Cited by 167Epigenetics and DNA MethylationFolate and B Vitamins ResearchNeurogenesis and neuroplasticity mechanisms

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Choline deficiency alters global histone methylation and epigenetic marking at the Rel site of the calbindin 1 gene

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Mehedint, Mihai G., Niculescu, Mihai D., Craciunescu, Corneliu N., Zeisel, Steven H.·2010·The FASEB Journal

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Abstract

Maternal choline availability is essential for fetal neurogenesis. Choline deprivation (CD) causes hypomethylation of specific CpG islands in genes controlling cell cycling in fetal hippocampus. We now report that, in C57BL/6 mice, CD during gestational days 12-17 also altered methylation of the histone H3 in E17 fetal hippocampi. In the ventricular and subventricular zones, monomethyl-lysine 9 of H3 (H3K9me1) was decreased by 25% (P<0.01), and in the pyramidal layer, dimethyl-lysine 9 of H3 (H3K9me2) was decreased by 37% (P<0.05). These changes were region specific and were not observed in whole-brain preparations. Also, the same effects of CD on H3 methylation were observed in E14 neural progenitor cells (NPCs) in culture. Changes in G9a histone methyltransferase might mediate altered H3K9me2,1. Gene expression of G9a was decreased by 80% in CD NPCs (P<0.001). In CD, H3 was hypomethylated upstream of the RE1 binding site in the calbindin 1 promoter, and 1 CpG site within the calbindin1 promoter was hypermethylated. REST binding to RE1 (recruits G9a) was decreased by 45% (P<0.01) in CD. These changes resulted in increased expression of calbindin 1 in CD (260%; P<0.05). Thus, CD modulates histone methylation in NPCs, and this could underlie the observed changes in neurogenesis.

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PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 316,394
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860
EMBOSS: the European molecular biology open software suite.
Rice, P., Longden, I., & Bleasby, A. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02024-2 · Cited by 9,466
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679
Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals
Jaenisch, R., & Bird, A. (2003) · Nature Genetics · doi:10.1038/ng1089 · Cited by 6,325
Histone demethylation mediated by the nuclear amine oxidase homolog LSD1
Shi, Y., Lan, F., Matson, C., Mulligan, P., Whetstine, J. R., Cole, P. A., Casero, R. A., & Shi, Y. (2004) · Cell · doi:10.1016/j.cell.2004.12.012 · Cited by 4,051
Histone demethylation by a family of JmjC domain-containing proteins
Tsukada, Y.-I., Fang, J., Erdjument‐Bromage, H., Warren, M., Borchers, C. H., Tempst, P., & Zhang, Y. (2005) · Nature · doi:10.1038/nature04433 · Cited by 2,244
The diverse functions of histone lysine methylation
Martin, C., & Zhang, Y. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1761 · Cited by 2,157
Active Genes Are Tri-Methylated at K4 of Histone H3
Santos-Rosa, H., Schneider, R., Bannister, A. J., Sherriff, J., Bernstein, B. E., Emre, N. C. T., Schreiber, S. L., Mellor, J., & Kouzarides, T. (2002) · Nature · doi:10.1038/nature01080 · Cited by 2,138
Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tailsPreprint
Zhang, Y., & Reinberg, D. (2001) · Genes & Development · doi:10.1101/gad.927301 · Cited by 1,639

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Authors: Mehedint, M. G., Niculescu, M. D., Craciunescu, C. N., & Zeisel, S. H.
Affiliations: University of North Carolina at Chapel Hill (US)
Corresponding author: Zeisel, Steven H.
ORCID: Niculescu, Mihai D.
Zeisel, Steven H.
Venue: The FASEB Journal
Publisher: Wiley
Published: 2009-09-14
Volume: 24
Issue: 1
Pages: 184-195
ISSN: 0892-6638 (ISSN-L)
1530-6860
DOI: 10.1096/fj.09-140145
PMC: PMC2797040
OpenAlex: W2070463636
Cited by: 167
References: 77
Citations by year: 2026: 3 · 2025: 1 · 2024: 9 · 2023: 2 · 2022: 13 · 2021: 12 · 2020: 12 · 2019: 11 · 2018: 4 · 2017: 15 · 2016: 11 · 2015: 8 · 2014: 12 · 2013: 7 · 2012: 27
FWCI: 6.31
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The FASEB Journal (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (AG-09525, DK-55865)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Nursing › Nutrition and Dietetics › Folate and B Vitamins Research
Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords: choline deficiency, histone H3 methylation, H3K9me1, H3K9me2, G9a, rest, neural progenitor cells, fetal hippocampus, neurogenesis, epigenetic regulation, CpG methylation, fetal development
MeSH terms: RE1-Silencing Transcription Factor, Animals, Base Sequence, Binding Sites, Cells, Cultured, Choline Deficiency, DNA, Female, Hippocampus, Histones, Methylation, Mice, Inbred C57BL, Mitosis, Models, Biological, Pregnancy, Promoter Regions, Genetic, Histone-Lysine N-Methyltransferase, Repressor Proteins, Apoptosis, CpG Islands, Epigenesis, Genetic, Mice, Embryonic Stem Cells, Calbindins, S100 Calcium Binding Protein G, Calbindin 1

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Choline deficiency alters global histone methylation and epigenetic marking at the Rel site of the calbindin 1 gene

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