child sustained attention: A 7-year follow-up of a randomized controlled feeding trial. FASEB J. 2022;36(1):e22054. doi: 10.1096/fj.202101217R.
  39. Shaw G.M., Finnell R.H., Blom H.J., et al. Choline and risk of neural tube defects in a folate-fortified population. Epidemiology. 2009;20(5):714–19. doi: 10.1097/EDE.0b013e3181ac9fe7.
  40. D’Souza S.W., Glazier J.D. Homocysteine Metabolism in Pregnancy and Developmental Impacts. Front Cell Dev Biol. 2022;10:802285. doi: 10.3389/fcell.2022.802285.
  41. Zeisel S.H., da Costa K.-A. Choline: An Essential Nutrient for Public Health. Nutr Rev. 2009;67(11):615–23. doi: 10.1111/j.1753-4887.2009.00246.x.
  42. Korsmo H.W., Jiang X., Caudill M.A. Choline: Exploring the Growing Science on Its Benefits for Moms and Babies. Nutrients. 2019;11(8):1823. doi: 10.3390/nu11081823.

Supplementary files

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2. Fig.1. Interrelation of cycles of metabolism of folic acid and choline as donors of methyl groups

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