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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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“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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Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
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“However these cells do require de novo gene expression with an increase in expression of the polyubiquitin gene, similar to apoptosis (Ohsumi, 2001; Gozuacik and Kimchi, 2004).”
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Loss of autophagy in the central nervous system causes neurodegeneration in mice
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“In yeast, the UBL protein Atg12 is covalently conjugated to Atg5 in a manner dependent on the E1 activating enzyme Atg7 and the E2 conjugating enzyme Atg10 (70, 113, 129).”
BackgroundImpairment of starvation-induced and constitutive autophagy in Atg7 -deficient mice
Komatsu, M., Waguri, S., Ueno, T., Iwata, J., Murata, S., Tanida, I., Ezaki, J., Mizushima, N., Ohsumi, Y., Uchiyama, Y., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200412022 · Cited by 2,331
“In mammals, there exist at least three Atg8 homologues that can all be activated by Atg7 (Tanida et al., 2001), GATE-16, GABARAP, and LC3 (Ohsumi, 2001), and they localize to the autophagosome (Kabeya et al., 2000, 2004).”
BackgroundInfluentialSelf-citationMizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T., & Ohsumi, Y. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0704 · Cited by 2,105
Self-citationApoptosis, Pyroptosis, and Necrosis: Mechanistic Description of Dead and Dying Eukaryotic Cells
Fink, S. L., & Cookson, B. T. (2005) · Infection and Immunity · doi:10.1128/iai.73.4.1907-1916.2005 · Cited by 2,270
“The sequestration process is under the control of GTPases (100) and phosphatidylinositol kinases (95) and involves novel ubiquitin-like conjugation systems (97).”
BackgroundHomeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
Komatsu, M., Waguri, S., Koike, M., Sou, Y.-S., Ueno, T., Hara, T., Mizushima, N., Iwata, J.-I., Ezaki, J., Murata, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.035 · Cited by 2,124
“To identify protein(s) that could interact with LC3, we employed the proteomic approach as described previously (Komatsu et al., 2004) and then identified a unique protein p62 as one of LC3-interacting proteins, in addition to LC3-modifying enzymes (Ohsumi, 2001) (Table S1).”
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“The molecular mechanism underlying autophagy has been extensively researched in the past decade, and the genes participating in this process, denoted ATGs (autophagy- related; Klionsky et al, 2003), were found to be conserved from yeast to man (Ohsumi, 2001; Huang and Klionsky, 2002).”
BackgroundLoss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production
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Fulda, S., Gorman, A. M., Hori, O., & Samali, A. (2010) · International Journal of Cell Biology · doi:10.1155/2010/214074 · Cited by 1,590
“Two major protein conjugation systems exist that are required for autophagosome formation, that is, the Atg12– Atg5 conjugation and Atg8-phosphatidylethanolamine conjugation systems [38].”
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“These vesicles sequester cytoplasmic constituents and then fuse with lysosomes (Levine and Klionsky, 2004; Ohsumi, 2001).”
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Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B., Liu, J., Bruns, N. E., Tsokos, M., Alt, F. W., & Finkel, T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712145105 · Cited by 1,510
“In this regard, one intriguing possibility is that the requisite covalent association between Atg5 and Atg12 that is mediated through a lysine residue on Atg5 might be a target of reversible acetylation (1).”
BackgroundLC3 conjugation system in mammalian autophagy
Tanida, I., Ueno, T., & Kominami, E. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.05.009 · Cited by 1,512
“Autophagy is the bulk degradation of proteins and organelles, a process essential for cellular maintenance and cell viability (for reviews (Kadowaki, Venerando, Miotto, & Mortimore, 1996; Klionsky, 2004; Ohsumi, 2001; Reggiori & Klionsky, 2002; Seglen et al., 1996; Thumm, 2002; Yoshimori, 2004)).”
BackgroundInfluentialUbiquitin: structures, functions, mechanisms
Pickart, C. M., & Eddins, M. J. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.09.019 · Cited by 1,491
“(The only known exceptions are Atg8 and Atg12, which share the same E1 [15].”
BackgroundLC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation
Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., & Yoshimori, T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01131 · Cited by 1,394
“Atg8 is post-translationally modified by a ubiquitylation-like system (Ohsumi, 2001).”
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Kirkin, V., McEwan, D. G., Novak, I., & Đikić, I. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.04.026 · Cited by 1,268
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BackgroundInfluentialRegulation of an ATG7 - beclin 1 Program of Autophagic Cell Death by Caspase-8
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The Atg12-Atg5 Conjugate Has a Novel E3-like Activity for Protein Lipidation in Autophagy
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“conjugation of Atg5 to Atg12 and the conversion of LC3-I to its phosphatidylethanolamine-conjugated form (LC3-II).(10) The”
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“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).”
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“, 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 574
“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).”
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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 604
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 586
“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 616
“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
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 591
Autophagy: machinery and regulation
Yin, Z., Pascual, C., & Klionsky, D. J. (2016) · Microbial Cell · doi:10.15698/mic2016.12.546 · Cited by 582
“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
Autophagy in the Eukaryotic Cell
Reggiori, F., & Klionsky, D. J. (2002) · Eukaryotic Cell · doi:10.1128/ec.01.1.11-21.2002 · Cited by 562
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
“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 552
The Molecular Mechanism of Autophagy
Wang, C.-W., & Klionsky, D. J. (2003) · Molecular Medicine · doi:10.1007/bf03402040 · Cited by 543
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
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
“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 535
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 535
“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 526
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
“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 519
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
“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.-J., Ge, H., Masurekar, M., 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 430
Role of autophagy in G2019S‐LRRK2‐associated neurite shortening in differentiated SH‐SY5Y cells
Plowey, E. D., Cherra, S. J., Liu, Y., & Chu, C. T. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05217.x · Cited by 517
“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 505
“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 493
“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 472
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 485
“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 495
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
“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 484
“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 407
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
Metadata
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › 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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