Centrosomal aggregates and Golgi fragmentation disrupt vesicular trafficking of DAT

Neurobiology of Aging

Volumn 33, Issue 10, 2012, Pages 2462-2477

  Diaz Corrales, Francisco J ^a   Miyazaki, Ikuko ^b   Asanuma, Masato ^b   Ruano, Diego ^c   Rios, Rosa M ^a  

^a CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^b OKAYAMA UNIVERSITY   (Japan)

^c UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Tubulin; Aggresome; Centrosome; Dopamine transporter; Golgi apparatus; Inclusion bodies; Lewy bodies; Microtubules; Neurodegeneration; Parkinson's disease; Proteasome; Protein aggregation

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; DOPAMINE TRANSPORTER; GAMMA TUBULIN; PROTEASOME; VIRUS GLYCOPROTEIN;

ACETYLATION; ARTICLE; BIOACCUMULATION; CELL AGGREGATION; CELL MEMBRANE TRANSPORT; CELL VACUOLE; CELL VIABILITY; CENTROSOME; CONTROLLED STUDY; ENZYME INHIBITION; GOLGI COMPLEX; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; TRANS GOLGI NETWORK;

BIOLOGICAL TRANSPORT; CELL LINE; CENTROSOME; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GOLGI APPARATUS; HUMANS; LEUPEPTINS; MICROTUBULES; PROTEASOME INHIBITORS; TUBULIN;

EID: 84864390880     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.11.014     Document Type: Article

References (51)

1. Adams J.R., van Netten H., Schulzer M., Mak E., McKenzie J., Strongosky A., Sossi V., Ruth T.J., Lee C.S., Farrer M., Gasser T., Uitti R.J., Calne D.B., Wszolek Z.K., Stoessl A.J. PET in LRRK2 mutations: comparison to sporadic Parkinson's disease and evidence for presymptomatic compensation. Brain 2005, 128:2777-2785.
2. Afonso-Oramas D., Cruz-Muros I., Barroso-Chinea P., Alvarez de la Rosa D., Castro-Hernandez J., Salas-Hernandez J., Giradlez T., Gonzalez-Hernandez T. The dopamine transporter is differentially regulated after dopaminergic lesion. Neurobiol. Dis 2010, 40:518-530.
3. Ardley H.C., Scott G.B., Rose S.A., Tan N.G., Markham A.F., Robinson P.A. Inhibition of proteasomal activity causes inclusion formation in neuronal and non-neuronal cells overexpressing Parkin. Mol. Biol. Cell 2003, 14:4541-4556.
4. Betarbet R., Sherer T.B., Greenamyre J.T. Ubiquitin-proteasome system and Parkinson's diseases. Exp. Neurol 2005, 191:S17-S27.
5. Cardenas J., Rivero S., Goud B., Bornens M., Rios R.M. Golgi localisation of GMAP210 requires two distinct cis-membrane binding mechanisms. BMC Biol 2009, 7:56.
6. Conde C., Cáceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci 2009, 10:319-332.
7. de Lau L.M., Breteler M.M. Epidemiology of Parkinson's disease. Lancet Neurol 2006, 5:525-535.
8. Diaz-Corrales F.J., Asanuma M., Miyazaki I., Miyoshi K., Ogawa N. Rotenone induces aggregation of gamma-tubulin protein and subsequent disorganization of the centrosome: relevance to formation of inclusion bodies and neurodegeneration. Neuroscience 2005, 133:117-135.
9. Didier C., Merdes A., Gairin J.E., Jabrane-Ferrat N. Inhibition of proteasome activity impairs centrosome-dependent microtubule nucleation and organization. Mol. Biol. Cell 2008, 19:1220-1229.
10. Fan J., Hu Z., Zeng L., Lu W., Tang X., Zhang J., Li T. Golgi apparatus and neurodegenerative diseases. Int. J. Dev. Neurosci 2008, 26:523-534.
11. Fujita Y., Ohama E., Takatama M., Al-Sarraj S., Okamoto K. Fragmentation of Golgi apparatus of nigral neurons with alpha-synuclein-positive inclusions in patients with Parkinson's disease. Acta Neuropathol 2006, 112:261-265.
12. Fukushima N., Furuta D., Hidaka Y., Moriyama R., Tsujiuchi T. Post-translational modifications of tubulin in the nervous system. J. Neurochem 2009, 109:683-693.
13. Gonatas N.K., Stieber A., Gonatas J.O. Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J. Neurol. Sci 2006, 246:21-30.
14. Gosavi N., Lee H.J., Lee J.S., Patel S., Lee S.J. Golgi fragmentation occurs in the cells with prefibrillar alpha-synuclein aggregates and precedes the formation of fibrillar inclusion. J. Biol. Chem 2002, 277:48984-48992.
15. Hirschberg K., Miller C.M., Ellenberg J., Presley J.F., Siggia E.D., Phair R.D., Lippincott-Schwartz J. Kinetic analysis of secretory protein traffic and characterization of golgi to plasma membrane transport intermediates in living cells. J. Cell Biol 1998, 143:1485-1503.
16. Infante C., Ramos-Morales F., Fedriani C., Bornens M., Rios R.M. GMAP-210, A cis-Golgi network-associated protein, is a minus end microtubule-binding protein. J. Cell Biol 1999, 145:83-98.
17. Jellinger K.A. Recent advances in our understanding of neurodegeneration. J. Neural Transm 2009, 116:1111-1162.
18. Johnston J.A., Ward C.L., Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol 1998, 143:1883-1898.
19. Kawaguchi Y., Kovacs J.J., McLaurin A., Vance J.M., Ito A., Yao T.P. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115:727-738.
20. Lee C.S., Samii A., Sossi V., Ruth T.J., Schulzer M., Holden J.E., Wudel J., Pal P.K., de la Fuente-Fernandez R., Calne D.B., Stoessl A.J. In vivo positron emission tomographic evidence for compensatory changes in presynaptic dopaminergic nerve terminals in Parkinson's disease. Ann. Neurol 2000, 47:493-503.
21. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
22. Levy O.A., Malagelada C., Greene L.A. Cell death pathways in Parkinson's disease: proximal triggers, distal effectors, and final steps. Apoptosis 2009, 14:478-500.
23. Li L.B., Chen N., Ramamoorthy S., Chi L., Cui X.N., Wang L.C., Reith M.E. The role of N-glycosylation in function and surface trafficking of the human dopamine transporter. J. Biol. Chem 2004, 279:21012-21020.
24. Liang Y.J., Zhen J., Chen N., Reith M.E. Interaction of catechol and non-catechol substrates with externally or internally facing dopamine transporters. J. Neurochem 2009, 109:981-994.
25. Lieu Z.Z., Derby M.C., Gleeson P.A. Structure and domain organization of the trans-Golgi network. The Golgi Apparatus-State of the Art 110 Years After Camilo Golgi's Discovery 2008, 358-374. Springer, Wien, Austria. A.A. Mironov, A.A. Pavelka (Eds.).
26. McNaught K.S., Mytilineou C., Jnobaptiste R., Yabut J., Shashidharan P., Jennert P., Olanow C.W. Impairment of the ubiquitin-proteasome system causes dopaminergic cell death and inclusion body formation in ventral mesencephalic cultures. J. Neurochem 2002, 81:301-306.
27. McNaught K.S., Olanow C.W. Protein aggregation in the pathogenesis of familial and sporadic Parkinson's disease. Neurobiol. Aging 2006, 27:530-545.
28. McNaught K.S., Shashidharan P., Perl D.P., Jenner P., Olanow C.W. Aggresome-related biogenesis of Lewy bodies. Eur. J. Neurosci 2002, 16:2136-2148.
29. Moudjou M., Bordes N., Paintrand M., Bornens M. gamma-Tubulin in mammalian cells: the centrosomal and the cytosolic forms. J. Cell Sci 1996, 109:875-887.
30. Mourelatos Z., Gonatas N.K., Stieber A., Gurney M.E., Dal Canto M.C. The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:5472-5477.
31. Nakagomi S., Barsoum M.J., Bossy-Wetzel E., Sütterlin C., Malhotra V., Lipton S.A. A Golgi fragmentation pathway in neurodegeneration. Neurobiol. Dis 2008, 29:221-231.
32. Nigg E.A., Raff J.W. Centrioles, centrosomes, and cilia in health and disease. Cell 2009, 139:663-678.
33. Olanow C.W., Perl D.P., DeMartino G.N., McNaught K.S. Lewy-body formation is an aggresome-related process: a hypothesis. Lancet Neurol 2004, 3:496-503.
34. Olzmann J.A., Li L., Chin L.S. Aggresome formation and neurodegenerative diseases: therapeutic implications. Curr. Med. Chem 2008, 15:47-60.
35. Piperno G., LeDizet M., Chang X.J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol 1987, 104:289-302.
36. Raynaud-Messina B., Merdes A. Gamma-tubulin complexes and microtubule organization. Curr. Opin. Cell Biol 2007, 19:24-30.
37. Ríos R.M., Sanchís A., Tassin A.M., Fedriani C., Bornens M. GMAP-210 recruits gamma-tubulin complexes to cis-Golgi membranes and is required for Golgi ribbon formation. Cell 2004, 118:323-335.
38. Rios R.M., Tassin A.M., Celati C., Antony C., Boissier M.C., Homberg J.C., Bornens M. A peripheral protein associated with the cis-Golgi network redistributes in the intermediate compartment upon brefeldin A treatment. J. Cell Biol 1994, 125:997-1013.
39. Shults C.W. Lewy bodies. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:1661-1668.
40. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997, 388:839-840.
41. Storch A., Ludolph A.C., Schwarz J. Dopamine transporter: involvement in selective dopaminergic neurotoxicity and degeneration. J. Neural Transm 2004, 111:1267-1286.
42. Sun F., Anantharam V., Zhang D., Latchoumycandane C., Kanthasamy A., Kanthasamy A.G. Proteasome inhibitor MG-132 induces dopaminergic degeneration in cell culture and animal models. Neurotoxicology 2006, 27:807-815.
43. Sytnyk V., Leshchyns'ka I., Dityatev A., Schachner M. Trans-Golgi network delivery of synaptic proteins in synaptogenesis. J. Cell Sci 2004, 117:381-388.
44. Tanaka M., Kim Y.M., Lee G., Junn E., Iwatsubo T., Mouradian M.M. Aggresomes formed by alpha-synuclein and synphilin-1 are cytoprotective. J. Biol. Chem 2004, 279:4625-4631.
45. Tang B.L. Protein trafficking mechanisms associated with neurite outgrowth and polarized sorting in neurons. J. Neurochem 2001, 79:923-930.
46. Thayanidhi N., Helm J.R., Nycz D.C., Bentley M., Liang Y., Hay J.C. Alpha-synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol. Biol. Cell 2010, 21:1850-1863.
47. Thyberg J., Moskalewski S. Role of microtubules in the organization of the Golgi complex. Exp. Cell Res 1999, 246:263-279.
48. Wakabayashi K., Tanji K., Mori F., Takahashi H. The Lewy body in Parkinson's disease: molecules implicated in the formation and degradation of alpha-synuclein aggregates. Neuropathology 2007, 27:494-506.
49. Waxman E.A., Covy J.P., Bukh I., Li X., Dawson T.M., Giasson B.I. Leucine-rich repeat kinase 2 expression leads to aggresome formation that is not associated with alpha-synuclein inclusions. J. Neuropathol. Exp. Neurol 2009, 68:785-796.
50. Xie W., Li X., Li C., Zhu W., Jankovic J., Le W. Proteasome inhibition modeling nigral neuron degeneration in Parkinson's disease. J. Neurochem 2010, 115:188-199.
51. Zahniser N.R., Sorkin A. Trafficking of dopamine transporters in psychostimulant actions. Semin. Cell Dev. Biol 2009, 20:411-417.