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EXTRA VIEW

Active contractility at E-cadherin junctions and its implications for cell extrusion in cancer

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Pages 315-322 | Received 14 Oct 2014, Accepted 14 Nov 2014, Published online: 06 Feb 2015

References

  • Wu SK, Gomez GA, Michael M, Verma S, Cox HL, Lefevre JG, Parton RG, Hamilton NA, Neufeld Z, Yap AS. Cortical F-actin stabilization generates apical-lateral patterns of junctional contractility that integrate cells into epithelia. Nat Cell Biol 2014; 16:167-78; PMID:4413434
  • Wu SK, Yap AS. Patterns in space: coordinating adhesion and actomyosin contractility at E-cadherin junctions. Cell Commun Adhes 2013; 20:201-12; PMID:24205985; http://dx.doi.org/10.3109/15419061.2013.856889
  • Engl W, Arasi B, Yap LL, Thiery JP, Viasnoff V. Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions. Nat Cell Biol 2014; 16:587-94; PMID:24859003; http://dx.doi.org/10.1038/ncb2973
  • Roh-Johnson M, Shemer G, Higgins CD, McClellan JH, Werts AD, Tulu US, Gao L, Betzig E, Kiehart DP, Goldstein B. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 2012; 335:1232-5; PMID:22323741; http://dx.doi.org/10.1126/science.1217869
  • Fernandez-Gonzalez R, Simoes Sde M, Roper JC, Eaton S, Zallen JA. Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 2009; 17:736-43; PMID:19879198; http://dx.doi.org/10.1016/j.devcel.2009.09.003
  • Martin AC, Gelbart M, Fernandez-Gonzalez R, Kaschube M, Wieschaus EF. Integration of contractile forces during tissue invagination. J Cell Biol 2010; 188:735-49; PMID:20194639; http://dx.doi.org/10.1083/jcb.200910099
  • Maitre JL, Berthoumieux H, Krens SF, Salbreux G, Julicher F, Paluch E, Heisenberg CP. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 2012; 338:253-6; PMID:22923438; http://dx.doi.org/10.1126/science.1225399
  • de Rooij J. Cadherin adhesion controlled by cortical actin dynamics. Nat Cell Biol 2014; 16:508-10; PMID:24875740
  • Rauzi M, Verant P, Lecuit T, Lenne PF. Nature and anisotropy of cortical forces orienting drosophila tissue morphogenesis. Nat Cell Biol 2008; PMID:18978783; http://dx.doi.org/10.1038/ncb1798
  • Smutny M, Wu SK, Gomez GA, Mangold S, Yap AS, Hamilton NA. Multicomponent analysis of junctional movements regulated by myosin II isoforms at the epithelial zonula adherens. PloS one 2011; 6:e22458; PMID:21799860; http://dx.doi.org/10.1371/journal.pone.0022458
  • Lugo-Martinez VH, Petit CS, Fouquet S, Le Beyec J, Chambaz J, Pincon-Raymond M, Cardot P, Thenet S. Epidermal growth factor receptor is involved in enterocyte anoikis through the dismantling of E-cadherin-mediated junctions. Am J Physiol Gastrointest Liver Physiol 2009; 296:G235-44; PMID:19056766; http://dx.doi.org/10.1152/ajpgi.90313.2008
  • Meng W, Mushika Y, Ichii T, Takeichi M. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 2008; 135:948-59; PMID:19041755; http://dx.doi.org/10.1016/j.cell.2008.09.040
  • Priya R, Yap AS, Gomez GA. E-cadherin supports steady-state rho signaling at the epithelial zonula adherens. Differentiation 2013; 86:117-8; PMID:23643492; http://dx.doi.org/10.1016/j.diff.2013.01.002
  • Truong Quang BA, Mani M, Markova O, Lecuit T, Lenne PF. Principles of E-Cadherin supramolecular organization in vivo. Curr Biol 2013; 23:2197-207; PMID:24184100; http://dx.doi.org/10.1016/j.cub.2013.09.015
  • Vaezi A, Bauer C, Vasioukhin V, Fuchs E. Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Developmental cell 2002; 3:367-81; PMID:12361600
  • Wu SK, Budnar S, Yap AS, Gomez GA. Pulsatile contractility of actomyosin networks organizes the cellular cortex at lateral cadherin junctions. Eur J Cell Biol 2014; 93:396-404; PMID:25269995; http://dx.doi.org/10.1016/j.ejcb.2014.09.001
  • Mangold S, Wu SK, Norwood SJ, Collins BM, Hamilton NA, Thorn P, Yap AS. Hepatocyte growth factor acutely perturbs actin filament anchorage at the epithelial zonula adherens. Curr Biol 2011; 21:503-7; PMID:21396819; http://dx.doi.org/10.1016/j.cub.2011.02.018
  • Otani T, Ichii T, Aono S, Takeichi M. Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J Cell Biol 2006; 175:135-46; PMID:17015620
  • Tang VW, Brieher WM. Alpha-Actinin-4/FSGS1 is required for Arp2/3-dependent actin assembly at the adherens junction. J Cell Biol 2012; 196:115-30; PMID:2232703
  • Kovacs EM, Goodwin M, Ali RG, Paterson AD, Yap AS. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 2002; 12:379-82; PMID:11882288
  • 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; 24:1689-99; PMID:25065757; http://dx.doi.org/10.1016/j.cub.2014.06.028
  • Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, Yap AS. Myosin 2 is a key rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 2005; 16:4531-42; PMID:16030252
  • Yonemura S, Hirao-Minakuchi K, Nishimura Y. Rho localization in cells and tissues. Exp Cell Res 2004; 295:300-14; PMID:15093731
  • 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; 12:696-702; PMID:20543839; http://dx.doi.org/10.1038/ncb2072
  • Ratheesh A, Gomez GA, Priya R, Verma S, Kovacs EM, Jiang K, Brown NH, Akhmanova A, Stehbens SJ, Yap AS. Centralspindlin and α-catenin regulate rho signalling at the epithelial zonula adherens. Nat Cell Biol 2012; 14:818-28; PMID:22750944; http://dx.doi.org/10.1038/ncb2532
  • (a) Verma S, Han SP, Michael M, Gomez GA, Yang Z, Teasdale RD, Ratheesh A, Kovacs EM, Ali RG, Yap AS. A WAVE2-Arp2/3 actin nucleator apparatus supports junctional tension at the epithelial zonula adherens. Mol Biol Cell 2012; 23:4601-10; PMID:23051739; http://dx.doi.org/10.1091/mbc.E12-08-0574; (b) Moore T, Wu SK, Michael M, Yap AS, Gomez GA, Neufeld Z. Self-organizing actomyosin patterns on the cell cortex at epithelial cell-cell junctions. Biophysical journal 2014; 107:2652-61.
  • Padrick SB, Rosen MK. Physical mechanisms of signal integration by WASP family proteins. Ann Rev Biochem 2010; 79:707-35; PMID:20533885; http://dx.doi.org/10.1146/annurev.biochem.77.060407
  • Kovacs EM, Verma S, Ali RG, Ratheesh A, Hamilton NA, Akhmanova A, Yap AS. N-WASP regulates the epithelial junctional actin cytoskeleton through a non-canonical post-nucleation pathway. Nat Cell Biol 2011; 13:934-43; PMID:21785420; http://dx.doi.org/10.1038/ncb2290
  • Han SP, Gambin Y, Gomez GA, Verma S, Giles N, Michael M, Wu SK, Guo Z, Johnston W, Sierecki E, et al. Cortactin scaffolds Arp2/3 and WAVE2 at the epithelial zonula adherens. J Biol Chem 2014; 289:7764-75; PMID:24469447; http://dx.doi.org/10.1074/jbc.M113.544478
  • 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; 11:1847-57; PMID:11728307
  • Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B, Montero M, Steele-Mortimer O. Dissemination of invasive salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Nat Acad Sci U S A 2010:17733-8; PMID:20876119; http://dx.doi.org/10.1073/pnas.1006098107
  • Marinari E, Mehonic A, Curran S, Gale J, Duke T, Baum B. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 2012; 484:542-5; PMID:22504180; http://dx.doi.org/10.1038/nature10984
  • Leung CT, Brugge JS. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 2012; 482:410-3; PMID:22318515; http://dx.doi.org/10.1038/nature10826
  • Slattum G, McGee KM, Rosenblatt J. P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 2009; 186:693-702; PMID:19720875; http://dx.doi.org/10.1083/jcb.200903079
  • Kajita M, Sugimura K, Ohoka A, Burden J, Suganuma H, Ikegawa M, Shimada T, Kitamura T, Shindoh M, Ishikawa S, et al. Filamin acts as a key regulator in epithelial defence against transformed cells. Nat Commun 2014; 5:4428; PMID:25079702; http://dx.doi.org/10.1038/ncomms5428
  • Kajita M, Hogan C, Harris AR, Dupre-Crochet S, Itasaki N, Kawakami K, Charras G, Tada M, Fujita Y. Interaction with surrounding normal epithelial cells influences signalling pathways and behaviour of Src-transformed cells. J Cell Sci 2010; 123:171-80; PMID:20026643; http://dx.doi.org/10.1242/jcs.057976
  • 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; 11:460-7; PMID:19287376; http://dx.doi.org/10.1038/ncb1853
  • Liotta LA, Kohn E. Anoikis: cancer and the homeless cell. Nature 2004; 430:973-4; PMID:15329701
  • Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000; 182:311-22; PMID:10653597
  • McFall A, Ulku A, Lambert QT, Kusa A, Rogers-Graham K, Der CJ. Oncogenic ras blocks anoikis by activation of a novel effector pathway independent of phosphatidylinositol 3-kinase. Mol Cell Biol 2001; 21:5488-99; PMID:11463831
  • Thullberg M, Gad A, Le Guyader S, Stromblad S. Oncogenic H-Ras V12 promotes anchorage-independent cytokinesis in human fibroblasts. Proc Nat Acad Sci U S A 2007; http://dx.doi.org/104:20338-43; PMID:18077377
  • Grieve AG, Rabouille C. Extracellular cleavage of E-cadherin promotes epithelial cell extrusion. J Cell Sci 2014; 127:3331-46; PMID:24895403; http://dx.doi.org/10.1242/jcs.147926
  • 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; 127:1229-41; PMID:24463819; http://dx.doi.org/10.1242/jcs.138289
  • Saravanan S, Meghana C, Narasimha M. Local, cell-nonautonomous feedback regulation of myosin dynamics patterns transitions in cell behavior: a role for tension and geometry? Mol Biol Cell 2013; 24:2350-61; PMID:23741052; http://dx.doi.org/10.1091/mbc.E12-12-0868
  • Hogan C, Kajita M, Lawrenson K, Fujita Y. Interactions between normal and transformed epithelial cells: their contributions to tumourigenesis. Int J Biochem Cell Biol 2011; 43:496-503; PMID:21187160; http://dx.doi.org/10.1016/j.biocel.2010.12.019
  • Liu JS, Farlow JT, Paulson AK, Labarge MA, Gartner ZJ. Programmed cell-to-cell variability in ras activity triggers emergent behaviors during mammary epithelial morphogenesis. Cell Rep 2012; 2:1461-70; PMID:23041312; http://dx.doi.org/10.1016/j.celrep.2012.08.037
  • 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; 22:3962-70; PMID:21900494; http://dx.doi.org/10.1091/mbc.E11-05-0469
  • Nowell PC. The clonal evolution of tumor cell populations. Science 1976; 194:23-8; PMID:959840
  • Fialkow PJ. Clonal origin of human tumors. Biochim Biophysica Acta 1976; 458:283-321; PMID:1067873
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230
  • Slattum G, Gu Y, Sabbadini R, Rosenblatt J. Autophagy in oncogenic K-Ras promotes basal extrusion of epithelial cells by degrading S1P. Curr Biol 2014; 24:19-28; PMID:24361067; http://dx.doi.org/10.1016/j.cub.2013.11.029
  • Burstein HJ, Polyak K, Wong JS, Lester SC, Kaelin CM. Ductal carcinoma in situ of the breast. N Eng J med 2004; 350:1430-41; PMID:15070793
  • Fodde R. The APC gene in colorectal cancer. Eur J Cancer 2002; 38:867-71; PMID:11978510
  • Yu X, Zech T, McDonald L, Gonzalez EG, Li A, Macpherson I, Schwarz JP, Spence H, Futo K, Timpson P, et al. N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J Cell Biol 2012; 199:527-44; PMID:23091069; http://dx.doi.org/10.1083/jcb.201203025
  • Gligorijevic B, Wyckoff J, Yamaguchi H, Wang Y, Roussos ET, Condeelis J. N-WASP-mediated invadopodium formation is involved in intravasation and lung metastasis of mammary tumors. J Cell Sci 2012; 125:724-34; PMID:22389406; http://dx.doi.org/10.1242/jcs.092726

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