Touch, grasp, deliver and control: Functional cross-talk between microtubules and cell adhesions

Traffic

Volumn 10, Issue 3, 2009, Pages 268-274

  Akhmanova, Anna ^a   Stehbens, Samantha J ^b   Yap, Alpha S ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Adherens junctions; Cadherins; Focal adhesions; Microtubules

Indexed keywords

CELL ADHESION; CELL CONTACT; CELL MIGRATION; CELL MOTILITY; CELL POLARITY; CELL TRANSPORT; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; FOCAL ADHESION; METABOLIC REGULATION; MICROTUBULE; MICROTUBULE ASSEMBLY; MOLECULAR INTERACTION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BIOLOGICAL TRANSPORT; CELL ADHESION; MICROTUBULES; MODELS, BIOLOGICAL; SUBSTRATE SPECIFICITY;

EID: 59849100330     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00869.x     Document Type: Review

References (61)

1. Dammerman A, Desai A, Oegema K. The minus end in sight. Curr Biol 2003;13:R614-R624.
2. Schuyler SC, Pellman D. Microtubule "plus-end-tracking proteins": The end is just the beginning. Cell 2001;105:421-424.
3. Akhmanova A, Steinmetz MO. Tracking the ends: A dynamic protein network controls the fate of microtubule tips. Nat Rev Mol Cell Biol 2008;9:309-322.
4. Kaverina I, Rottner K, Small JV. Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 1998;142:181-190.
5. Ezratty EJ, Partridge MA, Gundersen GG. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 2005;7:581-590.
6. Krylyshkina O, Anderson KI, Kaverina I, Upmann I, Manstein DJ, Small JV, Toomre DK. Nanometer targeting of microtubules to focal adhesions. J Cell Biol 2003;161:853-859.
7. Efimov A, Schiefermeier N, Grigoriev I, Ohi R, Brown MC, Turner CE, Small JV, Kaverina I. Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites. J Cell Sci 2008;121:196-204.
8. Palazzo AF, Cook TA, Alberts AS, Gundersen GG. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat Cell Biol 2001;3:723-729.
9. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 2004;303:836-839.
10. Etienne-Manneville S, Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocyte through PKCz. Cell 2001;106:489-498.
11. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol 2005;170:895-901.
12. Bacallao R, Antony C, Karsenti E, Stelzer E, 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.
13. Bartolini F, Gundersen GG. Generation of noncentrosomal microtubule arrays. J Cell Sci 2006;119:4155-4163.
14. Ligon LA, Holzbaur EL. Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly. Traffic 2007;8:808-819.
15. Ligon LA, Karki S, Tokito M, Holzbaur EL. Dynein binds to beta-catenin and may tether microtubules at adherens junctions. Nat Cell Biol 2001;3:913-917.
16. 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;119:1801-1811.
17. Broussard JA, Webb DJ, Kaverina I. Asymmetric focal adhesion disassembly in motile cells. Curr Opin Cell Biol 2008;20:85-90.
18. Kaverina I, Krylyshkina O, Small JV. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 1999;146:1033-1044.
19. Wu X, Kodama A, Fuchs E. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008;135:137-148.
20. Zaoui K, Honore S, Isnardon D, Braguer D, Badache A. Memo-RhoA-mDia1 signaling controls microtubules, the actin network, and adhesion site formation in migrating cells. J Cell Biol 2008;183:401-408.
21. Kaverina I, Krylyshkina O, Gimona M, Beningo K, Wang YL, Small JV. Enforced polarisation and locomotion of fibroblasts lacking microtubules. Curr Biol 2000;10:739-742.
22. Shpetner HS, Vallee RB. Dynamin is a GTPase stimulated to high levels of activity by microtubules. Nature 1992;355:733-735.
23. Lee E, De Camilli P. Dynamin at actin tails. Proc Natl Acad Sci U S A 2002;99:161-166.
24. Birkenfeld J, Nalbant P, Yoon SH, 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.
25. Peacock JG, Miller AL, Bradley WD, Rodriguez OC, Webb DJ, Koleske AJ. The Abl-related gene tyrosine kinase acts through p190RhoGAP to inhibit actomyosin contractility and regulate focal adhesion dynamics upon adhesion to fibronectin. Mol Biol Cell 2007;18:3860-3872.
26. Meng W, Mushika Y, Ichii T, Takeichi M. Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 2008;135:948-959.
27. Mary S, Charrasse S, Meriane M, Comunale F, Travo P, Blangy A, Gauthier-Rouviere C. Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol Biol Cell 2002;13:285-301.
28. 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;16:4531-4532.
29. Scott JA, Shewan AM, den Elzen NR, Loureiro JJ, Gertler FB, Yap AS. Ena/ VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol Biol Cell 2006;17:1085-1095.
30. Pearson CG, Bloom K. Dynamic microtubules lead the way for spindle positioning. Nat Rev Mol Cell Biol 2004;5:481-492.
31. Kaverina I, Krylyshkina O, Beningo K, Anderson K, Wang YL, Small JV. Tensile stress stimulates microtubule outgrowth in living cells. J Cell Sci 2002;115:2283-2291.
32. Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E. ACF7: An essential integrator of microtubule dynamics. Cell 2003;115:343-354.
33. Lechler T, Fuchs E. Desmoplakin: An unexpected regulator of microtubule organization in the epidermis. J Cell Biol 2007;176:147-154.
34. Franz CM, Ridley AJ. p120 catenin associates with microtubules: Inverse relationship between microtubule binding and Rho GTPase regulation. J Biol Chem 2004;279:6588-6594.
35. Brown MC, Turner CE. Roles for the tubulin- and PTP-PEST-binding paxillin LIM domains in cell adhesion and motility. Int J Biochem Cell Biol 2002;34:855-863.
36. Mimori-Kiyosue Y, Grigoriev I, Lansbergen G, Sasaki H, Matsui C, Severin F, Galjart N, Grosveld F, Vorobjev I, Tsukita S, Akhmanova A. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J Cell Biol 2005;168:141-153.
37. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. IQGAP1: A key regulator of adhesion and migration. J Cell Sci 2005;118:2085-2092.
38. Carramusa L, Ballestrem C, Zilberman Y, Bershadsky AD. Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J Cell Sci 2007;120:3870-3882.
39. Bershadsky AD, Ballestrem C, Carramusa L, Zilberman Y, Gilquin B, Khochbin S, Alexandrova AY, Verkhovsky AB, Shemesh T, Kozlov MM. Assembly and mechanosensory function of focal adhesions: Experiments and models. Eur J Cell Biol 2006;85:165-173.
40. Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 2008;181:523-536.
41. Matsui C, Kaieda S, Ikegami T, Mimori-Kiyosue Y. Identification of a link between the SAMP repeats of APC (adenomatous polyposis coli) tumor suppressor and the SH3 domain of DDEF. J Biol Chem 2008;283:33006-33020.
42. Lansbergen G, Grigoriev I, Mimori-Kiyosue Y, Ohtsuka T, Higa S, Kitajima I, Demmers J, Galjart N, Houtsmuller AB, Grosveld F, Akhmanova A. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev Cell 2006;11:21-32.
43. Wittmann T, Bokoch GM, Waterman-Storer CM. Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem 2004;279:6196-6203.
44. Xu FL, Saunders WS. Actin and microtubules: Working together to control spindle polarity. Cancer Cell 2008;14:197-199.
45. Krylyshkina O, Kaverina I, Kranewitter W, Steffen W, Alonso MC, Cross RA, Small JV. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J Cell Biol 2002;156:349-359.
46. Chen X, Kojima S, Borisy GG, Green KJ. p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J Cell Biol 2003;163:547-557.
47. Arregui CO, Balsamo J, Lilien J. Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant-negative mutant PTP1B. J Cell Biol 1998;143:861-873.
48. Hernandez MV, Sala MG, Balsamo J, Lilien J, Arregui CO. ER-bound PTP1B is targeted to newly forming cell-matrix adhesions. J Cell Sci 2006;119:1233-1243.
49. Hammond JW, Cai D, Verhey KJ. Tubulin modifications and their cellular functions. Curr Opin Cell Biol 2008;20:71-76.
50. Odell GM, Foe VE. An agent-based model contrasts opposite effects of dynamic and stable microtubules on cleavage furrow positioning. J Cell Biol 2008;183:471-483.
51. Yuce O, Piekny A, Glotzer M. An ECT2-centralspindlin complex regulates the localization and function of RhoA. J Cell Biol 2005;170:571-582.
52. Nishimura Y, Yonemura S. Centralspindlin regulates ECT2 and RhoA accumulation at the equatorial cortex during cytokinesis. J Cell Sci 2006;119:104-114.
53. Krendel M, Zenke FT, Bokoch GM. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 2002;4:294-301.
54. 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;18:3429-3439.
55. Basu R, Chang F. Shaping the actin cytoskeleton using microtubule tips. Curr Opin Cell Biol 2007;19:88-94.
56. Wittmann T, Waterman-Storer CM. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J Cell Biol 2005;169:929-939.
57. Dragestein KA, van Cappellen WA, van Haren J, Tsibidis GD, Akhmanova A, Knoch TA, Grosveld F, Galjart N. Dynamic behavior of GFP-CLIP-170 reveals fast protein turnover on microtubule plus ends. J Cell Biol 2008;180:729-737.
58. Rogers SL, Wiedemann U, Hacker U, Turck C, Vale RD. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol 2004;14:1827-1833.
59. Harris TJ, Peifer M. aPKC controls microtubule organization to balance adherens junction symmetry and planar polarity during development. Dev Cell 2007;12:727-738.
60. Nejsum LN, Nelson WJ. A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity. J Cell Biol 2007;178:323-335.
61. Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 2007;128:547-560.