Microtubules Regulate Focal Adhesion Dynamics through MAP4K4

Developmental Cell

Volumn 31, Issue 5, 2014, Pages 572-585

  Yue, Jiping ^a   Xie, Min ^b   Gou, Xuewen ^a   Lee, Philbert ^a   Schneider, Michael D ^c   Wu, Xiaoyang ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; GUANINE NUCLEOTIDE EXCHANGE FACTOR; IQ MOTIF AND SEC7 DOMAIN CONTAINING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE KINASE 4; UNCLASSIFIED DRUG; INTEGRIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; NF-KAPPA B KINASE; PROTEIN SERINE THREONINE KINASE;

ADULT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISSOLUTION; ENZYME STABILITY; FOCAL ADHESION; GENE INACTIVATION; HUMAN; HUMAN CELL; INTERNALIZATION; KERATINOCYTE; MICROTUBULE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; ANIMAL; CELL CULTURE; EXTRACELLULAR MATRIX; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; INTEGRINS; MAP KINASE KINASE KINASES; MICE; MICROTUBULES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 84918495009     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.025     Document Type: Article

References (35)

1. Akhmanova A., Steinmetz M.O. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 2008, 9:309-322.
2. 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.
3. Blanpain C., Fuchs E. Epidermal stem cells of the skin. Annu. Rev. Cell Dev. Biol. 2006, 22:339-373.
4. Calderwood D.A., Campbell I.D., Critchley D.R. Talins and kindlins: partners in integrin-mediated adhesion. Nat. Rev. Mol. Cell Biol. 2013, 14:503-517.
5. Chapman J.O., Li H., Lundquist E.A. The MIG-15 NIK kinase acts cell-autonomously in neuroblast polarization and migration in C. elegans. Dev. Biol. 2008, 324:245-257.
6. D'Souza-Schorey C., Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 2006, 7:347-358.
7. Dan I., Watanabe N.M., Kusumi A. The Ste20 group kinases as regulators of MAP kinase cascades. Trends Cell Biol. 2001, 11:220-230.
8. Dunphy J.L., Moravec R., Ly K., Lasell T.K., Melancon P., Casanova J.E. The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr. Biol. 2006, 16:315-320.
9. Ezratty E.J., Partridge M.A., Gundersen G.G. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 2005, 7:581-590.
10. Ezratty E.J., Bertaux C., Marcantonio E.E., Gundersen G.G. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J.Cell Biol. 2009, 187:733-747.
11. Franco S.J., Rodgers M.A., Perrin B.J., Han J., Bennin D.A., Critchley D.R., Huttenlocher A. Calpain-mediated proteolysis of talin regulates adhesion dynamics. Nat. Cell Biol. 2004, 6:977-983.
12. Goldspink D.A., Gadsby J.R., Bellett G., Keynton J., Tyrrell B.J., Lund E.K., Powell P.P., Thomas P., Mogensen M.M. The microtubule end-binding protein EB2 is a central regulator of microtubule reorganisation in apico-basal epithelial differentiation. J.Cell Sci. 2013, 126:4000-4014.
13. Gu Z., Noss E.H., Hsu V.W., Brenner M.B. Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J.Cell Biol. 2011, 193:61-70.
14. Hiroi T., Someya A., Thompson W., Moss J., Vaughan M. GEP100/BRAG2: activator of ADP-ribosylation factor 6 for regulation of cell adhesion and actin cytoskeleton via E-cadherin and alpha-catenin. Proc. Natl. Acad. Sci. USA 2006, 103:10672-10677.
15. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.
16. Kaverina I., Krylyshkina O., Small J.V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J.Cell Biol. 1999, 146:1033-1044.
17. Komarova Y., Lansbergen G., Galjart N., Grosveld F., Borisy G.G., Akhmanova A. EB1 and EB3 control CLIP dissociation from the ends of growing microtubules. Mol. Biol. Cell 2005, 16:5334-5345.
18. Komarova Y., De Groot C.O., Grigoriev I., Gouveia S.M., Munteanu E.L., Schober J.M., Honnappa S., Buey R.M., Hoogenraad C.C., Dogterom M., et al. Mammalian end binding proteins control persistent microtubule growth. J.Cell Biol. 2009, 184:691-706.
19. 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.
20. Kuo J.C., Han X., Hsiao C.T., Yates J.R., Waterman C.M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 2011, 13:383-393.
21. Lauffenburger D.A., Horwitz A.F. Cell migration: a physically integrated molecular process. Cell 1996, 84:359-369.
22. Lewellyn L., Cetera M., Horne-Badovinac S. Misshapen decreases integrin levels to promote epithelial motility and planar polarity in Drosophila. J.Cell Biol. 2013, 200:721-729.
23. Moravec R., Conger K.K., D'Souza R., Allison A.B., Casanova J.E. BRAG2/GEP100/IQSec1 interacts with clathrin and regulates α5β1 integrin endocytosis through activation of ADP ribosylation factor 5 (Arf5). J.Biol. Chem. 2012, 287:31138-31147.
24. Morishige M., Hashimoto S., Ogawa E., Toda Y., Kotani H., Hirose M., Wei S., Hashimoto A., Yamada A., Yano H., et al. GEP100 links epidermal growth factor receptor signalling to Arf6 activation to induce breast cancer invasion. Nat. Cell Biol. 2008, 10:85-92.
25. Ong S.E., Foster L.J., Mann M. Mass spectrometric-based approaches in quantitative proteomics. Methods 2003, 29:124-130.
26. Rodriguez O.C., Schaefer A.W., Mandato C.A., Forscher P., Bement W.M., Waterman-Storer C.M. Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 2003, 5:599-609.
27. Santy L.C. Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J.Biol. Chem. 2002, 277:40185-40188.
28. Schweitzer J.K., Sedgwick A.E., D'Souza-Schorey C. ARF6-mediated endocytic recycling impacts cell movement, cell division and lipid homeostasis. Semin. Cell Dev. Biol. 2011, 22:39-47.
29. Someya A., Sata M., Takeda K., Pacheco-Rodriguez G., Ferrans V.J., Moss J., Vaughan M. ARF-GEP(100), a guanine nucleotide-exchange protein for ADP-ribosylation factor 6. Proc. Natl. Acad. Sci. USA 2001, 98:2413-2418.
30. Someya A., Moss J., Nagaoka I. The guanine nucleotide exchange protein for ADP-ribosylation factor 6, ARF-GEP100/BRAG2, regulates phagocytosis of monocytic phagocytes in an ARF6-dependent process. J.Biol. Chem. 2010, 285:30698-30707.
31. Su Y.C., Treisman J.E., Skolnik E.Y. The Drosophila Ste20-related kinase misshapen is required for embryonic dorsal closure and acts through a JNK MAPK module on an evolutionarily conserved signaling pathway. Genes Dev. 1998, 12:2371-2380.
32. Wu X., Gan B., Yoo Y., Guan J.L. FAK-mediated src phosphorylation of endophilin A2 inhibits endocytosis of MT1-MMP and promotes ECM degradation. Dev. Cell 2005, 9:185-196.
33. Wu X., Kodama A., Fuchs E. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 2008, 135:137-148.
34. Wu X., Shen Q.T., Oristian D.S., Lu C.P., Zheng Q., Wang H.W., Fuchs E. Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3β. Cell 2011, 144:341-352.
35. Xue Y., Wang X., Li Z., Gotoh N., Chapman D., Skolnik E.Y. Mesodermal patterning defect in mice lacking the Ste20 NCK interacting kinase (NIK). Development 2001, 128:1559-1572.