Biogenesis and Cargo Selectivity of Autophagosomes

Weidberg, Hilla; Shvets, Elena; Elazar, Zvulun

doi:10.1146/annurev-biochem-052709-094552

Cited by 466Autophagy in Disease and TherapyUbiquitin and proteasome pathwaysCellular transport and secretion

Biogenesis and Cargo Selectivity of Autophagosomes

Weidberg, Hilla, Shvets, Elena, Elazar, Zvulun·2011·Annual Review of Biochemistry

DOI 10.1146/annurev-biochem-052709-094552

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Abstract

Autophagy is a major catabolic pathway in eukaryotes, which is required for the lysosomal/vacuolar degradation of cytoplasmic proteins and organelles. Interest in the autophagy pathway has recently gained momentum largely owing to identification of multiple autophagy-related genes and recognition of its involvement in various physiological conditions. Here we review current knowledge of the molecular mechanisms regulating autophagy in mammals and yeast, specifically the biogenesis of autophagosomes and the selectivity of their cargo recruitment. We discuss the different steps of autophagy, from the signal transduction events that regulate it to the completion of this pathway by fusion with the lysosome/vacuole. We also review research on the origin of the autophagic membrane, the molecular mechanism of autophagosome formation, and the roles of two ubiquitin-like protein families and other structural elements that are essential for this process. Finally, we discuss the various modes of autophagy and highlight their functional relevance for selective degradation of specific cargos.

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Selective autophagy uses receptor proteins such as SQSTM1/p62, NBR1, and AMBRA1 that contain an LIR and separate motifs for binding polyubiquitinated proteins, targeting ubiquitinated proteins to phagophores for degradation.
“Although autophagic cargo can be trapped passively within the autophagosome in nonselective autophagy, direct substrate recruitment to phagophores in selective autophagy is mediated by a series of receptor proteins (e.g., SQSTM1/p62 [sequestosome 1], NBR1, AMBRA1) that contain both an LC3-interacting region (LIR) and separate motifs for binding polyubiquitinated proteins [41].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [41]
Expansion of the phagophore membrane is guided by the ATG12-ATG5-ATG16L1 complex, which catalyzes insertion of LC3 into the phagophore membrane.
“Expansion then occurs through maturation of the extending phagophore membrane guided by the ATG12–ATG5-ATG16L1 complex, catalyzing insertion of MAP1LC3/LC3 (microtubule associated protein 1 light chain 3) into the phagophore membrane [40,41].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [41]
LC3-I undergoes proteolytic processing by ATG4 and conjugation to phosphatidylethanolamine through ATG7 and ATG3 to form lipidated LC3-II, which is incorporated into the phagophore membrane.
“Before membrane insertion, the unbound and immature LC3 precursor protein (LC3-I) undergoes proteolytic processing by ATG4, and conjugation to phosphatidylethanolamine through ATG7 and ATG3. The resulting mature, lipidated isoform (LC3-II) is incorporated into the phagophore membrane [41].”
From Autophagy and ALS: mechanistic insights and therapeutic implications (2022) · cites this paper as [41]

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Atg17 recruits Atg9 to organize the pre‐autophagosomal structure
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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
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
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An Overview of Autophagy: Morphology, Mechanism, and Regulation
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Self-consumption: the interplay of autophagy and apoptosis
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Autophagy modulation as a potential therapeutic target for diverse diseases
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Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling.
Lee, J., Giordano, S., & Zhang, J. (2012) · Biochemical Journal · doi:10.1042/bj20111451 · Cited by 1,438 · see citing works
Phosphorylation of p62 Activates the Keap1-Nrf2 Pathway during Selective Autophagy
Ichimura, Y., Waguri, S., Sou, Y., Kageyama, S., Hasegawa, J., Ishimura, R., Saito, T., Yang, Y., Kouno, T., Fukutomi, T., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.08.003 · Cited by 1,205 · see citing works
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Autophagy in malignant transformation and cancer progression
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The eIF2α/ATF4 pathway is essential for stress-induced autophagy gene expression
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Regulation of endoplasmic reticulum turnover by selective autophagy
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The LIR motif – crucial for selective autophagy
Birgisdottir, Å. B., Lamark, T., & Johansen, T. (2013) · Journal of Cell Science · doi:10.1242/jcs.126128 · Cited by 871 · see citing works
ER stress: Autophagy induction, inhibition and selection
Rashid, H.-O., Yadav, R. K., Kim, H., & Chae, H. (2015) · Autophagy · doi:10.1080/15548627.2015.1091141 · Cited by 796 · see citing works
Ubiquitination and selective autophagy
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Canonical and non-canonical autophagy: variations on a common theme of self-eating?
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“Arrival of Atg8 proteins at the autophagic membrane depends on the hierarchical recruitment of numerous auto phagic factors, including phosphatidylinositol-3phosphate-binding proteins [18].”
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Interplay between ROS and autophagy in cancer cells, from tumor initiation to cancer therapy
Poillet-Perez, L., Despouy, G., Delage-Mourroux, R., & Boyer-Guittaut, M. (2015) · Redox Biology · doi:10.1016/j.redox.2014.12.003 · Cited by 503 · see citing works
Aggrephagy: Selective Disposal of Protein Aggregates by Macroautophagy
Lamark, T., & Johansen, T. (2012) · International Journal of Cell Biology · doi:10.1155/2012/736905 · Cited by 490 · see citing works
Mechanisms of Autophagosome Biogenesis
Rubinsztein, D. C., Shpilka, T., & Elazar, Z. (2012) · Current Biology · doi:10.1016/j.cub.2011.11.034 · Cited by 489 · see citing works
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Altered lysosomal proteins in neural-derived plasma exosomes in preclinical Alzheimer disease
Goetzl, E. J., Boxer, A. L., Schwartz, J. B., Abner, E. L., Petersen, R. C., Miller, B. L., & Kapogiannis, D. (2015) · Neurology · doi:10.1212/wnl.0000000000001702 · Cited by 466 · see citing works
The ER–Golgi intermediate compartment is a key membrane source for the LC3 lipidation step of autophagosome biogenesis
Ge, L., Melville, D., Zhang, M., & Schekman, R. W. (2013) · eLife · doi:10.7554/elife.00947 · Cited by 440 · see citing works
Regulation of autophagy by the Rab GTPase network
Ao, X., Zou, L., & Wu, Y. (2014) · Cell Death & Differentiation · doi:10.1038/cdd.2013.187 · Cited by 411 · see citing works
Regulation and Function of Autophagy during Cell Survival and Cell DeathPreprint
Das, G., Shravage, B. V., & Baehrecke, E. H. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008813 · Cited by 413 · see citing works
ER exit sites are physical and functional core autophagosome biogenesis components
Graef, M., Friedman, J. R., Graham, C. I., Babu, M., & Nunnari, J. M. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-07-0381 · Cited by 380 · see citing works
Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43
Wang, I.-F., Guo, B.-S., Liu, Y.-C., Wu, C.-C., Yang, C.-H., Tsai, K.-J., & Shen, C.-K. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206362109 · Cited by 377 · see citing works
Autophagosome Biogenesis in Primary Neurons Follows an Ordered and Spatially Regulated Pathway
Maday, S., & Holzbaur, E. L. F. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.06.001 · Cited by 372 · see citing works
Beclin 1 and autophagy are required for the tumorigenicity of breast cancer stem-like/progenitor cells
Gong, C., Bauvy, C., Tonelli, G., Yue, W., Deloménie, C., Nicolas, V., Zhu, Y., Domergue, V., Marin‐Esteban, V., Tharinger, H., et al. (2012) · Oncogene · doi:10.1038/onc.2012.252 · Cited by 369 · see citing works
Autophagy, cancer stem cells and drug resistance
Smith, A. G., & Macleod, K. F. (2018) · The Journal of Pathology · doi:10.1002/path.5222 · Cited by 364 · see citing works
Expression of the autophagy substrate SQSTM1/p62 is restored during prolonged starvation depending on transcriptional upregulation and autophagy-derived amino acids
Sahani, M. H., Itakura, E., & Mizushima, N. (2014) · Autophagy · doi:10.4161/auto.27344 · Cited by 363 · see citing works
Polyglutamine tracts regulate beclin 1-dependent autophagy
Ashkenazi, A., Bento, C. F., Ricketts, T., Vicinanza, M., Siddiqi, F., Pavel, M., Squitieri, F., Hardenberg, M. C., Imarisio, S., Menzies, F. M., et al. (2017) · Nature · doi:10.1038/nature22078 · Cited by 357 · see citing works
LC3C, Bound Selectively by a Noncanonical LIR Motif in NDP52, Is Required for Antibacterial Autophagy
von Muhlinen, N., Akutsu, M., Ravenhill, B. J., Foeglein, Á., Bloor, S., Rutherford, T. J., Freund, S. M. V., Komander, D., & Randow, F. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.08.024 · Cited by 332 · see citing works
Autophagosome-Lysosome Fusion
Lőrincz, P., & Juhász, G. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.10.028 · Cited by 328 · see citing works
Autophagy and the Immune System
Kuballa, P., Nolte, W. M., Castoreno, A. B., & Xavier, R. J. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-074948 · Cited by 326 · see citing works
Cellular metabolic and autophagic pathways: Traffic control by redox signaling
Dodson, M. B., Darley-Usmar, V. M., & Zhang, J. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.05.014 · Cited by 325 · see citing works
Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy
Nakatogawa, H. (2013) · Essays in Biochemistry · doi:10.1042/bse0550039 · Cited by 315 · see citing works
Autophagy receptors link myosin VI to autophagosomes to mediate Tom1-dependent autophagosome maturation and fusion with the lysosome
Tumbarello, D. A., Waxse, B. J., Arden, S. D., Bright, N. A., Kendrick-Jones, J., & Buss, F. (2012) · Nature Cell Biology · doi:10.1038/ncb2589 · Cited by 301 · see citing works
p62/SQSTM1/A170: Physiology and pathology
Komatsu, M., Kageyama, S., & Ichimura, Y. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.07.004 · Cited by 301 · see citing works
Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy
Yuan, H., Russell, R. C., & Guan, K. (2013) · Autophagy · doi:10.4161/auto.26058 · Cited by 292 · see citing works
The Role of Lipids in the Control of Autophagy
Dall’Armi, C., Devereaux, K. A., & Paolo, G. D. (2013) · Current Biology · doi:10.1016/j.cub.2012.10.041 · Cited by 286 · see citing works
ATG8 Family Proteins Act as Scaffolds for Assembly of the ULK Complex
Alemu, E. A., Lamark, T., Torgersen, K. M., Birgisdottir, Å. B., Larsen, K. B., Jain, A., Olsvik, H. L., Øvervatn, A., Kirkin, V., & Johansen, T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.378109 · Cited by 288 · see citing works
Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity
Shen, S., Niso-Santano, M., Adjemian, S., Takehara, T., Malik, S. A., Minoux, H., Souquere, S., Mariño, G., Lachkar, S., Senovilla, L., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.09.013 · Cited by 285 · see citing works
Autophagosome formation—The role of ULK1 and Beclin1–PI3KC3 complexes in setting the stage
Wirth, M., Joachim, J., & Tooze, S. A. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.05.007 · Cited by 277 · see citing works
Self and Nonself: How Autophagy Targets Mitochondria and Bacteria
Randow, F., & Youle, R. J. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.03.012 · Cited by 271 · see citing works
Mitophagy and cancer
Chourasia, A. H., Boland, M. L., & Macleod, K. F. (2015) · Cancer & Metabolism · doi:10.1186/s40170-015-0130-8 · Cited by 271 · see citing works
Stress-induced self-cannibalism: on the regulation of autophagy by endoplasmic reticulum stress
Deegan, S., Saveljeva, S., Gorman, A. M., & Samali, A. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1173-4 · Cited by 273 · see citing works
Pex3‐anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae
Motley, A. M., Nuttall, J. M., & Hettema, E. H. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.151 · Cited by 267 · see citing works
Therapeutic Targeting of Autophagy in Disease: Biology and Pharmacology
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Authors: Weidberg, H., Shvets, E., & Elazar, Z.
Affiliations: Weizmann Institute of Science (IL)
Corresponding author: Weidberg, Hilla
Shvets, Elena
ORCID: Weidberg, Hilla
Elazar, Zvulun
Venue: Annual Review of Biochemistry
Publisher: Annual Reviews
Published: 2011-07-07
Volume: 80
Issue: 1
Pages: 125-156
ISSN: 0066-4154 (ISSN-L)
1545-4509
DOI: 10.1146/annurev-biochem-052709-094552
OpenAlex: W2052470191
Cited by: 466
References: 227
Citations by year: 2026: 4 · 2025: 10 · 2024: 15 · 2023: 14 · 2022: 24 · 2021: 26 · 2020: 21 · 2019: 28 · 2018: 25 · 2017: 31 · 2016: 40 · 2015: 38 · 2014: 46 · 2013: 59 · 2012: 68
FWCI: 7.10
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Biochemistry (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Keywords: autophagy, autophagosome formation, selective autophagy, autophagosome-lysosome fusion, ubiquitin-like proteins, autophagy-related genes, signal transduction, yeast autophagy, cytoplasmic degradation
MeSH terms: Animals, Autophagy, Intracellular Membranes, Phagosomes, Yeasts, Organelles, Signal Transduction, Biomarkers

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Biogenesis and Cargo Selectivity of Autophagosomes

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