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Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1–phosphatidylinositol-3-kinase complex
Open accessAbstract
Beclin 1, a mammalian autophagy protein that has been implicated in development, tumour suppression, neurodegeneration and cell death, exists in a complex with Vps34, the class III phosphatidylinositol-3-kinase (PI(3)K) that mediates multiple vesicle-trafficking processes including endocytosis and autophagy. However, the precise role of the Beclin 1-Vps34 complex in autophagy regulation remains to be elucidated. Combining mouse genetics and biochemistry, we have identified a large in vivo Beclin 1 complex containing the known proteins Vps34, p150/Vps15 and UVRAG, as well as two newly identified proteins, Atg14L (yeast Atg14-like) and Rubicon (RUN domain and cysteine-rich domain containing, Beclin 1-interacting protein). Characterization of the new proteins revealed that Atg14L enhances Vps34 lipid kinase activity and upregulates autophagy, whereas Rubicon reduces Vps34 activity and downregulates autophagy. We show that Beclin 1 and Atg14L synergistically promote the formation of double-membraned organelles that are associated with Atg5 and Atg12, whereas forced expression of Rubicon results in aberrant late endosomal/lysosomal structures and impaired autophagosome maturation. We hypothesize that by forming distinct protein complexes, Beclin 1 and its binding proteins orchestrate the precise function of the class III PI(3)K in regulating autophagy at multiple steps.
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In the citing paper
“Yeast Atg14 is the autophagy-specific subunit of the Vps34 complex I, 404 and a human homolog, named ATG14 (ATG14L/BARKOR), has been identified.[405][406][407][408]”
From Guidelines for the use and interpretation of assays for monitoring autophagy (2012) · cites this paper as [406]
Experimental — accuracy not yet measuredIn the citing paper
“the class III phosphoinositide 3-kinase (PI3K) complex regulates vesicle nucleation and phagophore formation”
From Autophagy in kidney homeostasis and disease (2020) · cites this paper as [10]
In the citing paper
“Defects in induction, maturation, or lysosomal clearance impair protein degradation (Zhong et al. 2009), (Pickford et al. 2008), (Ravikumar et al. 2005), (Webb et al. 2004), (Iwata et al. 2005), (Kimura et al. 2008), (Wong and Cuervo 2010), (Lee et al. 2010), and is assessable via LC3-II turnover or p62 degradation (Mizushima et al. 2010), (Ju et al. 2010), (Klionsky et al. 2008b), (Tanida et al.”
From TMEM55B downregulation promotes neurodegeneration in Alzheimer’s disease models (2026) · cites this paper as Zhong et al. 2009
In the citing paper
“Detection of endogenous phospho-ATG16L1 [823] has been demonstrated as a novel method to monitor autophagy induction.”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [823]
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Cites
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
Pankiv, 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
Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice
Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., et al. (2006) · Nature · doi:10.1038/nature04724 · Cited by 3,882
Loss of autophagy in the central nervous system causes neurodegeneration in mice
Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J.-I., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., et al. (2006) · Nature · doi:10.1038/nature04723 · Cited by 3,500
Induction of autophagy and inhibition of tumorigenesis by beclin 1
Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., & Levine, B. (1999) · Nature · doi:10.1038/45257 · Cited by 3,347
Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene
Qu, X., Yu, J., Bhagat, G., Furuya, N., Hibshoosh, H., Troxel, A., Rosen, J., Eskelinen, E.-L., Mizushima, N., Ohsumi, Y., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci20039 · Cited by 2,311
A 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 2,139
Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice.
Komatsu, M., Waguri, S., Koike, M., Sou, Y.-S., Ueno, T., Hara, T., Mizushima, N., Iwata, J.-I., Ezaki, J., Murata, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.035 · Cited by 2,124
Self-citationYue, Z., Jin, S., Yang, C., Levine, A. J., & Heintz, N. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2436255100 · Cited by 2,116
Self-citationLC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation
Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y., & Yoshimori, T. (2004) · Journal of Cell Science · doi:10.1242/jcs.01131 · Cited by 1,394
Flagged first, then by citations
Cited by
Sorted by citations
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
Self-citationCillà, S. D., Farruggio, S., Vujosevic, S., Raina, G., Filippini, D. A., Gatti, V., Clemente, N., Mary, D., Vezzola, D., Casini, G., et al. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479441 · Cited by 5,154
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
Autophagy: cellular and molecular mechanisms
Glick, D. R., Barth, S., & Macleod, K. F. (2010) · The Journal of Pathology · doi:10.1002/path.2697 · Cited by 3,995
The Role of Atg Proteins in Autophagosome Formation
Mizushima, N., Yoshimori, T., & Ohsumi, Y. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154005 · Cited by 2,978
Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1
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 2,897
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
The Beclin 1 network regulates autophagy and apoptosis
Kang, R., Zeh, H. J., Lotze, M. T., & Tang, D. (2011) · Cell Death & Differentiation · doi:10.1038/cdd.2010.191 · Cited by 2,485
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
Mammalian autophagy: core molecular machinery and signaling regulation
Yang, Z., & Klionsky, D. J. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.11.014 · Cited by 1,956
Regulation of Mammalian Autophagy in Physiology and Pathophysiology
Ravikumar, B., Sarkar, S., Davies, J. E., Futter, M., García-Arencibia, M., Green-Thompson, Z. W., Jiménez-Sánchez, M., Korolchuk, V. I., Lichtenberg, M., Luo, S., et al. (2010) · Physiological Reviews · doi:10.1152/physrev.00030.2009 · Cited by 1,789
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
Self-citationPhosphoinositides: Tiny Lipids With Giant Impact on Cell Regulation
Balla, T. (2013) · Physiological Reviews · doi:10.1152/physrev.00028.2012 · Cited by 1,638
Autophagy and autophagy-related proteins in cancer
Li, X., He, S., & Ma, B. (2020) · Molecular Cancer · doi:10.1186/s12943-020-1138-4 · Cited by 1,684
Self-citationThe emerging mechanisms of isoform-specific PI3K signalling
Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M., & Bilanges, B. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2882 · Cited by 1,767
ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase
Russell, R. C., Tian, Y., Yuan, H., Park, H. W., Chang, Y.-Y., Kim, J., Kim, H., Neufeld, T. P., Dillin, A., & Guan, K.-L. (2013) · Nature Cell Biology · doi:10.1038/ncb2757 · Cited by 1,529
Network organization of the human autophagy system
Behrends, C., Sowa, M. E., Gygi, S. P., & Harper, J. W. (2010) · Nature · doi:10.1038/nature09204 · Cited by 1,554
Autophagy modulation as a potential therapeutic target for diverse diseases
Rubinsztein, D. C., Codogno, P., & Levine, B. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3802 · Cited by 1,464
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
Architecture of the human interactome defines protein communities and disease networks
Huttlin, E. L., Bruckner, R. J., Paulo, J. A., Cannon, J. R., Ting, L., Baltier, K., Colby, G., Gebreab, F., Gygi, M. P., Parzen, H., et al. (2017) · Nature · doi:10.1038/nature22366 · Cited by 1,437
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 1,506
Wu, Y.-T., Tan, H.-L., Shui, G., Bauvy, C., Huang, Q., Wenk, M. R., Ong, C.-N., Codogno, P., & Shen, H.-M. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.080796 · Cited by 1,127
Historical landmarks of autophagy research
Ohsumi, Y. (2013) · Cell Research · doi:10.1038/cr.2013.169 · Cited by 1,125
Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways
Palmieri, M., Impey, S., Kang, H., di Ronza, A., Pelz, C., Sardiello, M., & Ballabio, A. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr306 · Cited by 1,022
Autophagy gone awry in neurodegenerative diseases
Wong, E., & Cuervo, A. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2575 · Cited by 815
Mechanisms governing autophagosome biogenesis
Nakatogawa, H. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0241-0 · Cited by 903
Autophagy, Immunity, and Microbial Adaptations
Deretic, V. P., & Levine, B. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.05.016 · Cited by 892
Beclin1 Controls the Levels of p53 by Regulating the Deubiquitination Activity of USP10 and USP13
Liu, J., Xia, H., Kim, M., Xu, L., Li, Y., Zhang, L., Cai, Y. C., Norberg, H. V., Zhang, T., Furuya, T., et al. (2011) · Cell · doi:10.1016/j.cell.2011.08.037 · Cited by 839
Differential Regulation of Distinct Vps34 Complexes by AMPK in Nutrient Stress and Autophagy
Kim, J., Kim, Y. C., Fang, C., Russell, R. C., Kim, J. H., Fan, W., Liu, R., Zhong, Q., & Guan, K. (2013) · Cell · doi:10.1016/j.cell.2012.12.016 · Cited by 829
Autophagy as a target for anticancer therapy
Jankú, F., McConkey, D. J., Hong, D. S., & Kurzrock, R. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.71 · Cited by 814
The Beclin 1–VPS34 complex – at the crossroads of autophagy and beyond
Funderburk, S. F., Wang, Q. J., & Yue, Z. (2010) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.03.002 · Cited by 804
Self-citationItakura, E., & Mizushima, N. (2010) · Autophagy · doi:10.4161/auto.6.6.12709 · Cited by 843
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
“In agreement with previous studies 14,15 , rapamycin-treated or nutrient-deprived Rubi-con macrophages exhibited increased numbers of LC3 puncta, compared with wild-type macrophages (Fig.”
RetractedAutophagy regulation by nutrient signaling
Russell, R. C., Yuan, H., & Guan, K. (2013) · Cell Research · doi:10.1038/cr.2013.166 · Cited by 740
Mammalian Autophagy: How Does It Work?
Bento, C. F., Renna, M., Ghislat, G., Puri, C., Ashkenazi, A., Vicinanza, M., Menzies, F. M., & Rubinsztein, D. C. (2016) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060815-014556 · Cited by 711
TBK-1 Promotes Autophagy-Mediated Antimicrobial Defense by Controlling Autophagosome Maturation
Pilli, M., Arko-Mensah, J., Ponpuak, M., Roberts, E., Master, S., Mandell, M. A., Dupont, N., Ornatowski, W., Jiang, S., Bradfute, S. B., et al. (2012) · Immunity · doi:10.1016/j.immuni.2012.04.015 · Cited by 655
Mechanisms of Autophagy Initiation
Hurley, J. H., & Young, L. N. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061516-044820 · Cited by 681
He, C., & Levine, B. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2010.01.001 · Cited by 681
Autophagy mediates degradation of nuclear lamina
Dou, Z., Xu, C., Donahue, G., Shimi, T., Pan, J.-A., Zhu, J., Ivanov, A., Capell, B. C., Drake, A. M., Shah, P. P., et al. (2015) · Nature · doi:10.1038/nature15548 · Cited by 655
Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity
Zhao, Y., Yang, J. H., Liao, W., Liu, X., Zhang, H., Wang, S., Wang, D., Feng, J., Yu, L., & Zhu, W. (2010) · Nature Cell Biology · doi:10.1038/ncb2069 · Cited by 632
ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes
Diao, J., Liu, R., Rong, Y., Zhao, M., Zhang, J., Lai, Y., Zhou, Q., Wilz, L., Li, J., Vivona, S., et al. (2015) · Nature · doi:10.1038/nature14147 · Cited by 611
The regulation of autophagy – unanswered questions
Chen, Y., & Klionsky, D. J. (2010) · Journal of Cell Science · doi:10.1242/jcs.064576 · Cited by 617
Machinery, 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 582
PLEKHM1 Regulates Autophagosome-Lysosome Fusion through HOPS Complex and LC3/GABARAP Proteins
McEwan, D. G., Popovic, D., Gubas, A., Terawaki, S., Suzuki, H., Stadel, D., Coxon, F. P., Miranda de Stegmann, D., Bhogaraju, S., Maddi, K., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2014.11.006 · Cited by 563
Grumati, P., Coletto, L., Sabatelli, P., Cescon, M., Angelin, A., Bertaggia, E., Blaauw, B., Urciuolo, A., Tiepolo, T., Merlini, L., et al. (2010) · Nature Medicine · doi:10.1038/nm.2247 · Cited by 540
Murrow, L. M., & Debnath, J. (2012) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-020712-163918 · Cited by 546
Matrix Protein 2 of Influenza A Virus Blocks Autophagosome Fusion with Lysosomes
Gannagé, M., Dormann, D., Albrecht, R., Dengjel, J., Torossi, T., Rämer, P. C., Lee, M., Strowig, T., Arrey, F., Conenello, G., et al. (2009) · Cell Host & Microbe · doi:10.1016/j.chom.2009.09.005 · Cited by 526
New insights into autophagosome–lysosome fusion
Nakamura, S., & Yoshimori, T. (2017) · Journal of Cell Science · doi:10.1242/jcs.196352 · Cited by 540
The dynamic interaction of AMBRA1 with the dynein motor complex regulates mammalian autophagy
Bartolomeo, S. D., Corazzari, M., Nazio, F., Oliverio, S., Lisi, G., Antonioli, M., Pagliarini, V., Matteoni, S., Fuoco, C., Giunta, L., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201002100 · Cited by 561
Mst1 inhibits autophagy by promoting the interaction between Beclin1 and Bcl-2
Maejima, Y., Kyoi, S., Zhai, P., Liu, T., Li, H., Ivessa, A., Sciarretta, S., Del Re, D. P., Zablocki, D. K., Hsu, C.-P., et al. (2013) · Nature Medicine · doi:10.1038/nm.3322 · Cited by 499
Autophagy in kidney homeostasis and disease
Tang, C., Livingston, M. J., Liu, Z., & Dong, Z. (2020) · Nature Reviews Nephrology · doi:10.1038/s41581-020-0309-2 · Cited by 496
Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes
Simonsen, A., & Tooze, S. A. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200907014 · Cited by 520
Autophagosome Formation and Molecular Mechanism of Autophagy
Tanida, I. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3482 · Cited by 505
Overview of macroautophagy regulation in mammalian cells
Mehrpour, M., Esclatine, A., Beau, I., & Codogno, P. (2010) · Cell Research · doi:10.1038/cr.2010.82 · Cited by 516
Luciani, A., Villella, V. R., Esposito, S., Brunetti-Pierri, N., Medina, D., Settembre, C., Gavina, M., Pulze, L., Giardino, I., Pettoello-Mantovani, M., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2090 · Cited by 467
Biogenesis 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
Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L
Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N. T., Izumi, T., Noda, T., & Yoshimori, T. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200911141 · Cited by 456
Virgin, H. W., & Levine, B. (2009) · Nature Immunology · doi:10.1038/ni.1726 · Cited by 462
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
Ge, L., Melville, D., Zhang, M., & Schekman, R. W. (2013) · eLife · doi:10.7554/elife.00947 · Cited by 450
Functions of autophagy in normal and diseased liver
Czaja, M. J., Ding, W., Donohue, T. M., Friedman, S. L., Js, K., Komatsu, M., Lemasters, J. J., Lemoine, A., Lin, J. D., Ou, J. J., et al. (2013) · Autophagy · doi:10.4161/auto.25063 · Cited by 439
Autophagy in osteoblasts is involved in mineralization and bone homeostasis
Nollet, M., Santucci-Darmanin, S., Breuil, V., Al-Sahlanee, R., Cros, C., Topi, M., Momier, D., Samson, M., Pagnotta, S., Cailleteau, L., et al. (2014) · Autophagy · doi:10.4161/auto.36182 · Cited by 422
Autophagy in lysosomal storage disorders
Lieberman, A. P., Puertollano, R., Raben, N., Slaugenhaupt, S., Walkley, S. U., & Ballabio, A. (2012) · Autophagy · doi:10.4161/auto.19469 · Cited by 399
Villella, V. R., Esposito, S., Bruscia, E. M., Maiuri, M. C., Raia, V., Kroemer, G., & Maiuri, L. (2013) · Frontiers in Pharmacology · doi:10.3389/fphar.2013.00001 · Cited by 390
Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function
Jaber, N. L., Dou, Z., Chen, J., Catanzaro, J. M., Jiang, Y.-P., Ballou, L. M., Selinger, E. S., Ouyang, X., Lin, R. Z., Zhang, J., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112848109 · Cited by 399
Tanaka, S., Hikita, H., Tatsumi, T., Sakamori, R., Nozaki, Y., Sakane, S., Shiode, Y., Nakabori, T., Saito, Y., Hiramatsu, N., et al. (2016) · Hepatology · doi:10.1002/hep.28820 · Cited by 376
Distinct Autophagosomal-Lysosomal Fusion Mechanism Revealed by Thapsigargin-Induced Autophagy Arrest
Ganley, I. G., Wong, P., Gammoh, N., & Jiang, X. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.04.024 · Cited by 397
Beclin-1-Dependent Autophagy Protects the Heart During Sepsis
Sun, Y., Yao, X., Zhang, Q.-J., Zhu, M., Liu, Z.-P., Ci, B., Xie, Y., Carlson, D., Rothermel, B. A., Sun, Y., et al. (2018) · Circulation · doi:10.1161/circulationaha.117.032821 · Cited by 381
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 375
Sarkar, S. (2013) · Biochemical Society Transactions · doi:10.1042/bst20130134 · Cited by 380
A current perspective of autophagosome biogenesis
Shibutani, S., & Yoshimori, T. (2013) · Cell Research · doi:10.1038/cr.2013.159 · Cited by 368
Park, J.-M., Jung, C. H., Seo, M., Otto, N. M., Grunwald, D., Kim, K. H., Moriarity, B., Kim, Y.-M., Starker, C., Nho, R. S., et al. (2016) · Autophagy · doi:10.1080/15548627.2016.1140293 · Cited by 341
Liang, Q., Seo, G. J., Choi, Y. J., Kwak, M., Ge, J., Rodgers, M. A., Shi, M., Leslie, B. J., Hopfner, K., Ha, T., et al. (2014) · Cell Host & Microbe · doi:10.1016/j.chom.2014.01.009 · Cited by 364
Gene Copy-Number Alterations: A Cost-Benefit Analysis
Tang, Y.-C., & Amon, A. (2013) · Cell · doi:10.1016/j.cell.2012.11.043 · Cited by 348
Starr, T., Child, R., Wehrly, T. D., Hansen, B. T., Hwang, S., López-Otı́n, C., Virgin, H. W., & Celli, J. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2011.12.002 · Cited by 356
LC3-Associated Phagocytosis in Myeloid Cells Promotes Tumor Immune Tolerance
Cunha, L. D., Yang, M., Carter, R., Guy, C., Harris, L., Crawford, J. C., Quarato, G., Boada-Romero, E., Kalkavan, H., Johnson, M. D. L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.061 · Cited by 334
Hale, A. N., Ledbetter, D., Gawriluk, T. R., & Rucker, E. B. (2013) · Autophagy · doi:10.4161/auto.24273 · Cited by 343
Beclin 1 Phosphorylation – at the Center of Autophagy Regulation
Menon, M., & Dhamija, S. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00137 · Cited by 350
Lim, J., Lachenmayer, M. L., Wu, S., Liu, W., Kundu, M., Wang, R., Komatsu, M., Oh, Y. J., Zhao, Y., & Yue, Z. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1004987 · Cited by 333
Self-citationAutophagy and the Immune System
Kuballa, P., Nolte, W. M., Castoreno, A. B., & Xavier, R. J. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-020711-074948 · Cited by 335
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
“Beclin1 is a component of the nucleation complex, along with ATG14, lipid kinase VPS34/PI3KIII, and VPS15/PIK3R4 (Itakura et al. 2008, Matsunaga et al. 2009, Sun et al. 2008, Zhong et al. 2009).”
BackgroundBodemann, B. O., Orvedahl, A., Cheng, T., Ram, R. R., Ou, Y.-H., Formstecher, É., Maiti, M., Hazelett, C. C., Wauson, E., Balakireva, M., et al. (2011) · Cell · doi:10.1016/j.cell.2010.12.018 · Cited by 325
The clearance of dying cells: table for two
Green, D. R., Oguin, T. H., & Martinez, J. (2016) · Cell Death & Differentiation · doi:10.1038/cdd.2015.172 · Cited by 314
Ponpuak, M., Davis, A. S., Roberts, E. A., Delgado, M. A., Dinkins, C., Zhao, Z., Virgin, H. W., Kyei, G. B., Johansen, T., Vergne, I., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.02.009 · Cited by 309
Why should autophagic flux be assessed?
Zhang, X.-J., Chen, S., Huang, K.-X., & Le, W.-D. (2013) · Acta Pharmacologica Sinica · doi:10.1038/aps.2012.184 · Cited by 312
Autophagy in diabetic nephropathy
Ding, Y., & Choi, M. E. (2015) · Journal of Endocrinology · doi:10.1530/joe-14-0437 · Cited by 306
The multiple roles of autophagy in cancer
Rosenfeldt, M. T., & Ryan, K. M. (2011) · Carcinogenesis · doi:10.1093/carcin/bgr031 · Cited by 311
A comprehensive glossary of autophagy-related molecules and processes (2ndedition)
Klionsky, D. J., Baehrecke, E. H., Brumell, J. H., Chu, C. T., Codogno, P., Cuervo, A. M., Debnath, J., Deretic, V. P., Elazar, Z., Eskelinen, E., et al. (2011) · Autophagy · doi:10.4161/auto.7.11.17661 · Cited by 298
Regulation of PIK3C3/VPS34 complexes by MTOR in nutrient stress-induced autophagy
Yuan, H., Russell, R. C., & Guan, K. (2013) · Autophagy · doi:10.4161/auto.26058 · Cited by 303
Coronavirus NSP6 restricts autophagosome expansion
Cottam, E. M., Whelband, M., & Wileman, T. E. (2014) · Autophagy · doi:10.4161/auto.29309 · Cited by 299
The Role of Lipids in the Control of Autophagy
Dall’Armi, C., Devereaux, K. A., & Paolo, G. D. (2013) · Current Biology · doi:10.1016/j.cub.2012.10.041 · Cited by 296
Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L)
Fan, W., Nassiri, A., & Zhong, Q. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016472108 · Cited by 285
Kudchodkar, S. B., & Levine, B. (2009) · Reviews in Medical Virology · doi:10.1002/rmv.630 · Cited by 286
Phospholipase D Signaling Pathways and Phosphatidic Acid as Therapeutic Targets in Cancer
Bruntz, R. C., Lindsley, C. W., & Brown, H. A. (2014) · Pharmacological Reviews · doi:10.1124/pr.114.009217 · Cited by 286
Autophagosome formation—The role of ULK1 and Beclin1–PI3KC3 complexes in setting the stage
Wirth, M., Joachim, J., & Tooze, S. A. (2013) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.05.007 · Cited by 292
mTORC1 Phosphorylates UVRAG to Negatively Regulate Autophagosome and Endosome Maturation
Kim, Y. M., Jung, C. H., Seo, M., Kim, E. K., Park, J.-M., Bae, S. S., & Kim, D. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.11.013 · Cited by 288
Control of autophagy initiation by phosphoinositide 3‐phosphatase jumpy
Vergne, I., Roberts, E., Elmaoued, R. A., Tosch, V., Delgado, M. A., Proikas‐Cezanne, T., Laporte, J., & Deretic, V. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.159 · Cited by 270
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
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
LC3-associated phagocytosis at a glance
Heckmann, B. L., & Green, D. R. (2019) · Journal of Cell Science · doi:10.1242/jcs.222984 · Cited by 280
Metadata
- Authors
- Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N., & Yue, Z.
- Affiliations
- Howard Hughes Medical Institute (US)
- Rockefeller University (US)
- Icahn School of Medicine at Mount Sinai (US)
- Albert Einstein College of Medicine (US)
- Corresponding author
- Yue, Zhenyu
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2009-03-08
- Volume
- 11
- Issue
- 4
- Pages
- 468-476
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC2664389
- OpenAlex
- W1983831622
- Cited by
- 1,005
- References
- 35
- Citations by year
- 2026: 29 · 2025: 43 · 2024: 38 · 2023: 48 · 2022: 63 · 2021: 62 · 2020: 69 · 2019: 51 · 2018: 57 · 2017: 58 · 2016: 72 · 2015: 56 · 2014: 64 · 2013: 77 · 2012: 64
- FWCI
- 49.02
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Public Health Service (RNS055683A)
- National Institute of Neurological Disorders and Stroke (R21NS055683, R01NS060123)
- National Center for Research Resources (RR00862, P41RR000862, RR 022220, U54RR022220)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › 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 › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- autophagy regulation, Beclin-1, ATG14L, Rubicon, Vps34, class III phosphatidylinositol 3-kinase, UVRAG, autophagosome maturation, late endosomes, lysosomes, ATG5, ATG12, lipid kinase activity
- MeSH terms
- Beclin-1, Amino Acid Sequence, Animals, Autophagy, Cell Membrane, HeLa Cells, Humans, Lysosomes, Molecular Sequence Data, Protein Binding, Proteins, Endosomes, Phosphatidylinositol Phosphates, Phosphatidylinositol 3-Kinases, NIH 3T3 Cells, Adaptor Proteins, Signal Transducing, Green Fluorescent Proteins, Apoptosis Regulatory Proteins, Mice
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