1,145
Views
12
CrossRef citations to date
0
Altmetric
Review

In life there is death: How epithelial tissue barriers are preserved despite the challenge of apoptosis

, , , &
Article: e1345353 | Received 03 May 2017, Accepted 19 Jun 2017, Published online: 07 Jul 2017

References

  • Shawki A, McCole DF. Mechanisms of intestinal epithelial barrier dysfunction by Adherent-Invasive Escherichia coli. Cell Mol Gastroenterol Hepatol 2017; 3(1):41-50; PMID:28174756; https://doi.org/10.1016/j.jcmgh.2016.10.004
  • Georas SN, Rezaee F. Epithelial barrier function: At the front line of asthma immunology and allergic airway inflammation. J Allergy Clin Immunol 2014; 134(3):509-20; PMID:25085341; https://doi.org/10.1016/j.jaci.2014.05.049
  • Catalioto RM, Maggi CA, Giuliani S. Intestinal epithelial barrier dysfunction in disease and possible therapeutical interventions. Curr Med Chem 2011; 18(3):398-426; PMID:21143118
  • Blander JM. A long-awaited merger of the pathways mediating host defence and programmed cell death. Nat Rev Immunol 2014; 14(9):601-18; PMID:25145756; https://doi.org/10.1038/nri3720
  • Yang Y, Jiang G, Zhang P, Fan J. Programmed cell death and its role in inflammation. Mil Med Res 2015; 2:12; PMID:26045969; https://doi.org/10.1186/s40779-015-0039-0
  • Elmore S. Apoptosis: A review of programmed cell death. Toxicol Pathol 2007; 35(4):495-516; PMID:17562483; https://doi.org/10.1080/01926230701320337
  • Atkin-Smith GK, Poon IK. Disassembly of the dying: Mechanisms and functions. Trends Cell Biol 2017; 27(2):151-62; PMID:27647018; https://doi.org/10.1016/j.tcb.2016.08.011
  • Grieve AG, Rabouille C. Extracellular cleavage of E-cadherin promotes epithelial cell extrusion. J Cell Sci 2014; 127(Pt 15):3331-46; PMID:24895403; https://doi.org/10.1242/jcs.147926
  • Rosenblatt J, Raff MC, Cramer LP. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 2001; 11(23):1847-57; PMID:11728307
  • Kerr JF, Wyllie AH, Currie AR. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26(4):239-57; PMID:4561027
  • Fulda S, Debatin KM. Extrinsic versus intrinsic apoptosis pathways in anticancer chemotherapy. Oncogene 2006; 25(34):4798-811; PMID:16892092; https://doi.org/10.1038/sj.onc.1209608
  • Russell JH, Ley TJ. Lymphocyte-mediated cytotoxicity. Annu Rev Immunol 2002; 20:323-70; PMID:11861606; https://doi.org/10.1146/annurev.immunol.20.100201.131730
  • Keefe D, Shi L, Feske S, Massol R, Navarro F, Kirchhausen T, Lieberman J. Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity 2005; 23(3):249-62; PMID:16169498; https://doi.org/10.1016/j.immuni.2005.08.001
  • Veugelers K, Motyka B, Frantz C, Shostak I, Sawchuk T, Bleackley RC. The granzyme B-serglycin complex from cytotoxic granules requires dynamin for endocytosis. Blood 2004; 103(10):3845-53; PMID:14739229; https://doi.org/10.1182/blood-2003-06-2156
  • Hacker DL, Fowler BC. Complementation of the host range restriction of southern cowpea mosaic virus in bean by southern bean mosaic virus. Virology 2000; 266(1):140-9; PMID:10612668; https://doi.org/10.1006/viro.1999.0072
  • Lane JD, Lucocq J, Pryde J, Barr FA, Woodman PG, Allan VJ, Lowe M. Caspase-mediated cleavage of the stacking protein GRASP65 is required for Golgi fragmentation during apoptosis. J Cell Biol 2002; 156(3):495-509; PMID:11815631; https://doi.org/10.1083/jcb.200110007
  • Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F, Smith CL, Youle RJ. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001; 1(4):515-25; PMID:11703942
  • Mills JC, Stone NL, Erhardt J, Pittman RN. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol 1998; 140(3):627-36; PMID:9456322
  • Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF. Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 2001; 3(4):339-45; PMID:11283606; https://doi.org/10.1038/35070009
  • Sebbagh M, Renvoize C, Hamelin J, Riche N, Bertoglio J, Breard J. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol 2001; 3(4):346-52; PMID:11283607; https://doi.org/10.1038/35070019
  • Tomiyoshi G, Horita Y, Nishita M, Ohashi K, Mizuno K. Caspase-mediated cleavage and activation of LIM-kinase 1 and its role in apoptotic membrane blebbing. Genes Cells 2004; 9(6):591-600; PMID:15189451; https://doi.org/10.1111/j.1356-9597.2004.00745.x
  • Arber S, Barbayannis FA, Hanser H, Schneider C, Stanyon CA, Bernard O, Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998; 393(6687):805-9; PMID:9655397; https://doi.org/10.1038/31729
  • Charras GT, Yarrow JC, Horton MA, Mahadevan L, Mitchison TJ. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 2005; 435(7040):365-9; PMID:15902261; https://doi.org/10.1038/nature03550
  • Moss DK, Betin VM, Malesinski SD, Lane JD. A novel role for microtubules in apoptotic chromatin dynamics and cellular fragmentation. J Cell Sci 2006; 119(Pt 11):2362-74; PMID:16723742; https://doi.org/10.1242/jcs.02959
  • Atkin-Smith GK, Tixeira R, Paone S, Mathivanan S, Collins C, Liem M, Goodall KJ, Ravichandran KS, Hulett MD, Poon IK. A novel mechanism of generating extracellular vesicles during apoptosis via a beads-on-a-string membrane structure. Nat Commun 2015; 6:7439; PMID:26074490; https://doi.org/10.1038/ncomms8439
  • Anderson JM, Van Itallie CM. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 2009; 1(2):a002584. https://doi.org/10.1101/cshperspect.a002584. PMID: 20066090
  • Silva MT. Secondary necrosis: The natural outcome of the complete apoptotic program. FEBS Lett 2010; 584(22):4491-9; PMID:20974143; https://doi.org/10.1016/j.febslet.2010.10.046
  • Kanuri G, Spruss A, Wagnerberger S, Bischoff SC, Bergheim I. Role of tumor necrosis factor alpha (TNFalpha) in the onset of fructose-induced nonalcoholic fatty liver disease in mice. J Nutr Biochem 2011; 22(6):527-34; PMID:20801629; https://doi.org/10.1016/j.jnutbio.2010.04.007
  • Kumagai Y, Takeuchi O, Akira S. TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliv Rev 2008; 60(7):795-804; PMID:18262306; https://doi.org/10.1016/j.addr.2007.12.004
  • Hornung V, Barchet W, Schlee M, Hartmann G. RNA recognition via TLR7 and TLR8. Handb Exp Pharmacol 2008; 183:71-86; PMID:18071655; https://doi.org/10.1007/978-3-540-72167-3_4
  • Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J, Borkowski AW, Martinez L, Greidinger EL, Yu BD, Gallo RL. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat Med 2012; 18(8):1286-90; PMID:22772463; https://doi.org/10.1038/nm.2861
  • Marshak-Rothstein A. Toll-like receptors in systemic autoimmune disease. Nat Rev Immunol 2006; 6(11):823-35; PMID:17063184; https://doi.org/10.1038/nri1957
  • Silva MT, Correia-Neves M. Neutrophils and macrophages: The main partners of phagocyte cell systems. Front Immunol 2012; 3:174; PMID:22783254; https://doi.org/10.3389/fimmu.2012.00174
  • Rabinovitch M. Professional and non-professional phagocytes: An introduction. Trends Cell Biol 1995; 5(3):85-7; PMID:14732160
  • Monks J, Rosner D, Geske FJ, Lehman L, Hanson L, Neville MC, Fadok VA. Epithelial cells as phagocytes: Apoptotic epithelial cells are engulfed by mammary alveolar epithelial cells and repress inflammatory mediator release. Cell Death Differ 2005; 12(2):107-14; PMID:15647754; https://doi.org/10.1038/sj.cdd.4401517
  • Juncadella IJ, Kadl A, Sharma AK, Shim YM, Hochreiter-Hufford A, Borish L, Ravichandran KS. Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 2013; 493(7433):547-51; PMID:23235830; https://doi.org/10.1038/nature11714
  • Cao WM, Murao K, Imachi H, Hiramine C, Abe H, Yu X, Dobashi H, Wong NC, Takahara J, Ishida T. Phosphatidylserine receptor cooperates with high-density lipoprotein receptor in recognition of apoptotic cells by thymic nurse cells. J Mol Endocrinol 2004; 32(2):497-505; PMID:15072554
  • Monks J, Smith-Steinhart C, Kruk ER, Fadok VA, Henson PM. Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol Reprod 2008; 78(4):586-94; PMID:18057312; https://doi.org/10.1095/biolreprod.107.065045
  • Couzinet S, Cejas E, Schittny J, Deplazes P, Weber R, Zimmerli S. Phagocytic uptake of Encephalitozoon cuniculi by nonprofessional phagocytes. Infect Immun 2000; 68(12):6939-45; PMID:11083817
  • Lauber K, Bohn E, Krober SM, Xiao YJ, Blumenthal SG, Lindemann RK, Marini P, Wiedig C, Zobywalski A, Baksh S, et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 2003; 113(6):717-30; PMID:12809603
  • Peter C, Waibel M, Radu CG, Yang LV, Witte ON, Schulze-Osthoff K, Wesselborg S, Lauber K. Migration to apoptotic “find-me” signals is mediated via the phagocyte receptor G2A. J Biol Chem 2008; 283(9):5296-305; PMID:18089568; https://doi.org/10.1074/jbc.M706586200
  • Gude DR, Alvarez SE, Paugh SW, Mitra P, Yu J, Griffiths R, Barbour SE, Milstien S, Spiegel S. Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a “come-and-get-me” signal. FASEB J 2008; 22(8):2629-38; PMID:18362204; https://doi.org/10.1096/fj.08-107169
  • Rosen H, Goetzl EJ. Sphingosine 1-phosphate and its receptors: An autocrine and paracrine network. Nat Rev Immunol 2005; 5(7):560-70; PMID:15999095; https://doi.org/10.1038/nri1650
  • Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER, Armstrong AJ, Penuela S, Laird DW, Salvesen GS, et al. Pannexin 1 channels mediate ‘find-me’ signal release and membrane permeability during apoptosis. Nature 2010; 467(7317):863-7; PMID:20944749; https://doi.org/10.1038/nature09413
  • Ravichandran KS. Find-me and eat-me signals in apoptotic cell clearance: Progress and conundrums. J Exp Med 2010; 207(9):1807-17; PMID:20805564; https://doi.org/10.1084/jem.20101157
  • Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461(7261):282-6; PMID:19741708; https://doi.org/10.1038/nature08296
  • Li W. Eat-me signals: Keys to molecular phagocyte biology and “appetite” control. J Cell Physiol 2012; 227(4):1291-7; PMID:21520079; https://doi.org/10.1002/jcp.22815
  • Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992; 148(7):2207-16; PMID:1545126
  • Martin SJ, Reutelingsperger CP, McGahon AJ, Rader JA, van Schie RC, LaFace DM, Green DR. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995; 182(5):1545-56; PMID:7595224
  • Balasubramanian K, Schroit AJ. Aminophospholipid asymmetry: A matter of life and death. Annu Rev Physiol 2003; 65:701-34; PMID:12471163.; https://doi.org/10.1146/annurev.physiol.65.092101.142459
  • Borisenko GG, Matsura T, Liu SX, Tyurin VA, Jianfei J, Serinkan FB, Kagan VE. Macrophage recognition of externalized phosphatidylserine and phagocytosis of apoptotic Jurkat cells–existence of a threshold. Arch Biochem Biophys 2003; 413(1):41-52; PMID:12706340
  • Bratton DL, Henson PM. Apoptotic cell recognition: will the real phosphatidylserine receptor(s) please stand up? Curr Biol 2008; 18(2):R76-9; PMID:18211846; https://doi.org/10.1016/j.cub.2007.11.024
  • Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002; 417(6885):182-7; PMID:12000961; https://doi.org/10.1038/417182a
  • Nagata S, Hanayama R, Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010; 140(5):619-30; PMID:20211132; https://doi.org/10.1016/j.cell.2010.02.014
  • Nakano T, Ishimoto Y, Kishino J, Umeda M, Inoue K, Nagata K, Ohashi K, Mizuno K, Arita H. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J Biol Chem 1997; 272(47):29411-4; PMID:9367994
  • Brown S, Heinisch I, Ross E, Shaw K, Buckley CD, Savill J. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature 2002; 418(6894):200-3; PMID:12110892; https://doi.org/10.1038/nature00811
  • Gardai SJ, McPhillips KA, Frasch SC, Janssen WJ, Starefeldt A, Murphy-Ullrich JE, Bratton DL, Oldenborg PA, Michalak M, Henson PM. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005; 123(2):321-34; PMID:16239148; https://doi.org/10.1016/j.cell.2005.08.032
  • Kinchen JM. A model to die for: Signaling to apoptotic cell removal in worm, fly and mouse. Apoptosis 2010; 15(9):998-1006; PMID:20461556; https://doi.org/10.1007/s10495-010-0509-5
  • Kinchen JM, Ravichandran KS. Phagosome maturation: Going through the acid test. Nat Rev Mol Cell Biol 2008; 9(10):781-95; PMID:18813294; https://doi.org/10.1038/nrm2515
  • Elliott MR, Ravichandran KS. Clearance of apoptotic cells: Implications in health and disease. J Cell Biol 2010; 189(7):1059-70; PMID:20584912; https://doi.org/10.1083/jcb.201004096
  • Henson PM. Dampening inflammation. Nat Immunol 2005; 6(12):1179-81; PMID:16369556; https://doi.org/10.1038/ni1205-1179
  • Hogan C, Dupre-Crochet S, Norman M, Kajita M, Zimmermann C, Pelling AE, Piddini E, Baena-Lopez LA, Vincent JP, Itoh Y, et al. Characterization of the interface between normal and transformed epithelial cells. Nat Cell Biol 2009; 11(4):460-7; PMID:19287376; https://doi.org/10.1038/ncb1853
  • Wu SK, Lagendijk AK, Hogan BM, Gomez GA, Yap AS. Active contractility at E-cadherin junctions and its implications for cell extrusion in cancer. Cell Cycle 2015; 14(3):315-22; PMID:25590779; https://doi.org/10.4161/15384101.2014.989127
  • Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien CB, Morcos PA, Rosenblatt J. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature 2012; 484(7395):546-9; PMID:22504183; https://doi.org/10.1038/nature10999
  • Marinari E, Mehonic A, Curran S, Gale J, Duke T, Baum B. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 2012; 484(7395):542-5; PMID:22504180; https://doi.org/10.1038/nature10984
  • Michael M, Meiring JC, Acharya BR, Matthews DR, Verma S, Han SP, Hill MM, Parton RG, Gomez GA, Yap AS. Coronin 1B reorganizes the architecture of F-actin networks for contractility at steady-state and apoptotic adherens junctions. Dev Cell 2016; 37(1):58-71; PMID:27046832; https://doi.org/10.1016/j.devcel.2016.03.008
  • Marshall TW, Lloyd IE, Delalande JM, Nathke I, Rosenblatt J. The tumor suppressor adenomatous polyposis coli controls the direction in which a cell extrudes from an epithelium. Mol Biol Cell 2011; 22(21):3962-70; PMID:21900494; https://doi.org/10.1091/mbc.E11-05-0469
  • Kuipers D, Mehonic A, Kajita M, Peter L, Fujita Y, Duke T, Charras G, Gale JE. Epithelial repair is a two-stage process driven first by dying cells and then by their neighbours. J Cell Sci 2014; 127(Pt 6):1229-41; PMID:24463819; https://doi.org/10.1242/jcs.138289
  • Lubkov V, Bar-Sagi D. E-cadherin-mediated cell coupling is required for apoptotic cell extrusion. Curr Biol 2014; 24(8):868-74; PMID:24704076; https://doi.org/10.1016/j.cub.2014.02.057
  • Kocgozlu L, Saw TB, Le AP, Yow I, Shagirov M, Wong E, Mege RM, Lim CT, Toyama Y, Ladoux B. Epithelial cell packing induces distinct modes of cell extrusions. Curr Biol 2016; 26(21):2942-50; PMID:27746027; https://doi.org/10.1016/j.cub.2016.08.057
  • Lecuit T, Yap AS. E-cadherin junctions as active mechanical integrators in tissue dynamics. Nat Cell Biol 2015; 17(5):533-9; PMID:25925582; https://doi.org/10.1038/ncb3136
  • Ratheesh A, Gomez GA, Priya R, Verma S, Kovacs EM, Jiang K, Brown NH, Akhmanova A, Stehbens SJ, Yap AS. Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 2012; 14(8):818-28; PMID:22750944; https://doi.org/10.1038/ncb2532
  • Smutny M, Cox HL, Leerberg JM, Kovacs EM, Conti MA, Ferguson C, Hamilton NA, Parton RG, Adelstein RS, Yap AS. Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat Cell Biol 2010; 12(7):696-702; PMID:20543839; https://doi.org/10.1038/ncb2072
  • Ratheesh A, Yap AS. A bigger picture: Classical cadherins and the dynamic actin cytoskeleton. Nat Rev Mol Cell Biol 2012; 13(10):673-9; PMID:22931853; https://doi.org/10.1038/nrm3431
  • Leerberg JM, Gomez GA, Verma S, Moussa EJ, Wu SK, Priya R, Hoffman BD, Grashoff C, Schwartz MA, Yap AS. Tension-sensitive actin assembly supports contractility at the epithelial zonula adherens. Curr Biol 2014; 24(15):1689-99; PMID:25065757; https://doi.org/10.1016/j.cub.2014.06.028
  • Acharya BR, Wu SK, Lieu ZZ, Parton RG, Grill SW, Bershadsky AD, Gomez GA, Yap AS. Mammalian diaphanous 1 mediates a pathway for E-cadherin to stabilize epithelial barriers through junctional contractility. Cell Rep 2017; 18(12):2854-67. https://doi.org/10.1016/j.celrep.2017.02.078. PMID: 28329679
  • Amano M, Nakayama M, Kaibuchi K. Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 2010; 67(9):545-54; PMID:20803696; https://doi.org/10.1002/cm.20472
  • Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420(6916):629-35; PMID:12478284; https://doi.org/10.1038/nature01148
  • Slattum G, McGee KM, Rosenblatt J. P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 2009; 186(5):693-702; PMID:19720875; https://doi.org/10.1083/jcb.200903079
  • Weigert A, Cremer S, Schmidt MV, von Knethen A, Angioni C, Geisslinger G, Brune B. Cleavage of sphingosine kinase 2 by caspase-1 provokes its release from apoptotic cells. Blood 2010; 115(17):3531-40; PMID:20197547; https://doi.org/10.1182/blood-2009-10-243444
  • Strub GM, Maceyka M, Hait NC, Milstien S, Spiegel S. Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol 2010; 688:141-55; PMID:20919652
  • Ancellin N, Colmont C, Su J, Li Q, Mittereder N, Chae SS, Stefansson S, Liau G, Hla T. Extracellular export of sphingosine kinase-1 enzyme. Sphingosine 1-phosphate generation and the induction of angiogenic vascular maturation. J Biol Chem 2002; 277(8):6667-75; PMID:11741921; https://doi.org/10.1074/jbc.M102841200
  • Kihara Y, Maceyka M, Spiegel S, Chun J. Lysophospholipid receptor nomenclature review: IUPHAR Review 8. Br J Pharmacol 2014; 171(15):3575-94; PMID:24602016; https://doi.org/10.1111/bph.12678
  • Gu Y, Forostyan T, Sabbadini R, Rosenblatt J. Epithelial cell extrusion requires the sphingosine-1-phosphate receptor 2 pathway. J Cell Biol 2011; 193(4):667-76; PMID:21555463; https://doi.org/10.1083/jcb.201010075
  • Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. Alpha-catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 2010; 12(6):533-42; PMID:20453849; https://doi.org/10.1038/ncb2055
  • Yao M, Qiu W, Liu R, Efremov AK, Cong P, Seddiki R, Payre M, Lim CT, Ladoux B, Mege RM, et al. Force-dependent conformational switch of alpha-catenin controls vinculin binding. Nat Commun 2014; 5:4525; PMID:25077739; https://doi.org/10.1038/ncomms5525
  • Buckley CD, Tan J, Anderson KL, Hanein D, Volkmann N, Weis WI, Nelson WJ, Dunn AR. Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force. Science 2014; 346(6209):1254211; PMID:25359979; https://doi.org/10.1126/science.1254211
  • De La Cruz EM, Ostap EM. Relating biochemistry and function in the myosin superfamily. Curr Opin Cell Biol 2004; 16(1):61-7; PMID:15037306; https://doi.org/10.1016/j.ceb.2003.11.011
  • Shao X, Li Q, Mogilner A, Bershadsky AD, Shivashankar GV. Mechanical stimulation induces formin-dependent assembly of a perinuclear actin rim. Proc Natl Acad Sci U S A 2015; 112(20):E2595-601; PMID:25941386; https://doi.org/10.1073/pnas.1504837112
  • Saw TB, Doostmohammadi A, Nier V, Kocgozlu L, Thampi S, Toyama Y, Marcq P, Lim CT, Yeomans JM, Ladoux B. Topological defects in epithelia govern cell death and extrusion. Nature 2017; 544(7649):212-6; PMID:28406198; https://doi.org/10.1038/nature21718

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.