Modulation of neurogenesis by targeting epigenetic enzymes using small molecules: An overview

ACS Chemical Neuroscience

Volumn 5, Issue 12, 2014, Pages 1164-1177

  Swaminathan, Amrutha ^a   Kumar, Manoj ^a   Sinha, Sarmistha Halder ^a   Schneider Anthony, Anne ^b   Boutillier, Anne Laurence ^b   Kundu, Tapas K ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Acetyltransferase; DNA methylation; Histone modifications; Memory; Neurodegeneration; Neurogenesis; Neurotherapeutics

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CILOSTAZOL; CURCUMIN; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; SOLASODINE; CHOLINE ACETYLTRANSFERASE;

ALZHEIMER DISEASE; BRAIN TUMOR; CEREBROVASCULAR ACCIDENT; DEGENERATIVE DISEASE; DNA METHYLATION; DRUG SYNTHESIS; DRUG TARGETING; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE MUTATION; GROUPS BY AGE; HISTONE ACETYLATION; HISTONE MODIFICATION; HUMAN; HUNTINGTON CHOREA; LEARNING; MEMORY; NERVOUS SYSTEM DEVELOPMENT; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; POSTNATAL DEVELOPMENT; PROTEIN TARGETING; REVIEW; ANIMAL; CELL DIFFERENTIATION; DRUG EFFECTS; ENZYMOLOGY; GENETIC EPIGENESIS; METABOLISM; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY;

MAMMALIA;

ANIMALS; CELL DIFFERENTIATION; CHOLINE O-ACETYLTRANSFERASE; DNA METHYLATION; EPIGENESIS, GENETIC; HISTONE ACETYLTRANSFERASES; HISTONES; NEURAL STEM CELLS; NEUROGENESIS; NEURONS;

EID: 84918591881     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn500117a     Document Type: Review

References (173)

1. Ming, G. L., and Song, H. (2011) Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 70, 687-702.
2. Karch, K. R., Denizio, J. E., Black, B. E., and Garcia, B. A. (2013) Identification and interrogation of combinatorial histone modifications. Front. Genet. 4, 264.
3. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705.
4. Spemann, H., and Mangold, H. (2001) Induction of embryonic primordia by implantation of organizers from a different species. 1923. Int. J. Dev. Biol. 45, 13-38.
5. Patapoutian, A., and Reichardt, L. F. (2000) Roles of Wnt proteins in neural development and maintenance. Curr. Opin. Neurobiol. 10, 392-399.
6. Louvi, A., and Artavanis-Tsakonas, S. (2006) Notch signalling in vertebrate neural development. Nat. Rev. Neurosci 7, 93-102.
7. Hemmati-Brivanlou, A., Kelly, O. G., and Melton, D. A. (1994) Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295.
8. Guerout, N., Li, X., and Barnabe-Heider, F. (2014) Cell fate control in the developing central nervous system. Exp. Cell Res. 321, 77-83.
9. Sidman, R. L., and Rakic, P. (1973) Neuronal migration, with special reference to developing human brain: A review. Brain Res. 62, 1-35.
10. Kuan, C. Y., Roth, K. A., Flavell, R. A., and Rakic, P. (2000) Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 23, 291-297.
11. Horner, P. J., and Gage, F. H. (2000) Regenerating the damaged central nervous system. Nature 407, 963-970.
12. Altman, J., and Das, G. D. (1965) Post-natal origin of microneurones in the rat brain. Nature 207, 953-956.
13. Reynolds, B. A., and Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
14. Yuan, T. F., and Arias-Carrion, O. (2011) Adult neurogenesis in the hypothalamus: Evidence, functions, and implications. CNS Neurol. Disord.: Drug Targets 10, 433-439.
15. Gemma, C., and Bachstetter, A. D. (2013) The role of microglia in adult hippocampal neurogenesis. Front. Cell. Neurosci. 7, 229.
16. Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., and Gage, F. H. (1998) Neurogenesis in the adult human hippocampus. Nat. Med. 4, 1313-1317.
17. Cayre, M., Strambi, C., and Strambi, A. (1994) Neurogenesis in an adult insect brain and its hormonal control. Nature 368, 57-59.
18. Kim, W. R., Christian, K., Ming, G. L., and Song, H. (2012) Time-dependent involvement of adult-born dentate granule cells in behavior. Behav. Brain Res. 227, 470-479.
19. Arruda-Carvalho, M., Sakaguchi, M., Akers, K. G., Josselyn, S. A., and Frankland, P. W. (2011) Posttraining ablation of adult-generated neurons degrades previously acquired memories. J. Neurosci. 31, 15113-15127.
20. Drew, M. R., Denny, C. A., and Hen, R. (2010) Arrest of adult hippocampal neurogenesis in mice impairs single- but not multiple-trial contextual fear conditioning. Behav. Neurosci. 124, 446-454.
21. Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., and Hen, R. (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470.
22. Aimone, J. B., Deng, W., and Gage, F. H. (2011) Resolving new memories: A critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 70, 589-596.
23. Trouche, S., Bontempi, B., Roullet, P., and Rampon, C. (2009) Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc. Natl. Acad. Sci. U. S. A. 106, 5919-5924.
24. Gu, Y., Arruda-Carvalho, M., Wang, J., Janoschka, S. R., Josselyn, S. A., Frankland, P. W., and Ge, S. (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat. Neurosci 15, 1700-1706.
25. Akers, K. G., Martinez-Canabal, A., Restivo, L., Yiu, A. P., De Cristofaro, A., Hsiang, H. L., Wheeler, A. L., Guskjolen, A., Niibori, Y., Shoji, H., Ohira, K., Richards, B. A., Miyakawa, T., Josselyn, S. A., and Frankland, P. W. (2014) Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 344, 598-602.
26. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A., and McMahon, A. P. (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
27. Fisher, A., and Caudy, M. (1998) The function of hairy-related bHLH repressor proteins in cell fate decisions. BioEssays 20, 298-306.
28. Chalmers, A. D., Welchman, D., and Papalopulu, N. (2002) Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. Dev. Cell 2, 171-182.
29. Geling, A., Plessy, C., Rastegar, S., Strahle, U., and Bally-Cuif, L. (2004) Her5 acts as a prepattern factor that blocks neurogenin1 and coe2 expression upstream of Notch to inhibit neurogenesis at the midbrain-hindbrain boundary. Development 131, 1993-2006.
30. Cau, E., Gradwohl, G., Casarosa, S., Kageyama, R., and Guillemot, F. (2000) Hes genes regulate sequential stages of neurogenesis in the olfactory epithelium. Development 127, 2323-2332.
31. Kiecker, C., and Lumsden, A. (2012) The role of organizers in patterning the nervous system. Annu. Rev. Neurosci. 35, 347-367.
32. Follert, P., Cremer, H., and Beclin, C. (2014) MicroRNAs in brain development and function: A matter of flexibility and stability. Front. Mol. Neurosci. 7, 5.
33. Ji, F., Lv, X., and Jiao, J. (2013) The role of microRNAs in neural stem cells and neurogenesis. J. Genet Genomics 40, 61-66.
34. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F., and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260.
35. Delcuve, G. P., Rastegar, M., and Davie, J. R. (2009) Epigenetic control. J. Cell. Physiol. 219, 243-250.
36. Tropberger, P., and Schneider, R. (2010) Going global: Novel histone modifications in the globular domain of H3. Epigenetics 5, 112-117.
37. Bernstein, B. E., Meissner, A., and Lander, E. S. (2007) The mammalian epigenome. Cell 128, 669-681.
38. Selvi, R. B., and Kundu, T. K. (2009) Reversible acetylation of chromatin: Implication in regulation of gene expression, disease and therapeutics. Biotechnol. J. 4, 375-390.
39. Serra, I., Avola, R., Condorelli, D. F., Surrentino, S., Renis, M., Kamiyama, M., Hashim, G. A., and Giuffrida, A. M. (1986) Acetylation and phosphorylation of histones and nonhistone chromosomal proteins in neuronal and glial nuclei purified from cerebral hemispheres of developing rat brain. J. Neurochem. 46, 1881-1887.
40. Cho, B., Kim, H. J., Kim, H., and Sun, W. (2011) Changes in the Histone Acetylation Patterns during the Development of the Nervous System. Exp. Neurobiol. 20, 81-84.
41. Yao, T. P., Oh, S. P., Fuchs, M., Zhou, N. D., Ch'ng, L. E., Newsome, D., Bronson, R. T., Li, E., Livingston, D. M., and Eckner, R. (1998) Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 93, 361-372.
42. Tanaka, Y., Naruse, I., Hongo, T., Xu, M., Nakahata, T., Maekawa, T., and Ishii, S. (2000) Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech. Dev. 95, 133-145.
43. Kalkhoven, E., Roelfsema, J. H., Teunissen, H., den Boer, A., Ariyurek, Y., Zantema, A., Breuning, M. H., Hennekam, R. C., and Peters, D. J. (2003) Loss of CBP acetyltransferase activity by PHD finger mutations in Rubinstein-Taybi syndrome. Hum. Mol. Genet. 12, 441-450.
44. Tsui, D., Voronova, A., Gallagher, D., Kaplan, D. R., Miller, F. D., and Wang, J. (2014) CBP regulates the differentiation of interneurons from ventral forebrain neural precursors during murine development. Dev. Biol. 385, 230-241.
45. Wang, J., Weaver, I. C., Gauthier-Fisher, A., Wang, H., He, L., Yeomans, J., Wondisford, F., Kaplan, D. R., and Miller, F. D. (2010) CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev. Cell 18, 114-125.
46. Lopez-Atalaya, J. P., Ciccarelli, A., Viosca, J., Valor, L. M., Jimenez-Minchan, M., Canals, S., Giustetto, M., and Barco, A. (2011) CBP is required for environmental enrichment-induced neurogenesis and cognitive enhancement. EMBO J. 30, 4287-4298.
47. Bu, P., Evrard, Y. A., Lozano, G., and Dent, S. Y. (2007) Loss of Gcn5 acetyltransferase activity leads to neural tube closure defects and exencephaly in mouse embryos. Mol. Cell. Biol. 27, 3405-3416.
48. Xu, W., Edmondson, D. G., Evrard, Y. A., Wakamiya, M., Behringer, R. R., and Roth, S. Y. (2000) Loss of Gcn5l2 leads to increased apoptosis and mesodermal defects during mouse development. Nat. Genet. 26, 229-232.
49. Martinez-Cerdeno, V., Lemen, J. M., Chan, V., Wey, A., Lin, W., Dent, S. R., and Knoepfler, P. S. (2012) N-Myc and GCN5 regulate significantly overlapping transcriptional programs in neural stem cells. PLoS One 7, e39456.
50. Merson, T. D., Dixon, M. P., Collin, C., Rietze, R. L., Bartlett, P. F., Thomas, T., and Voss, A. K. (2006) The transcriptional coactivator Querkopf controls adult neurogenesis. J. Neurosci. 26, 11359-11370.
51. de Ruijter, A. J., van Gennip, A. H., Caron, H. N., Kemp, S., and van Kuilenburg, A. B. (2003) Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem. J. 370, 737-749.
52. McQuown, S. C., and Wood, M. A. (2011) HDAC3 and the molecular brake pad hypothesis. Neurobiol. Learn. Mem. 96, 27-34.
53. Jawerka, M., Colak, D., Dimou, L., Spiller, C., Lagger, S., Montgomery, R. L., Olson, E. N., Wurst, W., Gottlicher, M., and Gotz, M. (2010) The specific role of histone deacetylase 2 in adult neurogenesis. Neuron Glia Biol. 6, 93-107.
54. Ajamian, F., Suuronen, T., Salminen, A., and Reeben, M. (2003) Upregulation of class II histone deacetylases mRNA during neural differentiation of cultured rat hippocampal progenitor cells. Neurosci. Lett. 346, 57-60.
55. Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X. F., and Yao, T. P. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458.
56. Ringrose, L., and Paro, R. (2007) Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134, 223-232.
57. Ng, R. K., and Gurdon, J. B. (2008) Epigenetic inheritance of cell differentiation status. Cell Cycle 7, 1173-1177.
58. Molofsky, A. V., Pardal, R., Iwashita, T., Park, I. K., Clarke, M. F., and Morrison, S. J. (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 425, 962-967.
59. Lim, D. A., Huang, Y. C., Swigut, T., Mirick, A. L., Garcia-Verdugo, J. M., Wysocka, J., Ernst, P., and Alvarez-Buylla, A. (2009) Chromatin remodelling factor Mll1 is essential for neurogenesis from postnatal neural stem cells. Nature 458, 529-533.
60. Sher, F., Rossler, R., Brouwer, N., Balasubramaniyan, V., Boddeke, E., and Copray, S. (2008) Differentiation of neural stem cells into oligodendrocytes: Involvement of the polycomb group protein Ezh2. Stem Cells 26, 2875-2883.
61. Zhang, J., Ji, F., Liu, Y., Lei, X., Li, H., Ji, G., Yuan, Z., and Jiao, J. (2014) Ezh2 regulates adult hippocampal neurogenesis and memory. J. Neurosci. 34, 5184-5199.
62. Hwang, W. W., Salinas, R. D., Siu, J. J., Kelley, K. W., Delgado, R. N., Paredes, M. F., Alvarez-Buylla, A., Oldham, M. C., and Lim, D. A. (2014) Distinct and separable roles for EZH2 in neurogenic astroglia. eLife 3, e02439.
63. Estaras, C., Akizu, N., Garcia, A., Beltran, S., de la Cruz, X., and Martinez-Balbas, M. A. (2012) Genome-wide analysis reveals that Smad3 and JMJD3 HDM co-activate the neural developmental program. Development 139, 2681-2691.
64. Jepsen, K., Solum, D., Zhou, T., McEvilly, R. J., Kim, H. J., Glass, C. K., Hermanson, O., and Rosenfeld, M. G. (2007) SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron. Nature 450, 415-419.
65. Iwase, S., Lan, F., Bayliss, P., de la Torre-Ubieta, L., Huarte, M., Qi, H. H., Whetstine, J. R., Bonni, A., Roberts, T. M., and Shi, Y. (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128, 1077-1088.
66. Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., and Wysocka, J. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470, 279-283.
67. Park, D. H., Hong, S. J., Salinas, R. D., Liu, S. J., Sun, S. W., Sgualdino, J., Testa, G., Matzuk, M. M., Iwamori, N., and Lim, D. A. (2014) Activation of Neuronal Gene Expression by the JMJD3 Demethylase Is Required for Postnatal and Adult Brain Neurogenesis. Cell Rep. 8, 1290-1299.
68. Suzuki, M. M., and Bird, A. (2008) DNA methylation landscapes: Provocative insights from epigenomics. Nat. Rev. Genet 9, 465-476.
69. Wu, S. C., and Zhang, Y. (2010) Active DNA demethylation: Many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620.
70. Goll, M. G., and Bestor, T. H. (2005) Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514.
71. Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., Gnirke, A., Jaenisch, R., and Lander, E. S. (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
72. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M., and Schubeler, D. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766.
73. Fan, G., Beard, C., Chen, R. Z., Csankovszki, G., Sun, Y., Siniaia, M., Biniszkiewicz, D., Bates, B., Lee, P. P., Kuhn, R., Trumpp, A., Poon, C., Wilson, C. B., and Jaenisch, R. (2001) DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21, 788-797.
74. Fan, G., Martinowich, K., Chin, M. H., He, F., Fouse, S. D., Hutnick, L., Hattori, D., Ge, W., Shen, Y., Wu, H., ten Hoeve, J., Shuai, K., and Sun, Y. E. (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132, 3345-3356.
75. Defossez, P. A., and Stancheva, I. (2011) Biological functions of methyl-CpG-binding proteins. Prog. Mol. Biol. Transl. Sci. 101, 377-398.
76. Zhao, X., Ueba, T., Christie, B. R., Barkho, B., McConnell, M. J., Nakashima, K., Lein, E. S., Eadie, B. D., Willhoite, A. R., Muotri, A. R., Summers, R. G., Chun, J., Lee, K. F., and Gage, F. H. (2003) Mice lacking methyl-CpG binding protein 1 have deficits in adult neurogenesis and hippocampal function. Proc. Natl. Acad. Sci. U. S. A. 100, 6777-6782.
77. 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.
78. Shahbazian, M., Young, J., Yuva-Paylor, L., Spencer, C., Antalffy, B., Noebels, J., Armstrong, D., Paylor, R., and Zoghbi, H. (2002) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron 35, 243-254.
79. Shahbazian, M. D., Antalffy, B., Armstrong, D. L., and Zoghbi, H. Y. (2002) Insight into Rett syndrome: MeCP2 levels display tissue- and cell-specific differences and correlate with neuronal maturation. Hum. Mol. Genet. 11, 115-124.
80. Shahbazian, M. D., and Zoghbi, H. Y. (2002) Rett syndrome and MeCP2: Linking epigenetics and neuronal function. Am. J. Hum. Genet. 71, 1259-1272.
81. Smrt, R. D., Eaves-Egenes, J., Barkho, B. Z., Santistevan, N. J., Zhao, C., Aimone, J. B., Gage, F. H., and Zhao, X. (2007) Mecp2 deficiency leads to delayed maturation and altered gene expression in hippocampal neurons. Neurobiol. Dis. 27, 77-89.
82. Tsujimura, K., Abematsu, M., Kohyama, J., Namihira, M., and Nakashima, K. (2009) Neuronal differentiation of neural precursor cells is promoted by the methyl-CpG-binding protein MeCP2. Exp. Neurol. 219, 104-111.
83. Ninkovic, J., Steiner-Mezzadri, A., Jawerka, M., Akinci, U., Masserdotti, G., Petricca, S., Fischer, J., von Holst, A., Beckers, J., Lie, C. D., Petrik, D., Miller, E., Tang, J., Wu, J., Lefebvre, V., Demmers, J., Eisch, A., Metzger, D., Crabtree, G., Irmler, M., Poot, R., and Gotz, M. (2013) The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13, 403-418.
84. Hsieh, J., Nakashima, K., Kuwabara, T., Mejia, E., and Gage, F. H. (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 101, 16659-16664.
85. Gao, Z., Ure, K., Ables, J. L., Lagace, D. C., Nave, K. A., Goebbels, S., Eisch, A. J., and Hsieh, J. (2009) Neurod1 is essential for the survival and maturation of adult-born neurons. Nat. Neurosci 12, 1090-1092.
86. Hao, Y., Creson, T., Zhang, L., Li, P., Du, F., Yuan, P., Gould, T. D., Manji, H. K., and Chen, G. (2004) Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J. Neurosci. 24, 6590-6599.
87. Yu, I. T., Park, J. Y., Kim, S. H., Lee, J. S., Kim, Y. S., and Son, H. (2009) Valproic acid promotes neuronal differentiation by induction of proneural factors in association with H4 acetylation. Neuropharmacology 56, 473-480.
88. Zhou, Q., Dalgard, C. L., Wynder, C., and Doughty, M. L. (2011) Valproic acid inhibits neurosphere formation by adult subventricular cells by a lithium-sensitive mechanism. Neurosci. Lett. 500, 202-206.
89. Zhou, Q., Dalgard, C. L., Wynder, C., and Doughty, M. L. (2011) Histone deacetylase inhibitors SAHA and sodium butyrate block G1-to-S cell cycle progression in neurosphere formation by adult subventricular cells. BMC Neurosci. 12, 50.
90. Shaked, M., Weissmuller, K., Svoboda, H., Hortschansky, P., Nishino, N., Wolfl, S., and Tucker, K. L. (2008) Histone deacetylases control neurogenesis in embryonic brain by inhibition of BMP2/4 signaling. PLoS One 3, e2668.
91. Balasubramanyam, K., Swaminathan, V., Ranganathan, A., and Kundu, T. K. (2003) Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278, 19134-19140.
92. Selvi, B. R., Jagadeesan, D., Suma, B. S., Nagashankar, G., Arif, M., Balasubramanyam, K., Eswaramoorthy, M., and Kundu, T. K. (2008) Intrinsically fluorescent carbon nanospheres as a nuclear targeting vector: Delivery of membrane-impermeable molecule to modulate gene expression in vivo. Nano Lett. 8, 3182-3188.
93. Selvi, R. B., Chatterjee, S., Jagadeesan, D., Chaturbedy, P., Suma, B. S., Eswaramoorthy, M., and Kundu, T. K. (2012) ATP driven clathrin dependent entry of carbon nanospheres prefer cells with glucose receptors. J. Nanobiotechnology 10, 35.
94. Chatterjee, S., Mizar, P., Cassel, R., Neidl, R., Selvi, B. R., Mohankrishna, D. V., Vedamurthy, B. M., Schneider, A., Bousiges, O., Mathis, C., Cassel, J. C., Eswaramoorthy, M., Kundu, T. K., and Boutillier, A. L. (2013) A novel activator of CBP/p300 acetyltransferases promotes neurogenesis and extends memory duration in adult mice. J. Neurosci. 33, 10698-10712.
95. Furdas, S. D., Kannan, S., Sippl, W., and Jung, M. (2012) Small molecule inhibitors of histone acetyltransferases as epigenetic tools and drug candidates. Arch Pharm. (Weinheim, Ger.) 345, 7-21.
96. Swank, M. W., and Sweatt, J. D. (2001) Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J. Neurosci. 21, 3383-3391.
97. Schmitt, M., and Matthies, H. (1979) Biochemical studies on histones of the central nervous system. III. Incorporation of [14C]-acetate into the histones of different rat brain regions during a learning experiment. Acta Biol. Med. Ger 38, 683-689.
98. Graff, J., and Tsai, L. H. (2013) Histone acetylation: Molecular mnemonics on the chromatin. Nat. Rev. Neurosci. 14, 97-111.
99. McQuown, S. C., Barrett, R. M., Matheos, D. P., Post, R. J., Rogge, G. A., Alenghat, T., Mullican, S. E., Jones, S., Rusche, J. R., Lazar, M. A., and Wood, M. A. (2011) HDAC3 is a critical negative regulator of long-term memory formation. J. Neurosci. 31, 764-774.
100. Guan, J. S., Haggarty, S. J., Giacometti, E., Dannenberg, J. H., Joseph, N., Gao, J., Nieland, T. J., Zhou, Y., Wang, X., Mazitschek, R., Bradner, J. E., DePinho, R. A., Jaenisch, R., and Tsai, L. H. (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459, 55-60.
101. Frankland, P. W., and Bontempi, B. (2005) The organization of recent and remote memories. Nat. Rev. Neurosci 6, 119-130.
102. Rouaux, C., Jokic, N., Mbebi, C., Boutillier, S., Loeffler, J. P., and Boutillier, A. L. (2003) Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J. 22, 6537-6549.
103. Jiang, H., Nucifora, F. C., Jr., Ross, C. A., and DeFranco, D. B. (2003) Cell death triggered by polyglutamine-expanded huntingtin in a neuronal cell line is associated with degradation of CREB-binding protein. Hum. Mol. Genet. 12, 1-12.
104. Marambaud, P., Wen, P. H., Dutt, A., Shioi, J., Takashima, A., Siman, R., and Robakis, N. K. (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 114, 635-645.
105. Nucifora, F. C., Jr., Sasaki, M., Peters, M. F., Huang, H., Cooper, J. K., Yamada, M., Takahashi, H., Tsuji, S., Troncoso, J., Dawson, V. L., Dawson, T. M., and Ross, C. A. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291, 2423-2428.
106. Huang, Y., Myers, S. J., and Dingledine, R. (1999) Transcriptional repression by REST: Recruitment of Sin3A and histone deacetylase to neuronal genes. Nat. Neurosci 2, 867-872.
107. Saha, R. N., and Pahan, K. (2006) HATs and HDACs in neurodegeneration: A tale of disconcerted acetylation homeostasis. Cell Death Differ. 13, 539-550.
108. Oliveira, A. M., Estevez, M. A., Hawk, J. D., Grimes, S., Brindle, P. K., and Abel, T. (2011) Subregion-specific p300 conditional knockout mice exhibit long-term memory impairments. Learn. Mem. 18, 161-169.
109. Duclot, F., Meffre, J., Jacquet, C., Gongora, C., and Maurice, T. (2010) Mice knock out for the histone acetyltransferase p300/CREB binding protein-associated factor develop a resistance to amyloid toxicity. Neuroscience 167, 850-863.
110. Pirooznia, S. K., Sarthi, J., Johnson, A. A., Toth, M. S., Chiu, K., Koduri, S., and Elefant, F. (2012) Tip60 HAT activity mediates APP induced lethality and apoptotic cell death in the CNS of a Drosophila Alzheimer's disease model. PLoS One 7, e41776.
111. Janssen, C., Schmalbach, S., Boeselt, S., Sarlette, A., Dengler, R., and Petri, S. (2010) Differential histone deacetylase mRNA expression patterns in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 69, 573-581.
112. Bardai, F. H., and D'Mello, S. R. (2011) Selective toxicity by HDAC3 in neurons: Regulation by Akt and GSK3beta. J. Neurosci. 31, 1746-1751.
113. Li, J., Chen, J., Ricupero, C. L., Hart, R. P., Schwartz, M. S., Kusnecov, A., and Herrup, K. (2012) Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia. Nat. Med. 18, 783-790.
114. Chestnut, B. A., Chang, Q., Price, A., Lesuisse, C., Wong, M., and Martin, L. J. (2011) Epigenetic regulation of motor neuron cell death through DNA methylation. J. Neurosci. 31, 16619-16636.
115. Dion, V., Lin, Y., Hubert, L., Jr., Waterland, R. A., and Wilson, J. H. (2008) Dnmt1 deficiency promotes CAG repeat expansion in the mouse germline. Hum. Mol. Genet. 17, 1306-1317.
116. Zhao, C., Deng, W., and Gage, F. H. (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.
117. Ohl, F., and Fuchs, E. (1999) Differential effects of chronic stress on memory processes in the tree shrew. Brain Res. Cognit. Brain Res. 7, 379-387.
118. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2003) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 100, 14385-14390.
119. Lazarov, O., and Marr, R. A. (2010) Neurogenesis and Alzheimer's disease: At the crossroads. Exp. Neurol. 223, 267-281.
120. Marxreiter, F., Regensburger, M., and Winkler, J. (2013) Adult neurogenesis in Parkinson's disease. Cell. Mol. Life Sci. 70, 459-473.
121. Steiner, B., Wolf, S., and Kempermann, G. (2006) Adult neurogenesis and neurodegenerative disease. Regener. Med. 1, 15-28.
122. Winner, B., Kohl, Z., and Gage, F. H. (2011) Neurodegenerative disease and adult neurogenesis. Eur. J. Neurosci. 33, 1139-1151.
123. van Praag, H., Shubert, T., Zhao, C., and Gage, F. H. (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J. Neurosci. 25, 8680-8685.
124. Warner-Schmidt, J. L., and Duman, R. S. (2006) Hippocampal neurogenesis: Opposing effects of stress and antidepressant treatment. Hippocampus 16, 239-249.
125. Kempermann, G., Brandon, E. P., and Gage, F. H. (1998) Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr. Biol. 8, 939-942.
126. Jessberger, S., Zhao, C., Toni, N., Clemenson, G. D., Jr., Li, Y., and Gage, F. H. (2007) Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J. Neurosci. 27, 9400-9407.
127. Kokaia, Z., Thored, P., Arvidsson, A., and Lindvall, O. (2006) Regulation of stroke-induced neurogenesis in adult brain - Recent scientific progress. Cereb. Cortex 16 (Suppl 1), i162-167.
128. Gil-Mohapel, J., Simpson, J. M., Ghilan, M., and Christie, B. R. (2011) Neurogenesis in Huntington's disease: Can studying adult neurogenesis lead to the development of new therapeutic strategies? Brain Res. 1406, 84-105.
129. Faraco, G., Pancani, T., Formentini, L., Mascagni, P., Fossati, G., Leoni, F., Moroni, F., and Chiarugi, A. (2006) Pharmacological inhibition of histone deacetylases by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain. Mol. Pharmacol. 70, 1876-1884.
130. Zhang, R. L., Zhang, Z. G., and Chopp, M. (2008) Ischemic stroke and neurogenesis in the subventricular zone. Neuropharmacology 55, 345-352.
131. Ren, M., Leng, Y., Jeong, M., Leeds, P. R., and Chuang, D. M. (2004) Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: Potential roles of histone deacetylase inhibition and heat shock protein induction. J. Neurochem. 89, 1358-1367.
132. Kim, H. J., Leeds, P., and Chuang, D. M. (2009) The HDAC inhibitor, sodium butyrate, stimulates neurogenesis in the ischemic brain. J. Neurochem. 110, 1226-1240.
133. Kim, H. J., Rowe, M., Ren, M., Hong, J. S., Chen, P. S., and Chuang, D. M. (2007) Histone deacetylase inhibitors exhibit antiinflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: Multiple mechanisms of action. J. Pharmacol. Exp. Ther. 321, 892-901.
134. Qi, X., Hosoi, T., Okuma, Y., Kaneko, M., and Nomura, Y. (2004) Sodium 4-phenylbutyrate protects against cerebral ischemic injury. Mol. Pharmacol. 66, 899-908.
135. Pla, P., Orvoen, S., Saudou, F., David, D. J., and Humbert, S. (2014) Mood disorders in Huntington's disease: From behavior to cellular and molecular mechanisms. Front. Behav. Neurosci. 8, 135.
136. Pla, P., Orvoen, S., Benstaali, C., Dodier, S., Gardier, A. M., David, D. J., Humbert, S., and Saudou, F. (2013) Huntingtin acts non cell-autonomously on hippocampal neurogenesis and controls anxiety-related behaviors in adult mouse. PLoS One 8, e73902.
137. Ransome, M. I., Renoir, T., and Hannan, A. J. (2012) Hippocampal neurogenesis, cognitive deficits and affective disorder in Huntington' s disease. Neural Plast. 2012, 874387.
138. Hay, D. G., Sathasivam, K., Tobaben, S., Stahl, B., Marber, M., Mestril, R., Mahal, A., Smith, D. L., Woodman, B., and Bates, G. P. (2004) Progressive decrease in chaperone protein levels in a mouse model of Huntington 's disease and induction of stress proteins as a therapeutic approach. Hum. Mol. Genet. 13, 1389-1405.
139. Zuccato, C., Ciammola, A., Rigamonti, D., Leavitt, B. R., Goffredo, D., Conti, L., MacDonald, M. E., Friedlander, R. M., Silani, V., Hayden, M. R., Timmusk, T., Sipione, S., and Cattaneo, E. (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293, 493-498.
140. Tagawa, K., Marubuchi, S., Qi, M. L., Enokido, Y., Tamura, T., Inagaki, R., Murata, M., Kanazawa, I., Wanker, E. E., and Okazawa, H. (2007) The induction levels of heat shock protein 70 differentiate the vulnerabilities to mutant huntingtin among neuronal subtypes. J. Neurosci. 27, 868-880.
141. Dompierre, J. P., Godin, J. D., Charrin, B. C., Cordelieres, F. P., King, S. J., Humbert, S., and Saudou, F. (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 27, 3571-3583.
142. Winner, B., Lie, D. C., Rockenstein, E., Aigner, R., Aigner, L., Masliah, E., Kuhn, H. G., and Winkler, J. (2004) Human wild-type alpha-synuclein impairs neurogenesis. J. Neuropathol. Exp. Neurol. 63, 1155-1166.
143. Winner, B., Rockenstein, E., Lie, D. C., Aigner, R., Mante, M., Bogdahn, U., Couillard-Despres, S., Masliah, E., and Winkler, J. (2008) Mutant alpha-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol. Aging 29, 913-925.
144. Hoglinger, G. U., Rizk, P., Muriel, M. P., Duyckaerts, C., Oertel, W. H., Caille, I., and Hirsch, E. C. (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 7, 726-735.
145. Chen, P. S., Peng, G. S., Li, G., Yang, S., Wu, X., Wang, C. C., Wilson, B., Lu, R. B., Gean, P. W., Chuang, D. M., and Hong, J. S. (2006) Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 11, 1116-1125.
146. Wu, X., Chen, P. S., Dallas, S., Wilson, B., Block, M. L., Wang, C. C., Kinyamu, H., Lu, N., Gao, X., Leng, Y., Chuang, D. M., Zhang, W., Lu, R. B., and Hong, J. S. (2008) Histone deacetylase inhibitors up-regulate astrocyte GDNF and BDNF gene transcription and protect dopaminergic neurons. Int. J. Neuropsychopharmacol. 11, 1123-1134.
147. Airaksinen, M. S., and Saarma, M. (2002) The GDNF family: Signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3, 383-394.
148. Verret, L., Trouche, S., Zerwas, M., and Rampon, C. (2007) Hippocampal neurogenesis during normal and pathological aging. Psychoneuroendocrinology 32 (Suppl 1), S26-30.
149. Lazarov, O., and Demars, M. P. (2012) All in the Family: How the APPs Regulate Neurogenesis. Front. Neurosci. 6, 81.
150. Krezymon, A., Richetin, K., Halley, H., Roybon, L., Lassalle, J. M., Frances, B., Verret, L., and Rampon, C. (2013) Modifications of hippocampal circuits and early disruption of adult neurogenesis in the tg2576 mouse model of Alzheimer's disease. PLoS One 8, e76497.
151. Schindowski, K., Belarbi, K., Bretteville, A., Ando, K., and Buee, L. (2008) Neurogenesis and cell cycle-reactivated neuronal death during pathogenic tau aggregation. Genes, Brain Behav. 7 (Suppl 1), 92-100.
152. Couillard-Despres, S., Iglseder, B., and Aigner, L. (2011) Neurogenesis, cellular plasticity and cognition: The impact of stem cells in the adult and aging brain - A mini-review. Gerontology 57, 559-564.
153. Ricobaraza, A., Cuadrado-Tejedor, M., Perez-Mediavilla, A., Frechilla, D., Del Rio, J., and Garcia-Osta, A. (2009) Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34, 1721-1732.
154. Qing, H., He, G., Ly, P. T., Fox, C. J., Staufenbiel, M., Cai, F., Zhang, Z., Wei, S., Sun, X., Chen, C. H., Zhou, W., Wang, K., and Song, W. (2008) Valproic acid inhibits Aβ production, neuritic plaque formation, and behavioral deficits in Alzheimer 's disease mouse models. J. Exp. Med. 205, 2781-2789.
155. Francis, Y. I., Fa, M., Ashraf, H., Zhang, H., Staniszewski, A., Latchman, D. S., and Arancio, O. (2009) Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer's disease. J. Alzheimer' s Dis. 18, 131-139.
156. Zhang, Z. Y., and Schluesener, H. J. (2013) Oral administration of histone deacetylase inhibitor MS-275 ameliorates neuroinflammation and cerebral amyloidosis and improves behavior in a mouse model. J. Neuropathol. Exp. Neurol. 72, 178-185.
157. Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R. C., Cota, P., Wittnam, J. L., Gogol-Doering, A., Opitz, L., Salinas-Riester, G., Dettenhofer, M., Kang, H., Farinelli, L., Chen, W., and Fischer, A. (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328, 753-756.
158. Parsons, D. W., Jones, S., Zhang, X., Lin, J. C., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I. M., Gallia, G. L., Olivi, A., McLendon, R., Rasheed, B. A., Keir, S., Nikolskaya, T., Nikolsky, Y., Busam, D. A., Tekleab, H., Diaz, L. A., Jr., Hartigan, J., Smith, D. R., Strausberg, R. L., Marie, S. K., Shinjo, S. M., Yan, H., Riggins, G. J., Bigner, D. D., Karchin, R., Papadopoulos, N., Parmigiani, G., Vogelstein, B., Velculescu, V. E., and Kinzler, K. W. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812.
159. Morales-Garcia, J. A., Luna-Medina, R., Alonso-Gil, S., Sanz-Sancristobal, M., Palomo, V., Gil, C., Santos, A., Martinez, A., and Perez-Castillo, A. (2012) Glycogen synthase kinase 3 inhibition promotes adult hippocampal neurogenesis in vitro and in vivo. ACS Chem. Neurosci. 3, 963-971.
160. Lecanu, L., Hashim, A. I., McCourty, A., Giscos-Douriez, I., Dinca, I., Yao, W., Vicini, S., Szabo, G., Erdelyi, F., Greeson, J., and Papadopoulos, V. (2011) The naturally occurring steroid solasodine induces neurogenesis in vitro and in vivo. Neuroscience 183, 251-264.
161. Anderson, K. D., Sengupta, J., Morin, M., Neve, R. L., Valenzuela, C. F., and Perrone-Bizzozero, N. I. (2001) Overexpression of HuD accelerates neurite outgrowth and increases GAP-43 mRNA expression in cortical neurons and retinoic acid-induced embryonic stem cells in vitro. Exp. Neurol. 168, 250-258.
162. Bolognani, F., Qiu, S., Tanner, D. C., Paik, J., Perrone- Bizzozero, N. I., and Weeber, E. J. (2007) Associative and spatial learning and memory deficits in transgenic mice overexpressing the RNA-binding protein HuD. Neurobiol. Learn. Mem. 87, 635-643.
163. Deschenes-Furry, J., Perrone-Bizzozero, N., and Jasmin, B. J. (2006) The RNA-binding protein HuD: A regulator of neuronal differentiation, maintenance and plasticity. BioEssays 28, 822-833.
164. Mobarak, C. D., Anderson, K. D., Morin, M., Beckel- Mitchener, A., Rogers, S. L., Furneaux, H., King, P., and Perrone-Bizzozero, N. I. (2000) The RNA-binding protein HuD is required for GAP-43 mRNA stability, GAP-43 gene expression, and PKC-dependent neurite outgrowth in PC12 cells. Mol. Biol. Cell 11, 3191-3203.
165. Li, Y., Luikart, B. W., Birnbaum, S., Chen, J., Kwon, C. H., Kernie, S. G., Bassel-Duby, R., and Parada, L. F. (2008) TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59, 399-412.
166. Altar, C. A. (1999) Neurotrophins and depression. Trends Pharmacol. Sci. 20, 59-61.
167. Nestler, E. J., Barrot, M., DiLeone, R. J., Eisch, A. J., Gold, S. J., and Monteggia, L. M. (2002) Neurobiology of depression. Neuron 34, 13-25.
168. Castren, E., Voikar, V., and Rantamaki, T. (2007) Role of neurotrophic factors in depression. Curr. Opin. Pharmacol. 7, 18-21.
169. Liu, X., Chan, C. B., Jang, S. W., Pradoldej, S., Huang, J., He, K., Phun, L. H., France, S., Xiao, G., Jia, Y., Luo, H. R., and Ye, K. (2010) A synthetic 7,8-dihydroxyflavone derivative promotes neurogenesis and exhibits potent antidepressant effect. J. Med. Chem. 53, 8274-8286.
170. Tanaka, Y., Tanaka, R., Liu, M., Hattori, N., and Urabe, T. (2010) Cilostazol attenuates ischemic brain injury and enhances neurogenesis in the subventricular zone of adult mice after transient focal cerebral ischemia. Neuroscience 171, 1367-1376.
171. Balasubramanyam, K., Varier, R. A., Altaf, M., Swaminathan, V., Siddappa, N. B., Ranga, U., and Kundu, T. K. (2004) Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J. Biol. Chem. 279, 51163-51171.
172. Arif, M., Vedamurthy, B. M., Choudhari, R., Ostwal, Y. B., Mantelingu, K., Kodaganur, G. S., and Kundu, T. K. (2010) Nitric oxide-mediated histone hyperacetylation in oral cancer: Target for a water-soluble HAT inhibitor, CTK7A. Chem. Biol. 17, 903-913.
173. Tiwari, S. K., Agarwal, S., Seth, B., Yadav, A., Nair, S., Bhatnagar, P., Karmakar, M., Kumari, M., Chauhan, L. K., Patel, D. K., Srivastava, V., Singh, D., Gupta, S. K., Tripathi, A., Chaturvedi, R. K., and Gupta, K. C. (2014) Curcumin-loaded nanoparticles potently induce adult neurogenesis and reverse cognitive deficits in Alzheimer's disease model via canonical Wnt/beta-catenin pathway. ACS Nano 8, 76-103.