Nucleocytoplasmic translocation of HDAC9 regulates gene expression and dendritic growth in developing cortical neurons

European Journal of Neuroscience

Volumn 31, Issue 9, 2010, Pages 1521-1532

  Sugo, Noriyuki ^a   Oshiro, Hiroaki ^a   Takemura, Mitsuhiro ^a   Kobayashi, Toshiaki ^a   Kohno, Yusuke ^a   Uesaka, Naofumi ^a   Song, Wen Jie ^b   Yamamoto, Nobuhiko ^a  

^a OSAKA UNIVERSITY   (Japan)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cerebral cortex; Dendrite; Differentiation; Histone modification; Rodent

Indexed keywords

HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 9; IMMEDIATE EARLY PROTEIN; PROTEIN C FOS; UNCLASSIFIED DRUG; CHROMATIN; HDAC9 PROTEIN, MOUSE; HDAC9 PROTEIN, RAT; REPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL STRUCTURE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; GENE EXPRESSION REGULATION; IN VIVO STUDY; MOUSE; NEOCORTEX; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; RAT; TRANSCRIPTION REGULATION; ACTION POTENTIAL; ACTIVE TRANSPORT; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL ENLARGEMENT; CELL NUCLEUS; CHROMATIN; CYTOLOGY; CYTOPLASM; DENDRITE; GENETICS; METABOLISM; NERVE CELL; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TUMOR CELL LINE;

ACTION POTENTIALS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL ENLARGEMENT; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN; CYTOPLASM; DENDRITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASES; MICE; MICE, INBRED C57BL; NEOCORTEX; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; REPRESSOR PROTEINS;

EID: 77951863880     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07218.x     Document Type: Article

References (60)

1. Aizawa, H., Hu, S.C., Bobb, K., Balakrishnan, K., Ince, G., Gurevich, I., Cowan, M. Ghosh, A. (2004) Dendrite development regulated by CREST, a calcium-regulated transcriptional activator. Science, 303, 197 202.
2. Alberts, A.S., Geneste, O. Treisman, R. (1998) Activation of SRF-regulated chromosomal templates by Rho-family GTPases requires a signal that also induces H4 hyperacetylation. Cell, 92, 475 487.
3. Bartel, D.P., Sheng, M., Lau, L.F. Greenberg, M.E. (1989) Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev., 3, 304 313.
4. Bolger, T.A. Yao, T.P. (2005) Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J. Neurosci., 25, 9544 9553.
5. Broide, R.S., Redwine, J.M., Aftahi, N., Young, W., Bloom, F.E. Winrow, C.J. (2007) Distribution of histone deacetylases 1-11 in the rat brain. J. Mol. Neurosci., 31, 47 58.
6. Chang, S., McKinsey, T.A., Zhang, C.L., Richardson, J.A., Hill, J.A. Olson, E.N. (2004) Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol., 24, 8467 8476.
7. Chawla, S., Vanhoutte, P., Arnold, F.J., Huang, C.L. Bading, H. (2003) Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem., 85, 151 159.
8. Cheung, P., Tanner, K.G., Cheung, W.L., Sassone-Corsi, P., Denu, J.M. Allis, C.D. (2000) Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell, 5, 905 915.
9. Crosio, C., Heitz, E., Allis, C.D., Borrelli, E. Sassone-Corsi, P. (2003) Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci., 116, 4905 4914.
10. Flint, A.C., Maisch, U.S. Kriegstein, A.R. (1997) Postnatal development of low [Mg2+] oscillations in neocortex. J. Neurophysiol., 78, 1990 1996.
11. Fox, K. (2002) Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience, 111, 799 814.
12. Fukuchi-Shimogori, T. Grove, E.A. (2001) Neocortex patterning by the secreted signaling molecule FGF8. Science, 294, 1071 1074.
13. Gaudilliere, B., Konishi, Y., de la Iglesia, N., Yao, G. Bonni, A. (2004) A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis. Neuron, 41, 229 241.
14. Grozinger, C.M. Schreiber, S.L. (2000) Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc. Natl Acad. Sci. USA, 97, 7835 7840.
15. Hattori, S., Murakami, F. Song, W.J. (2003) Quantitative relationship between Kv4.2 mRNA and A-type K+ current in rat striatal cholinergic interneurons during development. J. Neurophysiol., 90, 175 183.
16. Hensch, T.K. (2004) Critical period regulation. Annu. Rev. Neurosci., 27, 549 579.
17. Itoh, K., Stevens, B., Schachner, M. Fields, R.D. (1995) Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science, 270, 1369 1372.
18. Itoh, K., Ozaki, M., Stevens, B. Fields, R.D. (1997) Activity-dependent regulation of N-cadherin in DRG neurons: differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials. J. Neurobiol., 33, 735 748.
19. Katz, L.C. Crowley, J.C. (2002) Development of cortical circuits: lessons from ocular dominance columns. Nat. Rev. Neurosci., 3, 34 42.
20. Katz, L.C. Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133 1138.
21. Linseman, D.A., Bartley, C.M., Le, S.S., Laessig, T.A., Bouchard, R.J., Meintzer, M.K., Li, M. Heidenreich, K.A. (2003) Inactivation of the myocyte enhancer factor-2 repressor histone deacetylase-5 by endogenous Ca(2+)/calmodulin-dependent kinase II promotes depolarization-mediated cerebellar granule neuron survival. J. Biol. Chem., 278, 41472 41481.
22. Liu, Y., Randall, W.R. Schneider, M.F. (2005) Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J. Cell Biol., 168, 887 897.
23. Lyford, G.L., Yamagata, K., Kaufmann, W.E., Barnes, C.A., Sanders, L.K., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Lanahan, A.A. Worley, P.F. (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron, 14, 433 445.
24. Lyons, G.E., Micales, B.K., Schwarz, J., Martin, J.F. Olson, E.N. (1995) Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J. Neurosci., 15, 5727 5738.
25. Majdan, M. Shatz, C.J. (2006) Effects of visual experience on activity-dependent gene regulation in cortex. Nat. Neurosci., 9, 650 659.
26. Mao, Z., Bonni, A., Xia, F., Nadal-Vicens, M. Greenberg, M.E. (1999) Neuronal activity-dependent cell survival mediated by transcription factor MEF2. Science, 286, 785 790.
27. Maravall, M., Koh, I.Y., Lindquist, W.B. Svoboda, K. (2004) Experience-dependent changes in basal dendritic branching of layer 2/3 pyramidal neurons during a critical period for developmental plasticity in rat barrel cortex. Cereb. Cortex, 14, 655 664. (Pubitemid 38669510)
28. Maruyama, T., Matsuura, M., Suzuki, K. Yamamoto, N. (2008) Cooperative activity of multiple upper layer proteins for thalamocortical axon growth. Dev. Neurobiol., 68, 317 331.
29. McAllister, A.K., Lo, D.C. Katz, L.C. (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron, 15, 791 803.
30. McKinsey, T.A., Zhang, C.L., Lu, J. Olson, E.N. (2000) Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature, 408, 106 111.
31. Mejat, A., Ramond, F., Bassel-Duby, R., Khochbin, S., Olson, E.N. Schaeffer, L. (2005) Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat. Neurosci., 8, 313 321.
32. Miller, M. (1981) Maturation of rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons. J. Neurocytol., 10, 859 878. (Pubitemid 12233859)
33. Mirmiran, M. Corner, M. (1982) Neuronal discharge patterns in the occipital cortex of developing rats during active and quiet sleep. Brain Res., 255, 37 48.
34. Morrison, B.E., Majdzadeh, N., Zhang, X., Lyles, A., Bassel-Duby, R., Olson, E.N. D'Mello, S.R. (2006) Neuroprotection by histone deacetylase-related protein. Mol. Cell. Biol., 26, 3550 3564.
35. Niwa, H., Yamamura, K. Miyazaki, J. (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene, 108, 193 199.
36. Petrie, K., Guidez, F., Howell, L., Healy, L., Waxman, S., Greaves, M. Zelent, A. (2003) The histone deacetylase 9 gene encodes multiple protein isoforms. J. Biol. Chem., 278, 16059 16072.
37. Putignano, E., Lonetti, G., Cancedda, L., Ratto, G., Costa, M., Maffei, L. Pizzorusso, T. (2007) Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity. Neuron, 53, 747 759.
38. Redmond, L., Kashani, A.H. Ghosh, A. (2002) Calcium regulation of dendritic growth via CaM kinase IV and CREB-mediated transcription. Neuron, 34, 999 1010.
39. Ruthazer, E.S. Cline, H.T. (2002) Multiphoton imaging of neurons in living tissue: acquisition and analysis of time lapse morphological data. Real-Time Imaging, 8, 175 188.
40. Saito, T. Nakatsuji, N. (2001) Efficient gene transfer into the embryonic mouse brain using in vivo electroporation. Dev. Biol., 240, 237 246.
41. Sparrow, D.B., Miska, E.A., Langley, E., Reynaud-Deonauth, S., Kotecha, S., Towers, N., Spohr, G., Kouzarides, T. Mohun, T.J. (1999) MEF-2 function is modified by a novel co-repressor, MITR. EMBO J., 18, 5085 5098.
42. Strahl, B.D. Allis, C.D. (2000) The language of covalent histone modifications. Nature, 403, 41 45.
43. Sugo, N., Niimi, N., Aratani, Y., Takiguchi-Hayashi, K. Koyama, H. (2004) p53 Deficiency rescues neuronal apoptosis but not differentiation in DNA polymerase beta-deficient mice. Mol. Cell. Biol., 24, 9470 9477.
44. Tabata, H. Nakajima, K. (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience, 103, 865 872.
45. Tao, X., Finkbeiner, S., Arnold, D.B., Shaywitz, A.J. Greenberg, M.E. (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron, 20, 709 726.
46. Tropea, D., Kreiman, G., Lyckman, A., Mukherjee, S., Yu, H., Horng, S. Sur, M. (2006) Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex. Nat. Neurosci., 9, 660 668.
47. Turner, B.M. (2000) Histone acetylation and an epigenetic code. Bioessays, 22, 836 845.
48. Uesaka, N., Hirai, S., Maruyama, T., Ruthazer, E.S. Yamamoto, N. (2005) Activity dependence of cortical axon branch formation: a morphological and electrophysiological study using organotypic slice cultures. J. Neurosci., 25, 1 9.
49. Uesaka, N., Ruthazer, E.S. Yamamoto, N. (2006) The role of neural activity in cortical axon branching. Neuroscientist, 12, 102 106.
50. Wang, A.H., Kruhlak, M.J., Wu, J., Bertos, N.R., Vezmar, M., Posner, B.I., Bazett-Jones, D.P. Yang, X.J. (2000) Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol., 20, 6904 6912.
51. Wayman, G.A., Impey, S., Marks, D., Saneyoshi, T., Grant, W.F., Derkach, V. Soderling, T.R. (2006) Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron, 50, 897 909.
52. West, A.E., Griffith, E.C. Greenberg, M.E. (2002) Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci., 3, 921 931.
53. Wong, R.O. Ghosh, A. (2002) Activity-dependent regulation of dendritic growth and patterning. Nat. Rev. Neurosci., 3, 803 812.
54. Yang, X.J. Gregoire, S. (2005) Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol. Cell. Biol., 25, 2873 2884.
55. Yoneshima, H., Yamasaki, S., Voelker, C.C., Molnar, Z., Christophe, E., Audinat, E., Takemoto, M., Nishiwaki, M., Tsuji, S., Fujita, I. Yamamoto, N. (2006) Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices. Neuroscience, 137, 401 412.
56. Zhang, C.L., McKinsey, T.A. Olson, E.N. (2001) The transcriptional corepressor MITR is a signal-responsive inhibitor of myogenesis. Proc. Natl Acad. Sci. USA, 98, 7354 7359.
57. Zhang, C.L., McKinsey, T.A., Chang, S., Antos, C.L., Hill, J.A. Olson, E.N. (2002) Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell, 110, 479 488.
58. Zhong, Y., Takemoto, M., Fukuda, T., Hattori, Y., Murakami, F., Nakajima, D., Nakayama, M. Yamamoto, N. (2004) Identification of the genes that are expressed in the upper layers of the neocortex. Cereb. Cortex, 14, 1144 1152.
59. Zhou, X., Marks, P.A., Rifkind, R.A. Richon, V.M. (2001) Cloning and characterization of a histone deacetylase, HDAC9. Proc. Natl Acad. Sci. USA, 98, 10572 10577.
60. Zuo, Y., Yang, G., Kwon, E. Gan, W.B. (2005) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature, 436, 261 265.