The supply of choline is important for fetal progenitor cells

Seminars in Cell and Developmental Biology

Volumn 22, Issue 6, 2011, Pages 624-628

  Zeisel, Steven H ^a  

^a The University of North Carolina at Chapel Hill   (United States)

Author keywords

Angiogenesis; Choline; DNA methylation; Epigenetic; Neurogenesis

Indexed keywords

CHOLINE;

CELL METABOLISM; DIETARY INTAKE; EPIGENETICS; FETUS CELL; HUMAN; MATERNAL NUTRITION; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEURAL TUBE DEFECT; NONHUMAN; PREGNANT WOMAN; REVIEW;

RODENTIA;

EID: 80054732655     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2011.06.002     Document Type: Review

References (85)

1. Oppenheim R.W. Cell death during the development of the nervous system. Ann Rev Neurosci 1991, 14:453-501.
2. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 1995, 267:1456-1462.
3. Merry D., Korsmeyer S. Bcl-2 gene family in the nervous system. Annu Rev Neurosci 1997, 20:245-267.
4. Zeisel S.H. Choline: critical role during fetal development and dietary requirements in adults. Annu Rev Nutr 2006, 26:229-250.
5. Mehedint M.G., Niculescu M.D., Craciunescu C.N., Zeisel S.H. Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. FASEB J 2010, 24:184-195.
6. Albright C.D., Friedrich C.B., Brown E.C., Mar M.H., Zeisel S.H. Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Res 1999, 115:123-129.
7. Albright C.D., Tsai A.Y., Friedrich C.B., Mar M.H., Zeisel S.H. Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Res 1999, 113:13-20.
8. Craciunescu C.N., Albright C.D., Mar M.H., Song J., Zeisel S.H. Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J Nutr 2003, 133:3614-3618.
9. Albright C.D., Mar M.H., Friedrich C.B., Brown E.C., Zeisel S.H. 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.
10. Niculescu M.D., Craciunescu C.N., Zeisel S.H. Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. Faseb J 2006, 20:43-49.
11. Adams K.M., Kohlmeier M., Powell M., Zeisel S.H. Nutrition in medicine: nutrition education for medical students and residents. Nutr Clin Pract 2010, 25:471-480.
12. Albright C.D., Siwek D.F., Craciunescu C.N., Mar M.H., Kowall N.W., Williams C.L., et al. Choline availability during embryonic development alters the localization of calretinin in developing and aging mouse hippocampus. Nutr Neurosci 2003, 6:129-134.
13. Albright C.D., Tsai A.Y., Mar M.-H., Zeisel S.H. Choline availability modulates the expression of TGFß1 and cytoskeletal proteins in the hippocampus of developing rat brain. Neurochem Res 1998, 23:751-758.
14. Albright C.D., Mar M.H., Craciunescu C.N., Song J., Zeisel S.H. Maternal dietary choline availability alters the balance of netrin-1 and DCC neuronal migration proteins in fetal mouse brain hippocampus. Brain Res Dev Brain Res 2005, 159:149-154.
15. Holmes-McNary M.Q., Loy R., Mar M.-H., Albright C.D., Zeisel S.H. Apoptosis is induced by choline deficiency in fetal brain and in PC12 cells. Dev Brain Res 1997, 101:9-16.
16. Yen C.L., Mar M.H., Meeker R.B., Fernandes A., Zeisel S.H. Choline deficiency induces apoptosis in primary cultures of fetal neurons. FASEB J 2001, 15:1704-1710.
17. Niculescu M.D., Craciunescu C.N., Zeisel S.H. Gene expression profiling of choline-deprived neural precursor cells isolated from mouse brain. Brain Res 2005, 134:309-322.
18. 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, 107:12834-12839.
19. Jones J.P., Meck W., Williams C.L., Wilson W.A., Swartzwelder H.S. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brain Res 1999, 118:159-167.
20. Pyapali G., Turner D., Williams C., Meck W., Swartzwelder H.S. Prenatal choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J Neurophysiol 1998, 79:1790-1796.
21. Montoya D.A., White A.M., Williams C.L., Blusztajn J.K., Meck W.H., Swartzwelder H.S. Prenatal choline exposure alters hippocampal responsiveness to cholinergic stimulation in adulthood. Brain Res Dev Brain Res 2000, 123:25-32.
22. Meck W., Williams C. Perinatal choline supplementation increases the threshold for chunking in spatial memory. Neuroreport 1997, 8:3053-3059.
23. Meck W., Williams C. Characterization of the facilitative effects of perinatal choline supplementation on timing and temporal memory. Neuroreport 1997, 8:2831-2835.
24. Meck W., Williams C. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport 1997, 8:3045-3051.
25. Meck W.H., Smith R.A., Williams C.L. Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev Psychobiol 1988, 21:339-353.
26. Meck W.H., Williams C.L. Choline supplementation during prenatal development reduces proactive interference in spatial memory. Brain Res 1999, 118:51-59.
27. Meck W.H., Williams C.L. 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.
28. Williams C.L., Meck W.H., Heyer D.D., Loy R. Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain Res 1998, 794:225-238.
29. Glenn M.J., Kirby E.D., Gibson E.M., Wong-Goodrich S.J., Mellott T.J., Blusztajn J.K., et al. Age-related declines in exploratory behavior and markers of hippocampal plasticity are attenuated by prenatal choline supplementation in rats. Brain Res 2008, 1237:110-123.
30. Thomas J.D., Biane J.S., O'Bryan K.A., O'Neill T.M., Dominguez H.D. Choline supplementation following third-trimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav Neurosci 2007, 121:120-130.
31. Thomas J.D., Garrison M., O'Neill T.M. Perinatal choline supplementation attenuates behavioral alterations associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 2004, 26:35-45.
32. Thomas J.D., O'Neill T.M., Dominguez H.D. Perinatal choline supplementation does not mitigate motor coordination deficits associated with neonatal alcohol exposure in rats. Neurotoxicol Teratol 2004, 26:223-229.
33. Ward B.C., Agarwal S., Wang K., Berger-Sweeney J., Kolodny N.H. Longitudinal brain MRI study in a mouse model of Rett Syndrome and the effects of choline. Neurobiol Dis 2008, 31:110-119.
34. Nag N., Ward B., Berger-Sweeney J.E. Nutritional factors in a mouse model of Rett syndrome. Neurosci Biobehav Rev 2009, 33:586-592.
35. Zeisel S.H. Epigenetic mechanisms for nutrition determinants of later health outcomes. Am J Clin Nutr 2009, 89:1488S-1493S.
36. Finkelstein J.D. Pathways and regulation of homocysteine metabolism in mammals. Semin Thromb Hemost 2000, 26:219-225.
37. Park E.I., Garrow T.A. Interaction between dietary methionine and methyl donor intake on rat liver betaine-homocysteine methyltransferase gene expression and organization of the human gene. J Biol Chem 1999, 274:7816-7824.
38. Gregory J.F., Cuskelly G.J., Shane B., Toth J.P., Baumgartner T.G., Stacpoole P.W., et al. Primed, constant infusion with [2H3] serine allows in vivo kinetic measurement of serine turnover, homocysteine remethylation, and transsulfuration processes in human one-carbon metabolism. Am J Clin Nutr 2000, 72:1535-1541.
39. Vance D.E., Walkey C.J., Cui Z. Phosphatidylethanolamine N-methyltransferase from liver. Biochim Biophys Acta 1997, 1348:142-150.
40. Selhub J., Seyoum E., Pomfret E.A., Zeisel S.H. Effects of choline deficiency and methotrexate treatment upon liver folate content and distribution. Cancer Res 1991, 51:16-21.
41. Varela-Moreiras G., Selhub J., da Costa K., Zeisel S.H. Effect of chronic choline deficiency in rats on liver folate content and distribution. J Nutr Biochem 1992, 3:519-522.
42. Jacob R., Jenden D., Okoji R., Allman M., Swendseid M. Choline status of men and women is decreased by low dietary folate. FASEB J 1998, 12:A512.
43. Jacob R.A., Jenden D.J., Allman-Farinelli M.A., Swendseid M.E. Folate nutriture alters choline status of women and men fed low choline diets. J Nutr 1999, 129:712-717.
44. Kim Y.-I., Miller J.W., da Costa K.-A., Nadeau M., Smith D., Selhub J., et al. Folate deficiency causes secondary depletion of choline and phosphocholine in liver. J Nutr 1995, 124:2197-2203.
45. Holliday R., Grigg G.W. DNA methylation and mutation. Mutat Res 1993, 285:61-67.
46. Suzuki M.M., Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008, 9:465-476.
47. Jeltsch A. Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem 2002, 3:382.
48. Bird A.P. CpG-rich islands and the function of DNA methylation. Nature 1986, 321:209-213.
49. Felsenfeld G., Groudine M. Controlling the double helix. Nature 2003, 421:448-453.
50. Esteve P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 2006, 20:3089-3103.
51. Quina A.S., Buschbeck M., Di Croce L. Chromatin structure and epigenetics. Biochem Pharmacol 2006, 72:1563-1569.
52. Clouaire T., Stancheva I. Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin?. Cell Mol Life Sci 2008, 65:1509-1522.
53. Niculescu M.D., Yamamuro Y., Zeisel S.H. 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.
54. Zeisel S.H., Mar M.H., Howe J.C., Holden J.M. Concentrations of choline-containing compounds and betaine in common foods. J Nutr 2003, 133:1302-1307.
55. Zeisel S.H., Mar M.-H., Howe J.C., Holden J.M. Erratum: concentrations of choline-containing compounds and betaine in common foods. J. Nutr. 2003, 133:1302-1307. J Nutr 2003;133: 2918-2919.
56. Caudill M.A. Pre- and postnatal health: evidence of increased choline needs. J Am Diet Assoc 2010, 110:1198-1206.
57. Fischer L.M., Scearce J.A., Mar M.H., Patel J.R., Blanchard R.T., Macintosh B.A., et al. Ad libitum choline intake in healthy individuals meets or exceeds the proposed adequate intake level. J Nutr 2005, 135:826-829.
58. Xu X., Gammon M.D., Zeisel S.H., Bradshaw P.T., Wetmur J.G., Teitelbaum S.L., et al. High intakes of choline and betaine reduce breast cancer mortality in a population-based study. FASEB J 2009, 23:4022-4028.
59. Bidulescu A., Chambless L.E., Siega-Riz A.M., Zeisel S.H., Heiss G. Usual choline and betaine dietary intake and incident coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study. BMC Cardiovasc Disord 2007, 7:20.
60. Shaw G.M., Carmichael S.L., Yang W., Selvin S., Schaffer D.M. Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am J Epidemiol 2004, 160:102-109.
61. Cho E., Zeisel S.H., Jacques P., Selhub J., Dougherty L., Colditz G.A., et al. Dietary choline and betaine assessed by food-frequency questionnaire in relation to plasma total homocysteine concentration in the Framingham Offspring Study. Am J Clin Nutr 2006, 83:905-911.
62. Konstantinova S.V., Tell G.S., Vollset S.E., Ulvik A., Drevon C.A., Ueland P.M. Dietary patterns, food groups, and nutrients as predictors of plasma choline and betaine in middle-aged and elderly men and women. Am J Clin Nutr 2008, 88:1663-1669.
63. Jensen H.H., Batres-Marquez S.P., Carriquiry A., Schalinske K.L. Choline in the diets of the U.S. population: NHANES, 2003-2004. FASEB J 2007, 21:lb219.
64. Fischer L.M., daCosta K., Kwock L., Stewart P., Lu T.-S., Stabler S., et al. Sex and menopausal status influence human dietary requirements for the nutrient choline. Am J Clin Nutr 2007, 85:1275-1285.
65. Resseguie M.E., da Costa K.A., Galanko J.A., Patel M., Davis I.J., Zeisel S.H. Aberrant estrogen regulation of PEMT results in choline deficiency-associated liver dysfunction. J Biol Chem 2011, 286:1649-1658.
66. da Costa K.A., Kozyreva O.G., Song J., Galanko J.A., Fischer L.M., Zeisel S.H. Common genetic polymorphisms affect the human requirement for the nutrient choline. FASEB J 2006, 20:1336-1344.
67. Kohlmeier M., da Costa K.A., Fischer L.M., Zeisel S.H. Genetic variation of folate-mediated one-carbon transfer pathway predicts susceptibility to choline deficiency in humans. Proc Natl Acad Sci U S A 2005, 102:16025-16030.
68. McMahon K.E., Farrell P.M. Measurement of free choline concentrations in maternal and neonatal blood by micropyrolysis gas chromatography. Clin Chim Acta 1985, 149:1-12.
69. Zeisel S.H., 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.
70. Sweiry J.H., Page K.R., Dacke C.G., Abramovich D.R., Yudilevich D.L. 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 Dev Physiol 1986, 8:435-445.
71. Ozarda Ilcol Y., Uncu G., Ulus I.H. Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery and in newborns. Arch Physiol Biochem 2002, 110:393-399.
72. Chao C.K., Pomfret E.A., Zeisel S.H. Uptake of choline by rat mammary-gland epithelial cells. Biochem J 1988, 254:33-38.
73. Holmes-McNary M., Cheng W.L., Mar M.H., Fussell S., Zeisel S.H. Choline and choline esters in human and rat milk and infant formulas. Am J Clin Nutr 1996, 64:572-576.
74. Zeisel S.H., Char D., Sheard N.F. Choline, phosphatidylcholine and sphingomyelin in human and bovine milk and infant formulas. J Nutr 1986, 116:50-58.
75. Yang E.K., Blusztajn J.K., Pomfret E.A., Zeisel S.H. Rat and human mammary tissue can synthesize choline moiety via the methylation of phosphatidylethanolamine. Biochem J 1988, 256:821-828.
76. Ilcol Y.O., Ozbek R., Hamurtekin E., Ulus I.H. Choline status in newborns, infants, children, breast-feeding women, breast-fed infants and human breast milk. J Nutr Biochem 2005, 16:489-499.
77. Zeisel S.H., Epstein M.F., Wurtman R.J. Elevated choline concentration in neonatal plasma. Life Sci 1980, 26:1827-1831.
78. Zeisel S.H., Wurtman R.J. Developmental changes in rat blood choline concentration. Biochem J 1981, 198:565-570.
79. Shaw G.M., Schaffer D., Velie E.M., Morland K., Harris J.A. Periconceptional vitamin use, dietary folate, and the occurrence of neural tube defects. Epidemiology 1995, 6:219-226.
80. Daly L., Kirke P., Molloy A., Weir D., Scott J. Folate levels and neural tube defects. Implications for prevention. JAMA 1995, 274:1698-1702.
81. 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, 64:114-122.
82. 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, 16:619-621.
83. Shaw G.M., Carmichael S.L., Laurent C., Rasmussen S.A. Maternal nutrient intakes and risk of orofacial clefts. Epidemiology 2006, 17:285-291.
84. Shaw G.M., Finnell R.H., Blom H.J., Carmichael S.L., Vollset S.E., Yang W., et al. Choline and risk of neural tube defects in a folate-fortified population. Epidemiology 2009, 20:714-719.
85. Shaw G.M., Finnell R.H., Blom H.J., Carmichael S.L., Vollset S.E., Yang W., et al. Choline and risk of neural tube defects in a folate-fortified population. Epidemiology 2009, epub: 10.1097/EDE.0b013e3181ac9fe7.