Histone deacetylase inhibition rescues structural and functional brain deficits in a mouse model of Kabuki syndrome

Science Translational Medicine

Volumn 6, Issue 256, 2014, Pages

  Bjornsson, Hans T ^a   Benjamin, Joel S ^a   Zhang, Li ^a   Weissman, Jacqueline ^a,b   Gerber, Elizabeth E ^a   Chen, Yi Chun ^a   Vaurio, Rebecca G ^b   Potter, Michelle C ^a   Hansen, Kasper D ^a,c   Dietz, Harry C ^a,d  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AR 42; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; MLL2 PROTEIN, HUMAN; TUMOR PROTEIN;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; CASE REPORT; CONTROLLED STUDY; DENTATE GYRUS; DOSE RESPONSE; DRUG EFFECT; EMBRYO; ENZYME INHIBITION; FEMALE; FIBROBLAST; GRANULE CELL; HIPPOCAMPUS; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; KABUKI MAKEUP SYNDROME; MALE; MEMORY DISORDER; MOUSE; NONHUMAN; PATHOGENESIS; PERINATAL PERIOD; REPORTER GENE; RETROSPECTIVE STUDY; ABNORMALITIES; ABNORMALITIES, MULTIPLE; ANIMAL; BRAIN; DISEASE MODEL; FACE; GENETICS; HEMATOLOGIC DISEASES; NERVOUS SYSTEM DEVELOPMENT; PATHOPHYSIOLOGY; VESTIBULAR DISEASES;

ABNORMALITIES, MULTIPLE; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; FACE; FEMALE; HEMATOLOGIC DISEASES; HIPPOCAMPUS; HISTONE DEACETYLASE INHIBITORS; HUMANS; MALE; MICE; NEOPLASM PROTEINS; NEUROGENESIS; VESTIBULAR DISEASES;

EID: 84908377130     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3009278     Document Type: Article

References (53)

1. S. B. Ng, A. W. Bigham, K. J. Buckingham, M. C. Hannibal, M. J. McMillin, H. I. Gildersleeve, A. E. Beck, H. K. Tabor, G. M. Cooper, H. C. Mefford, C. Lee, E. H. Turner, J. D. Smith, M. J. Rieder, K. Yoshiura, N. Matsumoto, T. Ohta, N. Niikawa, D. A. Nickerson, M. J. Bamshad, J. Shendure, Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat. Genet. 42, 790-793 (2010).
2. D. Lederer, B. Grisart, M. C. Digilio, V. Benoit, M. Crespin, S. C. Ghariani, I. Maystadt, B. Dallapiccola, C. Verellen-Dumoulin, Deletion of KDM6A, a histone demethylase interacting with MLL2, in three patients with Kabuki syndrome. Am. J. Hum. Genet. 90, 119-124 (2012).
3. N. Miyake, S. Mizuno, N. Okamoto, H. Ohashi, M. Shiina, K. Ogata, Y. Tsurusaki, M. Nakashima, H. Saitsu, N. Niikawa, N. Matsumoto, KDM6A point mutations cause Kabuki syndrome. Hum. Mutat. 34, 108-110 (2013).
4. M. Brus, M. Keller, F. Lévy, Temporal features of adult neurogenesis: Differences and similarities across mammalian species. Front. Neurosci. 7, 135 (2013).
5. J. Altman, Are new neurons formed in the brains of adult mammals? Science 135, 1127-1128 (1962).
6. S. Hunter, P. Jones, A. Mitchell, R. Apweiler, T. K. Attwood, A. Bateman, T. Bernard, D. Binns, P. Bork, S. Burge, E. de Castro, P. Coggill, M. Corbett, U. Das, L. Daugherty, L. Duquenne, R. D. Finn, M. Fraser, J. Gough, D. Haft, N. Hulo, D. Kahn, E. Kelly, I. Letunic, D. Lonsdale, R. Lopez, M. Madera, J. Maslen, C. McAnulla, J. McDowall, C. McMenamin, H. Mi, P. Mutowo-Muellenet, N. Mulder, D. Natale, C. Orengo, S. Pesseat, M. Punta, A. F. Quinn, C. Rivoire, A. Sangrador-Vegas, J. D. Selengut, C. J. Sigrist, M. Scheremetjew, J. Tate, M. Thimmajanarthanan, P. D. Thomas, C. H. Wu, C. Yeats, S. Y. Yong, InterPro in 2011: New developments in the family and domain prediction database. Nucleic Acids Res. 40, D306-D312 (2012).
7. C. Kerimoglu, R. C. Agis-Balboa, A. Kranz, R. Stilling, S. Bahari-Javan, E. Benito-Garagorri, R. Halder, S. Burkhardt, A. F. Stewart, A. Fischer, Histone-methyltransferase MLL2 (KMT2B) is required for memory formation in mice. J. Neurosci. 33, 3452-3464 (2013).
8. N. Bögershausen, E. Bruford, E. B. Wollnik, Skirting the pitfalls: A clear-cut nomenclature for H3K4 methyltransferases. Clin. Genet. 83, 212-214 (2013).
9. Z. Guan, M. Giustetto, S. Lomvardas, J. H. Kim, M. C. Miniaci, J. H. Schwartz, D. Thanos, E. R. Kandel, Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111, 483-493 (2002).
10. S. Gupta, S. Y. Kim, S. Artis, D. L. Molfese, A. Schumacher, J. D. Sweatt, R. E. Paylor, F. D. Lubin, Histone methylation regulates memory formation. J. Neurosci. 30, 3589-3599 (2010).
11. M. Cohen-Armon, L. Visochek, A. Katzoff, D. Levitan, A. J. Susswein, R. Klein, M. Valbrun, J. H. Schwartz, Long-term memory requires polyADP-ribosylation. Science 304, 1820-1822 (2004).
12. M. S. Rao, A. K. Shetty, Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur. J. Neurosci. 19, 234-246 (2004).
13. R. P. Kesner, An analysis of the dentate gyrus function. Behav. Brain Res. 254, 1-7 (2013).
14. A. M. Morris, J. C. Churchwell, R. P. Kesner, P. E. Gilbert, Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations. Neurobiol. Learn. Mem. 97, 326-331 (2012).
15. J. R. Epp, A. K. Haack, L. A. Galea, Activation and survival of immature neurons in the dentate gyrus with spatial memory is dependent on time of exposure to spatial learning and age of cells at examination. Neurobiol. Learn. Mem. 95, 316-325 (2011).
16. A. M. Brickman, Y. Stern, S. A. Small, Hippocampal subregions differentially associate with standardized memory tests. Hippocampus 21, 923-928 (2011).
17. G. S. Baird, D. A. Zacharias, R. Y. Tsien, Circular permutation and receptor insertion within green fluorescent proteins. Proc. Natl. Acad. Sci. U.S.A. 96, 11241-11246 (1999).
18. A. Munshi, T. Tanaka, M. L. Hobbs, S. L. Tucker, V. M. Richon, R. E. Meyn, Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of γ-H2AX foci. Mol. Cancer Ther. 5, 1967-1974 (2006).
19. P. H. Huang, C. H. Chen, C. C. Chou, A. M. Sargeant, S. K. Kulp, C. M. Teng, J. C. Byrd, C. S. Chen, Histone deacetylase inhibitors stimulate histone H3 lysine 4 methylation in part via transcriptional repression of histone H3 lysine 4 demethylases. Mol. Pharmacol. 79, 197-206 (2011).
20. M. Vermeulen, K. W. Mulder, S. Denissov, V. W. Pijnappel, F. M. van Schaik, R. A. Varier, M. P. Baltissen, H. G. Stunnenberg, M. Mann, H. T. Timmers, Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58-69 (2007).
21. H. van Ingen, F. M. van Schaik, H. Wienk, J. Ballering, H. Rehmann, A. C. Dechesne, J. A. Kruijzer, R. M. Liskamp, H. T. Timmers, R. Boelens, Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16, 1245-1256 (2008).
22. A. Jacob, J. Oblinger, M. L. Bush, V. Brendel, G. Santarelli, A. R. Chaudhury, S. Kulp, K. M. La Perle, C. S. Chen, L. S. Chang, D. B. Welling, Preclinical validation of AR42, a novel histone deacetylase inhibitor, as treatment for vestibular schwannomas. Laryngoscope 122, 174-189 (2012).
23. S. Zhang, A. Suvannasankha, C. D. Crean, V. L. White, C. S. Chen, S. S. Farag, The novel histone deacetylase inhibitor, AR-42, inhibits gp130/Stat3 pathway and induces apoptosis and cell cycle arrest in multiple myeloma cells. Int. J. Cancer 129, 204-213 (2011).
24. C. Guo, C. C. Chang, M. Wortham, L. H. Chen, D. N. Kernagis, X. Qin, Y. W. Cho, J. T. Chi, G. A. Grant, R. E. McLendon, H. Yan, K. Ge, N. Papadopoulos, D. D. Bigner, Y. He, Global identification of MLL2-targeted loci reveals MLL2's role in diverse signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 109, 17603-17608 (2012).
25. L. H. Kasper, S. Lerach, J. Wang, S. Wu, T. Jeevan, P. K. Brindle, CBP/p300 double null cells reveal effect of coactivator level and diversity on CREB transactivation. EMBO J. 29, 3660-3672 (2010).
26. A. Garthe, G. Kempermann, An old test for new neurons: Refining the Morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front. Neurosci. 7, 63 (2013).
27. A. Ansorg, O. W. Witte, A. Urbach, Age-dependent kinetics of dentate gyrus neurogenesis in the absence of cyclin D2. BMC Neurosci. 13, 46 (2012).
28. S. Denis-Donini, A. Dellarole, P. Crociara, M. T. Francese, V. Bortolotto, G. Quadrato, P. L. Canonico, M. Orsetti, P. Ghi, M. Memo, S. A. Bonini, G. Ferrari-Toninelli, M. Grilli, Impaired adult neurogenesis associated with short-term memory defects in NF-κB p50-deficient mice. J. Neurosci. 28, 3911-3919 (2008).
29. M. Berdasco, M. Esteller, Genetic syndromes caused by mutations in epigenetic genes. Hum. Genet. 132, 359-383 (2013).
30. P. K. Dash, S. A. Orsi, A. N. Moore, Histone deactylase inhibition combined with behavioral therapy enhances learning and memory following traumatic brain injury. Neuroscience 163, 1-8 (2009).
31. C. G. Vecsey, J. D. Hawk, K. M. Lattal, J. M. Stein, S. A. Fabian, M. A. Attner, S. M. Cabrera, C. B. McDonough, P. K. Brindle, T. Abel, M. A. Wood, Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 27, 6128-6140 (2007).
32. J. Gräff, L. H. Tsai, The potential of HDAC inhibitors as cognitive enhancers. Annu. Rev. Pharmacol. Toxicol. 53, 311-330 (2013).
33. E. Korzus, M. G. Rosenfeld, M. Mayford, CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972 (2004).
34. +/- mice: A model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42, 947-959 (2004).
35. P. Yang, L. Guo, Z. J. Duan, C. G. Tepper, L. Xue, X. Chen, H. J. Kung, A. C. Gao, J. X. Zou, H. W. Chen, Histone methyltransferase NSD2/MMSET mediates constitutive NF-κB signaling for cancer cell proliferation, survival, and tumor growth via a feed-forward loop. Mol. Cell. Biol. 32, 3121-3131 (2012).
36. S. Lubitz, S. Glaser, J. Schaft, A. F. Stewart, K. Anastassiadis, Increased apoptosis and skewed differentiation in mouse embryonic stem cells lacking the histone methyltransferase Mll2. Mol. Biol. Cell 18, 2356-2366 (2007).
37. H. T. Bjornsson, M. D. Fallin, A. P. Feinberg, An integrated epigenetic and genetic approach to common human disease. Trends Genet. 20, 350-358 (2004).
38. C. J. Phiel, F. Zhang, E. Y. Huang, M. G. Guenther, M. A. Lazar, P. S. Klein, Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 276, 36734-36741 (2001).
39. S. M. Meeran, A. Ahmed, T. O. Tollefsbol, Epigenetic targets of bioactive dietary components for cancer prevention and therapy. Clin. Epigenetics 1, 101-116 (2010).
40. T. Shimazu, M. D. Hirschey, J. Newman, W. He, K. Shirakawa, N. Le Moan, C. A. Grueter, H. Lim, L. R. Saunders, R. D. Stevens, C. B. Newgard, R. V. Farese Jr., R. de Cabo, S. Ulrich, K. Akassoglou, E. Verdin, Suppression of oxidative stress by β-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 339, 211-214 (2013).
41. A. Martinez-Canabal, K. G. Akers, S. A. Josselyn, P. W. Frankland, Age-dependent effects of hippocampal neurogenesis suppression on spatial learning. Hippocampus 23, 66-74 (2013).
42. J. Guy, J. Gan, J. Selfridge, S. Cobb, A. Bird, Reversal of neurological defects in a mouse model of Rett syndrome. Science 315, 1143-1147 (2007).
43. I. Das, J. M. Park, J. H. Shin, S. K. Jeon, H. Lorenzi, D. J. Linden, P. F. Worley, R. H. Reeves, Hedgehog agonist therapy corrects structural and cognitive deficits in a Down syndrome mouse model. Sci. Transl. Med. 5, 201ra120 (2013).
44. C. Henderson, L. Wijetunge, M. N. Kinoshita, M. Shumway, R. S. Hammond, F. R. Postma, C. Brynczka, R. Rush, A. Thomas, R. Paylor, S. T. Warren, P. W. Vanderklish, P. C. Kind, R. L. Carpenter, M. F. Bear, A. M. Healy, Reversal of disease-related pathologies in the fragile X mouse model by selective activation of GABAB receptors with arbaclofen. Sci. Transl. Med. 4, 152ra128 (2012).
45. 2+ sensors with increased dynamic range. BMC Biotechnol. 7, 37 (2007).
46. G. D. Gilfillan, T. Hughes, Y. Sheng, H. S. Hjorthaug, T. Straub, K. Gervin, J. R. Harris, D. E. Undlien, R. Lyle, Limitations and possibilities of low cell number ChIP-seq. BMC Genomics 13, 645 (2012).
47. B. Langmead, S. L. Salzberg, Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
48. Y. Zhang, T. Liu, C. A. Meyer, J. Eeckhoute, D. S. Johnson, B. E. Bernstein, C. Nusbaum, R. M. Myers, M. Brown, W. Li, X. S. Liu, Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
49. A. R. Quinlan, I. M. Hall, BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
50. D. J. McCarthy, Y. Chen, G. K. Smyth, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res. 40, 4288-4297 (2012).
51. M. D. Robinson, D. J. McCarthy, G. K. Smyth, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
52. B. L. Loeys, E. E. Gerber, D. Riegert-Johnson, S. Iqbal, P. Whiteman, V. McConnell, C. R. Chillakuri, D. Macaya, P. J. Coucke, A. De Paepe, D. P. Judge, F. Wigley, E. C. Davis, H. J. Mardon, P. Handford, D. R. Keene, L. Y. Sakai, H. C. Dietz, Mutations in fibrillin-1 cause congenital scleroderma: Stiff skin syndrome. Sci. Transl. Med. 23, 23ra20 (2010).
53. A. Adamczyk, R. Mejias, K. Takamiya, J. Yocum, I. N. Krasnova, J. Calderon, J. L. Cadet, R. L. Huganir, M. V. Pletnikov, T. Wang, GluA3-deficiency in mice is associated with increased social and aggressive behavior and elevated dopamine in striatum. Behav. Brain Res. 229, 265-272 (2012).