Prenatal choline availability modulates hippocampal and cerebral cortical gene expression

FASEB Journal

Volumn 21, Issue 7, 2007, Pages 1311-1323

  Mellott, Tiffany J ^a   Follettie, Maximillian T ^b   Diesl, Veronica ^b   Hill, Andrew A ^b   Lopez Coviella, Ignacio ^a   Blusztajn, Jan Krzysztof ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

Author keywords

Development; Memory; Microarray; Nutrition; Pregnancy

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR 1C; 4 AMINOBUTYRIC ACID B RECEPTOR 1D; CHOLINE; EARLY GROWTH RESPONSE FACTOR 1; MESSENGER RNA; OLIGONUCLEOTIDE; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA2; SOMATOMEDIN B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZIF268; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; FEMALE; FETUS; FRONTAL CORTEX; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOBLOTTING; MICROARRAY ANALYSIS; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PRENATAL PERIOD; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CEREBRAL CORTEX; CHOLINE; CHOLINE DEFICIENCY; DIET; DNA PRIMERS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

RATTUS;

EID: 34247602513     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-6597com     Document Type: Article

References (98)

1. McCann, J. C., Hudes, M., and Ames, B. N. (2006) An overview of evidence for a causal relationship between dietary availability of choline during development and cognitive function in offspring. Neurosci. Biobehav. Rev. 30, 696-712
2. Blusztajn, J. K. (1998) Choline, a vital amine. Science 281, 794-795
3. Zeisel, S. H. Nutritional importance of choline for brain development. J. Am. Coll. Nutr. 23, 621S-626S 2004
4. Zeisel, S. H. (2006) Choline: Critical role during fetal development and dietary requirements in adults. Annu. Rev. Nutr. 26, 229-250
5. Klose, R. J., and Bird, A. P. (2006) Genomic DNA methylation: the mark and its mediators. Trends. Biochem. Sci. 31, 89-97
6. Meck, W. H., and Williams, C. L. (1997) Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport 8, 3045-3051
7. Meck, W. H., Smith, R. A., and Williams, C. L. (1988) Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev. Psychobiol. 21, 339-353
8. Williams, C. L., Meck, W. H., Heyer, D., and Loy, R. (1998) Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain. Res. 794, 225-238
9. Albright, C. D., Tsai, A. Y., Friedrich, C. B., Mar, M. H., and Zeisel, S. H. (1999) Choline availability alters embryonic development of the hippocampus and septum in the rat. Dev. Brain. Res. 113, 13-20
10. Albright, C. D., Friedrich, C. B., Brown, E. C., Mar, M. H., and Zeisel, S. H. (1999) Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Dev. Brain. Res. 115, 123-129
11. Craciunescu, C. N., Albright, C. D., Mar, M. H., Song, J., and Zeisel, S. H. (2003) Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J. Nutr. 133, 3614-3618
12. Cermak, J. M., Holler, T., Jackson, D. A., and Blusztajn, J. K. (1998) Prenatal availability of choline modifies development of the hippocampal cholinergic system. FASEB J. 12, 349-357
13. Fibiger, H. C. (1991) Cholinergic mechanisms in learning, memory and dementia: A review of recent evidence. Trends Neurosci. 14, 220-223
14. Mellott, T. J., Williams, C. L., Meck, W. H., and Blusztajn, J. K. (2004) Prenatal choline supplementation advances hippocampal development and enhances MAPK and CREB activation. FASEB J. 18, NIL412-NIL427
15. Jones, J. P. H. M. eck, W., Williams, C. L., Wilson, W. A., and Swartzwelder, H. S. (1999) Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Dev. Brain. Res. 118, 159-167
16. Pyapali, G. K., Turner, D. A., Williams, C. L., Meck, W. H., and Swartzwelder, H. S. (1998) Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J. Neurophysiol. 79, 1790-1796
17. Montoya, D., and Swartzwelder, H. S. (2000) Prenatal choline supplementation alters hippocampal N-methyl-d-aspartate receptor-mediated neurotransmission in adult rats. Neurosci. Lett. 296, 85-88
18. Bieri, J. G., Stoewsand, G. S., Briggs, G. M., Phillips, R. W., Woodard, J. C., and Kanapka, J. J. (1977) Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. J. Nutr. 107, 1340-1348
19. Bieri, J. G. (1980) Second report of the ad hoc committee on standards for nutritional studies. J. Nutr. 110, 1726
20. Chomczynski, P., and Sacchi, N. (1987) Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
21. Byrne, M. C., Whitley, M. Z., and Follettie, M. T. (2000) Preparation of mRNA for expression monitoring. In Current Protocols in Molecular Biology (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. D., Smith, J. A., and Struhl, K., eds) pp. 22.22.21-22.22.13, John Wiley and Sons, New York, USA
22. Hill, A. A., Brown, E. L., Whitley, M. Z., Tucker-Kellogg, G., Hunter, C. P., and Slonim, D. K. (2001) Evaluation of normalization procedures for oligonucleotide array data based on spiked cRNA controls. Genome Biol. 2, RESEARCH0055
23. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B. 57, 289-300
24. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95, 14863-14868
25. Goldenring, J. R., and DeLorenzo, R. J. (1986) Phosphorylation of MAP-2 at distinct sites by calmodulin- and cyclic AMP-dependent kinases. Ann. N. Y. Acad. Sci. 466, 457-459
26. Goldenring, J. R., Gonzalez, B., McGuire, J. S., Jr., and De-Lorenzo, R. J. (1983) Purification and characterization of a calmodulin-dependent kinase from rat brain cytosol able to phosphorylate tubulin and microtubule-associated proteins. J. Biol. Chem. 258, 12632-12640
27. Enslen, H., and Soderling, T. R. (1994) Roles of calmodulin-dependent protein kinases and phosphatase in calcium-dependent transcription of immediate early genes. J. Biol. Chem. 269, 20872-20877
28. Barria, A., Muller, D., Derkach, V., Griffith, L. C., and Soderling, T. R. (1997) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042-2045
29. Ochiishi, T., Terashima, T., and Yamauchi, T. (1994) Specific distribution of Ca2/calmodulin-dependent protein kinase II alpha and beta isoforms in some structures of the rat forebrain. Brain. Res. 659, 179-193
30. Mayford, M., Bach, M. E., Huang, Y. Y., Wang, L., Hawkins, R. D., and Kandel, E. R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science 274, 1678-1683
31. Silva, A. J., Wang, Y., Paylor, R., Wehner, J. M., Stevens, C. F., and Tonegawa, S. (1992) Alpha calcium/calmodulin kinase II mutant mice: deficient long-term potentiation and impaired spatial learning. Cold. Spring. Harb. Symp. Quant. Biol. 57, 527-539
32. Silva, A. J., Stevens, C. F., Tonegawa, S., and Wang, Y. (1992) Deficient hippocampal long-term potentiation in alpha-calciumcalmodulin kinase II mutant mice. Science 257, 201-206
33. Silva, A. J., Paylor, R., Wehner, J. M., and Tonegawa, S. (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 206-211
34. Glazewski, S., Chen, C. M., Silva, A., and Fox, K. (1996) Requirement for alpha-CaMKII in experience-dependent plasticity of the barrel cortex. Science 272, 421-423
35. Gordon, J. A., Cioffi, D., Silva, A. J., and Stryker, M. P. (1996) Deficient plasticity in the primary visual cortex of alpha-calcium/ calmodulin-dependent protein kinase II mutant mice. Neuron 17, 491-499
36. Giese, K. P., Fedorov, N. B., Filipkowski, R. K., and Silva, A. J. (1998) Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 279, 870-873
37. Chapman, P. F., Frenguelli, B. G., Smith, A., Chen, C. M., and Silva, A. J. (1995) The alpha-Ca2+/calmodulin kinase II: a bidirectional modulator of presynaptic plasticity. Neuron 14, 591-597
38. Benfenati, F., Valtorta, F., Rubenstein, J. L., Gorelick, F. S., Greengard, P., and Czernik, A. J. (1992) Synaptic vesicle-associated Ca2/calmodulin-dependent protein kinase II is a binding protein for synapsin I. Nature 359, 417-420
39. Fink, C. C., Bayer, K. U., Myers, J. W., Ferrell, J. E., Jr., Schulman, H., and Meyer, T. (2003) Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 39, 283-297
40. Ono, Y., Kikkawa, U., Ogita, K., Fujii, T., Kurokawa, T., Asaoka, Y., Sekiguchi, K., Ase, K., Igarashi, K., and Nishizuka, Y. (1987) Expression and properties of two types of protein kinase C: alternative splicing from a single gene. Science 236, 1116-1120
41. Paola, D., Domenicotti, C., Nitti, M., Vitali, A., Borghi, R., Cottalasso, D., Zaccheo, D., Odetti, P., Strocchi, P., Marinari, U. M., et al. (2000) Oxidative stress induces increase in intracellular amyloid beta-protein production and selective activation of betaI and betaII PKCs in NT2 cells. Biochem. Biophys. Res. Commun. 268, 642-646
42. Cardell, M., and Wieloch, T. (1993) Time course of the translocation and inhibition of protein kinase C during complete cerebral ischemia in the rat. J. Neurochem. 61, 1308-1314
43. Weeber, E. J., Atkins, C. M., Selcher, J. C., Varga, A. W., Mirnikjoo, B., Paylor, R., Leitges, M., and Sweatt, J. D. (2000) A role for the beta isoform of protein kinase C in fear conditioning. J. Neurosci. 20, 5906-5914
44. Ikarashi, Y., Yuzurihara, M., Takahashi, A., Hirohisa, I., Shiobara, T., and Maruyama, Y. (1999) Modulation of acetylcholine release via GABAA and GABAB receptors in rat striatum. Brain. Res. 816, 238-240
45. Nava, F., Carta, G., Bortolato, M., and Gessa, G. L. (2001) gamma-Hydroxybutyric acid and baclofen decrease extracellular acetylcholine levels in the hippocampus via GABA(B) receptors. Eur. J. Pharmacol. 430, 261-263
46. Wayman, G. A., Kaech, S., Grant, W. F., Davare, M., Impey, S., Tokumitsu, H., Nozaki, N., Banker, G., and Soderling, T. R. (2004) Regulation of axonal extension and growth cone motility by calmodulin-dependent protein kinase I. J. Neurosci. 24, 3786-3794
47. Schmitt, J. M., Guire, E. S., Saneyoshi, T., and Soderling, T. R. (2005) Calmodulin-dependent kinase kinase/calmodulin kinase I activity gates extracellular-regulated kinase-dependent long-term potentiation. J. Neurosci. 25, 1281-1290
48. Fazeli, M. S., Corbet, J., Dunn, M. J., Dolphin, A. C., and Bliss, T. V. (1993) Changes in protein synthesis accompanying longterm potentiation in the dentate gyrus in vivo. J. Neurosci. 13, 1346-1353
49. Davis, S., and Laroche, S. (1998) A molecular biological approach to synaptic plasticity and learning. C. R. Acad. Sci. III 321, 97-107
50. Milbrandt, J. (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238, 797-799
51. Lemaire, P., Revelant, O., Bravo, R., and Charnay, P. (1988) Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc. Natl. Acad. Sci. U. S. A. 85, 4691-4695
52. O'Donovan, K. J., Tourtellotte, W. G., Millbrandt, J., and Baraban, J. M. (1999) The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends. Neurosci. 22, 167-173
53. Jones, M. W., Errington, M. L., French, P. J., Fine, A., Bliss, T. V., Garel, S., Charnay, P., Bozon, B., Laroche, S., and Davis, S. (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4, 289-296
54. Hall, J., Thomas, K. L., and Everitt, B. J. (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 3, 533-535
55. Miyashita, Y., Kameyama, M., Hasegawa, I., and Fukushima, T. (1998) Consolidation of visual associative long-term memory in the temporal cortex of primates. Neurobiol. Learn. Mem. 70, 197-211
56. Bozon, B., Davis, S., and Laroche, S. (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40, 695-701
57. DeChiara, T. M., Robertson, E. J., and Efstratiadis, A. (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849-859
58. Rappolee, D. A., Sturm, K. S., Behrendtsen, O., Schultz, G. A., Pedersen, R. A., and Werb, Z. (1992) Insulin-like growth factor II acts through an endogenous growth pathway regulated by imprinting in early mouse embryos. Genes Dev. 6, 939-952
59. Holley, S. J., Hall, S. B., and Mellon, P. L. (2002) Complementary expression of IGF-II and IGFBP-5 during anterior pituitary development. Dev. Biol. 244, 319-328
60. Gonzalez-Parra, S., Rosato, R. R., Chowen, J. A., Argente, J., Groffen, C., Dits, N., and Drop, S. L. (2002) Inverse correlation between insulin-like growth factor (IGF)-binding protein-5 and IGF-I and II during postnatal development of the anterior pituitary gland. Horm. Res. 57, 10-14
61. Konishi, Y., Takahashi, K., Chui, D. H., Rosenfeld, R. G., Himeno, M., and Tabira, T. (1994) Insulin-like growth factor II promotes in vitro cholinergic development of mouse septal neurons: comparison with the effects of insulin-like growth factor I. Brain. Res. 649, 53-61
62. Kar, S., Seto, D., Dore, S., Hanisch, U., and Quirion, R. (1997) Insulin-like growth factors-I and -II differentially regulate endogenous acetylcholine release from the rat hippocampal formation. Proc. Natl. Acad. Sci. U. S. A. 94, 14054-14059
63. Meck, W. H., and Williams, C. L. (1999) Choline supplementation during prenatal development reduces proactive interference in spatial memory. Dev. Brain. Res. 118, 51-59
64. Niculescu, M. D., Craciunescu, C. N., and Zeisel, S. H. (2005) Gene expression profiling of choline-deprived neural precursor cells isolated from mouse brain. Brain Res. Mol. Brain. Res. 134, 309-322
65. Feil, R. (2006) Environmental and nutritional effects on the epigenetic regulation of genes. Mutat. Res. 600, 46-57
66. Locker, J., Reddy, T. V., and Lombardi, B. (1986) DNA methylation and hepatocarcinogenesis in rats fed a choline-devoid diet. Carcinogenesis 7, 1309-1312
67. Niculescu, M. D., Craciunescu, C. N., and Zeisel, S. H. (2006) Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. FASEB J. 20, 43-49
68. Tsujiuchi, T., Tsutsumi, M., Sasaki, Y., Takahama, M., and Konishi, Y. (1999) 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. 90, 909-913
69. Wainfan, E., Dizik, M., Stender, M., and Christman, J. K. (1989) Rapid appearance of hypomethylated DNA in livers of rats fed cancer-promoting, methyl-deficient diets. Cancer Res. 49, 4094-4097
70. Robertson, K. D., and Wolffe, A. P. (2000) DNA methylation in health and disease. Nat. Rev. Genet. 1, 11-19
71. Tucker, K. L. (2001) Methylated cytosine and the brain: a new base for neuroscience. Neuron 30, 649-652
72. Reinhart, B., Eljanne, M., and Chaillet, J. R. (2002) Shared role for differentially methylated domains of imprinted genes. Mol. Cell. Biol. 22, 2089-2098
73. Paulsen, M., and Ferguson-Smith, A. C. (2001) DNA methylation in genomic imprinting, development, and disease. J. Pathol. 195, 97-110
74. Li, E. (2002) Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662-673
75. Murrell, A., Heeson, S., Bowden, L., Constancia, M., Dean, W., Kelsey, G., and Reik, W. (2001) An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO. Rep. 2, 1101-1106
76. Eden, S., Constancia, M., Hashimshony, T., Dean, W., Goldstein, B., Johnson, A. C., Keshet, I., Reik, W., and Cedar, H. (2001) An upstream repressor element plays a role in Igf2 imprinting. EMBO J. 20, 3518-3525
77. Albright, C. D., Siwek, D. F., Craciunescu, C. N., Mar, M. H., Kowall, N. W., Williams, C. L., and Zeisel, S. H. (2003) Choline availability during embryonic development alters the localization of calretinin in developing and aging mouse hippocampus. Nutr. Neurosci. 6, 129-134
78. A receptor function in mouse brain. J. Pharmacol. Exp. Ther. 248, 1-6
79. Albright, C. D., Siwek, D. F., Craciunescu, C. N., Mar, M. H., Kowall, N. W., Williams, C. L., and Zeisel, S. H. (2003) Choline availability during embryonic development alters the localization of calretinin in developing and aging mouse hippocampus. Nutr. Neurosci. 6, 129-134
80. Isomoto, S., Kaibara, M., Sakurai-Yamashita, Y., Nagayama, Y., Uezono, Y., Yano, K., and Taniyama, K. (1998) Cloning and tissue distribution of novel splice variants of the rat GABAB receptor. Biochem. Biophys. Res. Commun. 253, 10-15
81. He, X. B., Hu, J. H., Wu, Q., Yan, Y. C., and Koide, S. S. (2001) Identification of GABA(B) receptor in rat testis and sperm. Biochem. Biophys. Res. Commun. 283, 243-247
82. Mohler, H., Benke, D., and Fritschy, J. M. (2001) GABA(B)-receptor isoforms molecular architecture and distribution. Life. Sci. 68, 2297-2300
83. Pfaff, T., Malitschek, B., Kaupmann, K., Prezeau, L., Pin, J. P., Bettler, B., and Karschin, A. (1999) Alternative splicing generates a novel isoform of the rat metabotropic GABA(B)R1 receptor. Eur. J. Neurosci. 11, 2874-2882
84. Schwarz, D. A., Barry, G., Eliasof, S. D., Petroski, R. E., Conlon, P. J., and Maki, R. A. (2000) Characterization of gamma-aminobutyric acid receptor GABAB(1e), a GABAB(1) splice variant encoding a truncated receptor. J. Biol. Chem. 275, 32174-32181
85. Wei, K., Eubanks, J. H., Francis, J., Jia, Z., and Snead, O. C., III (2001) Cloning and tissue distribution of a novel isoform of the rat GABA(B)R1 receptor subunit. Neuroreport 12, 833-837
86. Wei, K., Jia, Z., Wang, Y. T., Yang, J., Liu, C. C., and Snead, O. C., III (2001) Cloning and characterization of a novel variant of rat GABA(B)R1 with a truncated C-terminus. Brain Res. Mol. Brain Res. 89, 103-110
87. Charles, K. J., Evans, M. L., Robbins, M. J., Calver, A. R., Leslie, R. A., and Pangalos, M. N. (2001) Comparative immunohistochemical localisation of GABA(B1a), GABA(B1b) and GABA(B2) subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 106, 447-467
88. Clark, S. E., Garret, M., and Platt, B. (2001) Postnatal alterations of GABA receptor profiles in the rat superior colliculus. Neuroscience. 104, 441-454
89. Fritschy, J. M., Meskenaite, V., Weinmann, O., Honer, M., Benke, D., and Mohler, H. (1999) GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur. J. Neurosci. 11, 761-768
90. Zhang, J., Chrysis, D., and Underwood, L. E. (1998) Reduction of hepatic insulin-like growth factor I (IGF-I) messenger ribonucleic acid (mRNA) during fasting is associated with diminished splicing of IGF-I pre-mRNA and decreased stability of cytoplasmic IGF-I mRNA. Endocrinology 139, 4523-4530
91. Amir-Ahmady, B., and Salati, L. M. (2001) Regulation of the processing of glucose-6-phosphate dehydrogenase mRNA by nutritional status. J. Biol. Chem. 276, 10514-10523
92. Oomizu, S., Boyadjieva, N., and Sarkar, D. K. (2003) Ethanol and estradiol modulate alternative splicing of dopamine D2 receptor messenger RNA and abolish the inhibitory action of bromocriptine on prolactin release from the pituitary gland. Alcohol. Clin. Exp. Res. 27, 975-980
93. Honse, Y., Nixon, K. M., Browning, M. D., and Leslie, S. W. (2003) Cell surface expression of NR1 splice variants and NR2 subunits is modified by prenatal ethanol exposure. Neuroscience 122, 689-698
94. Kumari, M. (2001) Differential effects of chronic ethanol treatment on N-methyl-d-aspartate R1 splice variants in fetal cortical neurons. J. Biol. Chem. 276, 29764-29771
95. Petrie, J., Sapp, D. W., Tyndale, R. F., Park, M. K., Fanselow, M., and Olsen, R. W. (2001) Altered gabaa receptor subunit and splice variant expression in rats treated with chronic intermittent ethanol. Alcohol. Clin. Exp. Res. 25, 819-828
96. Zeisel, S. H., Mar, M. H., Zhou, Z. W., and Da Costa, K. A. (1995) Pregnancy and lactation are associated with diminished concentrations of choline and its metabolites in rat liver. J. Nutr. 125, 3049-3054
97. Garner, S. C., Mar, M. H., and Zeisel, S. H. (1995) Choline distribution and metabolism in pregnant rats and fetuses are influenced by the choline content of the maternal diet. J. Nutr. 125, 2851-2858
98. FNB (1998) Dietary Reference Intakes for Thiamin, Riboflavin, Niacin, Vitamin B6, Folate, Fitamin B12, Panthotenic Acid, Biotin, and Choline, National Academy Press, Washington, D.C.