Eaten alive: novel insights into autophagy from multicellular model systems

Zhang, Hong; Baehrecke, Eric H.

doi:10.1016/j.tcb.2015.03.001

Cited by 102Autophagy in Disease and TherapyGenetics, Aging, and Longevity in Model OrganismsCalcium signaling and nucleotide metabolism

Eaten alive: novel insights into autophagy from multicellular model systems

Open access

Zhang, Hong, Baehrecke, Eric H.·2015·Trends in Cell Biology

DOI 10.1016/j.tcb.2015.03.001PMC PMC4475674

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Abstract

Autophagy delivers cytoplasmic material to lysosomes for degradation. First identified in yeast, the core genes that control this process are conserved in higher organisms. Studies of mammalian cell cultures have expanded our understanding of the core autophagy pathway, but cannot reveal the unique animal-specific mechanisms for the regulation and function of autophagy. Multicellular organisms have different types of cells that possess distinct composition, morphology, and organization of intracellular organelles. In addition, the autophagic machinery integrates signals from other cells and environmental conditions to maintain cell, tissue and organism homeostasis. Here, we highlight how studies of autophagy in flies and worms have identified novel core autophagy genes and mechanisms, and provided insight into the context-specific regulation and function of autophagy.

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Apoptotic and autophagic machineries are highly interconnected during developmental cell death.
“Of note, the apoptotic and autophagic machineries are highly interconnected during developmental cell death [796].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [796]
The autophagic apparatus drives developmental clearance of apoptotic cells.
“In this context, the autophagic apparatus also drives the developmental clearance of apoptotic cells [796].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [796]

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Chang, T.-K., Shravage, B. V., Hayes, S. D., Powers, C. M., Simin, R. T., Wade Harper, J., & Baehrecke, E. H. (2013) · Nature Cell Biology · doi:10.1038/ncb2804 · Cited by 187 · see citing works
Self-citation
Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation
DeRenzo, C., Reese, K. J., & Seydoux, G. (2003) · Nature · doi:10.1038/nature01887 · Cited by 185 · see citing works
Effector caspase Dcp-1 and IAP protein Bruce regulate starvation-induced autophagy during Drosophila melanogaster oogenesis
Hou, Y.-C. C., Chittaranjan, S., Barbosa, S. G., McCall, K., & Gorski, S. M. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200712091 · Cited by 180 · see citing works
Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase.Preprint
Ogura, K., Wicky, C., Magnenat, L., Tobler, H., Mori, I., Müller, F., & Ohshima, Y. (1994) · Genes & Development · doi:10.1101/gad.8.20.2389 · Cited by 165 · see citing works
Unique insights into maternal mitochondrial inheritance in mice
Luo, S., Ge, Z., Wang, Z., Jiang, Z., Wang, Z., Ouyang, Y., Hou, Y., Schatten, H., & Sun, Q. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303231110 · Cited by 165 · see citing works
Segregation of germ granules in living Caenorhabditis elegans embryos: cell-type-specific mechanisms for cytoplasmic localisation
Hird, S. N., Paulsen, J. E., & Strome, S. (1996) · Development · doi:10.1242/dev.122.4.1303 · Cited by 163 · see citing works
Vacuolar Localization of Oligomeric α-Mannosidase Requires the Cytoplasm to Vacuole Targeting and Autophagy Pathway Components in Saccharomyces cerevisiae
Hutchins, M. U., & Klionsky, D. J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m101150200 · Cited by 157 · see citing works
Specification of the germ line
Strome, S. (2005) · WormBook · doi:10.1895/wormbook.1.9.1 · Cited by 149 · see citing works
The autophagy gene Wdr45/Wipi4 regulates learning and memory function and axonal homeostasis
Zhao, Y. G., Sun, L., Miao, G., Ji, C., Zhao, H., Sun, H., Miao, L., Yoshii, S. R., Mizushima, N., Wang, X., et al. (2015) · Autophagy · doi:10.1080/15548627.2015.1047127 · Cited by 148 · see citing works
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Paternal Mitochondrial Destruction after Fertilization Is Mediated by a Common Endocytic and Autophagic Pathway in Drosophila
Politi, Y., Gal, L., Kalifa, Y., Ravid, L., Elazar, Z., & Arama, E. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.04.005 · Cited by 146 · see citing works
Activation of autophagy during cell death requires the engulfment receptor Draper
Kary, C. S., Logan, M. A., Freeman, M. R., & Baehrecke, E. H. (2010) · Nature · doi:10.1038/nature09127 · Cited by 138 · see citing works
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Mice deficient in Epg5 exhibit selective neuronal vulnerability to degeneration
Zhao, H., Zhao, Y. G., Wang, X., Xu, L., Miao, L., Feng, D., Chen, Q., Kovács, A. L., Fan, D., & Zhang, H. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201211014 · Cited by 128 · see citing works
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TGF-β signaling
Savage‐Dunn, C. (2005) · WormBook · doi:10.1895/wormbook.1.22.1 · Cited by 125 · see citing works
The autophagic machinery is necessary for removal of cell corpses from the developing retinal neuroepithelium
Mellén, M., de la Rosa, E. J., & Boya, P. (2008) · Cell Death and Differentiation · doi:10.1038/cdd.2008.40 · Cited by 118 · see citing works
Atg9 Interacts with dTRAF2/TRAF6 to Regulate Oxidative Stress-Induced JNK Activation and Autophagy Induction
Tang, H.-W., Liao, H.-M., Peng, W.-H., Lin, H., Chen, C., & Chen, G. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.10.017 · Cited by 116 · see citing works
The Atg6/Vps30/Beclin 1 ortholog BEC-1 mediates endocytic retrograde transport in addition to autophagy inC. elegans
Ruck, A., Attonito, J. D., Garces, K. T., Núñez, L., Palmisano, N. J., Rubel, Z., Bai, Z., Nguyen, K. C. Q., Sun, L., Grant, B. D., et al. (2011) · Autophagy · doi:10.4161/auto.7.4.14391 · Cited by 114 · see citing works
Atg6 is required for multiple vesicle trafficking pathways and hematopoiesis in Drosophila
Shravage, B. V., Hill, J. H., Powers, C. M., Wu, L. P., & Baehrecke, E. H. (2013) · Development · doi:10.1242/dev.089490 · Cited by 108 · see citing works
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The SynMuv genes of Caenorhabditis elegans in vulval development and beyond
Fay, D. S., & Yochem, J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.03.016 · Cited by 103 · see citing works
The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51.Preprint
Ogura, K., Shirakawa, M., Barnes, T. M., Hekimi, S., & Ohshima, Y. (1997) · Genes & Development · doi:10.1101/gad.11.14.1801 · Cited by 88 · see citing works
Autophagy genes function sequentially to promote apoptotic cell corpse degradation in the engulfing cell
Li, W., Zou, W., Yang, Y., Chai, Y., Chen, B., Cheng, S., Tian, D., Wang, X., Vale, R. D., & Ou, G. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201111053 · Cited by 84 · see citing works
The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 inCaenorhabditis elegans
Ogura, K., & Goshima, Y. (2006) · Development · doi:10.1242/dev.02503 · Cited by 80 · see citing works
The scaffold protein EPG-7 links cargo–receptor complexes with the autophagic assembly machinery
Lin, L., Yang, P., Huang, X., Zhang, H., Lu, Q., & Zhang, H. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201209098 · Cited by 75 · see citing works
Self-citation
The p53-induced Gene Ei24 Is an Essential Component of the Basal Autophagy Pathway
Zhao, Y. G., Zhao, H., Miao, L., Wang, L., Sun, F., & Zhang, H. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.415968 · Cited by 72 · see citing works
Self-citation
Repression of Germline RNAi Pathways in Somatic Cells by Retinoblastoma Pathway Chromatin Complexes
Wu, X., Shi, Z., Cui, M., Han, M., & Ruvkun, G. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002542 · Cited by 70 · see citing works
epg-1 functions in autophagy-regulated processes and may encode a highly divergent Atg13 homolog in C. elegans
Tian, E., Wang, F.-X., Han, J.-H., & Zhang, H. (2009) · Autophagy · doi:10.4161/auto.5.5.8624 · Cited by 66 · see citing works
Self-citation
CUP-5, theC. elegansortholog of the mammalian lysosomal channel protein MLN1/TRPML1, is required for proteolytic degradation in autolysosomes
Sun, T., Wang, X., Lu, Q., Ren, H., & Zhang, H. (2011) · Autophagy · doi:10.4161/auto.7.11.17759 · Cited by 65 · see citing works
Self-citation
Genome‐wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development
Guo, B., Huang, X., Zhang, P., Qi, L., Liang, Q., Zhang, X., Huang, J. S., Fang, B., Hou, W., Han, J., et al. (2014) · EMBO Reports · doi:10.1002/embr.201338310 · Cited by 63 · see citing works
Self-citation
miR-14 Regulates Autophagy during Developmental Cell Death by Targeting ip3-kinase 2
Nelson, C., Ambros, V., & Baehrecke, E. H. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.09.011 · Cited by 61 · see citing works
Self-citation
Autophagy modulates miRNA‐mediated gene silencing and selectively degrades AIN‐1/GW182 in C. elegans
Zhang, P., & Zhang, H. (2013) · EMBO Reports · doi:10.1038/embor.2013.53 · Cited by 57 · see citing works
Self-citation
Autophagy genes function in apoptotic cell corpse clearance duringC. elegansembryonic development
Huang, S., Jia, K., Wang, Y., Zhou, Z., & Levine, B. (2012) · Autophagy · doi:10.4161/auto.22352 · Cited by 57 · see citing works
Arginine Methylation Modulates Autophagic Degradation of PGL Granules in C. elegans
Li, S., Yang, P., Tian, E., & Zhang, H. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.09.014 · Cited by 46 · see citing works
Self-citation
The C. elegans ATG101 homolog EPG-9 directly interacts with EPG-1/Atg13 and is essential for autophagy
Liang, Q., Yang, P.-G., Tian, E., Han, J.-H., & Zhang, H. (2012) · Autophagy · doi:10.4161/auto.21163 · Cited by 46 · see citing works
Self-citation
Autophagy genes coordinate with the class II PI/PtdIns 3-kinase PIKI-1 to regulate apoptotic cell clearance inC. elegans
Cheng, S., Wu, Y., Lu, Q., Yan, J., Zhang, H., & Wang, X. (2013) · Autophagy · doi:10.4161/auto.26323 · Cited by 44 · see citing works
Self-citation
Autophagy regulates tissue overgrowth in a context-dependent manner
Pérez, E., Das, G., Bergmann, A., & Baehrecke, E. H. (2014) · Oncogene · doi:10.1038/onc.2014.285 · Cited by 43 · see citing works
Self-citation
Autophagy activity contributes to programmed cell death inCaenorhabditis elegans
Wang, H., Lu, Q., Cheng, S., Wang, X., & Zhang, H. (2013) · Autophagy · doi:10.4161/auto.26152 · Cited by 39 · see citing works
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Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018.
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., et al. (2018) · Cell Death & Differentiation · doi:10.1038/s41418-017-0012-4 · Cited by 6,680 · see citing works
“Of note, the apoptotic and autophagic machineries are highly interconnected during developmental cell death [796].”
BackgroundSelf-citation
Life, death and autophagy
Doherty, J., & Baehrecke, E. H. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0201-5 · Cited by 626 · see citing works
Self-citation
Autophagy: machinery and regulation
Yin, Z., Pascual, C., & Klionsky, D. J. (2016) · Microbial Cell · doi:10.15698/mic2016.12.546 · Cited by 567 · see citing works
“During ovary development, caspases are needed for autophagy induction under stress conditions, whereas nurse cell apoptosis requires autophagic clearance of its inhibitor, Bruce [21].”
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
“…with the ER and is also linked to the ER by tubular membrane extensions, collectively referred to as ER–IM contacts (Hayashi-Nishino et al., 2009; Ylä-Anttila et al., 2009), at which lipid transfer between the ER and IMs may occur (Prinz, 2014; Phillips and Voeltz, 2016; Zhang and Hu, 2016).”
BackgroundSelf-citation
Regulation of Liver Metabolism by Autophagy
Madrigal‐Matute, J., & Cuervo, A. M. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.09.042 · Cited by 312 · see citing works
Autophagy in bone homeostasis and the onset of osteoporosis
Yin, X., Zhou, C., Li, J., Liu, R., Shi, B., Yuan, Q., & Zou, S. (2019) · Bone Research · doi:10.1038/s41413-019-0058-7 · Cited by 235 · see citing works
Autophagy in the eye: Development, degeneration, and aging
Boya, P., Esteban‐Martínez, L., Serrano‐Puebla, A., Gómez‐Sintes, R., & Villarejo‐Zori, B. (2016) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2016.08.001 · Cited by 231 · see citing works
KIF1A/UNC-104 Transports ATG-9 to Regulate Neurodevelopment and Autophagy at Synapses
Stavoe, A. K. H., Kargbo-Hill, S. E., Hall, D. H., & Colón-Ramos, D. A. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.06.012 · Cited by 211 · see citing works
Lysosomal cell death mechanisms in aging
Gómez-Sintes, R., Ledesma, M. D., & Boya, P. (2016) · Ageing Research Reviews · doi:10.1016/j.arr.2016.02.009 · Cited by 216 · see citing works
Mechanisms of Selective Autophagy in Normal Physiology and Cancer
Mancias, J. D., & Kimmelman, A. C. (2016) · Journal of Molecular Biology · doi:10.1016/j.jmb.2016.02.027 · Cited by 196 · see citing works
“Likewise, the field will continue to learn from studying selective autophagy pathways using in vivo models[121,197].”
Background
Guidelines and recommendations on yeast cell death nomenclature
Carmona‐Gutiérrez, D., Bauer, M. A., Zimmermann, A., Aguilera, A., Austriaco, N. P. G., Ayscough, K. R., Balzan, R., Bar‐Nun, S., Barrientos, A., Belenky, P. A., et al. (2017) · Microbial Cell · doi:10.15698/mic2018.01.607 · Cited by 187 · see citing works
Liquid–liquid phase separation in autophagy
Noda, N. N., Wang, Z., & Zhang, H. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.202004062 · Cited by 168 · see citing works
“P granule proteins in somatic blastomeres are quickly disassembled and removed, resulting in exclusive localization of P granules in the germline blastomeres and eventually in the germline precursor cells Z2 and Z3 (Fig. 3 B; Strome, 2005; Zhang and Baehrecke, 2015).”
BackgroundSelf-citation
Research progress on morphology and mechanism of programmed cell death
Chen, Y., Li, X., Yang, M., & Liu, S. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06712-8 · Cited by 160 · see citing works
“…[1, 42], and its morphological feature is the observation of double-membrane phagocytic components containing vesicles, namely, autophagosomes; the expansion and fragmentation of the endoplasmic reticulum, mitochondria and other organelles; and the slight agglutination of chromatin [43, 44] (Fig.”
Background
The lysosomal membrane protein LAMP2A promotes autophagic flux and prevents SNCA-induced Parkinson disease-like symptoms in the Drosophila brain
Issa, A.-R., Sun, J., Petitgas, C., Mesquita, A., Dulac, A., Robin, M., Mollereau, B., Jenny, A., Chérif‐Zahar, B., & Birman, S. (2018) · Autophagy · doi:10.1080/15548627.2018.1491489 · Cited by 152 · see citing works
Autophagy in stem cell aging
Revuelta, M., & Matheu, A. (2017) · Aging Cell · doi:10.1111/acel.12655 · Cited by 146 · see citing works
“…process implies the incorporation of proteins, organelles, and cytoplasm in a structure called the autophagosome, which once formed fuses with the lysosome to form autolysosomes and then releasing its content in the lysosomal lumen where it is degraded via acid hydrolases (Zhang & Baehrecke, 2015).”
Background
Beyond apoptosis: evidence of other regulated cell death pathways in the ovary throughout development and life
Stringer, J. M., Alesi, L. R., Winship, A., & Hutt, K. J. (2023) · Human Reproduction Update · doi:10.1093/humupd/dmad005 · Cited by 145 · see citing works
Role of chaperone‐mediated autophagy in metabolism
Tasset, I., & Cuervo, A. M. (2016) · FEBS Journal · doi:10.1111/febs.13677 · Cited by 144 · see citing works
Phase Separation, Transition, and Autophagic Degradation of Proteins in Development and Pathogenesis
Wang, Z., & Zhang, H. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.01.008 · Cited by 117 · see citing works
Self-citation
Protease signaling in animal and plant‐regulated cell death
Salvesen, G. S., Hempel, A., & Coll, N. S. (2015) · FEBS Journal · doi:10.1111/febs.13616 · Cited by 104 · see citing works
Structural Basis of the Differential Function of the Two C. elegans Atg8 Homologs, LGG-1 and LGG-2, in Autophagy
Wu, F., Watanabe, Y., Guo, X., Qi, X., Wang, P., Zhao, H., Wang, Z., Fujioka, Y., Hui, Z., Jin-Qi, R. E. N., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.11.019 · Cited by 103 · see citing works
“It has been largely assumed that during multicellular organism development, an autophagy gene is equally employed for removal of distinct cargo at different developmental stages (Zhang and Baehrecke, 2015).”
Self-citation
Regulation of morphine-induced synaptic alterations: Role of oxidative stress, ER stress, and autophagy
Cai, Y., Yang, L., Hu, G.-K., Chen, X., Niu, F., Yuan, L., Liu, H., Xiong, H., Arikkath, J., & Buch, S. (2016) · Journal of Cell Biology · doi:10.1083/jcb.201605065 · Cited by 102 · see citing works
“The role of autophagy in morphinemediated regulation of excitatory and inhibitory synapses Autophagy is an intracellular process that delivers cellular organelles and misfolded proteins from the autophagosomes to the lysosomes for degradation (Zhang and Baehrecke, 2015).”
Background
Genes associated with Parkinson's disease: regulation of autophagy and beyond
Beilina, A. G., & Cookson, M. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13266 · Cited by 93 · see citing works
Autophagy and primary cilia: dual interplay
Pampliega, O., & Cuervo, A. M. (2016) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2016.01.008 · Cited by 86 · see citing works
“Introduction Autophagy is a highly conserved intracellular process for the degradation of proteins and organelles in lysosomes [1].”
Background
Mechanisms and Pathophysiological Roles of the ATG8 Conjugation Machinery
Lystad, A. H., & Simonsen, A. (2019) · Cells · doi:10.3390/cells8090973 · Cited by 85 · see citing works
Expression of WIPI2B counteracts age-related decline in autophagosome biogenesis in neurons
Stavoe, A. K., Gopal, P. P., Gubas, A., Tooze, S. A., & Holzbaur, E. L. (2019) · eLife · doi:10.7554/elife.44219 · Cited by 82 · see citing works
The metabolic cross‐talk between epithelial cancer cells and stromal fibroblasts in ovarian cancer progression: Autophagy plays a role
Thuwajit, C., Ferraresi, A., Titone, R., Thuwajit, P., & Isidoro, C. (2017) · Medicinal Research Reviews · doi:10.1002/med.21473 · Cited by 84 · see citing works
Formation and maturation of autophagosomes in higher eukaryotes: a social network
Zhao, Y. G., & Zhang, H. (2018) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2018.04.003 · Cited by 71 · see citing works
Self-citation
Development of LC3/GABARAP sensors containing a LIR and a hydrophobic domain to monitor autophagy
Lee, Y., Jun, Y., Choi, H., Huh, Y. H., Kaang, B., Jang, D., & Lee, J. (2017) · The EMBO Journal · doi:10.15252/embj.201696315 · Cited by 66 · see citing works
“Extensive genetic studies in yeast and mammals have identified several autophagy-related genes ( ~ 40 genes in yeast) with specific roles in the autophagy pathway (Feng et al , 2014; Zhang & Baehrecke, 2015).”
Mitochondrial protein import regulates cytosolic protein homeostasis and neuronal integrity
Liu, W., Duan, X., Fang, X., Shang, W., & Tong, C. (2018) · Autophagy · doi:10.1080/15548627.2018.1474991 · Cited by 67 · see citing works
“To understand how autophagy processes are misregulated in Tom40 RNAi tissues, we carried out single and double-RNAi experiments to knockdown the expression of various core molecules of the autophagy pathway [40], alone or together with Tom40, and analyzed the patterns of ubiquitinated aggregates and Atg8a.”
Background
Reciprocal Crosstalk Between Autophagic and Endocrine Signaling in Metabolic Homeostasis
Sinha, R. A., Singh, B. K., & Yen, P. M. (2016) · Endocrine Reviews · doi:10.1210/er.2016-1103 · Cited by 63 · see citing works
“autophagy in mammals, however, there has been much work on the endocrine regulation of autophagy in invertebrates and have been well described elsewhere (85, 86).”
Background
Current questions and possible controversies in autophagy
Lindqvist, L., Simon, A. K., & Baehrecke, E. H. (2015) · Cell Death Discovery · doi:10.1038/cddiscovery.2015.36 · Cited by 62 · see citing works
Self-citation
USP19 (ubiquitin specific peptidase 19) promotes TBK1 (TANK-binding kinase 1) degradation via chaperone-mediated autophagy
Zhao, X., Di, Q., Yu, J., Quan, J., Xiao, Y., Zhu, H., Li, H., Jing, L., & Chen, W. (2021) · Autophagy · doi:10.1080/15548627.2021.1963155 · Cited by 61 · see citing works
“mode of cargo delivery to the lysosome [6,7].”
Background
Core autophagy genes and human diseases
Zhao, Y. G., & Zhang, H. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.08.003 · Cited by 54 · see citing works
Self-citation
The interplay of autophagy and non-apoptotic cell death pathways
(2020) · International Review of Cell and Molecular Biology · doi:10.1016/bs.ircmb.2019.12.004 · Cited by 50 · see citing works
Osteoporosis and autophagy: What is the relationship?
Florencio‐Silva, R., Sasso, G. R. D. S., Simões, M. D. J., Simões, R. S., Baracat, M. C. P., Sasso‐Cerri, E., & Cerri, P. S. (2017) · Revista da Associação Médica Brasileira · doi:10.1590/1806-9282.63.02.173 · Cited by 52 · see citing works
“Get the Balance Right”: Pathological Significance of Autophagy Perturbation in Neuromuscular Disorders
Castets, P., Frank, S., Sinnreich, M., & Rüegg, M. A. (2016) · Journal of Neuromuscular Diseases · doi:10.3233/jnd-160153 · Cited by 49 · see citing works
“1).”
Icariin alleviates osteoarthritis through PI3K/Akt/mTOR/ULK1 signaling pathway
Chen, Y., Pan, X., Zhao, J., Li, C., Lin, Y., Wang, Y., Liu, X., & Tian, M. (2022) · European journal of medical research · doi:10.1186/s40001-022-00820-x · Cited by 49 · see citing works
“Under stress conditions, the inactivation of mTOR can promote the formation of the ULK complex, and the ULK1/FIP200/Atg13 complex is essential for the formation of autophagosomes [33, 34].”
Background
Asperuloside alleviates osteoporosis by promoting autophagy and regulating Nrf2 activation
Huang, F., Wang, Y., Liu, J., Cheng, Y., Zhang, X., & Jiang, H. (2024) · Journal of Orthopaedic Surgery and Research · doi:10.1186/s13018-024-05320-8 · Cited by 45 · see citing works
20(S)-ginsenoside Rg3 sensitizes human non-small cell lung cancer cells to icotinib through inhibition of autophagy
Wang, X., Zhou, R., Zhang, N., & Zhao, J. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.02.023 · Cited by 45 · see citing works
USP8 maintains embryonic stem cell stemness via deubiquitination of EPG5
Gu, H., Shi, X.-X., Liu, C., Wang, C., Sui, N., Zhao, Y., Gong, J., Wang, F., Zhang, H., Li, W., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09430-4 · Cited by 43 · see citing works
Self-citation
Autophagy promotes programmed cell death and corpse clearance in specific cell types of the Arabidopsis root cap
Feng, Q., Rycke, R. M. D., Dagdas, Y., & Nowack, M. K. (2022) · Current Biology · doi:10.1016/j.cub.2022.03.053 · Cited by 44 · see citing works
Gemcitabine and mitomycin induced autophagy regulates cancer stem cell pool in urothelial carcinoma cells
Ojha, R., Jha, V., & Singh, S. K. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2015.12.002 · Cited by 41 · see citing works
Autophagy in Reproduction
Gao, H., Khawar, M. B., & Li, W. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-0602-4_21 · Cited by 39 · see citing works
The neuron-astrocyte-microglia triad in CA3 after chronic cerebral hypoperfusion in the rat: Protective effect of dipyridamole
Lana, D., Ugolini, F., Melani, A., Nosi, D., Pedata, F., & Giovannini, M. G. (2017) · Experimental Gerontology · doi:10.1016/j.exger.2017.06.006 · Cited by 36 · see citing works
Differential activation of eMI by distinct forms of cellular stress
Mesquita, A., Glenn, J., & Jenny, A. (2020) · Autophagy · doi:10.1080/15548627.2020.1783833 · Cited by 35 · see citing works
The Proton-Coupled Monocarboxylate Transporter Hermes Is Necessary for Autophagy during Cell Death
Velentzas, P. D., Zhang, L., Das, G., Chang, T.-K., Nelson, C., Kobertz, W. R., & Baehrecke, E. H. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.09.015 · Cited by 31 · see citing works
“, 2013) and hormones (Baehrecke, 2000), and studies in animals indicate that autophagy has complex regulation and functions in different cell contexts (Zhang and Baehrecke, 2015).”
BackgroundSelf-citation
The impact of age and frailty on skeletal muscle autophagy markers and specific strength: A cross-sectional comparison
Aas, S. N., Hamarsland, H., Cumming, K. T., Rognlien, S. H., Aase, O. J., Nordseth, M., Karsrud, S., Godager, S., Tømmerbakke, D., Handegard, V., et al. (2019) · Experimental Gerontology · doi:10.1016/j.exger.2019.110687 · Cited by 34 · see citing works
Autophagosomes fuse to phagosomes and facilitate the degradation of apoptotic cells in Caenorhabditis elegans
Peña-Ramos, O., Chiao, L. J., Liu, X., Yu, X., Yao, T., He, H., & Zhou, Z. (2022) · eLife · doi:10.7554/elife.72466 · Cited by 35 · see citing works
Calcium ions trigger the exposure of phosphatidylserine on the surface of necrotic cells
Furuta, Y., Peña-Ramos, O., Li, Z., Chiao, L. J., & Zhou, Z. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009066 · Cited by 33 · see citing works
“homolog of yeast ATG1 and mammalian ULK1 (UNC-51-like autophagy activating kinase), an important component of the autophagy pathway [57].”
Background
A conserved myotubularin-related phosphatase regulates autophagy by maintaining autophagic flux
Allen, E. A., Amato, C., Fortier, T. M., Velentzas, P. D., Wood, W., & Baehrecke, E. H. (2020) · The Journal of Cell Biology · doi:10.1083/jcb.201909073 · Cited by 32 · see citing works
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Do Fungi Undergo Apoptosis-Like Programmed Cell Death?
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Authors: Zhang, H., & Baehrecke, E. H.
Affiliations: Chinese Academy of Sciences (CN)
University of Massachusetts Chan Medical School (US)
Corresponding author: Zhang, Hong
Baehrecke, Eric H.
ORCID: Zhang, Hong
Baehrecke, Eric H.
Venue: Trends in Cell Biology
Publisher: Elsevier BV
Published: 2015-07
Volume: 25
Issue: 7
Pages: 376-387
ISSN: 0962-8924 (ISSN-L)
DOI: 10.1016/j.tcb.2015.03.001
PMC: PMC4475674
OpenAlex: W2067636508
Cited by: 102
References: 118
Citations by year: 2026: 3 · 2025: 5 · 2024: 4 · 2023: 1 · 2022: 11 · 2021: 13 · 2020: 7 · 2019: 12 · 2018: 13 · 2017: 10 · 2016: 16 · 2015: 7
FWCI: 1.99
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Trends in Cell Biology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
Funders: National Cancer Institute (R01CA159314, CA159314)
National Institute of General Medical Sciences (GM111658, GM079431, R01GM079431, R01GM111658)
National Institute of Allergy and Infectious Diseases (AI099708, R01AI099708)
Topics: Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
Keywords: autophagy, multicellular organisms, Drosophila, Caenorhabditis elegans, autophagy-related genes, lysosomal degradation, tissue homeostasis, cell-to-cell communication, autophagy regulation
MeSH terms: Animals, Autophagy, Drosophila melanogaster, Gene Expression Regulation, Homeostasis, Humans, Lysosomes, Models, Biological, Organ Specificity, Protein Kinases, Saccharomyces cerevisiae, Species Specificity, Ubiquitins, Signal Transduction, Caenorhabditis elegans

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Eaten alive: novel insights into autophagy from multicellular model systems

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