Identification of F-actin as the dynamic hub in a microbial-induced GTPase polarity circuit

Cell

Volumn 148, Issue 4, 2012, Pages 803-815

  Orchard, Robert C ^a   Kittisopikul, Mark ^a   Altschuler, Steven J ^a   Wu, Lani F ^a   Süel, Gürol M ^a   Alto, Neal M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTEGRIN; F ACTIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; PROTEIN CDC42;

ANIMAL CELL; ARTICLE; BACTERIUM ADHERENCE; CELL POLARITY; CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 84857260334     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.11.063     Document Type: Article

References (57)

1. K. Aktories Bacterial protein toxins that modify host regulatory GTPases Nat. Rev. Microbiol. 9 2011 487 498
2. M. Algrain, O. Turunen, A. Vaheri, D. Louvard, and M. Arpin Ezrin contains cytoskeleton and membrane binding domains accounting for its proposed role as a membrane-cytoskeletal linker J. Cell Biol. 120 1993 129 139
3. N.M. Alto, F. Shao, C.S. Lazar, R.L. Brost, G. Chua, S. Mattoo, S.A. McMahon, P. Ghosh, T.R. Hughes, C. Boone, and J.E. Dixon Identification of a bacterial type III effector family with G protein mimicry functions Cell 124 2006 133 145 (Pubitemid 43069315)
4. J. Banerjee, C.C. Fischer, and P.B. Wedegaertner The amino acid motif L/IIxxFE defines a novel actin-binding sequence in PDZ-RhoGEF Biochemistry 48 2009 8032 8043
5. J.M. Bellanger, C. Astier, C. Sardet, Y. Ohta, T.P. Stossel, and A. Debant The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin Nat. Cell Biol. 2 2000 888 892
6. C.N. Berger, V.F. Crepin, M.A. Jepson, A. Arbeloa, and G. Frankel The mechanisms used by enteropathogenic Escherichia coli to control filopodia dynamics Cell. Microbiol. 11 2009 309 322
7. J.L. Bos, H. Rehmann, and A. Wittinghofer GEFs and GAPs: critical elements in the control of small G proteins Cell 129 2007 865 877 (Pubitemid 46802708)
8. A. Bretscher, D. Chambers, R. Nguyen, and D. Reczek ERM-Merlin and EBP50 protein families in plasma membrane organization and function Annu. Rev. Cell Dev. Biol. 16 2000 113 143 (Pubitemid 32037502)
9. G. Buchwald, A. Friebel, J.E. Galán, W.D. Hardt, A. Wittinghofer, and K. Scheffzek Structural basis for the reversible activation of a Rho protein by the bacterial toxin SopE EMBO J. 21 2002 3286 3295 (Pubitemid 34760561)
10. C. Co, D.T. Wong, S. Gierke, V. Chang, and J. Taunton Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains Cell 128 2007 901 913 (Pubitemid 46341410)
11. D.G. Drubin, and W.J. Nelson Origins of cell polarity Cell 84 1996 335 344 (Pubitemid 26058559)
12. G. Giannone, B.J. Dubin-Thaler, H.G. Döbereiner, N. Kieffer, A.R. Bresnick, and M.P. Sheetz Periodic lamellipodial contractions correlate with rearward actin waves Cell 116 2004 431 443 (Pubitemid 38366319)
13. P. Hou, L. Estrada, A.W. Kinley, J.T. Parsons, A.B. Vojtek, and J.L. Gorski Fgd1, the Cdc42 GEF responsible for Faciogenital Dysplasia, directly interacts with cortactin and mAbp1 to modulate cell shape Hum. Mol. Genet. 12 2003 1981 1993 (Pubitemid 37038807)
14. Z. Huang, S.E. Sutton, A.J. Wallenfang, R.C. Orchard, X. Wu, Y. Feng, J. Chai, and N.M. Alto Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics Nat. Struct. Mol. Biol. 16 2009 853 860
15. A.B. Jaffe, and A. Hall Rho GTPases: biochemistry and biology Annu. Rev. Cell Dev. Biol. 21 2005 247 269 (Pubitemid 41740635)
16. B. Kenny, S. Ellis, A.D. Leard, J. Warawa, H. Mellor, and M.A. Jepson Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules Mol. Microbiol. 44 2002 1095 1107 (Pubitemid 34535543)
17. M. Machacek, L. Hodgson, C. Welch, H. Elliott, O. Pertz, P. Nalbant, A. Abell, G.L. Johnson, K.M. Hahn, and G. Danuser Coordination of Rho GTPase activities during cell protrusion Nature 461 2009 99 103
18. H. Miki, T. Sasaki, Y. Takai, and T. Takenawa Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP Nature 391 1998 93 96 (Pubitemid 28079222)
19. S. Miyamoto, S.K. Akiyama, and K.M. Yamada Synergistic roles for receptor occupancy and aggregation in integrin transmembrane function Science 267 1995 883 885
20. P. Nalbant, L. Hodgson, V. Kraynov, A. Toutchkine, and K.M. Hahn Activation of endogenous Cdc42 visualized in living cells Science 305 2004 1615 1619 (Pubitemid 39296355)
21. K.C. Park, F. Rivero, R. Meili, S. Lee, F. Apone, and R.A. Firtel Rac regulation of chemotaxis and morphogenesis in Dictyostelium EMBO J. 23 2004 4177 4189 (Pubitemid 39546156)
22. T.D. Pollard, and J.A. Cooper Actin, a central player in cell shape and movement Science 326 2009 1208 1212
23. J. Riedl, A.H. Crevenna, K. Kessenbrock, J.H. Yu, D. Neukirchen, M. Bista, F. Bradke, D. Jenne, T.A. Holak, and Z. Werb Lifeact: a versatile marker to visualize F-actin Nat. Methods 5 2008 605 607 (Pubitemid 351911864)
24. H.S. Saleh, U. Merkel, K.J. Geissler, T. Sperka, A. Sechi, C. Breithaupt, and H. Morrison Properties of an ezrin mutant defective in F-actin binding J. Mol. Biol. 385 2009 1015 1031
25. N. Simpson, R. Shaw, V.F. Crepin, R. Mundy, A.J. FitzGerald, N. Cummings, A. Straatman-Iwanowska, I. Connerton, S. Knutton, and G. Frankel The enteropathogenic Escherichia coli type III secretion system effector Map binds EBP50/NHERF1: implication for cell signalling and diarrhoea Mol. Microbiol. 60 2006 349 363
26. T.M. Svitkina, E.A. Bulanova, O.Y. Chaga, D.M. Vignjevic, S. Kojima, J.M. Vasiliev, and G.G. Borisy Mechanism of filopodia initiation by reorganization of a dendritic network J. Cell Biol. 160 2003 409 421 (Pubitemid 36182731)
27. J.A. Theriot, T.J. Mitchison, L.G. Tilney, and D.A. Portnoy The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization Nature 357 1992 257 260
28. T. Tobe, S.A. Beatson, H. Taniguchi, H. Abe, C.M. Bailey, A. Fivian, R. Younis, S. Matthews, O. Marches, and G. Frankel An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination Proc. Natl. Acad. Sci. USA 103 2006 14941 14946 (Pubitemid 44527833)
29. O. Turunen, T. Wahlström, and A. Vaheri Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family J. Cell Biol. 126 1994 1445 1453 (Pubitemid 24284609)
30. A. Upadhyay, H.L. Wu, C. Williams, T. Field, E.E. Galyov, J.M. van den Elsen, and S. Bagby The guanine-nucleotide-exchange factor BopE from Burkholderia pseudomallei adopts a compact version of the Salmonella SopE/SopE2 fold and undergoes a closed-to-open conformational change upon interaction with Cdc42 Biochem. J. 411 2008 485 493 (Pubitemid 351600733)
31. N. Watanabe, and T.J. Mitchison Single-molecule speckle analysis of actin filament turnover in lamellipodia Science 295 2002 1083 1086 (Pubitemid 34132240)
32. R. Wedlich-Soldner, and R. Li Spontaneous cell polarization: undermining determinism Nat. Cell Biol. 5 2003 267 270 (Pubitemid 36432283)
33. R. Wedlich-Soldner, S. Altschuler, L. Wu, and R. Li Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase Science 299 2003 1231 1235 (Pubitemid 36237464)
34. O.D. Weiner, W.A. Marganski, L.F. Wu, S.J. Altschuler, and M.W. Kirschner An actin-based wave generator organizes cell motility PLoS Biol. 5 2007 e221
35. J. Xu, F. Wang, A. Van Keymeulen, P. Herzmark, A. Straight, K. Kelly, Y. Takuwa, N. Sugimoto, T. Mitchison, and H.R. Bourne Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils Cell 114 2003 201 214 (Pubitemid 36936914)
36. B. Yu, I.R. Martins, P. Li, G.K. Amarasinghe, J. Umetani, M.E. Fernandez-Zapico, D.D. Billadeau, M. Machius, D.R. Tomchick, and M.K. Rosen Structural and energetic mechanisms of cooperative autoinhibition and activation of Vav1 Cell 140 2010 246 256
37. Banerjee, J., Fischer, C.C., and Wedegaertner, P.B. (2009). The amino acid motif L/IIxxFE defines a novel actin-binding sequence in PDZ-RhoGEF. Biochemistry 48, 8032-8043.
38. Bellanger, J.M., Astier, C., Sardet, C., Ohta, Y., Stossel, T.P., and Debant, A. (2000). The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat. Cell Biol. 2, 888-892.
39. Bi, F., Debreceni, B., Zhu, K., Salani, B., Eva, A., and Zheng, Y. (2001). Autoinhibition mechanism of proto-Dbl. Mol. Cell. Biol. 21, 1463-1474. (Pubitemid 32156366)
40. Diakowski, W., Grzybek, M., and Sikorski, A.F. (2006). Protein 4.1, a component of the erythrocyte membrane skeleton and its related homologue proteins forming the protein 4.1/FERM superfamily. Folia Histochem. Cytobiol. 44, 231-248. (Pubitemid 44696964)
41. Djinovic-Carugo, K., Gautel, M., Ylänne, J., and Young, P. (2002). The spectrin repeat: a structural platform for cytoskeletal protein assemblies. FEBS Lett. 513, 119-123. (Pubitemid 34242988)
42. Friebel, A., Ilchmann, H., Aepfelbacher, M., Ehrbar, K., Machleidt, W., and Hardt, W.D. (2001). SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J. Biol. Chem. 276, 34035-34040.
43. Hou, P., Estrada, L., Kinley, A.W., Parsons, J.T., Vojtek, A.B., and Gorski, J.L. (2003). Fgd1, the Cdc42 GEF responsible for Faciogenital Dysplasia, directly interacts with cortactin and mAbp1 to modulate cell shape. Hum. Mol. Genet. 12, 1981-1993. (Pubitemid 37038807)
44. Huang, Z., Sutton, S.E., Wallenfang, A.J., Orchard, R.C., Wu, X., Feng, Y., Chai, J., and Alto, N.M. (2009). Structural insights into host GTPase isoform selection by a family of bacterial GEF mimics. Nat. Struct. Mol. Biol. 16, 853-860.
45. Marchand, J.B., Kaiser, D.A., Pollard, T.D., and Higgs, H.N. (2001). Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3, 76-82. (Pubitemid 32114835)
46. Marco, E., Wedlich-Soldner, R., Li, R., Altschuler, S.J., and Wu, L.F. (2007). Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity. Cell 129, 411-422. (Pubitemid 46574971)
47. Mejillano, M.R., Kojima, S., Applewhite, D.A., Gertler, F.B., Svitkina, T.M., and Borisy, G.G. (2004). Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373. (Pubitemid 39061116)
48. Milo, R., Jorgensen, P., Moran, U., Weber, G., and Springer, M. (2010). BioNumbers - the database of key numbers in molecular and cell biology. Nucleic Acids Res. 38 (Database issue), D750-D753.
49. Obaishi, H., Nakanishi, H., Mandai, K., Satoh, K., Satoh, A., Takahashi, K., Miyahara, M., Nishioka, H., Takaishi, K., and Takai, Y. (1998). Frabin, a novel FGD1-related actin filament-binding protein capable of changing cell shape and activating c-Jun N-terminal kinase. J. Biol. Chem. 273, 18697-18700. (Pubitemid 28366250)
50. Olson, M.F., Sterpetti, P., Nagata, K., Toksoz, D., and Hall, A. (1997). Distinct roles for DH and PH domains in the Lbc oncogene. Oncogene 15, 2827-2831. (Pubitemid 28004571)
51. Rottner, K., Behrendt, B., Small, J.V., and Wehland, J. (1999). VASP dynamics during lamellipodia protrusion. Nat. Cell Biol. 1, 321-322. (Pubitemid 129495784)
52. Roy, C., Martin, M., and Mangeat, P. (1997). A dual involvement of the amino-terminal domain of ezrin in F- and G-actin binding. J. Biol. Chem. 272, 20088-20095. (Pubitemid 27340115)
53. Strauss, W. (1992). Partial Differential Equations: An Introduction (New York: John Wiley & Sons, Inc.).
54. Wedlich-Soldner, R., Altschuler, S., Wu, L., and Li, R. (2003). Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299, 1231-1235. (Pubitemid 36237464)
55. Yu, B., Martins, I.R., Li, P., Amarasinghe, G.K., Umetani, J., Fernandez-Zapico, M.E., Billadeau, D.D., Machius, M., Tomchick, D.R., and Rosen, M.K. (2010). Structural and energetic mechanisms of cooperative autoinhibition and activation of Vav1. Cell 140, 246-256.
56. Zhang, B., Wang, Z.X., and Zheng, Y. (1997). Characterization of the interactions between the small GTPase Cdc42 and its GTPase-activating proteins and putative effectors. Comparison of kinetic properties of Cdc42 binding to the Cdc42-interactive domains. J. Biol. Chem. 272, 21999-22007. (Pubitemid 27382823)
57. Zhao, L., Sukstanskii, A.L., Kroenke, C.D., Song, J., Piwnica-Worms, D., Ackerman, J.J., and Neil, J.J. (2008). Intracellular water specific MR of microbead-adherent cells: HeLa cell intracellular water diffusion. Magn. Reson. Med. 59, 79-84.