886
Views
5
CrossRef citations to date
0
Altmetric
SPECIAL TOPIC REVIEW: EPITHELIAL JUNCTIONS, EMT AND CANCER

Connections between cadherin-catenin proteins, spindle misorientation, and cancer

&
Article: e1045684 | Received 19 Feb 2015, Accepted 21 Apr 2015, Published online: 15 Jul 2015

References

  • Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol 1963; 17:375-412; PMID:13944428; http://dx.doi.org/10.1083/jcb.17.2.375
  • Gumbiner BM. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 2005; 6:622-34; PMID:16025097; http://dx.doi.org/10.1038/nrm1699
  • Perez-Moreno M, Jamora C, Fuchs E. Sticky business: orchestrating cellular signals at adherens junctions. Cell 2003; 112:535-48; PMID:12600316; http://dx.doi.org/10.1016/S0092-8674(03)00108-9
  • Pieters T, van Roy F. Role of cell-cell adhesion complexes in embryonic stem cell biology. J Cell Sci 2014; 127:2603-13; PMID:24931943; http://dx.doi.org/10.1242/jcs.146720
  • Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 1991; 251:1451-5; PMID:2006419; http://dx.doi.org/10.1126/science.2006419
  • Brieher WM, Yap AS. Cadherin junctions and their cytoskeleton(s). Curr Opin Cell Biol 2013; 25:39-46; PMID:23127608; http://dx.doi.org/10.1016/j.ceb.2012.10.010
  • Niessen CM, Leckband D, Yap AS. Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol Rev 2011; 91:691-731; PMID:21527735; http://dx.doi.org/10.1152/physrev.00004.2010
  • Perrais M, Chen X, Perez-Moreno M, Gumbiner BM. E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell 2007; 18:2013-25; PMID:17392517; http://dx.doi.org/10.1091/mbc.E06-04-0348
  • Birchmeier W, Behrens J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim Biophys Acta 1994; 1198:11-26; PMID:8199193
  • Berx G, Nollet F, van Roy F. Dysregulation of the E-cadherin/catenin complex by irreversible mutations in human carcinomas. Cell Adhes Commun 1998; 6:171-84; PMID:9823469; http://dx.doi.org/10.3109/15419069809004474
  • Jeanes A, Gottardi CJ, Yap AS. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 2008; 27:6920-9; PMID:19029934; http://dx.doi.org/10.1038/onc.2008.343
  • Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139:871-90; PMID:19945376; http://dx.doi.org/10.1016/j.cell.2009.11.007
  • Muthuswamy SK, Xue B. Cell polarity as a regulator of cancer cell behavior plasticity. Annu Rev Cell Dev Biol 2012; 28:599-625; PMID:22881459; http://dx.doi.org/10.1146/annurev-cellbio-092910-154244
  • Martin-Belmonte F, Perez-Moreno M. Epithelial cell polarity, stem cells and cancer. Nat Rev Cancer 2012; 12:23-38.
  • Bornens M. Organelle positioning and cell polarity. Nat Rev Mol Cell Biol 2008; 9:874-86; PMID:18946476; http://dx.doi.org/10.1038/nrm2524
  • Knoblich JA. Mechanisms of asymmetric stem cell division. Cell 2008; 132:583-97; PMID:18295577; http://dx.doi.org/10.1016/j.cell.2008.02.007
  • Knoblich JA. Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 2010; 11:849-60; PMID:21102610; http://dx.doi.org/10.1038/nrm3010
  • Quyn AJ, Appleton PL, Carey FA, Steele RJ, Barker N, Clevers H, Ridgway RA, Sansom OJ, Näthke IS. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 2010; 6:175-81; PMID:20144789; http://dx.doi.org/10.1016/j.stem.2009.12.007
  • De Mey JR, Freund JN. Understanding epithelial homeostasis in the intestine: An old battlefield of ideas, recent breakthroughs and remaining controversies. Tissue Barriers 2013; 1:e24965; PMID:24665395; http://dx.doi.org/10.4161/tisb.24965
  • Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, Brisken C, Minucci S, Di Fiore PP, Pelicci PG. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009; 138:1083-95; PMID:19766563; http://dx.doi.org/10.1016/j.cell.2009.06.048
  • Regan JL, Sourisseau T, Soady K, Kendrick H, McCarthy A, Tang C, Brennan K, Linardopoulos S, White DE, Smalley MJ. Aurora A kinase regulates mammary epithelial cell fate by determining mitotic spindle orientation in a Notch-dependent manner. Cell Rep 2013; 4:110-23; PMID:23810554; http://dx.doi.org/10.1016/j.celrep.2013.05.044
  • El-Hashash AH, Turcatel G, Al Alam D, Buckley S, Tokumitsu H, Bellusci S, Warburton D. Eya1 controls cell polarity, spindle orientation, cell fate and Notch signaling in distal embryonic lung epithelium. Development 2011; 138:1395-407; PMID:21385765; http://dx.doi.org/10.1242/dev.058479
  • El-Hashash AH, Warburton D. Cell polarity and spindle orientation in the distal epithelium of embryonic lung. Dev Dyn 2011; 240:441-5; PMID:21246661; http://dx.doi.org/10.1002/dvdy.22551
  • Lechler T, Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005; 437:275-80; PMID:16094321; http://dx.doi.org/10.1038/nature03922
  • Luxenburg C, Pasolli HA, Williams SE, Fuchs E. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat Cell Biol 2011; 13:203-14; PMID:21336301; http://dx.doi.org/10.1038/ncb2163
  • Williams SE, Beronja S, Pasolli HA, Fuchs E. Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 2011; 470:353-8; PMID:21331036; http://dx.doi.org/10.1038/nature09793
  • Niessen MT, Scott J, Zielinski JG, Vorhagen S, Sotiropoulou PA, Blanpain C, Leitges M, Niessen CM. aPKClambda controls epidermal homeostasis and stem cell fate through regulation of division orientation. J Cell Biol 2013; 202:887-900; PMID:24019538; http://dx.doi.org/10.1083/jcb.201307001
  • Williams SE, Ratliff LA, Postiglione MP, Knoblich JA, Fuchs E. Par3-mInsc and Galphai3 cooperate to promote oriented epidermal cell divisions through LGN. Nat Cell Biol 2014; 16:758-69; PMID:25016959; http://dx.doi.org/10.1038/ncb3001
  • Pease JC, Tirnauer JS. Mitotic spindle misorientation in cancer–out of alignment and into the fire. J Cell Sci 2011; 124:1007-16; PMID:21402874; http://dx.doi.org/10.1242/jcs.081406
  • Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG, Di Fiore PP. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010; 140:62-73; PMID:20074520; http://dx.doi.org/10.1016/j.cell.2009.12.007
  • O'Brien CA, Kreso A, Ryan P, Hermans KG, Gibson L, Wang Y, Tsatsanis A, Gallinger S, Dick JE. ID1 and ID3 regulate the self-renewal capacity of human colon cancer-initiating cells through p21. Cancer Cell 2012; 21:777-92; PMID:22698403; http://dx.doi.org/10.1016/j.ccr.2012.04.036
  • Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M, Clevers H. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012; 337:730-5; PMID:22855427; http://dx.doi.org/10.1126/science.1224676
  • Pine SR, Ryan BM, Varticovski L, Robles AI, Harris CC. Microenvironmental modulation of asymmetric cell division in human lung cancer cells. Proc Natl Acad Sci U S A 2010; 107:2195-200; PMID:20080668; http://dx.doi.org/10.1073/pnas.0909390107
  • Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature 2012; 488:527-30; PMID:22854777; http://dx.doi.org/10.1038/nature11344
  • Luders J, Stearns T. Microtubule-organizing centres: a re-evaluation. Nat Rev Mol Cell Biol 2007; 8:161-7; PMID:17245416; http://dx.doi.org/10.1038/nrm2100
  • Bornens M. The centrosome in cells and organisms. Science 2012; 335:422-6; PMID:22282802; http://dx.doi.org/10.1126/science.1209037
  • Tanaka TU. Kinetochore-microtubule interactions: steps towards bi-orientation. EMBO J 2010; 29:4070-82; PMID:21102558; http://dx.doi.org/10.1038/emboj.2010.294
  • Yamashita YM. The centrosome and asymmetric cell division. Prion 2009; 3:84-8; PMID:19458491; http://dx.doi.org/10.4161/pri.3.2.8821
  • Pelletier L, Yamashita YM. Centrosome asymmetry and inheritance during animal development. Curr Opin Cell Biol 2012; 24:541-6; PMID:22683192; http://dx.doi.org/10.1016/j.ceb.2012.05.005
  • Malumbres M. Physiological relevance of cell cycle kinases. Physiol Rev 2011; 91:973-1007; PMID:21742793; http://dx.doi.org/10.1152/physrev.00025.2010
  • Elric J, Etienne-Manneville S. Centrosome positioning in polarized cells: common themes and variations. Exp Cell Res 2014; 328:240-8; PMID:25218948; http://dx.doi.org/10.1016/j.yexcr.2014.09.004
  • Morin X, Bellaiche Y. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev Cell 2011; 21:102-19; PMID:21763612; http://dx.doi.org/10.1016/j.devcel.2011.06.012
  • Siller KH, Doe CQ. Spindle orientation during asymmetric cell division. Nat Cell Biol 2009; 11:365-74; PMID:19337318; http://dx.doi.org/10.1038/ncb0409-365
  • Williams SE, Fuchs E. Oriented divisions, fate decisions. Curr Opin Cell Biol 2013; 25:749-58; PMID:24021274; http://dx.doi.org/10.1016/j.ceb.2013.08.003
  • Culurgioni S, Alfieri A, Pendolino V, Laddomada F, Mapelli M. Inscuteable and NuMA proteins bind competitively to Leu-Gly-Asn repeat-enriched protein (LGN) during asymmetric cell divisions. Proc Natl Acad Sci U S A 2011; 108:20998-1003; PMID:22171003; http://dx.doi.org/10.1073/pnas.1113077108
  • Mapelli M, Gonzalez C. On the inscrutable role of Inscuteable: structural basis and functional implications for the competitive binding of NuMA and Inscuteable to LGN. Open Biol 2012; 2:120102; PMID:22977735; http://dx.doi.org/10.1098/rsob.120102
  • Hao Y, Du Q, Chen X, Zheng Z, Balsbaugh JL, Maitra S, Shabanowitz J, Hunt DF, Macara IG. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr Biol 2010; 20:1809-18; PMID:20933426; http://dx.doi.org/10.1016/j.cub.2010.09.032
  • Zheng Z, Zhu H, Wan Q, Liu J, Xiao Z, Siderovski DP, Du Q. LGN regulates mitotic spindle orientation during epithelial morphogenesis. J Cell Biol 2010; 189:275-88; PMID:20385777; http://dx.doi.org/10.1083/jcb.200910021
  • Peyre E, Jaouen F, Saadaoui M, Haren L, Merdes A, Durbec P, Morin X. A lateral belt of cortical LGN and NuMA guides mitotic spindle movements and planar division in neuroepithelial cells. J Cell Biol 2011; 193:141-54; PMID:21444683; http://dx.doi.org/10.1083/jcb.201101039
  • Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H, Miyata T, Matsuzaki F. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol 2008; 10:93-101; PMID:18084280; http://dx.doi.org/10.1038/ncb1673
  • Desai RA, Gao L, Raghavan S, Liu WF, Chen CS. Cell polarity triggered by cell-cell adhesion via E-cadherin. J Cell Sci 2009; 122:905-11; PMID:19258396; http://dx.doi.org/10.1242/jcs.028183
  • Dupin I, Camand E, Etienne-Manneville S. Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 2009; 185:779-86; PMID:19487453; http://dx.doi.org/10.1083/jcb.200812034
  • den Elzen N, Buttery CV, Maddugoda MP, Ren G, Yap AS. Cadherin adhesion receptors orient the mitotic spindle during symmetric cell division in mammalian epithelia. Mol Biol Cell 2009; 20:3740-50; PMID:19553471; http://dx.doi.org/10.1091/mbc.E09-01-0023
  • Song X, Zhu CH, Doan C, Xie T. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 2002; 296:1855-7; PMID:12052957; http://dx.doi.org/10.1126/science.1069871
  • Inaba M, Yuan H, Salzmann V, Fuller MT, Yamashita YM. E-cadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells. PLoS One 2010; 5:e12473; PMID:20824213; http://dx.doi.org/10.1371/journal.pone.0012473
  • Le Borgne R, Bellaiche Y, Schweisguth F. Drosophila E-cadherin regulates the orientation of asymmetric cell division in the sensory organ lineage. Curr Biol 2002; 12:95-104; PMID:11818059; http://dx.doi.org/10.1016/S0960-9822(01)00648-0
  • Kim S, Ishidate T, Sharma R, Soto MC, Conte D, Jr., Mello CC, Shirayama M. Wnt and CDK-1 regulate cortical release of WRM-1/beta-catenin to control cell division orientation in early Caenorhabditis elegans embryos. Proc Natl Acad Sci U S A 2013; 110:E918-27; PMID:23431196; http://dx.doi.org/10.1073/pnas.1300769110
  • Marthiens V, ffrench-Constant C. Adherens junction domains are split by asymmetric division of embryonic neural stem cells. EMBO Rep 2009; 10:515-20; PMID:19373255; http://dx.doi.org/10.1038/embor.2009.36
  • Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, Pisarek AJ, Stocker AM, Mutch CA, Funatsu N, Chenn A. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of beta-catenin signaling. Dev Cell 2010; 18:472-9; PMID:20230753; http://dx.doi.org/10.1016/j.devcel.2009.12.025
  • Humar B, Guilford P. Hereditary diffuse gastric cancer: a manifestation of lost cell polarity. Cancer Sci 2009; 100:1151-7; PMID:19432899; http://dx.doi.org/10.1111/j.1349-7006.2009.01163.x
  • Wu M, Smith CL, Hall JA, Lee I, Luby-Phelps K, Tallquist MD. Epicardial spindle orientation controls cell entry into the myocardium. Dev Cell 2010; 19:114-25; PMID:20643355; http://dx.doi.org/10.1016/j.devcel.2010.06.011
  • Bergstralh DT, Lovegrove HE, St Johnston D. Discs large links spindle orientation to apical-basal polarity in Drosophila epithelia. Curr Biol 2013; 23:1707-12; PMID:23891112; http://dx.doi.org/10.1016/j.cub.2013.07.017
  • Woolner S, Papalopulu N. Spindle position in symmetric cell divisions during epiboly is controlled by opposing and dynamic apicobasal forces. Dev Cell 2012; 22:775-87; PMID:22406140; http://dx.doi.org/10.1016/j.devcel.2012.01.002
  • Nakajima Y, Meyer EJ, Kroesen A, McKinney SA, Gibson MC. Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 2013; 500:359-62; PMID:23873041; http://dx.doi.org/10.1038/nature12335
  • Tinkle CL, Lechler T, Pasolli HA, Fuchs E. Conditional targeting of E-cadherin in skin: insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci U S A 2004; 101:552-7; PMID:14704278; http://dx.doi.org/10.1073/pnas.0307437100
  • Tunggal JA, Helfrich I, Schmitz A, Schwarz H, Gunzel D, Fromm M, Kemler R, Krieg T, Niessen CM. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J 2005; 24:1146-56; PMID:15775979; http://dx.doi.org/10.1038/sj.emboj.7600605
  • Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, van Beijnum JR, Griffioen AW, Vink J, Krimpenfort P, et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006; 10:437-49; PMID:17097565; http://dx.doi.org/10.1016/j.ccr.2006.09.013
  • Le Bras S, Le Borgne R. Epithelial cell division - multiplying without losing touch. J Cell Sci 2014; 127:5127-37; PMID:25344250; http://dx.doi.org/10.1242/jcs.151472
  • Ragkousi K, Gibson MC. Cell division and the maintenance of epithelial order. J Cell Biol 2014; 207:181-8; PMID:25349258; http://dx.doi.org/10.1083/jcb.201408044
  • Founounou N, Loyer N, Le Borgne R. Septins regulate the contractility of the actomyosin ring to enable adherens junction remodeling during cytokinesis of epithelial cells. Dev Cell 2013; 24:242-55; PMID:23410939; http://dx.doi.org/10.1016/j.devcel.2013.01.008
  • Guillot C, Lecuit T. Adhesion disengagement uncouples intrinsic and extrinsic forces to drive cytokinesis in epithelial tissues. Dev Cell 2013; 24:227-41; PMID:23410938; http://dx.doi.org/10.1016/j.devcel.2013.01.010
  • Herszterg S, Leibfried A, Bosveld F, Martin C, Bellaiche Y. Interplay between the dividing cell and its neighbors regulates adherens junction formation during cytokinesis in epithelial tissue. Dev Cell 2013; 24:256-70; PMID:23410940; http://dx.doi.org/10.1016/j.devcel.2012.11.019
  • Baker J, Garrod D. Epithelial cells retain junctions during mitosis. J Cell Sci 1993; 104 (Pt 2):415-25; PMID:7685036
  • Reinsch S, Karsenti E. Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J Cell Biol 1994; 126:1509-26; PMID:8089182; http://dx.doi.org/10.1083/jcb.126.6.1509
  • Kirschner MW, Mitchison T. Microtubule dynamics. Nature 1986; 324:621; PMID:3796729; http://dx.doi.org/10.1038/324621a0
  • Stehbens SJ, Akhmanova A, Yap AS. Microtubules and cadherins: a neglected partnership. Front Biosci (Landmark Ed) 2009; 14:3159-67; PMID:19273264; http://dx.doi.org/10.2741/3442
  • Akhmanova A, Stehbens SJ, Yap AS. Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 2009; 10:268-74; PMID:19175539; http://dx.doi.org/10.1111/j.1600-0854.2008.00869.x
  • Bellett G, Carter JM, Keynton J, Goldspink D, James C, Moss DK, Mogensen MM. Microtubule plus-end and minus-end capture at adherens junctions is involved in the assembly of apico-basal arrays in polarised epithelial cells. Cell Motil Cytoskeleton 2009; 66:893-908; PMID:19479825; http://dx.doi.org/10.1002/cm.20393
  • Karakesisoglou I, Yang Y, Fuchs E. An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol 2000; 149:195-208; PMID:10747097; http://dx.doi.org/10.1083/jcb.149.1.195
  • Mogensen MM, Tucker JB, Mackie JB, Prescott AR, Nathke IS. The adenomatous polyposis coli protein unambiguously localizes to microtubule plus ends and is involved in establishing parallel arrays of microtubule bundles in highly polarized epithelial cells. J Cell Biol 2002; 157:1041-8; PMID:12058019; http://dx.doi.org/10.1083/jcb.200203001
  • Bienz M. Spindles cotton on to junctions, APC and EB1. Nat Cell Biol 2001; 3:E67-8; PMID:11231588; http://dx.doi.org/10.1038/35060140
  • Ligon LA, Karki S, Tokito M, Holzbaur EL. Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol 2001; 3:913-7; PMID:11584273; http://dx.doi.org/10.1038/ncb1001-913
  • Ligon LA, Holzbaur EL. Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic 2007; 8:808-19; PMID:17550375; http://dx.doi.org/10.1111/j.1600-0854.2007.00574.x
  • Shahbazi MN, Megias D, Epifano C, Akhmanova A, Gundersen GG, Fuchs E, Perez-Moreno M. CLASP2 interacts with p120-catenin and governs microtubule dynamics at adherens junctions. J Cell Biol 2013; 203:1043-61; PMID:24368809; http://dx.doi.org/10.1083/jcb.201306019
  • Shahbazi MN, Perez-Moreno M. Microtubules CLASP to Adherens Junctions in epidermal progenitor cells. Bioarchitecture 2014; 4:25-30; PMID:24522006; http://dx.doi.org/10.4161/bioa.28177
  • 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
  • Kaplan DD, Meigs TE, Kelly P, Casey PJ. Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle. J Biol Chem 2004; 279:10829-32; PMID:14744872; http://dx.doi.org/10.1074/jbc.C400035200
  • Mbom BC, Nelson WJ, Barth A. beta-catenin at the centrosome: discrete pools of beta-catenin communicate during mitosis and may co-ordinate centrosome functions and cell cycle progression. Bioessays 2013; 35:804-9; PMID:23804296; http://dx.doi.org/10.1002/bies.201300045
  • Mbom BC, Siemers KA, Ostrowski MA, Nelson WJ, Barth AI. Nek2 phosphorylates and stabilizes beta-catenin at mitotic centrosomes downstream of Plk1. Mol Biol Cell 2014; 25:977-91; PMID:24501426; http://dx.doi.org/10.1091/mbc.E13-06-0349
  • Chilov D, Sinjushina N, Rita H, Taketo MM, Makela TP, Partanen J. Phosphorylated beta-catenin localizes to centrosomes of neuronal progenitors and is required for cell polarity and neurogenesis in developing midbrain. Dev Biol 2011; 357:259-68; PMID:21736876; http://dx.doi.org/10.1016/j.ydbio.2011.06.029
  • Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH, Jr., O'Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AI. beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev 2008; 22:91-105; PMID:18086858; http://dx.doi.org/10.1101/gad.1596308
  • Berrueta L, Kraeft SK, Tirnauer JS, Schuyler SC, Chen LB, Hill DE, Pellman D, Bierer BE. The adenomatous polyposis coli-binding protein EB1 is associated with cytoplasmic and spindle microtubules. Proc Natl Acad Sci U S A 1998; 95:10596-601; PMID:9724749; http://dx.doi.org/10.1073/pnas.95.18.10596
  • Askham JM, Vaughan KT, Goodson HV, Morrison EE. Evidence that an interaction between EB1 and p150(Glued) is required for the formation and maintenance of a radial microtubule array anchored at the centrosome. Mol Biol Cell 2002; 13:3627-45; PMID:12388762; http://dx.doi.org/10.1091/mbc.E02-01-0061
  • Fodde R, Kuipers J, Rosenberg C, Smits R, Kielman M, Gaspar C, van Es JH, Breukel C, Wiegant J, Giles RH, et al. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 2001; 3:433-8; PMID:11283620; http://dx.doi.org/10.1038/35070129
  • Kaplan KB, Burds AA, Swedlow JR, Bekir SS, Sorger PK, Nathke IS. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 2001; 3:429-32; PMID:11283619; http://dx.doi.org/10.1038/35070123
  • McCartney BM, Dierick HA, Kirkpatrick C, Moline MM, Baas A, Peifer M, Bejsovec A. Drosophila APC2 is a cytoskeletally-associated protein that regulates wingless signaling in the embryonic epidermis. J Cell Biol 1999; 146:1303-18; PMID:10491393; http://dx.doi.org/10.1083/jcb.146.6.1303
  • Miller RK, Rose MD. Kar9p is a novel cortical protein required for cytoplasmic microtubule orientation in yeast. J Cell Biol 1998; 140:377-90; PMID:9442113; http://dx.doi.org/10.1083/jcb.140.2.377
  • Lu B, Roegiers F, Jan LY, Jan YN. Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 2001; 409:522-5; PMID:11206549; http://dx.doi.org/10.1038/35054077
  • Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 2003; 301:1547-50; PMID:12970569; http://dx.doi.org/10.1126/science.1087795
  • Clevers H, Loh KM, Nusse R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 2014; 346:1248012; PMID:25278615; http://dx.doi.org/10.1126/science.1248012
  • Habib SJ, Chen BC, Tsai FC, Anastassiadis K, Meyer T, Betzig E, Nusse R. A localized Wnt signal orients asymmetric stem cell division in vitro. Science 2013; 339:1445-8; PMID:23520113; http://dx.doi.org/10.1126/science.1231077
  • Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004; 303:1483-7; PMID:15001769; http://dx.doi.org/10.1126/science.1094291
  • Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127:469-80; PMID:17081971; http://dx.doi.org/10.1016/j.cell.2006.10.018
  • Fleming ES, Temchin M, Wu Q, Maggio-Price L, Tirnauer JS. Spindle misorientation in tumors from APC(min/+) mice. Mol Carcinog 2009; 48:592-8; PMID:19123231; http://dx.doi.org/10.1002/mc.20506
  • Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434:843-50; PMID:15829953; http://dx.doi.org/10.1038/nature03319
  • Franz CM, Ridley AJ. p120 catenin associates with microtubules: inverse relationship between microtubule binding and Rho GTPase regulation. J Biol Chem 2004; 279:6588-94; PMID:14660598; http://dx.doi.org/10.1074/jbc.M312812200
  • Yanagisawa M, Kaverina IN, Wang A, Fujita Y, Reynolds AB, Anastasiadis PZ. A novel interaction between kinesin and p120 modulates p120 localization and function. J Biol Chem 2004; 279:9512-21; PMID:14676216; http://dx.doi.org/10.1074/jbc.M310895200
  • Chartier NT, Oddou CI, Laine MG, Ducarouge B, Marie CA, Block MR, Jacquier-Sarlin MR. Cyclin-dependent kinase 2/cyclin E complex is involved in p120 catenin (p120ctn)-dependent cell growth control: a new role for p120ctn in cancer. Cancer Res 2007; 67:9781-90; PMID:17942908; http://dx.doi.org/10.1158/0008-5472.CAN-07-0233
  • Daniel JM, Reynolds AB. The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol Cell Biol 1999; 19:3614-23; PMID:10207085
  • Kantidze OL, Kamalyukova IM, Razin SV. Association of the mammalian transcriptional regulator kaiso with centrosomes and the midbody. Cell Cycle 2009; 8:2303-4; PMID:19502788; http://dx.doi.org/10.4161/cc.8.14.8944
  • Soubry A, Staes K, Parthoens E, Noppen S, Stove C, Bogaert P, van Hengel J, van Roy F. The transcriptional repressor Kaiso localizes at the mitotic spindle and is a constituent of the pericentriolar material. PLoS One 2010; 5:e9203; PMID:20169156; http://dx.doi.org/10.1371/journal.pone.0009203
  • Anastasiadis PZ, Moon SY, Thoreson MA, Mariner DJ, Crawford HC, Zheng Y, Reynolds AB. Inhibition of RhoA by p120 catenin. Nat Cell Biol 2000; 2:637-44; PMID:10980705; http://dx.doi.org/10.1038/35023588
  • Anastasiadis PZ, Reynolds AB. Regulation of Rho GTPases by p120-catenin. Curr Opin Cell Biol 2001; 13:604-10; PMID:11544030; http://dx.doi.org/10.1016/S0955-0674(00)00258-1
  • Perez-Moreno M, Song W, Pasolli HA, Williams SE, Fuchs E. Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer. Proc Natl Acad Sci U S A 2008; 105:15399-404; PMID:18809907; http://dx.doi.org/10.1073/pnas.0807301105
  • Pereira AL, Pereira AJ, Maia AR, Drabek K, Sayas CL, Hergert PJ, Lince-Faria M, Matos I, Duque C, Stepanova T, et al. Mammalian CLASP1 and CLASP2 cooperate to ensure mitotic fidelity by regulating spindle and kinetochore function. Mol Biol Cell 2006; 17:4526-42; PMID:16914514; http://dx.doi.org/10.1091/mbc.E06-07-0579
  • Logarinho E, Maffini S, Barisic M, Marques A, Toso A, Meraldi P, Maiato H. CLASPs prevent irreversible multipolarity by ensuring spindle-pole resistance to traction forces during chromosome alignment. Nat Cell Biol 2012; 14:295-303; PMID:22307330; http://dx.doi.org/10.1038/ncb2423
  • Samora CP, Mogessie B, Conway L, Ross JL, Straube A, McAinsh AD. MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat Cell Biol 2011; 13:1040-50; PMID:21822276; http://dx.doi.org/10.1038/ncb2297
  • Bird SL, Heald R, Weis K. RanGTP and CLASP1 cooperate to position the mitotic spindle. Mol Biol Cell 2013; 24:2506-14; PMID:23783028; http://dx.doi.org/10.1091/mbc.E13-03-0150
  • Thery M, Bornens M. Cell shape and cell division. Curr Opin Cell Biol 2006; 18:648-57; PMID:17046223; http://dx.doi.org/10.1016/j.ceb.2006.10.001
  • Grill SW, Hyman AA. Spindle positioning by cortical pulling forces. Dev Cell 2005; 8:461-5; PMID:15809029; http://dx.doi.org/10.1016/j.devcel.2005.03.014
  • Palmer RE, Sullivan DS, Huffaker T, Koshland D. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J Cell Biol 1992; 119:583-93; PMID:1400594; http://dx.doi.org/10.1083/jcb.119.3.583
  • Vasioukhin V, Bauer C, Yin M, Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 2000; 100:209-19; PMID:10660044; http://dx.doi.org/10.1016/S0092-8674(00)81559-7
  • Adams CL, Chen YT, Smith SJ, Nelson WJ. Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein. J Cell Biol 1998; 142:1105-19; PMID:9722621; http://dx.doi.org/10.1083/jcb.142.4.1105
  • Perez-Moreno M, Fuchs E. Catenins: keeping cells from getting their signals crossed. Dev Cell 2006; 11:601-12; PMID:17084354; http://dx.doi.org/10.1016/j.devcel.2006.10.010
  • Scott JA, Yap AS. Cinderella no longer: alpha-catenin steps out of cadherin's shadow. J Cell Sci 2006; 119:4599-605; PMID:17093264; http://dx.doi.org/10.1242/jcs.03267
  • 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; http://dx.doi.org/10.1016/S0960-9822(02)00661-9
  • Padrick SB, Rosen MK. Physical mechanisms of signal integration by WASP family proteins. Annu Rev Biochem 2010; 79:707-35; PMID:20533885; http://dx.doi.org/10.1146/annurev.biochem.77.060407.135452
  • 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
  • Zhou K, Muroyama A, Underwood J, Leylek R, Ray S, Soderling SH, Lechler T. Actin-related protein2/3 complex regulates tight junctions and terminal differentiation to promote epidermal barrier formation. Proc Natl Acad Sci U S A 2013; 110:E3820-9; PMID:24043783; http://dx.doi.org/10.1073/pnas.1308419110
  • Lechler T. Arp2/3 complex function in the epidermis. Tissue Barriers 2014; 2:e944445; PMID:25610753
  • Gladden AB, Hebert AM, Schneeberger EE, McClatchey AI. The NF2 tumor suppressor, Merlin, regulates epidermal development through the establishment of a junctional polarity complex. Dev Cell 2010; 19:727-39; PMID:21074722; http://dx.doi.org/10.1016/j.devcel.2010.10.008
  • Ingber DE. The riddle of morphogenesis: a question of solution chemistry or molecular cell engineering? Cell 1993; 75:1249-52; PMID:8269508; http://dx.doi.org/10.1016/0092-8674(93)90612-T
  • Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009; 10:75-82; PMID:19197334; http://dx.doi.org/10.1038/nrm2594
  • Jaalouk DE, Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol 2009; 10:63-73; PMID:19197333; http://dx.doi.org/10.1038/nrm2597
  • DuFort CC, Paszek MJ, Weaver VM. Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 2011; 12:308-19; PMID:21508987; http://dx.doi.org/10.1038/nrm3112
  • Humphrey JD, Dufresne ER, Schwartz MA. Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 2014; 15:802-12; PMID:25355505; http://dx.doi.org/10.1038/nrm3896
  • Harris TJ, Tepass U. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 2010; 11:502-14; PMID:20571587; http://dx.doi.org/10.1038/nrm2927
  • le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, de Rooij J. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 2010; 189:1107-15; PMID:20584916; http://dx.doi.org/10.1083/jcb.201001149
  • Leckband DE, de Rooij J. Cadherin adhesion and mechanotransduction. Annu Rev Cell Dev Biol 2014; 30:291-315; PMID:25062360; http://dx.doi.org/10.1146/annurev-cellbio-100913-013212
  • 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; 12:533-42; PMID:20453849; http://dx.doi.org/10.1038/ncb2055
  • 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; 346:1254211; PMID:25359979; http://dx.doi.org/10.1126/science.1254211
  • Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, Rehmann H, de Rooij J. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 2012; 196:641-52; PMID:22391038; http://dx.doi.org/10.1083/jcb.201108120
  • Gumbiner BM, Kim NG. The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 2014; 127:709-17; PMID:24532814; http://dx.doi.org/10.1242/jcs.140103
  • Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010; 19:491-505; PMID:20951342; http://dx.doi.org/10.1016/j.devcel.2010.09.011
  • Halder G, Dupont S, Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol 2012; 13:591-600; PMID:22895435; http://dx.doi.org/10.1038/nrm3416
  • Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, Dupont S, Piccolo S. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013; 154:1047-59; PMID:23954413; http://dx.doi.org/10.1016/j.cell.2013.07.042
  • Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, et al. Role of YAP/TAZ in mechanotransduction. Nature 2011; 474:179-83; PMID:21654799; http://dx.doi.org/10.1038/nature10137
  • Tepass U. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu Rev Cell Dev Biol 2012; 28:655-85; PMID:22881460; http://dx.doi.org/10.1146/annurev-cellbio-092910-154033
  • Boggiano JC, Fehon RG. Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev Cell 2012; 22:695-702; PMID:22516196; http://dx.doi.org/10.1016/j.devcel.2012.03.013
  • Grusche FA, Richardson HE, Harvey KF. Upstream regulation of the hippo size control pathway. Curr Biol 2010; 20:R574-82; PMID:20619814; http://dx.doi.org/10.1016/j.cub.2010.05.023
  • Gaspar P, Tapon N. Sensing the local environment: actin architecture and Hippo signalling. Curr Opin Cell Biol 2014; 31:74-83; PMID:25259681; http://dx.doi.org/10.1016/j.ceb.2014.09.003
  • Wada K, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development 2011; 138:3907-14; PMID:21831922; http://dx.doi.org/10.1242/dev.070987
  • Yang S, Zhang L, Liu M, Chong R, Ding SJ, Chen Y, Dong J. CDK1 phosphorylation of YAP promotes mitotic defects and cell motility and is essential for neoplastic transformation. Cancer Res 2013; 73:6722-33; PMID:24101154; http://dx.doi.org/10.1158/0008-5472.CAN-13-2049
  • Tsukahara T, Tanno Y, Watanabe Y. Phosphorylation of the CPC by Cdk1 promotes chromosome bi-orientation. Nature 2010; 467:719-23; PMID:20739936; http://dx.doi.org/10.1038/nature09390
  • Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, Gessler M, Quaggin SE, Harrison R, Mount R, McNeill H. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 2008; 40:1010-5; PMID:18604206; http://dx.doi.org/10.1038/ng.179
  • Mao Y, Tournier AL, Bates PA, Gale JE, Tapon N, Thompson BJ. Planar polarization of the atypical myosin Dachs orients cell divisions in Drosophila. Genes Dev 2011; 25:131-6; PMID:21245166; http://dx.doi.org/10.1101/gad.610511
  • Wei C, Bhattaram VK, Igwe JC, Fleming E, Tirnauer JS. The LKB1 tumor suppressor controls spindle orientation and localization of activated AMPK in mitotic epithelial cells. PLoS One 2012; 7:e41118; PMID:22815934; http://dx.doi.org/10.1371/journal.pone.0041118
  • Mohseni M, Sun J, Lau A, Curtis S, Goldsmith J, Fox VL, Wei C, Frazier M, Samson O, Wong KK, et al. A genetic screen identifies an LKB1-MARK signalling axis controlling the Hippo-YAP pathway. Nat Cell Biol 2014; 16:108-17; PMID:24362629; http://dx.doi.org/10.1038/ncb2884
  • Thaiparambil JT, Eggers CM, Marcus AI. AMPK regulates mitotic spindle orientation through phosphorylation of myosin regulatory light chain. Mol Cell Biol 2012; 32:3203-17; PMID:22688514; http://dx.doi.org/10.1128/MCB.00418-12
  • Poon CL, Lin JI, Zhang X, Harvey KF. The sterile 20-like kinase Tao-1 controls tissue growth by regulating the Salvador-Warts-Hippo pathway. Dev Cell 2011; 21:896-906; PMID:22075148; http://dx.doi.org/10.1016/j.devcel.2011.09.012
  • Wojtala RL, Tavares IA, Morton PE, Valderrama F, Thomas NS, Morris JD. Prostate-derived sterile 20-like kinases (PSKs/TAOKs) are activated in mitosis and contribute to mitotic cell rounding and spindle positioning. J Biol Chem 2011; 286:30161-70; PMID:21705329; http://dx.doi.org/10.1074/jbc.M111.228320
  • Yue T, Tian A, Jiang J. The cell adhesion molecule echinoid functions as a tumor suppressor and upstream regulator of the Hippo signaling pathway. Dev Cell 2012; 22:255-67; PMID:22280890; http://dx.doi.org/10.1016/j.devcel.2011.12.011
  • Marie H, Pratt SJ, Betson M, Epple H, Kittler JT, Meek L, Moss SJ, Troyanovsky S, Attwell D, Longmore GD, et al. The LIM protein Ajuba is recruited to cadherin-dependent cell junctions through an association with alpha-catenin. J Biol Chem 2003; 278:1220-8; PMID:12417594; http://dx.doi.org/10.1074/jbc.M205391200
  • Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB, Longmore GD. Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr Biol 2010; 20:657-62; PMID:20303269; http://dx.doi.org/10.1016/j.cub.2010.02.035
  • Kim NG, Koh E, Chen X, Gumbiner BM. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci U S A 2011; 108:11930-5; PMID:21730131; http://dx.doi.org/10.1073/pnas.1103345108
  • Leung CY, Zernicka-Goetz M. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and -independent mechanisms. Nat Commun 2013; 4:2251; PMID:23903990; http://dx.doi.org/10.1038/ncomms3251
  • Hirate Y, Hirahara S, Inoue K, Suzuki A, Alarcon VB, Akimoto K, Hirai T, Hara T, Adachi M, Chida K, et al. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr Biol 2013; 23:1181-94; PMID:23791731; http://dx.doi.org/10.1016/j.cub.2013.05.014
  • Hirate Y, Sasaki H. The role of angiomotin phosphorylation in the Hippo pathway during preimplantation mouse development. Tissue Barriers 2014; 2:e28127; PMID:24843842; http://dx.doi.org/10.4161/tisb.28127
  • Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011; 144:782-95; PMID:21376238; http://dx.doi.org/10.1016/j.cell.2011.02.031
  • Silvis MR, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo FD, Lantz DM, Seykora JT, Vasioukhin V. alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 2011; 4:ra33; PMID:21610251; http://dx.doi.org/10.1126/scisignal.2001823

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.