Perinatal choline influences brain structure and function

Nutrition Reviews

Volumn 64, Issue 4, 2006, Pages 197-203

  Zeisel, Steven H ^a   Niculescu, Mihai D ^a  

^a University of North Carolina   (United States)

Author keywords

Brain development; Choline; Folate; Hippocampus; Memory

Indexed keywords

BETAINE; CHOLINE; FOLIC ACID; HOMOCYSTEINE; METHIONINE; METHYL GROUP;

APOPTOSIS; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL PROLIFERATION; DIETARY INTAKE; DRUG EFFECT; DRUG METABOLISM; DRUG TRANSPORT; EPIGENETICS; FATTY LIVER; FETAL ALCOHOL SYNDROME; GESTATION PERIOD; HUMAN; KIDNEY FUNCTION; LACTATION; MEMBRANE; MEMORY; MUSCLE INJURY; NEURAL TUBE DEFECT; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; POSTMENOPAUSE; PREGNANCY; REVIEW; RODENT; STEM CELL; VITAMIN DEFICIENCY;

BRAIN; CHOLINE; FEMALE; FETAL DEVELOPMENT; FOLIC ACID; HUMANS; INFANT, NEWBORN; LACTATION; MALE; METHIONINE; NOOTROPIC AGENTS; PERINATAL CARE; PREGNANCY;

RODENTIA;

EID: 33645816801     PISSN: 00296643     EISSN: 00296643     Source Type: Journal    
DOI: 10.1301/nr.2006.janr.197-203     Document Type: Review

References (85)

1. Zeisel SH, Blusztajn JK. Choline and human nutrition. Ann Rev. Nutr. 1994;14:269-296.
2. Blusztajn JK, Wurtman RJ. Choline and cholinergic neurons. Science. 1983;221:614-620.
3. Niculescu MD, Zeisel SH. Diet, methyl donors and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr. 2002;132:2333S-2335S.
4. da Costa KA, Gaffney CE, Fischer LM, Zeisel SH. Choline deficiency in mice and humans is associated with increased plasma homocysteine concentration after a methionine load. Am J Clin Nutr. 2005;81:440-444.
5. da Costa KA, Badea M, Fischer LM, Zeisel SH. Elevated serum creatine phosphokinase in choline-deficient humans: mechanistic studies in C2C12 mouse myoblasts. Am J Clin Nutr. 2004;80:163-170.
6. Food and Nutrition Board, Institute of Medicine, Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Vitamin B12, Pantothenic Acid, Biotin, and Choline. Washington, DC: National Academies Press; 1998. Available online at: http://www.nap.edu/openbook/0309065542/html/. Accessed March 27, 2006.
7. Cheng W-L, Holmes-McNary MQ, Mar M-H, Lien EL, Zeisel SH. Bioavailability of choline and choline esters from milk in rat pups. J Nutr Biochem. 1996;7:457-464.
8. Holmes-McNary M, Cheng WL, Mar. MH, Fussell S, Zeisel SH. Choline and choline esters in human and rat milk and infant formulas. Am J Clin Nutr. 1996;64:572-576.
9. Fischer LM, Scearce JA, Mar MH, et al. Ad libitum choline intake in healthy individuals meets or exceeds the proposed adequate intake level. J Nutr. 2005;135:826-829.
10. Shaw GM, Carmichael SL, Yang W, Selvin S, Schaffer DM. Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am J Epidemiol. 2004;160:102-109.
11. Zhu X, Mar MH, Song J, Zeisel SH. Deletion of the Pemt gene increases progenitor cell mitosis, DNA and protein methylation and decreases calretinin expression in embryonic day 17 mouse hippocampus. Brain Res Dev Brain Res. 2004;149:121-129.
12. Blusztajn JK, Zeisel SH, Wurtman RJ. Developmental changes in the activity of phosphatidylethanolamine N-methyltransferases in rat brain. Biochem J. 1985;232:505-511.
13. Walkey CJ, Yu L, Agellon LB, Vance DE. Biochemical and evolutionary significance of phospholipid methylation. J Biol Chem. 1998;273:27043-27046.
14. -/-) mice. J Nutr. 2002;132:68-71.
15. Zhu X, Song J, Mar MH, Edwards LJ, Zeisel SH. Phosphatidylethanolamine N-methyltransferase (PEMT) knockout mice have hepatic steatosis and abnormal hepatic choline metabolite concentrations despite ingesting a recommended dietary intake of choline. Biochem J. 2003;370:987-993.
16. Finkelstein JD. Pathways and regulation of homocysteine metabolism in mammals. Semin Thromb Hemost. 2000;26:219-225.
17. Olthof MR, van Vliet T, Verhoef P, Zock PL, Katan MB. Effect of homocysteine-lowering nutrients on blood lipids: results from four randomised, placebo-controlled studies in healthy humans. PLoS Med. 2005;2:e135.
18. Weisberg IS, Jacques PF, Selhub J, et al. The 1298A->C polymorphism in methylenetetrahydrofolate reductase (MTHFR): in vitro expression and association with homocysteine. Atherosclerosis. 2001;156:409-415.
19. Shelnutt KP, Kauwell GP, Chapman CM, et al. Folate status response to controlled folate intake is affected by the methylenetetrahydrofolate reductase 677C->T polymorphism in young women. J Nutr. 2003;133:4107-1411.
20. Jacques PF, Bostom AG, Wilson PW, Rich S, Rosenberg IH, Selhub J. Determinants of plasma total homocysteine concentration in the Framingham Offspring cohort. Am J Clin Nutr. 2001;73:613-621.
21. Watkins D, Ru M, Hwang HY, et al. Hyperhomocysteinemia due to methionine synthase deficiency, cblG: structure of the MTR gene, genotype diversity, and recognition of a common mutation, P1173L. Am J Hum Genet. 2002;71:143-153.
22. Mudd SH, Ebert MH, Scriver CR. Labile methyl group balances in the human: the role of sarcosine. Metabolism. 1980;29:707-720.
23. Sunden S, Renduchintala M, Park E, Miklasz S, Garrow T. Betaine-Homocysteine methyltransferase expression in porcine and human tissues and chromosomal localization of the human gene. Arch Biochem Biophys. 1997;345:171-174.
24. Steenge GR, Verhoef P, Katan MB. Betaine supplementation lowers plasma homocysteine in healthy men and women. J Nutr. 2003;133:1291-1295.
25. Wendel U, Bremer H. Betaine in the treatment of homocystinuria due to 5,10-methylenetetrahydrofolate reductase deficiency. Eur J Pediatr. 1984;142:147-150.
26. Sweiry JH, Yudilevich DL. Characterization of choline transport at maternal and fetal interfaces of the perfused guinea-pig placenta. J Physiol. 1985;366:251-266.
27. Sweiry JH, Page KR, Dacke CG, Abramovich DR, Yudilevich DL. Evidence of saturable uptake mechanisms at maternal and fetal sides of the perfused human placenta by rapid paired-tracer dilution: studies with calcium and choline. J Devel Physiol. 1986;8:435-445.
28. McMahon KE, Farrell PM. Measurement of free choline concentrations in maternal and neonatal blood by micropyrolysis gas chromatography. Clin Chim Acta. 1985;149:1-12.
29. Zeisel SH, Mar M-H, Zhou Z-W, da Costa K-A. Pregnancy and lactation are associated with diminished concentrations of choline and its metabolites in rat liver. J Nutr. 1995;125:3049-3054.
30. Velzing-Aarts FV, Holm PI, Fokkema MR, van der Dijs FP, Ueland PM, Muskiet FA. Plasma choline and betaine and their relation to plasma homocysteine in normal pregnancy. Am J Clin Nutr. 2005;81:1383-1389.
31. Hobbs CA, Cleves MA, Melnyk S, Zhao W, James SJ. Congenital heart defects and abnormal maternal biomarkers of methionine and homocysteine metabolism. Am J Clin Nutr. 2005;81:147-153.
32. Molloy A, Mills J, Cox C, et al. Choline and homocysteine interrelations in umbilical cord and maternal plasma at delivery. Am J Clin Nutr. 2005;82:836-842.
33. Zeisel SH, Wurtman RJ. Developmental changes in rat blood choline concentration. Biochem J. 1981;198:565-570.
34. Ozarda IY, Uncu G, Ulus IH. Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery and in newborns. Arch Physiol Biochem. 2002;110:393-399.
35. Cornford EM, Cornford ME. Nutrient transport and the blood-brain barrier in developing animals. Fed Proc. 1986;45:2065-2072.
36. Garner SC, Mar M-H, Zeisel SH. Choline distribution and metabolism in pregnant rats and fetuses are influenced by the choline content of the maternal diet. J Nutr. 1995;125:2851-2858.
37. Hoffman DR, Cornatzer WE, Duerre JA. Relationship between tissue levels of S-adenosylmethionine, S-adenosylhomocysteine, and transmethylation reactions. Can J Biochem. 1979;57:56-65.
38. Fisher MC, Zeisel SH, Mar MH, Sadler TW. Inhibitors of choline uptake and metabolism cause developmental abnormalities in neurulating mouse embryos. Teratology. 2001;64:114-122.
39. Fisher MC, Zeisel SH, Mar MH, Sadler TW. Perturbations in choline metabolism cause neural tube defects in mouse embryos in vitro. FASEB J. 2002;16:619-621.
40. Centers for Disease Control. Recommendations for the use of folic acid to reduce the number of cases of spina bifida and othe neural tube defects. Morbid Mortal Wkly Rep. 1992;41:1-7.
41. MRC Vitamin Study Research Group. Prevention of neural tube defects: results of the medical Research Council Vitamin Study. Lancet. 1991;338:131-137.
42. Craciunescu CN, Albright CD, Mar MH, Song J, Zeisel SH. Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J Nutr. 2003;133:3614-3618.
43. Craciunescu CN, Brown EC, Mar MH, Albright CD, Nadeau MR, Zeisel SH. Folic acid deficiency during late gestation decreases progenitor cell proliferation and increases apoptosis in fetal mouse brain. J Nutr. 2004;134:162-166.
44. Pyapali G, Turner D, Williams C, Meck W, Swartzwelder HS. Prenatal choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J Neurophysiol. 1998;79:1790-1796.
45. Montoya DA, White AM, Williams CL, Blusztajn JK, Meck WH, Swartzwelder HS. Prenatal choline exposure alters hippocampal responsiveness to cholinergic stimulation in adulthood. Brain Res Dev Brain Res. 2000;123:25-32.
46. Jones JP, Meck W, Williams CL, Wilson WA, Swartzwelder HS. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brain Res Dev Brain Res. 1999;118:159-167.
47. Meck W, Williams C. Perinatal choline supplementation increases the threshold for chunking in spatial memory. Neuroreport. 1997;8:3053-3059.
48. Meck W, Williams C. Characterization of the facilitative effects of perinatal choline supplementation on timing and temporal memory. Neuroreport. 1997;8:2831-2835.
49. Meck W, Williams C. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport. 1997;8:3045-3051.
50. Meck WH, Smith RA, Williams CL. Organizational changes in cholinergic activity and enhanced visuo-spatial memory as a function of choline administered prenatally or postnatally or both. Behav Neurosci. 1989;103:1234-1241.
51. Meck WH, Smith RA, Williams CL. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev Psychobiol. 1988;21:339-353.
52. Meck WH, Williams CL. Choline supplementation during prenatal development reduces proactive interference in spatial memory. Brain Res Dev Brain Res. 1999;118:51-59.
53. Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH. Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Res Dev Brain Res. 1999;115:123-129.
54. Albright CD, Tsai AY, Friedrich CB, Mar MH, Zeisel SH. Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Res Dev Brain Res. 1999;113:13-20.
55. Meck WH, Williams CL. Metabolic imprinting of choline by its availability during gestation: Implications for memory and attentional processing across the lifespan. Neurosci Biobehav Rev. 2003;27:385-399.
56. Williams CL, Meck WH, Heyer DD, Loy R. Hypertrophy of basal forebrain neurons and enhanced visuo-spatial memory in perinatally choline-supplemented rats. Brain Res. 1998;794:225-238.
57. Schenk F, Brandner C. Indirect effects of peri- and postnatal choline treatment on place-learning abilities in rat. Psychobiology. 1995;23:302-313.
58. Brandner C. Perinatal choline treatment modifies the effects of a visuo-spatial attractive cue upon spatial memory in naive adult rats. Brain Res. 2002;928:85-95.
59. Ricceri L, Berger-Sweeney J. Postnatal choline supplementation in preweanling mice: sexually dimorphic behavioral and neurochemical effects. Behav Neurosci. 1998;112:1387-1392.
60. Mohler E, Meck W, Williams C. Sustained attention in adult mice is modulated by prenatal choline availability. Int J Comp Psychol. 2001;14:136-150.
61. Tees RC. The influences of rearing environment and neonatal choline dietary supplementation on spatial learning and memory in adult rats. Behav Brain Res. 1999;105:173-188.
62. Tees RC. The influences of sex, rearing environment, and neonatal choline dietary supplementation on spatial and nonspatial learning and memory in adult rats. Dev Psychobiol. 1999;35:328-342.
63. Tees RC, Mohammadi E, Adam TJ. Altering the impact of early rearing on the rat's spatial memory with pre- and postnatal choline supplementation. Soc Neurosci Abstr. 1999;17:1401.
64. Thomas JD, Garrison M, O'Neill TM. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol. 2004;26:35-45.
65. Thomas JD, O'Neill TM, Dominguez HD. Perinatal choline supplementation does not mitigate motor coordination deficits associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol. 2004;26:223-229.
66. Niculescu MD, Craciunescu CN, Zeisel SH. Gene expression profiling of choline-deprived neural precursor cells isolated from mouse brain. Brain Res Mol Brain Res. 2005;134:309-322.
67. Albright CD, Mar MH, Friedrich CB, Brown EC, Zeisel SH. Maternal choline availability alters the localization of p15Ink4B and p27Kip1 cyclin-dependent kinase inhibitors in the developing fetal rat brain hippocampus. Dev Neurosci. 2001;23:100-106.
68. Shivapurkar N, Poirier LA. Tissue levels of S-adenosylmethionine and S-adenosylhomocysteine in rats fed methyl-deficient, amino acid-defined diets for one to five weeks. Carcinogenesis. 1983;4:1051-1057.
69. Zeisel SH, Zola T, daCosta K, Pomfret EA. Effect of choline deficiency on S-adenosylmethionine and methionine concentrations in rat liver. Biochem J. 1989;259:725-729.
70. Locker J, Reddy TV, Lombardi B. DNA methylation and hepatocarcinogenesis in rats fed a choline devoid diet. Carcinogenesis. 1986;7:1309-1312.
71. Tsujiuchi T, Tsutsumi M, Sasaki Y, Takahama M, Konishi Y. Hypomethylation of CpG sites and c-myc gene overexpression in hepatocellular carcinomas, but not hyperplastic nodules, induced by a choline-deficient L-amino acid-defined diet in rats. Jpn J Cancer Res. 1999;90:909-913.
72. Holliday R, Grigg GW. DNA methylation and mutation. Mutat Res. 1993;285:61-67.
73. Jaenisch R. DNA methylation and imprinting: why bother? Trends Genet. 1997;13:323-329.
74. Jones PA, Gonzalgo ML. Altered DNA methylation and genome instability: a new pathway to cancer? Proc Natl Acad Sci U S A. 1997;94:2103-2105.
75. Robertson KD, Wolffe AP. DNA methylation in health and disease. Nat Rev Genet. 2000;1:11-19.
76. Jeltsch A. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem. 2002;3:382.
77. Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132:2393S-2400S.
78. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003;23:5293-5300.
79. Bird AP. CpG-rich islands and the function of DNA methylation. Nature. 1986;321:209-213.
80. Niculescu MD, Yamamuro Y, Zeisel SH. Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin-dependent kinase inhibitor 3 gene. J Neurochem. 2004;89:1252-1259.
81. Christman JK, Sheikhnejad G, Dizik M, Abileah S, Wainfan E. Reversibility of changes in nucleic acid methylation and gene expression induced in rat liver by severe dietary methyl deficiency. Carcinogenesis. 1993;14:551-557.
82. Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12:949-957.
83. Dani S, Hori A, Walter G, eds. Principals of Neural Aging. Amsterdam: Elsevier; 1997.
84. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999;2:266-270.
85. Markakis EA, Gage FH. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol. 1999;406:449-460.