3,418
Views
38
CrossRef citations to date
0
Altmetric
Review

The role of microtubules in the regulation of epithelial junctions

&
Article: 1539596 | Received 06 Sep 2018, Accepted 11 Oct 2018, Published online: 05 Nov 2018

References

  • Pollard TD, Goldman RD. Overview of the cytoskeleton from an evolutionary perspective. Cold Spring Harb Perspect Biol. 2018;10(7):a030288. doi:10.1101/cshperspect.a030288.
  • Tilney LG, Bryan J, Bush DJ, Fujiwara K, Mooseker MS, Murphy DB, Snyder DH. Microtubules: evidence for 13 protofilaments. J Cell Biol. 1973;59(2 Pt 1):267–275.
  • Desai A, Mitchison TJ. Microtubule polymerization dynamics. Annu Rev Cell Dev Biol. 1997;13:83–117. doi:10.1146/annurev.cellbio.13.1.83.
  • Martin M, Akhmanova A. Coming into Focus: mechanisms of Microtubule Minus-End Organization. Trends Cell Biol. 2018;28(7):574–588. doi:10.1016/j.tcb.2018.02.011.
  • Gadadhar S, Bodakuntla S, Natarajan K, Janke C. The tubulin code at a glance. J Cell Sci. 2017;130(8):1347–1353. doi:10.1242/jcs.199471.
  • Muroyama A, Lechler T. Microtubule organization, dynamics and functions in differentiated cells. Development. 2017;144(17):3012–3021. doi:10.1242/dev.153171.
  • Bacallao R, Antony C, Dotti C, Karsenti E, Stelzer EH, Simons K. The subcellular organization of Madin-Darby Canine Kidney cells during the formation of a polarized epithelium. J Cell Biol. 1989;109:2817–2832.
  • Bré MH, Pepperkok R, Hill AM, Levilliers N, Ansorge W, Stelzer EH, Karsenti E. Regulation of microtubule dynamics and nucleation during polarization in MDCK II cells. J Cell Biol. 1990;111(6 Pt 2):3013–3021.
  • Waterman-Storer CM, Salmon WC, Salmon ED. Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells. Mol Biol Cell. 2000;11(7):2471–2483. doi:10.1091/mbc.11.7.2471.
  • Yano T, Matsui T, Tamura A, Uji M, Tsukita S. The association of microtubules with tight junctions is promoted by cingulin phosphorylation by AMPK. J Cell Biol. 2013;203(4):605–614. doi:10.1083/jcb.201304194.
  • Tanaka N, Meng W, Nagae S, Takeichi M. Nezha/CAMSAP3 and CAMSAP2 cooperate in epithelial-specific organization of noncentrosomal microtubules. Proc Natl Acad Sci U S A. 2012;109(49):20029–20034. doi:10.1073/pnas.1218017109.
  • Jiang K, Hua S, Mohan R, Grigoriev I, Yau KW, Liu Q, Katrukha EA, Altelaar AFM, Heck AJR, Hoogenraad CC, et al. Microtubule minus-end stabilization by polymerization-driven CAMSAP deposition. Dev Cell. 2014;28(3):295–309. doi:10.1016/j.devcel.2014.01.001.
  • Toya M, Kobayashi S, Kawasaki M, Shioi G, Kaneko M, Ishiuchi T, Misaki K, Meng W, Takeichi M. CAMSAP3 orients the apical-to-basal polarity of microtubule arrays in epithelial cells. Proc Natl Acad Sci U S A. 2016;113(2):332–337. doi:10.1073/pnas.1520638113.
  • Farquhar MG, Palade GE. Junctional complexes in various epithelia. J Cell Biol. 1963;17:375–412.
  • Takeichi M. Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling. Nat Rev Mol Cell Biol. 2014;15(6):397–410. doi:10.1038/nrm3802.
  • Godsel, L.M., et al. The molecular composition and function of desmosomes. Handb Exp Pharmacol. 2004;165:137–193.
  • Giannotta M, Trani M, Dejana E. VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev Cell. 2013;26(5):441–454. doi:10.1016/j.devcel.2013.08.020.
  • Umeda K, Ikenouchi J, Katahira-Tayama S, Furuse K, Sasaki H, Nakayama M, Matsui T, Tsukita S, Furuse M, Tsukita S. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell. 2006;126(4):741–754. doi:10.1016/j.cell.2006.06.043.
  • Citi S, Guerrera D, Spadaro D, Shah J. Epithelial junctions and Rho family GTPases: the zonular signalosome. Small GTPases. 2014;5(4):1–15. doi:10.4161/21541248.2014.973760.
  • Wen W, Zhang M. Protein complex assemblies in epithelial cell polarity and asymmetric cell division. J Mol Biol. 2017;430:3504–3520.
  • Charras G, Yap AS. Tensile forces and mechanotransduction at cell-cell junctions. Curr Biol. 2018;28(8):R445–R457. doi:10.1016/j.cub.2018.02.003.
  • Spadaro D, Le S, Laroche T, Mean I, Jond L, Yan J, Citi S. Tension-dependent stretching activates ZO-1 to control the junctional localization of its interactors. Curr Biol. 2017;27(24):3783–3795.e8. doi:10.1016/j.cub.2017.11.014.
  • Hatzfeld M, Keil R, Magin TM. Desmosomes and intermediate filaments: their consequences for tissue mechanics. Cold Spring Harb Perspect Biol. 2017;9(6):a029157. doi:10.1101/cshperspect.a029157.
  • Guillemot L, Paschoud S, Pulimeno P, Foglia A, Citi S. The cytoplasmic plaque of tight junctions: a scaffolding and signalling center. Biochim Biophys Acta Biomembr. 2008;1778(3):601–613. doi:10.1016/j.bbamem.2007.09.032.
  • Green KJ, Getsios S, Troyanovsky S, Godsel LM. Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol. 2010;2(2):a000125. doi:10.1101/cshperspect.a000125.
  • Van Itallie CM, Anderson JM. Architecture of tight junctions and principles of molecular composition. Semin Cell Dev Biol. 2014;36:157–165. doi:10.1016/j.semcdb.2014.08.011.
  • Meng W, Takeichi M. Adherens junction: molecular architecture and regulation. Cold Spring Harb Perspect Biol. 2009;1:a002899–a002899. doi:10.1101/cshperspect.a002899.
  • Niessen CM, Gottardi CJ. Molecular components of the adherens junction. Biochim Biophys Acta. 2008;1778(3):562–571. doi:10.1016/j.bbamem.2007.12.015.
  • Mandai K, Rikitake Y, Mori M, Takai Y. Nectins and nectin-like molecules in development and disease. Curr Top Dev Biol. 2015;112:197–231. doi:10.1016/bs.ctdb.2014.11.019.
  • Furuse M, Tsukita S. Claudins in occluding junctions of humans and flies. Trends Cell Biol. 2006;16(4):181–188. doi:10.1016/j.tcb.2006.02.006.
  • Lecuit T, Yap AS. E-cadherin junctions as active mechanical integrators in tissue dynamics. Nat Cell Biol. 2015;17(5):533–539. doi:10.1038/ncb3136.
  • Meza I, Ibarra G, Sabanero M, Martínez-Palomo A, Cereijido M. Occluding junctions and cytoskeletal components in a cultured transporting epithelium. J Cell Biol. 1980;87:746–754.
  • Rassat J, Robenek H, Themann H. Alterations of tight and gap junctions in mouse hepatocytes following administration of colchicine. Cell Tissue Res. 1982;223(1):187–200.
  • Yap AS, Stevenson BR, Abel KC, Cragoe EJ, Manley SW. Microtubule integrity is necessary for the epithelial barrier function of cultured thyroid cell monolayers. Exp Cell Res. 1995;218(2):540–550. doi:10.1006/excr.1995.1189.
  • Paschoud S, Yu D, Pulimeno P, Jond L, Turner JR, Citi S. Cingulin and paracingulin show similar dynamic behaviour, but are recruited independently to junctions. Mol Membr Biol. 2011;28(2):123–135. doi:10.3109/09687688.2010.538937.
  • Glotfelty LG, Zahs A, Iancu C, Shen L, Hecht GA. Microtubules are required for efficient epithelial tight junction homeostasis and restoration. Am J Physiol Cell Physiol. 2014;307(3):C245–54. doi:10.1152/ajpcell.00336.2013.
  • Simard-Bisson C, Bidoggia J, Larouche D, Guérin SL, Blouin R, Hirai S-I, Germain L. A role for DLK in microtubule reorganization to the cell periphery and in the maintenance of desmosomal and tight junction integrity. J Invest Dermatol. 2017;137(1):132–141. doi:10.1016/j.jid.2016.07.035.
  • Hsu C-Y, Lecland N, Pendaries V, Viodé C, Redoulès D, Paul C, Merdes A, Simon M, Bierkamp C. Stabilization of microtubules restores barrier function after cytokine-induced defects in reconstructed human epidermis. J Dermatol Sci. 2018;91(1):87–96. doi:10.1016/j.jdermsci.2018.04.008.
  • Fesenko I, Kurth T, Sheth B, Fleming TP, Citi S, Hausen P. Tight junction biogenesis in the early Xenopus embryo. Mech Dev. 2000;96:51–65.
  • Li D, Kuehn EW, Prekeris R. Kinesin-2 mediates apical endosome transport during epithelial lumen formation. Cell Logist. 2014;4(1):e28928. doi:10.4161/cl.28928.
  • Mangan AJ, Sietsema DV, Li D, Moore JK, Citi S, Prekeris R. Cingulin and actin mediate midbody-dependent apical lumen formation during polarization of epithelial cells. Nat Commun. 2016;7:12426. doi:10.1038/ncomms12426.
  • Ivanov AI, McCall IC, Babbin B, Samarin SN, Nusrat A, Parkos CA. Microtubules regulate disassembly of epithelial apical junctions. BMC Cell Biol. 2006;7:12. doi:10.1186/1471-2121-7-12.
  • Citi S. Protein kinase inhibitors prevent junction dissociation induced by low extracellular calcium in MDCK epithelial cells. J Cell Biol. 1992;117(1):169–178.
  • Citi S, Volberg T, Bershadsky AD, Denisenko N, Geiger B. Cytoskeletal involvement in the modulation of cell-cell junctions by the protein kinase inhibitor H-7. J Cell Sci. 1994;107(3):683–692.
  • Ivanov AI, McCall IC, Parkos CA, Nusrat A. Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell. 2004;15(6):2639–2651. doi:10.1091/mbc.e04-02-0163.
  • Ivanov AI, Bachar M, Babbin BA, Adelstein RS, Nusrat A, Parkos CA, Cordes N. A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS One. 2007;2(7):e658. doi:10.1371/journal.pone.0000658.
  • Samarin SN, Ivanov AI, Flatau G, Parkos CA, Nusrat A. Rho/Rho-associated kinase-II signaling mediates disassembly of epithelial apical junctions. Mol Biol Cell. 2007;18(9):3429–3439. doi:10.1091/mbc.e07-04-0315.
  • Ito S, Okuda S, Abe M, Fujimoto M, Onuki T, Nishimura T, Takeichi M. Induced cortical tension restores functional junctions in adhesion-defective carcinoma cells. Nat Commun. 2017;8(1):1834. doi:10.1038/s41467-017-01945-y.
  • Shultz T, Shmuel M, Hyman T, Altschuler Y. Beta-tubulin cofactor D and ARL2 take part in apical junctional complex disassembly and abrogate epithelial structure. FASEB J. 2008;22(1):168–182. doi:10.1096/fj.06-7786com.
  • Mary S, Charrasse S, Meriane M, Comunale F, Travo P, Blangy A, Gauthier-Rouvière C. Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol Biol Cell. 2002;13(1):285–301. doi:10.1091/mbc.01-07-0337.
  • Chen X, Kojima S-I, Borisy GG, Green KJ. p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J Cell Biol. 2003;163(3):547–557. doi:10.1083/jcb.200305137.
  • Teng J, Rai T, Tanaka Y, Takei Y, Nakata T, Hirasawa M, Kulkarni AB, Hirokawa N. The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat Cell Biol. 2005;7(5):474–482. doi:10.1038/ncb1249.
  • Acharya BR, Espenel C, Libanje F, Raingeaud J, Morgan J, Jaulin F, Kreitzer G. KIF17 regulates RhoA-dependent actin remodeling at epithelial cell-cell adhesions. J Cell Sci. 2016;129(5):957–970. doi:10.1242/jcs.173674.
  • Ligon LA, Holzbaur ELF. Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic. 2007;8(7):808–819. doi:10.1111/j.1600-0854.2007.00574.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(10):893–908. doi:10.1002/cm.20393.
  • Stehbens SJ, Paterson AD, Crampton MS, Shewan AM, Ferguson C, Akhmanova A, Parton RG, Yap AS. Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts. J Cell Sci. 2006;119(Pt 9):1801–1811. doi:10.1242/jcs.02903.
  • Rowning BA, Wells J, Wu M, Gerhart JC, Moon RT, Larabell CA. Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs. Proc Natl Acad Sci U S A. 1997;94(4):1224–1229.
  • Moss DK, Bellett G, Carter JM, Liovic M, Keynton J, Prescott AR, Lane EB, Mogensen MM. Ninein is released from the centrosome and moves bi-directionally along microtubules. J Cell Sci. 2007;120(Pt 17):3064–3074. doi:10.1242/jcs.010322.
  • Gavilan MP, Arjona M, Zurbano A, Formstecher E, Martinez-Morales JR, Bornens M, Rios RM, Gumbiner BM. Alpha-catenin-dependent recruitment of the centrosomal protein CAP350 to adherens junctions allows epithelial cells to acquire a columnar shape. PLoS Biol. 2015;13(3):e1002087. doi:10.1371/journal.pbio.1002087.
  • Goldspink DA, Rookyard C, Tyrrell BJ, Gadsby J, Perkins J, Lund EK, Galjart N, Thomas P, Wileman T, Mogensen MM. Ninein is essential for apico-basal microtubule formation and CLIP-170 facilitates its redeployment to non-centrosomal microtubule organizing centres. Open Biol. 2017;7(2):160274. doi:10.1098/rsob.160274.
  • Meng W, Mushika Y, Ichii T, Takeichi M. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell. 2008;135(5):948–959. doi:10.1016/j.cell.2008.09.040.
  • Sako-Kubota K, Tanaka N, Nagae S, Meng W, Takeichi M. Minus end-directed motor KIFC3 suppresses E-cadherin degradation by recruiting USP47 to adherens junctions. Mol Biol Cell. 2014;25(24):3851–3860. doi:10.1091/mbc.E14-07-1245.
  • Pasdar M, Krzeminski KA, Nelson WJ. Regulation of desmosome assembly in MDCK epithelial cells: coordination of membrane core and cytoplasmic plaque domain assembly at the plasma membrane. J Cell Biol. 1991;113:645–655.
  • Nekrasova OE, Amargo EV, Smith WO, Chen J, Kreitzer GE, Green KJ. Desmosomal cadherins utilize distinct kinesins for assembly into desmosomes. J Cell Biol. 2011;195(7):1185–1203. doi:10.1083/jcb.201106057.
  • Sumigray KD, Chen H, Lechler T. Lis1 is essential for cortical microtubule organization and desmosome stability in the epidermis. J Cell Biol. 2011;194(4):631–642. doi:10.1083/jcb.201104009.
  • Robitaille H, Proulx R, Robitaille K, Blouin R, Germain L. The mitogen-activated protein kinase kinase kinase dual leucine zipper-bearing kinase (DLK) acts as a key regulator of keratinocyte terminal differentiation. J Biol Chem. 2005;280(13):12732–12741. doi:10.1074/jbc.M411619200.
  • McHarg S, Hopkins G, Lim L, Garrod D, Klymkowsky M. Down-regulation of desmosomes in cultured cells: the roles of PKC, microtubules and lysosomal/proteasomal degradation. PLoS One. 2014;9(10):e108570. doi:10.1371/journal.pone.0108570.
  • Citi S, Sabanay H, Jakes R, Geiger B, Kendrick-Jones J. Cingulin, a new peripheral component of tight junctions. Nature. 1988;333:272–276. doi:10.1038/333272a0.
  • Citi S, Sabanay H, Kendrick-Jones J, Geiger B. Cingulin: characterization and localization. J Cell Sci. 1989;93(1):107–122.
  • Lizcano JM, Göransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Mäkelä TP, Hardie DG, et al. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. Embo J. 2004;23(4):833–843. doi:10.1038/sj.emboj.7600110.
  • Porat-Shliom N, Tietgens AJ, Van Itallie CM, Vitale-Cross L, Jarnik M, Harding OJ, Anderson JM, Gutkind JS, Weigert R, Arias IM. Liver kinase B1 regulates hepatocellular tight junction distribution and function in vivo. Hepatology. 2016;64(4):1317–1329. doi:10.1002/hep.28724.
  • D’Atri F, Citi S. Cingulin interacts with F-actin in vitro. FEBS Lett. 2001;507:21–24.
  • Ohnishi H, Nakahara T, Furuse K, Sasaki H, Tsukita S, Furuse M. JACOP, a novel plaque protein localizing at the apical junctional complex with sequence similarity to cingulin. J Biol Chem. 2004;279(44):46014–46022. doi:10.1074/jbc.M402616200.
  • Pulimeno P, Paschoud S, Citi S. A role for ZO-1 and PLEKHA7 in recruiting paracingulin to tight and adherens junctions of epithelial cells. J Biol Chem. 2011;286(19):16743–16750. doi:10.1074/jbc.M111.230862.
  • Umeda K, Matsui T, Nakayama M, Furuse K, Sasaki H, Furuse M, Tsukita S. Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. J Biol Chem. 2004;279(43):44785–44794. doi:10.1074/jbc.M406563200.
  • D’Atri F, Nadalutti F, Citi S. Evidence for a functional interaction between cingulin and ZO-1 in cultured cells. J Biol Chem. 2002;277(31):27757–27764. doi:10.1074/jbc.M203717200.
  • Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature. 2003;426(6966):570–574. doi:10.1038/nature02166.
  • Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol. 2000;2(8):540–547. doi:10.1038/35019582.
  • Joberty G, Petersen C, Gao L, Macara IG. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol. 2000;2(8):531–539. doi:10.1038/35019573.
  • Mizuno K, Suzuki A, Hirose T, Kitamura K, Kutsuzawa K, Futaki M, Amano Y, Ohno S. Self-association of PAR-3-mediated by the conserved N-terminal domain contributes to the development of epithelial tight junctions. J Biol Chem. 2003;278(33):31240–31250. doi:10.1074/jbc.M303593200.
  • Ahmed SM, Macara IG. The Par3 polarity protein is an exocyst receptor essential for mammary cell survival. Nat Commun. 2017;8:14867. doi:10.1038/ncomms14867.
  • Schmoranzer J, Fawcett JP, Segura M, Tan S, Vallee RB, Pawson T, Gundersen GG. Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr Biol. 2009;19(13):1065–1074. doi:10.1016/j.cub.2009.05.065.
  • Chen S, Chen J, Shi H, Wei M, Castaneda-Castellanos DR, Bultje RS, Pei X, Kriegstein AR, Zhang M, Shi S-H. Regulation of microtubule stability and organization by mammalian Par3 in specifying neuronal polarity. Dev Cell. 2013;24(1):26–40. doi:10.1016/j.devcel.2012.11.014.
  • Jiang T, McKinley RFA, McGill MA, Angers S, Harris TJC. A Par-1-Par-3-Centrosome cell polarity pathway and its tuning for isotropic cell adhesion. Curr Biol. 2015;25(20):2701–2708. doi:10.1016/j.cub.2015.08.063.
  • Du D, Xu F, Yu L, Zhang C, Lu X, Yuan H, Huang Q, Zhang F, Bao H, Jia L, et al. The tight junction protein, occludin, regulates the directional migration of epithelial cells. Dev Cell. 2010;18(1):52–63. doi:10.1016/j.devcel.2009.12.008.
  • Chausovsky A, Bershadsky AD, Borisy GG. Cadherin-mediated regulation of microtubule dynamics. Nat Cell Biol. 2000;2(11):797–804. doi:10.1038/35041037.
  • Dupin I, Camand E, Etienne-Manneville S. Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol. 2009;185(5):779–786. doi:10.1083/jcb.200812034.
  • Shtutman M, Chausovsky A, Prager-Khoutorsky M, Schiefermeier N, Boguslavsky S, Kam Z, Fuchs E, Geiger B, Borisy GG, Bershadsky AD. Signaling function of alpha-catenin in microtubule regulation. Cell Cycle. 2008;7(15):2377–2383. doi:10.4161/cc.6362.
  • Huang P, Senga T, Hamaguchi M. A novel role of phospho-beta-catenin in microtubule regrowth at centrosome. Oncogene. 2007;26(30):4357–4371. doi:10.1038/sj.onc.1210217.
  • Bahmanyar S, Kaplan DD, Deluca JG, Giddings TH, O’Toole ET, Winey M, Salmon ED, Casey PJ, Nelson WJ, Barth AIM. beta-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev. 2008;22(1):91–105. doi:10.1101/gad.1596308.
  • Bahmanyar S, Guiney EL, Hatch EM, Nelson WJ, Barth AIM. Formation of extra centrosomal structures is dependent on beta-catenin. J Cell Sci. 2010;123(Pt 18):3125–3135. doi:10.1242/jcs.064782.
  • 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(10):913–917. doi:10.1038/ncb1001-913.
  • Franz CM, Ridley AJ. p120 catenin associates with microtubules: inverse relationship between microtubule binding and Rho GTPase regulation. J Biol Chem. 2004;279(8):6588–6594. doi: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(10):9512–9521. doi:10.1074/jbc.M310895200.
  • Ichii T, Takeichi M. p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells. 2007;12(7):827–839. doi:10.1111/j.1365-2443.2007.01095.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(6):1043–1061.
  • Paschoud S, Jond L, Guerrera D, Citi S. PLEKHA7 modulates epithelial tight junction barrier function. Tissue Barriers. 2014;2(2):e28755. doi:10.4161/tisb.28755.
  • Pulimeno P, Bauer C, Stutz J, Citi S, Arkowitz RA. PLEKHA7 is an adherens junction protein with a tissue distribution and subcellular localization distinct from ZO-1 and E-Cadherin. PLoS One. 2010;5(8):e12207. doi:10.1371/journal.pone.0012207.
  • Kurita S, Yamada T, Rikitsu E, Ikeda W, Takai Y. Binding between the junctional proteins afadin and PLEKHA7 and implication in the formation of adherens junction in epithelial cells. J Biol Chem. 2013;288(41):29356–29368. doi:10.1074/jbc.M113.453464.
  • Guerrera D, Shah J, Vasileva E, Sluysmans S, Méan I, Jond L, Poser I, Mann M, Hyman AA, Citi S. PLEKHA7 recruits PDZD11 to adherens junctions to stabilize nectins. J Biol Chem. 2016;291(21):11016–11029. doi:10.1074/jbc.M115.712935.
  • Shah J, Guerrera D, Vasileva E, Sluysmans S, Bertels E, Citi S. PLEKHA7: cytoskeletal adaptor protein at center stage in junctional organization and signaling. Int J Biochem Cell Biol. 2016;75:112–116. doi:10.1016/j.biocel.2016.04.001.
  • Franke WW, Cowin P, Schmelz M, Kapprell HP. The desmosomal plaque and the cytoskeleton. Ciba Found Symp. 1987;125:26–48.
  • Garrod D, Chidgey M. Desmosome structure, composition and function. Biochim Biophys Acta. 2008;1778(3):572–587. doi:10.1016/j.bbamem.2007.07.014.
  • Lechler T, Fuchs E. Desmoplakin: an unexpected regulator of microtubule organization in the epidermis. J Cell Biol. 2007;176(2):147–154. doi:10.1083/jcb.200609109.
  • Sumigray KD, Lechler T. Control of cortical microtubule organization and desmosome stability by centrosomal proteins. Bioarchitecture. 2011;1(5):221–224. doi:10.4161/bioa.18403.
  • Sluysmans S, Vasileva E, Spadaro D, Shah J, Rouaud F, Citi S. The role of apical cell-cell junctions and associated cytoskeleton in mechanotransduction. Biol Cell. 2017;109(4):139–161. doi:10.1111/boc.201600075.
  • 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(9):804–809. doi:10.1002/bies.201300045.
  • Runkle EA, Sundstrom JM, Runkle KB, Liu X, Antonetti DA. Occludin localizes to centrosomes and modifies mitotic entry. J Biol Chem. 2011;286(35):30847–30858. doi:10.1074/jbc.M111.262857.
  • Ren Y, Li R, Zheng Y, Busch H. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem. 1998;273(52):34954–34960.
  • Krendel M, Zenke FT, Bokoch GM. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol. 2002;4(4):294–301. doi:10.1038/ncb773.
  • Chang Y-C, Nalbant P, Birkenfeld J, Chang Z-F, Bokoch GM. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell. 2008;19(5):2147–2153. doi:10.1091/mbc.e07-12-1269.
  • Birukova AA, Adyshev D, Gorshkov B, Bokoch GM, Birukov KG, Verin AD. GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol. 2006;290(3):L540–8. doi:10.1152/ajplung.00259.2005.
  • Birukova AA, Fu P, Xing J, Yakubov B, Cokic I, Birukov KG. Mechanotransduction by GEF-H1 as a novel mechanism of ventilator-induced vascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol. 2010;298(6):L837–48. doi:10.1152/ajplung.00263.2009.
  • Itoh K, Ossipova O, Sokol SY. GEF-H1 functions in apical constriction and cell intercalations and is essential for vertebrate neural tube closure. J Cell Sci. 2014;127(Pt 11):2542–2553. doi:10.1242/jcs.146811.
  • Sandí M-J, Marshall CB, Balan M, Coyaud É, Zhou M, Monson DM, Ishiyama N, Chandrakumar AA, La Rose J, Couzens AL, et al. MARK3-mediated phosphorylation of ARHGEF2 couples microtubules to the actin cytoskeleton to establish cell polarity. Sci Signal. 2017;10(503):eaan3286. doi:10.1126/scisignal.aan3286.
  • Nie M, Aijaz S, Leefa Chong San IV, Balda MS, Matter K. The Y-box factor ZONAB/DbpA associates with GEF-H1/Lfc and mediates Rho-stimulated transcription. EMBO Rep. 2009;10(10):1125–1131. doi:10.1038/embor.2009.182.
  • Cullis J, Meiri D, Sandi MJ, Radulovich N, Kent OA, Medrano M, Mokady D, Normand J, Larose J, Marcotte R, et al. The RhoGEF GEF-H1 is required for oncogenic RAS signaling via KSR-1. Cancer Cell. 2014;25(2):181–195. doi:10.1016/j.ccr.2014.01.025.
  • Dubois F, Keller M, Calvayrac O, Soncin F, Hoa L, Hergovich A, Parrini M-C, Mazières J, Vaisse-Lesteven M, Camonis J, et al. RASSF1A suppresses the invasion and metastatic potential of human non-small cell lung cancer cells by inhibiting YAP activation through the GEF-H1/RhoB pathway. Cancer Res. 2016;76(6):1627–1640. doi:10.1158/0008-5472.CAN-15-1008.
  • Birkenfeld J, Nalbant P, Yoon S-H, Bokoch GM. Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? Trends Cell Biol. 2008;18:210–219. doi:10.1016/j.tcb.2008.02.006.
  • Zenke FT, Krendel M, DerMardirossian C, King CC, Bohl BP, Bokoch GM. p21-activated kinase 1 phosphorylates and regulates 14-3-3 binding to GEF-H1, a microtubule-localized Rho exchange factor. J Biol Chem. 2004;279(18):18392–18400. doi:10.1074/jbc.M400084200.
  • Meiri D, Greeve MA, Brunet A, Finan D, Wells CD, LaRose J, Rottapel R. Modulation of Rho guanine exchange factor Lfc activity by protein kinase A-mediated phosphorylation. Mol Cell Biol. 2009;29(21):5963–5973. doi:10.1128/MCB.01268-08.
  • Birkenfeld J, Nalbant P, Bohl BP, Pertz O, Hahn KM, Bokoch GM. GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev Cell. 2007;12(5):699–712. doi:10.1016/j.devcel.2007.03.014.
  • Aijaz S, D’Atri F, Citi S, Balda MS, Matter K. Binding of GEF-H1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition. Dev Cell. 2005;8(5):777–786. doi:10.1016/j.devcel.2005.03.003.
  • Guillemot L, Hammar E, Kaister C, Ritz J, Caille D, Jond L, Bauer C, Meda P, Citi S. Disruption of the cingulin gene does not prevent tight junction formation but alters gene expression. J Cell Sci. 2004;117(Pt 22):5245–5256. doi:10.1242/jcs.01399.
  • Guillemot L, Citi S. Cingulin regulates claudin-2 expression and cell proliferation through the small GTPase RhoA. Mol Biol Cell. 2006;17(8):3569–3577. doi:10.1091/mbc.e06-02-0122.
  • Guillemot L, Schneider Y, Brun P, Castagliuolo I, Pizzuti D, Martines D, Jond L, Bongiovanni M, Citi S. Cingulin is dispensable for epithelial barrier function and tight junction structure, and plays a role in the control of claudin-2 expression and response to duodenal mucosa injury. J Cell Sci. 2012;125:5005–5012. doi:10.1242/jcs.101261.
  • Tian Y, Gawlak G, Tian X, Shah AS, Sarich N, Citi S, Birukova AA. Cingulin role in agonist-induced vascular endothelial permeability. J Biol Chem. 2016;291:23681–23692. doi:10.1074/jbc.M116.720763.
  • Raya-Sandino A, Castillo-Kauil A, Domínguez-Calderón A, Alarcón L, Flores-Benitez D, Cuellar-Perez F, López-Bayghen B, Chávez-Munguía B, Vázquez-Prado J, González-Mariscal L. Zonula occludens-2 regulates Rho proteins activity and the development of epithelial cytoarchitecture and barrier function. Biochim Biophys Acta. 2017;1864(10):1714–1733. doi:10.1016/j.bbamcr.2017.05.016.
  • White EA, Glotzer M. Centralspindlin: at the heart of cytokinesis. Cytoskeleton (Hoboken). 2012;69(11):882–892. doi:10.1002/cm.21065.
  • Yuce O, Piekny A, Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol. 2005;170(4):571–582. doi:10.1083/jcb.200501097.
  • Su KC, Takaki T, Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev Cell. 2011;21(6):1104–1115. doi:10.1016/j.devcel.2011.11.003.
  • Breznau EB, Murt M, Blasius TL, Verhey KJ, Miller AL. The MgcRacGAP SxIP motif tethers Centralspindlin to microtubule plus ends in Xenopus laevis. J Cell Sci. 2017;130(10):1809–1821. doi:10.1242/jcs.195891.
  • 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):818–828. doi:10.1038/ncb2532.
  • Guillemot L, Guerrera D, Spadaro D, Tapia R, Jond L, Citi S. MgcRacGAP interacts with cingulin and paracingulin to regulate Rac1 activation and development of the tight junction barrier during epithelial junction assembly. Mol Biol Cell. 2014;25(13):1995–2005. doi:10.1091/mbc.E13-11-0680.
  • Breznau EB, Semack AC, Higashi T, Miller AL. MgcRacGAP restricts active RhoA at the cytokinetic furrow and both RhoA and Rac1 at cell-cell junctions in epithelial cells. Mol Biol Cell. 2015;26(13):2439–2455. doi:10.1091/mbc.E14-11-1553.
  • Coleman PR, Hahn CN, Grimshaw M, Lu Y, Li X, Brautigan PJ, Beck K, Stocker R, Vadas MA, Gamble JR. Stress-induced premature senescence mediated by a novel gene, SENEX, results in an anti-inflammatory phenotype in endothelial cells. Blood. 2010;116(19):4016–4024. doi:10.1182/blood-2009-11-252700.
  • Chang GHK, Lay AJ, Ting KK, Zhao Y, Coleman PR, Powter EE, Formaz-Preston A, Jolly CJ, Bower NI, Hogan BM, et al. ARHGAP18: an endogenous inhibitor of angiogenesis, limiting tip formation and stabilizing junctions. Small GTPases. 2014;5(3):1–15. doi:10.4161/21541248.2014.975002.
  • Aleskandarany MA, Sonbul S, Surridge R, Mukherjee A, Caldas C, Diez-Rodriguez M, Ashankyty I, Albrahim KI, Elmouna AM, Aneja R, et al. Rho-GTPase activating-protein 18: a biomarker associated with good prognosis in invasive breast cancer. Br J Cancer. 2017;117(8):1176–1184. doi:10.1038/bjc.2017.261.
  • Lovelace MD, Powter EE, Coleman PR, Zhao Y, Parker A, Chang GH, Lay AJ, Hunter J, McGrath AP, Jormakka M, et al. The RhoGAP protein ARHGAP18/SENEX localizes to microtubules and regulates their stability in endothelial cells. Mol Biol Cell. 2017;28(8):1066–1078. doi:10.1091/mbc.E16-05-0285.
  • Janke C, Montagnac G. Causes and consequences of microtubule acetylation. Curr Biol. 2017;27(23):R1287–R1292. doi:10.1016/j.cub.2017.10.044.
  • van Haren J, Boudeau J, Schmidt S, Basu S, Liu Z, Lammers D, Demmers J, Benhari J, Grosveld F, Debant A, et al. Dynamic microtubules catalyze formation of navigator-TRIO complexes to regulate neurite extension. Curr Biol. 2014;24(15):1778–1785. doi:10.1016/j.cub.2014.06.037.
  • Timmerman I, Heemskerk N, Kroon J, Schaefer A, van Rijssel J, Hoogenboezem M, van Unen J, Goedhart J, Gadella TWJ, Yin T, et al. A local VE-cadherin and Trio-based signaling complex stabilizes endothelial junctions through Rac1. J Cell Sci. 2015;128(18):3514. doi:10.1242/jcs.179424.
  • Yano T, Yamazaki Y, Adachi M, Okawa K, Fort P, Uji M, Tsukita S, Tsukita S. Tara up-regulates E-cadherin transcription by binding to the Trio RhoGEF and inhibiting Rac signaling. J Cell Biol. 2011;193(2):319–332. doi:10.1083/jcb.201009100.
  • Gumbiner BM. Carcinogenesis: a balance between beta-catenin and APC. Curr Biol. 1997;7(7):R443–6.
  • Munemitsu S, Souza B, Müller O, Albert I, Rubinfeld B, Polakis P. The APC gene product associates with microtubules in vivo and promotes their assembly in vitro. Cancer Res. 1994;54(14):3676–3681.
  • Zumbrunn J, Kinoshita K, Hyman AA, Näthke IS. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr Biol. 2001;11(1):44–49.
  • Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJS, Chen M, Wallar BJ, Alberts AS, Gundersen GG. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol. 2004;6(9):820–830. doi:10.1038/ncb1160.
  • Morrison EE. The APC-EB1 interaction. Adv Exp Med Biol. 2009;656:41–50.
  • Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell. 2004;7(6):871–883. doi:10.1016/j.devcel.2004.10.017.
  • Rosin-Arbesfeld R, Ihrke G, Bienz M. Actin-dependent membrane association of the APC tumour suppressor in polarized mammalian epithelial cells. Embo J. 2001;20(21):5929–5939. doi:10.1093/emboj/20.21.5929.
  • Langford KJ, Askham J, Lee T, Adams M, Morrison E. Examination of actin and microtubule dependent APC localisations in living mammalian cells. BMC Cell Biol. 2006;7:3. doi:10.1186/1471-2121-7-3.
  • Wu Y, Griffin EE. Regulation of Cell Polarity by PAR-1/MARK Kinase. Curr Top Dev Biol. 2017;123:365–397. doi:10.1016/bs.ctdb.2016.11.001.
  • Guo S, Kemphues KJ. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell. 1995;81(4):611–620.
  • Hurov J, Piwnica-Worms H. The Par-1/MARK family of protein kinases: from polarity to metabolism. Cell Cycle. 2007;6(16):1966–1969. doi:10.4161/cc.6.16.4576.
  • Drewes G, Ebneth A, Preuss U, Mandelkow EM, Mandelkow E. MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell. 1997;89(2):297–308.
  • Kuhns S, Schmidt KN, Reymann J, Gilbert DF, Neuner A, Hub B, Carvalho R, Wiedemann P, Zentgraf H, Erfle H, et al. The microtubule affinity regulating kinase MARK4 promotes axoneme extension during early ciliogenesis. J Cell Biol. 2013;200(4):505–522. doi:10.1083/jcb.201206013.
  • Suzuki A, Hirata M, Kamimura K, Maniwa R, Yamanaka T, Mizuno K, Kishikawa M, Hirose H, Amano Y, Izumi N, et al. aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Curr Biol. 2004;14(16):1425–1435. doi:10.1016/j.cub.2004.08.021.
  • Cohen D, Brennwald PJ, Rodriguez-Boulan E, Müsch A. Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton. J Cell Biol. 2004;164(5):717–727. doi:10.1083/jcb.200308104.
  • Cohen D, Tian Y, Musch A. Par1b promotes hepatic-type lumen polarity in Madin Darby canine kidney cells via myosin II- and E-cadherin-dependent signaling. Mol Biol Cell. 2007;18(6):2203–2215. doi:10.1091/mbc.e07-02-0095.
  • Ducharme NA, Hales CM, Lapierre LA, Ham A-JL, Oztan A, Apodaca G, Goldenring JR. MARK2/EMK1/Par-1Balpha phosphorylation of Rab11-family interacting protein 2 is necessary for the timely establishment of polarity in Madin-Darby canine kidney cells. Mol Biol Cell. 2006;17(8):3625–3637. doi:10.1091/mbc.e05-08-0736.
  • Cohen D, Fernandez D, Lázaro-Diéguez F, Müsch A. The serine/threonine kinase Par1b regulates epithelial lumen polarity via IRSp53-mediated cell-ECM signaling. J Cell Biol. 2011;192(3):525–540. doi:10.1083/jcb.201007002.
  • Yamahashi Y, Saito Y, Murata-Kamiya N, Hatakeyama M. Polarity-regulating kinase partitioning-defective 1b (PAR1b) phosphorylates guanine nucleotide exchange factor H1 (GEF-H1) to regulate RhoA-dependent actin cytoskeletal reorganization. J Biol Chem. 2011;286(52):44576–44584. doi:10.1074/jbc.M111.267021.
  • Li X, Thome S, Ma X, Amrute-Nayak M, Finigan A, Kitt L, Masters L, James JR, Shi Y, Meng G, et al. MARK4 regulates NLRP3 positioning and inflammasome activation through a microtubule-dependent mechanism. Nat Commun. 2017;8:15986. doi:10.1038/ncomms15986.
  • Heidary Arash E, Shiban A, Song S, Attisano L. MARK4 inhibits Hippo signaling to promote proliferation and migration of breast cancer cells. EMBO Rep. 2017;18(3):420–436. doi:10.15252/embr.201642455.
  • Werner ME, Mitchell JW, Putzbach W, Bacon E, Kim SK, Mitchell BJ. Radial intercalation is regulated by the Par complex and the microtubule-stabilizing protein CLAMP/Spef1. J Cell Biol. 2014;206(3):367–376. doi:10.1083/jcb.201312045.
  • Kim SK, Zhang S, Werner ME, Brotslaw EJ, Mitchell JW, Altabbaa MM, Mitchell BJ. CLAMP/Spef1 regulates planar cell polarity signaling and asymmetric microtubule accumulation in the Xenopus ciliated epithelia. J Cell Biol. 2018;217(5):1633–1641. doi:10.1083/jcb.201706058.