Systematic analysis of ribophagy in human cells reveals bystander flux during selective autophagy
Open accessAbstract
Ribosomes are abundant cellular machines 1,2 that are regulated by assembly, supernumerary subunit turnover and nascent chain quality control mechanisms 1-5 . Moreover, nitrogen starvation in yeast has been reported to promote selective ribosome delivery to the vacuole in an autophagy conjugation system dependent manner, a process called 'ribophagy' 6,7 . However, whether ribophagy in mammals is selective or regulated is unclear. Using Ribo-Keima flux reporters, we find that starvation or mTOR inhibition promotes VPS34-dependent ribophagic flux, which, unlike yeast, is largely independent of ATG8 conjugation and occurs concomitantly with other cytosolic protein autophagic flux reporters 8,9 . Ribophagic flux was not induced upon inhibition of translational elongation or nascent chain uncoupling, but was induced in a comparatively selective manner under proteotoxic stress induced by arsenite 10 or chromosome mis-segregation 11 , dependent upon VPS34 and ATG8 conjugation. Unexpectedly, agents typically used to induce selective autophagy also promoted increased ribosome and cytosolic protein reporter flux, suggesting significant bulk or 'bystander' autophagy during what is often considered selective autophagy 12,13 . These results emphasize the importance of monitoring non-specific cargo flux when assessing selective autophagy pathways.
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NUFIP1 has been identified as one receptor involved in ribophagy, particularly in conditions requiring ribosomal recycling.
“NUFIP1 has been identified as one of the receptors involved in this process, particularly in conditions requiring ribosomal recycling [212].”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [212]
The passage on ribosomal stress (section labeled Abstract; page unavailable) says that stress may create a need to re-establish ribosome pools and reports increased ribophagic flux under some stress conditions. But our copy does not mention NUFIP1 or identify it as a ribophagy receptor (searched: NUFIP1 and ribophagy receptor). (LLM, conf=0.77)
Experimental — accuracy not yet measuredAlthough excessive ribophagy could compromise anabolic potential, a basal level of selective turnover is likely necessary to maintain a functional ribosomal pool during repeated cycles of loading and recovery.
“Although excessive activation of ribophagy could compromise anabolic potential, a basal level of selective turnover is likely necessary to maintain a functional ribosomal pool during repeated cycles of loading and recovery [211,212].”
From Ribosome Biogenesis as a Putative Bottleneck to Skeletal Muscle Hypertrophy: Mechanisms, Human Evidence, and Practical Modulators (2026) · cites this paper as [212]
The indexed passage labeled Abstract (page unavailable) reports very low basal ribophagic flux in HEK293 cells and says healthy ribosomes are important for cellular homeostasis. It does not establish that basal turnover is selective or necessary to maintain the ribosomal pool, and it does not examine excessive ribophagy, anabolic potential, or repeated loading and recovery. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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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
Genome engineering using the CRISPR-Cas9 system
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013) · Nature Protocols · doi:10.1038/nprot.2013.143 · Cited by 11,133 · 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
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
The economics of ribosome biosynthesis in yeast
Warner, J. R. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01460-7 · Cited by 1,933 · see citing works
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 · see citing works
Self-citationCargo recognition and trafficking in selective autophagy
Stolz, A., Ernst, A., & Dikic, I. (2014) · Nature Cell Biology · doi:10.1038/ncb2979 · Cited by 1,207 · see citing works
Phosphorylation of p62 Activates the Keap1-Nrf2 Pathway during Selective Autophagy
Ichimura, Y., Waguri, S., Sou, Y., Kageyama, S., Hasegawa, J., Ishimura, R., Saito, T., Yang, Y., Kouno, T., Fukutomi, T., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.08.003 · Cited by 1,205 · see citing works
Discovery of Atg5/Atg7-independent alternative macroautophagy
Nishida, Y., Arakawa, S., Fujitani, K., Yamaguchi, H., Mizuta, T., Kanaseki, T., Komatsu, M., Otsu, K., Tsujimoto, Y., & Shimizu, S. (2009) · Nature · doi:10.1038/nature08455 · Cited by 1,103 · see citing works
Anderson, P., & Kedersha, N. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200512082 · Cited by 984 · see citing works
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 828 · see citing works
Eukaryotic Stress Granules Are Cleared by Autophagy and Cdc48/VCP Function
Buchan, J. R., Kolaitis, R.-M., Taylor, J. P., & Parker, R. (2013) · Cell · doi:10.1016/j.cell.2013.05.037 · Cited by 737 · see citing works
Kraft, C., Deplazes, A., Sohrmann, M., & Peter, M. (2008) · Nature Cell Biology · doi:10.1038/ncb1723 · Cited by 733 · see citing works
Mechanisms of Autophagy Initiation
Hurley, J. H., & Young, L. N. (2017) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-061516-044820 · Cited by 655 · see citing works
A Sensitive and Quantitative Technique for Detecting Autophagic Events Based on Lysosomal Delivery
Katayama, H., Kogure, T., Mizushima, N., Yoshimori, T., & Miyawaki, A. (2011) · Chemistry & Biology · doi:10.1016/j.chembiol.2011.05.013 · Cited by 650 · see citing works
Yoshii, S. R., Kishi, C., Ishihara, N., & Mizushima, N. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.209338 · Cited by 612 · see citing works
The structure of the chromophore within DsRed, a red fluorescent protein from coral
Gross, L. A., Baird, G. S., Hoffman, R. C., Baldridge, K. K., & Tsien, R. Y. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.22.11990 · Cited by 612 · see citing works
Cleaning house: selective autophagy of organelles
Anding, A. L., & Baehrecke, E. H. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.02.016 · Cited by 576 · see citing works
Santaguida, S., Tighe, A., D’Alise, A. M., Taylor, S. S., & Musacchio, A. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201001036 · Cited by 538 · see citing works
The ATG conjugation systems are important for degradation of the inner autophagosomal membrane
Tsuboyama, K., Koyama-Honda, I., Sakamaki, Y., Koike, M., Morishita, H., & Mizushima, N. (2016) · Science · doi:10.1126/science.aaf6136 · Cited by 485 · see citing works
siRNA Screening of the Kinome Identifies ULK1 as a Multidomain Modulator of Autophagy
Chan, E. Y. W., Kır, S., & Tooze, S. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703663200 · Cited by 468 · see citing works
Anderson, D. J., Moigne, R. L., Djakovic, S. N., Kumar, B., Rice, J., Wong, S., Wang, J., Yao, B., Valle, E., Soly, S. K. V., et al. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.10.002 · Cited by 391 · see citing works
Mechanistic insights into mammalian stress granule dynamics
Panas, M. D., Ivanov, P. V., & Anderson, P. (2016) · The Journal of Cell Biology · doi:10.1083/jcb.201609081 · Cited by 374 · see citing works
Digesting the Expanding Mechanisms of Autophagy
Ktistakis, N. T., & Tooze, S. A. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.03.006 · Cited by 369 · see citing works
Dissecting the dynamic turnover of GFP-LC3 in the autolysosome
Ni, H., Bockus, A. B., Wozniak, A. L., Jones, K., Weinman, S. A., Yin, X., & Ding, W. (2011) · Autophagy · doi:10.4161/auto.7.2.14181 · Cited by 350 · see citing works
Sustained Mps1 activity is required in mitosis to recruit O-Mad2 to the Mad1–C-Mad2 core complex
Hewitt, L., Tighe, A., Santaguida, S., White, A. M., Jones, C. D., Musacchio, A., Green, S. A., & Taylor, S. S. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201002133 · Cited by 325 · see citing works
Proteome complexity and the forces that drive proteome imbalance
Harper, J. W., & Bennett, E. J. (2016) · Nature · doi:10.1038/nature19947 · Cited by 234 · see citing works
Self-citationUltrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells
Kishi‐Itakura, C., Koyama‐Honda, I., Itakura, E., & Mizushima, N. (2014) · Journal of Cell Science · doi:10.1242/jcs.156034 · Cited by 227 · see citing works
A conserved quality-control pathway that mediates degradation of unassembled ribosomal proteins
Sung, M., Porras-Yakushi, T. R., Reitsma, J. M., Huber, F. M., Sweredoski, M. J., Hoelz, A., Hess, S. Y., & Deshaies, R. J. (2016) · eLife · doi:10.7554/elife.19105 · Cited by 195 · see citing works
Aneuploidy-induced cellular stresses limit autophagic degradationPreprint
Santaguida, S., Vasile, E., White, E., & Amon, A. (2015) · Genes & Development · doi:10.1101/gad.269118.115 · Cited by 168 · see citing works
Cdc48 and Ufd3, new partners of the ubiquitin protease Ubp3, are required for ribophagy
Ossareh‐Nazari, B., Bonizec, M., Cohen, M. M., Dokudovskaya, S., Delalande, F., Schaeffer‐Reiss, C., DORSSELAER, A. V., & Dargemont, C. (2010) · EMBO Reports · doi:10.1038/embor.2010.74 · Cited by 157 · see citing works
Higgins, R., Gendron, J. M., Rising, L., Mak, R., Webb, K. J., Kaiser, S. E., Zuzow, N., Riviere, P. J., Yang, B., Fenech, E. J., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.026 · Cited by 149 · see citing works
Ribosomal proteins produced in excess are degraded by the ubiquitin–proteasome system
Sung, M., Reitsma, J. M., Sweredoski, M. J., Hess, S. Y., & Deshaies, R. J. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-05-0290 · Cited by 124 · see citing works
Target Selection during Protein Quality Control
Shao, S., & Hegde, R. S. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.10.007 · Cited by 79 · see citing works
Global Analysis of Cellular Protein Flux Quantifies the Selectivity of Basal Autophagy
Zhang, T., Shen, S., Qu, J., & Ghaemmaghami, S. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.040 · Cited by 70 · see citing works
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mTOR at the nexus of nutrition, growth, ageing and disease
Liu, G. Y., & Sabatini, D. M. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0199-y · Cited by 2,737 · see citing works
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 2,622 · see citing works
The mechanisms and roles of selective autophagy in mammals
Vargas, J. N. S., Hamasaki, M., Kawabata, T., Youle, R. J., & Yoshimori, T. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00542-2 · Cited by 1,030 · see citing works
Targeting Autophagy in Cancer: Recent Advances and Future Directions
Amaravadi, R. K., Kimmelman, A. C., & Debnath, J. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0292 · Cited by 928 · see citing works
Autophagy in inflammation, infection, and immunometabolism
Deretic, V. (2021) · Immunity · doi:10.1016/j.immuni.2021.01.018 · Cited by 862 · see citing works
Autophagy-Dependent Ferroptosis: Machinery and Regulation
Liu, J., Kuang, F., Kroemer, G., Klionsky, D. J., Kang, R., & Tang, D. (2020) · Cell chemical biology · doi:10.1016/j.chembiol.2020.02.005 · Cited by 811 · see citing works
Selective Autophagy: ATG8 Family Proteins, LIR Motifs and Cargo Receptors
Johansen, T., & Lamark, T. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.07.016 · Cited by 700 · see citing works
Autophagy: The Master of Bulk and Selective Recycling
Marshall, R. S., & Vierstra, R. D. (2018) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042817-040606 · Cited by 611 · see citing works
Selective autophagy of intracellular organelles: Recent research advances
Li, W., He, P., Huang, Y., Li, Y.-F., Lu, J., Li, M., Kurihara, H., Luo, Z., Meng, T., Onishi, M., et al. (2020) · Theranostics · doi:10.7150/thno.49860 · Cited by 510 · see citing works
Crosstalk Between Mammalian Autophagy and the Ubiquitin-Proteasome System
Kocatürk, N. M., & Gözüaçık, D. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00128 · Cited by 415 · see citing works
Autophagy as a molecular target for cancer treatment
Kocatürk, N. M., Akkoç, Y., Kığ, C., Bayraktar, O., Gözüaçık, D., & Kutlu, Ö. (2019) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2019.04.011 · Cited by 388 · see citing works
Autophagy, cancer stem cells and drug resistance
Smith, A. G., & Macleod, K. F. (2018) · The Journal of Pathology · doi:10.1002/path.5222 · Cited by 364 · see citing works
NUFIP1 is a ribosome receptor for starvation-induced ribophagy
Wyant, G. A., Abu-Remaileh, M., Frenkel, E. M., Laqtom, N. N., Dharamdasani, V., Lewis, C. A., Chan, S. H., Heinze, I., Ori, A., & Sabatini, D. M. (2018) · Science · doi:10.1126/science.aar2663 · Cited by 363 · see citing works
Signaling Pathways Involved in the Regulation of mRNA Translation
Roux, P. P., & Topisirović, I. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00070-18 · Cited by 314 · see citing works
Molecular logic of mTORC1 signalling as a metabolic rheostat
Valvezan, A. J., & Manning, B. D. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0038-7 · Cited by 295 · see citing works
An, H., Ordureau, A., Paulo, J. A., Shoemaker, C. J., Denic, V., & Harper, J. W. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.03.034 · Cited by 287 · see citing works
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Lahiri, V., Hawkins, W. D., & Klionsky, D. J. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.03.003 · Cited by 286 · see citing works
Cancer cells escape autophagy inhibition via NRF2-induced macropinocytosis
Su, H., Yang, F., Fu, R., Li, X., French, R. P., Mose, E. S., Pu, X., Trinh, B., Kumar, A., Liu, J., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.02.016 · Cited by 215 · see citing works
Luhr, M., Torgersen, M. L., Szalai, P., Hashim, A., Brech, A., Staerk, J., & Engedal, N. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.002829 · Cited by 208 · see citing works
Ordureau, A., Paulo, J. A., Zhang, J., An, H., Swatek, K. N., Cannon, J. R., Wan, Q., Komander, D., & Harper, J. W. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.11.013 · Cited by 198 · see citing works
Self-citationJia, J., Bissa, B., Brecht, L., Allers, L., Choi, S. W., Gu, Y., Zbinden, M., Burge, M. R., Timmins, G. S., Hallows, K. R., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.028 · Cited by 194 · see citing works
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Lamming, D. W., & Bar‐Peled, L. (2018) · Traffic · doi:10.1111/tra.12617 · Cited by 183 · see citing works
Eapen, V. V., Swarup, S., Hoyer, M., Paulo, J. A., & Harper, J. W. (2021) · eLife · doi:10.7554/elife.72328 · Cited by 162 · see citing works
Self-citationMeyer, C., Garzia, A., Morozov, P. S., Molina, H., & Tuschl, T. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.024 · Cited by 159 · see citing works
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Kumar, S. G., Gu, Y., Abudu, Y. P., Bruun, J., Jain, A., Farzam, F., Mudd, M. H., Anonsen, J. H., Rusten, T. E., Kasof, G. M., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.01.027 · Cited by 142 · see citing works
Balancing nutrient and energy demand and supply via autophagy
He, C. (2022) · Current Biology · doi:10.1016/j.cub.2022.04.071 · Cited by 137 · see citing works
The Impact of Oxidative Stress on Ribosomes: From Injury to Regulation
Shcherbik, N., & Pestov, D. G. (2019) · Cells · doi:10.3390/cells8111379 · Cited by 139 · see citing works
Systematic quantitative analysis of ribosome inventory during nutrient stress
An, H., Ordureau, A., Körner, M., Paulo, J. A., & Harper, J. W. (2020) · Nature · doi:10.1038/s41586-020-2446-y · Cited by 133 · see citing works
Self-citationDoes functional specialization of ribosomes really exist?
Ferretti, M., & Karbstein, K. (2019) · RNA · doi:10.1261/rna.069823.118 · Cited by 130 · see citing works
Mitochondrial Complex I Activity Is Required for Maximal Autophagy
Thomas, H. E., Zhang, Y., Stefely, J. A., Veiga, S. R., Thomas, G., Kozma, S. C., & Mercer, C. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.101 · Cited by 121 · see citing works
Diverse Functions of Autophagy in Liver Physiology and Liver Diseases
Ke, P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020300 · Cited by 115 · see citing works
Ordureau, A., Kraus, F., Zhang, J., An, H., Park, S., Ahfeldt, T., Paulo, J. A., & Harper, J. W. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.10.001 · Cited by 97 · see citing works
Self-citationElectron transport chain inhibition increases cellular dependence on purine transport and salvage
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Wu, D. A., Zhang, K., & Hu, P. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00551 · Cited by 100 · see citing works
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An, H., & Harper, J. W. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.001 · Cited by 98 · see citing works
Self-citationMammalian hybrid pre-autophagosomal structure HyPAS generates autophagosomes
Kumar, S. G., Javed, R., Mudd, M. H., Pallikkuth, S., Lidke, K. A., Jain, A., Tangavelou, K., Gudmundsson, S. R., Ye, C., Rusten, T. E., et al. (2021) · Cell · doi:10.1016/j.cell.2021.10.017 · Cited by 98 · see citing works
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Ke, P. (2020) · Cells · doi:10.3390/cells9040831 · Cited by 89 · see citing works
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Cavalli, G., & Cenci, S. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.01.015 · Cited by 90 · see citing works
Plant Selective Autophagy—Still an Uncharted Territory With a Lot of Hidden Gems
Stephani, M., & Dagdas, Y. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.06.028 · Cited by 84 · see citing works
Activity-Dependent Degradation of the Nascentome by the Neuronal Membrane Proteasome
Ramachandran, K. V., Fu, J. M., Schaffer, T. B., Na, C. H., Delannoy, M. R., & Margolis, S. S. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.013 · Cited by 80 · see citing works
iRQC, a surveillance pathway for 40S ribosomal quality control during mRNA translation initiation
Garshott, D. M., An, H., Sundaramoorthy, E., Leonard, M., Vicary, A. C., Harper, J. W., & Bennett, E. J. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109642 · Cited by 78 · see citing works
Self-citationPhosphoinositides in autophagy: current roles and future insights
Palamiuc, L., Ravi, A., & Emerling, B. M. (2019) · FEBS Journal · doi:10.1111/febs.15127 · Cited by 76 · see citing works
Autophagy in metabolism and quality control: opposing, complementary or interlinked functions?
Deretic, V. P., & Kroemer, G. (2021) · Autophagy · doi:10.1080/15548627.2021.1933742 · Cited by 76 · see citing works
Autophagy in cancer cell remodeling and quality control
Hernandez, G. A., & Perera, R. M. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.03.023 · Cited by 73 · see citing works
Mechanisms of Autophagy in Metabolic Stress Response.
Gross, A., & Graef, M. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.09.005 · Cited by 70 · see citing works
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Devenport, S. N., & Shah, Y. M. (2019) · Cells · doi:10.3390/cells8111349 · Cited by 75 · see citing works
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Sullivan, M. R., & Heiden, M. G. V. (2019) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2019.1611733 · Cited by 65 · see citing works
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Gu, Y., Abudu, Y. P., Kumar, S. G., Bissa, B., Choi, S. W., Jia, J., Lazarou, M., Eskelinen, E., Johansen, T., & Deretic, V. P. (2019) · The EMBO Journal · doi:10.15252/embj.2019101994 · Cited by 58 · see citing works
The bidirectional relationship between metabolism and cell cycle control
Diehl, F. F., Sapp, K. M., & Heiden, M. G. V. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.05.012 · Cited by 58 · see citing works
N-terminal β-strand underpins biochemical specialization of an ATG8 isoform
Zess, E. K., Jensen, C., Mireles, N. C., la Concepción, J. C. D., Sklenář, J., Stephani, M., Imre, R., Roitinger, E., Hughes, R., Belhaj, K., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000373 · Cited by 58 · see citing works
Stefely, J. A., Zhang, Y., Freiberger, E. C., Kwiecien, N. W., Thomas, H. E., Davis, A. M., Lowry, N. D., Vincent, C. E., Shishkova, E., Clark, N. A., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1719746 · Cited by 57 · see citing works
Oncogenic mutant RAS signaling activity is rescaled by the ERK/MAPK pathway
Gillies, T. E., Pargett, M., Silva, J. M., Teragawa, C., McCormick, F. P., & Albeck, J. G. (2020) · Molecular Systems Biology · doi:10.15252/msb.20209518 · Cited by 54 · see citing works
Selective Autophagy by Close Encounters of the Ubiquitin Kind
Vainshtein, A., & Grumati, P. (2020) · Cells · doi:10.3390/cells9112349 · Cited by 54 · see citing works
The dependency of autophagy and ubiquitin proteasome system during skeletal muscle atrophy
Singh, A. P., Phogat, J., Yadav, A., & Dabur, R. (2021) · Biophysical Reviews · doi:10.1007/s12551-021-00789-7 · Cited by 55 · see citing works
ATPase activity of DFCP1 controls selective autophagy
Nähse, V., Raiborg, C., Tan, K. W., Mørk, S., Torgersen, M. L., Wenzel, E. M., Nager, M., Salo, V. T., Johansen, T., Ikonen, E., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-39641-9 · Cited by 53 · see citing works
Translation machinery: the basis of translational control
Shu, Y., Zhou, G., & Xu, G. (2023) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2023.07.009 · Cited by 50 · see citing works
Targeting selective autophagy and beyond: From underlying mechanisms to potential therapies
Ma, W., Lü, Y., Jin, X., Lin, N., Zhang, L., & Song, Y. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.05.009 · Cited by 50 · see citing works
Martín‐Villanueva, S., Gutiérrez, G., Kressler, D., & de la Cruz, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094359 · Cited by 49 · see citing works
Cell- and Polymerase-Selective Metabolic Labeling of Cellular RNA with 2′-Azidocytidine
Wang, D., Zhang, Y., & Kleiner, R. E. (2020) · Journal of the American Chemical Society · doi:10.1021/jacs.0c04566 · Cited by 48 · see citing works
An RNA damage response network mediates the lethality of 5-FU in colorectal cancer
Chen, J.-K., Merrick, K. A., Kong, Y. W., Izrael-Tomasevic, A., Eng, G. M., Handly, E. D., Patterson, J. C., Cannell, I. G., Suárez-López, L., Hosios, A. M., et al. (2024) · Cell Reports Medicine · doi:10.1016/j.xcrm.2024.101778 · Cited by 50 · see citing works
PRKAA2, MTOR, and TFEB in the regulation of lysosomal damage response and autophagy
Shariq, M., Khan, M. F., Raj, R., Ahsan, N., & Kumar, P. (2024) · Journal of Molecular Medicine · doi:10.1007/s00109-023-02411-7 · Cited by 42 · see citing works
The Autophagy–RNA Interplay: Degradation and Beyond
Abildgaard, M. H., Brynjólfsdóttir, S. H., & Frankel, L. B. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.07.007 · Cited by 42 · see citing works
Physiological Functions of Intracellular Protein Degradation
McShane, E., & Selbach, M. (2022) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-120420-091943 · Cited by 39 · see citing works
mTOR- and LARP1-dependent regulation of TOP mRNA poly(A) tail and ribosome loading
Ogami, K., Oishi, Y., Sakamoto, K., Okumura, M., Yamagishi, R., Inoue, T., Hibino, M., Nogimori, T., Yamaguchi, N., Furutachi, K., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111548 · Cited by 38 · see citing works
PARK15/FBXO7 is dispensable for PINK1/Parkin mitophagy in iNeurons and HeLa cell systems
Kraus, F., Goodall, E. A., Smith, I. R. L., Jiang, Y., Paoli, J. C., Adolf, F., Zhang, J., Paulo, J. A., Schulman, B. A., & Harper, J. W. (2023) · EMBO Reports · doi:10.15252/embr.202256399 · Cited by 35 · see citing works
Self-citationAutophagy-mediated control of ribosome homeostasis in oncogene-induced senescence
López, A. R., Jørgensen, M. H., Havelund, J. F., Arendrup, F. S., Kolapalli, S. P., Nielsen, T. M., Pais, E., Beese, C. J., Abdul-Al, A., Vind, A., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113381 · Cited by 35 · see citing works
Ma, Q., Xin, J., Peng, Q., Li, N., Sun, S., Hou, H., Ma, G., Wang, N., Zhang, L., Tam, K. Y., et al. (2023) · EMBO Reports · doi:10.15252/embr.202255859 · Cited by 34 · see citing works
Li, K., Chen, H.-S., Li, D., Li, H., Wang, J., Jia, L., Wu, P.-F., Long, L., Hu, Z., Chen, J., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.07.026 · Cited by 33 · see citing works
The Ins and Outs of Autophagic Ribosome Turnover
Kazibwe, Z., Liu, A., MacIntosh, G. C., & Bassham, D. C. (2019) · Cells · doi:10.3390/cells8121603 · Cited by 34 · see citing works
Therapeutic Potential of Exploiting Autophagy Cascade Against Coronavirus Infection
Maity, S., & Saha, A. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.675419 · Cited by 28 · see citing works
Wong, C., & Venkatachalam, K. (2019) · Human Molecular Genetics · doi:10.1093/hmg/ddz104 · Cited by 33 · see citing works
Lei, H., Wang, G., Zhang, J., & Han, Q. (2018) · Oncology Reports · doi:10.3892/or.2018.6740 · Cited by 33 · see citing works
Brody, M. J., Vanhoutte, D., Bakshi, C. V., Liu, R., Correll, R. N., Sargent, M. A., & Molkentin, J. D. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007585 · Cited by 33 · see citing works
Ni, C., Schmitz, D. A., Lee, J., Pawłowski, K., Wu, J., & Buszczak, M. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110597 · Cited by 33 · see citing works
Rosignol, I., Villarejo‐Zori, B., Terešak, P., Sierra‐Filardi, E., Pereiro, X., Rodríguez‐Muela, N., Vecino, E., Vieira, H. L. A., Bell, K. C., & Boya, P. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21051882 · Cited by 32 · see citing works
RIOK3 mediates the degradation of 40S ribosomes
Huang, Z., Diehl, F. F., Wang, M., Li, Y., Song, A., Chen, F., Rosa-Mercado, N. A., Beckmann, R., Green, R., & Cheng, J. (2025) · Molecular Cell · doi:10.1016/j.molcel.2025.01.013 · Cited by 31 · see citing works
Rpl12 is a conserved ribophagy receptor
Chen, Y., Hu, J., Zhao, P., Fang, J., Kuang, Y., Liu, Z., Dong, S., Yao, W., Ding, Y., Wang, X., et al. (2025) · Nature Cell Biology · doi:10.1038/s41556-024-01598-2 · Cited by 29 · see citing works
When autophagy meets placenta development and pregnancy complications
Zhou, P., Wang, J., Wang, J., & Liu, X. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1327167 · Cited by 28 · see citing works
Nam, M., Xia, W., Mir, H., Jerrett, A. E., Spinelli, J. B., Huang, T. T., & Possemato, R. (2024) · Nature Metabolism · doi:10.1038/s42255-024-01166-w · Cited by 29 · see citing works
Eukaryotic ribosome quality control system: a potential therapeutic target for human diseases
Zhao, P., Yao, R.-Q., Zhang, Z., Zhu, S., Li, Y., Ren, C., Du, X., & Yao, Y.-M. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.70955 · Cited by 28 · see citing works
The Secrets of Alternative Autophagy
Urbańska, K., & Orzechowski, A. (2021) · Cells · doi:10.3390/cells10113241 · Cited by 28 · see citing works
Wu, M., Zhou, Z., Wang, X., Chen, B., Hafez, M. E., Shi, J.-F., Li, D., & Qian, R. (2022) · Analytical Chemistry · doi:10.1021/acs.analchem.1c04764 · Cited by 26 · see citing works
Autophagic flux measurement: Cargo degradation versus generation of degradation products
Mizushima, N. (2025) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2025.102463 · Cited by 24 · see citing works
Autophagy and antiviral defense
Ke, P. (2021) · IUBMB Life · doi:10.1002/iub.2582 · Cited by 23 · see citing works
Halat, L., Gyte, K., & Wasteneys, G. O. (2020) · PLANT PHYSIOLOGY · doi:10.1104/pp.20.00474 · Cited by 24 · see citing works
Ribosomal dormancy at the nexus of ribosome homeostasis and protein synthesis
Koli, S., & Shetty, S. (2024) · BioEssays · doi:10.1002/bies.202300247 · Cited by 23 · see citing works
Tiana, M., Acosta-Iborra, B., Hernández, R., Galiana, C., Fernández-Moreno, M. Á., Jimenez, B., & del Peso, L. (2020) · RNA · doi:10.1261/rna.072611.119 · Cited by 23 · see citing works
Mitochondria-associated membrane collapse impairs TBK1-mediated proteostatic stress response in ALS
Watanabe, S., Murata, Y., Oka, Y., Oiwa, K., Horiuchi, M., Iguchi, Y., Komine, O., Sobue, A., Katsuno, M., Ogi, T., et al. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2315347120 · Cited by 23 · see citing works
Hitchhiking on selective autophagy
Münch, C., & Đikić, I. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0036-0 · Cited by 22 · see citing works
Zhang, Y., Qian, C., Chu, C., Yang, X., Wu, Y., Cai, L., Yao, S., He, W., Guo, Z., & Chen, Y. (2025) · Angewandte Chemie International Edition · doi:10.1002/anie.202422874 · Cited by 20 · see citing works
Nutritional strategies for autophagy activation and health consequences of autophagy impairment
Kocot, A. M., & Wróblewska, B. (2022) · Nutrition · doi:10.1016/j.nut.2022.111686 · Cited by 21 · see citing works
Luhr, M., Szalai, P., & Engedal, N. (2018) · Journal of Visualized Experiments · doi:10.3791/57971 · Cited by 20 · see citing works
- Authors
- An, H., & Harper, J. W.
- Affiliations
- Harvard University (US)
- Corresponding author
- Harper, J. Wade
- Venue
- Nature Cell Biology
- Published
- 2017-12-11
- Volume
- 20
- Issue
- 2
- Pages
- 135-143
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC5786475
- OpenAlex
- W2774010248
- Cited by
- 181
- References
- 35
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 25 · 2023: 13 · 2022: 17 · 2021: 25 · 2020: 27 · 2019: 29 · 2018: 15
- FWCI
- 15.20
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- National Institute of General Medical Sciences (R01GM095567)
- National Institute of Neurological Disorders and Stroke (R37NS083524)
- Topics
- Health Sciences › Medicine › Epidemiology › 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 › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- ribophagy, selective autophagy, ribosome turnover, Vps34, ATG5, nutrient deprivation, mTOR inhibition, proteotoxic stress, arsenite, chromosome missegregation
- MeSH terms
- Autophagy-Related Protein 8 Family, Autophagy, Humans, Ribosomes, Vacuoles, Chromosome Segregation, Bystander Effect, Class III Phosphatidylinositol 3-Kinases, TOR Serine-Threonine Kinases
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