LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation
Abstract
Rat LC3, a homologue of yeast Atg8 (Aut7/Apg8), localizes to autophagosomal membranes after post-translational modifications. The C-terminal fragment of LC3 is cleaved immediately following synthesis to yield a cytosolic form called LC3-I. A subpopulation of LC3-I is further converted to an autophagosome-associating form, LC3-II. Because yeast Atg8 is conjugated with phosphatidylethanolamine (PE) by a ubiquitin-like system, it has been hypothesized that LC3 is modified in a similar manner. Here, we show that [(14)C]-ethanolamine was preferentially incorporated into LC3-II, suggesting that LC3-II is a PE-conjugated form. LC3-II can be a substrate of mammalian Atg4B, a homologue of yeast Atg8-PE deconjugase, supporting the idea that LC3-II is LC3-PE. Moreover, two other mammalian homologues of yeast Atg8, gamma-aminobutyric-acid-type-A-receptor-associated protein (GABARAP) and Golgi-associated ATPase enhancer of 16 kDa (GATE16) also generate form II, which are recovered in membrane fractions. Generation of the form II correlates with autophagosome association of GABARAP and GATE16. These results suggest that all mammalian Atg8 homologues receive a common modification to associate with autophagosomal membrane as the form II.
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The second GABARAP/GATE subfamily comprises GABARAP, GABARAPL1, GATE-16 (aka GABARAPL2) and GABARAP-L3.
“The second, the GABARAP/GATE subfamily, comprises GABARAP, GABARAPL1, GATE-16 (aka GABARAPL2) and GABARAP-L3 [29,30].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [30]
Lipidation of LC3-family proteins is required for recycling of TLR4, TREM2, and CD36.
“The requirement for ATG4, which converts LC3 to LC3-I (Kabeya et al., 2004) and the effect of RavZ, which irreversibly cleaves lipidated LC3 (Choy et al., 2012; Kwon et al., 2017), strongly suggest that lipidation of LC3-family proteins is required for recycling of these receptors.”
From LC3-Associated Endocytosis Facilitates β-Amyloid Clearance and Mitigates Neurodegeneration in Murine Alzheimer’s Disease (2019) · cites this paper as Kabeya et al., 2004
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1 retracted
Mariño, G., Urı́a, J. A., Puente, X. S., Quesada, V., Bordallo, J., & López-Otı́n, C. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208247200 · Cited by 208 · see citing works
RetractedLC3, 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-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-citationA 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-citationMolecular dissection of autophagy: two ubiquitin-like systems
Ohsumi, Y. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35056522 · Cited by 1,240 · cited 1× · see citing works
“Atg8 is post-translationally modified by a ubiquitylation-like system (Ohsumi, 2001).”
BackgroundSelf-citationSuzuki, 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-citationKirisako, T., Ichimura, Y., Okada, H., Kabeya, Y., Mizushima, N., Yoshimori, T., Ohsumi, M., Takao, T., Noda, T., & Ohsumi, Y. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.2.263 · Cited by 983 · 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 · cited 3× · see citing works
“Arrow indicates the cleavage site in yeast Atg8 by Aut2/Atg4 (Kirisako et al., 1999).”
BackgroundInfluentialSelf-citationMizushima, 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-citationGABAA-receptor-associated protein links GABAA receptors and the cytoskeleton
Wang, H., Bedford, F. K., Brandon, N. J., Moss, S. J., & Olsen, R. W. (1999) · Nature · doi:10.1038/16264 · Cited by 733 · see citing works
A New Protein Conjugation System in Human
Mizushima, N., Sugita, H., Yoshimori, T., & Ohsumi, Y. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.51.33889 · Cited by 521 · see citing works
Self-citationTanida, I., Tanida-Miyake, E., Ueno, T., & Kominami, E. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.c000752200 · Cited by 343 · see citing works
Tanaka, K., Nakafuku, M., Tamanoi, F., Kaziro, Y., Matsumoto, K., & Toh‐e, A. (1990) · Molecular and Cellular Biology · doi:10.1128/mcb.10.8.4303 · Cited by 292 · see citing works
Tanida, I., Tanida-Miyake, E., Komatsu, M., Ueno, T., & Kominami, E. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200385200 · Cited by 286 · see citing works
Molecular characterization of light chain 3. A microtubule binding subunit of MAP1A and MAP1B
Mann, S. S., & Hammarback, J. A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)78150-2 · Cited by 284 · see citing works
He, H., Dang, Y., Dai, F., Guo, Z., Wu, J., She, X., Pei, Y., Chen, Y., Ling, W., Wu, C., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303800200 · Cited by 273 · see citing works
Hemelaar, J., Lelyveld, V. S., Kessler, B. M., & Ploegh, H. L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308762200 · Cited by 247 · see citing works
GATE‐16, a membrane transport modulator, interacts with NSF and the Golgi v‐SNARE GOS‐28
Sagiv, Y., Legesse‐Miller, A., Porat, A., & Elazar, Z. (2000) · The EMBO Journal · doi:10.1093/emboj/19.7.1494 · Cited by 240 · see citing works
Kittler, J. T., Rostaing, P., Schiavo, G., Fritschy, J., Olsen, R. W., Triller, A., & Moss, S. J. (2001) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1005 · Cited by 227 · see citing works
Chen, L., Wang, H., Vicini, S., & Olsen, R. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.190133497 · Cited by 207 · see citing works
Yoshimori, 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-citationKneussel, M., Haverkamp, S., Fuhrmann, J. C., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.15.8594 · Cited by 176 · see citing works
Wang, H., & Olsen, R. W. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750644.x · Cited by 155 · see citing works
Xin, Y., Yu, L., Chen, Z., Zheng, L., Fu, Q., Jiang, J., Zhang, P., Gong, R., & Zhao, S. (2001) · Genomics · doi:10.1006/geno.2001.6555 · Cited by 113 · see citing works
GATE-16 and GABARAP are authentic modifiers mediated by Apg7 and Apg3
Tanida, I., Komatsu, M., Ueno, T., et al. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02907-8 · Cited by 99 · see citing works
Phosphatidylserine synthase I and II of mammalian cells
Kuge, O., & Nishijima, M. (1997) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/s0005-2760(97)00137-9 · Cited by 96 · see citing works
Scherz‐Shouval, R., Sagiv, Y., Shorer, H., & Elazar, Z. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m212108200 · Cited by 79 · see citing works
Mizushima, N., Yoshimori, T., & Ohsumi, Y. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03739-0 · Cited by 48 · see citing works
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Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Self-citationPankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J.-A., Outzen, H., Øvervatn, A., Bjørkøy, G., & Johansen, T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m702824200 · Cited by 4,578 · see citing works
Guidelines for the use and interpretation of assays for monitoring autophagy
Klionsky, D. J., Abdalla, F. C., Abeliovich, H., Abraham, R. T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J. A., et al. (2012) · Autophagy · doi:10.4161/auto.19496 · Cited by 3,996 · see citing works
Self-citationChemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury
Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G. D., Mitchison, T. J., Moskowitz, M. A., & Yuan, J. (2005) · Nature Chemical Biology · doi:10.1038/nchembio711 · Cited by 3,068 · 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-citationKlionsky, 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
Self-citationAn Overview of Autophagy: Morphology, Mechanism, and Regulation
Parzych, K. R., & Klionsky, D. J. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5371 · Cited by 2,521 · see citing works
How to Interpret LC3 Immunoblotting
Mizushima, N., & Yoshimori, T. (2007) · Autophagy · doi:10.4161/auto.4600 · Cited by 2,595 · 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-citationReactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4
Scherz‐Shouval, R., Shvets, E., Fass, E., Shorer, H., Gil, L., & Elazar, Z. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601623 · Cited by 2,101 · see citing works
Jung, C. H., Ro, S.-H., Cao, J., Otto, N. M., & Kim, D.-H. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.01.017 · Cited by 2,090 · see citing works
The machinery of macroautophagy
Feng, Y., He, D., Yao, Z., & Klionsky, D. J. (2014) · Cell Research · doi:10.1038/cr.2013.168 · Cited by 2,083 · see citing works
ULK-Atg13-FIP200 Complexes Mediate mTOR Signaling to the Autophagy Machinery
Jung, C. H., Jun, C. B., Ro, S.-H., Kim, Y.-M., Otto, N. M., Cao, J., Kundu, M., & Kim, D.-H. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-12-1249 · Cited by 2,025 · see citing works
Autophagy Is Activated for Cell Survival after Endoplasmic ReticulumStress
Ogata, M., Hino, S.-I., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., Murakami, T., Taniguchi, M., Tanii, I., Yoshinaga, K., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.01453-06 · Cited by 1,832 · see citing works
Tanida, I., Ueno, T., & Kominami, E. (2008) · Methods in Molecular Biology™ · doi:10.1007/978-1-59745-157-4_4 · Cited by 1,785 · see citing works
Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling.
Lee, J., Giordano, S., & Zhang, J. (2012) · Biochemical Journal · doi:10.1042/bj20111451 · Cited by 1,438 · see citing works
Essential role for Nix in autophagic maturation of erythroid cells
Sandoval, H., Thiagarajan, P., Dasgupta, S. K., Schumacher, A., Prchal, J. T., Chen, M., & Wang, J. (2008) · Nature · doi:10.1038/nature07006 · Cited by 1,185 · see citing works
Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy
Tanida, I., Minematsu-Ikeguchi, N., Ueno, T., & Kominami, E. (2005) · Autophagy · doi:10.4161/auto.1.2.1697 · Cited by 1,108 · see citing works
Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N., & Yue, Z. (2009) · Nature Cell Biology · doi:10.1038/ncb1854 · Cited by 1,005 · see citing works
Macroautophagy—a novel β-amyloid peptide-generating pathway activated in Alzheimer's disease
Yu, W. H., Cuervo, A. M., Kumar, A., Peterhoff, C. M., Schmidt, S. D., Lee, J.-H., Mohan, P. S., Mercken, M., Farmery, M. R., Tjernberg, L. O., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200505082 · Cited by 967 · see citing works
Neutrophil extracellular trap cell death requires both autophagy and superoxide generation
Remijsen, Q., Berghe, T. V., Wirawan, E., Asselbergh, B., Parthoens, E., De Rycke, R., Noppen, S., Delforge, M., Willems, J., & Vandenabeele, P. (2011) · Cell Research · doi:10.1038/cr.2010.150 · Cited by 818 · 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
Ubiquitination and selective autophagy
Shaid, S., Brandts, C. H., Serve, H., & Dikic, I. (2013) · Cell Death & Differentiation · doi:10.1038/cdd.2012.72 · Cited by 800 · see citing works
Martinez, J., Malireddi, R. K. S., Lu, Q., Cunha, L. D., Pelletier, S., Gingras, S., Orchard, R., Guan, J.-L., Tan, H., Peng, J., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3192 · Cited by 758 · see citing works
“Members of all three families have been identified on autophagosomes 37 .”
RetractedHanna, R. A., Quinsay, M. N., Orogo, A. M., Giang, K., Rikka, S., & Gustafsson, Å. B. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.322933 · Cited by 762 · see citing works
Combination of ERK and autophagy inhibition as a treatment approach for pancreatic cancer
Bryant, K. L., Stalnecker, C. A., Zeitouni, D., Klomp, J. E., Peng, S., Tikunov, A. P., Gunda, V., Pierobon, M., Waters, A. M., George, S. D., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0368-8 · Cited by 692 · see citing works
Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerød, L., Fisher, E. M. C., Isaacs, A., Brech, A., Stenmark, H., & Simonsen, A. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200702115 · Cited by 626 · see citing works
Self-citationBharath, L. P., Agrawal, M., McCambridge, G., Nicholas, D. A., Hasturk, H., Liu, J., Jiang, K., Liu, R., Guo, Z., Deeney, J., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.04.015 · Cited by 614 · see citing works
Wenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M., & Moraes, C. T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911570106 · Cited by 600 · see citing works
RetractedKuma, A., Matsui, M., & Mizushima, N. (2007) · Autophagy · doi:10.4161/auto.4012 · Cited by 555 · see citing works
Self-citationAtg8: an autophagy-related ubiquitin-like protein family.
Shpilka, T., Weidberg, H., Pietrokovski, S., & Elazar, Z. (2011) · Genome biology · doi:10.1186/gb-2011-12-7-226 · Cited by 543 · see citing works
“Although mammalian Atg8 proteins were originally implicated in intracellular trafficking processes, they are all found within autophagosomes [73-75].”
BackgroundHeckmann, B. L., Teubner, B. J. W., Tummers, B., Boada-Romero, E., Harris, L., Yang, M., Guy, C. S., Zakharenko, S. S., & Green, D. R. (2019) · Cell · doi:10.1016/j.cell.2019.05.056 · Cited by 503 · see citing works
“The requirement for ATG4, which converts LC3 to LC3-I (Kabeya et al., 2004) and the effect of RavZ, which irreversibly cleaves lipidated LC3 (Choy et al.”
InfluentialBiogenesis 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
MAPK/JNK signalling: a potential autophagy regulation pathway
Zhou, Y.-Y., Li, Y., Jiang, W.-Q., & Zhou, L.-F. (2015) · Bioscience Reports · doi:10.1042/bsr20140141 · Cited by 444 · see citing works
<scp>mTOR</scp> , metabolism, and the regulation of T‐cell differentiation and function
Waickman, A. T., & Powell, J. D. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01152.x · Cited by 420 · see citing works
A role for autophagy during hepatic stellate cell activation
Thoen, L. F. R., Guimarães, E. L. M., Dollé, L., Mannaerts, I., Najimi, M., Sokal, E., & van Grunsven, L. A. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2011.07.010 · Cited by 385 · see citing works
Mitochondrial Rab GAPs govern autophagosome biogenesis during mitophagy
Yamano, K., Fogel, A. I., Wang, C., van der Bliek, A. M., & Youle, R. J. (2014) · eLife · doi:10.7554/elife.01612 · Cited by 307 · see citing works
Histone deacetylase 6–mediated selective autophagy regulates COPD-associated cilia dysfunction
Lam, H. C., Cloonan, S. M., Bhashyam, A. R., Haspel, J. A., Singh, A., Sathirapongsasuti, J. F., Cervo, M., Yao, H., Chung, A. L., Mizumura, K., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69636 · Cited by 307 · see citing works
PIKfyve inhibition increases exosome release and induces secretory autophagy
Hessvik, N. P., Øverbye, A., Brech, A., Torgersen, M. L., Jakobsen, I. S., Sandvig, K., & Llorente, A. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2309-8 · Cited by 269 · see citing works
LC3-Associated Phagocytosis and Inflammation
Heckmann, B. L., Boada-Romero, E., Cunha, L. D., Magne, J., & Green, D. R. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.08.012 · Cited by 276 · see citing works
Molecular Mechanisms of Autophagy in the Cardiovascular System
Gatica, D., Chiong, M., Lavandero, S., & Klionsky, D. J. (2015) · Circulation Research · doi:10.1161/circresaha.114.303788 · Cited by 272 · see citing works
Minakaki, G., Menges, S., Kittel, A., Emmanouilidou, E., Schaeffner, I., Barkovits, K., Bergmann, A., Rockenstein, E., Adame, A., Marxreiter, F., et al. (2018) · Autophagy · doi:10.1080/15548627.2017.1395992 · Cited by 272 · see citing works
Autophagy modulates osteoarthritis‐related gene expression in human chondrocytes
Sasaki, H., Takayama, K., Matsushita, T., Ishida, K., Kubo, S., Matsumoto, T., Fujita, N., Oka, S., Kurosaka, M., & Kuroda, R. (2012) · Arthritis & Rheumatism · doi:10.1002/art.34323 · Cited by 266 · see citing works
Mitochondrial Dynamics and Mitophagy in Skeletal Muscle Health and Aging
Leduc-Gaudet, J.-P., Hussain, S. N. A., Barreiro, E., & Gouspillou, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158179 · Cited by 268 · see citing works
“The E1-like enzyme ATG7 activates ATG12 via the formation of a thioester bond between the C-terminus of ATG12 and the cysteine507 of ATG7 [85].”
BackgroundKamimoto, T., Shoji, S., Hidvegi, T., Mizushima, N., Umebayashi, K., Perlmutter, D. H., & Yoshimori, T. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m509409200 · Cited by 259 · see citing works
Self-citationIncreased autophagy in transgenic mice with a G93A mutant SOD1 gene
Morimoto, N., Nagai, M., Ohta, Y., Miyazaki, K., Kurata, T., Morimoto, M., Murakami, T., Takehisa, Y., Ikeda, Y., Kamiya, T., et al. (2007) · Brain Research · doi:10.1016/j.brainres.2007.06.045 · Cited by 223 · see citing works
Autophagy-regulating protease Atg4: structure, function, regulation and inhibition
Maruyama, T., & Noda, N. N. (2018) · The Journal of Antibiotics · doi:10.1038/ja.2017.104 · Cited by 190 · see citing works
Cannavino, J., Brocca, L., Sandri, M., Grassi, B., Bottinelli, R., & Pellegrino, M. A. (2015) · The Journal of Physiology · doi:10.1113/jphysiol.2014.286740 · Cited by 166 · see citing works
Fry, C. S., Drummond, M. J., Glynn, E. L., Dickinson, J. M., Gundermann, D. M., Timmerman, K. L., Walker, D. K., Volpi, E., & Rasmussen, B. B. (2013) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/gls209 · Cited by 165 · see citing works
BORC coordinates encounter and fusion of lysosomes with autophagosomes
Jia, R., Guardia, C. M., Pu, J., Chen, Y., & Bonifacino, J. S. (2017) · Autophagy · doi:10.1080/15548627.2017.1343768 · Cited by 160 · see citing works
Rowland, A. M., Richmond, J. E., Olsen, J. G., Hall, D. H., & Bamber, B. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.2279-05.2006 · Cited by 159 · see citing works
Calpain is required for macroautophagy in mammalian cells
Demarchi, F., Bertoli, C., Copetti, T., Tanida, I., Brancolini, C., Eskelinen, E.-L., & Schneider, C. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200601024 · Cited by 156 · see citing works
Characterization of macroautophagic flux in vivo using a leupeptin-based assay
Haspel, J., Shaik, R. S., Ifedigbo, E., Nakahira, K., Dolinay, T., Englert, J. A., & Choi, A. M. K. (2011) · Autophagy · doi:10.4161/auto.7.6.15100 · Cited by 152 · see citing works
Jamart, C., Naslain, D., Gilson, H., & Francaux, M. (2013) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00270.2013 · Cited by 148 · see citing works
LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy
Lai, S.-C., & Devenish, R. J. (2012) · Cells · doi:10.3390/cells1030396 · Cited by 116 · see citing works
Dectin-1–Dependent LC3 Recruitment to Phagosomes Enhances Fungicidal Activity in Macrophages
Tam, J. M., Mansour, M. K., Khan, N. S., Seward, M., Puranam, S., Tanne, A., Sokolovska, A., Becker, C. E., Acharya, M., Baird, M. A., et al. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu290 · Cited by 101 · see citing works
Holdgaard, S. G., Cianfanelli, V., Pupo, E., Lambrughi, M., Lubas, M., Nielsen, J. C., Eibes, S., Maiani, E., Harder, L. M., Wesch, N., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12094-9 · Cited by 84 · see citing works
Cann, G. M., Guignabert, C., Ying, L., Deshpande, N., Bekker, J. M., Wang, L., Zhou, B., & Rabinovitch, M. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21392 · Cited by 84 · see citing works
Autophagy in Pulmonary Diseases
Nakahira, K., Pabon Porras, M. A., & Choi, A. M. K. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201512-2468so · Cited by 78 · see citing works
Preserving Lysosomal Function in the Aging Brain: Insights from Neurodegeneration
Peng, W., Minakaki, G., Nguyen, M., & Krainc, D. (2019) · Neurotherapeutics · doi:10.1007/s13311-019-00742-3 · Cited by 79 · see citing works
Wang, M., Hossain, M. S., Tan, W., Coolman, B., Zhou, J., Liu, S., & Casey, P. J. (2010) · Oncogene · doi:10.1038/onc.2010.247 · Cited by 75 · see citing works
Lei, R., Zhao, F., Tang, C.-Y., Luo, M., Yang, S.-K., Cheng, W., Li, X.-W., & Duan, S.-B. (2018) · Cellular Physiology and Biochemistry · doi:10.1159/000488827 · Cited by 67 · see citing works
Thai, P. N., Seidlmayer, L. K., Miller, C., Ferrero, M., Dorn, G. W., Schaefer, S., Bers, D. M., & Dedkova, E. N. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00382 · Cited by 66 · see citing works
Comprehensive autophagy evaluation in cardiac disease models
Kaludercic, N., Maiuri, M. C., Kaushik, S., Fernández, Á. F., de Bruijn, J., Castoldi, F., Chen, Y., Ito, J., Mukai, R., Murakawa, T., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvz233 · Cited by 64 · see citing works
Takikita, S., Schreiner, C., Baum, R., Xie, T., Ralston, E., Plotz, P. H., & Raben, N. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015239 · Cited by 60 · see citing works
Alternative Macroautophagic Pathways
Juenemann, K., & Reits, E. A. (2012) · International Journal of Cell Biology · doi:10.1155/2012/189794 · Cited by 58 · see citing works
LC3B is indispensable for selective autophagy of p62 but not basal autophagy.
Maruyama, Y., Sou, Y.-S., Kageyama, S., Takahashi, T., Ueno, T., Tanaka, K., Komatsu, M., & Ichimura, Y. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.02.093 · Cited by 56 · see citing works
Arnold, C. R., Pritz, T., Brunner, S., Knabb, C., Salvenmoser, W., Holzwarth, B., Thedieck, K., & Grubeck-Loebenstein, B. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.01.018 · Cited by 42 · see citing works
- Authors
- Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., & Yoshimori, T.
- Affiliations
- National Institute for Basic Biology (JP)
- Nagahama Institute of Bio-Science and Technology (JP)
- National Institute of Genetics (JP)
- Corresponding author
- Yoshimori, Tamotsu
- Venue
- Journal of Cell Science
- Publisher
- The Company of Biologists
- Published
- 2004-06-01
- Volume
- 117
- Issue
- 13
- Pages
- 2805-2812
- ISSN
- 0021-9533 (ISSN-L)
- 1477-9137
- OpenAlex
- W2068153705
- Cited by
- 1,394
- References
- 29
- Citations by year
- 2026: 22 · 2025: 40 · 2024: 49 · 2023: 72 · 2022: 67 · 2021: 100 · 2020: 89 · 2019: 86 · 2018: 77 · 2017: 74 · 2016: 83 · 2015: 99 · 2014: 76 · 2013: 85 · 2012: 97
- FWCI
- 18.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Cell Science (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- 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
- LC3, GABARAP, autophagosomal membrane, LC3-II, phosphatidylethanolamine conjugation, ATG4B, autophagosomes, protein localization, ethanolamine incorporation
- MeSH terms
- Autophagy-Related Protein 8 Family, Animals, Carbon Radioisotopes, Carrier Proteins, Fluorescent Dyes, Glycine, HeLa Cells, Humans, Kinetics, Lysosomes, Microfilament Proteins, Microscopy, Fluorescence, Microtubule-Associated Proteins, Phagosomes, Precipitin Tests, Saccharomyces cerevisiae, Stem Cells, Subcellular Fractions, Substrate Specificity, Teratocarcinoma, Ethanolamine, Cell Line, Tumor, Intracellular Signaling Peptides and Proteins, Adaptor Proteins, Signal Transducing, Luminescent Agents, Apoptosis Regulatory Proteins, Mice
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