CLASPs link focal-adhesion-associated microtubule capture to localized exocytosis and adhesion site turnover

Nature Cell Biology

Volumn 16, Issue 6, 2014, Pages 558-570

  Stehbens, Samantha J ^a,c   Paszek, Matthew ^b,d   Pemble, Hayley ^a   Ettinger, Andreas ^a   Gierke, Sarah ^a   Wittmann, Torsten ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^d Cornell University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASP PROTEIN; CLASP1 PROTEIN; CLASP2 PROTEIN; LL5BETA PROTEIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CLASP1 PROTEIN, HUMAN; CLASP2 PROTEIN, HUMAN; HYBRID PROTEIN; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE INHIBITOR; MMP14 PROTEIN, HUMAN; PHLDB2 PROTEIN, HUMAN; PHOTOPROTEIN;

ARTICLE; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIUM CELL; EXOCYTOSIS; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; MICROTUBULE; PRIORITY JOURNAL; CELL ADHESION; CELL MOTION; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; KERATINOCYTE; METABOLISM; RNA INTERFERENCE; TIME; TRANSPORT VESICLE;

CARRIER PROTEINS; CELL ADHESION; CELL MOVEMENT; EXOCYTOSIS; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; HEK293 CELLS; HUMANS; KERATINOCYTES; LUMINESCENT PROTEINS; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE INHIBITORS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION; TRANSPORT VESICLES;

EID: 84901819506     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2975     Document Type: Article

References (62)

1. Parsons, J. T., Horwitz, A. R. & Schwartz, M. A. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol Cell Biol. 11, 633-643 (2010).
2. Gardel, M. L., Schneider, I. C., Aratyn-Schaus, Y. & Waterman, C. M. Mechanical integration of actin and adhesion dynamics in cell migration. Annu. Rev. Cell Dev. Biol. 26, 315-333 (2010).
3. Stehbens, S. & Wittmann, T. Targeting and transport: How microtubules control focal adhesion dynamics. J. Cell Biol. 198, 481-489 (2012).
4. Kaverina, I., Krylyshkina, O. & Small, J. V. Microtubule targeting of substrate contacts promotes their relaxation and dissociation. J. Cell Biol. 146, 1033-1044 (1999).
5. 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. 7, 581-590 (2005). (Pubitemid 40796981)
6. 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. 187, 733-747 (2009).
7. Rooney, C. et al. The Rac activator STEF (Tiam2) regulates cell migration by microtubule-mediated focal adhesion disassembly. EMBO Rep. 11, 292-298 (2010).
8. Kumar, P. & Wittmann, T. +TIPs: SxIPping along microtubule ends. Trends Cell Biol. 22, 418-428 (2012).
9. Matsumoto, S., Fumoto, K., Okamoto, T., Kaibuchi, K. & Kikuchi, A. Binding of APC and dishevelled mediates Wnt5a-regulated focal adhesion dynamics in migrating cells. EMBO J. 29, 1192-1204 (2010).
10. Wu, X., Kodama, A. & Fuchs, E. ACF7 regulates cytoskeletal-focal adhesion dynamics and migration and has ATPase activity. Cell 135, 137-148 (2008).
11. Kumar, P. et al. GSK3beta phosphorylation modulates CLASP-microtubule association and lamella microtubule attachment. J. Cell Biol. 184, 895-908 (2009).
12. Mimori-Kiyosue, Y. et al. CLASP1 and CLASP2 bind to EB1 and regulate microtubule plus-end dynamics at the cell cortex. J. Cell Biol. 168, 141-153 (2005). (Pubitemid 40111064)
13. Mimori-Kiyosue, Y. et al. Mammalian CLASPs are required for mitotic spindle organization and kinetochore alignment. Genes Cells 11, 845-857 (2006). (Pubitemid 44084022)
14. Miller, P. M. et al. Golgi-derived CLASP-dependent microtubules control Golgi organization and polarized trafficking in motile cells. Nat. Cell Biol. 11, 1069-1080 (2009).
15. Paszek, M. J. et al. Scanning angle interference microscopy reveals cell dynamics at the nanoscale. Nat. Methods 9, 825-827 (2012).
16. Krylyshkina, O. et al. Nanometer targeting of microtubules to focal adhesions. J. Cell Biol. 161, 853-859 (2003). (Pubitemid 36718419)
17. Kanchanawong, P. et al. Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584 (2010).
18. Meenderink, L. M. et al. P130Cas Src-binding and substrate domains have distinct roles in sustaining focal adhesion disassembly and promoting cell migration. PLoS ONE 5, e13412 (2010).
19. Webb, D. J. et al. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat. Cell Biol. 6, 154-161 (2004).
20. Stehbens, S. & Wittmann, T. Analysis of focal adhesion turnover: A quantitative live cell imaging example. Methods Cell Biol. http://dx.doi.org/10. 1016/B978-0-12-420138-5.00018-5 (2014).
21. Chang, Y. C., Nalbant, P., Birkenfeld, J., Chang, Z. F. & Bokoch, G. M. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol. Cell 19, 2147-2153 (2008).
22. Katoh, K., Kano, Y., Amano, M., Kaibuchi, K. & Fujiwara, K. Stress fiber organization regulated by MLCK and Rho-kinase in cultured human fibroblasts. Am. J. Physiol. Cell Physiol. 280, C1669-C1679 (2001).
23. Lansbergen, G. et al. CLASPs attach microtubule plus ends to the cell cortex through a complex with LL5beta. Dev Cell 11, 21-32 (2006). (Pubitemid 43960805)
24. Wang, Y. & McNiven, M. A. Invasive matrix degradation at focal adhesions occurs via protease recruitment by a FAK-p130Cas complex. J. Cell Biol. 196, 375-385 (2012).
25. Massimi, P., Zori, P., Roberts, S. & Banks, L. Differential regulation of cell-cell contact, invasion and anoikis by hScrib and hDlg in keratinocytes. PLoS ONE 7, e40279 (2012).
26. Davies, B., Brown, P. D., East, N., Crimmin, M. J. & Balkwill, F. R. A synthetic matrix metalloproteinase inhibitor decreases tumor burden and prolongs survival of mice bearing human ovarian carcinoma xenografts. Cancer Res. 53, 2087-2091 (1993). (Pubitemid 23145731)
27. Chao, W. T. & Kunz, J. Focal adhesion disassembly requires clathrin-dependent endocytosis of integrins. FEBS Lett. 583, 1337-1343 (2009).
28. Yu, X. et al. N-WASP coordinates the delivery and F-actin-mediated capture of MT1-MMP at invasive pseudopods. J. Cell Biol. 199, 527-544 (2012).
29. Grigoriev, I. et al. Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers. Curr. Biol. 21, 967-974 (2011).
30. Grigoriev, I. et al. Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13, 305-314 (2007). (Pubitemid 47163607)
31. White, J. et al. Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J. Cell Biol. 147, 743-760 (1999).
32. Toomre, D., Steyer, J. A., Keller, P., Almers, W. & Simons, K. Fusion of constitutive membrane traffic with the cell surface observed by evanescent wave microscopy. J. Cell Biol. 149, 33-40 (2000). (Pubitemid 30196697)
33. Paranavitane, V., Coadwell, W. J., Eguinoa, A., Hawkins, P. T. & Stephens, L. LL5beta is a phosphatidylinositol (3, 4, 5)-trisphosphate sensor that can bind the cytoskeletal adaptor, gamma-filamin. J. Biol. Chem. 278, 1328-1335 (2003). (Pubitemid 36790818)
34. Takabayashi, T. et al. LL5beta directs the translocation of filamin A and SHIP2 to sites of phosphatidylinositol 3, 4, 5-triphosphate (PtdIns(3, 4, 5)P3) accumulation, and PtdIns(3, 4, 5)P3 localization is mutually modified by co-recruited SHIP2. J. Biol. Chem. 285, 16155-16165 (2010).
35. Nakamura, F., Stossel, T. P. & Hartwig, J. H. The filamins: Organizers of cell structure and function. Cell Adh Migr 5, 160-169 (2011).
36. Carter, W. G., Wayner, E. A., Bouchard, T. S. & Kaur, P. The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J. Cell Biol. 110, 1387-1404 (1990).
37. Hotta, A. et al. Laminin-based cell adhesion anchors microtubule plus ends to the epithelial cell basal cortex through LL5alpha/beta. J. Cell Biol. 189, 901-917 (2010).
38. Franco, S. J. & Huttenlocher, A. Regulating cell migration: Calpains make the cut. J. Cell Sci. 118, 3829-3838 (2005). (Pubitemid 41410267)
39. Storr, S. J., Carragher, N. O., Frame, M. C., Parr, T. & Martin, S. G. The calpain system and cancer. Nat. Rev. Cancer 11, 364-374 (2011).
40. Takino, T., Saeki, H., Miyamori, H., Kudo, T. & Sato, H. Inhibition of membrane-type 1 matrix metalloproteinase at cell-matrix adhesions. Cancer Res. 67, 11621-11629 (2007).
41. Gonzalo, P. et al. MT1-MMP is required for myeloid cell fusion via regulation of Rac1 signaling. Dev. Cell 18, 77-89 (2010).
42. Shi, F. & Sottile, J. MT1-MMP regulates the turnover and endocytosis of extracellular matrix fibronectin. J. Cell Sci. 124, 4039-4050 (2011).
43. Overall, C. M. & Dean, R. A. Degradomics: Systems biology of the protease web Pleiotropic roles of MMPs in cancer. Cancer Metastasis Rev. 25, 69-75 (2006). (Pubitemid 43723983)
44. Mu, D. et al. The integrin α(v)β8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 157, 493-507 (2002). (Pubitemid 34839812)
45. Chan, K. M. et al. MT1-MMP inactivates ADAM9 to regulate FGFR2 signaling and calvarial osteogenesis. Dev Cell 22, 1176-1190 (2012).
46. Rowe, R. G. & Weiss, S. J. Breaching the basement membrane: Who, when and how?. Trends Cell Biol. 18, 560-574 (2008).
47. Friedl, P. & Wolf, K. Tube travel: The role of proteases in individual and collective cancer cell invasion. Cancer Res 68, 7247-7249 (2008).
48. Bravo-Cordero, J. J. et al. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 26, 1499-1510 (2007). (Pubitemid 46480932)
49. Wiesner, C., Azzouzi, K. E. & Linder, S. A specific subset of RabGTPases controls cell surface exposure of MT1-MMP, extracellular matrix degradation and 3D invasion of macrophages. J. Cell Sci. 126, 2820-2833 (2013).
50. Monteiro, P. et al. Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J. Cell Biol. 203, 1063-1079 (2013).
51. Suozzi, K. C., Wu, X. & Fuchs, E. Spectraplakins: Master orchestrators of cytoskeletal dynamics. J. Cell Biol. 197, 465-475 (2012).
52. Burgo, A. et al. A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev Cell 23, 166-180 (2012).
53. Gierke, S. & Wittmann, T. EB1-recruited microtubule +TIP complexes coordinate protrusion dynamics during 3D epithelial remodeling. Curr. Biol. 22, 753-762 (2012).
54. Boukamp, P. et al. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771 (1988). (Pubitemid 18089976)
55. Zhao, M. et al. Assembly and initial characterization of a panel of 85 genomically validated cell lines from diverse head and neck tumor sites. Clin Cancer Res. 17, 7248-7264 (2011).
56. Stehbens, S., Pemble, H., Murrow, L. & Wittmann, T. Imaging intracellular protein dynamics by spinning disk confocal microscopy. Methods Enzymol 504, 293-313 (2012).
57. Gierke, S., Kumar, P. & Wittmann, T. Analysis of microtubule polymerization dynamics in live cells. Methods Cell Biol. 97, 15-33 (2010).
58. Hu, K., Ji, L., Applegate, K. T., Danuser, G. & Waterman-Storer, C. M. Differential transmission of actin motion within focal adhesions. Science 315, 111-115 (2007). (Pubitemid 46196992)
59. Matanis, T. et al. Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat. Cell Biol. 4, 986-992 (2002). (Pubitemid 35469430)
60. Bryant, D. M. et al. A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035-1045 (2010).
61. Moffat, J. et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298 (2006).
62. Thompson, O. et al. Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS ONE 3, e3638 (2008).