Nuclear accumulation of HDAC4 in ATM deficiency promotes neurodegeneration in ataxia telangiectasia

Nature Medicine

Volumn 18, Issue 5, 2012, Pages 783-790

  Li, Jiali ^a   Chen, Jianmin ^a   Ricupero, Christopher L ^a   Hart, Ronald P ^a   Schwartz, Melanie S ^b   Kusnecov, Alexander ^b   Herrup, Karl ^a  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE DEACETYLASE 4; MYOCYTE ENHANCER FACTOR 2; PHOSPHOPROTEIN PHOSPHATASE 2A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATAXIA TELANGIECTASIA; BIOACCUMULATION; CELLULAR DISTRIBUTION; CHROMATIN; CYTOPLASM; DEACETYLATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; FEMALE; GENE EXPRESSION; GENE MUTATION; HUMAN; MALE; MOUSE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ATAXIA TELANGIECTASIA; CELL CYCLE PROTEINS; CELL NUCLEUS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA-BINDING PROTEINS; FEMALE; HISTONE DEACETYLASES; HISTONES; HYDROXAMIC ACIDS; MALE; MICE; MYOGENIC REGULATORY FACTORS; NEURODEGENERATIVE DISEASES; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA; MUS;

EID: 84860692938     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2709     Document Type: Article

References (40)

1. Barzilai, A., Biton, S. & Shiloh, Y. The role of the DNA damage response in neuronal development, organization and maintenance. DNA Repair (Amst.) 7, 1010-1027 (2008).
2. Bundey, S. Clinical and genetic features of ataxia-telangiectasia. Int. J. Radiat. Biol. 66, S23-S29 (1994).
3. Lavin, M.F. & Shiloh, Y. The genetic defect in ataxia-telangiectasia. Annu. Rev. Immunol. 15, 177-202 (1997). (Pubitemid 27169279)
4. Savitsky, K. et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749-1753 (1995).
5. Sedgwick, R.P. & Boder, E. Progressive ataxia in childhood with particular reference to ataxia-telangiectasia. Neurology 10, 705-715 (1960).
6. D'Mello, S.R. Histone deacetylases as targets for the treatment of human neurodegenerative diseases. Drug News Perspect. 22, 513-524 (2009).
7. Grozinger, C.M. & Schreiber, S.L. 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 (2000). (Pubitemid 30460734)
8. Haberland, M., Montgomery, R.L. & Olson, E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42 (2009).
9. Majdzadeh, N., Morrison, B.E. & D'Mello, S.R. Class IIA HDACs in the regulation of neurodegeneration. Front. Biosci. 13, 1072-1082 (2008). (Pubitemid 351594749)
10. Yang, X.J. & Seto, E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206-218 (2008). (Pubitemid 351301825)
11. Darcy, M.J., Calvin, K., Cavnar, K. & Ouimet, C.C. Regional and subcellular distribution of HDAC4 in mouse brain. J. Comp. Neurol. 518, 722-740 (2010).
12. Grozinger, C.M., Hassig, C.A. & Schreiber, S.L. Three proteins define a class of human histone deacetylases related to yeast Hda1p. Proc. Natl. Acad. Sci. USA 96, 4868-4873 (1999). (Pubitemid 29214503)
13. Wang, A.H. et al. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol. Cell. Biol. 19, 7816-7827 (1999). (Pubitemid 29493445)
14. Majdzadeh, N. et al. HDAC4 inhibits cell-cycle progression and protects neurons from cell death. Dev. Neurobiol. 68, 1076-1092 (2008). (Pubitemid 351904928)
15. McKinsey, T.A., Zhang, C.L., Lu, J. & Olson, E.N. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408, 106-111 (2000).
16. Wang, A.H. et al. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol. Cell. Biol. 20, 6904-6912 (2000).
17. Zhao, X. et al. The modular nature of histone deacetylase HDAC4 confers phosphorylation-dependent intracellular trafficking. J. Biol. Chem. 276, 35042-35048 (2001).
18. Bolger, T.A. & Yao, T.P. Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J. Neurosci. 25, 9544-9553 (2005). (Pubitemid 41464769)
19. Chen, B. & Cepko, C.L. HDAC4 regulates neuronal survival in normal and diseased retinas. Science 323, 256-259 (2009).
20. Youn, H.D., Grozinger, C.M. & Liu, J.O. Calcium regulates transcriptional repression of myocyte enhancer factor 2 by histone deacetylase 4. J. Biol. Chem. 275, 22563-22567 (2000). (Pubitemid 30621848)
21. Kuljis, R.O., Xu, Y., Aguila, M.C. & Baltimore, D. Degeneration of neurons, synapses, and neuropil and glial activation in a murine Atm knockout model of ataxia-telangiectasia. Proc. Natl. Acad. Sci. USA 94, 12688-12693 (1997). (Pubitemid 27492590)
22. Xu, Y. et al. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10, 2411-2422 (1996). (Pubitemid 26341877)
23. Backs, J., Backs, T., Bezprozvannaya, S., McKinsey, T.A. & Olson, E.N. Histone deacetylase 5 acquires calcium/calmodulin-dependent kinase II responsiveness by oligomerization with histone deacetylase 4. Mol. Cell. Biol. 28, 3437-3445 (2008). (Pubitemid 351657105)
24. Méjat, A. et al. Histone deacetylase 9 couples neuronal activity to muscle chromatin acetylation and gene expression. Nat. Neurosci. 8, 313-321 (2005). (Pubitemid 40300188)
25. Korzus, E., Rosenfeld, M.G. & Mayford, M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972 (2004). (Pubitemid 38798234)
26. Nervi, C. et al. Inhibition of histone deacetylase activity by trichostatin A modulates gene expression during mouse embryogenesis without apparent toxicity. Cancer Res. 61, 1247-1249 (2001). (Pubitemid 34292534)
27. Yoshida, M., Kijima, M., Akita, M. & Beppu, T. Potent and specific inhibition of mammalian histone deacetylase both in vivo and in vitro by trichostatin A. J. Biol. Chem. 265, 17174-17179 (1990).
28. Barlow, C. et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159-171 (1996). (Pubitemid 26259926)
29. Liu, Y., Randall, W.R. & Schneider, M.F. Activity-dependent and-independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J. Cell Biol. 168, 887-897 (2005). (Pubitemid 40397003)
30. Paroni, G. et al. PP2A regulates HDAC4 nuclear import. Mol. Biol. Cell 19, 655-667 (2008). (Pubitemid 351272153)
31. Shi, Y. Serine/threonine phosphatases: mechanism through structure. Cell 139, 468-484 (2009).
32. Matsuoka, S. et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007). (Pubitemid 46877472)
33. Chan, J.K., Sun, L., Yang, X.J., Zhu, G. & Wu, Z. Functional characterization of an amino-terminal region of HDAC4 that possesses MEF2 binding and transcriptional repressive activity. J. Biol. Chem. 278, 23515-23521 (2003). (Pubitemid 36830170)
34. Miska, E.A. et al. HDAC4 deacetylase associates with and represses the MEF2 transcription factor. EMBO J. 18, 5099-5107 (1999). (Pubitemid 29443811)
35. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
36. Li, H. et al. The Sequence Alignment/Map (SAM) format and SAMtools. Bioinformatics. 25, 2078-2079 (2009).
37. Fejes, A.P. et al. FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 24, 1729-1730 (2008).
38. Kaemmerer, W.F. et al. In vivo transduction of cerebellar Purkinje cells using adeno-associated virus vectors. Mol. Ther. 2, 446-457 (2000).
39. Cortés, M.L., Oehmig, A., Perry, K.F., Sanford, J.D. & Breakefield, X.O. Expression of human ATM cDNA in Atm-deficient mouse brain mediated by HSV-1 amplicon vector. Neuroscience 141, 1247-1256 (2006). (Pubitemid 44128694)
40. Cooper, J.F. & Kusnecov, A.W. Methylmercuric chloride induces activation of neuronal stress circuitry and alters exploratory behavior in the mouse. Neuroscience 148, 1048-1064 (2007). (Pubitemid 47419203)