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The Atg12-Atg5 Conjugate Has a Novel E3-like Activity for Protein Lipidation in Autophagy
Open accessAbstract
Autophagy is a bulk degradation process in eukaryotic cells; autophagosomes enclose cytoplasmic components for degradation in the lysosome/vacuole. Autophagosome formation requires two ubiquitin-like conjugation systems, the Atg12 and Atg8 systems, which are tightly associated with expansion of autophagosomal membrane. Previous studies have suggested that there is a hierarchy between these systems; the Atg12 system is located upstream of the Atg8 system in the context of Atg protein organization. However, the concrete molecular relationship is unclear. Here, we show using an in vitro Atg8 conjugation system that the Atg12-Atg5 conjugate, but not unconjugated Atg12 or Atg5, strongly enhances the formation of the other conjugate, Atg8-PE. The Atg12-Atg5 conjugate promotes the transfer of Atg8 from Atg3 to the substrate, phosphatidylethanolamine (PE), by stimulating the activity of Atg3. We also show that the Atg12-Atg5 conjugate interacts with both Atg3 and PE-containing liposomes. These results indicate that the Atg12-Atg5 conjugate is a ubiquitin-protein ligase (E3)-like enzyme for Atg8-PE conjugation reaction, distinctively promoting protein-lipid conjugation.
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“Two ubiquitin-like conjugation systems also contribute to autophagosome formation [23,24,25].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [25]
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“The last stage in transfer of LC3 to PE requires the E3 ubiquitin-ligase like activity of the ATG5ATG12:ATG16L1 complex where ATG5 induces a conformational change in the catalytic site of ATG3 leading to transfer of the C-terminal carboxyl group of LC3 from a thioester bond to amino groups exposed by PE [25].”
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Liang, W., Fu, L., Feng, M., Wang, X., Yun, Z., & Xu, J. (2023) · Toxics · doi:10.3390/toxics11070607 · Cited by 7
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“This reaction is catalyzed by a cascade of enzymes including E1-like enzyme Atg7, E2-like enzyme Atg3, and E3-like enzyme complex Atg12-Atg5 conjugate [9,10].”
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“Importantly, the product of the “upstream” conjugation reaction – the ATG5-12 complex – acts as an E3-like ligase (in association with ATG16) to aid the covalent attachment of ATG8 to PE, which means that the ATG5/12/16 complex acts to speed up the transfer of ATG8 from ATG3 to PE without conveying any additional spec…”
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Advances in the role of autophagy in the development of retinoblastoma (Review)
Wan, T., Fu, M., Wu, Z., Gao, X. J., & Zhou, S. (2021) · Oncology Letters · doi:10.3892/ol.2021.12893 · Cited by 4
“The connection between ATG5 and ATG12 requires the participation of the ubiquitin sample connection system (21).”
BackgroundNon-canonical roles of ATG8 for TFEB activation
Nakamura, S., Akayama, S., & Yoshimori, T. (2022) · Biochemical Society Transactions · doi:10.1042/bst20210813 · Cited by 6
Pan, L., Yang, Y., Chen, X., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1052779 · Cited by 4
Developing systems in yeast to address Alzheimer's disease
Dhakal, S., & Macreadie, I. G. (2022) · Methods in microbiology · doi:10.1016/bs.mim.2022.02.001 · Cited by 4
Autoimmune regulator regulates autophagy in THP-1 human monocytes
Shi, L., Hu, L., & Li, Y. (2010) · Frontiers of Medicine · doi:10.1007/s11684-010-0096-4 · Cited by 4
“Furthermore, it was reported [14] that AIRE function as E3 ubiquitin ligase, a feature similar to the Atg5-Atg12/Atg16L1 complex, which is crucial for Atg8/ LC3 lipidation in autophagy [ 15 ], and thus we presume AIRE might equally have a role in modulating autophagy.”
BackgroundQuah, S. Y., Wong, C. C., Wong, H. C., Ho, K. L., Manan, N. A., Deb, P. K., Sagineedu, S. R., & Stanslas, J. (2021) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2021.115605 · Cited by 3
Jordan, T. X., & Randall, G. C. (2014) · Wiley eBooks · doi:10.1002/9781118677551.ch6 · Cited by 4
Structural characterization of autophagy related protein complexes
Metje‐Sprink, J. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6331 · Cited by 4
Ding, G., Mugume, Y., Dueñas, M. E., Lee, Y., Liu, M., Nettleton, D. S., Zhao, X., Li, L., Bassham, D. C., & Nikolau, B. J. (2023) · Frontiers in Plant Science · doi:10.3389/fpls.2023.1093358 · Cited by 3
“lipidation of ATG8 with a phosphatidylethanolamine molecule (Ichimura et al., 2000; Hanada et al., 2007; Chung et al., 2010).”
BackgroundGómez-Martín, A., Fuentes, J. M., Jordán, J., Galindo, M. F., & Fernández-García, J. L. (2023) · Genes · doi:10.3390/genes14122171 · Cited by 3
“In addition, ATG16L1 forms an oligomeric complex with ATG12-ATG5 conjugates to enhance LC3/ATG8 conjugation with phosphatidylethanolamine by recruiting an LC3-ATG3 intermediate [13,14] and specifies the site of LC3 lipidation [15].”
BackgroundZhao, Z., Zhao, X., Wu, S., et al. (2025) · Theoretical and Applied Genetics · doi:10.1007/s00122-025-05026-3 · Cited by 3
“ATG5 has the ability to bind to membranes, and the ATG5–ATG12 conjugate has E3-like enzyme activity and promotes ATG conjugation to PE, while ATG16 promotes ATG8–PE conjugation (Hanada et al. 2007; Romanov et al. 2012).”
Autophagy Mechanisms for Brain Recovery. Keep It Clean, Keep It Alive
Viscomi, M. T., D’Amelio, M., Nobili, A., Cavallucci, V., Latini, L., Bisicchia, E., Sasso, V., & Molinari, M. (2017) · Contemporary clinical neuroscience · doi:10.1007/978-3-319-52067-4_2 · Cited by 3
“The second system mediates the conjugation of LC3 to phosphatidylethanolamine (PE) (Hanada et al. 2007; Mizushima et al. 2003).”
BackgroundCell Proliferation, Survival, Necrosis and Apoptosis
Mierke, C. T. (2020) · Biological and medical physics, biomedical engineering · doi:10.1007/978-3-030-58532-7_16 · Cited by 3
Uba1: A Potential Ubiquitin-like Activator Protein of Urm1 in Toxoplasma gondii
Xiao, Q., Li, J., Chen, J., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810298 · Cited by 3
“The ubiquitin-like system had been shown to be involved in mediating protein lipidation [23], either as E2 enzymes [24] or as E3 enzymes [25].”
BackgroundNovel Insights into Epigenetic Control of Autophagy in Cancer
Parveen, S., Rizvi, S. F., Hasan, A., Afaq, U., & Mir, S. S. (2022) · OBM Genetics · doi:10.21926/obm.genet.2204170 · Cited by 4
Hayat, M. A., Ding, J., Zhang, X., et al. (2023) · Animals · doi:10.3390/ani13152478 · Cited by 3
“For autophagosome formation to occur, the ATG8PE and ATG16–ATG5–ATG12 complexes must first be formed [43].”
BackgroundMitophagy Decreases in the Peripheral Vestibular System of Aged C57BL/6J Mice
Cho, S. I., Jo, E.-R., & Lee, S. M. (2023) · In Vivo · doi:10.21873/invivo.13426 · Cited by 4
Beyond the C-terminal Glycine of ATG8 Proteins – The Story of Some Neglected Amino Acids
Barz, S., Hofmann, K., Reggiori, F., & Kraft, C. (2024) · Journal of Molecular Biology · doi:10.1016/j.jmb.2024.168588 · Cited by 4
The battle between bacterial infection and autophagy in aquatic animals
Wang, Q., He, X., Jin, J. W., Yang, Y., Jänsch, L., & Li, S. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1614182 · Cited by 3
“Autophagosome formation is initiated by BECLIN 1, with LC3 lipidation via the ATG5 – 12 – 16L1 complex enabling bacterial capture (28, 29).”
The Molecular Mechanisms Underlying Autophagosome Formation in Yeast
Yamamoto, H., & Ohsumi, Y. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405529-2.00004-4 · Cited by 3
Self-citationTHE CELLULAR PROCESS OF AUTOPHAGY AND CONTROL OF AUTOPHAGY IN NEURONS
McKnight, N. C., Mizushima, N., & Yue, Z. (2012) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814350457_0001 · Cited by 3
Cell Death, Apoptosis, and Autophagy in Retinal Injury
Boulton, M. E., Mitter, S. K., Rao, H. V., & Dunn, W. A. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4557-0737-9.00024-2 · Cited by 3
Role of Autophagy in Brain Sculpture: Physiological and Pathological Implications
Nobili, A., Cavallucci, V., & D’Amelio, M. (2016) · Springer eBooks · doi:10.1007/978-3-319-30079-5_11 · Cited by 3
Regulation of the DNA Damage Response by Autophagy
Eapen, V. V., Waterman, D. P., Lemos, B. R., & Haber, J. E. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805420-8.00010-x · Cited by 3
Research Progress in Regulation of Reactive Oxygen Species in Plant Autophagy
Jing, H., Guangzhou, Z., Tan, X., et al. (2012) · Chinese Bulletin of Botany · doi:10.3724/sp.j.1259.2012.00534 · Cited by 3
Metadata
- Authors
- Hanada, T., Noda, N. N., Satomi, Y., Ichimura, Y., Fujioka, Y., Takao, T., Inagaki, F., & Ohsumi, Y.
- Affiliations
- National Institute for Basic Biology (JP)
- Hokkaido University (JP)
- Institute for Protein Research, The University of Osaka (JP)
- Corresponding author
- Ohsumi, Yoshinori
- ORCID
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2007-12
- Volume
- 282
- Issue
- 52
- Pages
- 37298-37302
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2040157483
- Semantic Scholar
- ac42037b48b9d80a5e5c15efd2379440ed23b91c
- Cited by
- 1,123
- References
- 28
- Citations by year
- 2026: 31 · 2025: 38 · 2024: 44 · 2023: 55 · 2022: 59 · 2021: 68 · 2020: 75 · 2019: 87 · 2018: 61 · 2017: 54 · 2016: 79 · 2015: 77 · 2014: 64 · 2013: 65 · 2012: 81
- FWCI
- 28.90
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Tokyo Tech Research Repository (Tokyo Institute of Technology) (submittedVersion)
- 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
- ATG12-ATG5 conjugate, protein lipidation, E3 ubiquitin ligase activity, autophagy, ATG3, ATG12, ATG8, phosphatidylethanolamine, autophagosome formation, liposome binding
- MeSH terms
- Autophagy-Related Protein 5, Autophagy-Related Protein 12, Autophagy, Escherichia coli, Lipids, Liposomes, Models, Biological, Protein Processing, Post-Translational, Saccharomyces cerevisiae, Time Factors, Gene Expression Regulation, Fungal, Ubiquitin, Saccharomyces cerevisiae Proteins, Ubiquitin-Protein Ligases
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