Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes
Open accessAbstract
Autophagy normally involves the formation of double-membrane autophagosomes that mediate bulk cytoplasmic and organelle degradation. Here we report the modification of single-membrane vacuoles in cells by autophagy proteins. LC3 (Light chain 3) a component of autophagosomes, is recruited to single-membrane entotic vacuoles, macropinosomes and phagosomes harbouring apoptotic cells, in a manner dependent on the lipidation machinery including ATG5 and ATG7, and the class III phosphatidylinositol-3-kinase VPS34. These downstream components of the autophagy machinery, but not the upstream mammalian Tor (mTor)-regulated ULK-ATG13-FIP200 complex, facilitate lysosome fusion to single membranes and the degradation of internalized cargo. For entosis, a live-cell-engulfment program, the autophagy-protein-dependent fusion of lysosomes to vacuolar membranes leads to the death of internalized cells. As pathogen-containing phagosomes can be targeted in a similar manner, the death of epithelial cells by this mechanism mimics pathogen destruction. These data demonstrate that proteins of the autophagy pathway can target single-membrane vacuoles in cells in the absence of pathogenic organisms.
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The internalised cell in a phagosome is decorated by LC3 and itself undergoes programmed cell death.
“The internalised cell in a phagosome is shown to be decorated by LC3 and itself undergoes programmed cell death [12].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [12]
The Introduction says LC3 is recruited to the entotic vacuole membrane surrounding an internalized cell, and that the cell is subsequently killed by its host. The Results section on apoptotic cell phagosomes likewise places LC3 on the phagosome membrane, not on the internalized cell itself. Thus the claim captures LC3 recruitment and cell death but misidentifies what LC3 decorates. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMicropinosomes and endocytic vesicles filled with extracellular fluid also recruited LC3.
“The same report also demonstrated that micropinosomes, and endocytic vesicles filled with extracellular fluid, also recruited LC3 [12].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [12]
The Results section, “Macropinosomes recruit LC3” (page unavailable), reports GFP-LC3 recruitment to about 50% of macropinosomes. The cited paper says macropinosomes, not micropinosomes; its macropinosome assays used vesicles labeled with dextran added to the culture medium. (LLM, conf=0.89)
Experimental — accuracy not yet measuredLC3 can be recruited to single-membrane phagosomes in a process termed LC3-associated phagocytosis (LAP).
“Recently, it has been demonstrated that LC3 can be recruited to other membranes including single-membrane phagosomes, in a process termed LC3-associated phagocytosis (LAP).”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [12]
In LAP, LC3 is recruited directly to the single-membrane phagosome, distinct from conventional autophagy where LC3 is incorporated into the double-membrane autophagosome.
“In LAP, distinct from the conventional autophagic pathway where LC3 is incorporated into the double-membrane autophagosome, LC3 is recruited directly to the single-membrane phagosome [12,16,18].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [12]
Some components of the macroautophagy apparatus, including LC3, ATG5, ATG7, and VPS34, are recruited to the cytosolic side of entotic cell-containing vesicles and promote their fusion with lysosomes in the absence of bona fide autophagosome formation.
“some (but not all) components of the macroautophagy apparatus, including microtubule associated protein 1 light chain 3 beta (MAP1LC3B; best known as LC3), autophagy related 5 (ATG5), ATG7, and phosphatidylinositol 3-kinase catalytic subunit type 3 (PIK3C3; best known as VPS34) are recruited to the cytosolic side of entotic cell-containing vesicles and promote their fusion with lysosomes (in the”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [704]
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 [704]
Lysosomal degradation of internalized entotic cells generates nutrients recovered by engulfing cells via a mechanism involving PIKFYVE.
“the lysosomal degradation of internalized entotic cells generates nutrients that are recovered by engulfing cells, via a mechanism that reportedly involves phosphoinositide kinase, FYVE-type zinc finger containing (PIKFYVE) [704, 707, 708].”
From Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. (2018) · cites this paper as [704]
Like conventional autophagy, LAP requires Beclin-1, Atg5, and Atg7 but proceeds independently of the autophagic pre-initiation complex, including Ulk1, Fip200/Atg17, and ATG13.
“Like conventional autophagy, LAP requires Beclin-1, Atg5, and Atg7 (Florey et al., 2011; Henault et al., 2012; Martinez et al., 2011; Sanjuan et al., 2007) but LAP proceeds independently of the autophagic pre-initiation complex, including Ulk1 (Henault et al., 2012; Martinez et al., 2011), Fip200/Atg17 (Florey et al., 2011; Henault et al., 2012), and ATG13 (Henault et al., 2012).”
From Noncanonical autophagy promotes the visual cycle (2013) · cites this paper as Florey et al., 2011
There is a functional convergence of autophagy and phagocytosis where components of the autophagy pathway are co-opted by phagocytosis to increase degradation of phagocytosed cargo by aiding lysosome/phagosome fusion and phagolysosome maturation.
“Recent studies from several laboratories (DeSelm et al., 2011; Florey et al., 2011; Henault et al., 2012; Martinez et al., 2011) have shown that there is a functional convergence of autophagy and phagocytosis where components of the autophagy pathway have been co-opted by phagocytosis to increase the efficient degradation of the phagocytosed cargo by aiding in lysosome/phagosome fusion as well as”
From Noncanonical autophagy promotes the visual cycle (2013) · cites this paper as Florey et al., 2011
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Martinez, J., Malireddi, R. K. S., Lu, Q., Cunha, L. D., Pelletier, S., Gingras, S., Orchard, R., Guan, J.-L., Tan, H., Peng, J., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3192 · Cited by 758 · see citing works
“These data support the idea that LAP does not require the activity of the pre-initiation complex 6–9 , Ambra1 or WIPI2.”
InfluentialRetractedMacrophage Autophagy Plays a Protective Role in Advanced Atherosclerosis
Liao, X., Sluimer, J. C., Wang, Y., Subramanian, M., Brown, K., Pattison, J. S., Robbins, J., Martinez, J., & Tabas, I. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.01.022 · Cited by 627 · see citing works
Caielli, S., Athale, S., Domic, B., Murat, E., Chandra, M., Banchereau, R., Baisch, J., Phelps, K., Clayton, S., Gong, M., et al. (2016) · Journal of Experimental Medicine · doi:10.1084/jem.20151876 · Cited by 501 · see citing works
Autophagy and cellular immune responses
Ma, Y., Galluzzi, L., Zitvogel, L., & Kroemer, G. (2013) · Immunity · doi:10.1016/j.immuni.2013.07.017 · Cited by 447 · see citing works
Lucin, K. M., O’Brien, C. E., Bieri, G., Czirr, E., Mosher, K. I., Abbey, R. J., Mastroeni, D. F., Rogers, J., Spencer, B., Masliah, E., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.046 · Cited by 374 · see citing works
Martinez, J., Cunha, L. D., Park, S., Yang, M., Lu, Q., Orchard, R., Li, Q.-Z., Yan, M., Janke, L., Guy, C., et al. (2016) · Nature · doi:10.1038/nature17950 · Cited by 381 · see citing works
RetractedCancer 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
Noncanonical autophagy promotes the visual cycle
Kim, J.-Y., Zhao, H., Martinez, J., Doggett, T. A., Kolesnikov, A. V., Tang, P. H., Ablonczy, Z., Chan, C.-C., Zhou, Z., Green, D. R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.012 · Cited by 347 · see citing works
Henault, J., Martinez, J., Riggs, J. M., Tian, J., Mehta, P., Clarke, L., Sasai, M., Latz, E., Brinkmann, M. M., Iwasaki, A., et al. (2012) · Immunity · doi:10.1016/j.immuni.2012.09.014 · Cited by 348 · see citing works
LC3-Associated Phagocytosis in Myeloid Cells Promotes Tumor Immune Tolerance
Cunha, L. D., Yang, M., Carter, R., Guy, C., Harris, L., Crawford, J. C., Quarato, G., Boada-Romero, E., Kalkavan, H., Johnson, M. D. L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.061 · Cited by 334 · see citing works
The clearance of dying cells: table for two
Green, D. R., Oguin, T. H., & Martinez, J. (2016) · Cell Death & Differentiation · doi:10.1038/cdd.2015.172 · Cited by 314 · 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-citationAspergillus Cell Wall Melanin Blocks LC3-Associated Phagocytosis to Promote Pathogenicity
Akoumianaki, T., Kyrmizi, I., Valsecchi, I., Gresnigt, M. S., Samonis, G., Drakos, E., Boumpas, D., Muszkieta, L., Prevost, M.-C., Kontoyiannis, D. P., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2015.12.002 · Cited by 218 · see citing works
Entosis 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-citationmTOR 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-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-citationAutophagy in the eye: implications for ocular cell health.
Frost, L. S., Mitchell, C. H., & Boesze-Battaglia, K. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.04.010 · Cited by 134 · 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-citationThe regulation of cancer cell death and metabolism by extracellular matrix attachment
Buchheit, C. L., Rayavarapu, R. R., & Schafer, Z. T. (2012) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2012.04.007 · Cited by 115 · see citing works
Mechanisms and consequences of entosis
Krishna, S., & Overholtzer, M. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2207-0 · Cited by 118 · see citing works
Self-citationLC3-Associated Phagocytosis (LAP): Connections with Host Autophagy
Lai, S.-C., & Devenish, R. J. (2012) · Cells · doi:10.3390/cells1030396 · Cited by 116 · see citing works
“The same report also demonstrated that micropinosomes, and endocytic vesicles filled with extracellular fluid, also recruited LC3 [12].”
BackgroundInfluentialLc3-associated phagocytosis—The highway to hell for phagocytosed microbes
Herb, M., Gluschko, A., & Schramm, M. (2020) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2019.04.016 · Cited by 103 · see citing works
Autophagy promotes mammalian survival by suppressing oxidative stress and p53
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Rubicon: <scp>LC</scp>3‐associated phagocytosis and beyond
Wong, S., Sil, P., & Martinez, J. (2018) · The FEBS Journal · doi:10.1111/febs.14354 · Cited by 101 · see citing works
Li, W., Zou, W., Yang, Y., Chai, Y., Chen, B., Cheng, S., Tian, D., Wang, X., Vale, R. D., & Ou, G. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201111053 · Cited by 84 · see citing works
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Entosis: Cell-in-Cell Formation that Kills Through Entotic Cell Death
Florey, O., Kim, S., & Overholtzer, M. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666151026100042 · Cited by 45 · see citing works
Self-citationAutophagy proteins regulate cell engulfment mechanisms that participate in cancer
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Self-citationWen, S., Shang, Z., Zhu, S., Chang, C., & Niu, Y. (2013) · The Prostate · doi:10.1002/pros.22676 · Cited by 32 · see citing works
Entosis Acts as a Novel Way within Sertoli Cells to Eliminate Spermatozoa in Seminiferous Tubule
Ahmed, N., Yang, P., Huang, Y., Chen, H., Liu, T., Wang, L., Nabi, F., Liu, Y., & Chen, Q. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00361 · Cited by 15 · see citing works
- Authors
- Florey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M., & Overholtzer, M.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- University of Arizona (US)
- Corresponding author
- Overholtzer, Michael
- Venue
- Nature Cell Biology
- Published
- 2011-10-16
- Volume
- 13
- Issue
- 11
- Pages
- 1335-1343
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC3223412
- OpenAlex
- W2018418660
- Cited by
- 459
- References
- 65
- Citations by year
- 2026: 15 · 2025: 26 · 2024: 34 · 2023: 30 · 2022: 39 · 2021: 36 · 2020: 29 · 2019: 35 · 2018: 31 · 2017: 25 · 2016: 36 · 2015: 27 · 2014: 27 · 2013: 34 · 2012: 30
- FWCI
- 22.67
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA154649, CA154649)
- 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 › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Keywords
- autophagy, entosis, macropinosomes, phagosome, LC3, ATG5, ATG7, Vps34, class III phosphatidylinositol 3-kinase, lysosome fusion, apoptotic cell engulfment, epithelial cell death, autophagosome formation
- MeSH terms
- Autophagy-Related Protein 5, Autophagy-Related Protein 7, Autophagy, Endocytosis, Humans, Intracellular Membranes, Lysosomes, Membrane Fusion, Microtubule-Associated Proteins, Time Factors, Transfection, Vacuoles, Proto-Oncogene Proteins c-bcl-2, RNA Interference, Ubiquitin-Activating Enzymes, Cell Line, Tumor, Papillomavirus E7 Proteins, Class III Phosphatidylinositol 3-Kinases
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