Inhibition of HDAC6 Modifies Tau Inclusion Body Formation and Impairs Autophagic Clearance

Journal of Molecular Neuroscience

Volumn 55, Issue 4, 2015, Pages 1031-1046

  Leyk, Janina ^a   Goldbaum, Olaf ^a   Noack, Monika ^a   Richter Landsberg, Christiane ^a  

^a UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

Apoptosis; LC3; Neurodegenerative diseases; Proteasome inhibition; Protein acetylation; Tau protein; Tubastatin A

Indexed keywords

ALPHA CRYSTALLIN; ALPHA TUBULIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BETA CRYSTALLIN; ENZYME INHIBITOR; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE 6; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; PROTEIN; PROTEIN AGGREGATE; PROTEIN P62; RAPAMYCIN; SHORT HAIRPIN RNA; TAU PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; HDAC6 PROTEIN, RAT; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; INDOLE DERIVATIVE; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; PROTEASOME; TUBASTATIN A;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL DEATH; CELL FUNCTION; CELL INCLUSION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; CYTOPLASM; DEGENERATIVE DISEASE; DOWN REGULATION; ENZYME INHIBITION; HEAT SHOCK RESPONSE; IMMUNOREACTIVITY; LIGHT CHAIN; MICROTUBULE; NONHUMAN; OLIGODENDROGLIA; PATHOPHYSIOLOGY; PROTEIN ACETYLATION; PROTEIN AGGREGATION; RAT; STRESS; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECTS; METABOLISM; PHAGOSOME; WISTAR RAT;

ANIMALS; AUTOPHAGY; CELL LINE; CELLS, CULTURED; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HSP70 HEAT-SHOCK PROTEINS; HYDROXAMIC ACIDS; INDOLES; MICROTUBULE-ASSOCIATED PROTEINS; OLIGODENDROGLIA; PHAGOSOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RATS, WISTAR; TAU PROTEINS;

EID: 84925500787     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0460-y     Document Type: Article

References (56)

1. Asthana J, Kapoor S, Mohan R, Panda D (2013) Inhibition of HDAC6 deacetylase activity increases its binding with microtubules and suppresses microtubule dynamic instability in MCF-7 cells. J Biol Chem 288:22516–26
2. Ballatore C, Lee VM, Trojanowski JQ (2007) Tau-mediated neurodegeneration in Alzheimer’s disease and related disorders. Nat Rev Neurosci 8:663–72
3. Banreti A, Sass M, Graba Y (2013) The emerging role of acetylation in the regulation of autophagy. Autophagy 9:819–29
4. Bauer NG, Richter-Landsberg C (2006) The dynamic instability of microtubules is required for aggresome formation in oligodendroglial cells after proteolytic stress. J Mol Neurosci 29:153–68
5. Boyault C, Gilquin B, Zhang Y et al (2006) HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J 25:3357–66
6. Boyault C, Sadoul K, Pabion M, Khochbin S (2007) HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 26:5468–76
7. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, Kozikowski AP (2010) Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 132:10842–6
8. Chiba Y, Takei S, Kawamura N et al (2012) Immunohistochemical localization of aggresomal proteins in glial cytoplasmic inclusions in multiple system atrophy. Neuropathol Appl Neurobiol 38:559–71
9. Cohen TJ, Guo JL, Hurtado DE et al (2011) The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat Commun 2:252
10. Cook C, Carlomagno Y, Gendron TF et al (2014) Acetylation of the KXGS motifs in tau is a critical determinant in modulation of tau aggregation and clearance. Hum Mol Genet 23:104–16
11. d’Ydewalle C, Bogaert E, Van Den Bosch L (2012) HDAC6 at the intersection of neuroprotection and neurodegeneration. Traffic 13:771–9
12. Ding H, Dolan PJ, Johnson GV (2008) Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem 106:2119–30
13. Dohm CP, Kermer P, Bahr M (2008) Aggregopathy in neurodegenerative diseases: mechanisms and therapeutic implication. Neurodegener Dis 5:321–38
14. Fiesel FC, Voigt A, Weber SS et al (2010) Knockdown of transactive response DNA-binding protein (TDP-43) downregulates histone deacetylase 6. EMBO J 29:209–21
15. Fort P, Marty L, Piechaczyk M et al (1985) Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res 13:1431–42
16. Goldbaum O, Richter-Landsberg C (2004) Proteolytic stress causes heat shock protein induction, tau ubiquitination, and the recruitment of ubiquitin to tau-positive aggregates in oligodendrocytes in culture. J Neurosci 24:5748–57
17. Goldbaum O, Oppermann M, Handschuh M et al (2003) Proteasome inhibition stabilizes tau inclusions in oligodendroglial cells that occur after treatment with okadaic acid. J Neurosci 23:8872–80
18. Goldbaum O, Vollmer G, Richter-Landsberg C (2006) Proteasome inhibition by MG-132 induces apoptotic cell death and mitochondrial dysfunction in cultured rat brain oligodendrocytes but not in astrocytes. Glia 53:891–901
19. Goldbaum O, Riedel M, Stahnke T, Richter-Landsberg C (2009) The small heat shock protein HSP25 protects astrocytes against stress induced by proteasomal inhibition. Glia 57:1566–77
20. He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67–93
21. Irwin DJ, Cohen TJ, Grossman M et al (2012) Acetylated tau, a novel pathological signature in Alzheimer’s disease and other tauopathies. Brain 135:807–18
22. Janen SB, Chaachouay H, Richter-Landsberg C (2010) Autophagy is activated by proteasomal inhibition and involved in aggresome clearance in cultured astrocytes. Glia 58:1766–74
23. Jellinger KA (2012) Interaction between pathogenic proteins in neurodegenerative disorders. J Cell Mol Med 16:1166–83
24. Johansen T, Lamark T (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7:279–96
25. Kawaguchi Y, Kovacs JJ, McLaurin A, Vance JM, Ito A, Yao TP (2003) The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115:727–38
26. Kirkin V, McEwan DG, Novak I, Dikic I (2009) A role for ubiquitin in selective autophagy. Mol Cell 34:259–69
27. Klionsky DJ, Abdalla FC, Abeliovich H et al (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445–544
28. Kopito RR (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10:524–30
29. Lee JY, Koga H, Kawaguchi Y et al (2010) HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J 29:969–80
30. Li Y, Shin D, Kwon SH (2013) Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J 280:775–93
31. Matsuyama A, Shimazu T, Sumida Y et al (2002) In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J 21:6820–31
32. Matthias P, Yoshida M, Khochbin S (2008) HDAC6 a new cellular stress surveillance factor. Cell Cycle 7:7–10
33. Miki Y, Mori F, Tanji K, Kakita A, Takahashi H, Wakabayashi K (2011) Accumulation of histone deacetylase 6, an aggresome-related protein, is specific to Lewy bodies and glial cytoplasmic inclusions. Neuropathology 31:561–8
34. Miller DW, Cookson MR, Dickson DW (2004) Glial cell inclusions and the pathogenesis of neurodegenerative diseases. Neuron Glia Biol 1:13–21
35. Min SW, Cho SH, Zhou Y et al (2010) Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 67:953–66
36. Mizushima N, Yoshimori T, Levine B (2010) Methods in mammalian autophagy research. Cell 140:313–26
37. Neuhoff V, Philipp K, Zimmer HG, Mesecke S (1979) A simple, versatile, sensitive and volume-independent method for quantitative protein determination which is independent of other external influences. Hoppe Seylers Z Physiol Chem 360:1657–70
38. Nixon RA (2006) Autophagy in neurodegenerative disease: friend, foe or turncoat? Trends Neurosci 29:528–35
39. Noack M, Leyk J, Richter-Landsberg C (2014) HDAC6 inhibition results in tau acetylation and modulates tau phosphorylation and degradation in oligodendrocytes. Glia 62:535–47
40. Odagiri S, Tanji K, Mori F et al (2013) Brain expression level and activity of HDAC6 protein in neurodegenerative dementia. Biochem Biophys Res Commun 430:394–9
41. Pandey UB, Nie Z, Batlevi Y et al (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447:859–63
42. Richter-Landsberg C (2007) Heat shock proteins: expression and functional roles in nerve cells and glia, in heat shock proteins in neural cells. Landes Bioscience, New York, pp 1–12
43. Richter-Landsberg C (2008) The cytoskeleton in oligodendrocytes. Microtubule dynamics in health and disease. J Mol Neurosci 35:55–63
44. Richter-Landsberg C, Bauer NG (2004) Tau-inclusion body formation in oligodendroglia: the role of stress proteins and proteasome inhibition. Int J Dev Neurosci 22:443–51
45. Richter-Landsberg C, Gorath M (1999) Developmental regulation of alternatively spliced isoforms of mRNA encoding MAP2 and tau in rat brain oligodendrocytes during culture maturation. J Neurosci Res 56:259–70
46. Richter-Landsberg C, Heinrich M (1996) OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J Neurosci Res 45:161–73
47. Richter-Landsberg C, Leyk J (2013) Inclusion body formation, macroautophagy, and the role of HDAC6 in neurodegeneration. Acta Neuropathol 126:793–807
48. Richter-Landsberg C, Vollgraf U (1998) Mode of cell injury and death after hydrogen peroxide exposure in cultured oligodendroglia cells. Exp Cell Res 244:218–29
49. Roach A, Boylan K, Horvath S, Prusiner SB, Hood LE (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell 34:799–806
50. Schwartz AL, Ciechanover A (2009) Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 49:73–96
51. Schwarz L, Goldbaum O, Bergmann M, Probst-Cousin S, Richter-Landsberg C (2012) Involvement of macroautophagy in multiple system atrophy and protein aggregate formation in oligodendrocytes. J Mol Neurosci 47:256–66
52. Seiberlich V, Borchert J, Zhukareva V, Richter-Landsberg C (2013) Inhibition of protein deubiquitination by PR-619 activates the autophagic pathway in OLN-t40 oligodendroglial cells. Cell Biochem Biophys 67:149–60
53. Taylor JP, Tanaka F, Robitschek J et al (2003) Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum Mol Genet 12:749–57
54. van Stipdonk MJ, Willems AA, Plomp AC, van Noort JM, Boog CJ (2000) Tolerance controls encephalitogenicity of alphaB-crystallin in the Lewis rat. J Neuroimmunol 103:103–11
55. Xilouri M, Stefanis L (2011) Autophagic pathways in Parkinson disease and related disorders. Expert Rev Mol Med 13:e8
56. Zilberman Y, Ballestrem C, Carramusa L, Mazitschek R, Khochbin S, Bershadsky A (2009) Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J Cell Sci 122:3531–41