Targeting and transport: How microtubules control focal adhesion dynamics

Journal of Cell Biology

Volumn 198, Issue 4, 2012, Pages 481-489

  Stehbens, Samantha ^a   Wittmann, Torsten ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; APC PROTEIN; CLATHRIN; CYTOPLASMIC LINKER ASSOCIATED PROTEIN; F ACTIN; GLYCOGEN SYNTHASE KINASE 3BETA; INTEGRIN; MATRIX METALLOPROTEINASE; PAXILLIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

CELL ADHESION; CELL MIGRATION; CYTOSKELETON; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXOCYTOSIS; EXTRACELLULAR MATRIX; MICROTUBULE; PRIORITY JOURNAL; REVIEW; RNA INTERFERENCE;

ANIMALS; ENDOCYTOSIS; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HUMANS; MICROTUBULES; SIGNAL TRANSDUCTION;

EID: 84866397855     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201206050     Document Type: Review

References (111)

1. Akhmanova, A., and M.O. Steinmetz. 2008. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9:309-322. http://dx.doi.org/10.1038/nrm2369
2. Akhmanova, A., C.C. Hoogenraad, K. Drabek, T. Stepanova, B. Dortland, T. Verkerk, W. Vermeulen, B.M. Burgering, C.I. De Zeeuw, F. Grosveld, and N. Galjart. 2001. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell. 104:923-935. http://dx.doi.org/10.1016/S0092-8674(01)00288-4
3. Aoki, K., and M.M. Taketo. 2007. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene. J. Cell Sci. 120:3327-3335. http://dx.doi.org/10.1242/jcs.03485
4. Applewhite, D.A., K.D. Grode, D. Keller, A.D. Zadeh, K.C. Slep, and S.L. Rogers. 2010. The spectraplakin Short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol. Biol. Cell. 21:1714-1724. (published erratum appears in Mol. Biol. Cell. 2010. 21:2097) http://dx.doi.org/10.1091/mbc.E10-01-0011
5. Arjonen, A., J. Alanko, S. Veltel, and J. Ivaska. 2012. Distinct recycling of active and inactive β1 integrins. Traffic. In press.
6. Barth, A.I., H.Y. Caro-Gonzalez, and W.J. Nelson. 2008. Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin. Cell Dev. Biol. 19:245-251. http://dx.doi.org/10.1016/j.semcdb.2008.02.003
7. Bate, N., A.R. Gingras, A. Bachir, R. Horwitz, F. Ye, B. Patel, B.T. Goult, and D.R. Critchley. 2012. Talin contains a C-terminal calpain2 cleavage site important in focal adhesion dynamics. PLoS ONE. 7:e34461. http://dx.doi.org/10.1371/journal.pone.0034461
8. Bhatt, A., I. Kaverina, C. Otey, and A. Huttenlocher. 2002. Regulation of focal complex composition and disassembly by the calcium-dependent protease calpain. J. Cell Sci. 115:3415-3425.
9. Bowen, J.R., D. Hwang, X. Bai, D. Roy, and E.T. Spiliotis. 2011. Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J. Cell Biol. 194:187-197. http://dx.doi.org/10.1083/jcb.201102076
10. Brandt, D.T., S. Marion, G. Griffiths, T. Watanabe, K. Kaibuchi, and R. Grosse. 2007. Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J. Cell Biol. 178:193-200. http://dx.doi.org/10.1083/jcb.200612071
11. Breitsprecher, D., R. Jaiswal, J.P. Bombardier, C.J. Gould, J. Gelles, and B.L. Goode. 2012. Rocket launcher mechanism of collaborative actin assembly defined by single-molecule imaging. Science. 336:1164-1168. http://dx.doi.org/10.1126/science.1218062
12. Bretscher, M.S. 1989. Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8:1341-1348.
13. Broussard, J.A., D.J. Webb, and I. Kaverina. 2008. Asymmetric focal adhesion disassembly in motile cells. Curr. Opin. Cell Biol. 20:85-90. http://dx.doi.org/10.1016/j.ceb.2007.10.009
14. Burnette, D.T., L. Ji, A.W. Schaefer, N.A. Medeiros, G. Danuser, and P. Forscher. 2008. Myosin II activity facilitates microtubule bundling in the neuronal growth cone neck. Dev. Cell. 15:163-169. http://dx.doi.org/10.1016/j.devcel.2008.05.016
15. Calderwood, D.A., Y. Fujioka, J.M. de Pereda, B. García-Alvarez, T. Nakamoto, B. Margolis, C.J. McGlade, R.C. Liddington, and M.H. Ginsberg. 2003. Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA. 100:2272-2277. http://dx.doi.org/10.1073/pnas.262791999
16. Callow, M.G., S. Zozulya, M.L. Gishizky, B. Jallal, and T. Smeal. 2005. PAK4 mediates morphological changes through the regulation of GEF-H1. J. Cell Sci. 118:1861-1872. http://dx.doi.org/10.1242/jcs.02313
17. Canman, J.C. 2009. Cytokinetic astralogy. J. Cell Biol. 187:757-759. http://dx.doi.org/10.1083/jcb.200911084
18. Carter, W.G., E.A. Wayner, T.S. Bouchard, and P. Kaur. 1990. The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J. Cell Biol. 110:1387-1404. http://dx.doi.org/10.1083/jcb.110.4.1387
19. Caswell, P.T., S. Vadrevu, and J.C. Norman. 2009. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 10:843-853. http://dx.doi.org/10.1038/nrm2799
20. Chang, Y.C., P. Nalbant, J. Birkenfeld, Z.F. Chang, and G.M. Bokoch. 2008. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol. Biol. Cell. 19:2147-2153. http://dx.doi.org/10.1091/mbc.E07-12-1269
21. Chao, W.T., and J. Kunz. 2009. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett. 583:1337-1343. http://dx.doi.org/10.1016/j.febslet.2009.03.037
22. Chao, W.T., F. Ashcroft, A.C. Daquinag, T. Vadakkan, Z. Wei, P. Zhang, M.E. Dickinson, and J. Kunz. 2010. Type I phosphatidylinositol phosphate kinase beta regulates focal adhesion disassembly by promoting beta1 integrin endocytosis. Mol. Cell. Biol. 30:4463-4479. http://dx.doi.org/10.1128/MCB.01207-09
23. Cortesio, C.L., L.R. Boateng, T.M. Piazza, D.A. Bennin, and A. Huttenlocher. 2011. Calpain-mediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J. Biol. Chem. 286:9998-10006. http://dx.doi.org/10.1074/jbc.M110.187294
24. Drabek, K., M. van Ham, T. Stepanova, K. Draegestein, R. van Horssen, C.L. Sayas, A. Akhmanova, T. Ten Hagen, R. Smits, R. Fodde, et al. 2006. Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr. Biol. 16:2259-2264. http://dx.doi.org/10.1016/j.cub.2006.09.065
25. Echarri, A., and M.A. Del Pozo. 2006. Caveolae internalization regulates integrin-dependent signaling pathways. Cell Cycle. 5:2179-2182. http://dx.doi.org/10.4161/cc.5.19.3264
26. Efimov, A., N. Schiefermeier, I. Grigoriev, R. Ohi, M.C. Brown, C.E. Turner, J.V. Small, and I. Kaverina. 2008. Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites. J. Cell Sci. 121:196-204. (published erratum appears in J. Cell Sci. 121:405) http://dx.doi.org/10.1242/jcs.012666
27. Eng, C.H., T.M. Huckaba, and G.G. Gundersen. 2006. The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol. Biol. Cell. 17:5004-5016. http://dx.doi.org/10.1091/mbc.E05-10-0914
28. Etienne-Manneville, S., J.B. Manneville, S. Nicholls, M.A. Ferenczi, and A. Hall. 2005. Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J. Cell Biol. 170:895-901. http://dx.doi.org/10.1083/jcb.200412172
29. Ezratty, E.J., M.A. Partridge, and G.G. Gundersen. 2005. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7:581-590. http://dx.doi.org/10.1038/ncb1262
30. Ezratty, E.J., C. Bertaux, E.E. Marcantonio, and G.G. Gundersen. 2009. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J. Cell Biol. 187:733-747. http://dx.doi.org/10.1083/jcb.200904054
31. Ferguson, S.M., and P. De Camilli. 2012. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13:75-88.
32. Franco, S.J., M.A. Rodgers, B.J. Perrin, J. Han, D.A. Bennin, D.R. Critchley, and A. Huttenlocher. 2004. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 6:977-983. http://dx.doi.org/10.1038/ncb1175
33. Gao, C., and Y.G. Chen. 2010. Dishevelled: The hub of Wnt signaling. Cell. Signal. 22:717-727. http://dx.doi.org/10.1016/j.cellsig.2009.11.021
34. Gierke, S., and T. Wittmann. 2012. EB1-recruited microtubule +TIP complexes coordinate protrusion dynamics during 3D epithelial remodeling. Curr. Biol. 22:753-762. http://dx.doi.org/10.1016/j.cub.2012.02.069
35. Grigoriev, I., G. Borisy, and I. Vorobjev. 2006. Regulation of microtubule dynamics in 3T3 fibroblasts by Rho family GTPases. Cell Motil. Cytoskeleton. 63:29-40. http://dx.doi.org/10.1002/cm.20107
36. Gu, Z., E.H. Noss, V.W. Hsu, and M.B. Brenner. 2011. Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J. Cell Biol. 193:61-70. http://dx.doi.org/10.1083/jcb.201007003
37. Guilluy, C., V. Swaminathan, R. Garcia-Mata, E.T. O'Brien, R. Superfine, and K. Burridge. 2011. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat. Cell Biol. 13:722-727. http://dx.doi.org/10.1038/ncb2254
38. Horgan, C.P., and M.W. McCaffrey. 2011. Rab GTPases and microtubule motors. Biochem. Soc. Trans. 39:1202-1206. http://dx.doi.org/10.1042/BST0391202
39. Hotta, A., T. Kawakatsu, T. Nakatani, T. Sato, C. Matsui, T. Sukezane, T. Akagi, T. Hamaji, I. Grigoriev, A. Akhmanova, et al. 2010. Laminin-based cell adhesion anchors microtubule plus ends to the epithelial cell basal cortex through LL5alpha/beta. J. Cell Biol. 189:901-917. http://dx.doi.org/10.1083/jcb.200910095
40. Huang, C., Z. Rajfur, N. Yousefi, Z. Chen, K. Jacobson, and M.H. Ginsberg. 2009. Talin phosphorylation by Cdk5 regulates Smurf1-mediated talin head ubiquitylation and cell migration. Nat. Cell Biol. 11:624-630. http://dx.doi.org/10.1038/ncb1868
41. Humphries, J.D., A. Byron, M.D. Bass, S.E. Craig, J.W. Pinney, D. Knight, and M.J. Humphries. 2009. Proteomic analysis of integrin-associated complexes identifies RCC2 as a dual regulator of Rac1 and Arf6. Sci. Signal. 2:ra51. http://dx.doi.org/10.1126/scisignal.2000396
42. Iizuka-Kogo, A., A. Shimomura, and T. Senda. 2005. Colocalization of APC and DLG at the tips of cellular protrusions in cultured epithelial cells and its dependency on cytoskeletons. Histochem. Cell Biol. 123:67-73. http://dx.doi.org/10.1007/s00418-004-0729-2
43. Jaulin, F., and G. Kreitzer. 2010. KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J. Cell Biol. 190:443-460. http://dx.doi.org/10.1083/jcb.201006044
44. Kanchanawong, P., G. Shtengel, A.M. Pasapera, E.B. Ramko, M.W. Davidson, H.F. Hess, and C.M. Waterman. 2010. Nanoscale architecture of integrinbased cell adhesions. Nature. 468:580-584. http://dx.doi.org/10.1038/nature09621
45. Karakesisoglou, I., Y. Yang, and E. Fuchs. 2000. An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J. Cell Biol. 149:195-208. http://dx.doi.org/10.1083/jcb.149.1.195
46. Kaverina, I., K. Rottner, and J.V. Small. 1998. Targeting, capture, and stabilization of microtubules at early focal adhesions. J. Cell Biol. 142:181-190. http://dx.doi.org/10.1083/jcb.142.1.181
47. Kaverina, I., O. Krylyshkina, and J.V. Small. 1999. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146:1033-1044. http://dx.doi.org/10.1083/jcb.146.5.1033
48. Kaverina, I., O. Krylyshkina, K. Beningo, K. Anderson, Y.L. Wang, and J.V. Small. 2002. Tensile stress stimulates microtubule outgrowth in living cells. J. Cell Sci. 115:2283-2291.
49. Kessenbrock, K., V. Plaks, and Z. Werb. 2010. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 141:52-67. http://dx.doi.org/10.1016/j.cell.2010.03.015
50. Kirschner, M., and T. Mitchison. 1986. Beyond self-assembly: from micro-tubules to morphogenesis. Cell. 45:329-342. http://dx.doi.org/10.1016/0092-8674(86)90318-1
51. Kiss, A.L. 2012. Caveolae and the regulation of endocytosis. Adv. Exp. Med. Biol. 729:14-28. http://dx.doi.org/10.1007/978-1-4614-1222-9_2
52. Kita, K., T. Wittmann, I.S. Näthke, and C.M. Waterman-Storer. 2006. Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol. Biol. Cell. 17:2331-2345. http://dx.doi.org/10.1091/mbc.E05-06-0498
53. Kodama, A., I. Karakesisoglou, E. Wong, A. Vaezi, and E. Fuchs. 2003. ACF7: an essential integrator of microtubule dynamics. Cell. 115:343-354. http://dx.doi.org/10.1016/S0092-8674(03)00813-4
54. Krendel, M., F.T. Zenke, and G.M. Bokoch. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4:294-301. http://dx.doi.org/10.1038/ncb773
55. Krylyshkina, O., I. Kaverina, W. Kranewitter, W. Steffen, M.C. Alonso, R.A. Cross, and J.V. Small. 2002. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J. Cell Biol. 156:349-359. http://dx.doi.org/10.1083/jcb.200105051
56. Krylyshkina, O., K.I. Anderson, I. Kaverina, I. Upmann, D.J. Manstein, J.V. Small, and D.K. Toomre. 2003. Nanometer targeting of micro-tubules to focal adhesions. J. Cell Biol. 161:853-859. http://dx.doi.org/10.1083/jcb.200301102
57. Kumar, P., and T. Wittmann. 2012. +TIPs: SxIPping along microtubule ends. Trends Cell Biol. 22:418-428. http://dx.doi.org/10.1016/j.tcb.2012.05.005
58. Kumar, P., K.S. Lyle, S. Gierke, A. Matov, G. Danuser, and T. Wittmann. 2009. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 184:895-908. http://dx.doi.org/10.1083/jcb.200901042
59. Kuo, J.C., X. Han, C.T. Hsiao, J.R. Yates III, and C.M. Waterman. 2011. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13:383-393. http://dx.doi.org/10.1038/ncb2216
60. Lansbergen, G., I. Grigoriev, Y. Mimori-Kiyosue, T. Ohtsuka, S. Higa, I. Kitajima, J. Demmers, N. Galjart, A.B. Houtsmuller, F. Grosveld, and A. Akhmanova. 2006. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev. Cell. 11:21-32. http://dx.doi.org/10.1016/j.devcel.2006.05.012
61. Lewis, A., H. Davis, M. Deheragoda, P. Pollard, E. Nye, R. Jeffery, S. Segditsas, P. East, R. Poulsom, G. Stamp, et al. 2012. The C-terminus of Apc does not influence intestinal adenoma development or progression. J. Pathol. 226:73-83. http://dx.doi.org/10.1002/path.2972
62. Machacek, M., L. Hodgson, C. Welch, H. Elliott, O. Pertz, P. Nalbant, A. Abell, G.L. Johnson, K.M. Hahn, and G. Danuser. 2009. Coordination of Rho GTPase activities during cell protrusion. Nature. 461:99-103. http://dx.doi.org/10.1038/nature08242
63. Margadant, C., H.N. Monsuur, J.C. Norman, and A. Sonnenberg. 2011. Mechanisms of integrin activation and trafficking. Curr. Opin. Cell Biol. 23:607-614. http://dx.doi.org/10.1016/j.ceb.2011.08.005
64. Matsumoto, S., K. Fumoto, T. Okamoto, K. Kaibuchi, and A. Kikuchi. 2010. Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J. 29:1192-1204. http://dx.doi.org/10.1038/emboj.2010.26
65. Meenderink, L.M., L.M. Ryzhova, D.M. Donato, D.F. Gochberg, I. Kaverina, and S.K. Hanks. 2010. P130Cas Src-binding and substrate domains have distinct roles in sustaining focal adhesion disassembly and promoting cell migration. PLoS ONE. 5:e13412. http://dx.doi.org/10.1371/journal.pone.0013412
66. Meiri, D., C.B. Marshall, M.A. Greeve, B. Kim, M. Balan, F. Suarez, C. Bakal, C. Wu, J. Larose, N. Fine, et al. 2012. Mechanistic insight into the micro-tubule and actin cytoskeleton coupling through dynein-dependent RhoGEF inhibition. Mol. Cell. 45:642-655. (published erratum appears in Mol. Cell. 2012. 45:844) http://dx.doi.org/10.1016/j.molcel.2012.01.027
67. Mimori-Kiyosue, Y., N. Shiina, and S. Tsukita. 2000. Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J. Cell Biol. 148:505-518. http://dx.doi.org/10.1083/jcb.148.3.505
68. Mimori-Kiyosue, Y., I. Grigoriev, G. Lansbergen, H. Sasaki, C. Matsui, F. Severin, N. Galjart, F. Grosveld, I. Vorobjev, S. Tsukita, and A. Akhmanova. 2005. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168:141-153. http://dx.doi.org/10.1083/jcb.200405094
69. Montenegro-Venegas, C., E. Tortosa, S. Rosso, D. Peretti, F. Bollati, M. Bisbal, I. Jausoro, J. Avila, A. Cáceres, and C. Gonzalez-Billault. 2010. MAP1B regulates axonal development by modulating Rho-GTPase Rac1 activity. Mol. Biol. Cell. 21:3518-3528. http://dx.doi.org/10.1091/mbc.E09-08-0709
70. Nalbant, P., Y.C. Chang, J. Birkenfeld, Z.F. Chang, and G.M. Bokoch. 2009. Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol. Biol. Cell. 20:4070-4082. http://dx.doi.org/10.1091/mbc.E09-01-0041
71. Näthke, I.S., C.L. Adams, P. Polakis, J.H. Sellin, and W.J. Nelson. 1996. The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J. Cell Biol. 134:165-179. http://dx.doi.org/10.1083/jcb.134.1.165
72. Nishimura, T., and K. Kaibuchi. 2007. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell. 13:15-28. http://dx.doi.org/10.1016/j.devcel.2007.05.003
73. Okada, K., F. Bartolini, A.M. Deaconescu, J.B. Moseley, Z. Dogic, N. Grigorieff, G.G. Gundersen, and B.L. Goode. 2010. Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J. Cell Biol. 189:1087-1096. http://dx.doi.org/10.1083/jcb.201001016
74. Palazzo, A.F., C.H. Eng, D.D. Schlaepfer, E.E. Marcantonio, and G.G. Gundersen. 2004. Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science. 303:836-839. http://dx.doi.org/10.1126/science.1091325
75. Paranavitane, V., W.J. Coadwell, A. Eguinoa, P.T. Hawkins, and L. Stephens. 2003. LL5beta is a phosphatidylinositol (3,4,5)-trisphosphate sensor that can bind the cytoskeletal adaptor, gamma-filamin. J. Biol. Chem. 278:1328-1335. http://dx.doi.org/10.1074/jbc.M208352200
76. Parsons, J.T., A.R. Horwitz, and M.A. Schwartz. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11:633-643. http://dx.doi.org/10.1038/nrm2957
77. Petrie, R.J., N. Gavara, R.S. Chadwick, and K.M. Yamada. 2012. Nonpolarized signaling reveals two distinct modes of 3D cell migration. J. Cell Biol. 197:439-455. http://dx.doi.org/10.1083/jcb.201201124
78. Piekny, A., M. Werner, and M. Glotzer. 2005. Cytokinesis: welcome to the Rho zone. Trends Cell Biol. 15:651-658. http://dx.doi.org/10.1016/j.tcb.2005.10.006
79. Ren, Y., R. Li, Y. Zheng, and H. Busch. 1998. Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273:34954-34960. http://dx.doi.org/10.1074/jbc.273.52.34954
80. Ren, X.D., W.B. Kiosses, and M.A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18:578-585. http://dx.doi.org/10.1093/emboj/18.3.578
81. Rid, R., N. Schiefermeier, I. Grigoriev, J.V. Small, and I. Kaverina. 2005. The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil. Cytoskeleton. 61:161-171. http://dx.doi.org/10.1002/cm.20076
82. Rinnerthaler, G., B. Geiger, and J.V. Small. 1988. Contact formation during fibroblast locomotion: involvement of membrane ruffles and microtubules. J. Cell Biol. 106:747-760. http://dx.doi.org/10.1083/jcb.106.3.747
83. Rodriguez, O.C., A.W. Schaefer, C.A. Mandato, P. Forscher, W.M. Bement, and C.M. Waterman-Storer. 2003. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5:599-609. http://dx.doi.org/10.1038/ncb0703-599
84. Rogers, S.L., U. Wiedemann, U. Häcker, C. Turck, and R.D. Vale. 2004. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 14:1827-1833. http://dx.doi.org/10.1016/j.cub.2004.09.078
85. Rooney, C., G. White, A. Nazgiewicz, S.A. Woodcock, K.I. Anderson, C. Ballestrem, and A. Malliri. 2010. The Rac activator STEF (Tiam2) regulates cell migration by microtubule-mediated focal adhesion disassembly. EMBO Rep. 11:292-298. http://dx.doi.org/10.1038/embor.2010.10
86. Salmon, W.C., M.C. Adams, and C.M. Waterman-Storer. 2002. Dual-wavelength fluorescent speckle microscopy reveals coupling of microtubule and actin movements in migrating cells. J. Cell Biol. 158:31-37. http://dx.doi.org/10.1083/jcb.200203022
87. Schober, M., S. Raghavan, M. Nikolova, L. Polak, H.A. Pasolli, H.E. Beggs, L.F. Reichardt, and E. Fuchs. 2007. Focal adhesion kinase modulates tension signaling to control actin and focal adhesion dynamics. J. Cell Biol. 176:667-680. http://dx.doi.org/10.1083/jcb.200608010
88. Shi, F., and J. Sottile. 2011. MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin. J. Cell Sci. 124:4039-4050. http://dx.doi.org/10.1242/jcs.087858
89. Small, J.V., and I. Kaverina. 2003. Microtubules meet substrate adhesions to arrange cell polarity. Curr. Opin. Cell Biol. 15:40-47. http://dx.doi.org/10.1016/S0955-0674(02)00008-X
90. Suozzi, K.C., X. Wu, and E. Fuchs. 2012. Spectraplakins: Master orchestrators of cytoskeletal dynamics. J. Cell Biol. 197:465-475. http://dx.doi.org/10.1083/jcb.201112034
91. Takino, T., Y. Watanabe, M. Matsui, H. Miyamori, T. Kudo, M. Seiki, and H. Sato. 2006. Membrane-type 1 matrix metalloproteinase modulates focal adhesion stability and cell migration. Exp. Cell Res. 312:1381-1389. http://dx.doi.org/10.1016/j.yexcr.2006.01.008
92. Takino, T., H. Saeki, H. Miyamori, T. Kudo, and H. Sato. 2007. Inhibition of membrane-type 1 matrix metalloproteinase at cell-matrix adhesions. Cancer Res. 67:11621-11629. http://dx.doi.org/10.1158/0008-5472. CAN-07-5251
93. Vasiliev, J.M., I.M. Gelfand, L.V. Domnina, O.Y. Ivanova, S.G. Komm, and L.V. Olshevskaja. 1970. Effect of colcemid on the locomotory behaviour of fibroblasts. J. Embryol. Exp. Morphol. 24:625-640.
94. Wang, Y., and M.A. McNiven. 2012. Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 196:375-385. http://dx.doi.org/10.1083/jcb.201105153
95. Wang, Y., H. Cao, J. Chen, and M.A. McNiven. 2011. A direct interaction between the large GTPase dynamin-2 and FAK regulates focal adhesion dynamics in response to active Src. Mol. Biol. Cell. 22:1529-1538. http://dx.doi.org/10.1091/mbc.E10-09-0785
96. Watanabe, T., S. Wang, J. Noritake, K. Sato, M. Fukata, M. Takefuji, M. Nakagawa, N. Izumi, T. Akiyama, and K. Kaibuchi. 2004. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev. Cell. 7:871-883. http://dx.doi.org/10.1016/j.devcel.2004.10.017
97. Watanabe, T., J. Noritake, M. Kakeno, T. Matsui, T. Harada, S. Wang, N. Itoh, K. Sato, K. Matsuzawa, A. Iwamatsu, et al. 2009. Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J. Cell Sci. 122:2969-2979. http://dx.doi.org/10.1242/jcs.046649
98. Waterman-Storer, C.M., R.A. Worthylake, B.P. Liu, K. Burridge, and E.D. Salmon. 1999. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1:45-50. http://dx.doi.org/10.1038/9018
99. Wehrle-Haller, B. 2012. Structure and function of focal adhesions. Curr. Opin. Cell Biol. 24:116-124. http://dx.doi.org/10.1016/j.ceb.2011.11.001
100. Wen, Y., C.H. Eng, J. Schmoranzer, N. Cabrera-Poch, E.J. Morris, M. Chen, B.J. Wallar, A.S. Alberts, and G.G. Gundersen. 2004. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat. Cell Biol. 6:820-830. http://dx.doi.org/10.1038/ncb1160
101. Wickström, S.A., A. Lange, M.W. Hess, J. Polleux, J.P. Spatz, M. Krüger, K. Pfaller, A. Lambacher, W. Bloch, M. Mann, et al. 2010a. Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev. Cell. 19:574-588. http://dx.doi.org/10.1016/j.devcel.2010.09.007
102. Wickström, S.A., A. Lange, E. Montanez, and R. Fässler. 2010b. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 29:281-291. http://dx.doi.org/10.1038/emboj.2009.376
103. Wiesner, C., J. Faix, M. Himmel, F. Bentzien, and S. Linder. 2010. KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macro-phages. Blood. 116:1559-1569. http://dx.doi.org/10.1182/blood-2009-12-257089
104. Wittmann, T., and C.M. Waterman-Storer. 2001. Cell motility: can Rho GTPases and microtubules point the way? J. Cell Sci. 114:3795-3803.
105. Wittmann, T., and C.M. Waterman-Storer. 2005. Spatial regulation of CLASP affinity for microtubules by Rac1 and GSK3beta in migrating epithelial cells. J. Cell Biol. 169:929-939. http://dx.doi.org/10.1083/jcb.200412114
106. Wittmann, T., G.M. Bokoch, and C.M. Waterman-Storer. 2003. Regulation of leading edge microtubule and actin dynamics downstream of Rac1. J. Cell Biol. 161:845-851. http://dx.doi.org/10.1083/jcb.200303082
107. Wolfenson, H., Y.I. Henis, B. Geiger, and A.D. Bershadsky. 2009. The heel and toe of the cell's foot: a multifaceted approach for understanding the structure and dynamics of focal adhesions. Cell Motil. Cytoskeleton. 66: 1017-1029. http://dx.doi.org/10.1002/cm.20410
108. Wu, B., B. Decourt, M.A. Zabidi, L.T. Wuethrich, W.H. Kim, Z. Zhou, K. MacIsaac, and D.M. Suter. 2008a. Microtubule-mediated Src tyrosine kinase trafficking in neuronal growth cones. Mol. Biol. Cell. 19:4611-4627. http://dx.doi.org/10.1091/mbc.E08-06-0603
109. Wu, X., A. Kodama, and E. Fuchs. 2008b. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell. 135: 137-148. http://dx.doi.org/10.1016/j.cell.2008.07.045
110. Wu, X., Q.T. Shen, D.S. Oristian, C.P. Lu, Q. Zheng, H.W. Wang, and E. Fuchs. 2011. Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3β. Cell. 144:341-352. http://dx.doi.org/10.1016/j.cell.2010.12.033
111. Zaoui, K., K. Benseddik, P. Daou, D. Salaün, and A. Badache. 2010. ErbB2 receptor controls microtubule capture by recruiting ACF7 to the plasma membrane of migrating cells. Proc. Natl. Acad. Sci. USA. 107: 18517-18522. http://dx.doi.org/10.1073/pnas.1000975107