ATAT1-enriched vesicles promote microtubule acetylation via axonal transport.

[en] Microtubules are polymerized dimers of alpha- and beta-tubulin that underlie a broad range of cellular activities. Acetylation of alpha-tubulin by the acetyltransferase ATAT1 modulates microtubule dynamics and functions in neurons. However, it remains unclear how this enzyme acetylates microtubules over long distances in axons. Here, we show that loss of ATAT1 impairs axonal transport in neurons in vivo, and cell-free motility assays confirm a requirement of alpha-tubulin acetylation for proper bidirectional vesicular transport. Moreover, we demonstrate that the main cellular pool of ATAT1 is transported at the cytosolic side of neuronal vesicles that are moving along axons. Together, our data suggest that axonal transport of ATAT1-enriched vesicles is the predominant driver of alpha-tubulin acetylation in axons.

Disciplines :

Neurology

Author, co-author :

Even, Aviel

Morelli, Giovanni

Broix, Loïc ; Université de Liège - ULiège > Stem Cells-Molecular Regulation of Neurogenesis

Scaramuzzino, Chiara

Turchetto, Silvia ; Université de Liège - ULiège > Stem Cells-Molecular Regulation of Neurogenesis

Gladwyn-Ng, Ivan

Le Bail, Romain ; Université de Liège - ULiège > Stem Cells-Molecular Regulation of Neurogenesis

Shilian, Michal

Freeman, Stephen

Magiera, Maria M.

More authors (10 more)

Language :

English

Title :

ATAT1-enriched vesicles promote microtubule acetylation via axonal transport.

Publication date :

2019

Journal title :

Science Advances

eISSN :

2375-2548

Publisher :

American Association for the Advancement of Science (AAAS), Washington, United States

Volume :

Issue :

Pages :

eaax2705

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Copyright (c) 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Available on ORBi :

since 16 January 2020

Statistics

Number of views

95 (25 by ULiège)

Number of downloads

141 (17 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

N. Hirokawa, S. Niwa, Y. Tanaka, Molecular motors in neurons: Transport mechanisms and roles in brain function, development, and disease. Neuron 68, 610–638 (2010).
C. Janke, J. C. Bulinski, Post-translational regulation of the microtubule cytoskeleton: Mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12, 773–786 (2011).
Y. Song, S. T. Brady, Post-translational modifications of tubulin: Pathways to functional diversity of microtubules. Trends Cell Biol. 25, 125–136 (2015).
J. P. Dompierre, J. D. Godin, B. C. Charrin, F. P. Cordelières, S. J. King, S. Humbert, F. Saudou, Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 27, 3571–3583 (2007).
N. A. Reed, D. Cai, T. L. Blasius, G. T. Jih, E. Meyhofer, J. Gaertig, K. J. Verhey, Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16, 2166–2172 (2006).
V. K. Godena, N. Brookes-Hocking, A. Moller, G. Shaw, M. Oswald, R. M. Sancho, C. C. J. Miller, A. J. Whitworth, K. J. De Vos, Increasing microtubule acetylation rescues axonal transport and locomotor deficits caused by LRRK2 Roc-COR domain mutations. Nat. Commun. 5, 5245 (2014).
J. S. Akella, D. Wloga, J. Kim, N. G. Starostina, S. Lyons-Abbott, N. S. Morrissette, S. T. Dougan, E. T. Kipreos, J. Gaertig, MEC-17 is an α-Tubulin acetyltransferase. Nature 467, 218–222 (2010).
T. Shida, J. G. Cueva, Z. Xu, M. B. Goodman, M. V. Nachury, The major α-Tubulin K40 acetyltransferase α-TAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc. Natl. Acad. Sci. U.S.A. 107, 21517–21522 (2010).
S. C. Howes, G. M. Alushin, T. Shida, M. V. Nachury, E. Nogales, Effects of tubulin acetylation and tubulin acetyltransferase binding on microtubule structure. Mol. Biol. Cell 25, 257–266 (2014).
Z. Xu, L. Schaedel, D. Portran, A. Aguilar, J. Gaillard, M. P. Marinkovich, M. Théry, M. V. Nachury, Microtubules acquire resistance from mechanical breakage through intralumenal acetylation. Science 356, 328–332 (2017).
C. Coombes, A. Yamamoto, M. M. Clellan, T. A. Reid, M. Plooster, G. W. G. Luxton, J. Alper, J. Howard, M. K. Gardner, Mechanism of microtubule lumen entry for the α-Tubulin acetyltransferase enzyme αTAT1. Proc. Natl. Acad. Sci. U.S.A. 113, E7176–E7184 (2016).
N. Ly, N. Elkhatib, E. Bresteau, O. Piétrement, M. Khaled, M. M. Magiera, C. Janke, E. L. Cam, A. D. Rutenberg, G. Montagnac, αTAT1 controls longitudinal spreading of acetylation marks from open microtubules extremities. Sci. Rep. 6, 35624 (2016).
L. Balabanian, C. L. Berger, A. G. Hendricks, Acetylated microtubules are preferentially bundled leading to enhanced kinesin-1 motility. Biophys. J. 113, 1551–1560 (2017).
G. W. Kim, L. Li, M. Gorbani, L. You, X. J. Yang, Mice lacking α-Tubulin acetyltransferase 1 are viable but display α-Tubulin acetylation deficiency and dentate gyrus distortion. J. Biol. Chem. 288, 20334–20350 (2013).
T. Shida, J. G. Cueva, Z. Xu, M. B. Goodman, M. V. Nachury, The major α-Tubulin K40 acetyltransferase αTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc. Natl. Acad. Sci. U.S.A. 107, 21517–21522 (2010).
G. Morelli, A. Even, I. Gladwyn-Ng, R. L. Bail, M. Shilian, J. D. Godin, E. Peyre, B. A. Hassan, A. Besson, J.-M. Rigo, M. Weil, B. Brône, L. Nguyen, p27Kip1 Modulates Axonal Transport by Regulating α-Tubulin Acetyltransferase 1 Stability. Cell Rep. 23, 2429–2442 (2018).
C. Hubbert, A. Guardiola, R. Shao, Y. Kawaguchi, A. Ito, A. Nixon, M. Yoshida, X.-F. Wang, T.-P. Yao, HDAC6 is a microtubule-associated deacetylase. Nature 417, 455–458 (2002).
K. V. Butler, J. Kalin, C. Brochier, G. Vistoli, B. Langley, A. P. Kozikowski, Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A. J. Am. Chem. Soc. 132, 10842–10846 (2010).
C. D. Nichols, J. Becnel, U. B. Pandey, Methods to assay Drosophila behavior. J. Vis. Exp. 7, 3795 (2012).
N. Kalebic, S. Sorrentino, E. Perlas, G. Bolasco, C. Martinez, P. A. Heppenstall, αTAT1 is the major α-Tubulin acetyltransferase in mice. Nat. Commun. 4, 1962 (2013).
S. Takamori, M. Holt, K. Stenius, E. A. Lemke, M. Grønborg, D. Riedel, H. Urlaub, S. Schenck, B. Brügger, P. Ringler, S. A. Müller, B. Rammner, F. Gräter, J. S. Hub, B. L. De Groot, G. Mieskes, Y. Moriyama, J. Klingauf, H. Grubmüller, J. Heuser, F. Wieland, R. Jahn, Molecular Anatomy of a Trafficking Organelle. Cell 127, 831–846 (2006).
G. H. H. Borner, M. Harbour, S. Hester, K. S. Lilley, M. S. Robinson, Comparative proteomics of clathrin-coated vesicles. J. Cell Biol. 175, 571–578 (2006).
M.-V. Hinckelmann, A. Virlogeux, C. Niehage, C. Poujol, D. Choquet, B. Hoflack, D. Zala, F. Saudou, Self-propelling vesicles define glycolysis as the minimal energy machinery for neuronal transport. Nat. Commun. 7, 13233 (2016).
D. Zala, M.-V. Hinckelmann, H. Yu, M. M. L. da Cunha, G. Liot, F. P. Cordelières, S. Marco, F. Saudou, Vesicular glycolysis provides on-board energy for fast axonal transport. Cell 152, 479–491 (2013).
G. Montagnac, V. Meas-Yedid, M. Irondelle, A. Castro-Castro, M. Franco, T. Shida, M. V. Nachury, A. Benmerah, J.-C. Olivo-Marin, P. Chavrier, αTAT1 catalyses microtubule acetylation at clathrin-coated pits. Nature 502, 567–570 (2013).
H.-J. Lee, S. Patel, S.-J. Lee, Intravesicular localization and exocytosis of α-synuclein and its aggregates. J. Neurosci. 25, 6016–6024 (2005).
R. Sainath, G. Gallo, The dynein inhibitor Ciliobrevin D inhibits the bidirectional transport of organelles along sensory axons and impairs NGF-mediated regulation of growth cones and axon branches. Dev. Neurobiol. 75, 757–777 (2015).
B. Neumann, M. A. Hilliard, Loss of MEC-17 leads to microtubule instability and axonal degeneration. Cell Rep. 6, 93–103 (2014).
S. J. Morley, Y. Qi, L. Iovino, L. Andolfi, D. Guo, N. Kalebic, L. Castaldi, C. Tischer, C. Portulano, G. Bolasco, K. Shirlekar, C. M. Fusco, A. Asaro, F. Fermani, M. Sundukova, U. Matti, L. Reymond, A. De Ninno, L. Businaro, K. Johnsson, M. Lazzarino, J. Ries, Y. Schwab, J. Hu, P. A. Heppenstall, Acetylated tubulin is essential for touch sensation in mice. eLife 5, e20813 (2016).
L. Li, D. Wei, Q. Wang, J. Pan, R. Liu, X. Zhang, L. Bao, MEC-17 deficiency leads to reduced α-Tubulin acetylation and impaired migration of cortical neurons. J. Neurosci. 32, 12673–12683 (2012).
J. A. Miller, S.-L. Ding, S. M. Sunkin, K. A. Smith, L. Ng, A. Szafer, A. Ebbert, Z. L. Riley, J. J. Royall, K. Aiona, J. M. Arnold, C. Bennet, D. Bertagnolli, K. Brouner, S. Butler, S. Caldejon, A. Carey, C. Cuhaciyan, R. A. Dalley, N. Dee, T. A. Dolbeare, B. A. C. Facer, D. Feng, T. P. Fliss, G. Gee, J. Goldy, L. Gourley, B. W. Gregor, G. Gu, R. E. Howard, J. M. Jochim, C. L. Kuan, C. Lau, C.-K. Lee, F. Lee, T. A. Lemon, P. Lesnar, B. M. Murray, N. Mastan, N. Mosqueda, T. Naluai-Cecchini, N.-K. Ngo, J. Nyhus, A. Oldre, E. Olson, J. Parente, P. D. Parker, S. E. Parry, A. Stevens, M. Pletikos, M. Reding, K. Roll, D. Sandman, M. Sarreal, S. Shapouri, N. V. Shapovalova, E. H. Shen, N. Sjoquist, C. R. Slaughterbeck, M. Smith, A. J. Sodt, D. Williams, L. Zöllei, B. Fischl, M. B. Gerstein, D. H. Geschwind, I. A. Glass, M. J. Hawrylycz, R. F. Hevner, H. Huang, A. R. Jones, J. A. Knowles, P. Levitt, J. W. Phillips, N. Šestan, P. Wohnoutka, C. Dang, A. Bernard, J. G. Hohmann, E. S. Lein, Transcriptional landscape of the prenatal human brain. Nature 508, 199–206 (2014).
I. A. Kent, P. S. Rane, R. B. Dickinson, A. J. Ladd, T. P. Lele, Transient pinning and pulling: A mechanism for bending microtubules. PLOS ONE 11, e0151322 (2016).
A. D. Bicek, E. Tüzel, A. Demtchouk, M. Uppalapati, W. O. Hancock, D. M. Kroll, D. J. Odde, Anterograde microtubule transport drives microtubule bending in LLC-PK1 epithelial cells. Mol. Biol. Cell 20, 2943–2953 (2009).
S. Triclin, D. Inoue, J. Gaillard, Z. M. Htet, M. De Santis, D. Portran, E. Derivery, C. Aumeier, L. Schaedel, K. John, C. Leterrier, S. Reck-Peterson, L. Blanchoin, M. Thery, Self-repair protects microtubules from their destruction by molecular motors. bioRxiv , 499020 (2018).
J. F. Díaz, I. Barasoain, J. M. Andreu, Fast kinetics of Taxol binding to microtubules. Effects of solution variables and microtubule-associated proteins. J. Biol. Chem. 278, 8407–8419 (2003).
D. Portran, L. Schaedel, Z. Xu, M. Théry, M. V. Nachury, Tubulin acetylation protects long-lived microtubules against mechanical ageing. Nat. Cell Biol. 19, 391–398 (2017).
M.-V. Hinckelmann, D. Zala, F. Saudou, Releasing the brake: Restoring fast axonal transport in neurodegenerative disorders. Trends Cell Biol. 23, 634–643 (2013).
J. W. Tsai, Y. Chen, A. R. Kriegstein, R. B. Vallee, LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170, 935–945 (2005).
V. Iefremova, G. Manikakis, O. Krefft, A. Jabali, K. Weynans, R. Wilkens, F. Marsoner, B. Brändl, F.-J. Müller, P. Koch, J. Ladewig, An organoid-based model of cortical development identifies non-cell-autonomous defects in Wnt signaling contributing to miller-dieker syndrome. Cell Rep. 19, 50–59 (2017).
E. Eden, R. Navon, I. Steinfeld, D. Lipson, Z. Yakhini, GOrilla: A tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10, 48 (2009).
S. Gluska, M. Chein, N. Rotem, A. Ionescu, E. Perlson, Tracking Quantum-Dot labeled neurotropic factors transport along primary neuronal axons in compartmental microfluidic chambers. Methods Cell Biol. 131, 365–387 (2016).
S. A. Shaver, C. A. Riedl, T. L. Parkes, M. B. Sokolowski, A. J. Hilliker, Isolation of larval behavioral mutants in Drosophila melanogaster. J. Neurogenet. 14, 193–205 (2000).
R. P. Chambers, G. B. Call, D. Meyer, J. Smith, J. A. Techau, K. Pearman, L. M. Buhlman, Nicotine increases lifespan and rescues olfactory and motor deficits in a Drosophila model of Parkinson's disease. Behav. Brain Res. 253, 95–102 (2013).
G. Morelli, A. Avila, S. Ravanidis, N. Aourz, R. L. Neve, I. Smolders, R. J. Harvey, J.-M. Rigo, L. Nguyen, B. Brône, Cerebral cortical circuitry formation requires functional glycine receptors. Cereb. Cortex 27, 1863–1877 (2016).
M. Barisic, R. S. e Sousa, S. K. Tripathy, M. M. Magiera, A. V. Zaytsev, A. L. Pereira, C. Janke, E. L. Grishchuk, H. Maiato, Mitosis. Microtubule detyrosination guides chromosomes during mitosis. Science 348, 799–803 (2015).