Directional Persistence of Migrating Cells Requires Kif1C-Mediated Stabilization of Trailing Adhesions

Developmental Cell

Volumn 23, Issue 6, 2012, Pages 1153-1166

  Theisen, Ulrike ^a   Straube, Ekkehard ^b   Straube, Anne ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

KIF1C PROTEIN; KINESIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ARTICLE; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; MICROTUBULE; PHENOTYPE; PRIORITY JOURNAL;

CELL ADHESION; CELL LINE; CELL MOVEMENT; FIBROBLASTS; FOCAL ADHESIONS; HUMANS; INTEGRIN ALPHA5BETA1; KINESIN; MICROTUBULES; MYOSIN TYPE II; PROTEIN TRANSPORT; RETINAL PIGMENT EPITHELIUM;

EID: 84870808809     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.11.005     Document Type: Article

References (45)

1. Akhmanova A., Hoogenraad C.C., Drabek K., Stepanova T., Dortland B., Verkerk T., Vermeulen W., Burgering B.M., De Zeeuw C.I., Grosveld F., Galjart N. Clasps are CLIP-115 and -170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 2001, 104:923-935.
2. Ally S., Larson A.G., Barlan K., Rice S.E., Gelfand V.I. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J. Cell Biol. 2009, 187:1071-1082.
3. Ballestrem C., Hinz B., Imhof B.A., Wehrle-Haller B. Marching at the front and dragging behind: differential alphaVbeta3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 2001, 155:1319-1332.
4. Barkus R.V., Klyachko O., Horiuchi D., Dickson B.J., Saxton W.M. Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol. Biol. Cell 2008, 19:274-283.
5. Beningo K.A., Dembo M., Kaverina I., Small J.V., Wang Y.L. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 2001, 153:881-888.
6. Bershadsky A., Chausovsky A., Becker E., Lyubimova A., Geiger B. Involvement of microtubules in the control of adhesion-dependent signal transduction. Curr. Biol. 1996, 6:1279-1289.
7. Brandt D.T., Grosse R. Get to grips: steering local actin dynamics with IQGAPs. EMBO Rep. 2007, 8:1019-1023.
8. Brown M.C., Turner C.E. Paxillin: adapting to change. Physiol. Rev. 2004, 84:1315-1339.
9. Caswell P.T., Norman J.C. Integrin trafficking and the control of cell migration. Traffic 2006, 7:14-21.
10. Cramer L.P. Forming the cell rear first: breaking cell symmetry to trigger directed cell migration. Nat. Cell Biol. 2010, 12:628-632.
11. Geiger B., Spatz J.P., Bershadsky A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 2009, 10:21-33.
12. Gundersen G.G., Bulinski J.C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci. USA 1988, 85:5946-5950.
13. Humphries J.D., Wang P., Streuli C., Geiger B., Humphries M.J., Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 2007, 179:1043-1057.
14. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
15. Ikegami K., Heier R.L., Taruishi M., Takagi H., Mukai M., Shimma S., Taira S., Hatanaka K., Morone N., Yao I., et al. Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc. Natl. Acad. Sci. USA 2007, 104:3213-3218.
16. Kaverina I., Straube A. Regulation of cell migration by dynamic microtubules. Semin. Cell Dev. Biol. 2011, 22:968-974.
17. Kaverina I., Krylyshkina O., Small J.V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 1999, 146:1033-1044.
18. Kolega J. Asymmetric distribution of myosin IIB in migrating endothelial cells is regulated by a rho-dependent kinase and contributes to tail retraction. Mol. Biol. Cell 2003, 14:4745-4757.
19. Kopp P., Lammers R., Aepfelbacher M., Woehlke G., Rudel T., Machuy N., Steffen W., Linder S. The kinesin KIF1C and microtubule plus ends regulate podosome dynamics in macrophages. Mol. Biol. Cell 2006, 17:2811-2823.
20. Krendel M., Zenke F.T., Bokoch G.M. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 2002, 4:294-301.
21. Krylyshkina O., Kaverina I., Kranewitter W., Steffen W., Alonso M.C., Cross R.A., Small J.V. Modulation of substrate adhesion dynamics via microtubule targeting requires kinesin-1. J. Cell Biol. 2002, 156:349-359.
22. Miller P.M., Folkmann A.W., Maia A.R., Efimova N., Efimov A., Kaverina I. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 2009, 11:1069-1080.
23. Mingle L.A., Okuhama N.N., Shi J., Singer R.H., Condeelis J., Liu G. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 2005, 118:2425-2433.
24. Mseka T., Bamburg J.R., Cramer L.P. ADF/cofilin family proteins control formation of oriented actin-filament bundles in the cell body to trigger fibroblast polarization. J. Cell Sci. 2007, 120:4332-4344.
25. Nalbant P., Chang Y.C., Birkenfeld J., Chang Z.F., Bokoch G.M. Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol. Biol. Cell 2009, 20:4070-4082.
26. Palamidessi A., Frittoli E., Garré M., Faretta M., Mione M., Testa I., Diaspro A., Lanzetti L., Scita G., Di Fiore P.P. Endocytic trafficking of Rac is required for the spatial restriction of signaling in cell migration. Cell 2008, 134:135-147.
27. Powelka A.M., Sun J., Li J., Gao M., Shaw L.M., Sonnenberg A., Hsu V.W. Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 2004, 5:20-36.
28. Reed N.A., Cai D., Blasius T.L., Jih G.T., Meyhofer E., Gaertig J., Verhey K.J. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 2006, 16:2166-2172.
29. Rid R., Schiefermeier N., Grigoriev I., Small J.V., Kaverina I. The last but not the least: the origin and significance of trailing adhesions in fibroblastic cells. Cell Motil. Cytoskeleton 2005, 61:161-171.
30. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
31. Rogers K.R., Weiss S., Crevel I., Brophy P.J., Geeves M., Cross R. KIF1D is a fast non-processive kinesin that demonstrates novel K-loop-dependent mechanochemistry. EMBO J. 2001, 20:5101-5113.
32. Samora C.P., Mogessie B., Conway L., Ross J.L., Straube A., McAinsh A.D. MAP4 and CLASP1 operate as a safety mechanism to maintain a stable spindle position in mitosis. Nat. Cell Biol. 2011, 13:1040-1050.
33. Schlager M.A., Kapitein L.C., Grigoriev I., Burzynski G.M., Wulf P.S., Keijzer N., de Graaff E., Fukuda M., Shepherd I.T., Akhmanova A., Hoogenraad C.C. Pericentrosomal targeting of Rab6 secretory vesicles by Bicaudal-D-related protein 1 (BICDR-1) regulates neuritogenesis. EMBO J. 2010, 29:1637-1651.
34. Tomishige M., Klopfenstein D.R., Vale R.D. Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 2002, 297:2263-2267.
35. Uchida A., Alami N.H., Brown A. Tight functional coupling of kinesin-1A and dynein motors in the bidirectional transport of neurofilaments. Mol. Biol. Cell 2009, 20:4997-5006.
36. Vicente-Manzanares M., Koach M.A., Whitmore L., Lamers M.L., Horwitz A.F. Segregation and activation of myosin IIB creates a rear in migrating cells. J. Cell Biol. 2008, 183:543-554.
37. Vicente-Manzanares M., Ma X., Adelstein R.S., Horwitz A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 2009, 10:778-790.
38. Waterman-Storer C.M., Worthylake R.A., Liu B.P., Burridge K., Salmon E.D. Microtubule growth activates Rac1 to promote lamellipodial protrusion in fibroblasts. Nat. Cell Biol. 1999, 1:45-50.
39. Weber G.F., Bjerke M.A., DeSimone D.W. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev. Cell 2012, 22:104-115.
40. Wehrle-Haller B., Imhof B. The inner lives of focal adhesions. Trends Cell Biol. 2002, 12:382-389.
41. Yadav S., Puri S., Linstedt A.D. A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol. Biol. Cell 2009, 20:1728-1736.
42. Yam P.T., Wilson C.A., Ji L., Hebert B., Barnhart E.L., Dye N.A., Wiseman P.W., Danuser G., Theriot J.A. Actin-myosin network reorganization breaks symmetry at the cell rear to spontaneously initiate polarized cell motility. J. Cell Biol. 2007, 178:1207-1221.
43. Yang J.T., Rayburn H., Hynes R.O. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 1993, 119:1093-1105.
44. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nat. Cell Biol. 2007, 9:858-867.
45. Zhang X., Jiang G., Cai Y., Monkley S.J., Critchley D.R., Sheetz M.P. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 2008, 10:1062-1068.