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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 (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
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The cell biology of the retinal pigment epithelium
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“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).”
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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 64
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“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.”
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“Microtubule-based motility is required for AV maturation as it mediates relocation of autophagosomes to the proximity of lysosomes (Mackeh et al., 2013).”
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“…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).”
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“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 33
The Tubulin Code and Tubulin-Modifying Enzymes in Autophagy and Cancer
Trisciuoglio, D., & Degrassi, F. (2021) · Cancers · doi:10.3390/cancers14010006 · Cited by 30
“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
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“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 32
“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
“crotubules impair autophagosome formation (18, 24).”
Broad-spectrum antitumor properties of Withaferin A: a proteomic perspective
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“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
“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
“the formation of autolysosomes, requires the regulated trafficking of these vesicles which depends of the microtubule network [11].”
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Lidocaine induces protective autophagy in rat C6 glioma cell line
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“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
“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).”
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Control of GABARAP‐mediated autophagy by the Golgi complex, centrosome and centriolar satellites
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“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].”
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“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.”
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“However, MTs 399 are not involved in autophagosome formation in basal autophagy (Mackeh et al., 2013).”
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“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
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Selective autophagy receptor Joka2 co-localizes with cytoskeleton in plant cells
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“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…”
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“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
“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
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“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).”
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“It has been shown that autophagosome movement in the cytoplasm is dependent on microtubules (46).”
Background
Metadata
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › 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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