Cited by 1,240Autophagy in Disease and TherapyUbiquitin and proteasome pathwaysCellular transport and secretion

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Molecular dissection of autophagy: two ubiquitin-like systems

Ohsumi, Yoshinori·2001·Nature Reviews Molecular Cell Biology

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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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THE UBIQUITIN SYSTEM
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Autophagy-deficient Schizosaccharomyces pombe mutants undergo partial sporulation during nitrogen starvation
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“One of the most striking findings with respect to function of the Atg proteins was the discovery of two ubiquitin-like conjugation systems involving Atg12p and Atg8p (Ohsumi, 2001).”
Background
Glutathione S -Transferase T1 and M1: Gene Sequence Variation and Functional Genomics
Moyer, A. M., Salavaggione, O. E., Hebbring, S. J., Moon, I., Hildebrandt, M. A. T., Eckloff, B. W., Schaid, D. J., Wieben, E. D., & Weinshilboum, R. M. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0635 · Cited by 72
Alternative Programs of Cell Death in Developing Retinal Tissue
Guimarães, C. A., Benchimol, M., Amarante-Mendes, G. P., & Linden, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306547200 · Cited by 74
Induction of autophagy in malignant rhabdoid tumor cells by the histone deacetylase inhibitor FK228 through AIF translocation
Watanabe, M., Adachi, S., Matsubara, H., Imai, T., Yui, Y., Mizushima, Y., Hiraumi, Y., Watanabe, K., Kamitsuji, Y., Toyokuni, S., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23897 · Cited by 72
Lost to translation: when autophagy targets mature ribosomes
Beau, I., Esclatine, A., & Codogno, P. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.05.001 · Cited by 75
Parkinson's disease: acid‐glucocerebrosidase activity and alpha‐synuclein clearance
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“conjugation systems (Ohsumi 2001), which is essential for MA (Komatsu et al.”
Background
The ER stress sensor IRE1 and MAP kinase ERK modulate autophagy induction in cells infected with coronavirus infectious bronchitis virus
Fung, T. S., & Liu, D. X. (2019) · Virology · doi:10.1016/j.virol.2019.05.002 · Cited by 71
“In starvation-induced autophagy, BECN1 is required for the production of PI3P and the nucleation of autophagosomes (Hosokawa et al., 2009; Backer, 2008) , whereas ATG5 constitutes one of the ubiquitin-like conjugation systems required for the expansion of isolation membranes (Ohsumi, 2001; Geng and Klionsky, 2008) .”
Role of proteasomes in the degradation of short-lived proteins in human fibroblasts under various growth conditions
Fuertes, G., Villarroya, A., & Knecht, E. (2003) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00382-5 · Cited by 71
Protein Tyrosine Phosphatase Nonreceptor Type 2 Regulates Autophagosome Formation in Human Intestinal Cells
Scharl, M. M., Wojtal, K. A., Becker, H. M., Fischbeck, A., Frei, P., Arikkat, J. M., Pesch, T., Kellermeier, S., Boone, D. L., Weber, A., et al. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21891 · Cited by 71
Inhibition of glycogen synthase kinase 3β promotes autophagy to protect mice from acute liver failure mediated by peroxisome proliferator-activated receptor α
Ren, F. Z., Zhang, L., Zhang, X., Shi, H., Wen, T., Bai, L., Zheng, S., Chen, Y., Chen, D., Li, L., et al. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.56 · Cited by 71
Autophagy-mediated Regulation of BACE1 Protein Trafficking and Degradation
Feng, T., Tammineni, P., Agrawal, C., Jeong, Y. Y., & Cai, Q. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.766584 · Cited by 69
Autophagy in the Regulation of Tissue Differentiation and Homeostasis
Perrotta, C., Cattaneo, M. G., Molteni, R., & Palma, C. D. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.602901 · Cited by 73
“…mutual influence between autophagy and synaptic machinery has been demonstrated by studies indicating that gain of function or loss of function of the synaptic protein Bassoon may suppress or enhance autophagy through direct interaction with Atg5 (Okerlund et al., 2017; Vanhauwaert et al., 2017).”
Background
Self-eating to grow and kill: autophagy in filamentous ascomycetes
Voigt, O., & Pöggeler, S. (2013) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-013-5221-2 · Cited by 70
“Molecular analyses of autophagy have been mostly performed in the unicellular budding yeast Saccharomyces cerevisiae and in Pichia pastoris (Dunn et al. 2005; Nakatogawa et al. 2009; Ohsumi 2001; Reggiori and Klionsky 2013).”
Method
The roles of autophagy in development and stress responses in Arabidopsis thaliana
Lv, X., Pu, X., Qin, G., Zhu, T., & Lin, H. (2014) · APOPTOSIS · doi:10.1007/s10495-014-0981-4 · Cited by 70
“The bound ATG8 is then donated from ATG7 to the E2-conjugating enzyme ATG3 by transesterification, and finally attached to PE with the aid of an ATG8-specific E3 ligase complex [109].”
Background
Macroautophagy and Chaperone‐Mediated Autophagy in Heart Failure: The Known and the Unknown
Ghosh, R., & Pattison, J. S. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/8602041 · Cited by 72
Autosis
Nah, J., Zablocki, D., & Sadoshima, J. (2020) · JACC Basic to Translational Science · doi:10.1016/j.jacbts.2020.04.014 · Cited by 72
“The Atg5-Atg12/Atg16 complex localizes at expanding phagophores and acts as an E3-like ligase to conjugate another ubiquitin-like molecule, Atg8 (light chain 3-I), to phosphatidylethanolamine to form LC3 (MAP1LC3; a light chain of the microtubule-associated protein 1, ortholog of yeast Atg8), which is essential for ta…”
Background
The Pro-Survival Role of Autophagy Depends on Bcl-2 Under Nutrition Stress Conditions
Xu, H., Wu, D., Gu, J., Ge, J., Wu, J., Han, R., Liang, Z., & Qin, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063232 · Cited by 76
“LC3 is a homologue of Apg8p essential for autophagy in yeast [27].”
Background
A possible involvement of endoplasmic reticulum stress in biliary epithelial autophagy and senescence in primary biliary cirrhosis
Sasaki, M., Miyakoshi, M., Sato, Y., & Nakanuma, Y. (2014) · Journal of Gastroenterology · doi:10.1007/s00535-014-1033-0 · Cited by 70
Stimulation of hepatocytic AMP-activated protein kinase by okadaic acid and other autophagy-suppressive toxins
SAMARI, H. R., MØLLER, M. T. N., HOLDEN, L., ASMYHR, T., & SEGLEN, P. O. (2005) · Biochemical Journal · doi:10.1042/bj20040609 · Cited by 58
Increased expression of mitochondrial proteins associated with autophagy in biliary epithelial lesions in primary biliary cirrhosis
Sasaki, M., Miyakoshi, M., Sato, Y., & Nakanuma, Y. (2012) · Liver International · doi:10.1111/liv.12049 · Cited by 69
“This evolutionarily conserved process is characterized by the formation of double membrane cytosolic vesicles, autophagosomes, which sequester cytoplasmic content and deliver it to lysosomes (14, 15).”
Background
Wild-type rabies virus induces autophagy in human and mouse neuroblastoma cell lines
Peng, J., Zhu, S., Hu, L., Ye, P., Wang, Y., Qin, T., Mei, M., Chen, H., & Guo, X. (2016) · Autophagy · doi:10.1080/15548627.2016.1196315 · Cited by 70
Autophagic flux control in neurodegeneration: Progress and precision targeting—Where do we stand?
Lumkwana, D., du Toit, A., Kinnear, C. J., & Loos, B. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.03.006 · Cited by 69
“These are classified into the following groups: (1) the ULK1 kinase complex, (2) the ATG9 cycling complex, (3) the class III phosphatidylinositol 3-kinase (P3K)/Vps 34 complex I, (4) the phosphatidylinositol 3-phosphate (PI3P) binding ATG2-ATG18 complex and (5) the ATG12-ATG5 and ATG8/LC3 (microtubule-associated prote…”
Influential
Molecular machinery required for autophagy and the cytoplasm to vacuole targeting (Cvt) pathway in S. cerevisiae
Khalfan, W., & Klionsky, D. J. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00343-5 · Cited by 69
Enhancement in efferocytosis of oxidized low-density lipoprotein-induced apoptotic RAW264.7 cells through Sirt1-mediated autophagy
Liu, B., Zhang, B., Guo, R., Li, S., & Xu, Y. (2013) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2013.1609 · Cited by 68
“We also detected the expression of two separate autophagy proteins, Atg5 and Atg7, which were ultimately required for the formation of the autophagosome and the subsequent induction of autophagy (45-47).”
From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features
Reumann, S., Voitsekhovskaja, O. V., & Lillo, C. (2010) · PROTOPLASMA · doi:10.1007/s00709-010-0190-0 · Cited by 70
Autophagy and Related processes in Trypanosomatids: Insights from Genomic and Bioinformatic Analyses
Herman, M., Gillies, S., Michels, P. A. M., & Rigden, D. J. (2006) · Autophagy · doi:10.4161/auto.2.2.2369 · Cited by 67
Augmentation of Oridonin-Induced Apoptosis Observed With Reduced Autophagy
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Atg8L/Apg8L is the fourth mammalian modifier of mammalian Atg8 conjugation mediated by human Atg4B, Atg7 and Atg3
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NADPH oxidase activation is required for pentylenetetrazole kindling-induced hippocampal autophagy
Zhu, X., Shen, K., Bai, Y., Zhang, A., Xia, Z., Chao, J., & Yao, H. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.03.004 · Cited by 68
Xanthohumol Impairs Autophagosome Maturation through Direct Inhibition of Valosin-Containing Protein
Sasazawa, Y., Kanagaki, S., Tashiro, E., Nogawa, T., Muroi, M., Kondoh, Y., Osada, H., & Imoto, M. (2012) · ACS Chemical Biology · doi:10.1021/cb200492h · Cited by 69
Structure biology of selective autophagy receptors
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“sosomal fusion, have been extensively studied for the last 10 years (2, 4-16).”
Background
Impact of Paneth Cell Autophagy on Inflammatory Bowel Disease
Wang, S., Shao, B., Zhao, S., Fang, J., Gu, L., Miao, C., Li, Z., & Bai, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00693 · Cited by 72

Authors: Ohsumi, Y.
Affiliations: National Institute for Basic Biology (JP)
Corresponding author: Ohsumi, Yoshinori
ORCID: Ohsumi, Yoshinori
Venue: Nature Reviews Molecular Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2001-03
Volume: 2
Issue: 3
Pages: 211-216
ISSN: 1471-0072 (ISSN-L)
1471-0080
DOI: 10.1038/35056522
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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Molecular dissection of autophagy: two ubiquitin-like systems

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