XInjury-Induced HDAC5 nuclear export is essential for axon regeneration

Cell

Volumn 155, Issue 4, 2013, Pages 894-

  Cho, Yongcheol ^a   Sloutsky, Roman ^b   Naegle, Kristen M ^b   Cavalli, Valeria ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HISTONE DEACETYLASE 5; MUTANT PROTEIN; PROTEIN KINASE C MU;

ANIMAL CELL; ARTICLE; AXONAL INJURY; CALCIUM TRANSPORT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GENE EXPRESSION; HISTONE ACETYLATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; SENSORY NERVE CELL; TRANSCRIPTION REGULATION;

EID: 84887959502     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.10.004     Document Type: Article

References (61)

1. N. Abe, and V. Cavalli Nerve injury signaling Curr. Opin. Neurobiol. 18 2008 276 283
2. N. Abe, S.H. Borson, M.J. Gambello, F. Wang, and V. Cavalli Mammalian target of rapamycin (mTOR) activation increases axonal growth capacity of injured peripheral nerves J. Biol. Chem. 285 2010 28034 28043
3. R.T. Ambron, and E.T. Walters Priming events and retrograde injury signals. A new perspective on the cellular and molecular biology of nerve regeneration Mol. Neurobiol. 13 1996 61 79
4. K. Befort, L. Karchewski, C. Lanoue, and C.J. Woolf Selective up-regulation of the growth arrest DNA damage-inducible gene Gadd45 alpha in sensory and motor neurons after peripheral nerve injury Eur. J. Neurosci. 18 2003 911 922
5. K. Ben-Yaakov, S.Y. Dagan, Y. Segal-Ruder, O. Shalem, D. Vuppalanchi, D.E. Willis, D. Yudin, I. Rishal, F. Rother, and M. Bader Axonal transcription factors signal retrogradely in lesioned peripheral nerve EMBO J. 31 2012 1350 1363
6. L.G. Bilsland, E. Sahai, G. Kelly, M. Golding, L. Greensmith, and G. Schiavo Deficits in axonal transport precede ALS symptoms in vivo Proc. Natl. Acad. Sci. USA 107 2010 20523 20528
7. A. Blesch, P. Lu, S. Tsukada, L.T. Alto, K. Roet, G. Coppola, D. Geschwind, and M.H. Tuszynski Conditioning lesions before or after spinal cord injury recruit broad genetic mechanisms that sustain axonal regeneration: superiority to camp-mediated effects Exp. Neurol. 235 2012 162 173
8. F. Bradke, J.W. Fawcett, and M.E. Spira Assembly of a new growth cone after axotomy: the precursor to axon regeneration Nat. Rev. Neurosci. 13 2012 183 193
9. E. Broude, M. McAtee, M.S. Kelley, and B.S. Bregman c-Jun expression in adult rat dorsal root ganglion neurons: differential response after central or peripheral axotomy Exp. Neurol. 148 1997 367 377
10. T. Buschmann, A. Martin-Villalba, J.D. Kocsis, S.G. Waxman, M. Zimmermann, and T. Herdegen Expression of Jun, Fos, and ATF-2 proteins in axotomized explanted and cultured adult rat dorsal root ganglia Neuroscience 84 1998 163 176
11. R.B. Campenot, D.D. Draker, and D.L. Senger Evidence that protein kinase C activities involved in regulating neurite growth are localized to distal neurites J. Neurochem. 63 1994 868 878
12. C. Cayrou, R.J. Denver, and J. Puymirat Suppression of the basic transcription element-binding protein in brain neuronal cultures inhibits thyroid hormone-induced neurite branching Endocrinology 143 2002 2242 2249
13. S. Chang, T.A. McKinsey, C.L. Zhang, J.A. Richardson, J.A. Hill, and E.N. Olson 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 2004 8467 8476
14. S. Chawla, P. Vanhoutte, F.J. Arnold, C.L. Huang, and H. Bading Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5 J. Neurochem. 85 2003 151 159
15. Y. Cho, and V. Cavalli HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration EMBO J. 31 2012 3063 3078
16. M. Domeniconi, N. Zampieri, T. Spencer, M. Hilaire, W. Mellado, M.V. Chao, and M.T. Filbin MAG induces regulated intramembrane proteolysis of the p75 neurotrophin receptor to inhibit neurite outgrowth Neuron 46 2005 849 855
17. G. Feng, R.H. Mellor, M. Bernstein, C. Keller-Peck, Q.T. Nguyen, M. Wallace, J.M. Nerbonne, J.W. Lichtman, and J.R. Sanes Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP Neuron 28 2000 41 51
18. W. Fischle, F. Dequiedt, M.J. Hendzel, M.G. Guenther, M.A. Lazar, W. Voelter, and E. Verdin Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR Mol. Cell 9 2002 45 57
19. P. Gaub, A. Tedeschi, R. Puttagunta, T. Nguyen, A. Schmandke, and S. Di Giovanni HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation Cell Death Differ. 17 2010 1392 1408
20. P. Gaub, Y. Joshi, A. Wuttke, U. Naumann, S. Schnichels, P. Heiduschka, and S. Di Giovanni The histone acetyltransferase p300 promotes intrinsic axonal regeneration Brain 134 2011 2134 2148
21. A. Ghosh-Roy, Z. Wu, A. Goncharov, Y. Jin, and A.D. Chisholm Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase J. Neurosci. 30 2010 3175 3183
22. C.H. Ha, J.Y. Kim, J. Zhao, W. Wang, B.S. Jhun, C. Wong, and Z.G. Jin PKA phosphorylates histone deacetylase 5 and prevents its nuclear export, leading to the inhibition of gene transcription and cardiomyocyte hypertrophy Proc. Natl. Acad. Sci. USA 107 2010 15467 15472
23. B.J. Iskandar, E. Rizk, B. Meier, N. Hariharan, T. Bottiglieri, R.H. Finnell, D.F. Jarrard, R.V. Banerjee, J.H. Skene, and A. Nelson Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation J. Clin. Invest. 120 2010 1603 1616
24. D. Kamber, H. Erez, and M.E. Spira Local calcium-dependent mechanisms determine whether a cut axonal end assembles a retarded endbulb or competent growth cone Exp. Neurol. 219 2009 112 125
25. N. Kedei, D.J. Lundberg, A. Toth, P. Welburn, S.H. Garfield, and P.M. Blumberg Characterization of the interaction of ingenol 3-angelate with protein kinase C Cancer Res. 64 2004 3243 3255
26. E.H. Koo, S.S. Sisodia, D.R. Archer, L.J. Martin, A. Weidemann, K. Beyreuther, P. Fischer, C.L. Masters, and D.L. Price Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport Proc. Natl. Acad. Sci. USA 87 1990 1561 1565
27. A. Lahm, C. Paolini, M. Pallaoro, M.C. Nardi, P. Jones, P. Neddermann, S. Sambucini, M.J. Bottomley, P. Lo Surdo, and A. Carfí Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases Proc. Natl. Acad. Sci. USA 104 2007 17335 17340
28. J.D. Leah, T. Herdegen, A. Murashov, M. Dragunow, and R. Bravo Expression of immediate early gene proteins following axotomy and inhibition of axonal transport in the rat central nervous system Neuroscience 57 1993 53 66
29. K. Liu, A. Tedeschi, K.K. Park, and Z. He Neuronal intrinsic mechanisms of axon regeneration Annu. Rev. Neurosci. 34 2011 131 152
30. G. Mandolesi, F. Madeddu, Y. Bozzi, L. Maffei, and G.M. Ratto Acute physiological response of mammalian central neurons to axotomy: ionic regulation and electrical activity FASEB J. 18 2004 1934 1936
31. T.A. McKinsey, C.L. Zhang, and E.N. Olson Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5 Proc. Natl. Acad. Sci. USA 97 2000 14400 14405
32. I.G. McQuarrie, and B. Grafstein Axon outgrowth enhanced by a previous nerve injury Arch. Neurol. 29 1973 53 55
33. I. Michaelevski, Y. Segal-Ruder, M. Rozenbaum, K.F. Medzihradszky, O. Shalem, G. Coppola, S. Horn-Saban, K. Ben-Yaakov, S.Y. Dagan, and I. Rishal Signaling to transcription networks in the neuronal retrograde injury response Sci. Signal. 3 2010 ra53
34. D.L. Moore, M.G. Blackmore, Y. Hu, K.H. Kaestner, J.L. Bixby, V.P. Lemmon, and J.L. Goldberg KLF family members regulate intrinsic axon regeneration ability Science 326 2009 298 301
35. H.R. Pelzel, C.L. Schlamp, and R.W. Nickells Histone H4 deacetylation plays a critical role in early gene silencing during neuronal apoptosis BMC Neurosci. 11 2010 62
36. E. Perlson, S. Hanz, K. Ben-Yaakov, Y. Segal-Ruder, R. Seger, and M. Fainzilber Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve Neuron 45 2005 715 726
37. R.B. Perry, E. Doron-Mandel, E. Iavnilovitch, I. Rishal, S.Y. Dagan, M. Tsoory, G. Coppola, M.K. McDonald, C. Gomes, and D.H. Geschwind Subcellular knockout of importin β1 perturbs axonal retrograde signaling Neuron 75 2012 294 305
38. A. Riccio Dynamic epigenetic regulation in neurons: enzymes, stimuli and signaling pathways Nat. Neurosci. 13 2010 1330 1337
39. P.M. Richardson, and V.M. Issa Peripheral injury enhances central regeneration of primary sensory neurones Nature 309 1984 791 793
40. I. Rishal, and M. Fainzilber Retrograde signaling in axonal regeneration Exp. Neurol. 223 2010 5 10
41. A.M. Shadiack, Y. Sun, and R.E. Zigmond Nerve growth factor antiserum induces axotomy-like changes in neuropeptide expression in intact sympathetic and sensory neurons J. Neurosci. 21 2001 363 371
42. S.D. Shields, H.S. Ahn, Y. Yang, C. Han, R.P. Seal, J.N. Wood, S.G. Waxman, and S.D. Dib-Hajj Nav1.8 expression is not restricted to nociceptors in mouse peripheral nervous system Pain 153 2012 2017 2030
43. J.E. Shin, Y. Cho, B. Beirowski, J. Milbrandt, V. Cavalli, and A. DiAntonio Dual leucine zipper kinase is required for retrograde injury signaling and axonal regeneration Neuron 74 2012 1015 1022
44. R. Sivasankaran, J. Pei, K.C. Wang, Y.P. Zhang, C.B. Shields, X.M. Xu, and Z. He PKC mediates inhibitory effects of myelin and chondroitin sulfate proteoglycans on axonal regeneration Nat. Neurosci. 7 2004 261 268
45. D.S. Smith, and J.H. Skene A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth J. Neurosci. 17 1997 646 658
46. A. Tedeschi Tuning the orchestra: transcriptional pathways controlling axon regeneration Front Mol Neurosci 4 2011 60
47. S.Y. Tsai, L.Y. Yang, C.H. Wu, S.F. Chang, C.Y. Hsu, C.P. Wei, S.J. Leu, J. Liaw, Y.H. Lee, and M.D. Tsai Injury-induced Janus kinase/protein kinase C-dependent phosphorylation of growth-associated protein 43 and signal transducer and activator of transcription 3 for neurite growth in dorsal root ganglion J. Neurosci. Res. 85 2007 321 331
48. R.B. Vega, B.C. Harrison, E. Meadows, C.R. Roberts, P.J. Papst, E.N. Olson, and T.A. McKinsey Protein kinases C and D mediate agonist-dependent cardiac hypertrophy through nuclear export of histone deacetylase 5 Mol. Cell. Biol. 24 2004 8374 8385
49. Q.J. Wang PKD at the crossroads of DAG and PKC signaling Trends Pharmacol. Sci. 27 2006 317 323
50. D.Y. Wu, J.Q. Zheng, M.A. McDonald, B. Chang, and J.L. Twiss PKC isozymes in the enhanced regrowth of retinal neurites after optic nerve injury Invest. Ophthalmol. Vis. Sci. 44 2003 2783 2790
51. X. Xiong, X. Wang, R. Ewanek, P. Bhat, A. Diantonio, and C.A. Collins Protein turnover of the Wallenda/DLK kinase regulates a retrograde response to axonal injury J. Cell Biol. 191 2010 211 223
52. X.F. Zhang, C.C. Shieh, M.L. Chapman, M.A. Matulenko, A.H. Hakeem, R.N. Atkinson, M.E. Kort, B.E. Marron, S. Joshi, and P. Honore A-887826 is a structurally novel, potent and voltage-dependent Na(v)1.8 sodium channel blocker that attenuates neuropathic tactile allodynia in rats Neuropharmacology 59 2010 201 207
53. N.E. Ziv, and M.E. Spira Spatiotemporal distribution of Ca2+ following axotomy and throughout the recovery process of cultured Aplysia neurons Eur. J. Neurosci. 5 1993 657 668
54. G. Zündorf, and G. Reiser Calcium dysregulation and homeostasis of neural calcium in the molecular mechanisms of neurodegenerative diseases provide multiple targets for neuroprotection Antioxid. Redox Signal. 14 2011 1275 1288
55. P. Baldi, and A.D. Long A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes Bioinformatics 17 2001 509 519
56. B.M. Bolstad, R.A. Irizarry, M. Astrand, and T.P. Speed A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bioinformatics 19 2003 185 193
57. E. Ersvaer, A.O. Kittang, P. Hampson, K. Sand, B.T. Gjertsen, J.M. Lord, and O. Bruserud The protein kinase C agonist PEP005 (ingenol 3-angelate) in the treatment of human cancer: a balance between efficacy and toxicity Toxins (Basel) 2 2010 174 194
58. L. Li, S. Shukla, A. Lee, S.H. Garfield, D.J. Maloney, S.V. Ambudkar, and S.H. Yuspa The skin cancer chemotherapeutic agent ingenol-3-angelate (PEP005) is a substrate for the epidermal multidrug transporter (ABCB1) and targets tumor vasculature Cancer Res. 70 2010 4509 4519
59. K.M. Naegle, M. Gymrek, B.A. Joughin, J.P. Wagner, R.E. Welsch, M.B. Yaffe, D.A. Lauffenburger, and F.M. White PTMScout, a Web resource for analysis of high throughput post-translational proteomics studies Mol. Cell. Proteomics 9 2010 2558 2570
60. S.M. Ogbourne, A. Suhrbier, B. Jones, S.J. Cozzi, G.M. Boyle, M. Morris, D. McAlpine, J. Johns, T.M. Scott, and K.P. Sutherland Antitumor activity of 3-ingenyl angelate: plasma membrane and mitochondrial disruption and necrotic cell death Cancer Res. 64 2004 2833 2839
61. A. Spandidos, X. Wang, H. Wang, and B. Seed PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification Nucleic Acids Res. 38 Database issue 2010 D792 D799