Skip to main content
SpringerLink
Log in

Microtubules Regulate Cell Migration and Neuronal Pathfinding

  • Chapter
  • First Online:
The Microtubule Cytoskeleton

  • 1046 Accesses

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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 159:731–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:923–935

    Article  CAS  PubMed  Google Scholar 

  • Akhtar N, Streuli CH (2013) An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat Cell Biol 15:17–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aman A, Piotrowski T (2008) Wnt/beta-catenin and Fgf signaling control collective cell migration by restricting chemokine receptor expression. Dev Cell 15:749–761

    Article  CAS  PubMed  Google Scholar 

  • Amano M, Nakayama M, Kaibuchi K (2010) Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton 67:545–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:193–200

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1714–1724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bachmann A, Straube A (2015) Kinesins in cell migration. Biochem Soc Trans 43:79–83

    Article  CAS  PubMed  Google Scholar 

  • Badano JL, Teslovich TM, Katsanis N (2005) The centrosome in human genetic disease. Nat Rev Genet 6:194–205

    Article  CAS  PubMed  Google Scholar 

  • 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):424–437

    Article  CAS  PubMed  Google Scholar 

  • Brahn E, Tang C, Banquerigo ML (1994) Regression of collagen-induced arthritis with taxol, a microtubule stabilizer. Arthritis Rheum 37:839–845

    Article  CAS  PubMed  Google Scholar 

  • 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 178:193–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 206:97–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bretscher MS (1989) Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J 8:1341–1348

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bretscher MS (2008) On the shape of migrating cells–a ‘front-to-back’ model. J Cell Sci 121:2625–2628

    Article  CAS  PubMed  Google Scholar 

  • Bretscher MS, Aguado-Velasco C (1998) Membrane traffic during cell locomotion. Curr Opin Cell Biol 10:537–541

    Article  CAS  PubMed  Google Scholar 

  • 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 2:1554–1562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briggs MW, Li Z, Sacks DB (2002) IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J Biol Chem 277:7453–7465

    Article  CAS  PubMed  Google Scholar 

  • Briggs MW, Sacks DB (2003a) IQGAP1 as signal integrator: Ca2+, calmodulin, Cdc42 and the cytoskeleton. FEBS Lett 542:7–11

    Article  CAS  PubMed  Google Scholar 

  • Briggs MW, Sacks DB (2003b) IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep 4:571–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buck KB, Zheng JQ (2002) Growth cone turning induced by direct local modification of microtubule dynamics. J Neurosci Off J Soc Neurosci 22:9358–9367

    CAS  Google Scholar 

  • Bulinski JC, Gundersen GG (1991) Stabilization of post-translational modification of microtubules during cellular morphogenesis. BioEssays News Rev Mol Cell Develop Biol 13:285–293

    Article  CAS  Google Scholar 

  • Burack MA, Silverman MA, Banker G (2000) The role of selective transport in neuronal protein sorting. Neuron 26:465–472

    Article  CAS  PubMed  Google Scholar 

  • 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:e1000216

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caspi M, Atlas R, Kantor A, Sapir T, Reiner O (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum Mol Genet 9:2205–2213

    Article  CAS  PubMed  Google Scholar 

  • Caswell P, Norman J (2008) Endocytic transport of integrins during cell migration and invasion. Trends Cell Biol 18:257–263

    Article  CAS  PubMed  Google Scholar 

  • 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 3:650–657

    Article  CAS  PubMed  Google Scholar 

  • 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 12:2047–2060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:2147–2153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chao WT, Kunz J (2009) Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett 583:1337–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 163:547–557

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:171–175

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 153:1288–1295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469–480

    Article  CAS  PubMed  Google Scholar 

  • 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 11:495–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cooper JA (2013) Cell biology in neuroscience: mechanisms of cell migration in the nervous system. J Cell Biol 202:725–734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:507–515

    CAS  Google Scholar 

  • 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 22:202–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 10:669–677

    Article  CAS  PubMed  Google Scholar 

  • de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG (2005) Centrosome localization determines neuronal polarity. Nature 436:704–708

    Article  PubMed  CAS  Google Scholar 

  • 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 14:840–850

    Article  PubMed  CAS  Google Scholar 

  • Dixit R, Ross JL, Goldman YE, Holzbaur EL (2008) Differential regulation of dynein and kinesin motor proteins by tau. Science 319:1086–1089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 16:2259–2264

    Article  CAS  PubMed  Google Scholar 

  • 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 70:811–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 130:1146–1158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunn GA, Zicha D, Fraylich PE (1997) Rapid, microtubule-dependent fluctuations of the cell margin. J Cell Sci 110(Pt 24):3091–3098

    CAS  PubMed  Google Scholar 

  • Dupin I, Camand E, Etienne-Manneville S (2009) Classical cadherins control nucleus and centrosome position and cell polarity. J Cell Biol 185:779–786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dziezanowski MA, DeStefano MJ, Rabinovitch M (1980) Effect of antitubulins on spontaneous and chemotactic migration of neutrophils under agarose. J Cell Sci 42:379–388

    CAS  PubMed  Google Scholar 

  • 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 44:209–224

    Article  CAS  PubMed  Google Scholar 

  • Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790–793

    Article  CAS  PubMed  Google Scholar 

  • 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 12:917–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:196–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 127:5179–5188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:153–163

    Article  CAS  PubMed  Google Scholar 

  • 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 127:2433–2447

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S (2004) Actin and microtubules in cell motility: which one is in control? Traffic 5:470–477

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S (2013) Microtubules in cell migration. Annu Rev Cell Dev Biol 29:471–499

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S, Hall A (2001) Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489–498

    Article  CAS  PubMed  Google Scholar 

  • Etienne-Manneville S, Hall A (2003) Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421:753–756

    Article  CAS  PubMed  Google Scholar 

  • 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 170:895–901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Euteneuer U, Schliwa M (1984) Persistent, directional motility of cells and cytoplasmic fragments in the absence of microtubules. Nature 310:58–61

    Article  CAS  PubMed  Google Scholar 

  • Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187:733–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ezratty EJ, Partridge MA, Gundersen GG (2005) Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat Cell Biol 7:581–590

    Article  CAS  PubMed  Google Scholar 

  • 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 109:5057–5062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 117:427–439

    Article  CAS  PubMed  Google Scholar 

  • 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 120:4388–4394

    Article  CAS  PubMed  Google Scholar 

  • 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 28:2331–2343

    Article  CAS  PubMed  Google Scholar 

  • Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10:445–457

    Article  CAS  PubMed  Google Scholar 

  • Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48:441–449

    Article  CAS  PubMed  Google Scholar 

  • Friedl P, Weigelin B (2008) Interstitial leukocyte migration and immune function. Nat Immunol 9:960–969

    Article  CAS  PubMed  Google Scholar 

  • Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374

    Article  CAS  PubMed  Google Scholar 

  • 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 43:369–378

    Article  CAS  PubMed  Google Scholar 

  • 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 274:26044–26050

    Article  CAS  PubMed  Google Scholar 

  • 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 109:873–885

    Article  CAS  PubMed  Google Scholar 

  • Ganguly A, Yang H, Sharma R, Patel KD, Cabral F (2012) The role of microtubules and their dynamics in cell migration. J Biol Chem 287:43359–43369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghosh-Roy A, Goncharov A, Jin Y, Chisholm AD (2012) Kinesin-13 and tubulin posttranslational modifications regulate microtubule growth in axon regeneration. Dev Cell 23:716–728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 274:2279–2285

    Article  CAS  PubMed  Google Scholar 

  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999a) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271

    Article  CAS  PubMed  Google Scholar 

  • 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 45:146–153

    Article  CAS  PubMed  Google Scholar 

  • 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 510:167–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomes ER, Jani S, Gundersen GG (2005) Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121:451–463

    Article  CAS  PubMed  Google Scholar 

  • 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 193:61–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gundersen GG, Bulinski JC (1988) Selective stabilization of microtubules oriented toward the direction of cell migration. Proc Natl Acad Sci U S A 85:5946–5950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall A (2012) Rho family GTPases. Biochem Soc Trans 40:1378–1382

    Article  CAS  PubMed  Google Scholar 

  • 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 18:708–712

    Google Scholar 

  • 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 204:669–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 15:3024–3033

    Article  CAS  PubMed  Google Scholar 

  • 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 370:216–218

    Article  CAS  PubMed  Google Scholar 

  • Hayashi K, Suzuki A, Ohno S (2012) PAR-1/MARK: a kinase essential for maintaining the dynamic state of microtubules. Cell Struct Funct 37:21–25

    Article  CAS  PubMed  Google Scholar 

  • 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 62:2125–2130

    CAS  PubMed  Google Scholar 

  • 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 63:60–71

    Article  CAS  PubMed  Google Scholar 

  • 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 14:865–873

    Article  CAS  PubMed  Google Scholar 

  • Heuberger J, Birchmeier W (2010) Interplay of cadherin-mediated cell adhesion and canonical Wnt signaling. Cold Spring Harb Perspect Biol 2:a002915

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang CF, Banker G (2012) The translocation selectivity of the kinesins that mediate neuronal organelle transport. Traffic 13:549–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Humbert PO, Grzeschik NA, Brumby AM, Galea R, Elsum I, Richardson HE (2008) Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27:6888–6907

    Article  CAS  PubMed  Google Scholar 

  • Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687

    Article  CAS  PubMed  Google Scholar 

  • Ichii T, Takeichi M (2007) p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells Devoted Mol Cell Mech 12:827–839

    Article  CAS  Google Scholar 

  • Insolera R, Shao W, Airik R, Hildebrandt F, Shi SH (2014) SDCCAG8 regulates pericentriolar material recruitment and neuronal migration in the developing cortex. Neuron 83:805–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 473:92–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 49:797–804

    Article  CAS  PubMed  Google Scholar 

  • 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 41:746–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 190:443–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 198:749–761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:295–309

    Article  CAS  PubMed  Google Scholar 

  • 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 107:12151–12156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253–265

    Article  CAS  PubMed  Google Scholar 

  • Jossin Y, Cooper JA (2011) Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat Neurosci 14:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 65:996–1006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassler S, Donninger H, Birrer MJ, Clark GJ (2012) RASSF1A and the taxol response in ovarian cancer. Mol Biol Int 2012:263267

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 26:1885–1890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaverina I, Krylyshkina O, Small JV (1999) Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J Cell Biol 146:1033–1044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaverina I, Rottner K, Small JV (1998) Targeting, capture, and stabilization of microtubules at early focal adhesions. J Cell Biol 142:181–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaverina I, Straube A (2011) Regulation of cell migration by dynamic microtubules. Semin Cell Dev Biol 22:968–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 67:588–602

    Article  CAS  PubMed  Google Scholar 

  • 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 128:45–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keren K, Pincus Z, Allen GM, Barnhart EL, Marriott G, Mogilner A, Theriot JA (2008) Mechanism of shape determination in motile cells. Nature 453:475–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:50–57

    Article  CAS  PubMed  Google Scholar 

  • Kislauskis EH, Zhu X, Singer RH (1997) beta-Actin messenger RNA localization and protein synthesis augment cell motility. J Cell Biol 136:1263–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:2331–2345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kodama A, Karakesisoglou I, Wong E, Vaezi A, Fuchs E (2003) ACF7: an essential integrator of microtubule dynamics. Cell 115:343–354

    Article  CAS  PubMed  Google Scholar 

  • 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 115:3527–3539

    CAS  PubMed  Google Scholar 

  • Komuro H, Rakic P (1998) Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J Neurosci Off J Soc Neurosci 18:1478–1490

    CAS  Google Scholar 

  • 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 17:2811–2823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kozlovsky N, Belmaker RH, Agam G (2002) GSK-3 and the neurodevelopmental hypothesis of schizophrenia. Eur Neuropsychopharmacol J Eur Coll Neuropsychopharmacol 12:13–25

    Article  CAS  Google Scholar 

  • Krendel M, Zenke FT, Bokoch GM (2002) Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat Cell Biol 4:294–301

    Article  CAS  PubMed  Google Scholar 

  • 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 18:910–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 161:853–859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 156:349–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 184:895–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 120:3563–3574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 80:7224–7228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 206:257–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 189:945–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lammermann T, Sixt M (2009) Mechanical modes of ‘amoeboid’ cell migration. Curr Opin Cell Biol 21:636–644

    Article  PubMed  CAS  Google Scholar 

  • Lawrence JB, Singer RH (1986) Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45:407–415

    Article  CAS  PubMed  Google Scholar 

  • Lee G, Leugers CJ (2012) Tau and tauopathies. Prog Mol Biol Transl Sci 107:263–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legate KR, Montanez E, Kudlacek O, Fassler R (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 7:20–31

    Article  CAS  PubMed  Google Scholar 

  • 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 27:2603–2615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 129:3281–3294

    CAS  PubMed  Google Scholar 

  • 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 2:150–160

    Article  CAS  PubMed  Google Scholar 

  • 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):3473–3483

    CAS  PubMed  Google Scholar 

  • 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 342:1245533

    Article  PubMed  CAS  Google Scholar 

  • Liu JS (2011) Molecular genetics of neuronal migration disorders. Curr Neurol Neurosci Rep 11:171–178

    Article  CAS  PubMed  Google Scholar 

  • 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 30:14896–14906

    Article  CAS  Google Scholar 

  • 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 135:53–63

    Article  CAS  PubMed  Google Scholar 

  • 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 23:1018–1023

    Article  CAS  PubMed  Google Scholar 

  • Luxton GW, Gundersen GG (2011) Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 23:579–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:140

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 461:99–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandeville JT, Lawson MA, Maxfield FR (1997) Dynamic imaging of neutrophil migration in three dimensions: mechanical interactions between cells and matrix. J Leukoc Biol 61:188–200

    CAS  PubMed  Google Scholar 

  • 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 102:9182–9187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margadant C, Monsuur HN, Norman JC, Sonnenberg A (2011) Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 23:607–614

    Article  CAS  PubMed  Google Scholar 

  • 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 13:285–301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 29:1192–1204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsushima K, Tokuraku K, Hasan MR, Kotani S (2012) Microtubule-associated protein 4 binds to actin filaments and modulates their properties. J Biochem 151:99–108

    Article  CAS  PubMed  Google Scholar 

  • 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:a002923

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 5:505–515

    Article  CAS  PubMed  Google Scholar 

  • Mehlen P, Puisieux A (2006) Metastasis: a question of life or death. Nat Rev Cancer 6:449–458

    Article  CAS  PubMed  Google Scholar 

  • Meyer KD, Morris JA (2009) Disc1 regulates granule cell migration in the developing hippocampus. Hum Mol Genet 18:3286–3297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 285:13121–13130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 165:407–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:1069–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 148:505–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 118:2425–2433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:1133–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):3839–3853

    CAS  PubMed  Google Scholar 

  • 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 21:3518–3528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 92:3046–3050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 178:1081–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadar VC, Ketschek A, Myers KA, Gallo G, Baas PW (2008) Kinesin-5 is essential for growth-cone turning. Curr Biol 18(24):1972–1977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakagawa S, Takeichi M (1998) Neural crest emigration from the neural tube depends on regulated cadherin expression. Development 125:2963–2971

    CAS  PubMed  Google Scholar 

  • Nakamura M, Zhou XZ, Lu KP (2001) Critical role for the EB1 and APC interaction in the regulation of microtubule polymerization. Curr Biol CB 11:1062–1067

    Article  CAS  PubMed  Google Scholar 

  • 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 20:4070–4082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 134:165–179

    Article  CAS  PubMed  Google Scholar 

  • Niethammer P, Bastiaens P, Karsenti E (2004) Stathmin-tubulin interaction gradients in motile and mitotic cells. Science 303:1862–1866

    Article  CAS  PubMed  Google Scholar 

  • Niggli V (2003) Microtubule-disruption-induced and chemotactic-peptide-induced migration of human neutrophils: implications for differential sets of signalling pathways. J Cell Sci 116:813–822

    Article  CAS  PubMed  Google Scholar 

  • Nishimura T, Kaibuchi K (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev Cell 13:15–28

    Article  CAS  PubMed  Google Scholar 

  • Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235–1244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1002698

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 91:583–592

    Article  PubMed  CAS  Google Scholar 

  • 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 189:1087–1096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oleynikov Y, Singer RH (1998) RNA localization: different zipcodes, same postman? Trends Cell Biol 8:381–383

    Article  CAS  PubMed  Google Scholar 

  • Osmani N, Peglion F, Chavrier P, Etienne-Manneville S (2010) Cdc42 localization and cell polarity depend on membrane traffic. J Cell Biol 191:1261–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 42:210–214

    CAS  PubMed  Google Scholar 

  • 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 134:135–147

    Article  CAS  PubMed  Google Scholar 

  • Palazzo AF, Eng CH, Schlaepfer DD, Marcantonio EE, Gundersen GG (2004) Localized stabilization of microtubules by integrin- and FAK-facilitated Rho signaling. Science 303:836–839

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1536–1541

    Article  CAS  PubMed  Google Scholar 

  • Paratcha G, Ledda F, Ibanez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867–879

    Article  CAS  PubMed  Google Scholar 

  • Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11:633–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 17:1623–1634

    Article  CAS  PubMed  Google Scholar 

  • 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 185:1159–1166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrie RJ, Doyle AD, Yamada KM (2009) Random versus directionally persistent cell migration. Nat Rev Mol Cell Biol 10:538–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 287:35333–35340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:2029–2037

    Article  CAS  PubMed  Google Scholar 

  • 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 28:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • 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 45:639–647

    Article  CAS  PubMed  Google Scholar 

  • 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 19:4462–4473

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 121:2406–2414

    Article  CAS  PubMed  Google Scholar 

  • 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 17:1261–1272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rappl A, Piontek G, Schlegel J (2008) EGFR-dependent migration of glial cells is mediated by reorganisation of N-cadherin. J Cell Sci 121:4089–4097

    Article  CAS  PubMed  Google Scholar 

  • Ratner S, Sherrod WS, Lichlyter D (1997) Microtubule retraction into the uropod and its role in T cell polarization and motility. J Immunol 159:1063–1067

    CAS  PubMed  Google Scholar 

  • 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 64:3191–3197

    Article  CAS  PubMed  Google Scholar 

  • 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 16:2166–2172

    Article  CAS  PubMed  Google Scholar 

  • 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 273:34954–34960

    Article  CAS  PubMed  Google Scholar 

  • 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 141:1282–1291

    Article  CAS  PubMed  Google Scholar 

  • 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 61:161–171

    Article  PubMed  Google Scholar 

  • 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 302:1704–1709

    Article  CAS  PubMed  Google Scholar 

  • Riederer BM (2007) Microtubule-associated protein 1B, a growth-associated and phosphorylated scaffold protein. Brain Res Bull 71:541–558

    Article  CAS  PubMed  Google Scholar 

  • Rieger S, Senghaas N, Walch A, Koster RW (2009) Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol 7:e1000240

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 28:1016–1028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochlin MW, Wickline KM, Bridgman PC (1996) Microtubule stability decreases axon elongation but not axoplasm production. J Neurosci Off J Soc Neurosci 16:3236–3246

    CAS  Google Scholar 

  • 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 5:599–609

    Article  CAS  PubMed  Google Scholar 

  • 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 14:1827–1833

    Article  CAS  PubMed  Google Scholar 

  • Roll-Mecak A, Vale RD (2008) Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature 451:363–367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:292–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:1516–1526

    Article  CAS  PubMed  Google Scholar 

  • 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 24:1301–1310

    Article  PubMed  Google Scholar 

  • Sanz-Moreno V, Marshall CJ (2010) The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr Opin Cell Biol 22:690–696

    Article  CAS  PubMed  Google Scholar 

  • 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 21:1681–1692

    Article  CAS  PubMed  Google Scholar 

  • Schober JM, Cain JM, Komarova YA, Borisy GG (2009) Migration and actin protrusion in melanoma cells are regulated by EB1 protein. Cancer Lett 284:30–36

    Article  CAS  PubMed  Google Scholar 

  • 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 134:1555–1566

    Article  CAS  PubMed  Google Scholar 

  • Schwartz MA (2001) Integrin signaling revisited. Trends Cell Biol 11:466–470

    Article  CAS  PubMed  Google Scholar 

  • 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:e17802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih W, Yamada S (2012) N-cadherin-mediated cell-cell adhesion promotes cell migration in a three-dimensional matrix. J Cell Sci 125:3661–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siegrist SE, Doe CQ (2007) Microtubule-induced cortical cell polarity. Genes Dev 21:483–496

    Article  CAS  PubMed  Google Scholar 

  • Sirajuddin M, Rice LM, Vale RD (2014) Regulation of microtubule motors by tubulin isotypes and post-translational modifications. Nat Cell Biol 16:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sit ST, Manser E (2011) Rho GTPases and their role in organizing the actin cytoskeleton. J Cell Sci 124:679–683

    Article  CAS  PubMed  Google Scholar 

  • Small JV, Kaverina I (2003) Microtubules meet substrate adhesions to arrange cell polarity. Curr Opin Cell Biol 15:40–47

    Article  CAS  PubMed  Google Scholar 

  • Spiczka KS, Yeaman C (2008) Ral-regulated interaction between Sec5 and paxillin targets Exocyst to focal complexes during cell migration. J Cell Sci 121:2880–2891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 18:926–931

    Article  CAS  PubMed  Google Scholar 

  • Stehbens S, Wittmann T (2012) Targeting and transport: how microtubules control focal adhesion dynamics. J Cell Biol 198:481–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 119:1801–1811

    Article  CAS  PubMed  Google Scholar 

  • 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 32:738–745

    Article  CAS  Google Scholar 

  • 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 327:704–707

    Article  CAS  PubMed  Google Scholar 

  • 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 189:681–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Straube A (2011) How to measure microtubule dynamics? Methods Mol Biol 777:1–14

    Article  CAS  PubMed  Google Scholar 

  • Straube A, Merdes A (2007) EB3 regulates microtubule dynamics at the cell cortex and is required for myoblast elongation and fusion. Curr Biol CB 17:1318–1325

    Article  CAS  PubMed  Google Scholar 

  • 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 30:7215–7226

    Article  CAS  Google Scholar 

  • Sudo H, Baas PW (2011) Strategies for diminishing katanin-based loss of microtubules in tauopathic neurodegenerative diseases. Hum Mol Genet 20:763–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sudo H, Maru Y (2008) LAPSER1/LZTS2: a pluripotent tumor suppressor linked to the inhibition of katanin-mediated microtubule severing. Hum Mol Genet 17:2524–2540

    Article  CAS  PubMed  Google Scholar 

  • 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 4:266–276

    Article  CAS  PubMed  Google Scholar 

  • Suzuki A, Ohno S (2006) The PAR-aPKC system: lessons in polarity. J Cell Sci 119:979–987

    Article  CAS  PubMed  Google Scholar 

  • 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:e8774

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 312:1381–1389

    Article  CAS  PubMed  Google Scholar 

  • Tanaka E, Ho T, Kirschner MW (1995) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139–155

    Article  CAS  PubMed  Google Scholar 

  • Tassan JP, Le Goff X (2004) An overview of the KIN1/PAR-1/MARK kinase family. Biol Cell Under Auspices Eur Cell Biol Org 96:193–199

    CAS  Google Scholar 

  • Theisen U, Straube E, Straube A (2012) Directional persistence of migrating cells requires Kif1C-mediated stabilization of trailing adhesions. Dev Cell 23:1153–1166

    Article  CAS  PubMed  Google Scholar 

  • 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 105:6714–6719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 14:3113–3128

    Article  CAS  PubMed  Google Scholar 

  • 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 16:133–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai JW, Bremner KH, Vallee RB (2007) Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10:970–979

    Article  CAS  PubMed  Google Scholar 

  • Tsai L-H, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46:383–388

    Article  CAS  PubMed  Google Scholar 

  • Tsvetkov AS, Samsonov A, Akhmanova A, Galjart N, Popov SV (2007) Microtubule-binding proteins CLASP1 and CLASP2 interact with actin filaments. Cell Motil Cytoskeleton 64:519–530

    Article  CAS  PubMed  Google Scholar 

  • 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 104:16182–16187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Vaart B, Akhmanova A, Straube A (2009) Regulation of microtubule dynamic instability. Biochem Soc Trans 37:1007–1013

    Article  PubMed  CAS  Google Scholar 

  • van Es JH, Giles RH, Clevers HC (2001) The many faces of the tumor suppressor gene APC. Exp Cell Res 264:126–134

    Article  PubMed  CAS  Google Scholar 

  • Van Haastert PJ, Devreotes PN (2004) Chemotaxis: signalling the way forward. Nat Rev Mol Cell Biol 5:626–634

    Article  PubMed  Google Scholar 

  • 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 24:1778–1785

    Article  PubMed  CAS  Google Scholar 

  • 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 24:625–640

    CAS  PubMed  Google Scholar 

  • 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 10:778–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 176:573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:820–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitriol EA, Zheng JQ (2012) Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73:1068–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:4260–4268

    Article  CAS  PubMed  Google Scholar 

  • Wakelam MJ (1985) The fusion of myoblasts. Biochem J 228:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 46:65–69

    Article  PubMed  CAS  Google Scholar 

  • 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 14:461

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, McNiven MA (2012) Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J Cell Biol 196:375–385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 122:2969–2979

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Sato K, Kaibuchi K (2009b) Cadherin-mediated intercellular adhesion and signaling cascades involving small GTPases. Cold Spring Harb Perspect Biol 1:a003020

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:871–883

    Article  CAS  PubMed  Google Scholar 

  • 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 139:417–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waterman-Storer CM, Salmon ED (1998) Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms. Curr Biol CB 8:798–806

    Article  CAS  PubMed  Google Scholar 

  • 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 11:2471–2483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:45–50

    Article  CAS  PubMed  Google Scholar 

  • 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 6:154–161

    Article  CAS  PubMed  Google Scholar 

  • Weber GF, Bjerke MA, DeSimone DW (2012) A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22:104–115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 6:820–830

    Article  CAS  PubMed  Google Scholar 

  • 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 187:2091–2096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:574–588

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 116:1559–1569

    Article  CAS  PubMed  Google Scholar 

  • 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 49:179–183

    Article  CAS  PubMed  Google Scholar 

  • 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 93:15221–15226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wittmann T, Bokoch GM, Waterman-Storer CM (2004) Regulation of microtubule destabilizing activity of Op18/stathmin downstream of Rac1. J Biol Chem 279:6196–6203

    Article  CAS  PubMed  Google Scholar 

  • 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 160:267–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 102:3262–3269

    Article  CAS  PubMed  Google Scholar 

  • Wu X, Kodama A, Fuchs E (2008) ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135:137–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Song SW, Sun J, Bruner JM, Fuller GN, Zhang W (2010) IIp45 inhibits cell migration through inhibition of HDAC6. J Biol Chem 285:3554–3560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 114:469–482

    Article  CAS  PubMed  Google Scholar 

  • 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 102:6884–6889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav S, Puri S, Linstedt AD (2009) A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol Biol Cell 20:1728–1736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 178:1207–1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 279:9512–9521

    Article  CAS  PubMed  Google Scholar 

  • 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 82:1058–1073

    Article  CAS  PubMed  Google Scholar 

  • 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 72:291–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yilmaz M, Christofori G (2009) EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 28:15–33

    Article  PubMed  Google Scholar 

  • 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 125:5702–5710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 19:1485–1498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:1871–1880

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaidel-Bar R, Itzkovitz S, Ma’ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9:858–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:361–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 279:41695–41705

    Article  CAS  PubMed  Google Scholar 

  • 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 42:897–912

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Cellular and Molecular Neurobiology, Institute of Zoology, TU Braunschweig, Braunschweig, 38106, Germany

    Ulrike Theisen

  2. Cytoskeletal Dynamics, Centre for Mechanochemical Cell Biology, Warwick Medical School, University of Warwick, Coventry, CV4 7AL, UK

    Anne Straube

Authors
  1. Ulrike Theisen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anne Straube
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulrike Theisen .

Editor information

Editors and Affiliations

  1. The Barcelona Institute of Science and T, Institute for Research in Biomedicine (I, Barcelona, Spain

    Jens Lüders

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer-Verlag Wien

About this chapter

Cite this chapter

Theisen, U., Straube, A. (2016). Microtubules Regulate Cell Migration and Neuronal Pathfinding. In: Lüders, J. (eds) The Microtubule Cytoskeleton. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1903-7_6

Download citation

Publish with us

Policies and ethics

Search

Navigation