High autophagic flux guards ESC identity through coordinating autophagy machinery gene program by FOXO1
Open accessAbstract
Although much is known about transcriptional networks that control embryonic stem cell (ESC) self-renewal and differentiation, the metabolic regulation of ESC is less clear. Autophagy is a catabolic process that is activated under both stress and normal conditions to degrade damaged organelles and aggregated proteins, and thus plays pivotal roles in somatic and adult stem cell function. However, if and how ESCs harness autophagy to regulate stemness remains largely unknown. Recently, we have defined that autophagy is essential for mitochondrial homeostasis regulation in pluripotency acquirement and maintenance. Here we identified high autophagic flux as an essential mechanism to maintain ESC identity. We show that mouse ESCs exhibit a high autophagic flux that is maintained by coordinating expression of autophagy core molecular machinery genes through FOXO1, a forkhead family transcription factor. Tapering autophagic flux by manipulating either Atg3 or Foxo1 expression compromised ESC self-renewal, pluripotency, and differentiation that could be restored by gain of wild-type but not function-deficient Atg3 or Foxo1 mutants, respectively. Our results define a newly recognized role of autophagic flux in mouse ESC identity maintenance that links cellular catabolism to ESC fate regulation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Proficient autophagic responses most often mediate cytoprotective rather than cytotoxic effects in adaptation to stress.
“Proficient autophagic responses (which are under tight transcriptional and post-translational regulation) [509 799–805] most often operate at the hub of adaptation to stress, hence mediating cytoprotective (rather than cytotoxic) effects [806–811].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [811]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Repertoires of Autophagy in the Pathogenesis of Ocular Diseases
Li, Y., Jiang, Q. L., Cao, G.-F., Yao, J., & Yan, B. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000373980 · Cited by 16,351 · see citing works
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197 · see citing works
AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1
Kim, J., Kundu, M., Viollet, B., & Guan, K.-L. (2011) · Nature Cell Biology · doi:10.1038/ncb2152 · Cited by 7,227 · see citing works
Methods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497 · see citing works
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
Regulation mechanisms and signaling pathways of autophagy
He, C., & Klionsky, D. J. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102808-114910 · Cited by 3,609 · see citing works
TFEB Links Autophagy to Lysosomal Biogenesis
Settembre, C., Di Malta, C., Polito, V. A., Arencibia, M. G., Vetrini, F., Erdin, S., Erdin, S. U., Huynh, T., Medina, D., Colella, P., et al. (2011) · Science · doi:10.1126/science.1204592 · Cited by 3,365 · see citing works
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 · see citing works
A Gene Network Regulating Lysosomal Biogenesis and Function
Sardiello, M., Palmieri, M., di Ronza, A., Medina, D. L., Valenza, M., Gennarino, V. A., Di Malta, C., Donaudy, F., Embrione, V., Polishchuk, R. S., et al. (2009) · Science · doi:10.1126/science.1174447 · Cited by 2,543 · see citing works
Cepharanthine potently enhances the sensitivity of anticancer agents in K562 cells
Ikeda, R., Che, X., Yamaguchi, T., Ushiyama, M., Zheng, C., Okumura, H., Takeda, Y., Shibayama, Y., Nakamura, K. T., Jeung, H., et al. (2005) · Cancer Science · doi:10.1111/j.1349-7006.2005.00057.x · Cited by 2,268 · see citing works
Nutrient-dependent mTORC1 Association with the ULK1–Atg13–FIP200 Complex Required for Autophagy
Hosokawa, N., Hara, T., Kaizuka, T., Kishi, C., Takamura, A., Miura, Y., Iemura, S.-I., Natsume, T., Takehana, K., Yamada, N., et al. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-12-1248 · Cited by 2,076 · 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
Self-citationMammalian 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 · see citing works
FoxO3 Controls Autophagy in Skeletal Muscle In Vivo
Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., et al. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.001 · Cited by 1,953 · see citing works
Autophagy: from phenomenology to molecular understanding in less than a decade
Klionsky, D. J. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2245 · Cited by 1,938 · see citing works
Autophagy in mammalian development and differentiation
Mizushima, N., & Levine, B. (2010) · Nature Cell Biology · doi:10.1038/ncb0910-823 · Cited by 1,555 · see citing works
Termination of autophagy and reformation of lysosomes regulated by mTOR
Yu, L., McPhee, C. K., Zheng, L., Mardones, G. A., Rong, Y., Peng, J., Mi, N., Zhao, Y., Liu, Z., Wan, F., et al. (2010) · Nature · doi:10.1038/nature09076 · Cited by 1,544 · see citing works
g:Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments
Reimand, J., Kull, M., Peterson, H., Hansen, J., & Vilo, J. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm226 · Cited by 1,525 · see citing works
Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., & Goldberg, A. L. (2007) · Cell Metabolism · doi:10.1016/j.cmet.2007.11.004 · Cited by 1,489 · see citing works
Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks
Alers, S., Löffler, A. S., Wesselborg, S., & Stork, B. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06159-11 · Cited by 1,483 · see citing works
Immunogenicity of induced pluripotent stem cells
Zhao, T., Zhang, Z., Rong, Z., & Xu, Y. (2011) · Nature · doi:10.1038/nature10135 · Cited by 1,449 · 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
Autophagy maintains stemness by preventing senescence
García-Prat, L., Martínez-Vicente, M., Perdiguero, E., Ortet, L., Rodríguez-Ubreva, J., Rebollo, E., Ruiz-Bonilla, V., Gutarra, S., Ballestar, E., Serrano, A. L., et al. (2016) · Nature · doi:10.1038/nature16187 · Cited by 1,355 · see citing works
Phosphorylation of ribosomal protein S6 is inhibitory for autophagy in isolated rat hepatocytes
Blommaart, E. F. C., Luiken, J. J. F. P., Blommaart, P. J. E., van Woerkom, G. M., & Meijer, A. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.5.2320 · Cited by 686 · see citing works
Metabolic Plasticity in Stem Cell Homeostasis and Differentiation
Folmes, C. D. L., Dzeja, P. P., Nelson, T. J., & Terzic, A. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.10.002 · Cited by 664 · see citing works
FOXO3A directs a protective autophagy program in haematopoietic stem cells
Warr, M. R., Binnewies, M., Flach, J., Reynaud, D., Garg, T., Malhotra, R., Debnath, J., & Passegué, E. (2013) · Nature · doi:10.1038/nature11895 · Cited by 625 · see citing works
FOXO transcription factors: key regulators of cellular quality control
Webb, A. E., & Brunet, A. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.02.003 · Cited by 620 · see citing works
FoxO transcription factors in the maintenance of cellular homeostasis during aging
Salih, D. A., & Brunet, A. (2008) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2008.02.005 · Cited by 604 · see citing works
Nutrient-sensing nuclear receptors coordinate autophagy
Lee, J. M., Wagner, M., Xiao, R., Kim, K. H., Feng, D., Lazar, M. A., & Moore, D. D. (2014) · Nature · doi:10.1038/nature13961 · Cited by 514 · see citing works
Sou, Y., Waguri, S., Iwata, J.-I., Ueno, T., Fujimura, T., Hara, T., Sawada, N., Yamada, A., Mizushima, N., Uchiyama, Y., et al. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-03-0309 · Cited by 475 · see citing works
Metabolic Regulation in Pluripotent Stem Cells during Reprogramming and Self-Renewal
Zhang, J., Nuebel, E., Daley, G. Q., Koehler, C. M., & Teitell, M. A. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.10.005 · Cited by 465 · see citing works
Transcriptional regulation of autophagy by an FXR–CREB axis
Seok, S., Fu, T., Choi, S., Yang, L., Zhu, R., Kumar, S., Sun, X., Yoon, G., KANG, Y. Y., Zhong, W., et al. (2014) · Nature · doi:10.1038/nature13949 · Cited by 428 · see citing works
FoxO Transcription Factors Promote Autophagy in Cardiomyocytes
Sengupta, A., Molkentin, J. D., & Yutzey, K. E. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.024406 · Cited by 428 · see citing works
Increased proteasome activity in human embryonic stem cells is regulated by PSMD11
Vilchez, D., Boyer, L., Morantte, I., Lutz, M., Merkwirth, C., Joyce, D., Spencer, B., Page, L., Masliah, E., Berggren, W. T., et al. (2012) · Nature · doi:10.1038/nature11468 · Cited by 388 · see citing works
Protein Synthesis upon Acute Nutrient Restriction Relies on Proteasome Function
Vabulas, R. M., & Hartl, F. U. (2005) · Science · doi:10.1126/science.1121925 · Cited by 339 · see citing works
ZKSCAN3 Is a Master Transcriptional Repressor of Autophagy
Chauhan, S., Jinesh, G. G., Chauhan, S. C., Manyam, G. C., Wang, J., Kamat, A. M., & Boyd, D. D. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.024 · Cited by 276 · see citing works
Nath, S., Dancourt, J., Shteyn, V., Puente, G., Fong, W. M., Nag, S., Bewersdorf, J., Yamamoto, A., Antonny, B., & Melia, T. J. (2014) · Nature Cell Biology · doi:10.1038/ncb2940 · Cited by 269 · see citing works
Lübke, T., Lobel, P., & Sleat, D. (2008) · Biochimica et Biophysica Acta · doi:10.1016/j.bbamcr.2008.09.018 · Cited by 267 · see citing works
FOXO1 is an essential regulator of pluripotency in human embryonic stem cells
Zhang, X., Yalcin, S., Lee, D., Yeh, T.-Y. J., Lee, S.-M., Su, J., Mungamuri, S. K., Rimmelé, P., Kennedy, M., Sellers, R. S., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2293 · Cited by 262 · see citing works
Wang, S., Xia, P., Ye, B., Huang, G., Liu, J., & Fan, Z. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.10.005 · Cited by 209 · see citing works
Atg5-independent autophagy regulates mitochondrial clearance and is essential for iPSC reprogramming
Ma, T., Li, J., Xu, Y., Chen, Y., Xu, T., Wang, H., Liu, K., Cao, N., Nie, B., Zhu, S., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3256 · Cited by 167 · see citing works
Self-citationAutophagy Driven by a Master Regulator of Hematopoiesis
Kang, Y.-A., Sanalkumar, R., O'Geen, H., Linnemann, A. K., Chang, C.-J., Bouhassira, E. E., Farnham, P. J., Keles, S., & Bresnick, E. H. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06166-11 · Cited by 153 · see citing works
Liu, K., Zhao, Q., Liu, P., Cao, J., Gong, J., Wang, C., Wang, W., Li, X., Sun, H., Zhang, C., et al. (2016) · Autophagy · doi:10.1080/15548627.2016.1212786 · Cited by 92 · see citing works
Self-citationAutophagy and mTORC1 regulate the stochastic phase of somatic cell reprogramming
Wu, Y., Li, Y., Zhang, H., Huang, Y., Zhao, P., Tang, Y., Qiu, X., Yue, Y., Li, W., Ni, S., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3172 · Cited by 85 · see citing works
Self-citationZhang, C., Cao, J., Li, X., Xu, H., Wang, W., Wang, L., Zhao, X., Li, W., Jiao, J., Hu, B., et al. (2016) · Science China Life Sciences · doi:10.1007/s11427-016-0114-9 · Cited by 59 · see citing works
Self-citationCells derived from iPSC can be immunogenic — Yes or No?
Cao, J., Li, X., Xiao, L., Zhang, C., Yu, H., & Zhao, T. (2014) · Protein & Cell · doi:10.1007/s13238-013-0003-2 · Cited by 58 · see citing works
Self-citationUnderstanding the roadmaps to induced pluripotency
Liu, K., Song, Y., Yu, H., & Zhao, T. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.205 · Cited by 36 · see citing works
Self-citationArriola, D. J., Mayo, S. L., Skarra, D. V., Benson, C. A., & Thackray, V. G. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.362103 · Cited by 36 · see citing works
Immunogenicity and functional evaluation of iPSC-derived organs for transplantation
Wang, L., Cao, J., Wang, Y., Lan, T., Liu, L., Wang, W., Jin, N., Gong, J., Zhang, C., Teng, F., et al. (2015) · Cell Discovery · doi:10.1038/celldisc.2015.15 · Cited by 24 · see citing works
Self-citationp18 inhibits reprogramming through inactivation of Cdk4/6
Zhu, S., Cao, J., Sun, H., Liu, K., Li, Y., & Zhao, T. (2016) · Scientific Reports · doi:10.1038/srep31085 · Cited by 15 · see citing works
Self-citationStem cell, basis and application
Li, J. (2015) · 中国科学通报：英文版 · doi:10.1007/s11434-015-0908-7 · Cited by 7 · see citing works
Progress in understanding epigenetic remodeling during induced pluripotency
Gao, R., Liu, X., & Gao, S. (2015) · 中国科学通报：英文版 · doi:10.1007/s11434-015-0919-4 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2013; 13: 132-141.
Cited by
Sorted by citations
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
NAD+ metabolism, stemness, the immune response, and cancer
Navas, L. E., & Carnero, A. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00354-w · Cited by 529 · see citing works
The FoxO–Autophagy Axis in Health and Disease
Cheng, Z. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.07.009 · Cited by 257 · see citing works
Beclin1-mediated interplay between autophagy and apoptosis: New understanding
Prerna, K., & Dubey, V. K. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.02.005 · Cited by 209 · see citing works
Autophagy in stem cells: repair, remodelling and metabolic reprogramming
Boya, P., Codogno, P., & Rodriguez-Muela, N. (2018) · Development · doi:10.1242/dev.146506 · Cited by 197 · see citing works
Autophagy and the Wnt signaling pathway: A focus on Wnt/β-catenin signaling
Lorzadeh, S., Kohan, L., Ghavami, S., & Azarpira, N. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2020.118926 · Cited by 174 · see citing works
Koyuncu, S., Saez, I., Lee, H. J., Gutiérrez-García, R., Pokrzywa, W., Fatima, A., Hoppe, T., & Vilchez, D. (2018) · Nature Communications · doi:10.1038/s41467-018-05320-3 · Cited by 97 · see citing works
The physiological roles of autophagy in the mammalian life cycle
Wang, L., Ye, X., & Zhao, T. (2018) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12464 · Cited by 103 · see citing works
Self-citationAutophagy maintains the stemness of ovarian cancer stem cells by FOXA2.
Peng, Q., Qin, J., Zhang, Y., Cheng, X., Wang, X., Lü, W., Xie, X., & Zhang, S. (2017) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-017-0644-8 · Cited by 99 · see citing works
Hassanpour, M., Rezabakhsh, A., Pezeshkian, M., Rahbarghazi, R., & Nouri, M. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1060-5 · Cited by 80 · see citing works
Modulation of autophagy as new approach in mesenchymal stem cell-based therapy
Jakovljevic, J., Harrell, C. R., Fellabaum, C., Arsenijević, A., Jovicic, N. U., & Volarević, V. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.05.061 · Cited by 67 · see citing works
Binding Features and Functions of ATG3
Fang, D., Xie, H., Hu, T., Shan, H., & Li, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.685625 · Cited by 60 · see citing works
Noormohammadi, A., Calculli, G., Gutiérrez-García, R., Khodakarami, A., Koyuncu, S., & Vı́lchez, D. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2602-1 · Cited by 53 · see citing works
Liu, K., Zhao, Q., Sun, H., Liu, L., Wang, C., Li, Z., Xu, Y., Wang, L., Zhang, L., Zhang, H., et al. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-04795-9 · Cited by 47 · see citing works
Self-citationGong, J., Gu, H., Zhao, L., Wang, L., Liu, P., Wang, F., Xu, H., & Zhao, T. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0054-z · Cited by 45 · see citing works
Self-citationLudikhuize, M. C., & Colman, M. J. R. (2020) · Antioxidants and Redox Signaling · doi:10.1089/ars.2020.8126 · 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-citationProtein quality control of cell stemness
Yan, P., Ren, J., Zhang, W., Qu, J. T., & Liu, G. (2020) · Cell Regeneration · doi:10.1186/s13619-020-00064-2 · Cited by 40 · see citing works
Nutrients in the fate of pluripotent stem cells
Lu, V., Roy, I. J., & Teitell, M. A. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2021.09.013 · Cited by 39 · see citing works
Zhao, C., Lin, K., & Wang, X. (2020) · Applied Materials Today · doi:10.1016/j.apmt.2020.100614 · Cited by 35 · see citing works
Dissection of two routes to naïve pluripotency using different kinase inhibitors
Martínez‐Val, A., Lynch, C. J., Calvo, I., Ximénez‐Embún, P., Garcı́a, F., Zarzuela, E., Serrano, M., & Muñoz, J. (2021) · Nature Communications · doi:10.1038/s41467-021-22181-5 · Cited by 26 · see citing works
Zhāng, Q., Wan, X.-X., Hu, X., Zhao, W., Ban, X.-X., Huang, Y., Yan, W., & Xiong, K. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.809656 · Cited by 28 · see citing works
Xiong, G., Tang, W., Zhang, D., He, D., Wei, G., Atala, A., Liang, X., Bleyer, A. J., Bleyer, M. E., Yu, J., et al. (2019) · Theranostics · doi:10.7150/thno.34050 · Cited by 28 · see citing works
Cellular metabolism and homeostasis in pluripotency regulation
Liu, K., Cao, J., Shi, X.-X., Wang, L., & Zhao, T. (2020) · Protein & Cell · doi:10.1007/s13238-020-00755-1 · Cited by 26 · see citing works
Self-citationThe intrinsic proteostasis network of stem cells
Llamas, E., Alirzayeva, H., Loureiro, R., & Vı́lchez, D. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.08.005 · Cited by 27 · see citing works
Autophagy induction during stem cell activation plays a key role in salivary gland self-renewal
Orhon, I., Rocchi, C., Villarejo‐Zori, B., Martinez, P. S., Baanstra, M., Brouwer, U., Boya, P., Coppes, R. P., & Reggiori, F. (2021) · Autophagy · doi:10.1080/15548627.2021.1924036 · Cited by 26 · see citing works
mTORC 1‐ PGC 1 axis regulates mitochondrial remodeling during reprogramming
Wang, L., Xu, X., Jiang, C., Ma, G., Huang, Y., Zhang, H., Lai, Y., Wang, M., Ahmed, T., Lin, R., et al. (2019) · FEBS Journal · doi:10.1111/febs.15024 · Cited by 25 · see citing works
Self-citationPINK1‐mediated mitophagy maintains pluripotency through optineurin
Wang, C., Liu, K., Cao, J., Wang, L., Zhao, Q., Li, Z., Zhang, H., Chen, Q., & Zhao, T. (2021) · Cell Proliferation · doi:10.1111/cpr.13034 · Cited by 23 · see citing works
Self-citationAutophagy and pluripotency: self-eating your way to eternal youth
Xu, Y., & Yang, X. (2022) · Trends in Cell Biology · doi:10.1016/j.tcb.2022.04.001 · Cited by 25 · see citing works
Zhou, J.-L., He, H., Zhang, J.-J., Liu, X., Yao, W., Li, C., Xu, T., Yin, S.-Y., Wu, D., Dou, C.-L., et al. (2022) · Autophagy · doi:10.1080/15548627.2022.2055285 · Cited by 18 · see citing works
Zhang, J., He, J. N., Johnson, J. L., Napolitano, G., Ramadass, M., Rahman, F., & Catz, S. D. (2019) · Autophagy · doi:10.1080/15548627.2019.1596475 · Cited by 18 · see citing works
The mTOR Pathway in Pluripotent Stem Cells: Lessons for Understanding Cancer Cell Dormancy
Alhasan, B. A., Gordeev, S. A., Knyazeva, A. R., Aleksandrova, K. V., Margulis, B. A., Guzhova, I. V., & Suvorova, I. I. (2021) · Membranes · doi:10.3390/membranes11110858 · Cited by 18 · see citing works
Mitochondrial dynamics and metabolism in induced pluripotency
Prieto, J., Ponsoda, X., Belmonte, J. C. I., & Torres, J. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.110870 · Cited by 17 · see citing works
Jin, B., Ren, J. F., Chen, J., Dong, Z., Chen, G., & Liu, D. (2022) · Cell and Tissue Research · doi:10.1007/s00441-022-03591-3 · Cited by 15 · see citing works
ATG5 attenuates inflammatory signaling in mouse embryonic stem cells to control differentiation
Li, S., Sun, J., Zhang, B.-W., Yang, L., Wan, Y.-C., Chen, B., Xu, N., Xu, Q., Fan, J., Shang, J.-N., et al. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.01.026 · Cited by 16 · see citing works
Autophagy in Muscle Regeneration: Mechanisms, Targets, and Therapeutic Perspective
Chu, Y., Yuan, X., Tao, Y., Yang, B. T., & Luo, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252211901 · Cited by 16 · see citing works
Li, S., Zhang, L., Zhang, G., Shangguan, G., Hou, X., Duan, W., Xi, Y., Xu, N., Zhang, B., Dong, J., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103296 · Cited by 14 · see citing works
Microtubule-dependent subcellular organisation of pluripotent cells
Hawdon, A., Aberkane, A., & Zenker, J. (2021) · Development · doi:10.1242/dev.199909 · Cited by 12 · see citing works
Forkhead box O proteins: steering the course of stem cell fate
Cheng, M., Nie, Y., Song, M., Chen, F., & Yu, Y. H. (2024) · Cell Regeneration · doi:10.1186/s13619-024-00190-1 · Cited by 12 · see citing works
The function of Foxo1 in spermatogonia development is independent of PI3K/PTEN signaling
Shen, Z., Chen, M., Gao, Y., Dong, F., Cen, C., Wu, H., Wang, N., Cui, X., Han, C., & Gao, F. (2022) · The FASEB Journal · doi:10.1096/fj.202200640rr · Cited by 11 · see citing works
Self-citationFoxO1 signaling in B cell malignancies and its therapeutic targeting
Hlavac, K., Petra, P., Ondrišová, L., & Mráz, M. (2024) · FEBS Letters · doi:10.1002/1873-3468.15057 · Cited by 11 · see citing works
Evaluating mitophagy in embryonic stem cells by using fluorescence-based imaging
Liu, K., Li, X., Li, Z., Cao, J., Li, X., Xu, Y., Liu, L., & Zhao, T. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.910464 · Cited by 9 · see citing works
Self-citationGoing through changes – the role of autophagy during reprogramming and differentiation
Petersen, M., Ebstrup, E. N., & Rodriguez, E. (2024) · Journal of Cell Science · doi:10.1242/jcs.261655 · Cited by 8 · see citing works
The Role of Nutrients in Maintaining Hematopoietic Stem Cells and Healthy Hematopoiesis for Life
Tadokoro, Y., & Hirao, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031574 · Cited by 10 · see citing works
Autophagy in Normal Stem Cells and Specialized Cells
Liu, K., Wang, L., & Zhao, T. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-981-15-0602-4_23 · Cited by 6 · see citing works
Self-citationApoptosis and Efferocytosis in Inflammatory Diseases
Purnama, C. A., Meiliana, A., Barliana, M. I., Dandan, K. L., & Wijaya, A. (2021) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v13i3.1608 · Cited by 5 · see citing works
The influence of high-order chromatin state in the regulation of stem cell fate
Chen, X., Lin, H., & Li, G. (2022) · Biochemical Society Transactions · doi:10.1042/bst20220763 · Cited by 4 · see citing works
Dynamic Autophagy Map in Mouse Female Germ Cells Throughout the Fetal to Postnatal Life
Jiang, G., Zhang, L., Zhao, J., Li, L., Huang, Z., & Wang, Z. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-00940-z · Cited by 5 · see citing works
Wang, Y., Cui, Y., Liu, X., Liang, S., Zhong, L., & Guo, R. (2025) · Stem Cell Research & Therapy · doi:10.1186/s13287-025-04231-7 · Cited by 3 · see citing works
Nazeerulla, F., Banerjee, I., Paul, M. K., Bisht, B., Basu, D. S., Bhutia, S. K., & Mukhopadhyay, S. (2026) · Life Sciences · doi:10.1016/j.lfs.2026.124277 · Cited by 3 · see citing works
Xiao, H., Tian, Y., Wang, Z., Li, W., Zhang, J., Han, L., Zhao, C., & Ding, J. (2025) · Marine Environmental Research · doi:10.1016/j.marenvres.2025.107203 · Cited by 3 · see citing works
Self-citationAssays for Monitoring Autophagy in Stem Cells
Chhatre, A. S., & Shravage, B. V. (2022) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-031-17362-2_1 · Cited by 1 · see citing works
Jia, Y., Guo, Z., Zhu, J., Qin, G., Sun, W., Yin, Y., Wang, H., & Guo, R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24010750 · Cited by 1 · see citing works
Inducible Ulk1 expression activates the p53 protein in mouse embryonic stem cells
Sutula, G. I., Alhasan, B. A., Vorobev, M. L., Guzhova, I. V., & Suvorova, I. I. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.07.133 · Cited by 1 · see citing works
集中度指数を指標とした集落分布パターン解析(2) : 平地農村の景観構造に関する基礎的研究(5)(計画・都市計画)
中園, 眞. (1992) · 日本建築学会中国支部研究報告集
集中度指数を指標とした集落分布パターン解析(1) : 平地農村の景観構造に関する基礎的研究(4)(計画・都市計画)
中園, 眞. (1992) · 日本建築学会中国支部研究報告集
Autophagy in Embryonic Stem Cells and Neural Stem Cells
Puri, D., Bivalkar-Mehla, S., & Subramanyam, D. (2022) · Stem cell biology and regenerative medicine · doi:10.1007/978-3-031-17362-2_3
Microtubule function in pluripotent mouse embryonic stem cells
Stockmann, L., Basu, S., & Galjart, N. (2026) · Trends in Cell Biology · doi:10.1016/j.tcb.2026.07.004
- Authors
- Liu, P., Liu, K., Gu, H., Wang, W., Gong, J., Zhu, Y., Zhao, Q., Cao, J., Han, C., Gao, F., Chen, Q., Li, W., Jiao, J., Hu, B., Zhou, Q., & Zhao, T.
- Affiliations
- Chinese Academy of Sciences (CN)
- Corresponding author
- Zhao, Tongbiao
- ORCID
- Venue
- Cell Death & Differentiation
- Published
- 2017-06-16
- Volume
- 24
- Issue
- 10
- Pages
- 1672-1680
- ISSN
- 1350-9047 (ISSN-L)
- 1476-5403
- PMC
- PMC5596427
- OpenAlex
- W2626062067
- Cited by
- 58
- References
- 52
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 1 · 2022: 12 · 2021: 10 · 2020: 9 · 2019: 6 · 2018: 7 · 2017: 2
- FWCI
- 5.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cell Death and Differentiation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (31271592, 31621004, 31570995)
- Chinese Academy of Sciences (XDA01040108, 31621004)
- National Key Research and Development Program of China (2013CB966901, 31621004)
- Thousand Young Talents Program of China
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › FOXO transcription factor regulation
- Keywords
- autophagic flux, embryonic stem cells, FOXO1, ATG3, stem cell self-renewal, pluripotency, mitochondrial homeostasis, stem cell fate regulation
- MeSH terms
- Mouse Embryonic Stem Cells, Cell Self Renewal, Forkhead Box Protein O1, Animals, Autophagy, Cell Differentiation, Cell Line, Gene Expression Regulation, Pluripotent Stem Cells, Mice, Gene Regulatory Networks
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
