Gudipaty SA, Conner CM, Rosenblatt J, Montell DJ (2018) Unconventional ways to live and die: cell death and survival in development, homeostasis, and disease. Annu Rev Cell Dev Biol 34:311–332. https://doi.org/10.1146/annurev-cellbio-100616-060748
CAS
Article
PubMed
Google Scholar
Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257
CAS
PubMed
PubMed Central
Google Scholar
Diamantis A, Magiorkinis E, Sakorafas GH, Androutsos G (2008) A brief history of apoptosis: from ancient to modern times. Onkologie 31(12):702–706. https://doi.org/10.1159/000165071
Article
PubMed
Google Scholar
Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516. https://doi.org/10.1080/01926230701320337
CAS
Article
PubMed
PubMed Central
Google Scholar
Ambrosini A, Gracia M, Proag A, Rayer M, Monier B, Suzanne M (2017) Apoptotic forces in tissue morphogenesis. Mech Dev 144(Pt A):33–42. https://doi.org/10.1016/j.mod.2016.10.001
CAS
Article
PubMed
Google Scholar
Saraste A, Pulkki K (2000) Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 45(3):528–537
CAS
Article
Google Scholar
Model MA (2014) Possible causes of apoptotic volume decrease: an attempt at quantitative review. Am J Physiol Cell Physiol 306(5):C417–C424. https://doi.org/10.1152/ajpcell.00328.2013
CAS
Article
PubMed
Google Scholar
Okada Y, Shimizu T, Maeno E, Tanabe S, Wang X, Takahashi N (2006) Volume-sensitive chloride channels involved in apoptotic volume decrease and cell death. J Membr Biol 209(1):21–29. https://doi.org/10.1007/s00232-005-0836-6
CAS
Article
PubMed
Google Scholar
Beauvais F, Michel L, Dubertret L (1995) Human eosinophils in culture undergo a striking and rapid shrinkage during apoptosis. Role of K+ channels. J Leukoc Biol 57(6):851–855
CAS
Article
Google Scholar
Barry MA, Reynolds JE, Eastman A (1993) Etoposide-induced apoptosis in human HL-60 cells is associated with intracellular acidification. Cancer Res 53(10 Suppl):2349–2357
CAS
PubMed
Google Scholar
Moran J, Hernandez-Pech X, Merchant-Larios H, Pasantes-Morales H (2000) Release of taurine in apoptotic cerebellar granule neurons in culture. Pflugers Arch 439(3):271–277
CAS
Article
Google Scholar
Flamenco P, Galizia L, Rivarola V, Fernandez J, Ford P, Capurro C (2009) Role of AQP2 during apoptosis in cortical collecting duct cells. Biol Cell 101(4):237–250. https://doi.org/10.1042/BC20080050
CAS
Article
PubMed
Google Scholar
Model MA, Schonbrun E (2013) Optical determination of intracellular water in apoptotic cells. J Physiol 591(23):5843–5849. https://doi.org/10.1113/jphysiol.2013.263228
CAS
Article
PubMed
PubMed Central
Google Scholar
Mills JC, Stone NL, Erhardt J, Pittman RN (1998) Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol 140(3):627–636
CAS
Article
Google Scholar
Tixeira R, Caruso S, Paone S, Baxter AA, Atkin-Smith GK, Hulett MD, Poon IK (2017) Defining the morphologic features and products of cell disassembly during apoptosis. Apoptosis 22(3):475–477. https://doi.org/10.1007/s10495-017-1345-7
Article
PubMed
Google Scholar
Wickman GR, Julian L, Mardilovich K, Schumacher S, Munro J, Rath N, Zander SA, Mleczak A, Sumpton D, Morrice N, Bienvenut WV, Olson MF (2013) Blebs produced by actin-myosin contraction during apoptosis release damage-associated molecular pattern proteins before secondary necrosis occurs. Cell Death Differ 20(10):1293–1305. https://doi.org/10.1038/cdd.2013.69
CAS
Article
PubMed
PubMed Central
Google Scholar
Atkin-Smith GK, Poon IKH (2017) Disassembly of the dying: mechanisms and functions. Trends Cell Biol 27(2):151–162. https://doi.org/10.1016/j.tcb.2016.08.011
CAS
Article
PubMed
Google Scholar
Moss DK, Betin VM, Malesinski SD, Lane JD (2006) A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation. J Cell Sci 119(Pt 11):2362–2374. https://doi.org/10.1242/jcs.02959
CAS
Article
PubMed
PubMed Central
Google Scholar
Poon IK, Chiu YH, Armstrong AJ, Kinchen JM, Juncadella IJ, Bayliss DA, Ravichandran KS (2014) Unexpected link between an antibiotic, pannexin channels and apoptosis. Nature 507(7492):329–334. https://doi.org/10.1038/nature13147
CAS
Article
PubMed
PubMed Central
Google Scholar
Atkin-Smith GK, Tixeira R, Paone S, Mathivanan S, Collins C, Liem M, Goodall KJ, Ravichandran KS, Hulett MD, Poon IK (2015) A novel mechanism of generating extracellular vesicles during apoptosis via a beads-on-a-string membrane structure. Nat Commun 6:7439. https://doi.org/10.1038/ncomms8439
Article
PubMed
PubMed Central
Google Scholar
Atkin-Smith GK, Paone S, Zanker DJ, Duan M, Phan TK, Chen W, Hulett MD, Poon IK (2017) Isolation of cell type-specific apoptotic bodies by fluorescence-activated cell sorting. Sci Rep 7:39846. https://doi.org/10.1038/srep39846
CAS
Article
PubMed
PubMed Central
Google Scholar
Kobayashi N, Karisola P, Pena-Cruz V, Dorfman DM, Jinushi M, Umetsu SE, Butte MJ, Nagumo H, Chernova I, Zhu B, Sharpe AH, Ito S, Dranoff G, Kaplan GG, Casasnovas JM, Umetsu DT, Dekruyff RH, Freeman GJ (2007) TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 27(6):927–940. https://doi.org/10.1016/j.immuni.2007.11.011
CAS
Article
PubMed
PubMed Central
Google Scholar
Sachet M, Liang YY, Oehler R (2017) The immune response to secondary necrotic cells. Apoptosis 22(10):1189–1204. https://doi.org/10.1007/s10495-017-1413-z
CAS
Article
PubMed
PubMed Central
Google Scholar
Rosenblatt J, Raff MC, Cramer LP (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11(23):1847–1857
CAS
Article
Google Scholar
Schutte B, Henfling M, Kolgen W, Bouman M, Meex S, Leers MP, Nap M, Bjorklund V, Bjorklund P, Bjorklund B, Lane EB, Omary MB, Jornvall H, Ramaekers FC (2004) Keratin 8/18 breakdown and reorganization during apoptosis. Exp Cell Res 297(1):11–26. https://doi.org/10.1016/j.yexcr.2004.02.019
CAS
Article
PubMed
Google Scholar
Byun Y, Chen F, Chang R, Trivedi M, Green KJ, Cryns VL (2001) Caspase cleavage of vimentin disrupts intermediate filaments and promotes apoptosis. Cell Death Differ 8(5):443–450. https://doi.org/10.1038/sj.cdd.4400840
CAS
Article
PubMed
Google Scholar
Rao L, Perez D, White E (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135(6 Pt 1):1441–1455
CAS
Article
Google Scholar
Seo MY, Rhee K (2018) Caspase-mediated cleavage of the centrosomal proteins during apoptosis. Cell Death Dis 9(5):571. https://doi.org/10.1038/s41419-018-0632-8
CAS
Article
PubMed
PubMed Central
Google Scholar
Sanchez-Alcazar JA, Rodriguez-Hernandez A, Cordero MD, Fernandez-Ayala DJ, Brea-Calvo G, Garcia K, Navas P (2007) The apoptotic microtubule network preserves plasma membrane integrity during the execution phase of apoptosis. Apoptosis 12(7):1195–1208. https://doi.org/10.1007/s10495-006-0044-6
Article
PubMed
Google Scholar
Oropesa-Avila M, Fernandez-Vega A, de la Mata M, Maraver JG, Cordero MD, Cotan D, de Miguel M, Calero CP, Paz MV, Pavon AD, Sanchez MA, Zaderenko AP, Ybot-Gonzalez P, Sanchez-Alcazar JA (2013) Apoptotic microtubules delimit an active caspase free area in the cellular cortex during the execution phase of apoptosis. Cell Death Dis 4:e527. https://doi.org/10.1038/cddis.2013.58
CAS
Article
PubMed
PubMed Central
Google Scholar
Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3(4):339–345. https://doi.org/10.1038/35070009
CAS
Article
PubMed
Google Scholar
Croft DR, Coleman ML, Li S, Robertson D, Sullivan T, Stewart CL, Olson MF (2005) Actin-myosin-based contraction is responsible for apoptotic nuclear disintegration. J Cell Biol 168(2):245–255. https://doi.org/10.1083/jcb.200409049
CAS
Article
PubMed
PubMed Central
Google Scholar
Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, Nomenclature Committee on Cell Death (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16(1):3–11. https://doi.org/10.1038/cdd.2008.150
CAS
Article
PubMed
Google Scholar
Gagliardi PA, Somale D, Puliafito A, Chiaverina G, di Blasio L, Oneto M, Bianchini P, Bussolino F, Primo L (2018) MRCKalpha is activated by caspase cleavage to assemble an apical actin ring for epithelial cell extrusion. J Cell Biol 217(1):231–249. https://doi.org/10.1083/jcb.201703044
CAS
Article
PubMed
PubMed Central
Google Scholar
Sebbagh M, Renvoize C, Hamelin J, Riche N, Bertoglio J, Breard J (2001) Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol 3(4):346–352. https://doi.org/10.1038/35070019
CAS
Article
PubMed
Google Scholar
Gagliardi PA, Primo L (2019) Irreversible activation of Rho-activated kinases resulted from evolution of proteolytic sites within disordered regions in coiled-coil domain. Mol Biol Evol 36(2):376–392. https://doi.org/10.1093/molbev/msy229
Article
PubMed
Google Scholar
Iwasaki T, Katayama T, Kohama K, Endo Y, Sawasaki T (2013) Myosin phosphatase is inactivated by caspase-3 cleavage and phosphorylation of myosin phosphatase targeting subunit 1 during apoptosis. Mol Biol Cell 24(6):748–756. https://doi.org/10.1091/mbc.E11-08-0740
CAS
Article
PubMed
PubMed Central
Google Scholar
Nakazono-Kusaba A, Takahashi-Yanaga F, Morimoto S, Furue M, Sasaguri T (2002) Staurosporine-induced cleavage of alpha-smooth muscle actin during myofibroblast apoptosis. J Investig Dermatol 119(5):1008–1013. https://doi.org/10.1046/j.1523-1747.2002.19525.x
CAS
Article
PubMed
Google Scholar
Brown SB, Bailey K, Savill J (1997) Actin is cleaved during constitutive apoptosis. Biochem J 323(Pt 1):233–237
CAS
Article
Google Scholar
Song Q, Wei T, Lees-Miller S, Alnemri E, Watters D, Lavin MF (1997) Resistance of actin to cleavage during apoptosis. Proc Natl Acad Sci USA 94(1):157–162
CAS
Article
Google Scholar
McKinley KL, Stuurman N, Royer LA, Schartner C, Castillo-Azofeifa D, Delling M, Klein OD, Vale RD (2018) Cellular aspect ratio and cell division mechanics underlie the patterning of cell progeny in diverse mammalian epithelia. eLife 7:e36739. https://doi.org/10.7554/elife.36739
Article
PubMed
PubMed Central
Google Scholar
Le Bras S, Le Borgne R (2014) Epithelial cell division—multiplying without losing touch. J Cell Sci 127(Pt 24):5127–5137. https://doi.org/10.1242/jcs.151472
CAS
Article
PubMed
Google Scholar
Torres AY, Malartre M, Pret AM, Agnes F (2017) JAK/STAT signaling is necessary for cell monosis prior to epithelial cell apoptotic extrusion. Cell Death Dis 8(5):e2814. https://doi.org/10.1038/cddis.2017.166
CAS
Article
PubMed
PubMed Central
Google Scholar
Katoh H, Fujita Y (2012) Epithelial homeostasis: elimination by live cell extrusion. Curr Biol 22(11):R453–R455. https://doi.org/10.1016/j.cub.2012.04.036
CAS
Article
PubMed
Google Scholar
Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, Morcos PA, Rosenblatt J (2012) Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 484(7395):546–549. https://doi.org/10.1038/nature10999
CAS
Article
PubMed
PubMed Central
Google Scholar
Kocgozlu L, Saw TB, Le AP, Yow I, Shagirov M, Wong E, Mege RM, Lim CT, Toyama Y, Ladoux B (2016) Epithelial cell packing induces distinct modes of cell extrusions. Curr Biol 26(21):2942–2950. https://doi.org/10.1016/j.cub.2016.08.057
CAS
Article
PubMed
PubMed Central
Google Scholar
Saw TB, Doostmohammadi A, Nier V, Kocgozlu L, Thampi S, Toyama Y, Marcq P, Lim CT, Yeomans JM, Ladoux B (2017) Topological defects in epithelia govern cell death and extrusion. Nature 544(7649):212–216. https://doi.org/10.1038/nature21718
CAS
Article
PubMed
PubMed Central
Google Scholar
Slattum G, Gu Y, Sabbadini R, Rosenblatt J (2014) Autophagy in oncogenic K-Ras promotes basal extrusion of epithelial cells by degrading S1P. Curr Biol 24(1):19–28. https://doi.org/10.1016/j.cub.2013.11.029
CAS
Article
PubMed
Google Scholar
Wu SK, Lagendijk AK, Hogan BM, Gomez GA, Yap AS (2015) Active contractility at E-cadherin junctions and its implications for cell extrusion in cancer. Cell Cycle 14(3):315–322. https://doi.org/10.4161/15384101.2014.989127
CAS
Article
PubMed
PubMed Central
Google Scholar
Kuipers D, Mehonic A, Kajita M, Peter L, Fujita Y, Duke T, Charras G, Gale JE (2014) Epithelial repair is a two-stage process driven first by dying cells and then by their neighbors. J Cell Sci 127(Pt 6):1229–1241. https://doi.org/10.1242/jcs.138289
CAS
Article
PubMed
Google Scholar
Lubkov V, Bar-Sagi D (2014) E-cadherin-mediated cell coupling is required for apoptotic cell extrusion. Curr Biol 24(8):868–874. https://doi.org/10.1016/j.cub.2014.02.057
CAS
Article
PubMed
Google Scholar
Michael M, Meiring JCM, Acharya BR, Matthews DR, Verma S, Han SP, Hill MM, Parton RG, Gomez GA, Yap AS (2016) Coronin 1B reorganizes the architecture of F-actin networks for contractility at steady-state and apoptotic adherens junctions. Dev Cell 37(1):58–71. https://doi.org/10.1016/j.devcel.2016.03.008
CAS
Article
PubMed
Google Scholar
Andrade D, Rosenblatt J (2011) Apoptotic regulation of epithelial cellular extrusion. Apoptosis 16(5):491–501. https://doi.org/10.1007/s10495-011-0587-z
CAS
Article
PubMed
PubMed Central
Google Scholar
Petrache I, Birukov K, Zaiman AL, Crow MT, Deng H, Wadgaonkar R, Romer LH, Garcia JG (2003) Caspase-dependent cleavage of myosin light chain kinase (MLCK) is involved in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis. FASEB J 17(3):407–416. https://doi.org/10.1096/fj.02-0672com
CAS
Article
PubMed
Google Scholar
Gu Y, Forostyan T, Sabbadini R, Rosenblatt J (2011) Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway. J Cell Biol 193(4):667–676. https://doi.org/10.1083/jcb.201010075
CAS
Article
PubMed
PubMed Central
Google Scholar
Marshall TW, Lloyd IE, Delalande JM, Nathke I, Rosenblatt J (2011) The tumor suppressor adenomatous polyposis coli controls the direction in which a cell extrudes from an epithelium. Mol Biol Cell 22(21):3962–3970. https://doi.org/10.1091/mbc.E11-05-0469
CAS
Article
PubMed
PubMed Central
Google Scholar
Maceyka M, Harikumar KB, Milstien S, Spiegel S (2012) Sphingosine-1-phosphate signaling and its role in disease. Trends Cell Biol 22(1):50–60. https://doi.org/10.1016/j.tcb.2011.09.003
CAS
Article
PubMed
Google Scholar
Slattum G, McGee KM, Rosenblatt J (2009) P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 186(5):693–702. https://doi.org/10.1083/jcb.200903079
CAS
Article
PubMed
PubMed Central
Google Scholar
Moreno E, Valon L, Levillayer F, Levayer R (2019) Competition for space induces cell elimination through compaction-driven ERK downregulation. Curr Biol 29(1):23–34 e28. https://doi.org/10.1016/j.cub.2018.11.007
CAS
Article
PubMed
PubMed Central
Google Scholar
Kiesslich R, Goetz M, Angus EM, Hu Q, Guan Y, Potten C, Allen T, Neurath MF, Shroyer NF, Montrose MH, Watson AJ (2007) Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology 133(6):1769–1778. https://doi.org/10.1053/j.gastro.2007.09.011
Article
PubMed
Google Scholar
Sternlicht MD (2006) Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res 8(1):201. https://doi.org/10.1186/bcr1368
CAS
Article
PubMed
Google Scholar
Brill A, Torchinsky A, Carp H, Toder V (1999) The role of apoptosis in normal and abnormal embryonic development. J Assist Reprod Genet 16(10):512–519
CAS
Article
Google Scholar
Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS (2008) Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321(5896):1683–1686. https://doi.org/10.1126/science.1157052
CAS
Article
PubMed
PubMed Central
Google Scholar
Monier B, Gettings M, Gay G, Mangeat T, Schott S, Guarner A, Suzanne M (2015) Apico-basal forces exerted by apoptotic cells drive epithelium folding. Nature 518(7538):245–248. https://doi.org/10.1038/nature14152
CAS
Article
PubMed
Google Scholar
Pearl EJ, Li J, Green JB (2017) Cellular systems for epithelial invagination. Philos Trans R Soc Lond Ser B Biol Sci. https://doi.org/10.1098/rstb.2015.0526
Article
Google Scholar