Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons

Nature Neuroscience

Volumn 13, Issue 4, 2010, Pages 423-430

  Feng, Jian ^a   Zhou, Yu ^b,e   Campbell, Susan L ^c   Le, Thuc ^a,b   Li, En ^d   Sweatt, J David ^c   Silva, Alcino J ^b   Fan, Guoping ^a  

^a Department of Human Genetics ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of Alabama at Birmingham   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e QINGDAO UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MONOCYTE CHEMOTACTIC PROTEIN 5; RANTES; STAT1 PROTEIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL LOSS; CELL SIZE; CONTROLLED STUDY; DEREGULATION; DNA METHYLATION; FOREBRAIN; GENE EXPRESSION; HIPPOCAMPUS; KNOCKOUT MOUSE; LEARNING; LEARNING DISORDER; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SYNAPSE; WILD TYPE;

AGE FACTORS; ANIMALS; CELLS, CULTURED; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEARNING; MALE; MEMORY; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEURONS; PROSENCEPHALON; SYNAPSES;

EID: 77950187447     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2514     Document Type: Article

References (50)

1. Tsankova, N., Renthal, W., Kumar, A. & Nestler, E.J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 8, 355-367 (2007).
2. Martinowich, K. et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302, 890-893 (2003).
3. Chen, W.G. et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302, 885-889 (2003).
4. Nelson, E.D., Kavalali, E.T. & Monteggia, L.M. Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J. Neurosci. 28, 395-406 (2008).
5. Feng, J., Fouse, S. & Fan, G. Epigenetic regulation of neural gene expression and neuronal function. Pediatr. Res. 61, 58R-63R (2007).
6. Guan, J.S. et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60 (2009).
7. 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. 79, 734-746 (2005).
8. Goto, K. et al. Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation 56, 39-44 (1994).
9. Okano, M., Bell, D.W., Haber, D.A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
10. Li, E., Bestor, T.H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
11. Fan, G. et al. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21, 788-797 (2001).
12. Golshani, P. , Hutnick, L., Schweizer, F. & Fan, G. Conditional Dnmt1 deletion in dorsal forebrain disrupts development of somatosensory barrel cortex and thalamocortical long-term potentiation. Thalamus Relat. Syst. 3, 227-233 (2005).
13. Hutnick, L.K. et al. DNA hypomethylation restricted to the murine forebrain induces cortical degeneration and impairs postnatal neuronal maturation. Hum. Mol. Genet. 18, 2875-2888 (2009).
14. Nguyen, S., Meletis, K., Fu, D., Jhaveri, S. & Jaenisch, R. Ablation of de novo DNA methyltransferase Dnmt3a in the nervous system leads to neuromuscular defects and shortened lifespan. Dev. Dyn. 236, 1663-1676 (2007).
15. Fan, G. et al. DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132, 3345-3356 (2005).
16. Endres, M., Fan, G., Meisel, A., Dirnagl, U. & Jaenisch, R. Effects of cerebral ischemia in mice lacking DNA methyltransferase 1 in post-mitotic neurons. Neuroreport 12, 3763-3766 (2001).
17. Miller, C.A. & Sweatt, J.D. Covalent modifcation of DNA regulates memory formation. Neuron 53, 857-869 (2007).
18. Levenson, J.M. et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J. Biol. Chem. 281, 15763-15773 (2006).
19. Jüttermann, R., Li, E. & Jaenisch, R. Toxicity of 5-aza-2′-deoxycytidine to mammalian cells is mediated primarily by covalent trapping of DNA methyltransferase rather than DNA demethylation. Proc. Natl. Acad. Sci. USA 91, 11797-11801 (1994).
20. Ooi, S.K. & Bestor, T.H. The colorful history of active DNA demethylation. Cell 133, 1145-1148 (2008).
21. Weaver, I.C. et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847-854 (2004).
22. Weaver, I.C. et al. Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J. Neurosci. 25, 11045-11054 (2005).
23. Ma, D.K. et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077 (2009).
24. Xu, G.L. et al. Chromosome instability and immunodefciency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-191 (1999).
25. Ouimet, C.C., McGuinness, T.L. & Greengard, P. Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc. Natl. Acad. Sci. USA 81, 5604-5608 (1984).
26. Huh, G.S. et al. Functional requirement for class I MHC in CNS development and plasticity. Science 290, 2155-2159 (2000).
27. Stevens, B. et al. The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164-1178 (2007).
28. Tropea, D. et al. Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci. 9, 660-668 (2006).
29. Neumann, H., Schmidt, H., Cavalie, A., Jenne, D. & Wekerle, H. Major histocompatibility complex (MHC) class I gene expression in single neurons of the central nervous system: differential regulation by interferon (IFN)-gamma and tumor necrosis factor (TNF)-alpha. J. Exp. Med. 185, 305-316 (1997).
30. Fouse, S.D. et al. Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2, 160-169 (2008).
31. Rhee, I. et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552-556 (2002).
32. Chen, T., Ueda, Y., Dodge, J.E., Wang, Z. & Li, E. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23, 5594-5605 (2003).
33. Liang, G. et al. Cooperativity between DNA methyltransferases in the maintenance methylation of repetitive elements. Mol. Cell. Biol. 22, 480-491 (2002).
34. Bachman, K.E., Rountree, M.R. & Baylin, S.B. Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J. Biol. Chem. 276, 32282-32287 (2001).
35. Boulanger, L.M. & Shatz, C.J. Immune signaling in neural development, synaptic plasticity and disease. Nat. Rev. Neurosci. 5, 521-531 (2004).
36. Perry, V.H. & O'Connor, V. C1q: the perfect complement for a synaptic feast? Nat. Rev. Neurosci. 9, 807-811 (2008).
37. Jackson-Grusby, L. et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27, 31-39 (2001).
38. Bhattacharya, S.K., Ramchandani, S., Cervoni, N. & Szyf, M. A mammalian protein with specifc demethylase activity for mCpG DNA. Nature 397, 579-583 (1999).
39. Barreto, G. et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445, 671-675 (2007).
40. Brooks, P.J., Marietta, C. & Goldman, D. DNA mismatch repair and DNA methylation in adult brain neurons. J. Neurosci. 16, 939-945 (1996).
41. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930 (2009).
42. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
43. Dodge, J.E. et al. Inactivation of Dnmt3b in mouse embryonic fbroblasts results in DNA hypomethylation, chromosomal instability, and spontaneous immortalization. J. Biol. Chem. 280, 17986-17991 (2005).
44. Han, Y.G. et al. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat. Neurosci. 11, 277-284 (2008).
45. Lu, X.H. et al. Bacterial artifcial chromosome transgenic mice expressing a truncated mutant parkin exhibit age-dependent hypokinetic motor defcits, dopaminergic neuron degeneration, and accumulation of proteinase K-resistant alpha-synuclein. J. Neurosci. 29, 1962-1976 (2009).
46. Cui, L. et al. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127, 59-69 (2006).
47. Ethell, I.M. et al. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31, 1001-1013 (2001).
48. Jiang, Y., Matevossian, A., Huang, H.S., Straubhaar, J. & Akbarian, S. Isolation of neuronal chromatin from brain tissue. BMC Neurosci. 9, 42 (2008).
49. Crain, P. F. Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry. Methods Enzymol. 193, 782-790 (1990).
50. Song, L.J.S., Kazim, L. & Karpf, A.R. Specifc method for the determination of genomic DNA methylation by liquid chromatography-electrospray ionization tandem mass spectrometry. Anal. Chem. 77, 504-510 (2005).