Choline nutrition programs brain development via DNA and histone methylation

Central Nervous System Agents in Medicinal Chemistry

Volumn 12, Issue 2, 2012, Pages 82-94

  Blusztajn, Jan Krzysztof ^a   Mellott, Tiffany J ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brain; Choline; DNA; Histone; Memory; Methylation; Nutrition; Pregnancy

Indexed keywords

5 METHYLTETRAHYDROFOLATE HOMOCYSTEINE METHYLTRANSFERASE; 5 METHYLTETRAHYDROFOLIC ACID; ACETYLCHOLINE; ADENOSYLHOMOCYSTEINASE; CHOLINE; CHOLINE DEHYDROGENASE; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; HOMOCYSTEINE; HOMOCYSTEINE METHYLTRANSFERASE; METHIONINE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; S ADENOSYLHOMOCYSTEINE;

ARTICLE; BRAIN DEVELOPMENT; COGNITION; DNA METHYLATION; FOOD INTAKE; GENE EXPRESSION; HISTONE METHYLATION; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; NUTRIGENOMICS; NUTRITION;

EID: 84862546546     PISSN: 18715249     EISSN: 18756166     Source Type: Journal    
DOI: 10.2174/187152412800792706     Document Type: Article

References (233)

1. Strecker, A. Über einige neue bestandheile der schweingalle. Ann. Chem. Pharmacie, 1862, 123, 353-360.
2. Baeyer, A. Synthese des Neurins. Justus Liebigs Annalen der Chemie, 1866, 140.
3. Loewi, O. Nobel lecture. Nobelprize.org 1936 http://www.nobelprize.org/nobel_prizes/medicine/laureates/1936/loewi-lecture.html (Accessed August 15, 2011)
4. Dale, H. Nobel lecture. Nobelprize.org 1936 http://www.nobelprize.org/nobel_prizes/medicine/laureates/1936/dale-lecture.html (Accessed August 15, 2011)
5. Mann, P. J.; Quastel, J. H. The oxidation of choline by rat liver. Biochem. J., 1937, 31, 869-878.
6. Du Vigneaud, V.; Simmonds, S.; Chandler, J. P.; Cohn, M. A further investigation of the role of betaine in transmethylation reactions in vivo. J. Biol. Chem., 1946, 165, 639-648.
7. Cantoni, G. L. S-Adenosylmethionine; a new intermediate formed enzymatically from L-methionine and adenosinetriphosphate. J. Biol. Chem., 1953, 204, 403-416.
8. Chiang, P. K.; Gordon, R. K.; Tal, J.; Zeng, G. C.; Doctor, B. P.; Pardhasaradhi, K.; McCann, P. P. S-adenosylmethionine and methylation. FASEB J, 1996, 10, 471-480.
9. Grillo, M. A.; Colombatto, S. S-adenosylmethionine and its products. Amino Acids, 2008, 34, 187-193.
10. Jeltsch, A. Molecular enzymology of mammalian DNA methyltransferases. Curr. Top. Microbiol. Immunol., 2006, 301, 203-225.
11. Teperino, R.; Schoonjans, K.; Auwerx, J. Histone methyl transferases and demethylases; can they link metabolism and transcription? Cell Metab., 2010, 12, 321-327.
12. Allan, F. N.; Bowie, D. J.; Macleod, J. J. R.; Robinson, W. L. Behavior of depancreatized dogs kept alive with insulin. Br. J. Exp. Pathol., 1924, 5, 75-83.
13. Hershey, J. M. Substitution of lecithin for raw pancreas in the diet of the depancreatized dog. Am. J. Physiol., 1930, 93, 657-658.
14. Best, C. H.; Huntsman, M. E. The effects of the components of lecithine upon deposition of fat in the liver. J. Physiol., 1932, 75, 405-412.
15. Best, C. H.; Channon, H. J.; Ridout, J. H. Choline and the dietary production of fatty livers. J. Physiol., 1934, 81, 409-421.
16. Zeisel, S. H.; Da Costa, K.-A.; Franklin, P. D.; Alexander, E. A.; Lamont, J. T.; Sheard, N. F.; Beiser, A. Choline, an essential nutrient for humans. FASEB J, 1991, 5, 2093-2098.
17. FNB Dietary reference intakes for thiamin, riboflavin, niacin, vitamin B6, folate, vitamin B12, panthotenic acid, biotin, and choline; National Academy Press: Washington, D.C., 1998.
18. Garner, S. C.; Mar, M. H.; Zeisel, S. H. 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.
19. Holmes-McNary, M. Q.; Cheng, W. L.; Mar, M. H.; Fussell, S.; Zeisel, S. H. Choline and choline esters in human and rat milk and in infant formulas. Am. J. Clin. Nutr., 1996, 64, 572-576.
20. 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.
21. da Costa, K. A.; Badea, M.; Fischer, L. M.; Zeisel, S. H. Elevated serum creatine phosphokinase in choline-deficient humans: mechanistic studies in C2C12 mouse myoblasts. Am. J. Clin. Nutr., 2004, 80, 163-170.
22. da Costa, K. A.; Niculescu, M. D.; Craciunescu, C. N.; Fischer, L. M.; Zeisel, S. H. Choline deficiency increases lymphocyte apoptosis and DNA damage in humans. Am. J. Clin. Nutr., 2006, 84, 88-94.
23. Jensen, H. H.; Batres-Marquez, S. P.; Carriquiry, A.; Schalinske, K. L. Choline in the diets of the US population: NHANES, 2003-2004. FASEB J, 2007, 21, LB219.
24. Fischer, L. M.; daCosta, K. A.; Kwock, L.; Stewart, P. W.; Lu, T. S.; Stabler, S. P.; Allen, R. H.; Zeisel, S. H. Sex and menopausal status influence human dietary requirements for the nutrient choline. Am. J. Clin. Nutr., 2007, 85, 1275-1285.
25. Waite, K. A.; Cabilio, N. R.; Vance, D. E. Choline deficiencyinduced liver damage is reversible in Pemt-/- mice. J. Nutr., 2002, 132, 68-71.
26. Walkey, C. J.; Yu, L.; Agellon, L. B.; Vance, D. E. Biochemical and evolutionary significance of phospholipid methylation. J. Biol. Chem., 1998, 273, 27043-27046.
27. Zhu, X. N.; Song, J. N.; Mar, M. H.; Edwards, L. J.; Zeisel, S. H. 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.
28. Resseguie, M.; Song, J.; Niculescu, M. D.; da Costa, K. A.; Randall, T. A.; Zeisel, S. H. Phosphatidylethanolamine Nmethyltransferase (PEMT) gene expression is induced by estrogen in human and mouse primary hepatocytes. FASEB J., 2007, 21, 2622-2632.
29. 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.
30. Caudill, M. A.; Dellschaft, N.; Solis, C.; Hinkis, S.; Ivanov, A. A.; Nash-Barboza, S.; Randall, K. E.; Jackson, B.; Solomita, G. N.; Vermeylen, F. Choline intake, plasma riboflavin, and the phosphatidylethanolamine N-methyltransferase G5465A genotype predict plasma homocysteine in folate-deplete Mexican-American men with the methylenetetrahydrofolate reductase 677TT genotype. J. Nutr., 2009, 139, 727-733.
31. 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.
32. Fischer, L. M.; da Costa, K. A.; Kwock, L.; Galanko, J.; Zeisel, S. H. Dietary choline requirements of women: effects of estrogen and genetic variation. Am. J. Clin. Nutr., 2010, 92, 1113-1119.
33. 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.
34. Holm, P. I.; Hustad, S.; Ueland, P. M.; Vollset, S. E.; Grotmol, T.; Schneede, J. Modulation of the homocysteine-betaine relationship by methylenetetrahydrofolate reductase 677 C->T genotypes and B-vitamin status in a large scale epidemiological study. J. Clin. Endocrinol. Metab., 2007, 92, 1535-1541.
35. Abratte, C. M.; Wang, W.; Li, R.; Moriarty, D. J.; Caudill, M. A. Folate intake and the MTHFR C677T genotype influence choline status in young Mexican American women. J. Nutr. Biochem., 2008, 19, 158-165.
36. Yan, J.; Wang, W.; Gregory, J. F., 3rd; Malysheva, O.; Brenna, J. T.; Stabler, S. P.; Allen, R. H.; Caudill, M. A. MTHFR C677T genotype influences the isotopic enrichment of one-carbon metabolites in folate-compromised men consuming d9-choline. Am. J. Clin. Nutr., 2011, 93, 348-355.
37. Sha, W.; da Costa, K. A.; Fischer, L. M.; Milburn, M. V.; Lawton, K. A.; Berger, A.; Jia, W.; Zeisel, S. H. Metabolomic profiling can predict which humans will develop liver dysfunction when deprived of dietary choline. FASEB J 2010, 24, 2962-2975.
38. Patterson, K. Y.; Bhagwat, A. S.; Williams, J. R.; Howe, J. C.; Holden, J. M.; Zeisel, S. H.; Da Costa, C. A.; Mar, H. USDA database for the choline content of common foods. Release two. 2008 http://www.ars.usda.gov/Services/docs.htm?docid=6232 (Accessed August 15, 2011)
39. Shaw, G. M.; Carmichael, S. L.; Laurent, C.; Rasmussen, S. A. Maternal nutrient intakes and risk of orofacial clefts. Epidemiology, 2006, 17, 285-291.
40. Mostowska, A.; Hozyasz, K. K.; Wojcicki, P.; Dziegelewska, M.; Jagodzinski, P. P. Associations of folate and choline metabolism gene polymorphisms with orofacial clefts. J. Med. Genet., 2009, 47, 809-815.
41. Xu, X.; Gammon, M. D.; Zeisel, S. H.; Lee, Y. L.; Wetmur, J. G.; Teitelbaum, S. L.; Bradshaw, P. T.; Neugut, A. I.; Santella, R. M.; Chen, J. Choline metabolism and risk of breast cancer in a population-based study. FASEB J, 2008, 22, 2045-2052.
42. Cho, E.; Willett, W. C.; Colditz, G. A.; Fuchs, C. S.; Wu, K.; Chan, A. T.; Zeisel, S. H.; Giovannucci, E. L. Dietary choline and betaine and the risk of distal colorectal adenoma in women. J. Natl. Cancer Inst., 2007, 99, 1224-1231.
43. Ibiebele, T. I.; Hughes, M. C.; Pandeya, N.; Zhao, Z.; Montgomery, G.; Hayward, N.; Green, A. C.; Whiteman, D. C.; Webb, P. M. High intake of folate from food sources is associated with reduced risk of esophageal cancer in an Australian population. J. Nutr., 2011, 141, 274-283.
44. 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.
45. Shaw, G. M.; Finnell, R. H.; Blom, H. J.; Carmichael, S. L.; Vollset, S. E.; Yang, W.; Ueland, P. M. Choline and risk of neural tube defects in a folate-fortified population. Epidemiology, 2009, 20, 714-719.
46. Enaw, J. O.; Zhu, H.; Yang, W.; Lu, W.; Shaw, G. M.; Lammer, E. J.; Finnell, R. H. CHKA and PCYT1A gene polymorphisms, choline intake and spina bifida risk in a California population. BMC Med., 2006, 4, 36.
47. 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. Dev. Brain Res., 1999, 115, 123-129.
48. 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. Dev Brain Res., 1999, 113, 13-20.
49. 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.
50. Meck, W. H.; Williams, C. L. Simultaneous temporal processing is sensitive to prenatal choline availability in mature and aged rats. Neuroreport, 1997, 8, 3045-3051.
51. Mellott, T. J.; Williams, C. L.; Meck, W. H.; Blusztajn, J. K. Prenatal choline supplementation advances hippocampal development and enhances MAPK and CREB activation. FASEB J, 2004, 18, NIL412-NIL427.
52. 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.
53. Meck, W. H.; Smith, R. A.; Williams, C. L. Organizational changes in cholinergic activity and enhanced visuospatial memory as a function of choline administered prenatally or postnatally or both. Behav. Neurosci., 1989, 103, 1234-1241.
54. Meck, W. H.; Williams, C. L. Characterization of the facilitative effects of perinatal choline supplementation on timing and temporal memory. Neuroreport, 1997, 8, 2831-2835.
55. Meck, W. H.; Williams, C. L. Perinatal choline supplementation increases the threshold for chunking in spatial memory. Neuroreport 1997, 8, 3053-3059.
56. Meck, W. H.; Williams, C. L. Choline supplementation during prenatal development reduces proactive interference in spatial memory. Dev. Brain Res., 1999, 118, 51-59.
57. Meck, W. H.; Williams, C. L.; Cermak, J. M.; Blusztajn, J. K. Developmental periods of choline sensitivity provide an ontogenetic mechanism for regulating memory capacity and agerelated dementia. Front. Integr. Neurosci., 2008, 1, 7.
58. Clelland, C. D.; Choi, M.; Romberg, C.; Clemenson, G. D., Jr.; Fragniere, A.; Tyers, P.; Jessberger, S.; Saksida, L. M.; Barker, R. A.; Gage, F. H.; Bussey, T. J. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science, 2009, 325, 210-213.
59. Kitamura, T.; Saitoh, Y.; Takashima, N.; Murayama, A.; Niibori, Y.; Ageta, H.; Sekiguchi, M.; Sugiyama, H.; Inokuchi, K. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell, 2009, 139, 814-827.
60. Glenn, M. J.; Gibson, E. M.; Kirby, E. D.; Mellott, T. J.; Blusztajn, J. K.; Williams, C. L. Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur. J. Neurosci., 2007, 25, 2473-2482.
61. Glenn, M. J.; Kirby, E. D.; Gibson, E. M.; Wong-Goodrich, S. J.; Mellott, T. J.; Blusztajn, J. K.; Williams, C. L. 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.
62. Wong-Goodrich, S. J.; Glenn, M. J.; Mellott, T. J.; Blusztajn, J. K.; Meck, W. H.; Williams, C. L. Spatial memory and hippocampal plasticity are differentially sensitive to the availability of choline in adulthood as a function of choline supply in utero. Brain Res., 2008, 1237, 153-166.
63. Wong-Goodrich, S. J.; Mellott, T. J.; Glenn, M. J.; Blusztajn, J. K.; Williams, C. L. Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus. Neurobiol. Dis., 2008, 30, 255-269.
64. Napoli, I.; Blusztajn, J. K.; Mellott, T. J. Prenatal choline supplementation in rats increases the expression of IGF2 and its receptor IGF2R and enhances IGF2-induced acetylcholine release in hippocampus and frontal cortex. Brain Res., 2008, 1237, 124-135.
65. Williams, C. L.; Meck, W. H.; Heyer, D.; Loy, R. Hypertrophy of basal forebrain neurons and enhanced visuospatial memory in perinatally choline-supplemented rats. Brain Res., 1998, 794, 225-238.
66. Fibiger, H. C. Cholinergic mechanisms in learning, memory and dementia: A review of recent evidence. TINS, 1991, 14, 220-223.
67. Sarter, M.; Parikh, V. Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci., 2005, 6, 48-56.
68. Cermak, J. M.; Holler, T.; Jackson, D. A.; Blusztajn, J. K. Prenatal availability of choline modifies development of the hippocampal cholinergic system. FASEB J, 1998, 12, 349-357.
69. Sweatt, J. D. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 2001, 76, 1-10.
70. Jones, J. P.; H Meck, W.; Williams, C. L.; Wilson, W. A.; Swartzwelder, H. S. Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Dev. Brain Res., 1999, 118, 159-167.
71. Pyapali, G. K.; Turner, D. A.; Williams, C. L.; Meck, W. H.; Swartzwelder, H. S. Prenatal dietary choline supplementation decreases the threshold for induction of long-term potentiation in young adult rats. J. Neurophysiol., 1998, 79, 1790-1796.
72. Montoya, D.; Swartzwelder, H. S. Prenatal choline supplementation alters hippocampal N-methyl-D-aspartate receptor-mediated neurotransmission in adult rats. Neurosci. Lett., 2000, 296, 85-88.
73. Mellott, T. J.; Follettie, M. T.; Diesl, V.; Hill, A. A.; Lopez-Coviella, I.; Blusztajn, J. K. Prenatal choline availability modulates hippocampal and cerebral cortical gene expression. FASEB J, 2007, 21, 1311-1323.
74. Chen, Z. X.; Riggs, A. D. DNA methylation and demethylation in mammals. J. Biol. Chem., 2011, 286, 18347-18353.
75. Hoffman, D. R.; Haning, J. A.; Cornatzer, W. E. Effect of a methyl-deficient diet on rat liver phosphatidylcholine biosyntheis. Can. J. Biochem., 1981, 59, 543-550.
76. Shivapurkar, N.; Poirier, L. A. 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.
77. Shivapurkar, N.; Wilson, M. J.; Hoover, K. L.; Mikol, Y. B.; Creasia, D.; Poirier, L. A. Hepatic DNA methylation and liver tumor formation in male C3H mice fed methionine- and cholinedeficient diets. J. Natl. Cancer Inst., 1986, 77, 213-217.
78. Svardal, A. M.; Ueland, P. M.; Berge, R. K.; Aarsland, A.; Aarsaether, N.; Lonning, P. E.; Refsum, H. Effect of methotrexate on homocysteine and other sulfur compounds in tissues of rats fed a normal or a defined, choline-deficient diet. Cancer Chemother. Pharmacol., 1988, 21, 313-8.
79. Zeisel, S. H.; Zola, T.; DaCosta, K.-A.; Pomfret, E. A. Effect of choline deficiency on S-adenosylmethionine and methionine concentrations in rat liver. Biochem. J. 1989, 259, 725-729.
80. Pomfret, E. A.; da Costa, K.; Zeisel, S. H. Effects of choline deficiency and methotrexate treatment upon rat liver. J. Nutr. Biochem., 1990, 1, 533-541.
81. Innis, S. M.; Davidson, A. G.; Melynk, S.; James, S. J. Cholinerelated supplements improve abnormal plasma methioninehomocysteine metabolites and glutathione status in children with cystic fibrosis. Am. J. Clin. Nutr., 2007, 85, 702-708.
82. Kovacheva, V. P.; Mellott, T. J.; Davison, J. M.; Wagner, N.; Lopez-Coviella, I.; Schnitzler, A. C.; Blusztajn, J. K. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. J. Biol. Chem., 2007, 282, 31777-31788.
83. Wolff, G. L.; Kodell, R. L.; Moore, S. R.; Cooney, C. A. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J., 1998, 12, 949-957.
84. Cooney, C. A.; Dave, A. A.; Wolff, G. L. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J.Nutr., 2002, 132, 2393S-2400S.
85. Waterland, R. A.; Jirtle, R. L. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol. Cell Biol., 2003, 23, 5293-300.
86. Waterland, R. A.; Dolinoy, D. C.; Lin, J. R.; Smith, C. A.; Shi, X.; Tahiliani, K. G. Maternal methyl supplements increase offspring DNA methylation at axin fused. Genesis, 2006, 44, 401-406.
87. Dolinoy, D. C.; Huang, D.; Jirtle, R. L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 13056-1361.
88. Waterland, R. A.; Travisano, M.; Tahiliani, K. G.; Rached, M. T.; Mirza, S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int. J. Obes. (Lond)., 2008, 1373-1379.
89. Cropley, J. E.; Suter, C. M.; Beckman, K. B.; Martin, D. I. Germ-line epigenetic modification of the murine A vy allele by nutritional supplementation. Proc. Natl. Acad. Sci. U. S.A., 2006, 103, 17308-17312.
90. Copeland, D. H.; Salmon, W. D. The Occurrence of Neoplasms in the Liver, Lungs, and other tissues of rats as a result of prolonged choline deficiency. Am. J. Pathol., 1946, 22, 1059-1079.
91. Engel, R. W.; Copeland, D. H.; Salmon, W. D. Carcinogenic effects associated with diets deficient in choline and related nutrients. Ann. N. Y. Acad. Sci., 1947, 49, 49-67.
92. Salmon, W. D.; Copeland, D. H. Liver carcinoma and related lesions in chronic choline deficiency. Ann. N. Y. Acad. Sci., 1954, 57, 665-677.
93. Shinozuka, H.; Katyal, S. L.; Perera, M. I. Choline deficiency and chemical carcinogenesis. Adv. Exp. Med. Biol., 1986, 206, 253-267.
94. Lombardi, B.; Chandar, N.; Locker, J. Nutritional model of hepatocarcinogenesis. Rats fed choline-devoid diet. Dig. Dis. Sci., 1991, 36, 979-984.
95. Newberne, P. M.; Rogers, A. E. Labile methyl groups and the promotion of cancer. Annu. Rev. Nutr., 1986, 6, 407-432.
96. Newberne, P. M. Lipotropic factors and oncogenesis. Adv. Exp. Med. Biol., 1986, 206, 223-251.
97. Feinberg, A. P.; Vogelstein, B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature, 1983, 301, 89-92.
98. Feinberg, A. P.; Tycko, B. The history of cancer epigenetics. Nat. Rev. Cancer, 2004, 4, 143-153.
99. Irizarry, R. A.; Ladd-Acosta, C.; Wen, B.; Wu, Z.; Montano, C.; Onyango, P.; Cui, H.; Gabo, K.; Rongione, M.; Webster, M.; Ji, H.; Potash, J. B.; Sabunciyan, S.; Feinberg, A. P. The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat. Genet., 2009, 41, 178-186.
100. Rodriguez-Paredes, M.; Esteller, M. Cancer epigenetics reaches mainstream oncology. Nat. Med., 2011, 17, 330-339.
101. Bhave, M. R.; Wilson, M. J.; Poirier, L. A. C-H-ras and c-K-ras gene hypomethylation in the livers and hepatomas of rats fed methyldeficient, amino acid-defined diets. Carcinogenesis, 1988, 9, 343-348.
102. Zapisek, W. F.; Cronin, G. M.; Lyn-Cook, B. D.; Poirier, L. A. The onset of oncogene hypomethylation in the livers of rats fed methyldeficient, amino acid-defined diets. Carcinogenesis, 1992, 13, 1869-1872.
103. Dizik, M.; Christman, J. K.; Wainfan, E. Alterations in expression and methylation of specific genes in livers of rats fed a cancer promoting methyl-deficient diet. Carcinogenesis, 1991, 12, 1307-1312.
104. Smith, M. L.; Yeleswarapu, L.; Scalamogna, P.; Locker, J.; Lombardi, B. P53 mutations in hepatocellular carcinomas induced by a choline-devoid diet in male Fischer 344 rats. Carcinogenesis, 1993, 14, 503-510.
105. Pogribny, I. P.; Miller, B. J.; James, S. J. Alterations in hepatic p53 gene methylation patterns during tumor progression with folate/methyl deficiency in the rat. Cancer Lett., 1997, 115, 31-38.
106. 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.
107. Pogribny, I. P.; James, S. J. De novo methylation of the p16INK4A gene in early preneoplastic liver and tumors induced by folate/methyl deficiency in rats. Cancer Lett., 2002, 187, 69-75.
108. James, S. J.; Pogribny, I. P.; Pogribna, M.; Miller, B. J.; Jernigan, S.; Melnyk, S. Mechanisms of DNA damage, DNA hypomethylation, and tumor progression in the folate/methyl-deficient rat model of hepatocarcinogenesis. J. Nutr., 2003, 133, 3740S-3747S.
109. Pogribny, I. P.; James, S. J.; Jernigan, S.; Pogribna, M. Genomic hypomethylation is specific for preneoplastic liver in folate/methyl deficient rats and does not occur in non-target tissues. Mutat. Res., 2004, 548, 53-59.
110. Pogribny, I. P.; Ross, S. A.; Wise, C.; Pogribna, M.; Jones, E. A.; Tryndyak, V. P.; James, S. J.; Dragan, Y. P.; Poirier, L. A. Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat. Res., 2006, 593, 80-87.
111. Asada, K.; Kotake, Y.; Asada, R.; Saunders, D.; Broyles, R. H.; Towner, R. A.; Fukui, H.; Floyd, R. A. LINE-1 hypomethylation in a choline-deficiency-induced liver cancer in rats: dependence on feeding period. J. Biomed. Biotechnol., 2006, 2006, 17142.
112. Tsujiuchi, T.; Shimizu, K.; Itsuzaki, Y.; Onishi, M.; Sugata, E.; Fujii, H.; Honoki, K. CpG site hypermethylation of E-cadherin and Connexin26 genes in hepatocellular carcinomas induced by a choline-deficient L-Amino Acid-defined diet in rats. Mol. Carcinog., 2007, 46, 269-274.
113. Shimizu, K.; Onishi, M.; Sugata, E.; Sokuza, Y.; Mori, C.; Nishikawa, T.; Honoki, K.; Tsujiuchi, T. Disturbance of DNA methylation patterns in the early phase of hepatocarcinogenesis induced by a choline-deficient L-amino acid-defined diet in rats. Cancer Sci., 2007, 98, 1318-1322.
114. Pogribny, I. P.; Shpyleva, S. I.; Muskhelishvili, L.; Bagnyukova, T. V.; James, S. J.; Beland, F. A. Role of DNA damage and alterations in cytosine DNA methylation in rat liver carcinogenesis induced by a methyl-deficient diet. Mutat. Res., 2009, 669, 56-62.
115. Robertson, K. D.; Jones, P. A. DNA methylation: past, present and future directions. Carcinogenesis, 2000, 21, 461-467.
116. Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev., 2002, 16, 6-21.
117. Bernstein, B. E.; Meissner, A.; Lander, E. S. The mammalian epigenome. Cell, 2007, 128, 669-681.
118. Meissner, A. Epigenetic modifications in pluripotent and differentiated cells. Nat. Biotechnol., 2010, 28, 1079-1088.
119. Portela, A.; Esteller, M. Epigenetic modifications and human disease. Nat. Biotechnol., 2010, 28, 1057-1068.
120. Waterland, R. A.; Lin, J. R.; Smith, C. A.; Jirtle, R. L. Postweaning diet affects genomic imprinting at the insulin-like growth factor 2 (Igf2) locus. Hum. Mol. Genet., 2006, 15, 705-716.
121. Paulsen, M.; Ferguson-Smith, A. C. DNA methylation in genomic imprinting, development, and disease. J. Pathol., 2001, 195, 97-110.
122. Li, E. Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet., 2002, 3, 662-673.
123. Reinhart, B.; Eljanne, M.; Chaillet, J. R. Shared role for differentially methylated domains of imprinted genes. Mol. Cell Biol., 2002, 22, 2089-2098.
124. Tucker, K. L. Methylated cytosine and the brain: a new base for neuroscience. Neuron, 2001, 30, 649-652.
125. Robertson, K. D.; Wolffe, A. P. DNA methylation in health and disease. Nat. Rev. Genet., 2000, 1, 11-19.
126. Nan, X.; Ng, H. H.; Johnson, C. A.; Laherty, C. D.; Turner, B. M.; Eisenman, R. N.; Bird, A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 1998, 393, 386-389.
127. Jones, P. L.; Veenstra, G. J.; Wade, P. A.; Vermaak, D.; Kass, S. U.; Landsberger, N.; Strouboulis, J.; Wolffe, A. P. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 1998, 19, 187-191.
128. Eden, S.; Hashimshony, T.; Keshet, I.; Cedar, H.; Thorne, A. W. DNA methylation models histone acetylation. Nature, 1998, 394, 842.
129. Takizawa, T.; Nakashima, K.; Namihira, M.; Ochiai, W.; Uemura, A.; Yanagisawa, M.; Fujita, N.; Nakao, M.; Taga, T. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell, 2001, 1, 749-758.
130. Klose, R. J.; Bird, A. P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci., 2006, 31, 89-97.
131. Barrett, R. M.; Wood, M. A. Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn Mem., 2008, 15, 460-467.
132. Klempnauer, K. H. Methylation-sensitive DNA binding by v-myb and c-myb proteins. Oncogene, 1993, 8, 111-115.
133. Campanero, M. R.; Armstrong, M. I.; Flemington, E. K. CpG methylation as a mechanism for the regulation of E2F activity. Proc. Natl. Acad. Sci. U. S. A., 2000, 97, 6481-6486.
134. Weih, F.; Nitsch, D.; Reik, A.; Schutz, G.; Becker, P. B. Analysis of CpG methylation and genomic footprinting at the tyrosine aminotransferase gene: DNA methylation alone is not sufficient to prevent protein binding in vivo. EMBO J., 1991, 10, 2559-2567.
135. Comb, M.; Goodman, H. M. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res., 1990, 18, 3975-3982.
136. Kirillov, A.; Kistler, B.; Mostoslavsky, R.; Cedar, H.; Wirth, T.; Bergman, Y. A role for nuclear NF-kappaB in B-cell-specific demethylation of the Igkappa locus. Nat. Genet., 1996, 13, 435-441.
137. Eden, S.; Constancia, M.; Hashimshony, T.; Dean, W.; Goldstein, B.; Johnson, A. C.; Keshet, I.; Reik, W.; Cedar, H. An upstream repressor element plays a role in Igf2 imprinting. EMBO J., 2001, 20, 3518-3525.
138. Murrell, A.; Heeson, S.; Bowden, L.; Constancia, M.; Dean, W.; Kelsey, G.; Reik, W. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep., 2001, 2, 1101-1106.
139. Inano, K.; Suetake, I.; Ueda, T.; Miyake, Y.; Nakamura, M.; Okada, M.; Tajima, S. Maintenance-type DNA methyltransferase is highly expressed in post- mitotic neurons and localized in the cytoplasmic compartment. J. Biochem. (Tokyo) 2000, 128, 315-321.
140. Trasler, J. M.; Trasler, D. G.; Bestor, T. H.; Li, E.; Ghibu, F. DNA methyltransferase in normal and Dnmtn/Dnmtn mouse embryos. Dev. Dyn., 1996, 206, 239-247.
141. Goto, K.; Numata, M.; Komura, J. I.; Ono, T.; Bestor, T. H.; Kondo, H. Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation, 1994, 56, 39-44.
142. Brooks, P. J.; Marietta, C.; Goldman, D. DNA mismatch repair and DNA methylation in adult brain neurons. J. Neurosci., 1996, 16, 939-945.
143. Tawa, R.; Ono, T.; Kurishita, A.; Okada, S.; Hirose, S. Changes of DNA methylation level during pre- and postnatal periods in mice. Differentiation, 1990, 45, 44-48.
144. Wilson, V. L.; Smith, R. A.; Ma, S.; Cutler, R. G. Genomic 5-methyldeoxycytidine decreases with age. J. Biol. Chem., 1987, 262, 9948-9951.
145. Ono, T.; Uehara, Y.; Kurishita, A.; Tawa, R.; Sakurai, H. Biological significance of DNA methylation in the ageing process. Age Ageing, 1993, 22, S34-S43.
146. Siegmund, K. D.; Connor, C. M.; Campan, M.; Long, T. I.; Weisenberger, D. J.; Biniszkiewicz, D.; Jaenisch, R.; Laird, P. W.; Akbarian, S. DNA Methylation in the Human Cerebral Cortex Is Dynamically Regulated throughout the Life Span and Involves Differentiated Neurons. PLoS ONE, 2007, 2, e895.
147. Hernandez, D. G.; Nalls, M. A.; Gibbs, J. R.; Arepalli, S.; van der Brug, M.; Chong, S.; Moore, M.; Longo, D. L.; Cookson, M. R.; Traynor, B. J.; Singleton, A. B. Distinct DNA methylation changes highly correlated with chronological age in the human brain. Hum. Mol. Genet., 2011, 20, 1164-1172.
148. Iwamoto, K.; Bundo, M.; Ueda, J.; Oldham, M. C.; Ukai, W.; Hashimoto, E.; Saito, T.; Geschwind, D. H.; Kato, T. Neurons show distinctive DNA methylation profile and higher interindividual variations compared with non-neurons. Genome Res., 2011, 21, 688-696.
149. Tachibana, M.; Sugimoto, K.; Nozaki, M.; Ueda, J.; Ohta, T.; Ohki, M.; Fukuda, M.; Takeda, N.; Niida, H.; Kato, H.; Shinkai, Y. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev., 2002, 16, 1779-1791.
150. Nicholson, T. B.; Chen, T.; Richard, S. The physiological and pathophysiological role of PRMT1-mediated protein arginine methylation. Pharmacol. Res., 2009, 60, 466-474.
151. Feng, J.; Chang, H.; Li, E.; Fan, G. Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J. Neurosci. Res., 2005, 79, 734-746.
152. Hsu, D. W.; Lin, M. J.; Lee, T. L.; Wen, S. C.; Chen, X.; Shen, C. K. Two major forms of DNA (cytosine-5) methyltransferase in human somatic tissues. Proc. Natl. Acad. Sci. U. S. A., 1999, 96, 9751-975
153. Okano, M.; Li, E. Genetic analyses of DNA methyltransferase genes in mouse model system. J. Nutr., 2002, 132, 2462S-2465S.
154. Singal, R.; vanWert, J. M. De novo methylation of an embryonic globin gene during normal development is strand specific and spreads from the proximal transcribed region. Blood, 2001, 98, 3441-3446.
155. Alonso-Aperte, E.; Varela-Moreiras, G. Brain folates and DNA methylation in rats fed a choline deficient diet or treated with low doses of methotrexate. Int. J. Vitam. Nutr. Res., 1996, 66, 232-236.
156. Wainfan, E.; Dizik, M.; Stender, M.; Christman, J. K. Rapid appearance of hypomethylated DNA in livers of rats fed cancerpromoting, methyl-deficient diets. Cancer Res., 1989, 49, 4094-4097.
157. Wilson, M. J.; Shivapurkar, N.; Poirier, L. A. Hypomethylation of epatic nuclear DNA in rats fed with a carcinogenic methyldeficient diet. Biochem. J., 1984, 218, 987-990.
158. Christman, J. K.; 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.
159. 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.
160. Kim, Y. I.; Pogribny, I. P.; Basnakian, A. G.; Miller, J. W.; Selhub, J.; James, S. J.; Mason, J. B. Folate deficiency in rats induces DNA strand breaks and hypomethylation within the p53 tumor suppressor gene. Am. J. Clin. Nutr., 1997, 65, 46-52.
161. 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.
162. Mehedint, M. G.; Craciunescu, C. N.; Zeisel, S. H. Maternal dietary choline deficiency decreases angiogenesis in fetal mouse hippocampus. Proc. Natl. Acad. Sci., U.S.A, 2010, 107, 12834-12839.
163. Shin, W.; Yan, J.; Abratte, C. M.; Vermeylen, F.; Caudill, M. A. Choline intake exceeding current dietary recommendations preserves markers of cellular methylation in a genetic subgroup of folate-compromised men. J. Nutr., 2010, 140, 975-980.
164. Kim, Y. I.; Christman, J. K.; Fleet, J. C.; Cravo, M. L.; Salomon, R. N.; Smith, D.; Ordovas, J.; Selhub, J.; Mason, J. B. Moderate folate deficiency does not cause global hypomethylation of hepatic and colonic DNA or c-myc-specific hypomethylation of colonic DNA in rats. Am. J. Clin. Nutr., 1995, 61, 1083-1090.
165. Song, J.; Sohn, K. J.; Medline, A.; Ash, C.; Gallinger, S.; Kim, Y. I. Chemopreventive effects of dietary folate on intestinal polyps in Apc+/-Msh2-/- mice. Cancer Res., 2000, 60, 3191-3199.
166. Sohn, K. J.; Stempak, J. M.; Reid, S.; Shirwadkar, S.; Mason, J. B.; Kim, Y. I. The effect of dietary folate on genomic and p53-specific DNA methylation in rat colon. Carcinogenesis, 2003, 24, 81-90.
167. Pogribny, I. P.; Karpf, A. R.; James, S. R.; Melnyk, S.; Han, T.; Tryndyak, V. P. Epigenetic alterations in the brains of Fisher 344 rats induced by long-term administration of folate/methyl-deficient diet. Brain Res., 2008, 1237, 25-34.
168. 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.
169. Ghoshal, K.; Li, X.; Datta, J.; Bai, S.; Pogribny, I.; Pogribny, M.; Huang, Y.; Young, D.; Jacob, S. T. A folate- and methyl-deficient diet alters the expression of DNA methyltransferases and methyl CpG binding proteins involved in epigenetic gene silencing in livers of F344 rats. J. Nutr., 2006, 136, 1522-1527.
170. Lopes, S.; Lewis, A.; Hajkova, P.; Dean, W.; Oswald, J.; Forne, T.; Murrell, A.; Constancia, M.; Bartolomei, M.; Walter, J.; Reik, W. Epigenetic modifications in an imprinting cluster are controlled by a hierarchy of DMRs suggesting long-range chromatin interactions. Hum. Mol. Genet., 2003, 12, 295-305.
171. Li, E.; Beard, C.; Jaenisch, R. Role for DNA methylation in genomic imprinting. Nature, 1993, 366, 362-365.
172. Bell, A. C.; Felsenfeld, G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature, 2000, 405, 482-485.
173. Chen, D. Y.; Stern, S. A.; Garcia-Osta, A.; Saunier-Rebori, B.; Pollonini, G.; Bambah-Mukku, D.; Blitzer, R. D.; Alberini, C. M. A critical role for IGF-II in memory consolidation and enhancement. Nature, 2011, 469, 491-497.
174. Tahiliani, M.; Koh, K. P.; Shen, Y.; Pastor, W. A.; Bandukwala, H.; Brudno, Y.; Agarwal, S.; Iyer, L. M.; Liu, D. R.; Aravind, L.; Rao, A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 2009, 324, 930-935.
175. Ito, S.; D'Alessio, A. C.; Taranova, O. V.; Hong, K.; Sowers, L. C.; Zhang, Y. Role of Tet proteins in 5mC to 5hmC conversion, EScell self-renewal and inner cell mass specification. Nature, 2010, 466, 1129-1133.
176. Ficz, G.; Branco, M. R.; Seisenberger, S.; Santos, F.; Krueger, F.; Hore, T. A.; Marques, C. J.; Andrews, S.; Reik, W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature, 2011, 473, 398-402.
177. Guo, J. U.; Su, Y.; Zhong, C.; Ming, G. L.; Song, H. Hydroxylation of 5-Methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell, 2011, 145, 423-434.
178. Ito, S.; Shen, L.; Dai, Q.; Wu, S. C.; Collins, L. B.; Swenberg, J. A.; He, C.; Zhang, Y. Tet Proteins Can Convert 5-Methylcytosine to 5-Formylcytosine and 5-Carboxylcytosine. Science, 2011.
179. He, Y. F.; Li, B. Z.; Li, Z.; Liu, P.; Wang, Y.; Tang, Q.; Ding, J.; Jia, Y.; Chen, Z.; Li, L.; Sun, Y.; Li, X.; Dai, Q.; Song, C. X.; Zhang, K.; He, C.; Xu, G. L. Tet-Mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science, 2011, 333, 1303-1307.
180. Valinluck, V.; Tsai, H. H.; Rogstad, D. K.; Burdzy, A.; Bird, A.; Sowers, L. C. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res., 2004, 32, 4100-4108.
181. Jin, S. G.; Kadam, S.; Pfeifer, G. P. Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res., 2010, 38, e125.
182. Kinney, S. M.; Chin, H. G.; Vaisvila, R.; Bitinaite, J.; Zheng, Y.; Esteve, P. O.; Feng, S.; Stroud, H.; Jacobsen, S. E.; Pradhan, S. Tissue specific distribution and dynamic changes of 5-hydroxymethylcytosine in mammalian genome. J. Biol. Chem., 2011, 286, 24685-24693.
183. Frommer, M.; McDonald, L. E.; Millar, D. S.; Collis, C. M.; Watt, F.; Grigg, G. W.; Molloy, P. L.; Paul, C. L. A genomic sequencing protocol that yields a positive display of 5- methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. U. S. A., 1992, 89, 1827-1831.
184. Flusberg, B. A.; Webster, D. R.; Lee, J. H.; Travers, K. J.; Olivares, E. C.; Clark, T. A.; Korlach, J.; Turner, S. W. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods.
185. Jin, S. G.; Wu, X.; Li, A. X.; Pfeifer, G. P. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res., 2011, 39, 5015-5024.
186. Song, C. X.; Szulwach, K. E.; Fu, Y.; Dai, Q.; Yi, C.; Li, X.; Li, Y.; Chen, C. H.; Zhang, W.; Jian, X.; Wang, J.; Zhang, L.; Looney, T. J.; Zhang, B.; Godley, L. A.; Hicks, L. M.; Lahn, B. T.; Jin, P.; He, C. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol., 2011, 29, 68-72.
187. Kriaucionis, S.; Heintz, N. The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain. Science, 2009, 324, 929-930.
188. Szulwach, K. E.; Li, X.; Li, Y.; Song, C. X.; Wu, H.; Dai, Q.; Irier, H.; Upadhyay, A. K.; Gearing, M.; Levey, A. I.; Vasanthakumar, A.; Godley, L. A.; Chang, Q.; Cheng, X.; He, C.; Jin, P. 5-hmCmediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci., 2011, 14, 1607-1616.
189. Jenuwein, T.; Allis, C. D. Translating the histone code. Science, 2001, 293, 1074-1080.
190. Jenuwein, T. The epigenetic magic of histone lysine methylation. FASEB J., 2006, 273, 3121-3135.
191. Strahl, B. D.; Allis, C. D. The language of covalent histone modifications. Nature, 2000, 403, 41-45.
192. Li, B.; Carey, M.; Workman, J. L. The role of chromatin during transcription. Cell, 2007, 128, 707-719.
193. Cao, R.; Wang, L. J.; Wang, H. B.; Xia, L.; Erdjument-Bromage, H.; Tempst, P.; Jones, R. S.; Zhang, Y. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science, 2002, 298, 1039-1043.
194. Rea, S.; Eisenhaber, F.; O'Carroll, D.; Strahl, B. D.; Sun, Z. W.; Schmid, M.; Opravil, S.; Mechtler, K.; Ponting, C. P.; Allis, C. D.; Jenuwein, T. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature, 2000, 406, 593-599.
195. Bernstein, B. E.; Mikkelsen, T. S.; Xie, X.; Kamal, M.; Huebert, D. J.; Cuff, J.; Fry, B.; Meissner, A.; Wernig, M.; Plath, K.; Jaenisch, R.; Wagschal, A.; Feil, R.; Schreiber, S. L.; Lander, E. S. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 2006, 125, 315-326.
196. Barski, A.; Cuddapah, S.; Cui, K.; Roh, T. Y.; Schones, D. E.; Wang, Z.; Wei, G.; Chepelev, I.; Zhao, K. High-resolution profiling of histone methylations in the human genome. Cell, 2007, 129, 823-837.
197. Mikkelsen, T. S.; Ku, M.; Jaffe, D. B.; Issac, B.; Lieberman, E.; Giannoukos, G.; Alvarez, P.; Brockman, W.; Kim, T. K.; Koche, R. P.; Lee, W.; Mendenhall, E.; O'Donovan, A.; Presser, A.; Russ, C.; Xie, X.; Meissner, A.; Wernig, M.; Jaenisch, R.; Nusbaum, C.; Lander, E. S.; Bernstein, B. E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature, 2007, 448, 553-560.
198. Heintzman, N. D.; Hon, G. C.; Hawkins, R. D.; Kheradpour, P.; Stark, A.; Harp, L. F.; Ye, Z.; Lee, L. K.; Stuart, R. K.; Ching, C. W.; Ching, K. A.; Antosiewicz-Bourget, J. E.; Liu, H.; Zhang, X.; Green, R. D.; Lobanenkov, V. V.; Stewart, R.; Thomson, J. A.; Crawford, G. E.; Kellis, M.; Ren, B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature, 2009, 459, 108-112.
199. Hawkins, R. D.; Hon, G. C.; Lee, L. K.; Ngo, Q.; Lister, R.; Pelizzola, M.; Edsall, L. E.; Kuan, S.; Luu, Y.; Klugman, S.; Antosiewicz-Bourget, J.; Ye, Z.; Espinoza, C.; Agarwahl, S.; Shen, L.; Ruotti, V.; Wang, W.; Stewart, R.; Thomson, J. A.; Ecker, J. R.; Ren, B. Distinct epigenomic landscapes of pluripotent and lineagecommitted human cells. Cell Stem Cell, 2010, 6, 479-491.
200. Noma, K.; Allis, C. D.; Grewal, S. I. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science, 2001, 293, 1150-1155.
201. Schneider, R.; Bannister, A. J.; Myers, F. A.; Thorne, A. W.; Crane-Robinson, C.; Kouzarides, T. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol., 2004, 6, 73-77.
202. Strahl, B. D.; Ohba, R.; Cook, R. G.; Allis, C. D. Methylation of histone H3 at lysine 4 is highly conserved and correlates with transcriptionally active nuclei in Tetrahymena. Proc. Natl. Acad. Sci. U. S. A., 1999, 96, 14967-14972.
203. Aagaard, L.; Laible, G.; Selenko, P.; Schmid, M.; Dorn, R.; Schotta, G.; Kuhfittig, S.; Wolf, A.; Lebersorger, A.; Singh, P. B.; Reuter, G.; Jenuwein, T. Functional mammalian homologues of the Drosophila PEV-modifier Su(var)3-9 encode centromereassociated proteins which complex with the heterochromatin component M31. EMBO J., 1999, 18, 1923-1938.
204. Zhu, X. N.; Mar, M. H.; Song, J. N.; Zeisel, S. H. Deletion of the Pemt gene increases progenitor cell mitosis, DNA and protein methylation and decreases calretinin expression in embryonic day 17 mouse hippocampus. Dev. Brain Res., 2004, 149, 121-129.
205. Dobosy, J. R.; Fu, V. X.; Desotelle, J. A.; Srinivasan, R.; Kenowski, M. L.; Almassi, N.; Weindruch, R.; Svaren, J.; Jarrard, D. F. A methyl-deficient diet modifies histone methylation and alters Igf2 and H19 repression in the prostate. Prostate, 2008, 68, 1187-1195.
206. Davison, J. M.; Mellott, T. J.; Kovacheva, V. P.; Blusztajn, J. K. Gestational choline supply regulates methylation of histone H3, expression of histone methyltransferases G9a (Kmt1c) and Suv39h1 (Kmt1a) and DNA methylation of their genes in rat fetal liver and brain. J. Biol. Chem., 2009, 284, 1982-1989.
207. Yang, Y.; Liu, Z.; Cermak, J. M.; Tandon, P.; Sarkisian, M. R.; Stafstrom, C. F.; Neill, J. C.; Blusztajn, J. K.; Holmes, G. L. Protective effects of prenatal choline supplementation on seizureinduced memory impairment. J. Neurosci., 2000, 20, RC109.
208. Holmes, G. L.; Yang, Y.; Liu, Z.; Cermak, J. M.; Sarkisian, M. R.; Stafstrom, C. E.; Neill, J. C.; Blusztajn, J. K. Seizure-induced memory impairment is reduced by choline supplementation before or after status epilepticus. Epilepsy Res., 2002, 48, 3-13.
209. Wong-Goodrich, S. J.; Mellott, T. J.; Liu, B.; Blusztajn, J. K.; Williams, C. L. Water maze experience and prenatal choline supplementation differentially promote long-term hippocampal recovery from seizures in adulthood. Hippocampus, 2011, 21, 584-608.
210. Thomas, J. D.; La Fiette, M. H.; Quinn, V. R.; Riley, E. P. Neonatal choline supplementation ameliorates the effects of prenatal alcohol exposure on a discrimination learning task in rats. Neurotoxicol. Teratol., 2000, 22, 703-711.
211. Thomas, J. D.; Biane, J. S.; O'Bryan K.A.; O'Neill T.M.; Dominguez, H. D. Choline supplementation following thirdtrimester-equivalent alcohol exposure attenuates behavioral alterations in rats. Behav. Neurosci., 2007, 121, 120-130.
212. Ryan, S. H.; Williams, J. K.; Thomas, J. D. Choline supplementation attenuates learning deficits associated with neonatal alcohol exposure in the rat: effects of varying the timing of choline administration. Brain Res., 2008, 1237, 91-100.
213. Thomas, J. D.; Abou, E. J.; Dominguez, H. D. Prenatal choline supplementation mitigates the adverse effects of prenatal alcohol exposure on development in rats. Neurotoxicol. Teratol., 2009, 31, 303-31.
214. Thomas, J. D.; Idrus, N. M.; Monk, B. R.; Dominguez, H. D. Prenatal choline supplementation mitigates behavioral alterations associated with prenatal alcohol exposure in rats. Birth Defects Res. A Clin. Mol. Teratol., 2010, 88, 827-887.
215. Thomas, J. D.; Tran, T. D. Choline supplementation mitigates race, but not delay, eyeblink conditioning deficits in rats exposed to alcohol during development. Hippocampus, 2011, 22, 619-630
216. Ricceri, L.; Berger-Sweeney, J. Postnatal choline supplementation in preweanling mice: sexually dimorphic behavioral and neurochemical effects. Behav. Neurosci., 1998, 112, 1387-1392.
217. Nag, N.; Berger-Sweeney, J. E. Postnatal dietary choline supplementation alters behavior in a mouse model of Rett syndrome. Neurobiol. Dis., 2007, 26, 473-480.
218. Stevens, K. E.; Adams, C. E.; Yonchek, J.; Hickel, C.; Danielson, J.; Kisley, M. A. Permanent improvement in deficient sensory inhibition in DBA/2 mice with increased perinatal choline. Psychopharmacology (Berl) 2008, 198, 413-420.
219. Nag, N.; Mellott, T. J.; Berger-Sweeney, J. E. Effects of postnatal dietary choline supplementation on motor regional brain volume and growth factor expression in a mouse model of Rett syndrome. Brain Res., 2008, 1237, 101-109.
220. 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.
221. Ward, B. C.; Kolodny, N. H.; Nag, N.; Berger-Sweeney, J. E. Neurochemical changes in a mouse model of Rett syndrome: changes over time and in response to perinatal choline nutritional supplementation. J. Neurochem., 2009, 108, 361-371.
222. Moon, J.; Chen, M.; Gandhy, S. U.; Strawderman, M.; Levitsky, D. A.; Maclean, K. N.; Strupp, B. J. Perinatal choline supplementation improves cognitive functioning and emotion regulation in the Ts65Dn mouse model of Down syndrome. Behav. Neurosci., 2010, 124, 346-361.
223. Kovacheva, V. P.; Davison, J. M.; Mellott, T. J.; Rogers, A. E.; Yang, S.; O'Brien, M. J.; Blusztajn, J. K. Raising gestational choline intake alters gene expression in DMBA-evoked mammary tumors and prolongs survival. FASEB J, 2009, 23, 1054-1063.
224. Chen, W. G.; Chang, Q.; Lin, Y. X.; Meissner, A.; West, A. E.; Griffith, E. C.; Jaenisch, R.; Greenberg, M. E. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science, 2003, 302, 885-889.
225. Martinowich, K.; Hattori, D.; Wu, H.; Fouse, S.; He, F.; Hu, Y.; Fan, G. P.; Sun, Y. E. DNA methylation-related chromatin remodeling in activity-dependent Bdnf gene regulation. Science, 2003, 302, 890-893.
226. Levenson, J. M.; Roth, T. L.; Lubin, F. D.; Miller, C. A.; Huang, I. C.; Desai, P.; Malone, L. M.; Sweatt, J. D. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J. Biol. Chem., 2006, 281, 15763-15773.
227. Nelson, E. D.; Kavalali, E. T.; Monteggia, L. M. Activitydependent suppression of miniature neurotransmission through the regulation of DNA methylation. J. Neurosci., 2008, 28, 395-406.
228. Yossifoff, M.; Kisliouk, T.; Meiri, N. Dynamic changes in DNA methylation during thermal control establishment affect CREB binding to the brain-derived neurotrophic factor promoter. Eur. J. Neurosci., 2008, 28, 2267-2277.
229. Miller, C. A.; Sweatt, J. D. Covalent modification of DNA regulates memory formation. Neuron, 2007, 53, 857-869.
230. Lubin, F. D.; Roth, T. L.; Sweatt, J. D. Epigenetic regulation of BDNF gene transcription in the consolidation of fear memory. J. Neurosci., 2008, 28, 10576-10586.
231. Miller, C. A.; Gavin, C. F.; White, J. A.; Parrish, R. R.; Honasoge, A.; Yancey, C. R.; Rivera, I. M.; Rubio, M. D.; Rumbaugh, G.; Sweatt, J. D. Cortical DNA methylation maintains remote memory. Nat. Neurosci., 2010, 13, 664-666.
232. Gupta, S.; Kim, S. Y.; Artis, S.; Molfese, D. L.; Schumacher, A.; Sweatt, J. D.; Paylor, R. E.; Lubin, F. D. Histone methylation regulates memory formation. J. Neurosci., 2010, 30, 3589-3599.
233. Poly, C.; Massaro, J. M.; Seshadri, S.; Wolf, P. A.; Cho, E.; Krall, E.; Jacques, P. F.; Au, R. The relation of dietary choline to cognitive performance and white-matter hyperintensity in the Framingham Offspring Cohort1,2. Am. J. Clin. Nutr., 2011, 94, 1584-1591.