Entosis Is Induced by Glucose Starvation
Open accessAbstract
Entosis is a mechanism of cell death that involves neighbor cell ingestion. This process occurs in cancers and promotes a form of cell competition, where winner cells engulf and kill losers. Entosis is driven by a mechanical differential that allows softer cells to eliminate stiffer cells. While this process can be induced by matrix detachment, whether other stressors can activate entosis is unknown. Here, we find that entosis is induced in adherent cells by glucose withdrawal. Glucose withdrawal leads to a bimodal distribution of cells based on their deformability, where stiffer cells appear in a manner requiring the energy-sensing AMP-activated protein kinase (AMPK). We show that loser cells with high levels of AMPK activity are eliminated by winners through entosis, which supports winner cell proliferation under nutrient-deprived conditions. Our findings demonstrate that entosis serves as a cellular response to metabolic stress that enables nutrient recovery through neighbor cell ingestion.
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Entosis can be triggered by differences in mechanical properties or responses to metabolic stress of cancer cells competing for proliferation.
“differences in the mechanical properties [696] or responses to metabolic stress [697] of cancer cells competing for proliferation.”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [697]
In glucose withdrawal, cells with high AMPK activity succumb to entosis, suggesting a possible function of entosis for nutrient recovery by cells with lower AMPK activity.
“in conditions of glucose withdrawal, cells displaying high 5′ AMP-activated protein kinase (AMPK) activity succumb to entosis, underscoring a possible function of this process for nutrient recovery by cells with comparatively lower AMPK activity (which a priori are metabolically fitter) [697].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [697]
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Cites
Ferroptosis: An Iron-Dependent Form of Nonapoptotic Cell Death
Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. J., Cantley, A. M., Yang, W. S., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.042 · Cited by 18,691 · see citing works
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
Autophagy fights disease through cellular self-digestion
Mizushima, N., Levine, B., Cuervo, A. M., & Klionsky, D. J. (2008) · Nature · doi:10.1038/nature06639 · Cited by 6,452 · see citing works
Role of AMP-Activated Protein Kinase in Mechanism of Metformin Action
Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13505 · Cited by 5,652 · see citing works
Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury
Degterev, A., Huang, Z., Boyce, M., Li, Y., Jagtap, P., Mizushima, N., Cuny, G. D., Mitchison, T. J., Moskowitz, M. A., & Yuan, J. (2005) · Nature Chemical Biology · doi:10.1038/nchembio711 · Cited by 3,068 · see citing works
Galluzzi, L., Vitale, I., Abrams, J. M., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., Dawson, T. M., Dawson, V. L., El-Deiry, W. S., Fulda, S., et al. (2012) · Cell Death & Differentiation · doi:10.1038/cdd.2011.96 · Cited by 2,421 · see citing works
Glutaminolysis and transferrin regulate ferroptosis
Gao, M., Monian, P., Quadri, N., Ramasamy, R., & Jiang, X. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.06.011 · Cited by 2,069 · see citing works
Debnath, J., Muthuswamy, S. K., & Brugge, J. S. (2003) · Methods · doi:10.1016/s1046-2023(03)00032-x · Cited by 2,001 · see citing works
Hypoxia, HIF1 and glucose metabolism in the solid tumour
Denko, N. C. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2468 · Cited by 1,707 · see citing works
Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells
Commisso, C., Davidson, S. M., Soydaner-Azeloglu, R. G., Parker, S. J., Kamphorst, J. J., Hackett, S., Grabocka, E., Nofal, M., Drebin, J. A., Thompson, C. B., et al. (2013) · Nature · doi:10.1038/nature12138 · Cited by 1,683 · see citing works
Micropipette aspiration of living cells
Hochmuth, R. M. (2000) · Journal of Biomechanics · doi:10.1016/s0021-9290(99)00175-x · Cited by 1,428 · see citing works
Linkermann, A., & Green, D. R. (2014) · New England Journal of Medicine · doi:10.1056/nejmra1310050 · Cited by 1,103 · see citing works
Mu, J., Brozinick, J. T., Valladares, O., Bucan, M., & Birnbaum, M. J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00251-9 · Cited by 924 · see citing works
A Nonapoptotic Cell Death Process, Entosis, that Occurs by Cell-in-Cell Invasion
Overholtzer, M., Mailleux, A. A., Mouneimne, G., Normand, G., Schnitt, S. J., King, R. W., Cibas, E. S., & Brugge, J. S. (2007) · Cell · doi:10.1016/j.cell.2007.10.040 · Cited by 748 · see citing works
Self-citationLiu, Y., Shoji-Kawata, S., Sumpter, R. M., Wei, Y., Ginet, V., Zhang, L., Posner, B., Tran, K. A., Green, D. R., Xavier, R. J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319661110 · Cited by 607 · cited 2× · see citing works
“, 2012]) and autophagic cell death are now known to contribute to cell death induced by viral infection (Linkermann and Green, 2014) and nutrient deprivation (Gao et al., 2015; Liu et al., 2013) and to programmed cell death during development (Nelson et al.”
Development of an optimized backbone of FRET biosensors for kinases and GTPases
Komatsu, N., Aoki, K., Yamada, M., Yukinaga, H., Fujita, Y., Kamioka, Y., & Matsuda, M. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-01-0072 · Cited by 580 · see citing works
Florey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M., & Overholtzer, M. (2011) · Nature Cell Biology · doi:10.1038/ncb2363 · Cited by 459 · see citing works
Self-citationThe utilization of extracellular proteins as nutrients is suppressed by mTORC1
Palm, W., Park, Y., Wright, K., Pavlova, N. N., Tuveson, D. A., & Thompson, C. B. (2015) · Cell · doi:10.1016/j.cell.2015.06.017 · Cited by 457 · see citing works
Mechanism of Action of A-769662, a Valuable Tool for Activation of AMP-activated Protein Kinase
Göransson, O., McBride, A., Hawley, S. A., Ross, F. A., Shpiro, N., Foretz, M., Viollet, B., Hardie, D. G., & Sakamoto, K. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m706536200 · Cited by 433 · see citing works
Nutrient Sensing, Metabolism, and Cell Growth Control
Yuan, H.-X., Xiong, Y., & Guan, K. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.019 · Cited by 357 · see citing works
Superoxide is a mediator of an altruistic aging program in <i>Saccharomyces cerevisiae</i>
Fabrizio, P., Battistella, L., Vardavas, R., Gattazzo, C., Liou, L.-L., Diaspro, A., Dossen, J. W., Gralla, E. B., & Longo, V. D. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200404002 · Cited by 355 · see citing works
Okoshi, R., Ozaki, T., Yamamoto, H., Ando, K., Koida, N., Ono, S., Koda, T., Kamijo, T., Nakagawara, A., & Kizaki, H. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705232200 · Cited by 277 · see citing works
Chemical Genetic Screen for AMPKα2 Substrates Uncovers a Network of Proteins Involved in Mitosis
Banko, M. R., Allen, J. J., Schaffer, B. E., Wilker, E., Tsou, P., White, J. L., Villén, J., Wang, B., Kim, S. R., Sakamoto, K., et al. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.11.005 · Cited by 240 · see citing works
Competition between human cells by entosis
Sun, Q., Luo, T., Ren, Y., Florey, O., Shirasawa, S., Sasazuki, T., Robinson, D. N., & Overholtzer, M. (2014) · Cell Research · doi:10.1038/cr.2014.138 · Cited by 233 · see citing works
Self-citationMéndez‐Lucas, A., Hyroššová, P., Novellasdemunt, L., Viñals, F., & Perales, J. C. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.566927 · Cited by 200 · see citing works
Why yeast cells can undergo apoptosis: death in times of peace, love, and war
Büttner, S., Eisenberg, T., Herker, E., Carmona‐Gutiérrez, D., Kroemer, G., & Madeo, F. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200608098 · Cited by 193 · see citing works
A non-genetic route to aneuploidy in human cancers
Krajcovic, M., Johnson, N. B., Sun, Q., Normand, G., Hoover, N., Yao, E., Richardson, A. L., King, R. W., Cibas, E. S., Schnitt, S. J., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2174 · Cited by 188 · see citing works
Self-citationAMPK governs lineage specification through Tfeb-dependent regulation of lysosomesPreprint
Young, N. P., Kamireddy, A., Nostrand, J. L. V., Eichner, L. J., Shokhirev, M. N., Dayn, Y., & Shaw, R. J. (2016) · Genes & Development · doi:10.1101/gad.274142.115 · Cited by 177 · see citing works
A Fluorescent Reporter of AMPK Activity and Cellular Energy Stress
Tsou, P., Zheng, B., Hsu, C., Sasaki, A. T., & Cantley, L. C. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.03.006 · Cited by 158 · see citing works
mTOR regulates phagosome and entotic vacuole fission
Krajcovic, M., Krishna, S., Akkari, L., Joyce, J. A., & Overholtzer, M. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-07-0408 · Cited by 149 · see citing works
Self-citationInduction of entosis by epithelial cadherin expression
Sun, Q., Cibas, E. S., Huang, H., Hodgson, L., & Overholtzer, M. (2014) · Cell Research · doi:10.1038/cr.2014.137 · Cited by 148 · see citing works
Self-citationSparta, B., Pargett, M., Minguet, M., Distor, K., Bell, G. R. R., & Albeck, J. G. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.662247 · Cited by 113 · see citing works
Self-citationSullivan, J. E., Carey, F., Carling, D., & Beri, R. K. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.1627 · Cited by 83 · see citing works
14-3-3 Coordinates Microtubules, Rac, and Myosin II to Control Cell Mechanics and Cytokinesis
Zhou, Q., Kee, Y.-S., Poirier, C. C., Jelinek, C., Osborne, J., Divi, S. N., Surcel, A., Will, M. E., Eggert, U., Müller‐Taubenberger, A., et al. (2010) · Current Biology · doi:10.1016/j.cub.2010.09.048 · Cited by 78 · see citing works
Self-citationAMPK Regulates Mitotic Spindle Orientation through Phosphorylation of Myosin Regulatory Light Chain
Thaiparambil, J. T., Eggers, C. M., & Marcus, A. I. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00418-12 · Cited by 68 · see citing works
Apoptosis in yeast – mechanisms and benefits to a unicellular organism
Gourlay, C. W., Du, W., & Ayscough, K. R. (2006) · Molecular Microbiology · doi:10.1111/j.1365-2958.2006.05486.x · Cited by 62 · see citing works
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
Effects of activation of AMPK on human breast cancer cell lines with different genetic backgrounds
El-Masry, O. S., BROWN, B. L., & Dobson, P. R. M. (2011) · Oncology Letters · doi:10.3892/ol.2011.458 · Cited by 43 · see citing works
Bultot, L., Horman, S., Neumann, D., Walsh, M. P., Hue, L., & Rider, M. H. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.11.022 · Cited by 37 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Linkermann A, Green DR. Necroptosis. N. Engl. J. Med. 2014; 370:455-465. [PubMed: 24476434]
- Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular selfdigestion. Nature. 2008; 451:1069-1075. [PubMed: 18305538]
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
The molecular machinery of regulated cell death
Tang, D., Kang, R., Berghe, T. V., Vandenabeele, P., & Kroemer, G. (2019) · Cell Research · doi:10.1038/s41422-019-0164-5 · Cited by 2,595 · see citing works
The hallmarks of cancer metabolism: still emerging
Pavlova, N. N., Zhu, J., & Thompson, C. B. (2022) · Cell Metabolism · doi:10.1016/j.cmet.2022.01.007 · Cited by 1,418 · see citing works
A guide to cell death pathways
Yuan, J., & Ofengeim, D. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00689-6 · Cited by 972 · see citing works
Doherty, J., & Baehrecke, E. H. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0201-5 · Cited by 626 · see citing works
The Coming Decade of Cell Death Research: Five Riddles
Green, D. R. (2019) · Cell · doi:10.1016/j.cell.2019.04.024 · Cited by 561 · see citing works
The Apoptosis Paradox in Cancer
Morana, O., Wood, W., & Gregory, C. D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031328 · Cited by 430 · see citing works
Diversity and complexity of cell death: a historical review
Park, W., Wei, S., Kim, B., Kim, B., Bae, S., Chae, Y. C., Ryu, D., & Ha, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01078-x · Cited by 364 · see citing works
Cell death mechanisms in eukaryotes
Nirmala, J. G., & Lopus, M. (2019) · Cell Biology and Toxicology · doi:10.1007/s10565-019-09496-2 · Cited by 266 · see citing works
Finicle, B. T., Jayashankar, V., & Edinger, A. L. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0048-x · Cited by 231 · see citing works
Hayashi, A., Fan, J., Chen, R., Ho, Y.-J., Makohon-Moore, A. P., Lecomte, N., Zhong, Y., Hong, J., Huang, J., Sakamoto, H., et al. (2020) · Nature Cancer · doi:10.1038/s43018-019-0010-1 · Cited by 204 · see citing works
Self-citationCell-in-cell phenomena in cancer
Fais, S., & Overholtzer, M. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0073-9 · Cited by 192 · see citing works
Self-citationDurgan, J., & Florey, O. (2022) · Science Advances · doi:10.1126/sciadv.abo1274 · Cited by 176 · see citing works
Cell competition in development, homeostasis and cancer
van Neerven, S. M., & Vermeulen, L. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00538-y · Cited by 154 · see citing works
Li, S., Xiong, G.-J., Huang, N., & Sheng, Z. (2020) · Nature Metabolism · doi:10.1038/s42255-020-00289-0 · Cited by 144 · see citing works
Vishwakarma, M., & Piddini, E. (2020) · Nature reviews. Cancer · doi:10.1038/s41568-019-0231-8 · Cited by 147 · see citing works
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Santagostino, S. F., Assenmacher, C., Tarrant, J. C., Adedeji, A. O., & Radaelli, E. (2021) · Veterinary Pathology · doi:10.1177/03009858211005537 · Cited by 133 · see citing works
Micronuclei and Genome Chaos: Changing the System Inheritance
Ye, C. J., Sharpe, Z. J., Alemara, S., Mackenzie, S., Liu, G., Abdallah, B. Y., Horne, S. D., Regan, S. M., & Heng, H. H. (2019) · Genes · doi:10.3390/genes10050366 · Cited by 123 · see citing works
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Tonnessen-Murray, C. A., Frey, W. D., Rao, S. G., Shahbandi, A., Ungerleider, N. A., Olayiwola, J. O., Murray, L. B., Vinson, B. T., Chrisey, D. B., Lord, C. J., et al. (2019) · Journal of Cell Biology · doi:10.1083/jcb.201904051 · Cited by 127 · see citing works
Muir, A., Danai, L. V., & Heiden, M. G. V. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.035758 · Cited by 121 · see citing works
Preliminary evidence for the presence of multiple forms of cell death in diabetes cardiomyopathy
Wei, J., Zhao, Y., Liang, H., Du, W., & Wang, L. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.08.026 · Cited by 106 · see citing works
Genome chaos: Creating new genomic information essential for cancer macroevolution
Heng, J., & Heng, H. H. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.11.003 · Cited by 101 · see citing works
Polyploidy formation in cancer cells: How a Trojan horse is born
Waś, H., Borkowska, A., Olszewska, A., Klemba, A., Marciniak, M., Synowiec, A., & Kiéda, C. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.03.003 · Cited by 98 · see citing works
Mechanisms and Pathophysiological Roles of the ATG8 Conjugation Machinery
Lystad, A. H., & Simonsen, A. (2019) · Cells · doi:10.3390/cells8090973 · Cited by 89 · see citing works
Cancer cell cannibalism: Multiple triggers emerge for entosis
Durgan, J., & Florey, O. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2018.03.004 · Cited by 84 · see citing works
CYBB/NOX2 in conventional DCs controls T cell encephalitogenicity during neuroinflammation
Keller, C. W., Kotur, M. B., Mundt, S., Dokalis, N., Ligeon, L., Shah, A. M., Prinz, M., Becher, B., Münz, C., & Lünemann, J. D. (2020) · Autophagy · doi:10.1080/15548627.2020.1756678 · Cited by 85 · see citing works
Significance of Programmed Cell Death Pathways in Neurodegenerative Diseases
Guo, D., Liu, Z., Zhou, J., Ke, C., & Li, D. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25189947 · Cited by 81 · see citing works
Aizawa, S., Brar, G., & Tsukamoto, H. (2019) · Gut and Liver · doi:10.5009/gnl18486 · Cited by 77 · see citing works
Two-Dimensional Nanomaterial-based catalytic Medicine: Theories, advanced catalyst and system design
Zeng, W., Zhang, H., Xue, Y., Chen, T., Pei, Z., & Ji, X. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114241 · Cited by 77 · see citing works
Population Dynamics in Cell Death: Mechanisms of Propagation
Riegman, M., Bradbury, M. S., & Overholtzer, M. (2019) · Trends in cancer · doi:10.1016/j.trecan.2019.07.008 · Cited by 77 · see citing works
Self-citationCentrosome dysfunction: a link between senescence and tumor immunity
Wu, Q., Li, B., Liu, L., Sun, S., & Sun, S. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00214-7 · Cited by 76 · see citing works
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Tanimura, N., & Fujita, Y. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.05.011 · Cited by 73 · see citing works
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Mihlan, M., Wissmann, S., Gavrilov, A., Kaltenbach, L., Britz, M., Franke, K., Hummel, B., Imle, A., Suzuki, R., Stecher, M., et al. (2024) · Cell · doi:10.1016/j.cell.2024.07.014 · Cited by 74 · see citing works
Sendtner, N., Seitz, R., Brandl, N., Müller, M., & Gülow, K. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262010240 · Cited by 75 · see citing works
Genetic and clinical correlates of entosis in pancreatic ductal adenocarcinoma
Hayashi, A., Yavas, A., McIntyre, C. A., Ho, Y.-J., Erakky, A., Wong, W., Varghese, A. M., Melchor, J. P., Overholtzer, M., O'Reilly, E. M., et al. (2020) · Modern Pathology · doi:10.1038/s41379-020-0549-5 · Cited by 68 · see citing works
Self-citationDeterminants of nutrient limitation in cancer
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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Ye, C. J., Stilgenbauer, L., Moy, A., Liu, G., & Heng, H. H. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.01082 · Cited by 62 · see citing works
Types of Cell Death from a Molecular Perspective
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p53-dependent elimination of aneuploid mitotic offspring by entosis
Liang, J., Niu, Z., Zhang, B., Yu, X., Zheng, Y., Wang, C., Ren, H., Wang, M., Ruan, B., Qin, H., et al. (2020) · Cell Death and Differentiation · doi:10.1038/s41418-020-00645-3 · Cited by 66 · see citing works
Transient cell-in-cell formation underlies tumor relapse and resistance to immunotherapy
Gutwillig, A., Santana-Magal, N., Farhat-Younis, L., Rasoulouniriana, D., Madi, A., Luxenburg, C., Cohen, J., Padmanabhan, K., Shomron, N., Shapira, G., et al. (2022) · eLife · doi:10.7554/elife.80315 · Cited by 57 · see citing works
Liu, P., Wang, L., & Yu, H. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1410637 · Cited by 56 · see citing works
Biological relevance of cell-in-cell in cancers
Mackay, H. L., & Muller, P. A. J. (2019) · Biochemical Society Transactions · doi:10.1042/bst20180618 · Cited by 56 · see citing works
The inducible role of autophagy in cell death: emerging evidence and future perspectives
Huang, X., Yan, H., Xu, Z., Yang, B., Luo, P., & He, Q. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02135-w · Cited by 57 · see citing works
Supply and demand: Cellular nutrient uptake and exchange in cancer
Papalazarou, V., & Maddocks, O. D. K. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.08.026 · Cited by 52 · see citing works
Jin, X., Jin, W., Tong, L., Zhao, J., Zhang, L., & Lin, N. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.04.020 · Cited by 54 · see citing works
Wang, X., Li, Y., Li, J., Li, L., Zhu, H., Chen, H., Kong, R., Wang, G., Wang, Y., Hu, J., et al. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00311 · Cited by 53 · see citing works
Torrence, M. E., & Manning, B. D. (2017) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030617-050329 · Cited by 52 · see citing works
Wang, M., Niu, Z., Qin, H., Ruan, B., Zheng, Y., Ning, X., Gu, S., Gao, L., Chen, Z., Wang, X., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108071 · Cited by 50 · see citing works
CDKN2A inhibits formation of homotypic cell-in-cell structures
Liang, J., Fan, J., Wang, M., Niu, Z., Zhang, Z., Yuan, L., Tai, Y., Chen, Z., Song, S., Wang, X., et al. (2018) · Oncogenesis · doi:10.1038/s41389-018-0056-4 · Cited by 49 · see citing works
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Chen, F., Lu, Y., Lin, J., Kang, R., & Liu, J. (2023) · Antioxidants and Redox Signaling · doi:10.1089/ars.2023.0340 · Cited by 50 · see citing works
Classification of Cell-in-Cell Structures: Different Phenomena with Similar Appearance
Borensztejn, K., Tyrna, P., Gaweł, A. M., Dziuba, I., Wójcik, C., Biały, Ł. P., & Młynarczuk-Biały, I. (2021) · Cells · doi:10.3390/cells10102569 · Cited by 47 · see citing works
CRISPRthripsis: The Risk of CRISPR/Cas9-induced Chromothripsis in Gene Therapy
Amendola, M., Brusson, M., & Miccio, A. (2022) · Stem Cells Translational Medicine · doi:10.1093/stcltm/szac064 · Cited by 46 · see citing works
The impact of non-genetic heterogeneity on cancer cell death
Inde, Z., & Dixon, S. J. (2017) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2017.1412395 · Cited by 44 · see citing works
Antifungal Peptides of the AFP Family Revisited: Are These Cannibal Toxins?
Meyer, V., & Jung, S. (2018) · Microorganisms · doi:10.3390/microorganisms6020050 · Cited by 41 · see citing works
Avenues to molecular imaging of dying cells: Focus on cancer
Rybczynska, A. A., Boersma, H. H., de Jong, S., Gietema, J. A., Noordzij, W., Dierckx, R., Elsinga, P. H., & van Waarde, A. (2018) · Medicinal Research Reviews · doi:10.1002/med.21495 · Cited by 40 · see citing works
Macropinocytosis and autophagy crosstalk in nutrient scavenging
Florey, O., & Overholtzer, M. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2018.0154 · Cited by 39 · see citing works
Self-citationCell Death by Entosis: Triggers, Molecular Mechanisms and Clinical Significance
Kianfar, M., Balcerak, A., Chmielarczyk, M., Tarnowski, L. J., & Grzybowska, E. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094985 · Cited by 38 · see citing works
Apoptotic signaling: Beyond cell death
Nano, M., & Montell, D. J. (2023) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2023.11.002 · Cited by 37 · see citing works
Isobavachalcone reveals novel characteristics of methuosis-like cell death in leukemia cells
Yang, L., Song, L., Zhao, S., Ma, C., Wu, D., & Wu, Y. (2019) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2019.03.011 · Cited by 38 · see citing works
Novel Methylselenoesters Induce Programed Cell Death via Entosis in Pancreatic Cancer Cells
Khalkar, P., Díaz-Argelich, N., Palop, J. A., Sanmartín, C., & Fernandes, A. P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19102849 · Cited by 37 · see citing works
TRAIL signaling promotes entosis in colorectal cancer
Bozkurt, E., Düßmann, H., Salvucci, M., Cavanagh, B., Schaeybroeck, S. V., Longley, D. B., Martin, S. J., & Prehn, J. H. M. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202010030 · Cited by 37 · see citing works
Cell-in-Cell–Mediated Entosis Reveals a Progressive Mechanism in Pancreatic Cancer
Song, J., Xu, R., Zhang, H., Xue, X., Ruze, R., Chen, Y., Yin, X., Wang, C., & Zhao, Y. (2023) · Gastroenterology · doi:10.1053/j.gastro.2023.08.035 · Cited by 35 · see citing works
How the mechanobiome drives cell behavior, viewed through the lens of control theory
Kothari, P., Johnson, C., Sandone, C., Iglesias, P. A., & Robinson, D. N. (2019) · Journal of Cell Science · doi:10.1242/jcs.234476 · Cited by 34 · see citing works
Self-citationMechanisms and significance of entosis for tumour growth and progression
Gaptulbarova, K. A., Tsydenova, I. A., Dolgasheva, D. S., Kravtsova, E. A., Ibragimova, M. K., Vtorushin, S. V., & Литвяков, Н. В. (2024) · Cell Death Discovery · doi:10.1038/s41420-024-01877-9 · Cited by 33 · see citing works
Entosis: the core mechanism and crosstalk with other cell death programs
Kim, S.-H., Lee, D., Kim, S. E., & Overholtzer, M. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01227-w · Cited by 33 · see citing works
Self-citationExpression profiling identified IL-8 as a regulator of homotypic cell-in-cell formation
Ruan, B., Wang, C., Chen, A., Liang, J., Niu, Z., Zheng, Y., Fan, J., Gao, L., Huang, H., Wang, X., et al. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.8.089 · Cited by 33 · see citing works
Cell-in-Cell Structures in the Liver: A Tale of Four E’s
Davies, S. P., Terry, L. V., Wilkinson, A. L., & Stamataki, Z. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00650 · Cited by 33 · see citing works
Prospects and challenges of cancer systems medicine: from genes to disease networks
Karimi, M. R., Karimi, A. H., Abolmaali, S., Sadeghi, M., & Schmitz, U. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab343 · Cited by 33 · see citing works
Dynamin-Independent Mechanisms of Endocytosis and Receptor Trafficking
Gundu, C., Arruri, V. K., Yadav, P., Navik, U., Kumar, A., Amalkar, V. S., Vikram, A., & Gaddam, R. R. (2022) · Cells · doi:10.3390/cells11162557 · Cited by 30 · see citing works
Cholesterol inhibits entotic cell-in-cell formation and actomyosin contraction
Ruan, B., Zhang, B., Chen, A., Yuan, L., Liang, J., Wang, M., Zhang, Z., Fan, J., Yu, X., Zhang, X., et al. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.11.197 · Cited by 28 · see citing works
Cell-in-cell phenomena, cannibalism, and autophagy: is there a relationship?
Fais, S., & Overholtzer, M. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0111-7 · Cited by 28 · see citing works
Self-citationInduction of entosis in prostate cancer cells by nintedanib and its therapeutic implications
Liu, J., Wang, L., Zhang, Y., Li, S., Sun, F., Wang, G., Yang, T., Dong, W., Guo, L., & Xiao, H. (2019) · Oncology Letters · doi:10.3892/ol.2019.9951 · Cited by 27 · see citing works
Wang, S., Li, L., Zhou, Y., He, Y., Wei, Y., & Tao, A. (2019) · Experimental Cell Research · doi:10.1016/j.yexcr.2019.05.028 · Cited by 27 · see citing works
In Silico Investigations of Multi-Drug Adaptive Therapy Protocols
Thomas, D. S., Cisneros, L. H., Anderson, A. R. A., & Maley, C. C. (2022) · Cancers · doi:10.3390/cancers14112699 · Cited by 27 · see citing works
Entosis is induced by ultraviolet radiation
Chen, R., Ram, A. R., Albeck, J. G., & Overholtzer, M. (2021) · iScience · doi:10.1016/j.isci.2021.102902 · Cited by 25 · see citing works
Self-citationLoss of 4.1N in epithelial ovarian cancer results in EMT and matrix-detached cell death resistance
Wang, D., Zhang, L., Hu, A., Wang, Y., Liu, Y., Yang, J., Du, N., An, X., Wu, C., & Liu, C. (2020) · Protein & Cell · doi:10.1007/s13238-020-00723-9 · Cited by 23 · see citing works
Solovieva, M. E., Shatalin, Y. V., Odinokova, I. V., Krestinina, O. V., Baburina, Y. L., Mishukov, A. A., Lomovskaya, Y. V., Pavlik, L., Mikheeva, I. B., Holmuhamedov, E., et al. (2022) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2022.130184 · Cited by 24 · see citing works
Mechanoregulation of Metastasis beyond the Matrix
Er, E. E., Tello‐Lafoz, M., & Huse, M. (2022) · Cancer Research · doi:10.1158/0008-5472.can-22-0419 · Cited by 21 · see citing works
Song, J., Ruze, R., Chen, Y., Xu, R., Yin, X., Wang, C., Xu, Q., & Zhao, Y. (2022) · BMC Cancer · doi:10.1186/s12885-022-09983-6 · Cited by 24 · see citing works
Contractility kits promote assembly of the mechanoresponsive cytoskeletal network
Kothari, P., Srivastava, V., Aggarwal, V., Tchernyshyov, I., Eyk, J. E. V., Ha, T., & Robinson, D. N. (2018) · Journal of Cell Science · doi:10.1242/jcs.226704 · Cited by 24 · see citing works
Self-citationAlmangush, A., Mäkitie, A. A., Hagström, J., Haglund, C. H., Kowalski, L. P., Nieminen, P. A., Coletta, R. D., Salo, T. A., & Leivo, I. V. V. (2020) · BMC Cancer · doi:10.1186/s12885-020-07342-x · Cited by 23 · see citing works
Cell-in-Cell Events in Oral Squamous Cell Carcinoma
da Rocha, L. D. O. S., Souza, B. S. D. F., Lambert, D., & Rocha, C. A. G. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.931092 · Cited by 23 · see citing works
Rewiring cancer metabolism: oncogenic signaling pathways and targeted therapeutics
Lyu, S., Gildor, N., Zhang, Q. H., & Liao, C. (2025) · Science China Life Sciences · doi:10.1007/s11427-025-2979-3 · Cited by 26 · see citing works
Metabolism‐Based Molecular Subtyping Endows Effective Ketogenic Therapy in p53‐Mutant Colon Cancer
Tang, M., Xu, H., Huang, H., Kuang, H., Wang, C., Li, Q., Zhang, X., Ge, Y., Song, M., Zhang, X., et al. (2022) · Advanced Science · doi:10.1002/advs.202201992 · Cited by 22 · see citing works
Metabolic regulation of cell competition
Esteban‐Martínez, L., & Torres, M. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.02.011 · Cited by 21 · see citing works
Komatsu, M., Ichikawa, H., Chiwaki, F., Sakamoto, H., Komatsuzaki, R., Asaumi, M., Tsunoyama, K., Fukagawa, T., Matsushita, H., Boku, N., et al. (2022) · Oncogene · doi:10.1038/s41388-022-02469-6 · Cited by 21 · see citing works
Wang, S., Liu, B., Huang, J., He, H., Li, L., & Tao, A. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113665 · Cited by 20 · see citing works
Molecular mechanisms underlying cell-in-cell formation: core machineries and beyond
Niu, Z., He, M., & Sun, Q. (2021) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjab015 · Cited by 19 · see citing works
I Spy in the Developing Fly a Multitude of Ways to Die
Yalonetskaya, A., Mondragon, A. A., Elguero, J., & McCall, K. (2018) · Journal of Developmental Biology · doi:10.3390/jdb6040026 · Cited by 19 · see citing works
Cell death classification: A new insight based on molecular mechanisms
Dehghan, S., Kheshtchin, N., Hassannezhad, S., & Soleimani, M. (2023) · Experimental Cell Research · doi:10.1016/j.yexcr.2023.113860 · Cited by 18 · see citing works
RNA modifications act as regulators of cell death
Xu, L., Zhang, C., Yin, H., Gong, S., Wu, N., Ren, Z., & Zhang, Y. (2021) · RNA Biology · doi:10.1080/15476286.2021.1925460 · Cited by 18 · see citing works
Surveying the landscape of emerging and understudied cell death mechanisms
Leak, L. B., & Dixon, S. J. (2023) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2023.119432 · Cited by 17 · see citing works
Mechanisms of oncogenic cell competition–Paths of victory
Gutiérrez-Martínez, A., Sew, W. Q. G., Molano-Fernández, M., Carretero, M., & Herranz, H. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.05.015 · Cited by 16 · see citing works
Orai1 is an Entotic Ca 2+ Channel for Non‐Apoptotic Cell Death, Entosis in Cancer Development
Lee, A. R., & Park, C. Y. (2023) · Advanced Science · doi:10.1002/advs.202205913 · Cited by 16 · see citing works
Varela, M., van der Vaart, M., Groenewoud, A., & Meijer, A. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/514125 · Cited by 16 · see citing works
Canine oral primary melanoma cells exhibit shift to mesenchymal phenotype and phagocytic behaviour
Schmid, F., Brodesser, D., Reifinger, M., Forte, S., Semp, P., Eberspächer‐Schweda, M. C., Wolschek, M. F., Brandt, S., KLEITER, M. M., & Pratscher, B. (2019) · Veterinary and Comparative Oncology · doi:10.1111/vco.12464 · Cited by 15 · see citing works
Biomechanical Microenvironment Regulates Fusogenicity of Breast Cancer Cells
Zhu, P., Tseng, N.-H., Xie, T., Li, N., Fitts-Sprague, I., Peyton, S. R., & Sun, Y. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b00861 · Cited by 14 · see citing works
Methods for the Study of Entotic Cell Death
Hamann, J. C., Kim, S. E., & Overholtzer, M. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-8873-0_28 · Cited by 13 · see citing works
Self-citationHomotypic cell-in-cell structures as an adverse prognostic predictor of hepatocellular carcinoma
Wang, R., Zhu, Y., Zhong, H., Gao, X., Sun, Q., & He, M. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1007305 · Cited by 13 · see citing works
- Authors
- Hamann, J. C., Surcel, A., Chen, R., Teragawa, C., Albeck, J. G., Robinson, D. N., & Overholtzer, M.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Johns Hopkins University (US)
- University of California, Davis (US)
- Corresponding author
- Overholtzer, Michael
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2017-07
- Volume
- 20
- Issue
- 1
- Pages
- 201-210
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC5559205
- OpenAlex
- W2731058674
- Cited by
- 203
- References
- 39
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 18 · 2023: 19 · 2022: 24 · 2021: 40 · 2020: 20 · 2019: 27 · 2018: 18 · 2017: 7
- FWCI
- 8.05
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- Funders
- NIH (CA154649, GM66817)
- Benjamin Friedman Research Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- entosis, glucose deprivation, cell competition, AMPK, cell deformability, metabolic stress, nutrient deprivation, cell death, cancer
- MeSH terms
- AMP-Activated Protein Kinase Kinases, Glucose, Humans, Protein Kinases, Stress, Physiological, Cell Proliferation, Entosis, MCF-7 Cells
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