The ATG conjugation systems are important for degradation of the inner autophagosomal membrane
Abstract
Open sesame!: The autophagosome is a double-membraned intracellular structure involved in the disposal of damaged or defunct organelles. Autophagosome formation requires a number of autophagy-related (ATG) proteins. Among them, the key conjugation systems ATG8 and ATG12 are widely exploited in the detection of autophagy in many organisms. However, their precise function in autophagy remains unknown. Tsuboyama et al. identified an unexpected role of ATG3, an important enzyme in the ATG conjugation systems, in efficient degradation and opening of the inner autophagosomal membrane after fusion with lysosomes (see the Perspective by Levine). Their live-imaging system revealed the entire life of an autophagosome in mammalian cells. Science , this issue p. 1036 ; see also p. 968
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
ATG conjugation systems including Atg7 are not absolutely essential for autophagosome formation.
“But, as to autophagosome formation, ATG conjugation systems including Atg7 are not absolutely essential13.”
From Loss of autophagy in dopaminergic neurons causes Lewy pathology and motor dysfunction in aged mice (2018) · cites this paper as [13]
Cites
Genome engineering using the CRISPR-Cas9 system
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013) · Nature Protocols · doi:10.1038/nprot.2013.143 · Cited by 11,133 · see citing works
LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., & Yoshimori, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.21.5720 · Cited by 6,605 · see citing works
Self-citationAutophagy: 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
Self-citationMethods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497 · see citing works
Self-citationThe role of autophagy during the early neonatal starvation period
Kuma, A., Hatano, M., Matsui, M., Yamamoto, A., Nakaya, H., Yoshimori, T., Ohsumi, Y., Tokuhisa, T., & Mizushima, N. (2004) · Nature · doi:10.1038/nature03029 · Cited by 2,865 · see citing works
Self-citationImpairment of starvation-induced and constitutive autophagy in <i>Atg7</i> -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 · see citing works
Self-citationA ubiquitin-like system mediates protein lipidation
Ichimura, Y., Kirisako, T., Takao, T., Satomi, Y., Shimonishi, Y., Ishihara, N., Mizushima, N., Tanida, I., Kominami, E., Ohsumi, M., et al. (2000) · Nature · doi:10.1038/35044114 · Cited by 2,064 · see citing works
Self-citationLoss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1β production
Saitoh, T., Fujita, N., Jang, M. H., Uematsu, S., Yang, B., Satoh, T., Omori, H., Noda, T., Yamamoto, N., Komatsu, M., et al. (2008) · Nature · doi:10.1038/nature07383 · Cited by 2,020 · see citing works
A protein conjugation system essential for autophagy
Mizushima, N., Noda, T., Yoshimori, T., Tanaka, Y., Ishii, T., George, M. D., Klionsky, D. J., Ohsumi, M., & Ohsumi, Y. (1998) · Nature · doi:10.1038/26506 · Cited by 1,701 · see citing works
Self-citationDissection of Autophagosome Formation Using Apg5-Deficient Mouse Embryonic Stem Cells
Mizushima, N., Yamamoto, A., Hatano, M., Kobayashi, Y., Kabeya, Y., Suzuki, K., Tokuhisa, T., Ohsumi, Y., & Yoshimori, T. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.4.657 · Cited by 1,361 · see citing works
Self-citationItakura, E., Kishi‐Itakura, C., & Mizushima, N. (2012) · Cell · doi:10.1016/j.cell.2012.11.001 · Cited by 1,327 · see citing works
Self-citationThe autophagosome: origins unknown, biogenesis complex
Lamb, C. A., Yoshimori, T., & Tooze, S. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3696 · Cited by 1,307 · see citing works
Beclin 1 Forms Two Distinct Phosphatidylinositol 3-Kinase Complexes with Mammalian Atg14 and UVRAG
Itakura, E., Kishi, C., Inoue, K., & Mizushima, N. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-01-0080 · Cited by 1,176 · see citing works
Self-citationDiscovery of Atg5/Atg7-independent alternative macroautophagy
Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., Komatsu, M., Otsu, K., Tsujimoto, Y., & Shimizu, S. (2009) · Nature · doi:10.1038/nature08455 · Cited by 1,103 · see citing works
Suzuki, K., Kirisako, T., Kamada, Y., Mizushima, N., Noda, T., & Ohsumi, Y. (2001) · The EMBO Journal · doi:10.1093/emboj/20.21.5971 · Cited by 1,034 · see citing works
Self-citationFormation Process of Autophagosome Is Traced with Apg8/Aut7p in Yeast
Kirisako, T., Baba, M., Ishihara, N., Miyazawa, K., Ohsumi, M., Yoshimori, T., Noda, T., & Ohsumi, Y. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.2.435 · Cited by 881 · see citing works
Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response
Saitoh, T., Fujita, N., Hayashi, T., Takahara, K., Satoh, T., Lee, H., Matsunaga, K., Kageyama, S., Omori, H., Noda, T., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911267106 · Cited by 854 · see citing works
The Nonparametric Behrens-Fisher Problem: Asymptotic Theory and a Small-Sample Approximation
Brunner, E., & Munzel, U. (2000) · Biometrical Journal · doi:10.1002/(sici)1521-4036(200001)42:1 · Cited by 630 · see citing works
An Atg4B Mutant Hampers the Lipidation of LC3 Paralogues and Causes Defects in Autophagosome Closure
Fujita, N., Hayashi, M., Fukumoto, H., Omori, H., Yamamoto, A., Noda, T., & Yoshimori, T. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-03-0312 · Cited by 527 · 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
Self-citationp62 targeting to the autophagosome formation site requires self-oligomerization but not LC3 binding
Itakura, E., & Mizushima, N. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201009067 · Cited by 418 · see citing works
Self-citationHosokawa, N., Hara, Y., & Mizushima, N. (2006) · FEBS Letters · doi:10.1016/j.febslet.2006.04.008 · Cited by 262 · see citing works
Self-citationTemporal analysis of recruitment of mammalian ATG proteins to the autophagosome formation site
Koyama‐Honda, I., Itakura, E., Fujiwara, T. K., & Mizushima, N. (2013) · Autophagy · doi:10.4161/auto.25529 · Cited by 234 · see citing works
Self-citationGan, B., Xu, P., Nagy, T., Alcaraz, A., Gu, H., & Guan, J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200604129 · Cited by 231 · see citing works
Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells
Kishi‐Itakura, C., Koyama‐Honda, I., Itakura, E., & Mizushima, N. (2014) · Journal of Cell Science · doi:10.1242/jcs.156034 · Cited by 227 · see citing works
Self-citationYoshimori, T., Yamagata, F., Yamamoto, A., Mizushima, N., Kabeya, Y., Nara, A., Miwako, I., Ohashi, M., Ohsumi, M., & Ohsumi, Y. (2000) · Molecular Biology of the Cell · doi:10.1091/mbc.11.2.747 · Cited by 190 · see citing works
Self-citationFIP200 regulates targeting of Atg16L1 to the isolation membrane
Nishimura, T., Kaizuka, T., Cadwell, K., Sahani, M. H., Saitoh, T., Akira, S., Virgin, H. W., & Mizushima, N. (2013) · EMBO Reports · doi:10.1038/embor.2013.6 · Cited by 185 · see citing works
Self-citationHuman Herpesvirus‐6 Induces MVB Formation, and Virus Egress Occurs by an Exosomal Release Pathway
Mori, Y., Koike, M., Moriishi, E., Kawabata, A., Tang, H., Oyaizu, H., Uchiyama, Y., & Yamanishi, K. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00796.x · Cited by 182 · see citing works
Self-citationThe late stages of autophagy: how does the end begin?
Noda, T., Fujita, N., & Yoshimori, T. (2009) · Cell Death and Differentiation · doi:10.1038/cdd.2009.54 · Cited by 178 · see citing works
Getting ready for building: signaling and autophagosome biogenesis
Abada, A., & Elazar, Z. (2014) · EMBO Reports · doi:10.15252/embr.201439076 · Cited by 171 · see citing works
Uemura, T., Yamamoto, M., Kametaka, A., Sou, Y., Yabashi, A., Yamada, A., Annoh, H., Kametaka, S., Komatsu, M., & Waguri, S. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01327-13 · Cited by 141 · see citing works
Atg13 Is Essential for Autophagy and Cardiac Development in Mice
Kaizuka, T., & Mizushima, N. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01005-15 · Cited by 106 · see citing works
Self-citationLoss of Atg12, but not Atg5, in pro-opiomelanocortin neurons exacerbates diet-induced obesity.
Malhotra, R., Warne, J. P., Salas, E., Xu, A. W., & Debnath, J. (2015) · PubMed Central · doi:10.1080/15548627.2014.998917 · Cited by 94 · see citing works
Autophagosome closure requires membrane scission
Knorr, R. L., Lipowsky, R., & Dimova, R. (2015) · Autophagy · doi:10.1080/15548627.2015.1091552 · Cited by 93 · see citing works
Lymphotoxin‐β receptor mediates NEMO‐independent NF‐κB activation
Saitoh, T., Nakano, H., Yamamoto, N., & Yamaoka, S. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03622-0 · Cited by 69 · see citing works
Role of the Atg9a gene in intrauterine growth and survival of fetal mice
Kojima, T., Yamada, T., Akaishi, R., Furuta, I., Saitoh, T., Nakabayashi, K., Nakayama, K., Nakayama, K., Akira, S., & Minakami, H. (2015) · Reproductive Biology · doi:10.1016/j.repbio.2015.05.001 · Cited by 44 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biological Functions of Autophagy Genes: A Disease Perspective
Levine, B., & Kroemer, G. (2019) · Cell · doi:10.1016/j.cell.2018.09.048 · Cited by 2,832 · see citing works
Mechanism and medical implications of mammalian autophagy
Dikic, I., & Elazar, Z. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0003-4 · Cited by 2,771 · see citing works
Klionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion
Mauthe, M., Orhon, I., Rocchi, C., Zhou, X., Luhr, M., Hijlkema, K.-J., Coppes, R. P., Engedal, N., Mari, M., & Reggiori, F. (2018) · Autophagy · doi:10.1080/15548627.2018.1474314 · Cited by 2,122 · see citing works
Molecular definitions of autophagy and related processes
Galluzzi, L., Baehrecke, E. H., Ballabio, A., Boya, P., Bravo‐San Pedro, J. M., Cecconi, F., Choi, A. M., Chu, C. T., Codogno, P., Colombo, M. I., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201796697 · Cited by 1,646 · see citing works
Self-citationAutophagy pathway: Cellular and molecular mechanisms
Yu, L., Chen, Y., & Tooze, S. A. (2017) · Autophagy · doi:10.1080/15548627.2017.1378838 · Cited by 1,488 · see citing works
Molecular mechanisms and physiological functions of mitophagy
Onishi, M., Yamano, K., Sato, M., Matsuda, N., & Okamoto, K. (2021) · The EMBO Journal · doi:10.15252/embj.2020104705 · Cited by 1,429 · see citing works
Autophagy and autophagy-related pathways in cancer
Debnath, J., Gammoh, N., & Ryan, K. M. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00585-z · Cited by 1,443 · see citing works
Monitoring and Measuring Autophagy
Yoshii, S. R., & Mizushima, N. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18091865 · Cited by 1,107 · see citing works
Self-citationAutophagy-Independent Functions of the Autophagy Machinery
Galluzzi, L., & Green, D. R. (2019) · Cell · doi:10.1016/j.cell.2019.05.026 · Cited by 863 · see citing works
“This latter step, which appears to involve (at least to some extent) the conjugation systems responsible for elongation (Tsuboyama et al., 2016), is critical to discriminate bona fide autophagic responses from autophagy-independent functions of the autophagic machinery (Galluzzi et al.”
BackgroundMechanisms governing autophagosome biogenesis
Nakatogawa, H. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0241-0 · Cited by 876 · see citing works
Pharmacological modulation of autophagy: therapeutic potential and persisting obstacles
Galluzzi, L., Bravo-San Pedro, J. M., Levine, B., Green, D. R., & Kroemer, G. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.22 · Cited by 842 · see citing works
Yim, W. W., & Mizushima, N. (2020) · Cell Discovery · doi:10.1038/s41421-020-0141-7 · Cited by 800 · see citing works
Self-citationSelective Autophagy: ATG8 Family Proteins, LIR Motifs and Cargo Receptors
Johansen, T., & Lamark, T. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.07.016 · Cited by 700 · see citing works
A brief history of autophagy from cell biology to physiology and disease
Mizushima, N. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0092-5 · Cited by 696 · see citing works
Self-citationBuilding and decoding ubiquitin chains for mitophagy
Harper, J. W., Ordureau, A., & Heo, J. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.129 · Cited by 668 · see citing works
Nguyen, T. N., Padman, B. S., Usher, J. L., Oorschot, V. M. J., Ramm, G., & Lazarou, M. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201607039 · Cited by 649 · see citing works
Autophagy genes in biology and disease
Yamamoto, H., Zhang, S., & Mizushima, N. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-022-00562-w · Cited by 631 · see citing works
Self-citationMachinery, regulation and pathophysiological implications of autophagosome maturation
Zhao, Y. G., Codogno, P., & Zhang, H. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00392-4 · Cited by 574 · see citing works
Promoting the clearance of neurotoxic proteins in neurodegenerative disorders of ageing
Boland, B., Yu, W. H., Corti, O., Mollereau, B., Henriques, A., Bézard, E., Pastores, G., Rubinsztein, D. C., Nixon, R. A., Duchen, M. R., et al. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.109 · Cited by 552 · see citing works
The Role of Autophagy in the Heart
Sciarretta, S., Maejima, Y., Zablocki, D., & Sadoshima, J. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121427 · Cited by 547 · see citing works
A Diversity of Selective Autophagy Receptors Determines the Specificity of the Autophagy Pathway
Kirkin, V., & Rogov, V. V. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.09.005 · Cited by 524 · see citing works
New insights into autophagosome–lysosome fusion
Nakamura, S., & Yoshimori, T. (2017) · Journal of Cell Science · doi:10.1242/jcs.196352 · Cited by 520 · see citing works
Selective autophagy of intracellular organelles: Recent research advances
Li, W., He, P., Huang, Y., Li, Y.-F., Lu, J., Li, M., Kurihara, H., Luo, Z., Meng, T., Onishi, M., et al. (2020) · Theranostics · doi:10.7150/thno.49860 · Cited by 510 · see citing works
The ATG conjugation systems in autophagy
Mizushima, N. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.12.001 · Cited by 481 · see citing works
Self-citationNecrotic, apoptotic and autophagic cell fates triggered by nanoparticles
Mohammadinejad, R., Moosavi, M. A., Tavakol, S., Vardar, D. Ö., Hosseini, A., Rahmati, M., Dini, L., Hussain, S., Mandegary, A., & Klionsky, D. J. (2018) · Autophagy · doi:10.1080/15548627.2018.1509171 · Cited by 464 · see citing works
Smith, M. D., Harley, M. E., Kemp, A. J., Wills, J. C., Lee, M. W., Arends, M. J., von Kriegsheim, A., Behrends, C., & Wilkinson, S. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.024 · Cited by 443 · see citing works
Mechanisms of Selective Autophagy
Lamark, T., & Johansen, T. (2021) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120219-035530 · Cited by 429 · see citing works
Crosstalk Between Mammalian Autophagy and the Ubiquitin-Proteasome System
Kocatürk, N. M., & Gözüaçık, D. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00128 · Cited by 415 · see citing works
Diverse Cellular Roles of Autophagy
Morishita, H., & Mizushima, N. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100818-125300 · Cited by 376 · see citing works
Self-citationAutophagy as a molecular target for cancer treatment
Kocatürk, N. M., Akkoç, Y., Kığ, C., Bayraktar, O., Gözüaçık, D., & Kutlu, Ö. (2019) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2019.04.011 · Cited by 388 · see citing works
Matsuzawa, Y., Hwang, S., & Cadwell, K. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-042617-053253 · Cited by 378 · see citing works
Autophagosome maturation: An epic journey from the ER to lysosomes
Zhao, Y. G., & Zhang, H. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201810099 · Cited by 362 · see citing works
Autophagy and disease: unanswered questions
Yang, Y., & Klionsky, D. J. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-019-0480-9 · Cited by 369 · see citing works
Intrinsically Disordered Protein TEX264 Mediates ER-phagy
Chino, H., Hatta, T., Natsume, T., & Mizushima, N. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.03.033 · Cited by 362 · see citing works
Self-citationAn autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure
Takahashi, Y., He, H., Tang, Z., Hattori, T., Liu, Y., Young, M. M., Serfass, J. M., Chen, L., Gebru, M. T., Chen, C., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05254-w · Cited by 365 · see citing works
Stavoe, A. K. H., & Holzbaur, E. L. F. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100818-125242 · Cited by 328 · see citing works
Autophagy-monitoring and autophagy-deficient mice
Kuma, A., Komatsu, M., & Mizushima, N. (2017) · Autophagy · doi:10.1080/15548627.2017.1343770 · Cited by 336 · see citing works
Self-citationDedicated SNAREs and specialized TRIM cargo receptors mediate secretory autophagy
Kimura, T., Jia, J., Kumar, S. G., Choi, S. W., Gu, Y., Mudd, M. H., Dupont, N., Jiang, S., Peters, R. S., Farzam, F., et al. (2016) · The EMBO Journal · doi:10.15252/embj.201695081 · Cited by 329 · see citing works
Autophagosome biogenesis: From membrane growth to closure
Melia, T. J., Lystad, A. H., & Simonsen, A. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.202002085 · Cited by 324 · see citing works
Lőrincz, P., & Juhász, G. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.10.028 · Cited by 328 · see citing works
PINK1 and Parkin: emerging themes in mitochondrial homeostasis.
McWilliams, T. G., & Muqit, M. (2017) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2017.03.013 · Cited by 315 · see citing works
Structure, lipid scrambling activity and role in autophagosome formation of ATG9A
Maeda, S., Yamamoto, H., Kinch, L. N., Garza, C. M., Takahashi, S., Otomo, C., Grishin, N. V., Forli, S., Mizushima, N., & Otomo, T. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-00520-2 · Cited by 305 · see citing works
Self-citationAn, H., Ordureau, A., Paulo, J. A., Shoemaker, C. J., Denic, V., & Harper, J. W. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.03.034 · Cited by 287 · see citing works
Kageyama, S., Gudmundsson, S. R., Sou, Y., Ichimura, Y., Tamura, N., Kazuno, S., Ueno, T., Miura, Y., Noshiro, D., Abe, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20185-1 · Cited by 290 · see citing works
Wetting regulates autophagy of phase-separated compartments and the cytosol
Agudo‐Canalejo, J., Schultz, S. W., Chino, H., Migliano, S. M., Saito, C., Koyama‐Honda, I., Stenmark, H., Brech, A., May, A. I., Mizushima, N., et al. (2021) · Nature · doi:10.1038/s41586-020-2992-3 · Cited by 275 · see citing works
Self-citationMitochondrial degradation: Mitophagy and beyond
Uoselis, L., Nguyen, T. N., & Lazarou, M. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.08.021 · Cited by 270 · see citing works
New insights regarding SNARE proteins in autophagosome-lysosome fusion
Tian, X., Teng, J., & Chen, J. (2020) · Autophagy · doi:10.1080/15548627.2020.1823124 · Cited by 257 · see citing works
Autophagosomal YKT6 is required for fusion with lysosomes independently of syntaxin 17
Matsui, T., Jiang, P., Nakano, S., Sakamaki, Y., Yamamoto, H., & Mizushima, N. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201712058 · Cited by 256 · see citing works
Self-citationRedundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells
Agrotis, A., Pengo, N., Burden, J. J., & Ketteler, R. (2019) · Autophagy · doi:10.1080/15548627.2019.1569925 · Cited by 239 · see citing works
Autophagosome Maturation and Fusion
Reggiori, F., & Ungermann, C. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.01.002 · Cited by 235 · see citing works
LC3/GABARAPs drive ubiquitin-independent recruitment of Optineurin and NDP52 to amplify mitophagy
Padman, B. S., Nguyen, T. N., Uoselis, L., Skulsuppaisarn, M., Nguyen, L. K., & Lazarou, M. (2019) · Nature Communications · doi:10.1038/s41467-019-08335-6 · Cited by 234 · see citing works
Reggiori, F., & Molinari, M. (2022) · Physiological Reviews · doi:10.1152/physrev.00038.2021 · Cited by 220 · see citing works
Chowdhury, S., Otomo, C., Leitner, A., Ohashi, K., Aebersold, R. H., Lander, G. C., & Otomo, T. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1811874115 · Cited by 219 · see citing works
Outstanding Questions in Mitophagy: What We Do and Do Not Know
Montava‐Garriga, L., & Ganley, I. G. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.032 · Cited by 209 · see citing works
Iorio, R., Celenza, G., & Petricca, S. (2021) · Cells · doi:10.3390/cells11010030 · Cited by 218 · see citing works
Puri, C., Vicinanza, M., Ashkenazi, A., Gratian, M. J., Zhang, Q., Bento, C. F., Renna, M., Menzies, F. M., & Rubinsztein, D. C. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.03.008 · Cited by 206 · see citing works
Activation and targeting of ATG8 protein lipidation
Martens, S., & Fracchiolla, D. (2020) · Cell Discovery · doi:10.1038/s41421-020-0155-1 · Cited by 206 · see citing works
Critical role of mitochondrial ubiquitination and the OPTN–ATG9A axis in mitophagy
Yamano, K., Kikuchi, R., Kojima, W., Hayashida, R., Koyano, F., Kawawaki, J., Shoda, T., Demizu, Y., Naito, M., Tanaka, K., et al. (2020) · Journal of Cell Biology · doi:10.1083/jcb.201912144 · Cited by 205 · see citing works
Oxidation of Atg3 and Atg7 mediates inhibition of autophagy
Frudd, K., Burgoyne, T., & Burgoyne, J. R. (2018) · Nature Communications · doi:10.1038/s41467-017-02352-z · Cited by 202 · see citing works
Emerging roles of ATG7 in human health and disease
Collier, J. J., Suomi, F., Oláhová, M., McWilliams, T. G., & Taylor, R. W. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202114824 · Cited by 191 · see citing works
Developmental Consequences of Defective ATG7-Mediated Autophagy in Humans
Collier, J. J., Guissart, C., Oláhová, M., Sasorith, S., Piron‐Prunier, F., Suomi, F., Zhang, D., Martinez-Lopez, N., Leboucq, N., Bahr, A., et al. (2021) · New England Journal of Medicine · doi:10.1056/nejmoa1915722 · Cited by 193 · see citing works
Systematic analysis of ribophagy in human cells reveals bystander flux during selective autophagy
An, H., & Harper, J. W. (2018) · Nature Cell Biology · doi:10.1038/s41556-017-0007-x · Cited by 181 · see citing works
Accumulation of autophagosomes confers cytotoxicity
Button, R. W., Roberts, S. L., Willis, T. L., Hanemann, C. O., & Luo, S. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.782276 · Cited by 179 · see citing works
Dysregulation of autophagy as a common mechanism in lysosomal storage diseases
Seranova, E., Connolly, K. J., Zatyka, M., Rosenstock, T. R., Barrett, T. G., Tuxworth, R. I., & Sarkar, S. (2017) · Essays in Biochemistry · doi:10.1042/ebc20170055 · Cited by 175 · see citing works
Crosstalk between cGAS–STING signaling and cell death
Murthy, A. M. V., Robinson, N., & Kumar, S. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00624-8 · Cited by 170 · see citing works
Molecular mechanisms and physiological roles of Atg5/Atg7-independent alternative autophagy
Arakawa, S., Honda, S., Yamaguchi, H., & Shimizu, S. (2017) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.93.023 · Cited by 172 · see citing works
Autophagy and endocytosis – interconnections and interdependencies
Birgisdottir, Å. B., & Johansen, T. (2020) · Journal of Cell Science · doi:10.1242/jcs.228114 · Cited by 170 · see citing works
Autophagosome biogenesis comes out of the black box
Chang, C., Jensen, L. E., & Hurley, J. H. (2021) · Nature Cell Biology · doi:10.1038/s41556-021-00669-y · Cited by 171 · see citing works
Endosomal Rab cycles regulate Parkin-mediated mitophagy
Yamano, K., Wang, C., Sarraf, S. A., Münch, C., Kikuchi, R., Noda, N. N., Hizukuri, Y., Kanemaki, M. T., Harper, J. W., Tanaka, K., et al. (2018) · eLife · doi:10.7554/elife.31326 · Cited by 172 · see citing works
Mechanism of Stx17 recruitment to autophagosomes via IRGM and mammalian Atg8 proteins
Kumar, S., Jain, A., Farzam, F., Jia, J., Gu, Y., Choi, S. W., Mudd, M. H., Claude‐Taupin, A., Wester, M. J., Lidke, K. A., et al. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201708039 · Cited by 161 · see citing works
Emerging degrader technologies engaging lysosomal pathways
Ding, Y., Xing, D., Fei, Y., & Lu, B. (2022) · Chemical Society Reviews · doi:10.1039/d2cs00624c · Cited by 162 · see citing works
Davies, A. K., Itzhak, D. N., Edgar, J. R., Archuleta, T. L., Hirst, J., Jackson, L. P., Robinson, M. S., & Borner, G. H. H. (2018) · Nature Communications · doi:10.1038/s41467-018-06172-7 · Cited by 153 · see citing works
Autophagosomal Content Profiling Reveals an LC3C-Dependent Piecemeal Mitophagy Pathway
Guerroué, F. L., Eck, F., Jung, J., Starzetz, T., Mittelbronn, M. G. A., Kaulich, M., & Behrends, C. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.10.029 · Cited by 150 · see citing works
Choi, M. E. (2019) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021119-034658 · Cited by 150 · see citing works
Shoemaker, C. J., Huang, T. Q., Weir, N. R., Polyakov, N. J., Schultz, S. W., & Denic, V. (2019) · PLoS Biology · doi:10.1371/journal.pbio.2007044 · Cited by 145 · see citing works
Huang, Q., Liu, Y., Zhang, S., Yap, Y. T., Li, W., Zhang, D., Gardner, A., Zhang, L., Song, S., Hess, R. A., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1783822 · Cited by 144 · see citing works
A pulse-chasable reporter processing assay for mammalian autophagic flux with HaloTag
Yim, W. W., Yamamoto, H., & Mizushima, N. (2022) · eLife · doi:10.7554/elife.78923 · Cited by 144 · see citing works
Self-citationHistory of the Selective Autophagy Research: How Did It Begin and Where Does It Stand Today?
Kirkin, V. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.010 · Cited by 139 · see citing works
Acetylation of STX17 (syntaxin 17) controls autophagosome maturation
Shen, Q., Shi, Y. P., Liu, J., Su, H., Huang, J., Zhang, Y., Peng, C., Zhou, T., Sun, Q., Wan, W., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1752471 · Cited by 143 · see citing works
Mitochondrial-derived vesicles compensate for loss of LC3-mediated mitophagy
Towers, C. G., Wodetzki, D., Thorburn, J., Smith, K. R., Caino, M. C., & Thorburn, A. M. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.06.003 · Cited by 143 · see citing works
NCOA4 drives ferritin phase separation to facilitate macroferritinophagy and microferritinophagy
Ohshima, T., Yamamoto, H., Sakamaki, Y., Saito, C., & Mizushima, N. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202203102 · Cited by 143 · see citing works
Self-citationVaites, L. P., Paulo, J. A., Huttlin, E. L., & Harper, J. W. (2017) · Molecular and Cellular Biology · doi:10.1128/mcb.00392-17 · Cited by 136 · see citing works
Autophagy and cancer: Modulation of cell death pathways and cancer cell adaptations
Towers, C. G., Wodetzki, D., & Thorburn, A. M. (2019) · The Journal of Cell Biology · doi:10.1083/jcb.201909033 · Cited by 139 · see citing works
STX17 dynamically regulated by Fis1 induces mitophagy via hierarchical macroautophagic mechanism
Xian, H., Yang, Q., Xiao, L., Shen, H., & Liou, Y. (2019) · Nature Communications · doi:10.1038/s41467-019-10096-1 · Cited by 135 · see citing works
Goodwin, J. M., Walkup, W. G., Hooper, K. M., Li, T., Kishi‐Itakura, C., Ng, A., Lehmberg, T. Z., Jha, A., Kommineni, S., Fletcher, K., et al. (2021) · Science Advances · doi:10.1126/sciadv.abj2485 · Cited by 130 · see citing works
Role of autophagy in Zika virus infection and pathogenesis
Chiramel, A. I., & Best, S. M. (2017) · Virus Research · doi:10.1016/j.virusres.2017.09.006 · Cited by 127 · see citing works
Beyond Autophagy: The Expanding Roles of ATG8 Proteins
Nieto-Torres, J. L., Leidal, A. M., Debnath, J., & Hansen, M. (2021) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2021.01.004 · Cited by 128 · see citing works
Loss of autophagy in dopaminergic neurons causes Lewy pathology and motor dysfunction in aged mice
Sato, S., Uchihara, T., Fukuda, T., Noda, S., Kondo, H., Saiki, S., Komatsu, M., Uchiyama, Y., Tanaka, K., & Hattori, N. (2018) · Scientific Reports · doi:10.1038/s41598-018-21325-w · Cited by 125 · see citing works
AMPK: a key regulator of energy stress and calcium-induced autophagy
Saikia, R., & Joseph, J. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-021-02125-8 · Cited by 125 · see citing works
Mammalian mitophagy – from in vitro molecules to in vivo models
Rodger, C. E., McWilliams, T. G., & Ganley, I. G. (2017) · FEBS Journal · doi:10.1111/febs.14336 · Cited by 121 · see citing works
Role and mechanism of autophagy‐regulating factors in tumorigenesis and drug resistance
Usman, R. M., Razzaq, F., Akbar, A., Farooqui, A. A., Iftikhar, A., Latif, A., Hassan, H., Zhao, J., Carew, J. S., Nawrocki, S. T., et al. (2020) · Asia-Pacific Journal of Clinical Oncology · doi:10.1111/ajco.13449 · Cited by 120 · see citing works
Targeted Protein Degradation via Lysosomes
Paudel, R. R., Lu, D., Chowdhury, S. R., Monroy, E. Y., & Wang, J. (2022) · Biochemistry · doi:10.1021/acs.biochem.2c00310 · Cited by 120 · see citing works
Emerging Principles of Selective ER Autophagy
Wilkinson, S. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.05.012 · Cited by 117 · see citing works
Fujita, N., Huang, W., Lin, T.-H., Groulx, J., Jean, S., Nguyen, J., Kuchitsu, Y., Koyama‐Honda, I., Mizushima, N., Fukuda, M., et al. (2017) · eLife · doi:10.7554/elife.23367 · Cited by 114 · see citing works
Self-citationNwadike, C., Williamson, L. E., Gallagher, L. E., Guan, J., & Chan, E. Y. W. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00023-18 · Cited by 113 · see citing works
LC3 subfamily in cardiolipin-mediated mitophagy: a comparison of the LC3A, LC3B and LC3C homologs
Iriondo, M. N., Etxaniz, A., Varela, Y. R., Ballesteros, U., Hervás, J. H., Montes, L. R., Goñi, F. M., & Alonso, A. (2022) · Autophagy · doi:10.1080/15548627.2022.2062111 · Cited by 113 · see citing works
Receptor‐mediated clustering of FIP200 bypasses the role of LC3 lipidation in autophagy
Ohnstad, A. E., Delgado, J. M., North, B. J., Nasa, I., Kettenbach, A. N., Schultz, S. W., & Shoemaker, C. J. (2020) · The EMBO Journal · doi:10.15252/embj.2020104948 · Cited by 111 · see citing works
Tan, H. W. S., Lu, G. X., Dong, H., Cho, Y.-L., Natalia, A., Wang, L., Chan, C., Kappei, D., Taneja, R., Ling, S., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31213-7 · Cited by 112 · see citing works
Membrane Trafficking in Autophagy
Søreng, K., Neufeld, T. P., & Simonsen, A. (2017) · International review of cytology · doi:10.1016/bs.ircmb.2017.07.001 · Cited by 110 · see citing works
- Authors
- Tsuboyama, K., Koyama-Honda, I., Sakamaki, Y., Koike, M., Morishita, H., & Mizushima, N.
- Affiliations
- The University of Tokyo (JP)
- Department of Biochemistry and Molecular Biology, Graduate School and Faculty of Medicine, The University of Tokyo, Tokyo 113-0033, Japan.
- Tokyo Medical and Dental University (JP)
- Juntendo University (JP)
- Corresponding author
- Tsuboyama, Kotaro
- Mizushima, Noboru
- Venue
- Science
- Published
- 2016-11-25
- Volume
- 354
- Issue
- 6315
- Pages
- 1036-1041
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W2533025094
- Cited by
- 485
- References
- 36
- Citations by year
- 2026: 25 · 2025: 30 · 2024: 55 · 2023: 39 · 2022: 50 · 2021: 64 · 2020: 69 · 2019: 57 · 2018: 47 · 2017: 43 · 2016: 6
- FWCI
- 47.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- macroautophagy, autophagosome formation, STX17, autophagosome-lysosome fusion, autophagy-related proteins
- MeSH terms
- Autophagosomes, Autophagy-Related Protein 8 Family, Autophagy-Related Protein 12, Autophagy, HeLa Cells, Humans, Intracellular Membranes, Lysosomes, Membrane Fusion, Phosphatidylethanolamines, Qa-SNARE Proteins, HEK293 Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review