Autophagy and microtubules - new story, old players
Abstract
Summary: Both at a basal level and after induction (especially in response to nutrient starvation), the function of autophagy is to allow cells to degrade and recycle damaged organelles, proteins and other biological constituents. Here, we focus on the role microtubules have in autophagosome formation, autophagosome transport across the cytoplasm and in the formation of autolysosomes. Recent insights into the exact relationship between autophagy and microtubules now point to the importance of microtubule dynamics, tubulin post-translational modifications and microtubule motors in the autophagy process. Such factors regulate signaling pathways that converge to stimulate autophagosome formation. They also orchestrate the movements of pre-autophagosomal structures and autophagosomes or more globally organize and localize immature and mature autophagosomes and lysosomes. Most of the factors that now appear to link microtubules to autophagosome formation or to autophagosome dynamics and fate were identified initially without the notion that sequestration, recruitment and/or interaction with microtubules contribute to their function. Spatial and temporal coordination of many stages in the life of autophagosomes thus underlines the integrative role of microtubules and progressively reveals hidden parts of the autophagy machinery.
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Post-translational modifications of tubulin such as acetylation and tyrosination/detyrosination can act either singly or in concert with other modifications to control motor recruitment in a cargo-specific manner.
“Post-translational modifications of tubulin such as acetylation and tyrosination/detyrosination can act either singly or in concert with other modifications to control motor recruitment in a cargo-specific manner (Hammond et al., 2008; Mackeh et al., 2013).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Mackeh et al., 2013
Cites
1 retracted
Acharya, B. R., Bhattacharyya, S., Choudhury, D., & Chakrabarti, G. (2011) · APOPTOSIS · doi:10.1007/s10495-011-0613-1 · Cited by 69 · see citing works
RetractedAMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1
Kim, J., Kundu, M., Viollet, B., & Guan, K.-L. (2011) · Nature Cell Biology · doi:10.1038/ncb2152 · Cited by 7,227 · see citing works
Autophagy: Renovation of Cells and Tissues
Mizushima, N., & Komatsu, M. (2011) · Cell · doi:10.1016/j.cell.2011.10.026 · Cited by 6,467 · see citing works
Microtubules as a target for anticancer drugs
Jordan, M. A., & Wilson, L. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1317 · Cited by 4,534 · see citing works
Levine, B., & Klionsky, D. J. (2004) · Developmental Cell · doi:10.1016/s1534-5807(04)00099-1 · Cited by 3,671 · see citing works
Autophagy and the Integrated Stress Response
Kroemer, G., Mariño, G., & Levine, B. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.023 · Cited by 3,506 · see citing works
Dynamic instability of microtubule growth
Mitchison, T., & Kirschner, M. (1984) · Nature · doi:10.1038/312237a0 · Cited by 3,337 · see citing works
The Role of Atg Proteins in Autophagosome Formation
Mizushima, N., Yoshimori, T., & Ohsumi, Y. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154005 · Cited by 2,978 · see citing works
MICROTUBULE POLYMERIZATION DYNAMICS
Desai, A. B., & Mitchison, T. J. (1997) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.13.1.83 · Cited by 2,570 · see citing works
The Beclin 1 network regulates autophagy and apoptosis
Kang, R., Zeh, H. J., Lotze, M. T., & Tang, D. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.191 · Cited by 2,485 · see citing works
Sancak, Y., Bar-Peled, L., Zoncu, R., Markhard, A. L., Nada, S., & Sabatini, D. M. (2010) · Cell · doi:10.1016/j.cell.2010.02.024 · Cited by 2,464 · see citing works
HDAC6 is a microtubule-associated deacetylase
Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X.-F., & Yao, T.-P. (2002) · Nature · doi:10.1038/417455a · Cited by 2,403 · see citing works
Autophagosome formation: core machinery and adaptations
Xie, Z., & Klionsky, D. J. (2007) · Nature Cell Biology · doi:10.1038/ncb1007-1102 · Cited by 2,165 · see citing works
Rubinsztein, D. C., Mariño, G., & Kroemer, G. (2011) · Cell · doi:10.1016/j.cell.2011.07.030 · Cited by 2,107 · see citing works
ULK-Atg13-FIP200 Complexes Mediate mTOR Signaling to the Autophagy Machinery
Jung, C. H., Jun, C. B., Ro, S.-H., Kim, Y.-M., Otto, N. M., Cao, J., Kundu, M., & Kim, D.-H. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-12-1249 · Cited by 2,025 · see citing works
Mammalian autophagy: core molecular machinery and signaling regulation
Yang, Z., & Klionsky, D. J. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.11.014 · Cited by 1,956 · see citing works
Axe, E. L., Walker, S. A., Manifava, M., Chandra, P., Roderick, H. L., Habermann, A., Griffiths, G., & Ktistakis, N. T. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200803137 · Cited by 1,885 · see citing works
Regulation of Mammalian Autophagy in Physiology and Pathophysiology
Ravikumar, B., Sarkar, S., Davies, J. E., Futter, M., Garcı́a-Arencibia, M., Green-Thompson, Z. W., Jiménez-Sánchez, M., Korolchuk, V. I., Lichtenberg, M., Luo, S., et al. (2010) · Physiological Reviews · doi:10.1152/physrev.00030.2009 · Cited by 1,726 · see citing works
Microtubule nucleation by γ-tubulin complexes
Kollman, J. M., Merdes, A., Mourey, L., & Agard, D. A. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3209 · Cited by 1,583 · see citing works
The Human Sir2 Ortholog, SIRT2, Is an NAD+-Dependent Tubulin Deacetylase
North, B. J., Marshall, B. L., Borra, M. T., Denu, J. M., & Verdin, E. M. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00038-8 · Cited by 1,542 · see citing works
Kawaguchi, Y., Kovacs, J. J., McLaurin, A. C., Vance, J. M., Ito, A., & Yao, T. (2003) · Cell · doi:10.1016/s0092-8674(03)00939-5 · Cited by 1,529 · see citing works
Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks
Alers, S., Löffler, A. S., Wesselborg, S., & Stork, B. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06159-11 · Cited by 1,483 · see citing works
Autophagy modulation as a potential therapeutic target for diverse diseases
Rubinsztein, D. C., Codogno, P., & Levine, B. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3802 · Cited by 1,429 · see citing works
Self-citationJNK1-Mediated Phosphorylation of Bcl-2 Regulates Starvation-Induced Autophagy
Wei, Y., Pattingre, S., Sinha, S., Bassik, M., & Levine, B. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.06.001 · Cited by 1,329 · see citing works
HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS.
Pandey, U. B., Nie, Z., Batlevi, Y., McCray, B. A., Ritson, G. P., Nedelsky, N. B., Schwartz, S. L., DiProspero, N. A., Knight, M. A., Schuldiner, O., et al. (2007) · Nature · doi:10.1038/nature05853 · Cited by 1,234 · see citing works
Regulation of the mTOR Complex 1 Pathway by Nutrients, Growth Factors, and Stress
Sengupta, S., Peterson, T. R., & Sabatini, D. M. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.026 · Cited by 1,234 · see citing works
The Atg12-Atg5 Conjugate Has a Novel E3-like Activity for Protein Lipidation in Autophagy
Hanada, T., Noda, N. N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F., & Ohsumi, Y. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.c700195200 · Cited by 1,123 · cited 2× · see citing works
“Both contribute to the expansion and the closure of the vesicle in concert with two ubiquitin-like conjugation systems, resulting in the ATG12–ATG5-ATG16L complex and the phosphatidylethanolamine (PtdEtn) conjugate of microtubuleassociated protein 1 light chain 3 [LC3 (MLP3); the mammalian ortholog of Atg8 in budding…”
BackgroundThe Atg16L Complex Specifies the Site of LC3 Lipidation for Membrane Biogenesis in Autophagy
Fujita, N., Itoh, T., Omori, H., Fukuda, M., Noda, T., & Yoshimori, T. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-12-1257 · Cited by 1,083 · see citing works
The role of the Atg1/ULK1 complex in autophagy regulation
Mizushima, N. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.12.004 · Cited by 1,062 · see citing works
A subdomain of the endoplasmic reticulum forms a cradle for autophagosome formation
Hayashi, M., Fujita, N., Noda, T., Yamaguchi, A., Yoshimori, T., & Yamamoto, A. (2009) · Nature Cell Biology · doi:10.1038/ncb1991 · Cited by 1,050 · see citing works
Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice
Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E.-L., Hartmann, D., Lüllmann-Rauch, R., Janssen, P. M. L., Blanz, J., von Figura, K., & Saftig, P. (2000) · Nature · doi:10.1038/35022595 · Cited by 925 · see citing works
Microtubule Acetylation Promotes Kinesin-1 Binding and Transport
Reed, N. A., Cai, D., Blasius, T. L., Jih, G. T., Meyhofer, E., Gaertig, J., & Verhey, K. J. (2006) · Current Biology · doi:10.1016/j.cub.2006.09.014 · Cited by 919 · see citing works
Role for Rab7 in maturation of late autophagic vacuoles
Jäger, S., Bucci, C., Tanida, I., Ueno, T., Kominami, E., Säftig, P., & Eskelinen, E. (2004) · Journal of Cell Science · doi:10.1242/jcs.01370 · Cited by 907 · see citing works
Lysosomal positioning coordinates cellular nutrient responses
Korolchuk, V. I., Saiki, S., Lichtenberg, M., Siddiqi, F. H., Roberts, E. A., Imarisio, S., Jahreiss, L., Sarkar, S., Futter, M., Menzies, F. M., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2204 · Cited by 891 · see citing works
Autophagy, Immunity, and Microbial Adaptations
Deretic, V. P., & Levine, B. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.05.016 · Cited by 865 · see citing works
Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions
Janke, C., & Bulinski, J. C. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3227 · Cited by 838 · see citing works
Dompierre, J. P., Godin, J. D., Charrin, B. C., Cordelières, F. P., King, S. J., Humbert, S., & Saudou, F. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0037-07.2007 · Cited by 792 · see citing works
Autophagy in the Cellular Energetic Balance
Singh, R., & Cuervo, A. M. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.04.004 · Cited by 788 · see citing works
The Beclin 1–VPS34 complex – at the crossroads of autophagy and beyond
Funderburk, S. F., Wang, Q. J., & Yue, Z. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.03.002 · Cited by 778 · see citing works
HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo
Zhang, Y., Li, N., Caron, C., Matthias, G., Hess, D., Khochbin, S., & Matthias, P. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg115 · Cited by 740 · see citing works
Polson, H. E. J., de Lartigue, J., Rigden, D. J., Reedijk, M., Urbé, S., Clague, M. J., & Tooze, S. A. (2010) · Autophagy · doi:10.4161/auto.6.4.11863 · Cited by 712 · see citing works
Chen, Y., McMillan‐Ward, E., Kong, J., Israels, S. J., & Gibson, S. B. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402233 · Cited by 689 · see citing works
Rab7 is required for the normal progression of the autophagic pathway in mammalian cells
Gutierrez, M. G., Munafó, D. B., Berón, W., & Colombo, M. I. (2004) · Journal of Cell Science · doi:10.1242/jcs.01114 · Cited by 680 · see citing works
3D tomography reveals connections between the phagophore and endoplasmic reticulum
Ylä‐Anttila, P., Vihinen, H., Jokitalo, E., & Eskelinen, E. (2009) · Autophagy · doi:10.4161/auto.5.8.10274 · Cited by 670 · see citing works
Pankiv, S., Alemu, E. A., Brech, A., Bruun, J., Lamark, T., Øvervatn, A., Bjørkøy, G., & Johansen, T. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200907015 · Cited by 645 · see citing works
Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules
Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A., & Margolis, B. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.5.959 · Cited by 609 · see citing works
Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity
Zhao, Y., Yang, J. H., Liao, W., Liu, X., Zhang, H., Wang, S., Wang, D., Feng, J., Yu, L., & Zhu, W. (2010) · Nature Cell Biology · doi:10.1038/ncb2069 · Cited by 607 · see citing works
Zalckvar, E., Berissi, H., Mizrachy, L., Idelchuk, Y., Koren, I., Eisenstein, M., Sabanay, H., Pinkas‐Kramarski, R., & Kimchi, A. (2009) · The EMBO Reports · doi:10.1038/embor.2008.246 · Cited by 592 · see citing works
mDia mediates Rho-regulated formation and orientation of stable microtubules
Palazzo, A. F., Cook, T. A., Alberts, A. S., & Gundersen, G. G. (2001) · Nature Cell Biology · doi:10.1038/35087035 · Cited by 582 · see citing works
Orsi, A., Razi, M., Dooley, H. C., Robinson, D. J., Weston, A., Collinson, L., & Tooze, S. A. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-09-0746 · Cited by 570 · see citing works
The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy
Bartolomeo, S. D., Corazzari, M., Nazio, F., Oliverio, S., Lisi, G., Antonioli, M., Pagliarini, V., Matteoni, S., Fuoco, C., Giunta, L., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201002100 · Cited by 519 · see citing works
Lee, J., Nagano, Y., Taylor, J. P., Lim, K. L., & Yao, T. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201001039 · Cited by 517 · see citing works
Johansson, M., Rocha, N., Zwart, W., Jordens, I., Janssen, L., Kuijl, C., Olkkonen, V. M., & Neefjes, J. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200606077 · Cited by 505 · see citing works
Asymmetric CLASP-Dependent Nucleation of Noncentrosomal Microtubules at the trans-Golgi Network
Efimov, A., Kharitonov, A., Efimova, N., Lončarek, J., Miller, P. M., Andreyeva, N., Gleeson, P. A., Galjart, N., Maia, A. R. R., McLeod, I. X., et al. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.04.002 · Cited by 498 · see citing works
Atg101, a novel mammalian autophagy protein interacting with Atg13
Hosokawa, N., Sasaki, T., Iemura, S.-I., Natsume, T., Hara, T., & Mizushima, N. (2009) · Autophagy · doi:10.4161/auto.5.7.9296 · Cited by 488 · see citing works
Overview of macroautophagy regulation in mammalian cells
Mehrpour, M., Esclatine, A., Beau, I., & Codogno, P. (2010) · Cell Research · doi:10.1038/cr.2010.82 · Cited by 488 · see citing works
Self-citationDynein mutations impair autophagic clearance of aggregate-prone proteins
Ravikumar, B., Acevedo‐Arozena, A., Imarisio, S., Berger, Z., Vacher, C., O’Kane, C. J., Brown, S. D. M., & Rubinsztein, D. C. (2005) · Nature Genetics · doi:10.1038/ng1591 · Cited by 458 · see citing works
The Itinerary of Autophagosomes: From Peripheral Formation to Kiss‐and‐Run Fusion with Lysosomes
Jahreiss, L., Menzies, F. M., & Rubinsztein, D. C. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00701.x · Cited by 453 · see citing works
Microtubules Facilitate Autophagosome Formation and Fusion of Autophagosomes with Endosomes
Köchl, R., Hu, X. W., Chan, E. Y. W., & Tooze, S. A. (2005) · Traffic · doi:10.1111/j.1600-0854.2005.00368.x · Cited by 436 · see citing works
Dynein-dependent Movement of Autophagosomes Mediates Efficient Encounters with Lysosomes
Kimura, S., Noda, T., & Yoshimori, T. (2008) · Cell Structure and Function · doi:10.1247/csf.08005 · Cited by 434 · see citing works
Microtubules and signal transduction
Gundersen, G. G., & Cook, T. A. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80010-6 · Cited by 407 · see citing works
Autophagosome Precursor Maturation Requires Homotypic Fusion
Moreau, K., Ravikumar, B., Renna, M., Puri, C., & Rubinsztein, D. C. (2011) · Cell · doi:10.1016/j.cell.2011.06.023 · Cited by 382 · see citing works
Organization of organelles and membrane traffic by microtubules
Cole, N. B., & Lippincott‐Schwartz, J. (1995) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(95)80045-x · Cited by 323 · see citing works
The Golgi Complex Is a Microtubule-organizing Organelle
Chabin-Brion, K., Marceiller, J., Perez, F., Settegrana, C., Drechou, A., Durand, G., & Poüs, C. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.7.2047 · Cited by 319 · see citing works
Self-citationMitosis is not a key target of microtubule agents in patient tumors
Komlodi-Pasztor, E., Sackett, D., Wilkerson, J., & Fojo, T. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2010.228 · Cited by 312 · cited 1× · see citing works
“However, human tumour cells divide more slowly than cultured cell lines and tumour cells in animal models (for a review, see Komlodi-Pasztor et al., 2011).”
BackgroundSingle molecule imaging reveals differences in microtubule track selection between Kinesin motors
Cai, D., McEwen, D. P., Martens, J. R., Meyhofer, E., & Verhey, K. J. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000216 · Cited by 300 · see citing works
Miller, P. M., Folkmann, A. W., Maia, A. R. R., Efimova, N., Efimov, A., & Kaverina, I. (2009) · Nature Cell Biology · doi:10.1038/ncb1920 · Cited by 294 · see citing works
Fass, E., Shvets, E., Degani, I., Hirschberg, K., & Elazar, Z. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607031200 · Cited by 286 · see citing works
Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B
Mann, S. S., & Hammarback, J. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)78150-2 · Cited by 284 · see citing works
Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons
Hammond, J. W., Huang, C.-F., Kaech, S., Jacobson, C., Banker, G., & Verhey, K. J. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-01-0044 · Cited by 281 · see citing works
Detection of GTP-Tubulin Conformation in Vivo Reveals a Role for GTP Remnants in Microtubule Rescues
Dimitrov, A., Quesnoit, M., Moutel, S., Cantaloube, I., Poüs, C., & Perez, F. (2008) · Science · doi:10.1126/science.1165401 · Cited by 273 · see citing works
Self-citationDifferential turnover of tyrosinated and detyrosinated microtubules
Webster, D. R., Gundersen, G. G., Bulinski, J. C., & Borisy, G. G. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.24.9040 · Cited by 261 · see citing works
The formin mDia2 stabilizes microtubules independently of its actin nucleation activity
Bartolini, F., Moseley, J. B., Schmoranzer, J., Cassimeris, L., Goode, B. L., & Gundersen, G. G. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200709029 · Cited by 237 · see citing works
Multiple roles of the cytoskeleton in autophagy
Monastyrska, I., Rieter, E., Klionsky, D. J., & Reggiori, F. (2009) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2009.00082.x · Cited by 223 · see citing works
Geeraert, C., Ratier, A., Pfisterer, S. G., Perdiz, D., Cantaloube, I., Rouault, A., Pattingre, S., Proikas‐Cezanne, T., Codogno, P., & Poüs, C. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.091553 · Cited by 204 · see citing works
Self-citationBim Inhibits Autophagy by Recruiting Beclin 1 to Microtubules
Luo, S., Garcı́a-Arencibia, M., Zhao, R., Puri, C., Toh, P. P. C., Sadiq, O., & Rubinsztein, D. C. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.040 · Cited by 203 · see citing works
Acetylated microtubules are required for fusion of autophagosomes with lysosomes
Xie, R., Nguyen, S., McKeehan, W. L., & Liu, L. (2010) · BMC Cell Biology · doi:10.1186/1471-2121-11-89 · Cited by 203 · see citing works
Cytoskeletal elements are required for the formation and maturation of autophagic vacuoles
Aplin, A. E., Jasionowski, T., Tuttle, D. L., Lenk, S. E., & Dunn, W. A. (1992) · Journal of Cellular Physiology · doi:10.1002/jcp.1041520304 · Cited by 192 · see citing works
Guanosinetriphosphatase activity of tubulin associated with microtubule assembly.
David-Pfeuty, T., Erickson, H., & Pantaloni, D. (1977) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.74.12.5372 · Cited by 182 · see citing works
Involvement of microtubule motors in basolateral and apical transport in kidney cells
Lafont, F., Burkhardt, J. K., & Simons, K. (1994) · Nature · doi:10.1038/372801a0 · Cited by 181 · see citing works
Cortical control of microtubule stability and polarization
Gundersen, G. G., Gomes, E. R., & Wen, Y. (2003) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2003.11.010 · Cited by 179 · see citing works
Posttranslational Acetylation of α-Tubulin Constrains Protofilament Number in Native Microtubules
Cueva, J. G., Hsin, J., Huang, K. C., & Goodman, M. B. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.012 · Cited by 178 · see citing works
Webb, J. L., Ravikumar, B., & Rubinsztein, D. C. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.02.003 · Cited by 167 · see citing works
From signaling pathways to microtubule dynamics: the key players
Etienne‐Manneville, S. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.11.008 · Cited by 163 · see citing works
Differential microtubule requirements for transcytosis in MDCK cells.
Hunziker, W., Mâle, P., & Mellman, I. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07560.x · Cited by 160 · see citing works
Topalidou, I., Keller, C., Kalebic, N., Nguyen, K. C. Q., Somhegyi, H., Politi, K. A., Heppenstall, P. A., Hall, D. H., & Chalfie, M. (2012) · Current Biology · doi:10.1016/j.cub.2012.03.066 · Cited by 159 · see citing works
UNC-51/ATG1 kinase regulates axonal transport by mediating motor–cargo assemblyPreprint
Toda, H., Mochizuki, H., Flores, R., Josowitz, R., Krasieva, T. B., LaMorte, V. J., Suzuki, E., Gindhart, J. G., Furukubo-Tokunaga, K., & Tomoda, T. (2008) · Genes & Development · doi:10.1101/gad.1734608 · Cited by 141 · see citing works
Lin, S. X. H., Gundersen, G. G., & Maxfield, F. R. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.01-05-0224 · Cited by 133 · see citing works
Detyrosinated (Glu) microtubules are stabilized by an ATP-sensitive plus-end cap
Infante, A. S., Stein, M. S., Zhai, Y., Borisy, G. G., & Gundersen, G. G. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.22.3907 · Cited by 127 · see citing works
Cardoso, C. M. P., Groth‐Pedersen, L., Høyer-Hansen, M. H., Kirkegaard, T., Corcelle, E., Andersen, J., Jäättelä, M., & Nylandsted, J. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004424 · Cited by 125 · see citing works
Xie, R., Nguyen, S., McKeehan, K. A., Wang, F., McKeehan, W. L., & Leyuan, L. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.206532 · Cited by 123 · see citing works
Luminal Localization of α-tubulin K40 Acetylation by Cryo-EM Analysis of Fab-Labeled Microtubules
Soppina, V., Herbstman, J. F., Skiniotis, G., & Verhey, K. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048204 · Cited by 116 · see citing works
Veldhoen, R. A., Banman, S. L., Hemmerling, D., Odsen, R., Simmen, T., Simmonds, A. J., Underhill, D. A., & Goping, I. S. (2012) · Oncogene · doi:10.1038/onc.2012.92 · Cited by 114 · see citing works
Amenta, J. S., Sargus, M. J., & Baccino, F. M. (1977) · Biochemical Journal · doi:10.1042/bj1680223 · Cited by 109 · see citing works
Kouno, T., Mizuguchi, M., Tanida, I., Ueno, T., Kanematsu, T., Mori, Y., Shinoda, H., Hirata, M., Kominami, E., & Kawano, K. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m413565200 · Cited by 103 · see citing works
Tubulin Acetylation Alone Does Not Affect Kinesin-1 Velocity and Run Length In Vitro
Walter, W. J., Beránek, V., Fischermeier, E., & Diez, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042218 · Cited by 97 · see citing works
Push-me-pull-you: how microtubules organize the cell interior
Tolić, I. M. (2008) · European Biophysics Journal · doi:10.1007/s00249-008-0321-0 · Cited by 92 · see citing works
Elastic and damping forces generated by confined arrays of dynamic microtubules
Howard, J. (2006) · Physical Biology · doi:10.1088/1478-3975/3/1/006 · Cited by 90 · see citing works
Kamath, K., Okouneva, T., Larson, G., Panda, D., Wilson, L., & Jordan, M. A. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0113 · Cited by 88 · see citing works
Lorin, S., Borges, A., Santos, L. R. D., Souquère, S., Pierron, G., Ryan, K. M., Codogno, P., & Djavaheri‐Mergny, M. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-1270 · Cited by 82 · see citing works
Self-citationArduíno, D. M., Esteves, A. R., Cortes, L., Silva, D. F., Patel, B., Grazina, M. M., Swerdlow, R. H., Oliveira, C. R., & Cardoso, S. M. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds309 · Cited by 82 · see citing works
Guignot, J., Bernet‐Camard, M., Poüs, C., Plançon, L., Bouguénec, C. L., & Servin, A. L. (2001) · Infection and Immunity · doi:10.1128/iai.69.3.1856-1868.2001 · Cited by 78 · see citing works
Self-citationMizuno, M., & Singer, S. J. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.5.1321 · Cited by 65 · see citing works
Lysosome positioning coordinates mTORC1 activity and autophagy
Poüs, C., & Codogno, P. (2011) · Nature Cell Biology · doi:10.1038/ncb0411-342 · Cited by 63 · see citing works
Self-citationFunctional Specialization of Stable and Dynamic Microtubules in Protein Traffic in WIF-B Cells
Poüs, C., Chabin-Brion, K., Drechou, A., Barbot, L., Phung-Koskas, T., Settegrana, C., Bourguet‐Kondracki, M., Maurice, M., Cassio, D., Guyot, M., et al. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.1.153 · Cited by 51 · see citing works
Self-citationMicrotubule depolymerization inhibits transport of cathepsin D from the Golgi apparatus to lysosomes
Scheel, J., Matteoni, R., Ludwig, T., Hoflack, B., & Kreis, T. E. (1990) · Journal of Cell Science · doi:10.1242/jcs.96.4.711 · Cited by 46 · see citing works
Joseph, R. A., Shepard, B. D., Kannarkat, G. T., Rutledge, T. W., Tuma, D. J., & Tuma, P. L. (2007) · Hepatology · doi:10.1002/hep.22014 · Cited by 40 · see citing works
New Targets for Acetylation in Autophagy
Hamaï, A., & Codogno, P. (2012) · Science Signaling · doi:10.1126/scisignal.2003187 · Cited by 36 · see citing works
Self-citationReunanen, H., Marttinen, M. T., & Hirsimäki, P. (1988) · Experimental and Molecular Pathology · doi:10.1016/0014-4800(88)90048-2 · Cited by 32 · see citing works
What is the advantage of a transient precursor in autophagosome biogenesis?
Ktistakis, N. T., Andrews, S., & Long, J. (2011) · Autophagy · doi:10.4161/auto.7.1.13697 · Cited by 18 · see citing works
Flagged first, then by citations
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Sorted by citations
The cell biology of the retinal pigment epithelium
Lakkaraju, A., Umapathy, A., Tan, L. X., Daniele, L., Philp, N. J., Boesze-Battaglia, K., & Williams, D. S. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100846 · Cited by 422 · see citing works
“Post-translational modifications of tubulin such as acetylation and tyrosination/detyrosination can act either singly or in concert with other modifications to control motor recruitment in a cargo-specific manner (Hammond et al., 2008; Mackeh et al., 2013).”
BackgroundThe Cytoskeleton-Autophagy Connection
Kast, D. J., & Dominguez, R. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.061 · Cited by 267 · see citing works
Mitophagy in Cancer: A Tale of Adaptation
Vara‐Pérez, M., Felipe‐Abrio, B., & Agostinis, P. (2019) · Cells · doi:10.3390/cells8050493 · Cited by 256 · see citing works
“autophagy (and mitophagy by extension) is highly sensitive to microtubule-dynamics modulators since microtubules are essential for the autophagosome fusion with the lysosome [295,296].”
BackgroundAutophagy regulation and its role in cancer
Lorin, S., Hamaï, A., Mehrpour, M., & Codogno, P. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.06.007 · Cited by 247 · see citing works
Self-citationPharmacologic agents targeting autophagy
Vakifahmetoglu-Norberg, H., Xia, H., & Yuan, J. (2015) · Journal of Clinical Investigation · doi:10.1172/jci73937 · Cited by 240 · see citing works
“The destabilization of microtubules by either vinblastine (64), nocodazole, or cytochalasin B and D blocks the maturation of autophagosomes (65); conversely, taxol-mediated microtubule stabilization increases the fusion between autophagic vacuoles and lysosomes (66, 67).”
Targeting autophagy in disease: established and new strategies
Koçak, M., Erdi, S. E., Jorba, G., Maestro, I., Farrés, J., Kirkin, V., Martı́nez, A., & Pleß, O. (2021) · Autophagy · doi:10.1080/15548627.2021.1936359 · Cited by 229 · see citing works
“in water 84, yes 1 nM (EC50) n/a Experimental [202]”
BackgroundInfluentialZhang, W., Xu, C., Sun, J., Shen, H., Wang, J., & Yang, C. (2022) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2022.01.008 · Cited by 214 · see citing works
Dual roles for autophagy: Degradation and secretion of Alzheimer's disease Aβ peptide
Nilsson, P., & Saido, T. C. (2014) · BioEssays · doi:10.1002/bies.201400002 · Cited by 202 · see citing works
The cytoskeleton in cell-autonomous immunity: structural determinants of host defence
Mostowy, S., & Shenoy, A. R. (2015) · Nature reviews. Immunology · doi:10.1038/nri3877 · Cited by 175 · see citing works
Autophagy: A Druggable Process
Morel, É., Mehrpour, M., Botti, J., Dupont, N., Hamaï, A., Nascimbeni, A. C., & Codogno, P. (2017) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104936 · Cited by 168 · see citing works
Self-citationAutophagy is required for ectoplasmic specialization assembly in sertoli cells
Liu, C., Wang, H., Shang, Y., Liu, W., Song, Z., Zhao, H., Wang, L., Jia, P., Gao, F., Xu, Z., et al. (2016) · Autophagy · doi:10.1080/15548627.2016.1159377 · Cited by 154 · see citing works
“Many studies regarding the relationship between the cytoskeleton and autophagy focused on autophagosome formation and transportation.(45,46) Few studies have investigated how autophagy modulates cytoskeletal organization.”
BackgroundCoyne, A. N., Siddegowda, B. B., Estes, P. S., Johannesmeyer, J., Kovalik, T., Daniel, S. G., Pearson, A., Bowser, R. P., & Zarnescu, D. C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2526-14.2014 · Cited by 153 · see citing works
“Also, SGs can be cleared by autophagy (Buchan et al., 2013), and microtubules are used to transport autophagosomes to the microtubule organizing center where they fuse with lysosomes (Mackeh et al., 2013; Nixon, 2013).”
BackgroundChauhan, S., Ahmed, Z., Bradfute, S. B., Arko‐Mensah, J., Mandell, M. A., Choi, S. W., Kimura, T., Blanchet, F. P., Waller, A., Mudd, M. H., et al. (2015) · Nature Communications · doi:10.1038/ncomms9620 · Cited by 138 · see citing works
“Starvation-induced acetylation (K-40) of microtubules increases the recruitment of molecular motors kinesin-1 and JIP-1 (JNK-interacting protein 1) to microtubules leading to c-Jun N-terminal kinase-1 (JNK1) phosphorylation and activation 36,37 .”
InfluentialAutophagy in Age-Associated Neurodegeneration
Metaxakis, A., Ploumi, C., & Tavernarakis, N. (2018) · Cells · doi:10.3390/cells7050037 · Cited by 121 · see citing works
“Once sealed, the autophagosomes are associated with microtubules and transported to the perinuclear region, where the lysosomes have already accumulated, in response to stress [49].”
BackgroundNowosad, A., Creff, J., Jeannot, P., Culerrier, R. M., Codogno, P., Manenti, S., Nguyen, L., & Besson, A. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03759-9 · Cited by 125 · see citing works
Self-citationTubulin hyperacetylation is adaptive in cardiac proteotoxicity by promoting autophagy
McLendon, P. M., Ferguson, B. S., Osińska, H. E., Bhuiyan, M. S., James, J. F., McKinsey, T. A., & Robbins, J. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1415589111 · Cited by 121 · see citing works
Crosstalk between Apoptosis and Autophagy: Molecular Mechanisms and Therapeutic Strategies in Cancer
El‐Khattouti, A., Selimović, D., Haïkel, Y., & Hassan, M. (2013) · Journal of Cell Death · doi:10.4137/jcd.s11034 · Cited by 121 · see citing works
An mTORC1-to-CDK1 Switch Maintains Autophagy Suppression during Mitosis
Odle, R., Walker, S. A., Oxley, D., Kidger, A. M., Balmanno, K., Gilley, R., Okkenhaug, H., Florey, O., Ktistakis, N. T., & Cook, S. J. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.10.016 · Cited by 113 · see citing works
Autophagy in adhesion and migration
Kenific, C. M., Wittmann, T., & Debnath, J. (2016) · Journal of Cell Science · doi:10.1242/jcs.188490 · Cited by 108 · see citing works
“Similarly, the binding of LC3 proteins to microtubules might also contribute to the delivery of autophagy proteins to focal adhesions for disassembly (Mackeh et al., 2013).”
BackgroundMicrotubules: Evolving roles and critical cellular interactions
Logan, C. M., & Menko, A. S. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219867296 · Cited by 110 · see citing works
Cardiac microtubules in health and heart disease
Caporizzo, M. A., Chen, C. Y., & Prosser, B. L. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219868960 · Cited by 109 · see citing works
Toops, K. A., Tan, L. X., Jiang, Z., Radu, R. A., & Lakkaraju, A. (2015) · Molecular Biology of the Cell · doi:10.1091/mbc.e14-05-1028 · Cited by 105 · see citing works
Mackeh, R., Lorin, S., Ratier, A., Mejdoubi‐Charef, N., Baillet, A., Bruneel, A., Hamaï, A., Codogno, P., Poüs, C., & Perdiz, D. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.507400 · Cited by 99 · see citing works
Self-citationCentriolar Satellites Control GABARAP Ubiquitination and GABARAP-Mediated Autophagy
Joachim, J., Razi, M., Judith, D., Wirth, M., Calamita, E., Encheva, V., Dynlacht, B. D., Snijders, A. P., O’Reilly, N., Jefferies, H. B. J., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.021 · Cited by 101 · see citing works
Benischke, A., Vasanth, S., Miyai, T., Katikireddy, K. R., White, T. L., Chen, Y., Halilovic, A., Price, M. O., Price, F. W., Liton, P. B., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-06523-2 · Cited by 99 · see citing works
“LC3-II is a critical component of autophagosomes that is integrated in the membrane following conjugation of the cytosolic LC3-I with phosphotidylethanolamine 26 .”
WD40-repeat 47, a microtubule-associated protein, is essential for brain development and autophagy
Kannan, M., Bayam, E., Wagner, C., Rinaldi, B., Kretz, P. F., Tilly, P., Roos, M., McGillewie, L., Bär, S., Minocha, S., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713625114 · Cited by 99 · see citing works
“Microtubules seem an important player in the autophagy process in mammals (43); however, their specific implication in autophagy is unclear (44).”
BackgroundThe Role of HDAC6 in Autophagy and NLRP3 Inflammasome
Chang, P., Li, H., Hu, H., Li, Y., & Wang, T. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.763831 · Cited by 101 · see citing works
Emerging roles for the autophagy machinery in extracellular vesicle biogenesis and secretion
Leidal, A. M., & Debnath, J. (2021) · FASEB BioAdvances · doi:10.1096/fba.2020-00138 · Cited by 90 · see citing works
RASSF1A, puppeteer of cellular homeostasis, fights tumorigenesis, and metastasis—an updated review
Dubois, F., Bergot, E., Zalcman, G., & Levallet, G. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-2169-x · Cited by 93 · see citing works
Enhancing autophagy in Alzheimer's disease through drug repositioning
Eshraghi, M., Ahmadi, M., Afshar, S., Lorzadeh, S., Adlimoghaddam, A., Rezvani Jalal, N., West, R., Dastghaib, S., Igder, S., Torshizi, S. R. N., et al. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108171 · Cited by 89 · see citing works
“MTs importantly contribute to autophagy flux in neurons by facilitating the formation of autophagosomes, the transport of autophagosomes into the axons, the maturation of autophagosome, and the formation of autolysosomes (Köchl, Hu, Chan, & Tooze, 2006; Mackeh et al., 2013).”
BackgroundActin nucleation by WH2 domains at the autophagosome
Coutts, A. S., & Thangue, N. B. L. (2015) · Nature Communications · doi:10.1038/ncomms8888 · Cited by 83 · see citing works
“Macroautophagy (referred to as autophagy) is a catabolic process important for cell survival and numerous environmental cues can stimulate autophagy, which is maintained at basal levels to ensure cellular homeostasis 1, 2, 3 .”
Sanyal, C., Pietsch, N., Ramírez‐Ríos, S., Peris, L., Carrier, L., & Moutin, M. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.12.006 · Cited by 80 · see citing works
Targeting autophagy in breast cancer
Maycotte, P. (2014) · World Journal of Clinical Oncology · doi:10.5306/wjco.v5.i3.224 · Cited by 80 · see citing works
Host cell autophagy contributes to Plasmodium liver development
Thieleke‐Matos, C., Lopes‐da‐Silva, M., Cabrita‐Santos, L., Portal, M. D., Rodrigues, I. P., Zuzarte‐Luís, V., Ramalho, J. S., Futter, C. E., Mota, M. M., Barral, D. C., et al. (2015) · Cellular Microbiology · doi:10.1111/cmi.12524 · Cited by 78 · see citing works
“Possibly not a coincidence, it is in the perinuclear area that most autophagic vesicles fuse with late endosomes/ lysosomes (Kimura et al., 2008; Mackeh et al., 2013).”
BackgroundPellegrini, F. R., Martino, S. D., Fianco, G., Ventura, I., Valente, D., Fiore, M., Trisciuoglio, D., & Degrassi, F. (2023) · Autophagy · doi:10.1080/15548627.2023.2170962 · Cited by 75 · see citing works
Huenchuguala, S., Muñoz, P., Zavala, P., Villa, M., Cuevas, C., Ahumada, U., Graumann, R., Nore, B., Couve, E., Mannervik, B., et al. (2014) · Autophagy · doi:10.4161/auto.27720 · Cited by 69 · see citing works
Vac8 spatially confines autophagosome formation at the vacuole in S. cerevisiae
Hollenstein, D. M., Gómez‐Sánchez, R., Ciftci, A., Kriegenburg, F., Mari, M. C., Torggler, R., Licheva, M., Reggiori, F., & Kraft, C. (2019) · Journal of Cell Science · doi:10.1242/jcs.235002 · Cited by 67 · see citing works
“This transport is mediated by the microtubular network (Mackeh et al., 2013).”
BackgroundCohignac, V., Landry, M., Ridoux, A., Pinault, M., Annangi, B., Gerdil, A., Herlin‐Boime, N., Mayne–L'Hermite, M., Haruta, M., Codogno, P., et al. (2018) · Autophagy · doi:10.1080/15548627.2018.1474993 · Cited by 66 · see citing works
“Because, microtubules are essential to the transport of autophagosomes to lysosomes, we next examined the cytoskeleton structure by TUBA/ α -tubulin immunostaining [20].”
Self-citationLiu, J., Kang, Y., Yin, S., Chen, A., Wu, J., Liang, H., & Shao, L. (2019) · Small · doi:10.1002/smll.201901073 · Cited by 65 · see citing works
Selective autophagy: Lysophagy
Hasegawa, J., Maejima, I., Iwamoto, R., & Yoshimori, T. (2014) · Methods · doi:10.1016/j.ymeth.2014.12.014 · Cited by 64 · see citing works
Cheng, X., Wang, Y., Gong, Y., Li, F., Guo, Y., Hu, S., Liu, J., & Pan, L. (2016) · Autophagy · doi:10.1080/15548627.2016.1185590 · Cited by 62 · see citing works
Autophagy and Mitochondrial Dysfunction in Tenon Fibroblasts from Exfoliation Glaucoma Patients
Want, A., Gillespie, S. R., Wang, Z., Gordon, R., Iomini, C., Ritch, R. H., Wolosin, J. M., & Bernstein, A. M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157404 · Cited by 61 · see citing works
“The free cytosolic isoform (LC3-I) is converted by lipidation into an isoform (LC3-II), which binds to the developing autophagasomes and helps in the tethering of the maturing autophagosome to microtubules [36].”
BackgroundLu, G. X., Yi, J., Gubaš, A., Wang, Y., Wu, Y., Ren, Y., Wu, M., Shi, Y. P., Ouyang, C., Tan, H. W. S., et al. (2019) · Autophagy · doi:10.1080/15548627.2019.1596484 · Cited by 60 · see citing works
“It has been reported that microtubules play a critical role in stress (such as starvation)-induced autophagosome formation and autophagosome-lysosome fusion [41], while disruption of microtubules does not affect basal autophagy [42–44].”
BackgroundTubulin Post-Translational Modifications: The Elusive Roles of Acetylation
Carmona, B., Marinho, H. S., Matos, C. L., Nolasco, S., & Soares, H. (2023) · Biology · doi:10.3390/biology12040561 · Cited by 58 · see citing works
Wang, Y., Zheng, X., Yu, B., Han, S., Guo, J., Tang, H., Yu, A. Y. L., Deng, H., Hong, Y., & Liu, Y. (2015) · Autophagy · doi:10.1080/15548627.2015.1113365 · Cited by 58 · see citing works
“Whereas an agreement has been reached on the role of microtubules in autophagosome movement,(48-51) the involvement of microtubules in autolysosome formation has been under debate.(6,33) Likewise, microtubules have initially been believed to have little or no effects on autophagic sequestration in early studies,(52,53…”
BackgroundInfluentialThe role of APC-mediated actin assembly in microtubule capture and focal adhesion turnover
Juanes, M. A., Isnardon, D., Badache, A., Brasselet, S., Mavrakis, M., & Goode, B. L. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201904165 · Cited by 53 · see citing works
“4 FAs (Mackeh et al., 2013; Kenific et al., 2016), where LC3 interacts with phosphorylated Src and Paxillin, leading to autophagic turnover of FAs and Paxillin degradation (Sharifi et al.”
Zheng, Z., Zhou, Y., Ye, L., Lu, Q., Zhang, K., Zhang, J., Xie, L., Wu, Y., Xu, K., Zhang, H., et al. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113138 · Cited by 53 · see citing works
The type III intermediate filament vimentin regulates organelle distribution and modulates autophagy
Biskou, O., Casanova, V., Hooper, K. M., Kemp, S. E., Wright, G. P., Satsangi, J. J., Barlow, P. G., & Stevens, C. (2019) · PLoS ONE · doi:10.1371/journal.pone.0209665 · Cited by 52 · see citing works
The Microtubule-associated Protein EB1 Links AIM2 Inflammasomes with Autophagy-dependent Secretion
Wang, L., Huang, H., Huang, M.-P., Liou, W., Chang, Y., Wu, C., Ojcius, D. M., & Chang, Y. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.559153 · Cited by 52 · see citing works
Arun, R. P., Sivanesan, D., Vidyasekar, P., & Verma, R. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-06416-4 · Cited by 52 · see citing works
Perdiz, D., Lorin, S., Leroy-Gori, I., & Poüs, C. (2017) · Cellular Signalling · doi:10.1016/j.cellsig.2017.07.020 · Cited by 51 · see citing works
Self-citationRole of Autophagy in Proteostasis: Friend and Foe in Cardiac Diseases
Li, J., Zhang, D., Wiersma, M., & Brundel, B. J. J. M. (2018) · Cells · doi:10.3390/cells7120279 · Cited by 54 · see citing works
“In autolysosomes, lysosomal hydrolases degrade the cargo into recyclable ATP, amino acids, and fatty acids (Figure 1a) [15,16].”
BackgroundLC3B phosphorylation regulates FYCO1 binding and directional transport of autophagosomes
Nieto-Torres, J. L., Shanahan, S.-L., Chassefeyre, R., Chaiamarit, T., Zaretski, S., Landeras-Bueno, S., Verhelle, A., Encalada, S. E., & Hansen, M. (2021) · Current Biology · doi:10.1016/j.cub.2021.05.052 · Cited by 52 · see citing works
Protein complexes and neighborhoods driving autophagy
Sankar, D. S., & Dengjel, J. (2020) · Autophagy · doi:10.1080/15548627.2020.1847461 · Cited by 51 · see citing works
“These help in autophagosome formation, motility and fusion with lysosomes [43,45,46].”
BackgroundShear stress induces noncanonical autophagy in intestinal epithelial monolayers
Kim, S. W., Ehrman, J. D., Ahn, M., Kondo, J., Lopez, A. A., Oh, Y. S., Kim, X. H., Crawley, S. W., Goldenring, J. R., Tyska, M. J., et al. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-01-0021 · Cited by 49 · see citing works
“Microtubules are known to transport various pre- and postautophagy vesicles (Mackeh et al., 2013), as well as regulate microtubule-associated protein 1A/1B-light chain 3 (LC3), a central component of the autophagy machinery.”
BackgroundConnecting autophagy: AMBRA1 and its network of regulation
Cianfanelli, V., Nazio, F., & Cecconi, F. (2015) · Molecular & Cellular Oncology · doi:10.4161/23723548.2014.970059 · Cited by 43 · see citing works
“It is evident that interactions of BECLIN 1 with the cytoskeleton are highly relevant to proper autophagy regulation but several open questions remain, for example: (i) Are these cytoskeletonmediated regulation mechanisms coordinated and/or correlated? (ii) Do they capture distinct pools of BECLIN 1? (iii) Do their up…”
BackgroundAlzheimer's disease genes and autophagy
Yoon, S., & Kim, D. (2016) · Brain Research · doi:10.1016/j.brainres.2016.03.018 · Cited by 47 · see citing works
Regulation of actin nucleation and autophagosome formation
Coutts, A. S., & Thangue, N. B. L. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2224-z · Cited by 47 · see citing works
“Both systems have been implicated in autophagic processes under a variety of conditions (for a review on the role of microtubules in autophagy see [131]).”
BackgroundBrindisi, M., Ulivieri, C., Alfano, G., Gemma, S., Balaguer, F. D. A., Khan, T., Grillo, A., Chemi, G., Menchon, G., Prota, A. E., et al. (2018) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2018.11.004 · Cited by 47 · see citing works
Bonet‐Ponce, L., Sáez-Atiénzar, S., da Casa, C., Sancho-Pellúz, J., Barcia, J. M., Martínez‐Gil, N., Nava, E., Jordán, J., Romero, F. J., & Galindo, M. F. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9509-3 · Cited by 45 · see citing works
Bejarano, E., Murray, J. W., Wang, X., Pampliega, O., Yin, D., Patel, B., Yuste, A., Wolkoff, A. W., & Cuervo, A. M. (2018) · Aging Cell · doi:10.1111/acel.12777 · Cited by 45 · see citing works
“Microtubule-based motility is required for AV maturation as it mediates relocation of autophagosomes to the proximity of lysosomes (Mackeh et al., 2013).”
BackgroundInfluentialLAMP2 Cardiomyopathy: Consequences of Impaired Autophagy in the Heart
Alcalai, R., Arad, M., Wakimoto, H., Yadin, D., Gorham, J., Wang, L., Burns, E., Maron, B. J., Roberts, W. C., Konno, T., et al. (2021) · Journal of the American Heart Association · doi:10.1161/jaha.120.018829 · Cited by 42 · see citing works
The role of Runx2 in facilitating autophagy in metastatic breast cancer cells
Tandon, M., Othman, A. H., Ashok, V., Stein, G. S., & Pratap, J. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25916 · Cited by 41 · see citing works
“…post-translational modifications of microtubules, including acetylation of α-tubulin subunits, upon nutrient deprivation and autophagic response (Geeraert et al., 2010; Jahreiss, Menzies, & Rubinsztein, 2008; Kochl, Hu, Chan, & Tooze, 2006; Mackeh et al., 2013; Xie, Nguyen, McKeehan, & Liu, 2010).”
BackgroundFSIP1 regulates autophagy in breast cancer
Liu, C., Sun, L., Yang, J., Liu, T., Yang, Y., Kim, S., Ou, X., Wang, Y., Sun, L., Zaidi, M., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809681115 · Cited by 41 · see citing works
Wang, L.-L., Jin, X.-H., Cai, M.-Y., Li, H.-G., Chen, J.-W., Wang, F., Wang, C.-Y., Hu, W.-W., Liu, F., & Xie, D. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.11.003 · Cited by 40 · see citing works
A current view of molecular dissection in autophagy machinery
Al‐Bari, M. A. A. (2020) · Journal of Physiology and Biochemistry · doi:10.1007/s13105-020-00746-0 · Cited by 38 · see citing works
Li, S., Liu, C., Gu, L., Wang, L., Shang, Y., Liu, Q., Wan, J., Shi, J. Y., Wang, F., Xu, Z., et al. (2016) · Open Biology · doi:10.1098/rsob.160177 · Cited by 36 · see citing works
Phenotypic Drug Screening for Dysferlinopathy Using Patient-Derived Induced Pluripotent Stem Cells
Kokubu, Y., Nagino, T., Sasa, K., Oikawa, T., Miyake, K., Kume, A., Fukuda, M., Fuse, H., Tozawa, R., & Sakurai, H. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.18-0280 · Cited by 34 · see citing works
Molecular mechanisms of mammalian autophagy
Trelford, C. B., & Guglielmo, G. M. D. (2021) · Biochemical Journal · doi:10.1042/bcj20210314 · Cited by 34 · see citing works
Noh, M. R., Woo, C.-H., Park, M.-J., In Kim, J., & Park, K. M. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.02.001 · Cited by 33 · see citing works
Ouyang, C., Mu, J., Lu, Q., Li, J., Zhu, H., Wang, Q., Zou, M., & Xie, Z. (2019) · Autophagy · doi:10.1080/15548627.2019.1707488 · Cited by 33 · see citing works
“First, microtubules interact with ATG proteins, including LC3, ULK1, BECN1, ATG5, and ATG12, supporting the assembly of preautophagosomal structure [51].”
BackgroundKundu, S., Kim, T. H., Yoon, J. H., Shin, H.-S., Lee, J., Jung, J. H., & Kim, H. S. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2659 · Cited by 32 · see citing works
The Tubulin Code and Tubulin-Modifying Enzymes in Autophagy and Cancer
Trisciuoglio, D., & Degrassi, F. (2021) · Cancers · doi:10.3390/cancers14010006 · Cited by 30 · see citing works
“MT dynamics and MT-based motors have been implicated for a long time in both autophagosome formation and trafficking by studies using drugs interfering with MT assembly and dynamics [109].”
BackgroundThe role of autophagic cell death in cardiac disease
Nah, J., Zablocki, D., & Sadoshima, J. (2022) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2022.08.362 · Cited by 30 · see citing works
Liu, S., Su, Y., Lu, Z., Zou, X., Xu, L., Teng, Y., Wang, Z., & Wang, T. (2023) · Journal of Virology · doi:10.1128/jvi.00302-23 · Cited by 29 · see citing works
“Consisting of MTs, actin filaments (AFs), and intermediate filaments (IFs), the cytoskeleton provides shape and structural integrity to eukaryotic cells (51, 52).”
BackgroundPoillet-Perez, L., Jacquet, M., Hervouet, É., Gauthier, T., Fraîchard, A., Borg, C., Pallandre, J., Gonzalez, B. J., Ramdani, Y., Boyer‐Guittaut, M., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.19639 · Cited by 29 · see citing works
“Moreover, GABARAPL1 is known to interact with microtubules and favor their polymerization [14], and microtubules have been shown to regulate autophagosome/lysosome fusion by relocalizing these organelles to the juxtanuclear region during autophagy [67, 68].”
BackgroundAlcohol-induced microtubule acetylation leads to the accumulation of large, immobile lipid droplets
Groebner, J. L., Bravo, M. G., Rothberg, M. L., Adhikari, R., Tuma, D. J., & Tuma, P. L. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00026.2019 · Cited by 29 · see citing works
“crotubules impair autophagosome formation (18, 24).”
Broad-spectrum antitumor properties of Withaferin A: a proteomic perspective
Dom, M. P., Berghe, W. V., & Ostade, X. V. (2019) · RSC Medicinal Chemistry · doi:10.1039/c9md00296k · Cited by 29 · see citing works
Liu, G., Fu, T., Han, Y., Hu, S., Zhang, X., Zheng, M., Hao, P., Pan, L., & Kang, J. (2020) · Analytical Chemistry · doi:10.1021/acs.analchem.9b05355 · Cited by 29 · see citing works
Takano, N., Hiramoto, M., Yamada, Y., Kokuba, H., Tokuhisa, M., Hino, H., & Miyazawa, K. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02210-4 · Cited by 29 · see citing works
“Microtubule-based such retrograde transport is used for endosomal trafficking and is carried out by dynein, which is involved in autophagy regulation [37, 38].”
BackgroundKisspeptin inhibits cancer growth and metastasis via activation of EIF2AK2
Kim, T., & Cho, S. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7578 · Cited by 27 · see citing works
“Vesicle trafficking has been associated with cytoskeletal dynamics (31).”
Chambraud, B., Daguinot, C., Guillemeau, K., Genet, M., Dounane, O., Méduri, G., Poüs, C., Baulieu, E. E., & Giustiniani, J. (2021) · Autophagy · doi:10.1080/15548627.2021.1875611 · Cited by 27 · see citing works
“the formation of autolysosomes, requires the regulated trafficking of these vesicles which depends of the microtubule network [11].”
BackgroundSelf-citationSakurai, S., Tomita, T., Shimizu, T., & Ohto, U. (2017) · Acta Crystallographica Section F Structural Biology Communications · doi:10.1107/s2053230x17001911 · Cited by 25 · see citing works
Lidocaine induces protective autophagy in rat C6 glioma cell line
Izdebska, M., Hałas‐Wiśniewska, M., Zielińska, W., Klimaszewska‐Wiśniewska, A., Grzanka, D., & Gagat, M. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4668 · Cited by 26 · see citing works
“Destabilization of this cytoskeleton element delays the arrival of autophagosomes near lysosomes and thus, inhibits their fusion (69,82,83).”
BackgroundCanonical and Non-canonical TGFβ Signaling Activate Autophagy in an ULK1-Dependent Manner
Trelford, C. B., & Guglielmo, G. M. D. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.712124 · Cited by 25 · see citing works
“The phosphorylation status and activation of ATG1—Unc 51-like kinase 1 (ULK1) in mammals—is determined by a balance between mechanistic target of rapamycin (mTOR) and 5′ adenosine monophosphate activated protein kinase (AMPK) activity (Hosokawa et al., 2009; Makhov et al., 2014).”
BackgroundEfe, E. Y., Mazumder, A., Lee, J., Gaigneaux, A., Radogna, F., Nasim, M. J., Christov, C., Jacob, C., Kim, K., Dicato, M. A., et al. (2017) · Cancer Letters · doi:10.1016/j.canlet.2017.09.011 · Cited by 25 · see citing works
Olenieva, V. D., Lytvyn, D. I., Yemets, A. I., Catherine Bergounioux, A., & Blume, Y. B. (2017) · Cell Biology International · doi:10.1002/cbin.10843 · Cited by 24 · see citing works
Control of GABARAP‐mediated autophagy by the Golgi complex, centrosome and centriolar satellites
Joachim, J., & Tooze, S. A. (2017) · Biology of the Cell · doi:10.1111/boc.201700046 · Cited by 24 · see citing works
“Furthermore, microtubules and the (non-ciliated) centrosome also regulate autophagy [Mackeh et al., 2013; Joachim et al., 2015] and we have now discovered a role for centriolar satellites in the regulation of autophagy [Joachim et al., 2017].”
BackgroundRamesh, G., Das, S., & Rao, B. S. S. (2020) · Journal of Pharmacy and Pharmacology · doi:10.1111/jphp.13354 · Cited by 23 · see citing works
“A healthy microtubule network is necessary for the completion of autophagic process.([56]) Earlier, Ber has been shown to disrupt microtubule Figure 8 Functional alterations in mitochondria in HepG2 cells treated with X-rays in combination with Ber.”
BackgroundGlon, D., Vilmen, G., Perdiz, D., Hernández, E., Beauclair, G., Quignon, F., Berlioz‐Torrent, C., Maréchal, V., Poüs, C., Lussignol, M., et al. (2022) · PLoS Pathogens · doi:10.1371/journal.ppat.1010371 · Cited by 23 · see citing works
“However, MTs 399 are not involved in autophagosome formation in basal autophagy (Mackeh et al., 2013).”
Self-citationKawasaki, F., Koonce, N. L., Guo, L., Fatima, S., Qiu, C., Moon, M. T., Zheng, Y., & Ordway, R. W. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.026385 · Cited by 23 · see citing works
“Previous studies have shown that clearance of protein aggregates can be localized to the perinuclear compartment of the cell through microtubule-based transport (Mackeh et al., 2013).”
Human GABARAP can restore autophagosome biogenesis in aC. elegans lgg-1mutant
Jenzer, C., Manil-Ségalen, M., Lefebvre, C., Largeau, C., Glatigny, A., & Legouis, R. (2014) · Autophagy · doi:10.4161/auto.29745 · Cited by 22 · see citing works
Selective autophagy receptor Joka2 co-localizes with cytoskeleton in plant cells
Zientara‐Rytter, K., & Sirko, A. (2014) · Plant Signaling & Behavior · doi:10.4161/psb.28523 · Cited by 22 · see citing works
“Despite the increasing interest in autophagy, the recognition of proteins connecting it with other cellular components, such as the cytoskeleton, is limited and mostly refers to yeasts and mammals.(16,17) In yeasts, the MTs are not essential for bulk autophagy despite the fact that in vitro the Atg8 protein binds to t…”
BackgroundMiyahara, K., Kazama, H., Kokuba, H., KOMATSU, S., Hirota, A., Takemura, J., Hirasawa, K., Moriya, S., Abe, A., Hiramoto, M., et al. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3673 · Cited by 22 · see citing works
“Microtubules support the assembly of pre-autophagosomal structures and mediate trafficking of autophagosomes toward lysosomes (38).”
BackgroundHost cell autophagy promotes BK virus infection
Bouley, S. J., Maginnis, M. S., Derdowski, A., Gee, G. V., O’Hara, B. A., Nelson, C. D. S., Bara, A. M., Atwood, W. J., & Dugan, A. S. (2014) · Virology · doi:10.1016/j.virol.2014.03.009 · Cited by 20 · see citing works
“Other studies have shown that acidification is necessary for viral infection (Mateo et al., 2013; Mackeh et al., 2013) Moreover, BKPyV infection requires an acidification event to occur within 2 h following infection (Eash et al., 2004; Jiang et al., 2009) .”
Proprotein convertase 7 (PCSK7) reduces apoA‐V levels
Ashraf, Y., Duval, S., Sachan, V., Essalmani, R., Susan‐Resiga, D., Roubtsova, A., Hamelin, J., Gerhardy, S., Kirchhofer, D., Tagliabracci, V. S., et al. (2020) · FEBS Journal · doi:10.1111/febs.15212 · Cited by 20 · see citing works
Li, Z., Liu, X., Ma, J., Zhang, T., Gao, X., & Liu, L. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4517 · Cited by 20 · see citing works
“Previous studies also reported that an intact microtubule cytoskeleton was required for autophagy and that microtubule disruption interfered with autophagy by impairing autolysosome formation (46,54).”
BackgroundXu, L., Wu, X., Zhao, S., Hu, H., Wang, S., Zhang, Y., Chen, J., Zhang, X., Zhao, Y., Ma, R., et al. (2024) · Advanced Materials · doi:10.1002/adma.202313869 · Cited by 21 · see citing works
Favero, G. D., Woelflingseder, L., Janker, L., Neuditschko, B., Seriani, S., Gallina, P., Sbaizero, O., Gerner, C., & Marko, D. (2018) · Scientific Reports · doi:10.1038/s41598-018-29728-5 · Cited by 20 · see citing works
Rontogianni, S., Iskit, S., van Doorn, S., Peeper, D. S., & Altelaar, M. A. F. (2019) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra119.001800 · Cited by 19 · see citing works
“It has been shown that autophagosome movement in the cytoplasm is dependent on microtubules (46).”
Background
- Authors
- Mackeh, R., Perdiz, D., Lorin, S., Codogno, P., & Poüs, C.
- Affiliations
- Université Paris-Sud (FR)
- Inserm (FR)
- Corresponding author
- Codogno, Patrice
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2013-03-01
- Volume
- 126
- Issue
- 5
- Pages
- 1071-1080
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W2098921256
- Semantic Scholar
- bd987f4dde12826f66e2891ff2e65de145d37370
- Cited by
- 212
- References
- 110
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 13 · 2023: 13 · 2022: 20 · 2021: 20 · 2020: 20 · 2019: 21 · 2018: 17 · 2017: 20 · 2016: 16 · 2015: 10 · 2014: 18 · 2013: 3
- FWCI
- 11.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- autophagy, microtubules, autophagosome formation, autophagosome transport, autolysosomes, microtubule dynamics, tubulin post-translational modifications, microtubule motor proteins, nutrient deprivation, organelle degradation
- MeSH terms
- Animals, Autophagy, Humans, Lysosomes, Microtubules, Models, Biological, Phagocytosis, Protein Processing, Post-Translational, Tubulin
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