Microtubules Regulate Cell Migration and Neuronal Pathfinding



While many cell types are able to generate cellular movement through the action of the actomyosin cytoskeleton alone, microtubules are important for establishing and maintaining polarity, regulating the force-generating machinery and cell adhesion. Therefore, directionally persistent cell migration and neuronal pathfinding often require microtubules.

The microtubule cytoskeleton itself is organised asymmetrically to allow differential regulation of the migration machinery at the front and the rear of the cell. Microtubules position organelles such as the nucleus, the centrosome and the Golgi. Transport of mRNAs, vesicles, receptors and signalling components to the cell edges occurs along microtubules. These cargoes in turn support force generation by the actin cytoskeleton, act as a source of membrane lipids and regulate polarity signalling, adhesion, cell-cell communication and chemical gradient sensing. Microtubules themselves and especially the dynamic plus ends act as signalling platforms to control adhesion turnover and membrane protrusion. The rapid turnover of microtubules allows cells to quickly adapt to extracellular signals and change migration direction in response to guidance cues. Microtubule dynamics and organisation are in turn controlled by cortical cues. These feedback mechanisms ensure robustness and adaptation to environmental influences.

Given the fundamental importance of cell migration for embryonic development, the immune system and wound healing, impaired microtubule function leads to birth defects and diseases. Likewise, drugs targeting microtubules are routinely used to prevent excessive cell migration in cancer metastasis and chronic inflammatory diseases.


Focal Adhesion Kinase Focal Adhesion Adenomatous Polyposis Coli Growth Cone Microtubule Dynamic 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Abal M, Piel M, Bouckson-Castaing V, Mogensen M, Sibarita JB, Bornens M (2002) Microtubule release from the centrosome in migrating cells. J Cell Biol 159:731–737PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, Verkerk T, Vermeulen W, Burgering BM, De Zeeuw CI, Grosveld F, Galjart N (2001) Clasps are CLIP-115 and −170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104:923–935PubMedCrossRefGoogle Scholar
  3. Akhtar N, Streuli CH (2013) An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat Cell Biol 15:17–27PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aman A, Piotrowski T (2008) Wnt/beta-catenin and Fgf signaling control collective cell migration by restricting chemokine receptor expression. Dev Cell 15:749–761PubMedCrossRefGoogle Scholar
  5. Amano M, Nakayama M, Kaibuchi K (2010) Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton 67:545–554PubMedPubMedCentralCrossRefGoogle Scholar
  6. Andrew N, Insall RH (2007) Chemotaxis in shallow gradients is mediated independently of PtdIns 3-kinase by biased choices between random protrusions. Nat Cell Biol 9:193–200PubMedCrossRefGoogle Scholar
  7. Applewhite DA, Grode KD, Keller D, Zadeh AD, Slep KC, Rogers SL (2010) The spectraplakin Short stop is an actin-microtubule cross-linker that contributes to organization of the microtubule network. Mol Biol Cell 21:1714–1724PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bachmann A, Straube A (2015) Kinesins in cell migration. Biochem Soc Trans 43:79–83PubMedCrossRefGoogle Scholar
  9. Badano JL, Teslovich TM, Katsanis N (2005) The centrosome in human genetic disease. Nat Rev Genet 6:194–205PubMedCrossRefGoogle Scholar
  10. Bhuwania R, Castro-Castro A, Linder S (2014) Microtubule acetylation regulates dynamics of KIF1C-powered vesicles and contact of microtubule plus ends with podosomes. Eur J Cell Biol 93(10–12):424–437PubMedCrossRefGoogle Scholar
  11. Brahn E, Tang C, Banquerigo ML (1994) Regression of collagen-induced arthritis with taxol, a microtubule stabilizer. Arthritis Rheum 37:839–845PubMedCrossRefGoogle Scholar
  12. Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R (2007) Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J Cell Biol 178:193–200PubMedPubMedCentralCrossRefGoogle Scholar
  13. Braun A, Dang K, Buslig F, Baird MA, Davidson MW, Waterman CM, Myers KA (2014) Rac1 and Aurora A regulate MCAK to polarize microtubule growth in migrating endothelial cells. J Cell Biol 206:97–112PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bretscher MS (1989) Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J 8:1341–1348PubMedPubMedCentralGoogle Scholar
  15. Bretscher MS (2008) On the shape of migrating cells–a ‘front-to-back’ model. J Cell Sci 121:2625–2628PubMedCrossRefGoogle Scholar
  16. Bretscher MS, Aguado-Velasco C (1998) Membrane traffic during cell locomotion. Curr Opin Cell Biol 10:537–541PubMedCrossRefGoogle Scholar
  17. Breuss M, Heng JI, Poirier K, Tian G, Jaglin XH, Qu Z, Braun A, Gstrein T, Ngo L, Haas M, Bahi-Buisson N, Moutard ML, Passemard S, Verloes A, Gressens P, Xie Y, Robson KJ, Rani DS, Thangaraj K, Clausen T, Chelly J, Cowan NJ, Keays DA (2012) Mutations in the beta-tubulin gene TUBB5 cause microcephaly with structural brain abnormalities. Cell Rep 2:1554–1562PubMedPubMedCentralCrossRefGoogle Scholar
  18. Briggs MW, Li Z, Sacks DB (2002) IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J Biol Chem 277:7453–7465PubMedCrossRefGoogle Scholar
  19. Briggs MW, Sacks DB (2003a) IQGAP1 as signal integrator: Ca2+, calmodulin, Cdc42 and the cytoskeleton. FEBS Lett 542:7–11PubMedCrossRefGoogle Scholar
  20. Briggs MW, Sacks DB (2003b) IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep 4:571–574PubMedPubMedCentralCrossRefGoogle Scholar
  21. Buck KB, Zheng JQ (2002) Growth cone turning induced by direct local modification of microtubule dynamics. J Neurosci Off J Soc Neurosci 22:9358–9367Google Scholar
  22. Bulinski JC, Gundersen GG (1991) Stabilization of post-translational modification of microtubules during cellular morphogenesis. BioEssays News Rev Mol Cell Develop Biol 13:285–293CrossRefGoogle Scholar
  23. Burack MA, Silverman MA, Banker G (2000) The role of selective transport in neuronal protein sorting. Neuron 26:465–472PubMedCrossRefGoogle Scholar
  24. Cai D, McEwen DP, Martens JR, Meyhofer E, Verhey KJ (2009) Single molecule imaging reveals differences in microtubule track selection between Kinesin motors. PLoS Biol 7:e1000216PubMedPubMedCentralCrossRefGoogle Scholar
  25. Caspi M, Atlas R, Kantor A, Sapir T, Reiner O (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum Mol Genet 9:2205–2213PubMedCrossRefGoogle Scholar
  26. Caswell P, Norman J (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18:257–263PubMedCrossRefGoogle Scholar
  27. Cavallaro U, Niedermeyer J, Fuxa M, Christofori G (2001) N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 3:650–657PubMedCrossRefGoogle Scholar
  28. Chabin-Brion K, Marceiller J, Perez F, Settegrana C, Drechou A, Durand G, Pous C (2001) The Golgi complex is a microtubule-organizing organelle. Mol Biol Cell 12:2047–2060PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chang YC, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM (2008) GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 19:2147–2153PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583:1337–1343PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chen X, S-i K, Borisy GG, Green KJ (2003) p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J Cell Biol 163:547–557PubMedPubMedCentralCrossRefGoogle Scholar
  32. Chi Z, Melendez AJ (2007) Role of cell adhesion molecules and immune-cell migration in the initiation, onset and development of atherosclerosis. Cell Adh Migr 1:171–175PubMedPubMedCentralCrossRefGoogle Scholar
  33. Chia EW, Grainger R, Harper JL (2008) Colchicine suppresses neutrophil superoxide production in a murine model of gouty arthritis: a rationale for use of low-dose colchicine. Br J Pharmacol 153:1288–1295PubMedPubMedCentralCrossRefGoogle Scholar
  34. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469–480PubMedCrossRefGoogle Scholar
  35. Colvin RA, Means TK, Diefenbach TJ, Moita LF, Friday RP, Sever S, Campanella GS, Abrazinski T, Manice LA, Moita C, Andrews NW, Wu D, Hacohen N, Luster AD (2010) Synaptotagmin-mediated vesicle fusion regulates cell migration. Nat Immunol 11:495–502PubMedPubMedCentralCrossRefGoogle Scholar
  36. Cooper JA (2013) Cell biology in neuroscience: mechanisms of cell migration in the nervous system. J Cell Biol 202:725–734PubMedPubMedCentralCrossRefGoogle Scholar
  37. Coopman PJ, Do MT, Thompson EW, Mueller SC (1998) Phagocytosis of cross-linked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin Cancer Res Off J Am Assoc Cancer Res 4:507–515Google Scholar
  38. Cornfine S, Himmel M, Kopp P, El Azzouzi K, Wiesner C, Kruger M, Rudel T, Linder S (2011) The kinesin KIF9 and reggie/flotillin proteins regulate matrix degradation by macrophage podosomes. Mol Biol Cell 22:202–215PubMedPubMedCentralCrossRefGoogle Scholar
  39. Cui DH, Jiang KD, Jiang SD, Xu YF, Yao H (2005) The tumor suppressor adenomatous polyposis coli gene is associated with susceptibility to schizophrenia. Mol Psychiatry 10:669–677PubMedCrossRefGoogle Scholar
  40. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708PubMedCrossRefGoogle Scholar
  41. Del Rio JA, Gonzalez-Billault C, Urena JM, Jimenez EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, La Torre A, Wandosell F, Avila J, Soriano E (2004) MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr Biol CB 14:840–850PubMedCrossRefGoogle Scholar
  42. Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086–1089PubMedPubMedCentralCrossRefGoogle Scholar
  43. Drabek K, van Ham M, Stepanova T, Draegestein K, van Horssen R, Sayas CL, Akhmanova A, Ten Hagen T, Smits R, Fodde R, Grosveld F, Galjart N (2006) Role of CLASP2 in microtubule stabilization and the regulation of persistent motility. Curr Biol CB 16:2259–2264PubMedCrossRefGoogle Scholar
  44. Draberova E, Vinopal S, Morfini G, Liu PS, Sladkova V, Sulimenko T, Burns MR, Solowska J, Kulandaivel K, de Chadarevian JP, Legido A, Mork SJ, Janacek J, Baas PW, Draber P, Katsetos CD (2011) Microtubule-severing ATPase spastin in glioblastoma: increased expression in human glioblastoma cell lines and inverse roles in cell motility and proliferation. J Neuropathol Exp Neurol 70:811–826PubMedPubMedCentralCrossRefGoogle Scholar
  45. Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146–1158PubMedPubMedCentralCrossRefGoogle Scholar
  46. Dunn GA, Zicha D, Fraylich PE (1997) Rapid, microtubule-dependent fluctuations of the cell margin. J Cell Sci 110(Pt 24):3091–3098PubMedGoogle Scholar
  47. Dupin I, Camand E, Etienne-Manneville S (2009) Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 185:779–786PubMedPubMedCentralCrossRefGoogle Scholar
  48. Dziezanowski MA, DeStefano MJ, Rabinovitch M (1980) Effect of antitubulins on spontaneous and chemotactic migration of neutrophils under agarose. J Cell Sci 42:379–388PubMedGoogle Scholar
  49. Ebneth A, Drewes G, Mandelkow EM, Mandelkow E (1999) Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil Cytoskeleton 44:209–224PubMedCrossRefGoogle Scholar
  50. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793PubMedCrossRefGoogle Scholar
  51. Efimov A, Kharitonov A, Efimova N, Loncarek J, Miller PM, Andreyeva N, Gleeson P, Galjart N, Maia AR, McLeod IX, Yates JR 3rd, Maiato H, Khodjakov A, Akhmanova A, Kaverina I (2007) Asymmetric CLASP-dependent nucleation of noncentrosomal microtubules at the trans-Golgi network. Dev Cell 12:917–930PubMedPubMedCentralCrossRefGoogle Scholar
  52. Efimov A, Schiefermeier N, Grigoriev I, Ohi R, Brown MC, Turner CE, Small JV, Kaverina I (2008) Paxillin-dependent stimulation of microtubule catastrophes at focal adhesion sites. J Cell Sci 121:196–204PubMedPubMedCentralCrossRefGoogle Scholar
  53. Efimova N, Grimaldi A, Bachmann A, Frye K, Zhu X, Feoktistov A, Straube A, Kaverina I (2014) Podosome-regulating kinesin KIF1C translocates to the cell periphery in a CLASP-dependent manner. J Cell Sci 127:5179–5188PubMedPubMedCentralCrossRefGoogle Scholar
  54. Errico A, Ballabio A, Rugarli EI (2002) Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11:153–163PubMedCrossRefGoogle Scholar
  55. Eskova A, Knapp B, Matelska D, Reusing S, Arjonen A, Lisauskas T, Pepperkok R, Russell R, Eils R, Ivaska J, Kaderali L, Erfle H, Starkuviene V (2014) An RNAi screen identifies KIF15 as a novel regulator of the endocytic trafficking of integrin. J Cell Sci 127:2433–2447PubMedCrossRefGoogle Scholar
  56. Etienne-Manneville S (2004) Actin and microtubules in cell motility: which one is in control? Traffic 5:470–477PubMedCrossRefGoogle Scholar
  57. Etienne-Manneville S (2013) Microtubules in cell migration. Annu Rev Cell Dev Biol 29:471–499PubMedCrossRefGoogle Scholar
  58. Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489–498PubMedCrossRefGoogle Scholar
  59. Etienne-Manneville S, Hall A (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421:753–756PubMedCrossRefGoogle Scholar
  60. Etienne-Manneville S, Manneville JB, Nicholls S, Ferenczi MA, Hall A (2005) Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J Cell Biol 170:895–901PubMedPubMedCentralCrossRefGoogle Scholar
  61. Euteneuer U, Schliwa M (1984) Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules. Nature 310:58–61PubMedCrossRefGoogle Scholar
  62. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187:733–747PubMedPubMedCentralCrossRefGoogle Scholar
  63. Ezratty EJ, Partridge MA, Gundersen GG (2005) Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7:581–590PubMedCrossRefGoogle Scholar
  64. Fahrion JK, Komuro Y, Li Y, Ohno N, Littner Y, Raoult E, Galas L, Vaudry D, Komuro H (2012) Rescue of neuronal migration deficits in a mouse model of fetal Minamata disease by increasing neuronal Ca2+ spike frequency. Proc Natl Acad Sci U S A 109:5057–5062PubMedPubMedCentralCrossRefGoogle Scholar
  65. Faux MC, Ross JL, Meeker C, Johns T, Ji H, Simpson RJ, Layton MJ, Burgess AW (2004) Restoration of full-length adenomatous polyposis coli (APC) protein in a colon cancer cell line enhances cell adhesion. J Cell Sci 117:427–439PubMedCrossRefGoogle Scholar
  66. Francavilla C, Loeffler S, Piccini D, Kren A, Christofori G, Cavallaro U (2007) Neural cell adhesion molecule regulates the cellular response to fibroblast growth factor. J Cell Sci 120:4388–4394PubMedCrossRefGoogle Scholar
  67. Friedl P, Entschladen F, Conrad C, Niggemann B, Zanker KS (1998a) CD4+ T lymphocytes migrating in three-dimensional collagen lattices lack focal adhesions and utilize beta1 integrin-independent strategies for polarization, interaction with collagen fibers and locomotion. Eur J Immunol 28:2331–2343PubMedCrossRefGoogle Scholar
  68. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10:445–457PubMedCrossRefGoogle Scholar
  69. Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48:441–449PubMedCrossRefGoogle Scholar
  70. Friedl P, Weigelin B (2008) Interstitial leukocyte migration and immune function. Nat Immunol 9:960–969PubMedCrossRefGoogle Scholar
  71. Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374PubMedCrossRefGoogle Scholar
  72. Friedl P, Zanker KS, Brocker EB (1998b) Cell migration strategies in 3-D extracellular matrix: differences in morphology, cell matrix interactions, and integrin function. Microsc Res Tech 43:369–378PubMedCrossRefGoogle Scholar
  73. Fukata M, Kuroda S, Nakagawa M, Kawajiri A, Itoh N, Shoji I, Matsuura Y, Yonehara S, Fujisawa H, Kikuchi A, Kaibuchi K (1999) Cdc42 and Rac1 regulate the interaction of IQGAP1 with beta-catenin. J Biol Chem 274:26044–26050PubMedCrossRefGoogle Scholar
  74. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K (2002) Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109:873–885PubMedCrossRefGoogle Scholar
  75. Ganguly A, Yang H, Sharma R, Patel KD, Cabral F (2012) The role of microtubules and their dynamics in cell migration. J Biol Chem 287:43359–43369PubMedPubMedCentralCrossRefGoogle Scholar
  76. Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD (2012) Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev Cell 23:716–728PubMedPubMedCentralCrossRefGoogle Scholar
  77. Glaven JA, Whitehead I, Bagrodia S, Kay R, Cerione RA (1999) The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J Biol Chem 274:2279–2285PubMedCrossRefGoogle Scholar
  78. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999a) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271PubMedCrossRefGoogle Scholar
  79. Gleeson JG, Minnerath SR, Fox JW, Allen KM, Luo RF, Hong SE, Berg MJ, Kuzniecky R, Reitnauer PJ, Borgatti R, Mira AP, Guerrini R, Holmes GL, Rooney CM, Berkovic S, Scheffer I, Cooper EC, Ricci S, Cusmai R, Crawford TO, Leroy R, Andermann E, Wheless JW, Dobyns WB, Walsh CA et al (1999b) Characterization of mutations in the gene doublecortin in patients with double cortex syndrome. Ann Neurol 45:146–153PubMedCrossRefGoogle Scholar
  80. Godinho SA, Picone R, Burute M, Dagher R, Su Y, Leung CT, Polyak K, Brugge JS, Thery M, Pellman D (2014) Oncogene-like induction of cellular invasion from centrosome amplification. Nature 510:167–171PubMedPubMedCentralCrossRefGoogle Scholar
  81. Gomes ER, Jani S, Gundersen GG (2005) Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121:451–463PubMedCrossRefGoogle Scholar
  82. Gu Z, Noss EH, Hsu VW, Brenner MB (2011) Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J Cell Biol 193:61–70PubMedPubMedCentralCrossRefGoogle Scholar
  83. Gundersen GG, Bulinski JC (1988) Selective stabilization of microtubules oriented toward the direction of cell migration. Proc Natl Acad Sci U S A 85:5946–5950PubMedPubMedCentralCrossRefGoogle Scholar
  84. Hall A (2012) Rho family GTPases. Biochem Soc Trans 40:1378–1382PubMedCrossRefGoogle Scholar
  85. Hamshere ML, Walters JT, Smith R, Richards AL, Green E, Grozeva D, Jones I, Forty L, Jones L, Gordon-Smith K, Riley B, O’Neill FA, Kendler KS, Sklar P, Purcell S, Kranz J, Schizophrenia Psychiatric Genome-wide Association Study C, Wellcome Trust Case Control C, Wellcome Trust Case Control C, Morris D, Gill M, Holmans P, Craddock N, Corvin A, Owen MJ, O’Donovan MC (2013) Genome-wide significant associations in schizophrenia to ITIH3/4, CACNA1C and SDCCAG8, and extensive replication of associations reported by the Schizophrenia PGC. Mol Psychiatry 18:708–712Google Scholar
  86. Harada T, Swift J, Irianto J, Shin JW, Spinler KR, Athirasala A, Diegmiller R, Dingal PC, Ivanovska IL, Discher DE (2014) Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 204:669–682PubMedPubMedCentralCrossRefGoogle Scholar
  87. Hashimoto R, Numakawa T, Ohnishi T, Kumamaru E, Yagasaki Y, Ishimoto T, Mori T, Nemoto K, Adachi N, Izumi A, Chiba S, Noguchi H, Suzuki T, Iwata N, Ozaki N, Taguchi T, Kamiya A, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Sawa A, Kunugi H (2006) Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet 15:3024–3033PubMedCrossRefGoogle Scholar
  88. Hattori M, Adachi H, Tsujimoto M, Arai H, Inoue K (1994) Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected]. Nature 370:216–218PubMedCrossRefGoogle Scholar
  89. Hayashi K, Suzuki A, Ohno S (2012) PAR-1/MARK: a kinase essential for maintaining the dynamic state of microtubules. Cell Struct Funct 37:21–25PubMedCrossRefGoogle Scholar
  90. Hegerfeldt Y, Tusch M, Brocker EB, Friedl P (2002) Collective cell movement in primary melanoma explants: plasticity of cell-cell interaction, beta1-integrin function, and migration strategies. Cancer Res 62:2125–2130PubMedGoogle Scholar
  91. Heintz TG, Heller J, Zhao R, Caceres A, Eva R, Fawcett JW (2014) Kinesin KIF4A transports integrin beta1 in developing axons of cortical neurons. Mol Cell Neurosci 63:60–71PubMedCrossRefGoogle Scholar
  92. Hennah W, Thomson P, McQuillin A, Bass N, Loukola A, Anjorin A, Blackwood D, Curtis D, Deary IJ, Harris SE, Isometsa ET, Lawrence J, Lonnqvist J, Muir W, Palotie A, Partonen T, Paunio T, Pylkko E, Robinson M, Soronen P, Suominen K, Suvisaari J, Thirumalai S, St Clair D, Gurling H, Peltonen L, Porteous D (2009) DISC1 association, heterogeneity and interplay in schizophrenia and bipolar disorder. Mol Psychiatry 14:865–873PubMedCrossRefGoogle Scholar
  93. Heuberger J, Birchmeier W (2010) Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2:a002915PubMedPubMedCentralCrossRefGoogle Scholar
  94. Huang CF, Banker G (2012) The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 13:549–564PubMedPubMedCentralCrossRefGoogle Scholar
  95. Humbert PO, Grzeschik NA, Brumby AM, Galea R, Elsum I, Richardson HE (2008) Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27:6888–6907PubMedCrossRefGoogle Scholar
  96. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687PubMedCrossRefGoogle Scholar
  97. Ichii T, Takeichi M (2007) p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells Devoted Mol Cell Mech 12:827–839CrossRefGoogle Scholar
  98. Insolera R, Shao W, Airik R, Hildebrandt F, Shi SH (2014) SDCCAG8 regulates pericentriolar material recruitment and neuronal migration in the developing cortex. Neuron 83:805–822PubMedPubMedCentralCrossRefGoogle Scholar
  99. Ishizuka K, Kamiya A, Oh EC, Kanki H, Seshadri S, Robinson JF, Murdoch H, Dunlop AJ, Kubo K, Furukori K, Huang B, Zeledon M, Hayashi-Takagi A, Okano H, Nakajima K, Houslay MD, Katsanis N, Sawa A (2011) DISC1-dependent switch from progenitor proliferation to migration in the developing cortex. Nature 473:92–96PubMedPubMedCentralCrossRefGoogle Scholar
  100. Jacobson C, Schnapp B, Banker GA (2006) A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49:797–804PubMedCrossRefGoogle Scholar
  101. Jaglin XH, Poirier K, Saillour Y, Buhler E, Tian G, Bahi-Buisson N, Fallet-Bianco C, Phan-Dinh-Tuy F, Kong XP, Bomont P, Castelnau-Ptakhine L, Odent S, Loget P, Kossorotoff M, Snoeck I, Plessis G, Parent P, Beldjord C, Cardoso C, Represa A, Flint J, Keays DA, Cowan NJ, Chelly J (2009) Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat Genet 41:746–752PubMedPubMedCentralCrossRefGoogle Scholar
  102. Jaulin F, Kreitzer G (2010) KIF17 stabilizes microtubules and contributes to epithelial morphogenesis by acting at MT plus ends with EB1 and APC. J Cell Biol 190:443–460PubMedPubMedCentralCrossRefGoogle Scholar
  103. Jenkins B, Decker H, Bentley M, Luisi J, Banker G (2012) A novel split kinesin assay identifies motor proteins that interact with distinct vesicle populations. J Cell Biol 198:749–761PubMedPubMedCentralCrossRefGoogle Scholar
  104. Jiang K, Hua S, Mohan R, Grigoriev I, Yau KW, Liu Q, Katrukha EA, Altelaar AF, Heck AJ, Hoogenraad CC, Akhmanova A (2014) Microtubule minus-end stabilization by polymerization-driven CAMSAP deposition. Dev Cell 28:295–309PubMedCrossRefGoogle Scholar
  105. Jolly AL, Kim H, Srinivasan D, Lakonishok M, Larson AG, Gelfand VI (2010) Kinesin-1 heavy chain mediates microtubule sliding to drive changes in cell shape. Proc Natl Acad Sci U S A 107:12151–12156PubMedPubMedCentralCrossRefGoogle Scholar
  106. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253–265PubMedCrossRefGoogle Scholar
  107. Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14:697–703PubMedPubMedCentralCrossRefGoogle Scholar
  108. Kamiya A, Tan PL, Kubo K, Engelhard C, Ishizuka K, Kubo A, Tsukita S, Pulver AE, Nakajima K, Cascella NG, Katsanis N, Sawa A (2008) Recruitment of PCM1 to the centrosome by the cooperative action of DISC1 and BBS4: a candidate for psychiatric illnesses. Arch Gen Psychiatry 65:996–1006PubMedPubMedCentralCrossRefGoogle Scholar
  109. Kassler S, Donninger H, Birrer MJ, Clark GJ (2012) RASSF1A and the taxol response in ovarian cancer. Mol Biol Int 2012:263267PubMedPubMedCentralCrossRefGoogle Scholar
  110. Katz ZB, Wells AL, Park HY, Wu B, Shenoy SM, Singer RH (2012) beta-Actin mRNA compartmentalization enhances focal adhesion stability and directs cell migration. Genes Dev 26:1885–1890PubMedPubMedCentralCrossRefGoogle Scholar
  111. Kaverina I, Krylyshkina O, Small JV (1999) Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 146:1033–1044PubMedPubMedCentralCrossRefGoogle Scholar
  112. Kaverina I, Rottner K, Small JV (1998) Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 142:181–190PubMedPubMedCentralCrossRefGoogle Scholar
  113. Kaverina I, Straube A (2011) Regulation of cell migration by dynamic microtubules. Semin Cell Dev Biol 22:968–974PubMedPubMedCentralCrossRefGoogle Scholar
  114. Kawauchi T, Sekine K, Shikanai M, Chihama K, Tomita K, Kubo K, Nakajima K, Nabeshima Y, Hoshino M (2010) Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67:588–602PubMedCrossRefGoogle Scholar
  115. Keays DA, Tian G, Poirier K, Huang GJ, Siebold C, Cleak J, Oliver PL, Fray M, Harvey RJ, Molnar Z, Pinon MC, Dear N, Valdar W, Brown SD, Davies KE, Rawlins JN, Cowan NJ, Nolan P, Chelly J, Flint J (2007) Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128:45–57PubMedPubMedCentralCrossRefGoogle Scholar
  116. Keren K, Pincus Z, Allen GM, Barnhart EL, Marriott G, Mogilner A, Theriot JA (2008) Mechanism of shape determination in motile cells. Nature 453:475–480PubMedPubMedCentralCrossRefGoogle Scholar
  117. Kholmanskikh SS, Koeller HB, Wynshaw-Boris A, Gomez T, Letourneau PC, Ross ME (2006) Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat Neurosci 9:50–57PubMedCrossRefGoogle Scholar
  118. Kislauskis EH, Zhu X, Singer RH (1997) beta-Actin messenger RNA localization and protein synthesis augment cell motility. J Cell Biol 136:1263–1270PubMedPubMedCentralCrossRefGoogle Scholar
  119. Kita K, Wittmann T, Nathke IS, Waterman-Storer CM (2006) Adenomatous polyposis coli on microtubule plus ends in cell extensions can promote microtubule net growth with or without EB1. Mol Biol Cell 17:2331–2345PubMedPubMedCentralCrossRefGoogle Scholar
  120. Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E (2003) ACF7: an essential integrator of microtubule dynamics. Cell 115:343–354PubMedCrossRefGoogle Scholar
  121. Komarova YA, Vorobjev IA, Borisy GG (2002) Life cycle of MTs: persistent growth in the cell interior, asymmetric transition frequencies and effects of the cell boundary. J Cell Sci 115:3527–3539PubMedGoogle Scholar
  122. Komuro H, Rakic P (1998) Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J Neurosci Off J Soc Neurosci 18:1478–1490Google Scholar
  123. Kopp P, Lammers R, Aepfelbacher M, Woehlke G, Rudel T, Machuy N, Steffen W, Linder S (2006) The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol Biol Cell 17:2811–2823PubMedPubMedCentralCrossRefGoogle Scholar
  124. Kozlovsky N, Belmaker RH, Agam G (2002) GSK-3 and the neurodevelopmental hypothesis of schizophrenia. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 12:13–25CrossRefGoogle Scholar
  125. Krendel M, Zenke FT, Bokoch GM (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4:294–301PubMedCrossRefGoogle Scholar
  126. Kroboth K, Newton IP, Kita K, Dikovskaya D, Zumbrunn J, Waterman-Storer CM, Nathke IS (2007) Lack of adenomatous polyposis coli protein correlates with a decrease in cell migration and overall changes in microtubule stability. Mol Biol Cell 18:910–918PubMedPubMedCentralCrossRefGoogle Scholar
  127. Krylyshkina O, Anderson KI, Kaverina I, Upmann I, Manstein DJ, Small JV, Toomre DK (2003) Nanometer targeting of microtubules to focal adhesions. J Cell Biol 161:853–859PubMedPubMedCentralCrossRefGoogle Scholar
  128. Krylyshkina O, Kaverina I, Kranewitter W, Steffen W, Alonso MC, Cross RA, Small JV (2002) Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J Cell Biol 156:349–359PubMedPubMedCentralCrossRefGoogle Scholar
  129. Kumar P, Lyle KS, Gierke S, Matov A, Danuser G, Wittmann T (2009) GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J Cell Biol 184:895–908PubMedPubMedCentralCrossRefGoogle Scholar
  130. Kumar S, Xu J, Perkins C, Guo F, Snapper S, Finkelman FD, Zheng Y, Filippi MD (2012) Cdc42 regulates neutrophil migration via crosstalk between WASp, CD11b, and microtubules. Blood 120:3563–3574PubMedPubMedCentralCrossRefGoogle Scholar
  131. Kupfer A, Dennert G, Singer SJ (1983) Polarization of the Golgi apparatus and the microtubule-organizing center within cloned natural killer cells bound to their targets. Proc Natl Acad Sci U S A 80:7224–7228PubMedPubMedCentralCrossRefGoogle Scholar
  132. Kushner EJ, Ferro LS, Liu JY, Durrant JR, Rogers SL, Dudley AC, Bautch VL (2014) Excess centrosomes disrupt endothelial cell migration via centrosome scattering. J Cell Biol 206:257–272PubMedPubMedCentralCrossRefGoogle Scholar
  133. Lacroix B, van Dijk J, Gold ND, Guizetti J, Aldrian-Herrada G, Rogowski K, Gerlich DW, Janke C (2010) Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J Cell Biol 189:945–954PubMedPubMedCentralCrossRefGoogle Scholar
  134. Lammermann T, Sixt M (2009) Mechanical modes of ‘amoeboid’ cell migration. Curr Opin Cell Biol 21:636–644PubMedCrossRefGoogle Scholar
  135. Lawrence JB, Singer RH (1986) Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45:407–415PubMedCrossRefGoogle Scholar
  136. Lee G, Leugers CJ (2012) Tau and tauopathies. Prog Mol Biol Transl Sci 107:263–293PubMedPubMedCentralCrossRefGoogle Scholar
  137. Legate KR, Montanez E, Kudlacek O, Fassler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7:20–31PubMedCrossRefGoogle Scholar
  138. Lehembre F, Yilmaz M, Wicki A, Schomber T, Strittmatter K, Ziegler D, Kren A, Went P, Derksen PW, Berns A, Jonkers J, Christofori G (2008) NCAM-induced focal adhesion assembly: a functional switch upon loss of E-cadherin. EMBO J 27:2603–2615PubMedPubMedCentralCrossRefGoogle Scholar
  139. Lele Z, Folchert A, Concha M, Rauch GJ, Geisler R, Rosa F, Wilson SW, Hammerschmidt M, Bally-Cuif L (2002) parachute/n-cadherin is required for morphogenesis and maintained integrity of the zebrafish neural tube. Development 129:3281–3294PubMedGoogle Scholar
  140. Li D, Xie S, Ren Y, Huo L, Gao J, Cui D, Liu M, Zhou J (2011) Microtubule-associated deacetylase HDAC6 promotes angiogenesis by regulating cell migration in an EB1-dependent manner. Protein Cell 2:150–160PubMedCrossRefGoogle Scholar
  141. Liao G, Nagasaki T, Gundersen GG (1995) Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion. J Cell Sci 108(Pt 11):3473–3483PubMedGoogle Scholar
  142. Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R, Ketelaar T, Emons AM, Mulder BM, Kirik V, Ehrhardt DW (2013) A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:1245533PubMedCrossRefGoogle Scholar
  143. Liu JS (2011) Molecular genetics of neuronal migration disorders. Curr Neurol Neurosci Rep 11:171–178PubMedCrossRefGoogle Scholar
  144. Liu M, Nadar VC, Kozielski F, Kozlowska M, Yu W, Baas PW (2010) Kinesin-12, a mitotic microtubule-associated motor protein, impacts axonal growth, navigation, and branching. J Neurosci Off J Soc Neurosci 30:14896–14906CrossRefGoogle Scholar
  145. Liu R, Woolner S, Johndrow JE, Metzger D, Flores A, Parkhurst SM (2008) Sisyphus, the Drosophila myosin XV homolog, traffics within filopodia transporting key sensory and adhesion cargos. Development 135:53–63PubMedCrossRefGoogle Scholar
  146. Lu W, Fox P, Lakonishok M, Davidson MW, Gelfand VI (2013) Initial neurite outgrowth in Drosophila neurons is driven by kinesin-powered microtubule sliding. Curr Biol CB 23:1018–1023PubMedCrossRefGoogle Scholar
  147. Luxton GW, Gundersen GG (2011) Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 23:579–588PubMedPubMedCentralCrossRefGoogle Scholar
  148. Ma B, Savas JN, Yu MS, Culver BP, Chao MV, Tanese N (2011) Huntingtin mediates dendritic transport of beta-actin mRNA in rat neurons. Sci Rep 1:140PubMedPubMedCentralCrossRefGoogle Scholar
  149. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn KM, Danuser G (2009) Coordination of Rho GTPase activities during cell protrusion. Nature 461:99–103PubMedPubMedCentralCrossRefGoogle Scholar
  150. Mandeville JT, Lawson MA, Maxfield FR (1997) Dynamic imaging of neutrophil migration in three dimensions: mechanical interactions between cells and matrix. J Leukoc Biol 61:188–200PubMedGoogle Scholar
  151. Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F, Proksch E, de Strooper B, Hartmann D, Saftig P (2005) ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci U S A 102:9182–9187PubMedPubMedCentralCrossRefGoogle Scholar
  152. Margadant C, Monsuur HN, Norman JC, Sonnenberg A (2011) Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 23:607–614PubMedCrossRefGoogle Scholar
  153. Mary S, Charrasse S, Meriane M, Comunale F, Travo P, Blangy A, Gauthier-Rouviere C (2002) Biogenesis of N-cadherin-dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol Biol Cell 13:285–301PubMedPubMedCentralCrossRefGoogle Scholar
  154. Matsumoto S, Fumoto K, Okamoto T, Kaibuchi K, Kikuchi A (2010) Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J 29:1192–1204PubMedPubMedCentralCrossRefGoogle Scholar
  155. Matsushima K, Tokuraku K, Hasan MR, Kotani S (2012) Microtubule-associated protein 4 binds to actin filaments and modulates their properties. J Biochem 151:99–108PubMedCrossRefGoogle Scholar
  156. McCrea PD, Gu D, Balda MS (2009) Junctional music that the nucleus hears: cell-cell contact signaling and the modulation of gene activity. Cold Spring Harb Perspect Biol 1:a002923PubMedPubMedCentralCrossRefGoogle Scholar
  157. McLean GW, Carragher NO, Avizienyte E, Evans J, Brunton VG, Frame MC (2005) The role of focal-adhesion kinase in cancer - a new therapeutic opportunity. Nat Rev Cancer 5:505–515PubMedCrossRefGoogle Scholar
  158. Mehlen P, Puisieux A (2006) Metastasis: a question of life or death. Nat Rev Cancer 6:449–458PubMedCrossRefGoogle Scholar
  159. Meyer KD, Morris JA (2009) Disc1 regulates granule cell migration in the developing hippocampus. Hum Mol Genet 18:3286–3297PubMedPubMedCentralCrossRefGoogle Scholar
  160. Mierke CT, Kollmannsberger P, Zitterbart DP, Diez G, Koch TM, Marg S, Ziegler WH, Goldmann WH, Fabry B (2010) Vinculin facilitates cell invasion into three-dimensional collagen matrices. J Biol Chem 285:13121–13130PubMedPubMedCentralCrossRefGoogle Scholar
  161. Miller AL, Wang Y, Mooseker MS, Koleske AJ (2004) The Abl-related gene (Arg) requires its F-actin-microtubule cross-linking activity to regulate lamellipodial dynamics during fibroblast adhesion. J Cell Biol 165:407–419PubMedPubMedCentralCrossRefGoogle Scholar
  162. Miller PM, Folkmann AW, Maia AR, Efimova N, Efimov A, Kaverina I (2009) Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat Cell Biol 11:1069–1080PubMedPubMedCentralCrossRefGoogle Scholar
  163. Mimori-Kiyosue Y, Shiina N, Tsukita S (2000) Adenomatous polyposis coli (APC) protein moves along microtubules and concentrates at their growing ends in epithelial cells. J Cell Biol 148:505–518PubMedPubMedCentralCrossRefGoogle Scholar
  164. Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G (2005) Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J Cell Sci 118:2425–2433PubMedPubMedCentralCrossRefGoogle Scholar
  165. Mohn JL, Alexander J, Pirone A, Palka CD, Lee SY, Mebane L, Haydon PG, Jacob MH (2014) Adenomatous polyposis coli protein deletion leads to cognitive and autism-like disabilities. Mol Psychiatry 19:1133–1142PubMedPubMedCentralCrossRefGoogle Scholar
  166. Monier-Gavelle F, Duband JL (1995) Control of N-cadherin-mediated intercellular adhesion in migrating neural crest cells in vitro. J Cell Sci 108(Pt 12):3839–3853PubMedGoogle Scholar
  167. Montenegro-Venegas C, Tortosa E, Rosso S, Peretti D, Bollati F, Bisbal M, Jausoro I, Avila J, Caceres A, Gonzalez-Billault C (2010) MAP1B regulates axonal development by modulating Rho-GTPase Rac1 activity. Mol Biol Cell 21:3518–3528PubMedPubMedCentralCrossRefGoogle Scholar
  168. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P (1995) Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci U S A 92:3046–3050PubMedPubMedCentralCrossRefGoogle Scholar
  169. Myers KA, Baas PW (2007) Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J Cell Biol 178:1081–1091PubMedPubMedCentralCrossRefGoogle Scholar
  170. Nadar VC, Ketschek A, Myers KA, Gallo G, Baas PW (2008) Kinesin-5 is essential for growth-cone turning. Curr Biol 18(24):1972–1977PubMedPubMedCentralCrossRefGoogle Scholar
  171. Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963–2971PubMedGoogle Scholar
  172. Nakamura M, Zhou XZ, Lu KP (2001) Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr Biol CB 11:1062–1067PubMedCrossRefGoogle Scholar
  173. Nalbant P, Chang YC, Birkenfeld J, Chang ZF, Bokoch GM (2009) Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol Biol Cell 20:4070–4082PubMedPubMedCentralCrossRefGoogle Scholar
  174. Nathke IS, Adams CL, Polakis P, Sellin JH, Nelson WJ (1996) The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration. J Cell Biol 134:165–179PubMedCrossRefGoogle Scholar
  175. Niethammer P, Bastiaens P, Karsenti E (2004) Stathmin-tubulin interaction gradients in motile and mitotic cells. Science 303:1862–1866PubMedCrossRefGoogle Scholar
  176. Niggli V (2003) Microtubule-disruption-induced and chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. J Cell Sci 116:813–822PubMedCrossRefGoogle Scholar
  177. Nishimura T, Kaibuchi K (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13:15–28PubMedCrossRefGoogle Scholar
  178. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235–1244PubMedPubMedCentralCrossRefGoogle Scholar
  179. O’Donnell L, Rhodes D, Smith SJ, Merriner DJ, Clark BJ, Borg C, Whittle B, O’Connor AE, Smith LB, McNally FJ, de Kretser DM, Goodnow CC, Ormandy CJ, Jamsai D, O’Bryan MK (2012) An essential role for katanin p80 and microtubule severing in male gamete production. PLoS Genet 8:e1002698PubMedPubMedCentralCrossRefGoogle Scholar
  180. O’Sullivan D, Miller JH, Northcote PT, La Flamme AC (2013) Microtubule-stabilizing agents delay the onset of EAE through inhibition of migration. Immunol Cell Biol 91:583–592PubMedCrossRefGoogle Scholar
  181. Okada K, Bartolini F, Deaconescu AM, Moseley JB, Dogic Z, Grigorieff N, Gundersen GG, Goode BL (2010) Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J Cell Biol 189:1087–1096PubMedPubMedCentralCrossRefGoogle Scholar
  182. Oleynikov Y, Singer RH (1998) RNA localization: different zipcodes, same postman? Trends Cell Biol 8:381–383PubMedCrossRefGoogle Scholar
  183. Osmani N, Peglion F, Chavrier P, Etienne-Manneville S (2010) Cdc42 localization and cell polarity depend on membrane traffic. J Cell Biol 191:1261–1269PubMedPubMedCentralCrossRefGoogle Scholar
  184. Ozmen M, Yilmaz Y, Caliskan M, Minareci O, Aydinli N (2000) Clinical features of 21 patients with lissencephaly type I (agyria-pachygyria). Turk J Pediatr 42:210–214PubMedGoogle Scholar
  185. Palamidessi A, Frittoli E, Garre M, Faretta M, Mione M, Testa I, Diaspro A, Lanzetti L, Scita G, Di Fiore PP (2008) Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 134:135–147PubMedCrossRefGoogle Scholar
  186. Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG (2004) Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303:836–839PubMedCrossRefGoogle Scholar
  187. Palazzo AF, Joseph HL, Chen YJ, Dujardin DL, Alberts AS, Pfister KK, Vallee RB, Gundersen GG (2001) Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol CB 11:1536–1541PubMedCrossRefGoogle Scholar
  188. Paratcha G, Ledda F, Ibanez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867–879PubMedCrossRefGoogle Scholar
  189. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11:633–643PubMedPubMedCentralCrossRefGoogle Scholar
  190. Pegtel DM, Ellenbroek SI, Mertens AE, van der Kammen RA, de Rooij J, Collard JG (2007) The Par-Tiam1 complex controls persistent migration by stabilizing microtubule-dependent front-rear polarity. Curr Biol CB 17:1623–1634PubMedCrossRefGoogle Scholar
  191. Peris L, Wagenbach M, Lafanechere L, Brocard J, Moore AT, Kozielski F, Job D, Wordeman L, Andrieux A (2009) Motor-dependent microtubule disassembly driven by tubulin tyrosination. J Cell Biol 185:1159–1166PubMedPubMedCentralCrossRefGoogle Scholar
  192. Petrie RJ, Doyle AD, Yamada KM (2009) Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10:538–549PubMedPubMedCentralCrossRefGoogle Scholar
  193. Pfister AS, Hadjihannas MV, Rohrig W, Schambony A, Behrens J (2012) Amer2 protein interacts with EB1 protein and adenomatous polyposis coli (APC) and controls microtubule stability and cell migration. J Biol Chem 287:35333–35340PubMedPubMedCentralCrossRefGoogle Scholar
  194. Pilz DT, Matsumoto N, Minnerath S, Mills P, Gleeson JG, Allen KM, Walsh CA, Barkovich AJ, Dobyns WB, Ledbetter DH, Ross ME (1998) LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum Mol Genet 7:2029–2037PubMedCrossRefGoogle Scholar
  195. Poirier K, Keays DA, Francis F, Saillour Y, Bahi N, Manouvrier S, Fallet-Bianco C, Pasquier L, Toutain A, Tuy FP, Bienvenu T, Joriot S, Odent S, Ville D, Desguerre I, Goldenberg A, Moutard ML, Fryns JP, van Esch H, Harvey RJ, Siebold C, Flint J, Beldjord C, Chelly J (2007) Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A). Hum Mutat 28:1055–1064PubMedCrossRefGoogle Scholar
  196. Poirier K, Lebrun N, Broix L, Tian G, Saillour Y, Boscheron C, Parrini E, Valence S, Pierre BS, Oger M, Lacombe D, Genevieve D, Fontana E, Darra F, Cances C, Barth M, Bonneau D, Bernadina BD, N’Guyen S, Gitiaux C, Parent P, des Portes V, Pedespan JM, Legrez V, Castelnau-Ptakine L, Nitschke P, Hieu T, Masson C, Zelenika D, Andrieux A, Francis F, Guerrini R, Cowan NJ, Bahi-Buisson N, Chelly J (2013) Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat Genet 45:639–647PubMedCrossRefGoogle Scholar
  197. Poirier K, Saillour Y, Bahi-Buisson N, Jaglin XH, Fallet-Bianco C, Nabbout R, Castelnau-Ptakhine L, Roubertie A, Attie-Bitach T, Desguerre I, Genevieve D, Barnerias C, Keren B, Lebrun N, Boddaert N, Encha-Razavi F, Chelly J (2010) Mutations in the neuronal ss-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects. Hum Mol Genet 19:4462–4473PubMedPubMedCentralCrossRefGoogle Scholar
  198. Pouthas F, Girard P, Lecaudey V, Ly TB, Gilmour D, Boulin C, Pepperkok R, Reynaud EG (2008) In migrating cells, the Golgi complex and the position of the centrosome depend on geometrical constraints of the substratum. J Cell Sci 121:2406–2414PubMedCrossRefGoogle Scholar
  199. Qi J, Wang J, Romanyuk O, Siu CH (2006) Involvement of Src family kinases in N-cadherin phosphorylation and beta-catenin dissociation during transendothelial migration of melanoma cells. Mol Biol Cell 17:1261–1272PubMedPubMedCentralCrossRefGoogle Scholar
  200. Rappl A, Piontek G, Schlegel J (2008) EGFR-dependent migration of glial cells is mediated by reorganisation of N-cadherin. J Cell Sci 121:4089–4097PubMedCrossRefGoogle Scholar
  201. Ratner S, Sherrod WS, Lichlyter D (1997) Microtubule retraction into the uropod and its role in T cell polarization and motility. J Immunol 159:1063–1067PubMedGoogle Scholar
  202. Recher C, Ysebaert L, Beyne-Rauzy O, Mansat-De Mas V, Ruidavets JB, Cariven P, Demur C, Payrastre B, Laurent G, Racaud-Sultan C (2004) Expression of focal adhesion kinase in acute myeloid leukemia is associated with enhanced blast migration, increased cellularity, and poor prognosis. Cancer Res 64:3191–3197PubMedCrossRefGoogle Scholar
  203. Reed NA, Cai D, Blasius TL, Jih GT, Meyhofer E, Gaertig J, Verhey KJ (2006) Microtubule acetylation promotes kinesin-1 binding and transport. Curr Biol CB 16:2166–2172PubMedCrossRefGoogle Scholar
  204. Ren Y, Li R, Zheng Y, Busch H (1998) Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J Biol Chem 273:34954–34960PubMedCrossRefGoogle Scholar
  205. Revenu C, Streichan S, Dona E, Lecaudey V, Hufnagel L, Gilmour D (2014) Quantitative cell polarity imaging defines leader-to-follower transitions during collective migration and the key role of microtubule-dependent adherens junction formation. Development 141:1282–1291PubMedCrossRefGoogle Scholar
  206. Rid R, Schiefermeier N, Grigoriev I, Small JV, Kaverina I (2005) The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil Cytoskeleton 61:161–171PubMedCrossRefGoogle Scholar
  207. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302:1704–1709PubMedCrossRefGoogle Scholar
  208. Riederer BM (2007) Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein. Brain Res Bull 71:541–558PubMedCrossRefGoogle Scholar
  209. Rieger S, Senghaas N, Walch A, Koster RW (2009) Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol 7:e1000240PubMedPubMedCentralCrossRefGoogle Scholar
  210. Rivero S, Cardenas J, Bornens M, Rios RM (2009) Microtubule nucleation at the cis-side of the Golgi apparatus requires AKAP450 and GM130. EMBO J 28:1016–1028PubMedPubMedCentralCrossRefGoogle Scholar
  211. Rochlin MW, Wickline KM, Bridgman PC (1996) Microtubule stability decreases axon elongation but not axoplasm production. J Neurosci Off J Soc Neurosci 16:3236–3246Google Scholar
  212. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman-Storer CM (2003) Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat Cell Biol 5:599–609PubMedCrossRefGoogle Scholar
  213. Rogers SL, Wiedemann U, Hacker U, Turck C, Vale RD (2004) Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr Biol CB 14:1827–1833PubMedCrossRefGoogle Scholar
  214. Roll-Mecak A, Vale RD (2008) Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature 451:363–367PubMedPubMedCentralCrossRefGoogle Scholar
  215. Rooney C, White G, Nazgiewicz A, Woodcock SA, Anderson KI, Ballestrem C, Malliri A (2010) The Rac activator STEF (Tiam2) regulates cell migration by microtubule-mediated focal adhesion disassembly. EMBO Rep 11:292–298PubMedPubMedCentralCrossRefGoogle Scholar
  216. Saillour Y, Broix L, Bruel-Jungerman E, Lebrun N, Muraca G, Rucci J, Poirier K, Belvindrah R, Francis F, Chelly J (2014) Beta tubulin isoforms are not interchangeable for rescuing impaired radial migration due to Tubb3 knockdown. Hum Mol Genet 23:1516–1526PubMedCrossRefGoogle Scholar
  217. Sakakibara A, Sato T, Ando R, Noguchi N, Masaoka M, Miyata T (2014) Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization. Cereb Cortex 24:1301–1310PubMedCrossRefGoogle Scholar
  218. Sanz-Moreno V, Marshall CJ (2010) The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr Opin Cell Biol 22:690–696PubMedCrossRefGoogle Scholar
  219. Sapir T, Frotscher M, Levy T, Mandelkow EM, Reiner O (2012) Tau’s role in the developing brain: implications for intellectual disability. Hum Mol Genet 21:1681–1692PubMedCrossRefGoogle Scholar
  220. Schober JM, Cain JM, Komarova YA, Borisy GG (2009) Migration and actin protrusion in melanoma cells are regulated by EB1 protein. Cancer Lett 284:30–36PubMedCrossRefGoogle Scholar
  221. Schreiber SC, Giehl K, Kastilan C, Hasel C, Muhlenhoff M, Adler G, Wedlich D, Menke A (2008) Polysialylated NCAM represses E-cadherin-mediated cell-cell adhesion in pancreatic tumor cells. Gastroenterology 134:1555–1566PubMedCrossRefGoogle Scholar
  222. Schwartz MA (2001) Integrin signaling revisited. Trends Cell Biol 11:466–470PubMedCrossRefGoogle Scholar
  223. Shieh JC, Schaar BT, Srinivasan K, Brodsky FM, McConnell SK (2011) Endocytosis regulates cell soma translocation and the distribution of adhesion proteins in migrating neurons. PLoS One 6:e17802PubMedPubMedCentralCrossRefGoogle Scholar
  224. Shih W, Yamada S (2012) N-cadherin-mediated cell-cell adhesion promotes cell migration in a three-dimensional matrix. J Cell Sci 125:3661–3670PubMedPubMedCentralCrossRefGoogle Scholar
  225. Siegrist SE, Doe CQ (2007) Microtubule-induced cortical cell polarity. Genes Dev 21:483–496PubMedCrossRefGoogle Scholar
  226. Sirajuddin M, Rice LM, Vale RD (2014) Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol 16:335–344PubMedPubMedCentralCrossRefGoogle Scholar
  227. Sit ST, Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124:679–683PubMedCrossRefGoogle Scholar
  228. Small JV, Kaverina I (2003) Microtubules meet substrate adhesions to arrange cell polarity. Curr Opin Cell Biol 15:40–47PubMedCrossRefGoogle Scholar
  229. Spiczka KS, Yeaman C (2008) Ral-regulated interaction between Sec5 and paxillin targets Exocyst to focal complexes during cell migration. J Cell Sci 121:2880–2891PubMedPubMedCentralCrossRefGoogle Scholar
  230. Steffen A, Le Dez G, Poincloux R, Recchi C, Nassoy P, Rottner K, Galli T, Chavrier P (2008) MT1-MMP-dependent invasion is regulated by TI-VAMP/VAMP7. Curr Biol CB 18:926–931PubMedCrossRefGoogle Scholar
  231. Stehbens S, Wittmann T (2012) Targeting and transport: how microtubules control focal adhesion dynamics. J Cell Biol 198:481–489PubMedPubMedCentralCrossRefGoogle Scholar
  232. Stehbens SJ, Paterson AD, Crampton MS, Shewan AM, Ferguson C, Akhmanova A, Parton RG, Yap AS (2006) Dynamic microtubules regulate the local concentration of E-cadherin at cell-cell contacts. J Cell Sci 119:1801–1811PubMedCrossRefGoogle Scholar
  233. Steinecke A, Gampe C, Valkova C, Kaether C, Bolz J (2012) Disrupted-in-Schizophrenia 1 (DISC1) is necessary for the correct migration of cortical interneurons. J Neurosci Off J Soc Neurosci 32:738–745CrossRefGoogle Scholar
  234. Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, Hoogenraad CC, Tolic-Norrelykke IM, Bradke F (2010) Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704–707PubMedCrossRefGoogle Scholar
  235. Stramer B, Moreira S, Millard T, Evans I, Huang CY, Sabet O, Milner M, Dunn G, Martin P, Wood W (2010) Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo. J Cell Biol 189:681–689PubMedPubMedCentralCrossRefGoogle Scholar
  236. Straube A (2011) How to measure microtubule dynamics? Methods Mol Biol 777:1–14PubMedCrossRefGoogle Scholar
  237. Straube A, Merdes A (2007) EB3 regulates microtubule dynamics at the cell cortex and is required for myoblast elongation and fusion. Curr Biol CB 17:1318–1325PubMedCrossRefGoogle Scholar
  238. Sudo H, Baas PW (2010) Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J Neurosci Off J Soc Neurosci 30:7215–7226CrossRefGoogle Scholar
  239. Sudo H, Baas PW (2011) Strategies for diminishing katanin-based loss of microtubules in tauopathic neurodegenerative diseases. Hum Mol Genet 20:763–778PubMedPubMedCentralCrossRefGoogle Scholar
  240. Sudo H, Maru Y (2008) LAPSER1/LZTS2: a pluripotent tumor suppressor linked to the inhibition of katanin-mediated microtubule severing. Hum Mol Genet 17:2524–2540PubMedCrossRefGoogle Scholar
  241. Sun X, Li F, Dong B, Suo S, Liu M, Li D, Zhou J (2013) Regulation of tumor angiogenesis by the microtubule-binding protein CLIP-170. Protein Cell 4:266–276PubMedCrossRefGoogle Scholar
  242. Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979–987PubMedCrossRefGoogle Scholar
  243. Takesono A, Heasman SJ, Wojciak-Stothard B, Garg R, Ridley AJ (2010) Microtubules regulate migratory polarity through Rho/ROCK signaling in T cells. PLoS One 5:e8774PubMedPubMedCentralCrossRefGoogle Scholar
  244. Takino T, Watanabe Y, Matsui M, Miyamori H, Kudo T, Seiki M, Sato H (2006) Membrane-type 1 matrix metalloproteinase modulates focal adhesion stability and cell migration. Exp Cell Res 312:1381–1389PubMedCrossRefGoogle Scholar
  245. Tanaka E, Ho T, Kirschner MW (1995) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139–155PubMedCrossRefGoogle Scholar
  246. Tassan JP, Le Goff X (2004) An overview of the KIN1/PAR-1/MARK kinase family. Biol Cell Under Auspices Eur Cell Biol Org 96:193–199Google Scholar
  247. Theisen U, Straube E, Straube A (2012) Directional persistence of migrating cells requires Kif1C-mediated stabilization of trailing adhesions. Dev Cell 23:1153–1166PubMedCrossRefGoogle Scholar
  248. Tobin JL, Di Franco M, Eichers E, May-Simera H, Garcia M, Yan J, Quinlan R, Justice MJ, Hennekam RC, Briscoe J, Tada M, Mayor R, Burns AJ, Lupski JR, Hammond P, Beales PL (2008) Inhibition of neural crest migration underlies craniofacial dysmorphology and Hirschsprung’s disease in Bardet-Biedl syndrome. Proc Natl Acad Sci U S A 105:6714–6719PubMedPubMedCentralCrossRefGoogle Scholar
  249. Toyo-Oka K, Sasaki S, Yano Y, Mori D, Kobayashi T, Toyoshima YY, Tokuoka SM, Ishii S, Shimizu T, Muramatsu M, Hiraiwa N, Yoshiki A, Wynshaw-Boris A, Hirotsune S (2005) Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration. Hum Mol Genet 14:3113–3128PubMedCrossRefGoogle Scholar
  250. Tsai FC, Seki A, Yang HW, Hayer A, Carrasco S, Malmersjo S, Meyer T (2014) A polarized Ca2+, diacylglycerol and STIM1 signalling system regulates directed cell migration. Nat Cell Biol 16:133–144PubMedPubMedCentralCrossRefGoogle Scholar
  251. Tsai JW, Bremner KH, Vallee RB (2007) Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10:970–979PubMedCrossRefGoogle Scholar
  252. Tsai L-H, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383–388PubMedCrossRefGoogle Scholar
  253. Tsvetkov AS, Samsonov A, Akhmanova A, Galjart N, Popov SV (2007) Microtubule-binding proteins CLASP1 and CLASP2 interact with actin filaments. Cell Motil Cytoskeleton 64:519–530PubMedCrossRefGoogle Scholar
  254. Umeshima H, Hirano T, Kengaku M (2007) Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc Natl Acad Sci U S A 104:16182–16187PubMedPubMedCentralCrossRefGoogle Scholar
  255. van der Vaart B, Akhmanova A, Straube A (2009) Regulation of microtubule dynamic instability. Biochem Soc Trans 37:1007–1013PubMedCrossRefGoogle Scholar
  256. van Es JH, Giles RH, Clevers HC (2001) The many faces of the tumor suppressor gene APC. Exp Cell Res 264:126–134PubMedCrossRefGoogle Scholar
  257. Van Haastert PJ, Devreotes PN (2004) Chemotaxis: signalling the way forward. Nat Rev Mol Cell Biol 5:626–634PubMedCrossRefGoogle Scholar
  258. van Haren J, Boudeau J, Schmidt S, Basu S, Liu Z, Lammers D, Demmers J, Benhari J, Grosveld F, Debant A, Galjart N (2014) Dynamic microtubules catalyze formation of navigator-TRIO complexes to regulate neurite extension. Curr Biol CB 24:1778–1785PubMedCrossRefGoogle Scholar
  259. Vasiliev JM, Gelfand IM, Domnina LV, Ivanova OY, Komm SG, Olshevskaja LV (1970) Effect of colcemid on the locomotory behaviour of fibroblasts. J Embryol Exp Morphol 24:625–640PubMedGoogle Scholar
  260. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778–790PubMedPubMedCentralCrossRefGoogle Scholar
  261. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF (2007) Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol 176:573–580PubMedPubMedCentralCrossRefGoogle Scholar
  262. Vinogradova T, Paul R, Grimaldi AD, Loncarek J, Miller PM, Yampolsky D, Magidson V, Khodjakov A, Mogilner A, Kaverina I (2012) Concerted effort of centrosomal and Golgi-derived microtubules is required for proper Golgi complex assembly but not for maintenance. Mol Biol Cell 23:820–833PubMedPubMedCentralCrossRefGoogle Scholar
  263. Vitriol EA, Zheng JQ (2012) Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73:1068–1081PubMedPubMedCentralCrossRefGoogle Scholar
  264. Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, Foell D, Gerke V, Manitz MP, Nacken W, Werner S, Sorg C, Roth J (2004) MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 104:4260–4268PubMedCrossRefGoogle Scholar
  265. Wakelam MJ (1985) The fusion of myoblasts. Biochem J 228:1–12PubMedPubMedCentralCrossRefGoogle Scholar
  266. Wang CQ, Qu X, Zhang XY, Zhou CJ, Liu GX, Dong ZQ, Wei FC, Sun SZ (2010) Overexpression of Kif2a promotes the progression and metastasis of squamous cell carcinoma of the oral tongue. Oral Oncol 46:65–69PubMedCrossRefGoogle Scholar
  267. Wang J, Ma S, Ma R, Qu X, Liu W, Lv C, Zhao S, Gong Y (2014) KIF2A silencing inhibits the proliferation and migration of breast cancer cells and correlates with unfavorable prognosis in breast cancer. BMC Cancer 14:461PubMedPubMedCentralCrossRefGoogle Scholar
  268. Wang Y, McNiven MA (2012) Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J Cell Biol 196:375–385PubMedPubMedCentralCrossRefGoogle Scholar
  269. Watanabe T, Noritake J, Kakeno M, Matsui T, Harada T, Wang S, Itoh N, Sato K, Matsuzawa K, Iwamatsu A, Galjart N, Kaibuchi K (2009a) Phosphorylation of CLASP2 by GSK-3beta regulates its interaction with IQGAP1, EB1 and microtubules. J Cell Sci 122:2969–2979PubMedCrossRefGoogle Scholar
  270. Watanabe T, Sato K, Kaibuchi K (2009b) Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. Cold Spring Harb Perspect Biol 1:a003020PubMedPubMedCentralCrossRefGoogle Scholar
  271. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K (2004) Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell 7:871–883PubMedCrossRefGoogle Scholar
  272. Waterman-Storer CM, Salmon ED (1997) Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J Cell Biol 139:417–434PubMedPubMedCentralCrossRefGoogle Scholar
  273. Waterman-Storer CM, Salmon ED (1998) Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol CB 8:798–806PubMedCrossRefGoogle Scholar
  274. Waterman-Storer CM, Salmon WC, Salmon ED (2000) Feedback interactions between cell-cell adherens junctions and cytoskeletal dynamics in newt lung epithelial cells. Mol Biol Cell 11:2471–2483PubMedPubMedCentralCrossRefGoogle Scholar
  275. Waterman-Storer CM, Worthylake RA, Liu BP, Burridge K, Salmon ED (1999) Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat Cell Biol 1:45–50PubMedCrossRefGoogle Scholar
  276. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF (2004) FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6:154–161PubMedCrossRefGoogle Scholar
  277. Weber GF, Bjerke MA, DeSimone DW (2012) A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22:104–115PubMedPubMedCentralCrossRefGoogle Scholar
  278. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS, Gundersen GG (2004) EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nat Cell Biol 6:820–830PubMedCrossRefGoogle Scholar
  279. Werr J, Xie X, Hedqvist P, Ruoslahti E, Lindbom L (1998) beta1 integrins are critically involved in neutrophil locomotion in extravascular tissue In vivo. J Exp Med 187:2091–2096PubMedPubMedCentralCrossRefGoogle Scholar
  280. Wickstrom SA, Lange A, Hess MW, Polleux J, Spatz JP, Kruger M, Pfaller K, Lambacher A, Bloch W, Mann M, Huber LA, Fassler R (2010) Integrin-linked kinase controls microtubule dynamics required for plasma membrane targeting of caveolae. Dev Cell 19:574–588PubMedPubMedCentralCrossRefGoogle Scholar
  281. Wiesner C, Faix J, Himmel M, Bentzien F, Linder S (2010) KIF5B and KIF3A/KIF3B kinesins drive MT1-MMP surface exposure, CD44 shedding, and extracellular matrix degradation in primary macrophages. Blood 116:1559–1569PubMedCrossRefGoogle Scholar
  282. Willemsen MH, Vissers LE, Willemsen MA, van Bon BW, Kroes T, de Ligt J, de Vries BB, Schoots J, Lugtenberg D, Hamel BC, van Bokhoven H, Brunner HG, Veltman JA, Kleefstra T (2012) Mutations in DYNC1H1 cause severe intellectual disability with neuronal migration defects. J Med Genet 49:179–183PubMedCrossRefGoogle Scholar
  283. Williamson T, Gordon-Weeks PR, Schachner M, Taylor J (1996) Microtubule reorganization is obligatory for growth cone turning. Proc Natl Acad Sci U S A 93:15221–15226PubMedPubMedCentralCrossRefGoogle Scholar
  284. Wittmann T, Bokoch GM, Waterman-Storer CM (2004) Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem 279:6196–6203PubMedCrossRefGoogle Scholar
  285. Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker EB, Friedl P (2003a) Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J Cell Biol 160:267–277PubMedPubMedCentralCrossRefGoogle Scholar
  286. Wolf K, Muller R, Borgmann S, Brocker EB, Friedl P (2003b) Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 102:3262–3269PubMedCrossRefGoogle Scholar
  287. Wu X, Kodama A, Fuchs E (2008) ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135:137–148PubMedPubMedCentralCrossRefGoogle Scholar
  288. Wu Y, Song SW, Sun J, Bruner JM, Fuller GN, Zhang W (2010) IIp45 inhibits cell migration through inhibition of HDAC6. J Biol Chem 285:3554–3560PubMedPubMedCentralCrossRefGoogle Scholar
  289. Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH (2003) Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114:469–482PubMedCrossRefGoogle Scholar
  290. Xu J, Wang F, Van Keymeulen A, Rentel M, Bourne HR (2005) Neutrophil microtubules suppress polarity and enhance directional migration. Proc Natl Acad Sci U S A 102:6884–6889PubMedPubMedCentralCrossRefGoogle Scholar
  291. Yadav S, Puri S, Linstedt AD (2009) A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol Biol Cell 20:1728–1736PubMedPubMedCentralCrossRefGoogle Scholar
  292. Yam PT, Wilson CA, Ji L, Hebert B, Barnhart EL, Dye NA, Wiseman PW, Danuser G, Theriot JA (2007) Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J Cell Biol 178:1207–1221PubMedPubMedCentralCrossRefGoogle Scholar
  293. Yanagisawa M, Kaverina IN, Wang A, Fujita Y, Reynolds AB, Anastasiadis PZ (2004) A novel interaction between kinesin and p120 modulates p120 localization and function. J Biol Chem 279:9512–9521PubMedCrossRefGoogle Scholar
  294. Yau KW, van Beuningen SF, Cunha-Ferreira I, Cloin BM, van Battum EY, Will L, Schatzle P, Tas RP, van Krugten J, Katrukha EA, Jiang K, Wulf PS, Mikhaylova M, Harterink M, Pasterkamp RJ, Akhmanova A, Kapitein LC, Hoogenraad CC (2014) Microtubule minus-end binding protein CAMSAP2 controls axon specification and dendrite development. Neuron 82:1058–1073PubMedCrossRefGoogle Scholar
  295. Ye X, Lee YC, Choueiri M, Chu K, Huang CF, Tsai WW, Kobayashi R, Logothetis CJ, Yu-Lee LY, Lin SH (2012) Aberrant expression of katanin p60 in prostate cancer bone metastasis. Prostate 72:291–300PubMedPubMedCentralCrossRefGoogle Scholar
  296. Yilmaz M, Christofori G (2009) EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 28:15–33PubMedCrossRefGoogle Scholar
  297. Yoo SK, Lam PY, Eichelberg MR, Zasadil L, Bement WM, Huttenlocher A (2012) The role of microtubules in neutrophil polarity and migration in live zebrafish. J Cell Sci 125:5702–5710PubMedPubMedCentralCrossRefGoogle Scholar
  298. Yu W, Qiang L, Solowska JM, Karabay A, Korulu S, Baas PW (2008) The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19:1485–1498PubMedPubMedCentralCrossRefGoogle Scholar
  299. Yvon AM, Walker JW, Danowski B, Fagerstrom C, Khodjakov A, Wadsworth P (2002) Centrosome reorientation in wound-edge cells is cell type specific. Mol Biol Cell 13:1871–1880PubMedPubMedCentralCrossRefGoogle Scholar
  300. Zaidel-Bar R, Itzkovitz S, Ma’ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9:858–867PubMedPubMedCentralCrossRefGoogle Scholar
  301. Zhang D, Grode KD, Stewman SF, Diaz-Valencia JD, Liebling E, Rath U, Riera T, Currie JD, Buster DW, Asenjo AB, Sosa HJ, Ross JL, Ma A, Rogers SL, Sharp DJ (2011) Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat Cell Biol 13:361–370PubMedPubMedCentralCrossRefGoogle Scholar
  302. Zhang Y, Chen K, Tu Y, Wu C (2004) Distinct roles of two structurally closely related focal adhesion proteins, alpha-parvins and beta-parvins, in regulation of cell morphology and survival. J Biol Chem 279:41695–41705PubMedCrossRefGoogle Scholar
  303. Zhou FQ, Zhou J, Dedhar S, Wu YH, Snider WD (2004) NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897–912PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Cellular and Molecular Neurobiology, Institute of ZoologyTU BraunschweigBraunschweigGermany
  2. 2.Cytoskeletal Dynamics, Centre for Mechanochemical Cell Biology, Warwick Medical SchoolUniversity of WarwickCoventryUK

Personalised recommendations