N-WASP regulates the epithelial junctional actin cytoskeleton through a non-canonical post-nucleation pathway

Nature Cell Biology

Volumn 13, Issue 8, 2011, Pages 934-943

  Kovacs, Eva M ^a   Verma, Suzie ^a   Ali, Radiya G ^a   Ratheesh, Aparna ^a   Hamilton, Nicholas A ^a   Akhmanova, Anna ^b   Yap, Alpha S ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; SMALL INTERFERING RNA;

ACTIN FILAMENT; ARTICLE; CELL JUNCTION; CELL NUCLEUS; CELL STRAIN CACO 2; CONTROLLED STUDY; CYTOSKELETON; EPITHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN STABILITY; RNA INTERFERENCE;

ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTINS; ADHERENS JUNCTIONS; CACO-2 CELLS; CARRIER PROTEINS; CYTOSKELETON; EPITHELIUM; HUMANS; MUTATION; RNA INTERFERENCE; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 79960984867     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2290     Document Type: Article

References (44)

1. Harris, T. J. & Tepass, U. Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514 (2010).
2. Mege, R. M., Gavard, J. & Lambert, M. Regulation of cellcell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18, 541-548 (2006).
3. Boller, K., Vestweber, D. & Kemler, R. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J. Cell Biol. 100, 327-332 (1985). (Pubitemid 15151911)
4. Sawyer, J. K., Harris, N. J., Slep, K. C., Gaul, U. & Peifer, M. The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction. J. Cell Biol. 186, 57-73 (2009).
5. Costa, M. et al. A putative catenincadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J. Cell Biol. 141, 297-308 (1998). (Pubitemid 28182660)
6. Miyaguchi, K. Ultrastructure of the zonula adherens revealed by rapid-freeze deep-etching. J. Struct. Biol. 132, 169-178 (2000). (Pubitemid 32202930)
7. Hirokawa, N., Keller, T. C., 3rd, Chasan, R & Mooseker, M. S. Mechanism of brush border contractility studied by the quick-freeze, deep-etch method. J. Cell Biol. 96, 1325-1336 (1983). (Pubitemid 13029637)
8. Kwiatkowski A. V. et al. In vitro and in vivo reconstitution of the cad-herincatenin-actin complex from Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 107 14591-14596 (2010).
9. Smutny, M. et al. Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat. Cell Biol. 12, 696-702 (2010).
10. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. & Nelson, W. J. Deconstructing the cadherincatenin-actin complex. Cell 123, 889-901 (2005).
11. Padrick, S. B. & Rosen, M. K. Physical mechanisms of signal integration by WASP family proteins. Annu. Rev. Biochem. 79, 707-735 (2010).
12. Pollard, T. D. & Borisy, G. G. Cellular motility driven by assembly and disassembly of actin-laments. Cell 112, 453-465 (2003). (Pubitemid 36263079)
13. Machesky, L. M. & Insall, R. H. Signaling to actin dynamics. J. Cell Biol. 146, 267-272 (1999). (Pubitemid 29369765)
14. Miki, H., Sasaki, T., Takai, Y. & Takenawa, T. Induction of-lopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96 (1998). (Pubitemid 28079222)
15. Shewan, A. M. et al. Myosin 2 is a key rho kinase target necessary for the local concentration of E-cadherin at cellcell contacts. Mol. Biol. Cell 16, 4531-4532 (2005).
16. Zhang, J. et al. Actin at cellcell junctions is composed of two dynamic and functional populations. J. Cell Sci. 118, 5549-5562 (2005). (Pubitemid 43079295)
17. Chesarone, M. A. & Goode, B. L. Actin nucleation and elongation factors: mechanisms and interplay. Curr. Opin. Cell Biol. 21, 28-37 (2009).
18. Symons, M. H. & Mitchison, T. J. Control of actin polymerization in live and permeabilized-broblasts. J. Cell Biol. 114, 503-513 (1991). (Pubitemid 21909819)
19. Verma, S. et al. Arp2/3 activity is necessary for efcient formation of E-cadherin adhesive contacts. J. Biol. Chem. 279, 34062-34070 (2004). (Pubitemid 39063058)
20. Chan, A. Y. et al. EGF stimulates an increase in actin nucleation and-lament number at the leading edge of the lamellipod in mammary adenocarcinoma cells. J. Cell Sci. 111, 199-211 (1998). (Pubitemid 28064145)
21. Kovacs, E. M., Goodwin, M., Ali, R. G., Paterson, A. D. & Yap, A. S. Cadherin-directed actin assembly: E-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr. Biol. 12, 379-382 (2002). (Pubitemid 34209284)
22. Nolen, B. J. et al. Characterization of two classes of small molecule inhibitors of Arp2/3 complex. Nature 460, 1031-1034 (2009).
23. Ivanov, A. I., Hunt, D., Utech, M., Nusrat, A. & Parkos, C. A. Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol. Biol. Cell 16, 2636-2650 (2005). (Pubitemid 40741212)
24. Kueh, H. Y., Charras, G. T., Mitchison, T. J. & Brieher, W. M. Actin disassembly by colin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers. J. Cell Biol. 182, 341-353 (2008).
25. Yarar, D., To, W., Abo, A. & Welch, M. D. The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr. Biol. 9, 555-558 (1999). (Pubitemid 29257114)
26. Rohatgi, R. et al. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231 (1999).
27. Kato, M. et al. WICH, a novel verprolin homology domain-containing protein that functions cooperatively with N-WASP in actin-microspike formation. Biochem. Biophys. Res. Commun. 291, 41-47 (2002). (Pubitemid 34681135)
28. Aspenstrom, P. The mammalian verprolin homologue WIRE participates in receptor-mediated endocytosis and regulation of the actin-lament system by distinct mechanisms. Exp. Cell Res. 298, 485-498 (2004). (Pubitemid 38950865)
29. Anton, I. M., Jones, G. E., Wandosell, F., Geha, R. & Ramesh, N. WASP-interacting protein (WIP): working in polymerisation and much more. Trends Cell Biol. 17, 555-562 (2007). (Pubitemid 350087660)
30. Chou, H. C. et al. WIP regulates the stability and localization of WASP to podosomes in migrating dendritic cells. Curr. Biol. 16, 2337-2344 (2006).
31. Volkman, B. F., Prehoda, K. E., Scott, J. A., Peterson, F. C. & Lim, W. A. Structure of the N-WASP EVH1 domain-WIP complex: insight into the molecular basis of Wiskott-Aldrich Syndrome. Cell 111, 565-576 (2002). (Pubitemid 35356561)
32. Peterson, F. C. et al. Multiple WASP-interacting protein recognition motifs are required for a functional interaction with N-WASP. J. Biol. Chem. 282, 8446-8453 (2007). (Pubitemid 47093567)
33. Moreau, V. et al. A complex of N-WASP and WIP integrates signalling cascades that lead to actin polymerization. Nat. Cell Biol. 2, 441-448 (2000).
34. Kato, M. & Takenawa, T. WICH, a member of WASP-interacting protein family, cross-links actin-laments. Biochem. Biophys. Res. Commun. 328, 1058-1066 (2005). (Pubitemid 40238742)
35. Otani, T., Ichii, T., Aono, S. & Takeichi, M. Cdc42 GEF Tuba regulates the junctional conguration of simple epithelial cells. J. Cell Biol. 175, 135-146 (2006). (Pubitemid 44537205)
36. Martinez-Quiles, N. et al. WIP regulates N-WASP-mediated actin polymerization and-lopodium formation. Nat. Cell Biol. 3, 484-491 (2001). (Pubitemid 32422084)
37. Leibfried, A., Fricke, R., Morgan, M. J., Bogdan, S. & Bellaiche, Y. Drosophila Cip4 and WASp dene a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis. Curr. Biol. 18, 1639-1648 (2008).
38. Schindelhauer, D. et al. Wiskott-Aldrich syndrome: no strict genotype-phenotype correlations but clustering of missense mutations in the amino-terminal part of the WASP gene product. Hum. Genet. 98, 68-76 (1996). (Pubitemid 26181285)
39. Watanabe, N. & Mitchison, T. J. Single-molecule speckle analysis of actin-lament turnover in lamellipodia. Science 295, 1083-1086 (2002). (Pubitemid 34132240)
40. Lommel, S. et al. Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella-exneri are abolished in N-WASP-defective cells. EMBO Rep. 2, 850-857 (2001). (Pubitemid 32982755)
41. Grigoriev, I. et al. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18, 177-182 (2008).
42. Reynolds, A. et al. Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330 (2004). (Pubitemid 38295766)
43. Rubinson, D. A. et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33, 401-406 (2003). (Pubitemid 36278858)
44. Vitriol, E. A., Uetrecht, A. C., Shen, F., Jacobson, K. & Bear, J. E. Enhanced EGFP-chromophore-assisted laser inactivation using decient cells rescued with functional EGFP-fusion proteins. Proc. Natl Acad. Sci. USA 104, 6702-6707 (2007). (Pubitemid 47175564)