HDAC6 inhibitor blocks amyloid beta-induced impairment of mitochondrial transport in hippocampal neurons

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Kim, Chaeyoung ^a   Choi, Heesun ^a   Jung, Eun Sun ^a   Lee, Wonik ^a   Oh, Soojung ^b   Jeon, Noo Li ^b   Mook Jung, Inhee ^a  

^a Seoul National University College of Medicine   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TUBULIN; AMYLOID BETA PROTEIN; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE 6 INHIBITOR; HISTONE DEACETYLASE INHIBITOR; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MOTILITY; CONTROLLED STUDY; DEACETYLATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYO; ENZYME INHIBITION; FEMALE; GENETIC TRANSFECTION; HIPPOCAMPUS; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; MICROFLUIDICS; NERVE FIBER TRANSPORT; NONHUMAN; PHARMACOLOGICAL BLOCKING; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

ACETYLATION; AMYLOID BETA-PEPTIDES; ANIMALS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELLS, CULTURED; FEMALE; HIPPOCAMPUS; HISTONE DEACETYLASES; IMMUNOHISTOCHEMISTRY; MITOCHONDRIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; TUBULIN;

EID: 84865179881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042983     Document Type: Article

References (44)

1. Janke C, Kneussel M, (2010) Tubulin post-translational modifications: encoding functions on the neuronal microtubule cytoskeleton. Trends Neurosci 33: 362-372.
2. Fukushima N, Furuta D, Hidaka Y, Moriyama R, Tsujiuchi T, (2009) Post-translational modifications of tubulin in the nervous system. J Neurochem 109: 683-693.
3. Hammond JW, Cai D, Verhey KJ, (2008) Tubulin modifications and their cellular functions. Curr Opin Cell Biol 20: 71-76.
4. Dent EW, Gertler FB, (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40: 209-227.
5. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, et al. (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol 16: 2166-2172.
6. Bulinski JC, (2007) Microtubule modification: acetylation speeds anterograde traffic flow. Curr Biol 17: R18-20.
7. Zhang Y, Gilquin B, Khochbin S, Matthias P, (2006) Two catalytic domains are required for protein deacetylation. J Biol Chem 281: 2401-2404.
8. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, et al. (2005) Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307: 1282-1288.
9. Hempen B, Brion JP, (1996) Reduction of acetylated alpha-tubulin immunoreactivity in neurofibrillary tangle-bearing neurons in Alzheimer's disease. J Neuropathol Exp Neurol 55: 964-972.
10. Henriques AG, Vieira SI, da Cruz ESEF, da Cruz ESOA, (2010) Abeta promotes Alzheimer's disease-like cytoskeleton abnormalities with consequences to APP processing in neurons. J Neurochem 113: 761-771.
11. Ding H, Dolan PJ, Johnson GV, (2008) Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem 106: 2119-2130.
12. Calkins MJ, Reddy PH, (2011) Amyloid beta impairs mitochondrial anterograde transport and degenerates synapses in Alzheimer's disease neurons. Biochim Biophys Acta 1812: 507-513.
13. Decker H, Lo KY, Unger SM, Ferreira ST, Silverman MA, (2010) Amyloid-beta peptide oligomers disrupt axonal transport through an NMDA receptor-dependent mechanism that is mediated by glycogen synthase kinase 3beta in primary cultured hippocampal neurons. J Neurosci 30: 9166-9171.
14. Rui Y, Tiwari P, Xie Z, Zheng JQ, (2006) Acute impairment of mitochondrial trafficking by beta-amyloid peptides in hippocampal neurons. J Neurosci 26: 10480-10487.
15. Du H, Guo L, Yan S, Sosunov AA, McKhann GM, et al. (2010) Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc Natl Acad Sci U S A 107: 18670-18675.
16. Hirai K, Aliev G, Nunomura A, Fujioka H, Russell RL, et al. (2001) Mitochondrial abnormalities in Alzheimer's disease. J Neurosci 21: 3017-3023.
17. Rice SE, Gelfand VI, (2006) Paradigm lost: milton connects kinesin heavy chain to miro on mitochondria. J Cell Biol 173: 459-461.
18. Frederick RL, Shaw JM, (2007) Moving mitochondria: establishing distribution of an essential organelle. Traffic 8: 1668-1675.
19. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, et al. (2002) HDAC6 is a microtubule-associated deacetylase. Nature 417: 455-458.
20. Zhang Y, Li N, Caron C, Matthias G, Hess D, et al. (2003) HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22: 1168-1179.
21. Butler KV, Kalin J, Brochier C, Vistoli G, Langley B, et al. (2010) Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J Am Chem Soc 132: 10842-10846.
22. Silva DF, Esteves AR, Arduino DM, Oliveira CR, Cardoso SM, (2011) Amyloid-beta-Induced Mitochondrial Dysfunction Impairs the Autophagic Lysosomal Pathway in a Tubulin Dependent Pathway. J Alzheimers Dis 26 (3): 565-581.
23. Varadi A, Johnson-Cadwell LI, Cirulli V, Yoon Y, Allan VJ, et al. (2004) Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J Cell Sci 117: 4389-4400.
24. Anesti V, Scorrano L, (2006) The relationship between mitochondrial shape and function and the cytoskeleton. Biochim Biophys Acta 1757: 692-699.
25. Lee JS, Yoon YG, Yoo SH, Jeong NY, Jeong SH, et al. (2011) Histone deacetylase inhibitors induce mitochondrial elongation. J Cell Physiol 227 (7): 2856-2869.
26. Caspersen C, Wang N, Yao J, Sosunov A, Chen X, et al. (2005) Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J 19: 2040-2041.
27. Morfini GA, Burns M, Binder LI, Kanaan NM, LaPointe N, et al. (2009) Axonal transport defects in neurodegenerative diseases. J Neurosci 29: 12776-12786.
28. Chang DT, Reynolds IJ, (2006) Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 80: 241-268.
29. Wang X, Su B, Siedlak SL, Moreira PI, Fujioka H, et al. (2008) Amyloid-beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci U S A 105: 19318-19323.
30. Lei P, Ayton S, Bush AI, Adlard PA, (2011) GSK-3 in Neurodegenerative Diseases. Int J Alzheimers Dis 2011: 189246.
31. Chen S, Owens GC, Makarenkova H, Edelman DB, (2010) HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS One 5: e10848.
32. d'Ydewalle C, Krishnan J, Chiheb DM, Van Damme P, Irobi J, et al. (2011) HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease. Nat Med 17: 968-974.
33. Zilberman Y, Ballestrem C, Carramusa L, Mazitschek R, Khochbin S, et al. (2009) Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J Cell Sci 122: 3531-3541.
34. Goldstein LS, Yang Z, (2000) Microtubule-based transport systems in neurons: the roles of kinesins and dyneins. Annu Rev Neurosci 23: 39-71.
35. Dompierre JP, Godin JD, Charrin BC, Cordelieres FP, King SJ, et al. (2007) Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J Neurosci 27: 3571-3583.
36. Wang X, Perry G, Smith MA, Zhu X, (2010) Amyloid-beta-derived diffusible ligands cause impaired axonal transport of mitochondria in neurons. Neurodegener Dis 7: 56-59.
37. Reddy PH, (2007) Mitochondrial dysfunction in aging and Alzheimer's disease: strategies to protect neurons. Antioxid Redox Signal 9: 1647-1658.
38. Mattson MP, Gleichmann M, Cheng A, (2008) Mitochondria in neuroplasticity and neurological disorders. Neuron 60: 748-766.
39. Misko A, Jiang S, Wegorzewska I, Milbrandt J, Baloh RH, (2010) Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci 30: 4232-4240.
40. Cha MY, Han SH, Son SM, Hong HS, Choi YJ, et al. (2012) Mitochondria-specific accumulation of amyloid beta induces mitochondrial dysfunction leading to apoptotic cell death. PLoS One 7: e34929.
41. Miller KE, Sheetz MP, (2004) Axonal mitochondrial transport and potential are correlated. J Cell Sci 117: 2791-2804.
42. Kaech S, Banker G, (2006) Culturing hippocampal neurons. Nat Protoc 1: 2406-2415.
43. Park JW, Vahidi B, Taylor AM, Rhee SW, Jeon NL, (2006) Microfluidic culture platform for neuroscience research. Nat Protoc 1: 2128-2136.
44. Boo JH, Song H, Kim JE, Kang DE, Mook-Jung I, (2009) Accumulation of phosphorylated beta-catenin enhances ROS-induced cell death in presenilin-deficient cells. PLoS One 4: e4172.