DNA hypomethylation restricted to the murine forebrain induces cortical degeneration and impairs postnatal neuronal maturation

Human Molecular Genetics

Volumn 18, Issue 15, 2009, Pages 2875-2888

  Hutnick, Leah K ^a   Golshani, Peyman ^a   Namihira, Masakasu ^a   Xue, Zhigang ^a   Matynia, Anna ^a   Yang, X William ^b   Silva, Alcino J ^a,b   Schweizer, Felix E ^a   Fan, Guoping ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; ION CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX ATROPHY; BRAIN MATURATION; CELL SPECIFICITY; CELL SURVIVAL; CONTROLLED STUDY; DNA METHYLATION; FOREBRAIN; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LEARNING DISORDER; MEMORY DISORDER; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL NECROSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL;

ANIMALS; CEREBRAL CORTEX; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; NEUROGENESIS; NEURONS; PROSENCEPHALON;

MURINAE; MUS;

EID: 67650711853     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp222     Document Type: Article

References (48)

1. Bestor, T.H. (2000) The DNA methyltransferases of mammals. Hum. Mol. Genet., 9, 2395-2402.
2. Robertson, K.D. and Wolffe, A.P. (2000) DNA methylation in health and disease. Nat. Rev. Genet., 1, 11-19.
3. Suzuki, M.M. and Bird, A. (2008) DNA methylation landscapes: Provocative insights from epigenomics. Nat. Rev. Genet., 9, 465-476.
4. Goto, K., Numata, M., Komura, J.I., Ono, T., Bestor, T.H. and Kondo, H. (1994) Expression of DNA methyltransferase gene in mature and immature neurons as well as proliferating cells in mice. Differentiation, 56, 39-44.
5. Feng, J., Fouse, S.D. and Fan, G. (2007) Epigenetic regulation of neural gene expression and neuronal function. Pediatr. Res., 61, 58R-63R.
6. Watt, F. and Molloy, P.L. (1988) Cytosine methylation prevents binding to DNA of a HeLa cell transcription factor required for optimal expression of the adenovirus major late promoter. Genes Dev., 2 1136-1143.
7. Klose, R.J. and Bird, A.P. (2006) Genomic DNA methylation: The mark and its mediators. Trends Biochem. Sci., 31, 89-97.
8. Amir, R.E., Van den Veyver, I.B., Wan, M., Tran, C.Q., Francke, U. and Zoghbi, H.Y. (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet., 23 185-188.
9. Martinowich, K., Hattori, D., Wu, H., Fouse, S., He, F., Hu, Y., Fan, G. and Sun, Y.E. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science, 302, 890-893.
10. Chen, W.G., Chang, Q., Lin, Y., Meissner, A., West, A.E., Griffith, E.C., Jaenisch, R. and Greenberg, M.E. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science, 302, 885-889.
11. Horike, S., Cai, S., Miyano, M., Cheng, J.F. and Kohwi-Shigematsu, T. (2005) Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet., 37, 31-40.
12. Chen, R.Z., Akbarian, S., Tudor, M. and Jaenisch, R. (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet., 27, 327-331.
13. Guy, J., Hendrich, B., Holmes, M., Martin, J.E. and Bird, A. (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet., 27, 322-326.
14. Fan, G., Beard, C., Chen, R.Z., Csankovszki, G., Sun, Y., Siniaia, M., Biniszkiewicz, D., Bates, B., Lee, P.P., Kuhn, R. et al. (2001) DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci., 21, 788-797.
15. Takizawa, T., Nakashima, K., Namihira, M., Ochiai, W., Uemura, A., Yanagisawa, M., Fujita, N., Nakao, M. and Taga, T. (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell, 1, 749-758.
16. Fan, G., Martinowich, K., Chin, M.H., He, F., Fouse, S.D., Hutnick, L., Hattori, D., Ge, W., Shen, Y., Wu, H. et al. (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development, 132, 3345-3356.
17. Shimozaki, K., Namihira, M., Nakashima, K. and Taga, T. (2005) Stage-and site-specific DNA demethylation during neural cell development from embryonic stem cells. J. Neurochem., 93, 432-439.
18. Iwasato, T., Datwani, A., Wolf, A.M., Nishiyama, H., Taguchi, Y., Tonegawa, S., Knopfel, T., Erzurumlu, R.S. and Itohara, S. (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature, 406, 726-731.
19. Gorski, J.A., Talley, T., Qiu, M., Puelles, L., Rubenstein, J.L. and Jones, K.R. (2002) Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci., 22, 6309-6314.
20. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
21. Kuff, E.L. and Fewell, J.W. (1985) Intracisternal A-particle gene expression in normal mouse thymus tissue: Gene products and strain-related variability. Mol. Cell. Biol., 5, 474-483.
22. Walsh, C.P. and Bestor, T.H. (1999) Cytosine methylation and mammalian development. Genes Dev., 13, 26-34.
23. Gaudet, F., Rideout, W.M. 3rd, Meissner, A., Dausman, J., Leonhardt, H. and Jaenisch, R. (2004) Dnmt1 expression in pre- and postimplantation embryogenesis and the maintenance of IAP silencing. Mol. Cell. Biol. 24, 1640-1648.
24. Molyneaux, B.J., Arlotta, P., Menezes, J.R. and Macklis, J.D. (2007) Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci., 8, 427-437.
25. Fouse, S.D., Shen, Y., Pellegrini, M., Cole, S., Meissner, A., Van Neste, L., Jaenisch, R. and Fan, G. (2008) 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.
26. Gong, S., Zheng, C., Doughty, M.L., Losos, K., Didkovsky, N., Schambra, U.B., Nowak, N.J., Joyner, A., Leblanc, G., Hatten, M.E. et al. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature, 425, 917-925.
27. Birnbaum, S.G., Varga, A.W., Yuan, L.L., Anderson, A.E., Sweatt, J.D. and Schrader, L.A. (2004) Structure and function of Kv4-family transient potassium channels. Physiol. Rev., 84, 803-833.
28. Rhodes, K.J., Carroll, K.I., Sung, M.A., Doliveira, L.C., Monaghan, M.M., Burke, S.L., Strassle, B.W., Buchwalder, L., Menegola, M., Cao, J. et al. (2004) KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. J. Neurosci., 24, 7903-7915.
29. Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E. et al. (2001) Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet., 27, 31-39.
30. Costa, R.M., Honjo, T. and Silva, A.J. (2003) Learning and memory deficits in Notch mutant mice. Curr. Biol., 13, 1348-1354.
31. Chen, T., Hevi, S., Gay, F., Tsujimoto, N., He, T., Zhang, B., Ueda, Y. and Li, E. (2007) Complete inactivation of DNMT1 leads to mitotic catastrophe in human cancer cells. Nat. Genet., 39, 391-396.
32. Li, H.S., Wang, D., Shen, Q., Schonemann, M.D., Gorski, J.A., Jones, K.R., Temple, S., Jan, L.Y. and Jan, Y.N. (2003) Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron, 40, 1105-1118.
33. Nelson, E.D., Kavalali, E.T. and Monteggia, L.M. (2008) Activity-dependent suppression of miniature neurotransmission through the regulation of DNA methylation. J. Neurosci., 28, 395-406.
34. Ma, D.K., Jang, M.H., Guo, J.U., Kitabatake, Y., Chang, M.L., Pow-Anpongkul, N., Flavell, R.A., Lu, B., Ming, G.L. and Song, H. (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science, 323, 1074-1077.
35. Golshani, P., Hutnick, L., Schweizer, F. and Fan, G. (2005) Conditional Dnmt1 deletion in dorsal forebrain disrupts development of somatosensory barrel cortex and thalamocortical long-term potentiation. Thalamus Relat. Syst., 3, 227-233.
36. Luhmann, H.J., Karpuk, N., Qu, M. and Zilles, K. (1998) Characterization of neuronal migration disorders in neocortical structures. II. Intracellular in vitro recordings. J. Neurophysiol., 80 92-102.
37. Silva, L.R., Gutnick, M.J. and Connors, B.W. (1991) Laminar distribution of neuronal membrane properties in neocortex of normal and reeler mouse. J. Neurophysiol., 66, 2034-2040.
38. Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G.W., Kuhlman, S.J., Welker, E. and Huang, Z.J. (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci., 24, 9598-9611.
39. Jiang, B., Kitamura, A., Yasuda, H., Sohya, K., Maruyama, A., Yanagawa, Y., Obata, K. and Tsumoto, T. (2004) Brain-derived neurotrophic factor acutely depresses excitatory synaptic transmission to GABAergic neurons in visual cortical slices. Eur. J. Neurosci., 20, 709-718.
40. Jin, X., Hu, H., Mathers, P.H. and Agmon, A. (2003) Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures. J. Neurosci., 23, 5662-5673.
41. Mattson, M.P., Kruman, I.I. and Duan, W. (2002) Folic acid and homocysteine in age-related disease. Ageing Res. Rev., 1, 95-111.
42. Kruman, I.I., Culmsee, C., Chan, S.L., Kruman, Y., Guo, Z., Penix, L. and Mattson, M.P. (2000) Homocysteine elicits a DNA damage response in neurons that promotes apoptosis and hypersensitivity to excitotoxicity. J. Neurosci., 20, 6920-6926.
43. Duan, W., Ladenheim, B., Cutler, R.G., Kruman, I.I., Cadet, J.L. and Mattson, M.P. (2002) Dietary folate deficiency and elevated homocysteine levels endanger dopaminergic neurons in models of Parkinson's disease. J. Neurochem., 80, 101-110.
44. Morris, R.G.M. (1981) Spatial localization does not require the presence of local cues. Learning and Motivation, 12, 239-236.
45. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G. and Silva, A.J. (1994) Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell, 79, 59-68.
46. Golshani, P. and Jones, E.G. (1999) Synchronized paroxysmal activity in the developing thalamocortical network mediated by corticothalamic projections and 'silent' synapses. J. Neurosci., 19, 2865-2875.
47. Golshani, P., Liu, X.B. and Jones, E.G. (2001) Differences in quantal amplitude reflect GluR4- subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc. Natl. Acad. Sci. USA, 98, 4172-4177.
48. Hamam, B.N. and Kennedy, T.E. (2003) Visualization of the dendritic arbor of neurons in intact 500 microm thick brain slices. J. Neurosci. Methods, 123, 61-67.