A Nonapoptotic Cell Death Process, Entosis, that Occurs by Cell-in-Cell Invasion
Open accessAbstract
Epithelial cells require attachment to extracellular matrix (ECM) to suppress an apoptotic cell death program termed anoikis. Here we describe a nonapoptotic cell death program in matrix-detached cells that is initiated by a previously unrecognized and unusual process involving the invasion of one cell into another, leading to a transient state in which a live cell is contained within a neighboring host cell. Live internalized cells are either degraded by lysosomal enzymes or released. We term this cell internalization process entosis and present evidence for entosis as a mechanism underlying the commonly observed "cell-in-cell" cytological feature in human cancers. Further we propose that entosis is driven by compaction force associated with adherens junction formation in the absence of integrin engagement and may represent an intrinsic tumor suppression mechanism for cells that are detached from ECM.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Entosis is a live-cell engulfment pathway occurring between two neighbouring cells, one of which will be actively engulfed by the other to form a cell-in-cell structure.
“Entosis is a live-cell engulfment pathway occurring between two neighbouring cells, one of which will be actively engulfed by the other to form a ‘cell-in-cell’ structure [35].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [35]
Entosis is mainly triggered by detachment of epithelial cells from the extracellular matrix and consequent loss of integrin signaling.
“Entosis is mainly triggered by the detachment of epithelial cells from the extracellular matrix and consequent loss of integrin signaling [263, 694]”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [694]
Once engulfed, entotic cells are often eliminated by a RCD subroutine independent of BCL2 proteins and caspases, but relying at least in part on LC3-associated phagocytosis.
“Once engulfed, entotic cells are often eliminated by a RCD subroutine that occurs independently of BCL2 proteins and caspases [694, 704], but relies (at least in part) on a specific autophagy-related process commonly known as LC3-associated phagocytosis (LAP) [509, 705, 706].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [694]
Abrogation of entosis by a chemical ROCK inhibitor favors anchorage-independent growth of malignant cells.
“abrogation of entosis by a chemical ROCK inhibitor reportedly favors the anchorage-independent growth of malignant cells [694].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [694]
Uptake of entotic cells is an integrin-independent process promoted by formation of junctions between engulfing and entotic cells involving CDH1 and CTNNA1.
“the uptake of entotic cells is an integrin-independent process promoted by the formation of junctions between engulfing and entotic cells that involve the adhesion proteins cadherin 1 (CDH1; also known as E-cadherin) and catenin alpha 1 (CTNNA1) [694, 699].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [694]
Entotic cell death has been documented in several human neoplasms, presumably operating as an oncosuppressor mechanism.
“Entotic cell death has been documented in several human neoplasms, presumably operating as an oncosuppressor mechanism [694, 695, 701, 709, 710].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [694]
Cites
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321 · see citing works
Disruption of epithelial cell-matrix interactions induces apoptosis
Frisch, S., & Francis, H. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.4.619 · Cited by 3,272 · 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
Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension
Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., Tamakawa, H., Yamagami, K., Inui, J., Maekawa, M., et al. (1997) · Nature · doi:10.1038/40187 · Cited by 2,862 · see citing works
Programmed Cell Death in Animal Development
Jacobson, M. D., Weil, M., & RAFF, M. C. (1997) · Cell · doi:10.1016/s0092-8674(00)81873-5 · Cited by 2,685 · see citing works
The extracellular matrix as a cell survival factor.
Meredith, J. E., Fazeli, B., & Schwartz, M. A. (1993) · Molecular Biology of the Cell · doi:10.1091/mbc.4.9.953 · Cited by 1,540 · see citing works
A receptor for phosphatidylserine-specific clearance of apoptotic cells
Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A. M., Ezekowitz, R. A. B., & Henson, P. M. (2000) · Nature · doi:10.1038/35011084 · Cited by 1,491 · see citing works
Kraupp, B. G., Ruttkay-Nedecký, B., Koudelka, H., Bukowska, K., Bursch, W., & Schulte‐Hermann, R. (1995) · Hepatology · doi:10.1002/hep.1840210534 · Cited by 1,167 · see citing works
Transforming properties of YAP , a candidate oncogene on the chromosome 11q22 amplicon
Overholtzer, M., Zhang, J., Smolen, G. A., Muir, B., Li, W., Sgroi, D. C., Deng, C., Brugge, J. S., & Haber, D. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605579103 · Cited by 885 · see citing works
Self-citationDebnath, J., Mills, K. R., Collins, N. L., Reginato, M. J., Muthuswamy, S. K., & Brugge, J. S. (2002) · Cell · doi:10.1016/s0092-8674(02)01001-2 · Cited by 763 · see citing works
Self-citationGilmore, A. P. (2005) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4401723 · Cited by 597 · see citing works
Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite
Aikawa, M., Miller, L., Johnson, J. G., & Rabbege, J. R. (1978) · The Journal of Cell Biology · doi:10.1083/jcb.77.1.72 · Cited by 582 · see citing works
Sekine, A., Fujiwara, M., & Narumiya, S. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)81834-8 · Cited by 541 · see citing works
Adams, C. L., Chen, Y., Smith, S. J., & Nelson, W. J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.4.1105 · Cited by 528 · see citing works
Grasl‐Kraupp, B. (1995) · Hepatology · doi:10.1016/0270-9139(95)90071-3 · Cited by 517 · see citing works
Does Autophagy Contribute To Cell Death?
Debnath, J., Baehrecke, E. H., & Kroemer, G. (2005) · Autophagy · doi:10.4161/auto.1.2.1738 · Cited by 444 · see citing works
Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines
Shi, Q., & King, R. W. (2005) · Nature · doi:10.1038/nature03958 · Cited by 396 · see citing works
Self-citationInterdigital cell death can occur through a necrotic and caspase-independent pathway
Chautan, M., Chazal, G., Cecconi, F., Gruß, P., & Golstein, P. (1999) · Current Biology · doi:10.1016/s0960-9822(99)80425-4 · Cited by 325 · see citing works
Integrin-dependent actomyosin contraction regulates epithelial cell scattering
de Rooij, J., Kerstens, A., Danuser, G. M., Schwartz, M. A., & Waterman, C. M. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200506152 · Cited by 324 · see citing works
Caspase-independent cell death?
Lockshin, R. A., & Zakeri, Z. F. (2004) · Oncogene · doi:10.1038/sj.onc.1207514 · Cited by 270 · see citing works
Cytomechanics of cadherin-mediated cell—cell adhesion
Adams, C. L., & Nelson, W. J. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80031-8 · Cited by 259 · see citing works
Sauzeau, V., Mellionnec, E. L., Bertoglio, J. H., Scalbert, E., Pacaud, P., & Loirand, G. (2001) · Circulation Research · doi:10.1161/hh1101.092034 · Cited by 258 · see citing works
Mailleux, A. A., Overholtzer, M., Schmelzle, T., Bouillet, P., Strasser, A., & Brugge, J. S. (2007) · Developmental Cell · doi:10.1016/j.devcel.2006.12.003 · Cited by 255 · see citing works
Self-citationRyan, P. L., Foty, R. A., Kohn, J., & Steinberg, M. S. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.071615398 · Cited by 245 · see citing works
Monks, J., Rosner, D., Geske, F. J., Lehman, L. A., Hanson, L., Neville, M. C., & Fadok, V. A. (2005) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401517 · Cited by 225 · see citing works
Opitz, C., & Soldati‐Favre, D. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03056.x · Cited by 209 · see citing works
An auxiliary mode of apoptotic DNA fragmentation provided by phagocytesPreprint
McIlroy, D., Tanaka, M., Sakahira, H., Fukuyama, H., Suzuki, M., Yamamura, K., Ohsawa, Y., Uchiyama, Y., & Nagata, S. (2000) · Genes & Development · doi:10.1101/gad.14.5.549 · Cited by 193 · see citing works
Autocrine CSF-1R activation promotes Src-dependent disruption of mammary epithelial architecture
Wrobel, C. N., Debnath, J., Lin, E., Beausoleil, S. A., Roussel, M. F., & Brugge, J. S. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200309102 · Cited by 106 · see citing works
Self-citationCell cannibalism in ductal carcinoma of breast
Abodief, W. T., Dey, P., & Al‐Hattab, O. (2006) · Cytopathology · doi:10.1111/j.1365-2303.2006.00326.x · Cited by 86 · see citing works
Cell cannibalism: Diagnostic marker of malignancy
Gupta, K., & Dey, P. (2003) · Diagnostic Cytopathology · doi:10.1002/dc.10234 · Cited by 76 · see citing works
Brouwer, M., de Ley, L., Feltkamp, C. A., Elema, J. D., & Jongsma, A. (1984) · PubMed · Cited by 56 · see citing works
内殖可能基層上での組織の伸展は細胞‐細胞 対 細胞‐基層粘着性の競合の結果である
Ryan, P. L., Foty, R. A., Kohn, J., & Steinberg, M. S. (2001) · Cited by 49 · see citing works
Phagocytic tumor cell activity in oat cell carcinoma of the lung.
DeSimone, P. A., East, R., & Powell, R. D. (1980) · PubMed · Cited by 45 · see citing works
Context based mixture model for cell phase identification in automated fluorescence microscopy
Wang, M., Zhou, X., King, R. W., & Wong, S. T. C. (2007) · BMC Bioinformatics · doi:10.1186/1471-2105-8-32 · Cited by 36 · see citing works
Self-citationGiant-cell carcinoma of the lung. A cytologic study.
Craig, I. D., Desrosiers, P., & Lefcoe, M. S. (1983) · PubMed · Cited by 34 · see citing works
Jin, J., & Woodgett, J. R. (2005) · Oncogene · doi:10.1038/sj.onc.1208704 · Cited by 30 · see citing works
The exfoliative cytology of endometrial stromal sarcoma in peritoneal fluid.
Hong, I. S. (1981) · PubMed · Cited by 29 · see citing works
Uei, Y., WATANABE, Y., Hirota, T., Yamamoto, H., & Watanabe, H. (1980) · PubMed · Cited by 21 · see citing works
Flagged first, then by citations
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
Self-citationClassification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009
Kroemer, G., Galluzzi, L., Vandenabeele, P., Abrams, J., Alnemri, E. S., Baehrecke, E. H., Blagosklonny, M. V., El-Deiry, W. S., Golstein, P., Green, D. R., et al. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2008.150 · Cited by 3,399 · see citing works
Doherty, G. J., & McMahon, H. T. (2009) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.78.081307.110540 · Cited by 3,075 · 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
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
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
The Double-Edged Sword of Autophagy Modulation in Cancer
White, E., & DiPaola, R. S. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-5023 · Cited by 1,137 · see citing works
Fricker, M., Tolkovsky, A. M., Borutaitė, V., Coleman, M. P., & Brown, G. C. (2018) · Physiological Reviews · doi:10.1152/physrev.00011.2017 · Cited by 1,122 · see citing works
Cell Death SignalingPreprint
Green, D. R., & Llambi, F. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a006080 · Cited by 1,117 · see citing works
Essential versus accessory aspects of cell death: recommendations of the NCCD 2015
Galluzzi, L., Bravo-San Pedro, J. M., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Alnemri, E. S., Altucci, L., Andrews, D., Annicchiarico-Petruzzelli, M., et al. (2015) · Cell Death & Differentiation · doi:10.1038/cdd.2014.137 · Cited by 1,002 · see citing works
Fundamental Mechanisms of Regulated Cell Death and Implications for Heart Disease
Re, D. P. D., Amgalan, D., Linkermann, A., Liu, Q., & Kitsis, R. N. (2019) · Physiological Reviews · doi:10.1152/physrev.00022.2018 · Cited by 979 · 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
The clearance of dead cells by efferocytosis
Boada-Romero, E., Martinez, J., Heckmann, B. L., & Green, D. R. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-0232-1 · Cited by 893 · see citing works
Regulated cell death (RCD) in cancer: key pathways and targeted therapies
Peng, F., Liao, M., Qin, R., Zhu, S., Peng, C. Y., Fu, L., Chen, Y., & Han, B. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01110-y · Cited by 850 · see citing works
Lysosomal membrane permeabilization and cell death
Wang, F., Gómez‐Sintes, R., & Boya, P. (2018) · Traffic · doi:10.1111/tra.12613 · Cited by 781 · see citing works
Curcumin and Cancer Cells: How Many Ways Can Curry Kill Tumor Cells Selectively?
Ravindran, J., Prasad, S., & Aggarwal, B. B. (2009) · The AAPS Journal · doi:10.1208/s12248-009-9128-x · Cited by 768 · see citing works
Defining the Hallmarks of Metastasis
Welch, D. R., & Hurst, D. R. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-0458 · Cited by 695 · 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
Cell death assays for drug discovery
Kepp, O., Galluzzi, L., Lipinski, M. M., Yuan, J., & Kroemer, G. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3373 · Cited by 556 · see citing works
Canonical and non-canonical autophagy: variations on a common theme of self-eating?
Codogno, P., Mehrpour, M., & Proikas‐Cezanne, T. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3249 · Cited by 545 · see citing works
Caspase-mediated cleavage of phospholipid flippase for apoptotic phosphatidylserine exposure
Segawa, K., Kurata, S., Yanagihashi, Y., Brummelkamp, T. R., Matsuda, F., & Nagata, S. (2014) · Science · doi:10.1126/science.1252809 · Cited by 528 · see citing works
Wong, P., Puente, C., Ganley, I. G., & Jiang, X. (2013) · Autophagy · doi:10.4161/auto.23323 · Cited by 494 · see citing works
Biodegradable Polymer Nanogels for Drug/Nucleic Acid Delivery
Li, Y., Maciel, D., Rodrigues, J., Shi, X., & Tomás, H. (2015) · Chemical Reviews · doi:10.1021/cr500131f · Cited by 480 · 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 roles of metallothioneins in carcinogenesis
Si, M., & Lang, J. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0645-x · Cited by 457 · see citing works
The hallmarks of COVID-19 disease
Tang, D., Comish, P. B., & Kang, R. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008536 · Cited by 448 · see citing works
Overcoming anoikis – pathways to anchorage-independent growth in cancer
Guadamillas, M. C., Cerezo, A., & del Pozo, M. Á. (2011) · Journal of Cell Science · doi:10.1242/jcs.072165 · Cited by 425 · 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 431 · see citing works
Asymmetric division of contractile domains couples cell positioning and fate specification
Maître, J., Turlier, H., Illukkumbura, R., Eismann, B., Niwayama, R., Nédélec, F., & Hiiragi, T. (2016) · Nature · doi:10.1038/nature18958 · Cited by 381 · see citing works
Modes of Regulated Cell Death in Cancer
Koren, E., & Fuchs, Y. (2021) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0789 · Cited by 378 · see citing works
Male germ cell apoptosis: regulation and biology
Shaha, C., Tripathi, R. P., & Mishra, D. P. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0124 · Cited by 372 · see citing works
Cancer cell survival during detachment from the ECM: multiple barriers to tumour progression
Buchheit, C. L., Weigel, K. J., & Schafer, Z. T. (2014) · Nature Reviews Cancer · doi:10.1038/nrc3789 · Cited by 367 · see citing works
Nag, S. A. (2012) · Frontiers in Pharmacology · doi:10.3389/fphar.2012.00025 · Cited by 355 · 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
Fusion of tumour cells with bone marrow-derived cells: a unifying explanation for metastasis
Pawelek, J. M., & Chakraborty, A. K. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2371 · Cited by 324 · see citing works
Eaten alive! Cell death by primary phagocytosis: ‘phagoptosis’
Brown, G. C., & Neher, J. J. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.05.002 · Cited by 320 · see citing works
Sabbah, M., Emami, S., Redeuilh, G., Julien-Grille, S., Prevost, G. P., Zimber, A., Ouelaa-Benslama, R., Bracke, M., Wever, O. D., & Gespach, C. P. (2008) · Drug Resistance Updates · doi:10.1016/j.drup.2008.07.001 · Cited by 322 · see citing works
Stat3 controls lysosomal-mediated cell death in vivo
Kreuzaler, P. A., Staniszewska, A. D., Li, W., Omidvar, N., Kedjouar, B., Turkson, J., Poli, V., Flavell, R. A., Clarkson, R. W. E., & Watson, C. J. (2011) · Nature Cell Biology · doi:10.1038/ncb2171 · Cited by 312 · see citing works
Persistent Cancer Cells: The Deadly Survivors
Shen, S., Vagner, S., & Robert, C. (2020) · Cell · doi:10.1016/j.cell.2020.10.027 · Cited by 305 · see citing works
Alternative cell death mechanisms in development and beyondPreprint
Yuan, J., & Kroemer, G. (2010) · Genes & Development · doi:10.1101/gad.1984410 · Cited by 290 · 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
Cytokinesis defects and cancer
Lens, S. M. A., & Medema, R. H. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0084-6 · Cited by 266 · see citing works
Maltese, W. A., & Overmeyer, J. H. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2014.02.028 · Cited by 254 · see citing works
Family Iridoviridae: Poor Viral Relations No Longer
Chinchar, V. G., Hyatt, A. D., Miyazaki, T., & Williams, T. (2008) · Current topics in microbiology and immunology · doi:10.1007/978-3-540-68618-7_4 · Cited by 252 · 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-citationFinicle, B. T., Jayashankar, V., & Edinger, A. L. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0048-x · Cited by 228 · see citing works
Integrins and cell-fate determination
Streuli, C. H. (2009) · Journal of Cell Science · doi:10.1242/jcs.018945 · Cited by 220 · see citing works
V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation
Florey, O., Gammoh, N., Kim, S. E., Jiang, X., & Overholtzer, M. (2014) · Autophagy · doi:10.4161/15548627.2014.984277 · Cited by 212 · see citing works
Self-citationCell Fusion as a Hidden Force in Tumor Progression
Lü, X., & Kang, Y. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2159 · Cited by 211 · see citing works
Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila
Ohsawa, S., Sugimura, K., Takino, K., Xu, T., Miyawaki, A., & Igaki, T. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.02.007 · Cited by 200 · see citing works
The cell biology of cell-in-cell structures
Overholtzer, M., & Brugge, J. S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2504 · Cited by 202 · see citing works
Self-citationHayashi, 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-citationEntosis Is Induced by Glucose Starvation
Hamann, J. C., Surcel, A., Chen, R., Teragawa, C., Albeck, J. G., Robinson, D. N., & Overholtzer, M. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.06.037 · Cited by 203 · see citing works
Self-citationKim, S. M., Nguyen, T. T., Ravi, A., Kubiniok, P., Finicle, B. T., Jayashankar, V., Malacrida, L., Hou, J., Robertson, J., Gao, D., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-1215 · Cited by 199 · see citing works
Macrophage Clearance of Apoptotic Cells: A Critical Assessment
Gordon, S., & Plüddemann, A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00127 · Cited by 201 · see citing works
Mechanisms for Cell-to-Cell Transmission of HIV-1
Bracq, L., Xie, M., Bénichou, S., & Bouchet, J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00260 · Cited by 192 · see citing works
Emerging roles of ATG7 in human health and disease
Collier, J. J., Suomi, F., Oláhová, M., McWilliams, T. G., & Taylor, R. W. (2021) · EMBO Molecular Medicine · doi:10.15252/emmm.202114824 · Cited by 191 · see citing works
Cell-in-cell phenomena in cancer
Fais, S., & Overholtzer, M. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0073-9 · Cited by 190 · see citing works
Self-citationA 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-citationDanese, A., Patergnani, S., Bonora, M., Wieckowski, M. R., Previati, M., Giorgi, C., & Pinton, P. (2017) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2017.01.003 · Cited by 184 · see citing works
Brock, C. K., Wallin, S. T., Ruiz, O. E., Samms, K. M., Mandal, A., Sumner, E. A., & Eisenhoffer, G. T. (2019) · Nature Communications · doi:10.1038/s41467-019-09010-6 · Cited by 185 · see citing works
The essentials of developmental apoptosis
Voss, A. K., & Strasser, A. (2020) · F1000Research · doi:10.12688/f1000research.21571.1 · Cited by 183 · see citing works
Durgan, J., & Florey, O. (2022) · Science Advances · doi:10.1126/sciadv.abo1274 · Cited by 176 · see citing works
Andème‐Onzighi, C., Christopher, D. A., Cho, E. J., Chang, S.-C., & Staehelin, L. A. (2008) · The Plant Cell · doi:10.1105/tpc.108.058339 · Cited by 173 · see citing works
Cell death pathways of particulate matter toxicity
Peixoto, M. S., Galvão, M. F. D. O., & de Medeiros, S. R. B. (2017) · Chemosphere · doi:10.1016/j.chemosphere.2017.08.076 · Cited by 171 · see citing works
Autophagy-Regulating microRNAs and Cancer
Gözüaçık, D., Akkoç, Y., Öztürk, D. G., & Koçak, M. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00065 · Cited by 172 · see citing works
Vural, D. F., Cebesoy, S., & Karakaş, M. F. (2013) · Journal of Entomology and Zoology Studies · Cited by 171 · see citing works
Hepatocyte entry leads to degradation of autoreactive CD8 T cells
Benseler, V., Warren, A., Vo, M., Holz, L. E., Tay, S. S., Le Couteur, D. G., Breen, E., Allison, A. C., van Rooijen, N., McGuffog, C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1112251108 · Cited by 164 · see citing works
Remodeling mechanisms of the mammary gland during involution
Watson, C. J., & Kreuzaler, P. A. (2011) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113414cw · Cited by 166 · see citing works
Cancer cells enter dormancy after cannibalizing mesenchymal stem/stromal cells (MSCs)
Bartosh, T. J., Ullah, M., Zeitouni, S., Beaver, J., & Prockop, D. J. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612290113 · Cited by 164 · see citing works
Mazzone, M., Selfors, L. M., Albeck, J. G., Overholtzer, M., Šale, S., Carroll, D. L., Pandya, D., Lu, Y., Mills, G. B., Aster, J. C., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1000896107 · Cited by 163 · see citing works
Self-citationKilling a cancer: what are the alternatives?
Kreuzaler, P. A., & Watson, C. J. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3264 · Cited by 162 · see citing works
Vasquez, Y. M., Wang, X., Wetendorf, M., Franco, H. L., Mo, Q., Wang, T., Lanz, R. B., Young, S. L., Lessey, B. A., Spencer, T. E., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007787 · Cited by 160 · see citing works
Entosis Allows Timely Elimination of the Luminal Epithelial Barrier for Embryo Implantation
Li, Y., Sun, X., & Dey, S. K. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.03.035 · Cited by 155 · 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-citationCell Competition: Mechanisms and Physiological Roles
Claverı́a, C., & Torres, M. (2016) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125142 · Cited by 156 · see citing works
Research progress on morphology and mechanism of programmed cell death
Chen, Y., Li, X., Yang, M., & Liu, S. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-06712-8 · Cited by 160 · see citing works
Induction 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-citationPIKfyve Regulates Vacuole Maturation and Nutrient Recovery following Engulfment
Krishna, S., Palm, W., Lee, Y., Yang, W., Bandyopadhyay, U., Xu, H., Florey, O., Thompson, C. B., & Overholtzer, M. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.001 · Cited by 140 · see citing works
Self-citationCancer stem cell niche models and contribution by mesenchymal stroma/stem cells
Melzer, C., von der Ohe, J., Lehnert, H., Ungefroren, H., & Hass, R. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0595-x · Cited by 149 · see citing works
Reactive Oxygen Species, Oxidative Damage and Cell Death
Ghosh, N., Das, A., Chaffee, S. M., Roy, S., & Sen, C. K. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-805417-8.00004-4 · Cited by 152 · see citing works
Exploiting Metabolic Vulnerabilities of Cancer with Precision and Accuracy
Wolpaw, A. J., & Dang, C. V. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.11.006 · Cited by 147 · see citing works
Gudipaty, S. A., Conner, C. M., Rosenblatt, J., & Montell, D. J. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060748 · Cited by 145 · see citing works
Hurst, D. R., & Welch, D. R. (2011) · International review of cytology · doi:10.1016/b978-0-12-385859-7.00003-3 · Cited by 136 · see citing works
Tumour microenvironment factors shaping the cancer metabolism landscape
Anastasiou, D. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.412 · Cited by 136 · see citing works
Wu, J., Ye, J., Kong, W., Zhang, S., & Zheng, Y. (2020) · Cell Proliferation · doi:10.1111/cpr.12915 · Cited by 133 · see citing works
Gaur, S., Wen, Y., Song, J. H., Parikh, N. U., Mangala, L. S., Blessing, A. M., Ivan, C., Wu, S. Y., Varkaris, A. S., Shi, Y., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4971 · Cited by 135 · see citing works
Autophagy proteins in macroendocytic engulfment
Florey, O., & Overholtzer, M. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.04.005 · Cited by 132 · see citing works
Self-citationThe Role of Microglia in Synaptic Stripping and Synaptic Degeneration: A Revised Perspective
Perry, V. H., & O'Connor, V. M. (2010) · ASN NEURO · doi:10.1042/an20100024 · Cited by 131 · see citing works
Pathophysiological role of different tubular epithelial cell death modes in acute kidney injury
Sancho-Martínez, S. M., López-Novoa, J. M., & López-Hernández, F. J. (2015) · Clinical Kidney Journal · doi:10.1093/ckj/sfv069 · Cited by 130 · see citing works
Wen, S., Niu, Y., Lee, S. O., & Chang, C. (2013) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2013.07.008 · Cited by 131 · see citing works
Mechanisms of Regulated Cell Death: Current Perspectives
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
Cytokinesis, ploidy and aneuploidy
Lacroix, B., & Maddox, A. (2012) · Journal of Pathology · doi:10.1002/path.3013 · Cited by 144 · see citing works
Brown, G. C. (2024) · Nature Reviews Immunology · doi:10.1038/s41577-023-00921-6 · Cited by 129 · see citing works
Chemotherapy-induced senescent cancer cells engulf other cells to enhance their survival
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
Antioxidant Enzymes Mediate Survival of Breast Cancer Cells Deprived of Extracellular Matrix
Davison, C. A., Durbin, S., Thau, M. R., Zellmer, V. R., Chapman, S. E., Diener, J. M., Wathen, C. A., Leevy, W. M., & Schafer, Z. T. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-2482 · Cited by 124 · see citing works
CDK5 is essential for TGF-β1-induced epithelial-mesenchymal transition and breast cancer progression
Liang, Q. Y., Li, L., Zhang, J., Yang, L., Wang, L., Liu, D., Feng, J., Hou, P., Yao, R., Zhang, Y., et al. (2013) · Scientific Reports · doi:10.1038/srep02932 · Cited by 123 · see citing works
Kim, M. E., Shrestha, B. R., Blazeski, R., Mason, C. A., & Grueber, W. B. (2012) · Neuron · doi:10.1016/j.neuron.2011.10.033 · Cited by 123 · see citing works
Mitosis can drive cell cannibalism through entosis
Durgan, J., Tseng, Y.-Y., Hamann, J. C., Domart, M.-C., Collinson, L., Hall, A., Overholtzer, M., & Florey, O. (2017) · eLife · doi:10.7554/elife.27134 · Cited by 117 · see citing works
Self-citationHidden Behind Autophagy: The Unconventional Roles of ATG Proteins
Bestebroer, J., V’kovski, P., Mauthe, M., & Reggiori, F. (2013) · Traffic · doi:10.1111/tra.12091 · Cited by 120 · see citing works
- Authors
- Overholtzer, M., Mailleux, A. A., Mouneimne, G., Normand, G., Schnitt, S. J., King, R. W., Cibas, E. S., & Brugge, J. S.
- Affiliations
- Harvard University (US)
- Beth Israel Deaconess Medical Center (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Brugge, Joan S.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2007-11
- Volume
- 131
- Issue
- 5
- Pages
- 966-979
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2112497627
- Cited by
- 748
- References
- 38
- Citations by year
- 2026: 30 · 2025: 50 · 2024: 61 · 2023: 63 · 2022: 44 · 2021: 55 · 2020: 43 · 2019: 54 · 2018: 51 · 2017: 44 · 2016: 28 · 2015: 38 · 2014: 23 · 2013: 39 · 2012: 31
- FWCI
- 8.73
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 2121 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (T32-CA 09361, CA 089393, T32CA009361, CA080111, P01CA080111, P50CA089393)
- National Institute of General Medical Sciences (GM66492)
- 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, non-apoptotic cell death, anoikis, extracellular matrix detachment, cellular internalization, lysosomal degradation, adherens junctions, tumor suppression, epithelial cells, tumor cytology
- MeSH terms
- Actins, Autophagy, Breast Neoplasms, Carcinoma, Cell Adhesion, Cell Communication, Extracellular Matrix, Humans, Lysosomes, Models, Biological, Tumor Cells, Cultured, Cadherins, Apoptosis, rho GTP-Binding Proteins, Adherens Junctions, Myosin Type II, rho-Associated Kinases
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
