Molecular dissection of autophagy: two ubiquitin-like systems
Abstract
Recent analyses of the genes required for autophagy--intracellular bulk protein degradation--in yeast have revealed two ubiquitin-like systems, both of which are involved in the membrane dynamics of the process. Molecular dissection of these systems is now revealing some surprises.
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Decreased nutrient availability universally activates autophagy, at least in part by inhibiting TOR signalling.
“One universal activator of autophagy is a decrease in nutrient availability and this stimulation occurs, at least in part, by the inhibition of TOR (target of rapamycin) signalling 74 .”
From The common biology of cancer and ageing (2007) · cites this paper as [74]
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“Yeast genetics have revealed that two ubiquitylation-like conjugation systems are required for autophagosome formation (Ohsumi, 2001).”
BackgroundAutophagosome Formation in Mammalian Cells.
Mizushima, N., Ohsumi, Y., & Yoshimori, T. (2002) · Cell Structure and Function · doi:10.1247/csf.27.421 · Cited by 877 · see citing works
Self-citationAutophagy Regulates Programmed Cell Death during the Plant Innate Immune Response
Liu, Y., Schiff, M., Czymmek, K. J., Tallóczy, Z., Levine, B., & Dinesh‐Kumar, S. P. (2005) · Cell · doi:10.1016/j.cell.2005.03.007 · Cited by 865 · see citing works
“Autophagy is a highly regulated process during which cytoplasmic materials are enclosed in doublemembrane bound vesicles that are then targeted to the vacuole or lysosome for degradation (Levine and Klionsky, 2004; Ohsumi, 2001).”
BackgroundAn Overview of the Molecular Mechanism of Autophagy
Yang, Z., & Klionsky, D. J. (2009) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-00302-8_1 · Cited by 835 · see citing works
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“The molecular mechanism of autophagy has been investigated in yeast and mammalian cells.(4,5) The Atg5-dependent”
BackgroundThe Kennedy pathway— De novo synthesis of phosphatidylethanolamine and phosphatidylcholine
Gibellini, F., & Smith, T. (2010) · IUBMB Life · doi:10.1002/iub.337 · Cited by 833 · see citing works
“PE or PE-derived ethanolamine-phosphoglycerol can be in some specialized circumstances attached to protein residues (such as the elongation factor 1A or to ATG8 in autophagy) as a posttranslational modification in some specialized circumstances (26, 27).”
BackgroundAutophagy: in sickness and in health
Cuervo, A. M. (2004) · Trends in Cell Biology · doi:10.1016/j.tcb.2003.12.002 · Cited by 816 · see citing works
Structural Basis for Sorting Mechanism of p62 in Selective Autophagy
Ichimura, Y., Kumanomidou, T., Sou, Y.-S., Mizushima, T., Ezaki, J., Ueno, T., Kominami, E., Yamane, T., Tanaka, K., & Komatsu, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m802182200 · Cited by 803 · 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
“Phagophore expansion and closure require several ubiquitinlike (UBL) proteins that take part in 2 conjugation reactions.(79,80) ATG12-ATG5-ATG16L1, a product formed in the first conjugation reaction, stimulates the recruitment and conversion of proteolytically processed cytosolic MAP1LC3/LC3 (microtubule-associated pr…”
BackgroundProtein Turnover Via Autophagy: Implications for Metabolism
Mizushima, N., & Klionsky, D. J. (2007) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.27.061406.093749 · Cited by 793 · see citing works
“Structure-function relationship of Atg12, a ubiquitin-like modifier essential for autophagy.”
BackgroundInfluentialMizushima, N., Kuma, A., Kobayashi, Y., Yamamoto, A., Matsubae, M., Takao, T., Natsume, T., Ohsumi, Y., & Yoshimori, T. (2003) · Journal of Cell Science · doi:10.1242/jcs.00381 · Cited by 791 · see citing works
Self-citationVitamin D3 Induces Autophagy in Human Monocytes/Macrophages via Cathelicidin
Yuk, J., Shin, D., Lee, H., Yang, C., Jin, H. S., Kim, K., Lee, Z., Lee, S.-H., Kim, J., & Jo, E. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.08.004 · Cited by 787 · see citing works
Origin and function of ubiquitin-like proteins
Hochstrasser, M. (2009) · Nature · doi:10.1038/nature07958 · Cited by 784 · see citing works
Autophagy-dependent cell death
Denton, D., & Kumar, S. (2019) · Cell Death & Differentiation · doi:10.1038/s41418-018-0252-y · Cited by 777 · see citing works
Azad, M. B., Chen, Y., & Gibson, S. B. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2270 · Cited by 761 · see citing works
Autophagy in metazoans: cell survival in the land of plenty
Lum, J., DeBerardinis, R., & Thompson, C. (2005) · Nature reviews. Molecular cell biology · doi:10.1038/nrm1660 · Cited by 842 · see citing works
Another way to die: autophagic programmed cell death
Tsujimoto, Y., & Shimizu, S. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401777 · Cited by 755 · see citing works
Autosis and autophagic cell death: the dark side of autophagy
Liu, Y., & Levine, B. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.143 · Cited by 746 · see citing works
“conjugation of Atg5 to Atg12 and the conversion of LC3-I to its phosphatidylethanolamine-conjugated form (LC3-II).(10) The”
BackgroundAutophagy: A lysosomal degradation pathway with a central role in health and disease
Eskelinen, E., & Säftig, P. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2008.07.014 · Cited by 699 · see citing works
“hagosome formation, the Atg12-Atg5 and the Atg8-phosphatidyl ethanolamine systems [53].”
BackgroundPhagosome maturation: aging gracefully
Vieira, O. V., Botelho, R. J., & Grinstein, S. (2002) · Biochemical Journal · doi:10.1042/bj20020691 · Cited by 675 · see citing works
Autophagic programmed cell death by selective catalase degradation
Yu, L., Wan, F., Dutta, S., Welsh, S., Liu, Z., Freundt, E. C., Baehrecke, E. H., & Lenardo, M. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511288103 · Cited by 668 · see citing works
Autophagy Controls Salmonella Infection in Response to Damage to the Salmonella-containing Vacuole
Birmingham, C. L., Smith, A. C., Bakowski, M. A., Yoshimori, T., & Brumell, J. H. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m509157200 · Cited by 658 · see citing works
Autophagy, amyloidogenesis and Alzheimer disease
Nixon, R. A. (2007) · Journal of Cell Science · doi:10.1242/jcs.019265 · Cited by 749 · see citing works
“This process has been reviewed in detail (Shintani and Klionsky, 2004; Levine and Klionsky, 2004; Seglen and Bohley, 1992; Dunn, 1994; Ohsumi, 2001; Mizushima et al., 2002).”
MethodAtg9 vesicles are an important membrane source during early steps of autophagosome formation
Yamamoto, H., Kakuta, S., Watanabe, T. M., Kitamura, A., Sekito, T., Kondo-Kakuta, C., Ichikawa, R., Kinjo, M., & Ohsumi, Y. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201202061 · Cited by 659 · see citing works
“Autophagy is a major cellular process, conserved in eukaryotic cells, that mediates bulk degradation of cytoplasmic proteins and organelles in response to starvation (Ohsumi, 2001; Klionsky, 2007; Nakatogawa et al., 2009).”
Self-citationAutophagy: The Master of Bulk and Selective Recycling
Marshall, R. S., & Vierstra, R. D. (2018) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040606 · Cited by 611 · see citing works
“The next step centers on a signature conjugation pathway analogous to ubiquitylation that decorates the phagophore with the Ub-fold protein ATG8 [known as MICROTUBULEASSOCIATED PROTEIN 1 LIGHT CHAIN 3 (MAP1LC3) or GAMMA-AMINOBUTYRIC ACID RECEPTOR–ASSOCIATED PROTEIN (GABARAP) in animals] (137) (Figure 3a).”
BackgroundDoherty, J., & Baehrecke, E. H. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0201-5 · Cited by 626 · see citing works
Regulation and role of autophagy in mammalian cells
Meijer, A. J., & Codogno, P. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.02.002 · Cited by 615 · see citing works
“, Ohsumi, Y., & Yoshimori, T. (2001b). Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network.”
BackgroundInfluentialAutophagic Nutrient Recycling in Arabidopsis Directed by the ATG8 and ATG12 Conjugation Pathways
Thompson, A. R., Doelling, J. H., Suttangkakul, A., & Vierstra, R. D. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.060673 · Cited by 612 · see citing works
“Here, individual proteins, protein complexes, and entire organelles become engulfed in membrane-bound vesicles, which are delivered to the vacuole (yeast/plants) or lysosome (animals; Ohsumi, 2001; Klionsky, 2004; Thompson and Vierstra, 2005).”
BackgroundInfluentialDoelling, J. H., Walker, J. M., Friedman, E. M., Thompson, A. R., & Vierstra, R. D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m204630200 · Cited by 599 · see citing works
Autophagy: Pathways for Self-Eating in Plant Cells
Liu, Y., & Bassham, D. C. (2012) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105441 · Cited by 591 · see citing works
Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S., & Ohsumi, Y. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.011024 · Cited by 595 · see citing works
Self-citationBarretto, N., Jukneliene, D., Ratia, K. M., Chen, Z., Mesecar, A. D., & Baker, S. C. (2005) · Journal of Virology · doi:10.1128/jvi.79.24.15189-15198.2005 · Cited by 589 · see citing works
“At least 16 genes (termed Apg for autophagy-defective) and two UBL modification systems are required for autophagy in Saccharomyces cerevisiae (38, 39).”
BackgroundThe Adaptor Protein p62/SQSTM1 Targets Invading Bacteria to the Autophagy Pathway
Zheng, Y. T., Shahnazari, S., Brech, A., Lamark, T., Johansen, T., & Brumell, J. H. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900441 · Cited by 581 · see citing works
“Recently, macroautophagy (hereafter referred to as autophagy), an important cellular pathway for the degradation of longlived proteins and damaged organelles by delivering them to the lysosome (1, 2), was shown to be involved in the innate immune response to bacteria (2, 3).”
BackgroundSarkar, S., Ravikumar, B., Floto, R. A., & Rubinsztein, D. C. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.110 · Cited by 578 · see citing works
Arico, S., Petiot, A., Bauvy, C., Dubbelhuis, P. F., Meijer, A. J., Codogno, P., & Ogier‐Denis, É. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c100319200 · Cited by 576 · see citing works
Autophagy: machinery and regulation
Yin, Z., Pascual, C., & Klionsky, D. J. (2016) · Microbial Cell · doi:10.15698/mic2016.12.546 · Cited by 567 · see citing works
“Atg8 undergoes a different type of conjugation, being covalently attached to the lipid phosphatidylethanolamine.”
InfluentialKuma, A., Matsui, M., & Mizushima, N. (2007) · Autophagy · doi:10.4161/auto.4012 · Cited by 555 · see citing works
Autophagy in the Eukaryotic Cell
Reggiori, F., & Klionsky, D. J. (2002) · Eukaryotic Cell · doi:10.1128/ec.01.1.11-21.2002 · Cited by 551 · see citing works
Yoshimoto, K., Hanaoka, H., Sato, S., Kato, T., Tabata, S., Noda, T., & Ohsumi, Y. (2004) · The Plant Cell · doi:10.1105/tpc.104.025395 · Cited by 603 · see citing works
“ATG4 proteins had a significant but low level of identity with the yeast Atg4 protein (ATG4a-yeast Atg4, 26%; ATG4byeast Atg4, 29%).”
BackgroundInfluentialSelf-citationAutophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance
Nedjic, J., Aichinger, M., Emmerich, J., Mizushima, N., & Klein, L. (2008) · Nature · doi:10.1038/nature07208 · Cited by 81 · see citing works
The Molecular Mechanism of Autophagy
Wang, C.-W., & Klionsky, D. J. (2003) · Molecular Medicine · doi:10.1007/bf03402040 · Cited by 530 · see citing works
Autophagy and aging: keeping that old broom working
Cuervo, A. M. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.10.002 · Cited by 527 · see citing works
Health benefits of resveratrol: Evidence from clinical studies
Singh, A. P., Singh, R., Verma, S. S., Rai, V., Kaschula, C. H., Maiti, P., & Gupta, S. C. (2019) · Medicinal Research Reviews · doi:10.1002/med.21565 · Cited by 523 · see citing works
“Autophagy is a highly dynamic and evolutionarily conserved self‐catabolic process that helps to maintain cellular homeostasis through lysosome‐mediated degradation of unneeded proteins and organelles.(210,211) The defects in autophagy are associated with tumorigenesis and in the pathogenesis of other human diseases.”
BackgroundRegulation of macroautophagy by mTOR and Beclin 1 complexes
Pattingre, S., Espert, L., Biard‐Piechaczyk, M., & Codogno, P. (2007) · Biochimie · doi:10.1016/j.biochi.2007.08.014 · Cited by 521 · see citing works
The Role of Autophagy in Mammalian Development: Cell Makeover Rather than Cell Death
Cecconi, F., & Levine, B. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.08.012 · Cited by 521 · see citing works
“Most of the genes involved in macroautophagy (hereafter autophagy), the so-called Autophagy-related (Atg) genes, have been discovered in S. cerevisiae (Ohsumi, 2001).”
BackgroundMechanisms of killing by anti-CD20 monoclonal antibodies
Glennie, M. J., French, R. R., Cragg, M. S., & Taylor, R. P. (2007) · Molecular Immunology · doi:10.1016/j.molimm.2007.06.151 · Cited by 515 · see citing works
Skeletal Muscle Is a Primary Target of SOD1G93A-Mediated Toxicity
Dobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Bonconpagni, S., Belia, S., Wannenes, F., Nicoletti, C., Del Prete, Z., et al. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2008.09.002 · Cited by 513 · see citing works
“This pathway is activated and operates under environmental stress conditions and in various pathological situations (Ohsumi, 2001).”
BackgroundAutophagy: a regulated bulk degradation process inside cells
Yoshimori, T. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2003.07.023 · Cited by 511 · see citing works
Matrix Protein 2 of Influenza A Virus Blocks Autophagosome Fusion with Lysosomes
Gannagé, M., Dormann, D., Albrecht, R., Dengjel, J., Torossi, T., Rämer, P. C., Lee, M., Strowig, T., Arrey, F., Conenello, G., et al. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.09.005 · Cited by 526 · see citing works
“While the function of most of these is still unknown, two ubiquitin-like systems have been characterized as essential for autophagosome generation (Ohsumi, 2001).”
BackgroundAutophagy in chronically ischemic myocardium
Yan, L., Vatner, D. E., Kim, S., Ge, H., Masurekar, M. R., Massover, W. H., Yang, G., Matsui, Y., Sadoshima, J., & Vatner, S. F. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506843102 · Cited by 497 · see citing works
Role of autophagy in G2019S‐LRRK2‐associated neurite shortening in differentiated SH‐SY5Y cells
Plowey, E., Cherra, S. J., Liu, Y.-J., & Chu, C. T. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05217.x · Cited by 523 · see citing works
“To determine whether autophagy plays an active role in neurite blunting, we utilized RNAi mediated knockdown of the essential autophagy proteins LC3/Atg8 and Atg7 (Ohsumi 2001).”
BackgroundAutophagosome Formation and Molecular Mechanism of Autophagy
Tanida, I. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3482 · Cited by 489 · see citing works
“4) (11, 81, 110).”
Autophagy: Many paths to the same end
Cuervo, A. M. (2004) · Molecular and Cellular Biochemistry · doi:10.1023/b:mcbi.0000041848.57020.57 · Cited by 476 · see citing works
“The reader is directed to recent reviews containing thorough descriptions of autophagyrelated proteins [10, 13, 14].”
BackgroundDiversity in the Mechanisms of Neuronal Cell Death
Yuan, J., Lipinski, M. M., & Degterev, A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00601-9 · Cited by 467 · see citing works
Sou, Y., Waguri, S., Iwata, J.-I., Ueno, T., Fujimura, T., Hara, T., Sawada, N., Yamada, A., Mizushima, N., Uchiyama, Y., et al. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-03-0309 · Cited by 475 · see citing works
“Among them, gene products involved in Atg (autophagy) conjugation systems were identified, in which the enzymatic reactions involved are, in principle, analogous to the ubiquitin conjugation system, including E1 (activating enzyme) and E2 (conjugating enzyme) (Ohsumi, 2001).”
BackgroundAutophagy and neurodegeneration: when the cleaning crew goes on strike
Martínez‐Vicente, M., & Cuervo, A. M. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70076-5 · Cited by 472 · see citing works
Autophagy facilitates glycolysis during Ras-mediated oncogenic transformation
Lock, R., Roy, S., Kenific, C. M., Su, J. S., Salas, E., Ronen, S. M., & Debnath, J. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-06-0500 · Cited by 467 · see citing works
“Our experiments point to an unexpected requirement for autophagy competence in facilitating glycolysis, which promotes adhesion-independent transformation driven by oncogenic Ras.”
BackgroundComplex interplay between autophagy and oxidative stress in the development of pulmonary disease
Ornatowski, W., Lü, Q., Yegambaram, M., Flores, A. G., Zemskov, E. A., Maltepe, E., Fineman, J. R., Wang, T., & Black, S. M. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101679 · Cited by 474 · see citing works
“After the activation of PtdIns3K complex, the phagophore expands and elongates by membrane addition, which is accomplished by two essential ubiquitin-like (Ubl) conjugation systems, which involve the Ubl proteins ATG12 and microtubule-associated protein light chain 3 (LC3) [66,67].”
BackgroundNF-κB Activation Represses Tumor Necrosis Factor-α-induced Autophagy
Djavaheri‐Mergny, M., Amelotti, M., Mathieu, J., Besançon, F., Bauvy, C., Souquère, S., Pierron, G., & Codogno, P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m602097200 · Cited by 467 · see citing works
Biogenesis and Cargo Selectivity of Autophagosomes
Weidberg, H., Shvets, E., & Elazar, Z. (2011) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052709-094552 · Cited by 466 · see citing works
- Authors
- Ohsumi, Y.
- Affiliations
- National Institute for Basic Biology (JP)
- Corresponding author
- Ohsumi, Yoshinori
- ORCID
- Ohsumi, Yoshinori
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2001-03
- Volume
- 2
- Issue
- 3
- Pages
- 211-216
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- OpenAlex
- W2792139654
- Cited by
- 1,240
- References
- 45
- Citations by year
- 2026: 13 · 2025: 25 · 2024: 30 · 2023: 44 · 2022: 39 · 2021: 34 · 2020: 64 · 2019: 65 · 2018: 51 · 2017: 54 · 2016: 59 · 2015: 44 · 2014: 58 · 2013: 56 · 2012: 67
- FWCI
- 7.06
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Molecular Cell Biology (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, ubiquitin-like proteins, membrane dynamics, yeast, autophagy-related genes
- MeSH terms
- Autophagy-Related Protein 8 Family, Autophagy-Related Protein 7, Autophagy, Lysosomes, Microscopy, Electron, Microtubule-Associated Proteins, Models, Biological, Proteins, Saccharomyces cerevisiae, Ubiquitins, Vacuoles, Saccharomyces cerevisiae Proteins
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