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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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“Nowadays, it has been reported that more than thirty-five Autophagy-Related Genes (ATG) participate in autophagy processes including those that express microtubule-associated protein light chain 3 (LC3), Beclin-1, and other autophagy-related proteins (38).”
BackgroundAutophagy activation is required for myofibroblast differentiation during healing of oral mucosa
Vescarelli, E., Pilloni, A., Dominici, F., Pontecorvi, P., Angeloni, A., Polimeni, A., Ceccarelli, S., & Marchese, C. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12767 · Cited by 49
Mitofusin 2 Exerts a Protective Role in Ischemia Reperfusion Injury Through Increasing Autophagy
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“chain 3 (MAP–LC3/Atg8/LC3) to phosphatidylethanolamine (PE).(18) LC3 (cytosolic) is cleaved at its C terminus by Atg4 to form LC3-I, which is covalently conjugated to PE by Atg3 catalysis to form LC3-II.”
BackgroundLi, S., Zhou, Y., Fan, J., Cao, S., Cao, T., Huang, F., Zhuang, S., Wang, Y., Yu, X., & Mao, H. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.08.013 · Cited by 47
“ated protein light chain 3 (LC3), Beclin-1, and other autophagy-related (ATG) proteins.(11,12) LC3 is known to exist on autophagosome membrane and serves as a specific marker of autophagy.”
BackgroundFas-mediated autophagy requires JNK activation in HeLa cells
Zhang, Y., Wu, Y., Cheng, Y., Zhao, Z., Tashiro, S., Onodera, S., & Ikejima, T. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.10.151 · Cited by 47
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“Atg5–Atg12 forms a complex with Atg16L1 and associates with the isolation membrane [4].”
Mammalian Apg12p, but not the Apg12p · Apg5p conjugate, facilitates LC3 processing
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“In the elongation/enclosure step of autophagosome formation, Atg5 and Atg16 can form the Atg12-Atg5-Atg16 complex [47].”
BackgroundSasazawa, Y., Sato, N., Umezawa, K., & Simizu, S. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.606293 · Cited by 46
“Autophagy is initiated by the formation of a small membrane particle, called the autophagosomes, mediated by signaling cascades, including autophagy-related genes and microtubule-association 1 light chain 3 (LC3)(2) (1).”
BackgroundInflammatory Bowel Disease: Dysfunction of Autophagy?
Scharl, M. M., & Rogler, G. (2012) · Digestive Diseases · doi:10.1159/000342588 · Cited by 49
Impairment of autophagy: From hereditary disorder to drug intoxication
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“LC3 is a homolog of the yeast autophagy-related protein Apg8p [15] and is used to mark the initiation of autophagy [16,17].”
Distinct temporal requirements for autophagy and the proteasome in yeast meiosis
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“Atg12 and Atg8 are 2 ubiquitin-like proteins that are essential for autophagy.(19) After transferring wild-type strains into liquid SPM at various times, the yeast began to sporulate very quickly, an almost 100% sporulation rate was achieved in approximately 24 h, but either”
BackgroundYoung, P. G., Passalacqua, M. J., Chappell, K., Llinas, R. J., & Bartel, B. (2019) · Autophagy · doi:10.1080/15548627.2019.1569915 · Cited by 46
“protein that decorates the phagophore via conjugation to phosphatidylethanolamine [8,25,26], and this ATG8 lipidation requires ATG3, ATG4, ATG5, ATG7, ATG10, ATG12, and”
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Up‐regulation of autophagy in small intestine Paneth cells in response to total‐body γ‐irradiation
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“phosphatidylethanolamine on the forming isolation membrane is mediated by E-1- and E-2-like enzymes Atg7 and Atg3 [15–17].”
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Autophagy During Vertebrate Development
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“The complex Atg12/Atg5/Atg16L mediates LC3-PE by binding to the autophagosome membranes [53,54] and promotes the elongation and isolation of the autophagosome [3,30] (Figure 2C).”
BackgroundCrocin-Elicited Autophagy Rescues Myocardial Ischemia/Reperfusion Injury via Paradoxical Mechanisms
Zeng, C., Li, H., Fan, Z., Zhong, L., Guo, Z., Guo, Y., & Xi, Y. (2016) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x16500282 · Cited by 45
Chung, K. M., Jeong, E.-J., Park, H., An, H., & Yu, S. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00116 · Cited by 47
“Atg7 is required for Atg12-Atg5 conjugation and LC3 lipidation (Ohsumi, 2001) and we generated Atg7 stable knockdown HCN cells by genetically suppressing Atg7 expression with the lentivirus expressing Atg7-targeting shRNA.”
Fluid Shear Stress Promotes Autophagy in Hepatocellular Carcinoma Cells
Wang, X., Zhang, Y., Feng, T., Su, G., He, J., Gao, W., Shen, Y., & Liu, X. (2018) · International Journal of Biological Sciences · doi:10.7150/ijbs.27055 · Cited by 46
“During the process of autophagy, LC3B will bind to autophagosomes, and LC3I gradually converted to LC3II, the ratio of LC3 II/I becomes higher [33, 34].”
BackgroundPhospholipid turnover and acyl chain remodeling in the yeast ER
Patton, J. L., & de Kroon, A. I. P. M. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2019.05.006 · Cited by 45
“PE serves as precursor in an essential step of the synthesis of the glycosylphosphatidylinositol (GPI) anchor that attaches a subset of plasma membrane proteins to the membrane [16,17], and it becomes covalently bound to Atg8 in the assembly of autophagosomes [18].”
Yan, L., Gong, Y., Shao, M., Ruan, G., Xie, H., Liao, X., Wang, X., Han, Q., Zhou, X., Zhu, L., et al. (2020) · Oncology Letters · doi:10.3892/ol.2020.11573 · Cited by 46
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“Autophagy is a major intracellular degradation mechanism for longed-lived proteins and organelles, and operates and promotes survival during starvation (Ohsumi, 2001; Levine and Klionsky, 2004).”
BackgroundThe Physiological Role of Irisin in the Regulation of Muscle Glucose Homeostasis
Yano, N., Zhao, Y., & Zhao, T. C. (2021) · Endocrines · doi:10.3390/endocrines2030025 · Cited by 46
Mechanisms of Cell Survival in Myocardial Hibernation
Depré, C., & Vatner, S. F. (2005) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2005.04.006 · Cited by 44
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Host and Viral Factors in HIV-Mediated Bystander Apoptosis
Garg, H., & Joshi, A. (2017) · Viruses · doi:10.3390/v9080237 · Cited by 48
“Autophagy is characterized by the formation of membrane bound compartments that engulf cytoplasmic material, involves the autophagy-related (Atg) group of proteins [185] and has been described in several bacterial and viral infections including HIV [182,186–188].”
BackgroundMitophagy in neurodegenerative disease pathogenesis
Yang, K., Yan, Y., Yu, A., Zhang, R., Zhang, Y., Qiu, Z., Li, Z., Zhang, Q., Wu, S., & Li, F. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.385281 · Cited by 43
“Decades of studies in yeast have defined the molecular participants in this pathway (Ohsumi et al., 1993; Ohsumi, 1994, 1997, 1999, 2001, 2014), and we gradually found that nonselective autophagy plays a critical role in the stability of cells.”
BackgroundOrigin and Evolution of Self-Consumption: Autophagy
Hughes, T., & Rusten, T. E. (2008) · Advances in experimental medicine and biology · doi:10.1007/978-0-387-74021-8_9 · Cited by 48
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OsATG8c-Mediated Increased Autophagy Regulates the Yield and Nitrogen Use Efficiency in Rice
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“We then investigated the autophagy progression by Acridine Orange staining which showed acidic compartments containing hydrolytic enzymes [52].”
RetractedThe autophagy receptor NBR1 directs the clearance of photodamaged chloroplasts
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“This evolutionarily conserved process is characterized by the formation of double membrane cytosolic vesicles (called autophagosomes), which sequester cytoplasmic content and then fuse with lysosomes [9, 10].”
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“As expected, the irreversible inhibition of PI3K did not induce the autophagy pathway, as it is widely proved that the generation of PIP3 is necessary for the autophagosome formation, and wortmannin is considered to act as an autophagy inhibitor (Ohsumi, 2001).”
BackgroundRole and mechanisms of autophagy in alcohol-induced liver injury
Chao, X., & Ding, W. (2019) · Advances in pharmacology · doi:10.1016/bs.apha.2019.01.008 · Cited by 43
“Beclin1 is a component of the autophagy-promoting class III phosphoinositide 3 (PI3)-kinase complexes, which also contains Atg14L, p150 (the yeast ortholog is Vps15) and the class-III PI3 kinase VPS34 (Kihara, Noda, Ishihara, & Ohsumi, 2001).”
BackgroundInfluentialTeichert, I., Pöggeler, S., & Nowrousian, M. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10504-3 · Cited by 42
“4) (Ohsumi 2001).”
c-myc Induces Autophagy in Rat 3Y1 Fibroblast Cells
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Functional Amino Acids and Autophagy: Diverse Signal Transduction and Application
Liu, C., Ji, L., Hu, J., Zhao, Y., Johnston, L. J., Zhang, X., & Ma, X. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111427 · Cited by 44
“Autophagy steps are hierarchically controlled by two complexes: namely the unc-51-like kinase 1 (ULK1) complex [10] and class III phosphatidylinositol 3-kinase (PtdIns(3)K) complex [12], as well as by two ubiquitin-like conjugation systems, namely the Atg8-lipid phosphatidylethanolamine (PE) and Atg12-Atg5 systems [13…”
BackgroundRole of Protein Tyrosine Phosphatases in Regulating the Immune System
Spalinger, M. R., McCole, D. F., Rogler, G., & Scharl, M. M. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000297 · Cited by 41
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“Autophagy requires the modification of two proteins, ATG12 and ATG8 (LC3), via enzymatic pathways that are similar to ubiquitin conjugation (36).”
BackgroundWang, H., Liu, C., Mei, X., Cao, Y., Guo, Z., Yuan, Y., Zhao, Z., Song, C., Guo, Y., & Shen, Z. (2017) · Oncotarget · doi:10.18632/oncotarget.21203 · Cited by 42
“In eukaryotes, the autophagic vesicles require a pair of essential ubiquitin-like conjugation systems, Atg12-Atg5 and Atg8 (LC3)phosphatidylethanolamine (LC3-PE) [32].”
BackgroundRen, W., Sang, C., Shi, D., Song, X., Zhou, M., & Chen, C. (2018) · Current Genetics · doi:10.1007/s00294-018-0810-3 · Cited by 41
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“Exposure of human neurons to CXCL12(5-67) caused a reduction in the autophagy-associated molecule LC3 (P<0.”
BackgroundMethodInfluentialAutophagy in MHC Class II Presentation of Endogenous Antigens
Gannagé, M., & Münz, C. (2009) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-00302-8_6 · Cited by 40
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Calmodulin‐related CML 24 interacts with ATG 4b and affects autophagy progression in A rabidopsis
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Autophagic Survival Precedes Programmed Cell Death in Wheat Seedlings Exposed to Drought Stress
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“ATG8 conjugates to the lipid phosphatidyl ethanolamine (PE) to form ATG8-PE, inducing autophagosome formation [8].”
BackgroundMolecular Mechanism and Regulation of Autophagy and Its Potential Role in Epilepsy
Zhu, H., Wang, W., & Li, Y. (2022) · Cells · doi:10.3390/cells11172621 · Cited by 44
Moal, V. L.-L., Comenge, Y., Ruby, V., Amsellem, R., Nicolas, V., & Servin, A. L. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01595.x · Cited by 40
“The formation of a cup-shaped initial membrane, known as the phagophore or isolation membrane, requires the entire set of autophagy (Atg)-related genes plus two ubiquitin-like conjugation systems: Atg12-Atg5 conjugation and further downstream, Atg8 conjugation to phosphatidylethanolamide (Ohsumi, 2001).”
BackgroundAutophagy in Chronic Myeloid Leukaemia: Stem Cell Survival and Implication in Therapy
Helgason, G. V., Mukhopadhyay, A., Karvela, M., Salomoni, P., Calabretta, B., & Holyoake, T. L. (2013) · Current Cancer Drug Targets · doi:10.2174/15680096113139990088 · Cited by 42
“The expansion of the phagophores to autophagosomes leading to autophagosome maturation, also depends on two ubiquitinlike conjugation systems forming complexes essential for autophagy [36]: 1) The ATG12/ ATG5/ATG16 and 2) ATG8-PE (phosphatidylethanolamine) (ATG8 is also known as microtubule-associated protein 1 light…”
BackgroundDopamine- and zinc-induced autophagosome formation facilitates PC12 cell survival
Hung, H., Huang, W., & Pan, C. (2013) · Cell Biology and Toxicology · doi:10.1007/s10565-013-9261-2 · Cited by 39
“Two conjugation systems consisting of Atg8- phosphatidylethanolamine (Atg8-PE) and Atg12– Atg5, respectively, are involved in the formation of autophagosomes (Ohsumi 2001).”
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Protein tyrosine phosphatase non-receptor type 2 and inflammatory bowel disease
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Autophagy and the invisible line between life and death
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Oxidative Stress and Autophagy
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“…the short-lived proteins are broken up inside ubiquitin-proteasome system, intracellular organelles and long-lived proteins are benefited from as they are destroyed in autophagy system and decomposed into the building stones similar to amino acids to be used again inside the cell [58, 59].”
BackgroundConophylline inhibits high fat diet-induced non-alcoholic fatty liver disease in mice
Ohashi, T., Nakade, Y., Ibusuki, M., Kitano, R., Yamauchi, T., Kimoto, S., Inoue, T., Kobayashi, Y., Sumida, Y., Ito, K., et al. (2019) · PLoS ONE · doi:10.1371/journal.pone.0210068 · Cited by 39
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“During autophagy, phagophores engulf parts of the cytoplasm to form autophagosomes, and subsequently fuse with lysosomes to become autolysosomes, whose contents are eventually degraded by lysosomal hydrolytic enzymes (Kamada et al. 2004; Klionsky 2007; Mizushima 2007; Ohsumi 2001).”
BackgroundThe phosphatidylinositol 3-phosphate-binding protein SNX4 controls ATG9A recycling and autophagy
Ravussin, A., Brech, A., Tooze, S. A., & Stenmark, H. (2021) · Journal of Cell Science · doi:10.1242/jcs.250670 · Cited by 38
“Macroautophagy (hereafter referred to as autophagy) controls numerous fundamental physiological functions (Levine and Klionsky, 2004; Mizushima, 2005; Ohsumi, 2001).”
BackgroundEaten alive: autophagy and neuronal cell death after hypoxia-ischemia.
Chu, C. T. (2008) · American Journal of Pathology · doi:10.2353/ajpath.2008.071064 · Cited by 43
Mitoxosome: a mitochondrial platform for cross‐talk between cellular stress and antiviral signaling
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“ATG16L1, ATG5, and ATG7 have been reported to have a common role (through the process of autophagy) in CD (114).”
BackgroundInfluentialImmune surveillance of intracellular pathogens via autophagy
Schmid, D., & Münz, C. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401727 · Cited by 46
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Radiation Combined Injury: DNA Damage, Apoptosis, and Autophagy
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“membrane-enclosed vacuole, and transported to lysosomes or late endosomes for biodegradation (29, 59).”
Autophagy in cerebral ischemia and the effects of traditional Chinese medicine
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“The autophagosome then fuses with the lysosome to form the single-layered autolysosome, in which cellular contents are ultimately degraded (Ohsumi, 2001; Wang and Klionsky, 2003; Yoshimori, 2004; Mizushima et al., 2008).”
BackgroundProtective effect of L-carnitine in cyclophosphamide-induced germ cell apoptosis
Zhu, B., Zheng, Y., Zhang, Y., Cao, Y.-S., Zhang, L., Li, X., Liu, T., Jiao, Z.-Z., Wang, Q., & Zhao, Z. (2015) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b1500015 · Cited by 39
Ginet, V., Puyal, J., Rummel, C., Aubry, D., Breton, C. S., Cloux, A.-J., Majjigapu, S. R., Sordat, B., Vogel, P., Bruzzone, S., et al. (2014) · Autophagy · doi:10.4161/auto.27722 · Cited by 38
“In the past decade, autophagy has been extensively studied.(12,16,40) In most studies, autophagy functions as a survival mechanism under stress conditions(41-44) and its role in cell death is less well established.”
BackgroundRole of autophagy in the maintenance and function of cancer stem cells
Vitale, I., Manic, G., Dandrea, V., & Maria, R. D. (2015) · The International Journal of Developmental Biology · doi:10.1387/ijdb.150082iv · Cited by 39
“…of LC3 by the protease ATG4, which produces the cytosolic form LC3-I, followed by the sequential action of the E1-like enzyme ATG7, the E2-like enzyme ATG3 and the E3-ligase complex ATG5-ATG12-ATG16L1, which catalyzes the covalent conjugation of PE to LC3-I(Noda et al., 2008, Ohsumi, 2001).”
BackgroundHepatic Lysosomal iNOS Activity Impairs Autophagy in Obesity
Qian, Q., Zhang, Z., Li, M., Savage, K., Cheng, D., Rauckhorst, A. J., Ankrum, J. A., Taylor, E. B., Ding, W., Xiao, Y., et al. (2019) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2019.03.005 · Cited by 38
“The lysosome is the major site for processing autophagic cargoes.(34) To determinewhether the iNOS-mediated lysosomal nitrosative stress contributes to autophagic dysfunction, we”
BackgroundCytoprotective role of autophagy during paclitaxel-induced apoptosis in Saos-2 osteosarcoma cells
Kim, H. J., Lee, S. G., Kim, Y.-J., Park, J., Lee, K. Y., Yoo, Y. H., & Kim, J. (2013) · International Journal of Oncology · doi:10.3892/ijo.2013.1884 · Cited by 39
Molecular Mechanisms Underlying Initiation and Activation of Autophagy
Wei, Z. J., Hu, X., Wu, Y., Zhou, L., Zhao, M., & Lin, Q. (2024) · Biomolecules · doi:10.3390/biom14121517 · Cited by 37
Role of autophagy in cancer prevention, development and therapy
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“Each system is composed of two ubiquitin-like proteins, ATG8 (also known as microtubuleassociated protein 1 light-chain 3, hereafter called LC3) and ATG12, and three enzymes (ATG3, ATG7 and ATG10) that are required for conjugation reactions [11].”
BackgroundAn improved method for high-throughput quantification of autophagy in mammalian cells
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Ubiquitin pathways regulate the pathogenesis of chronic liver disease
Park, J.-S., Ma, H., & Roh, Y. (2021) · Biochemical Pharmacology · doi:10.1016/j.bcp.2021.114764 · Cited by 40
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Peroxisomes are present in murine spermatogonia and disappear during the course of spermatogenesis
Lüers, G. H., Thiele, S., Schad, A., Völkl, A., Yokota, S., & Seitz, J. (2005) · Histochemistry and Cell Biology · doi:10.1007/s00418-005-0114-9 · Cited by 37
“: +49-6421-2864021 A. Schad Æ A. Völkl Institute for Anatomy and Cell Biology, University of Heidelberg, Heidelberg, Germany S. Yokota Department of Biology, Yamanashi University, Kofu, Japan macropexophagy or micropexophagy (Ohsumi 2001; Reggiori and Klionsky 2002; Farre and Subramani 2004).”
PML-RAR&x03B1; enhances autophagic activity through inhibiting Akt/mTOR pathwayPreprint
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“In the past decade, the molecular mechanism of autophagy was widely investigated in yeast and mammalian cells.(3,4) More than Autophagy is a highly conserved, closely regulated homeostatic cellular activity that allows for the bulk degradation of long-lived proteins and cytoplasmic organelles.”
BackgroundCaccamo, A., Shaw, D. M., Guarino, F., Messina, A., Walker, A. W., & Oddo, S. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv193 · Cited by 35
“good indicators of autophagy induction (13,14).”
BackgroundDivya, T., Anandasadagopan, S. K., & Sudhandiran, G. (2017) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2017.04.003 · Cited by 36
Wang, H., Zhou, Y., Zhu, Q., Zang, H., Cai, J., Wang, J., Cui, L., Meng, X., Zhu, G., & Li, J. (2019) · Journal of Dairy Science · doi:10.3168/jds.2019-16414 · Cited by 38
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“The first ATG gene was identified from yeast, and at least 32 ATGs have been shown to participate in yeast autophagy [5,6].”
BackgroundRegulation of basal autophagy by transient receptor potential melastatin 7 (TRPM7) channel
Oh, H. G., Chun, Y. S., Park, C., Kim, T., Park, M. K., & Chung, S. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.05.007 · Cited by 40
SmATG7 is required for viability in the homothallic ascomycete Sordaria macrospora
Nolting, N., Bernhards, Y., & Pöggeler, S. (2009) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2009.03.008 · Cited by 36
The Interplay Between Autophagy and Regulated Necrosis
Zhang, L., Cui, T., & Wang, X. (2022) · Antioxidants and Redox Signaling · doi:10.1089/ars.2022.0110 · Cited by 39
“The cysteine protease activity of ATG4 promotes the cleavage of nascent LC3, following conjugation with phosphatidylethanolamine (PE) and subsequent incorporation into the phagophore membrane with the assistance of ATG7 and ATG3 (Glick et al, 2010; Ohsumi, 2001).”
Xin, L., Xiao, Z., Ma, X., He, F., Yao, H., & Liu, Z. (2014) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2014.05.005 · Cited by 35
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Santarelli, R., Granato, M., Pentassuglia, G., Lacconi, V., Montani, M. S. G., Gonnella, R., Tafani, M., Torrisi, M. R., Faggioni, A., & Cirone, M. (2016) · Autophagy · doi:10.1080/15548627.2016.1235122 · Cited by 35
“primary monocytes by reducing CAST and ATG5, the latter protein playing an important role in the autophagic process.(2,53)”
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“Chemical Screenings Identify that CI-994 Improves HLC Differentiation Of the three genes we successfully validated, ATG7 encodes autophagy-related protein 7 (Ohsumi, 2001); RPS6KA2 encodes ribosomal protein S6 kinase alpha-2, amember of the ribosomal S6 kinase family of serine and threonine kinases that signals downst…”
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Studying plant autophagy: challenges and recommended methodologies
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“…processed by the ATG4 protease to expose a C-terminal glycine residue and is covalently modified with the attachment of the membrane lipid PE via ubiquitin-like reactions that promote the formation of the ATG8–PE adduct (Ohsumi 2001; Yoshimoto et al. 2004; Hanada et al. 2007; Fujita et al. 2008).”
BackgroundMethodNanomaterial-mediated host directed therapy of tuberculosis by manipulating macrophage autophagy
Liu, Y., Wang, J., Yang, J., Xia, J., Yu, J., Chen, D., Huang, Y., Yang, F., Ruan, Y., Xu, J., et al. (2024) · Journal of Nanobiotechnology · doi:10.1186/s12951-024-02875-w · Cited by 39
“Following initiation, two main mechanisms involving ubiquitin-like (UBL) proteins are responsible for phagosome expansion [50] (Fig.”
BackgroundChapter 6 Monitoring Autophagy in Alzheimer's Disease and Related Neurodegenerative Diseases
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Regulation of autophagy in hematological malignancies: role of reactive oxygen species
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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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