Dimeric WH2 domains in Vibrio VopF promote actin filament barbed-end uncapping and assisted elongation

Nature Structural and Molecular Biology

Volumn 20, Issue 9, 2013, Pages 1069-1076

  Pernier, Julien ^a   Orban, Jozsef ^a,b   Avvaru, Balendu Sankara ^a   Jégou, Antoine ^a   Romet Lemonne, Guillaume ^a   Guichard, Bérengère ^a   Carlier, Marie France ^a  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b UNIVERSITY OF PÉCS   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; G ACTIN; PROFILIN; UNCLASSIFIED DRUG; WASP HOMOLOGY 2 PROTEIN;

ACTIN FILAMENT; ARTICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATORY MECHANISM; VIBRIO;

ACTIN CAPPING PROTEINS; ACTINS; ANIMALS; BACTERIAL PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RABBITS; RECOMBINANT PROTEINS; VIBRIO CHOLERAE; WISKOTT-ALDRICH SYNDROME PROTEIN FAMILY;

BACTERIA (MICROORGANISMS); VIBRIO; VIBRIO CHOLERAE; VIBRIO PARAHAEMOLYTICUS;

EID: 84883742350     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2639     Document Type: Article

References (48)

1. Insall, R.H. & Machesky, L.M. Actin dynamics at the leading edge: from simple machinery to complex networks. Dev. Cell 17, 310-322 (2009).
2. Bugyi, B. & Carlier, M.F. Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449-470 (2010).
3. Rottner, K. & Stradal, T.E. Actin dynamics and turnover in cell motility. Curr. Opin. Cell Biol. 23, 569-578 (2011).
4. Campellone, K.G. Cytoskeleton-modulating effectors of enteropathogenic and enterohaemorrhagic Escherichia coli: Tir, EspFU and actin pedestal assembly. FEBS J. 277, 2390-2402 (2010).
5. Haglund, C.M. & Welch, M.D. Pathogens and polymers: microbe-host interactions illuminate the cytoskeleton. J. Cell Biol. 195, 7-17 (2011).
6. Dodding, M.P. & Way, M. Nck-and N-WASP-dependent actin-based motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6, 536-550 (2009).
7. Haglund, C.M., Choe, J.E., Skau, C.T., Kovar, D.R. & Welch, M.D. Rickettsia Sca2 is a bacterial formin-like mediator of actin-based motility. Nat. Cell Biol. 12, 1057-1063 (2010).
8. Tam, V.C., Serruto, D., Dziejman, M., Brieher, W. & Mekalanos, J.J. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1, 95-107 (2007). (Pubitemid 46554917)
9. Liverman, A.D. et al. Arp2/3-independent assembly of actin by Vibrio type III effector VopL. Proc. Natl. Acad. Sci. USA 104, 17117-17122 (2007). (Pubitemid 350211001)
10. Rottner, K., Hänisch, J. & Campellone, K.G. WASH, WHAMM and JMY: regulation of Arp2/3 complex and beyond. Trends Cell Biol. 20, 650-661 (2010).
11. Wellington, A. et al. Spire contains actin binding domains and is related to ascidian posterior end mark-5. Development 126, 5267-5274 (1999). (Pubitemid 30015920)
12. Carroll, E.A. et al. Cordon-bleu is a conserved gene involved in neural tube formation. Dev. Biol. 262, 16-31 (2003). (Pubitemid 37153102)
13. Paunola, E., Mattila, P.K. & Lappalainen, P. WH2 domain: a small, versatile adapter for actin monomers. FEBS Lett. 513, 92-97 (2002). (Pubitemid 34242984)
14. Dominguez, R. Actin filament nucleation and elongation factors-structure-function relationships. Crit. Rev. Biochem. Mol. Biol. 44, 351-366 (2009).
15. Carlier, M.F., Husson, C., Renault, L. & Didry, D. Control of actin assembly by the WH2 domains and their multifunctional tandem repeats in Spire and Cordon-Bleu. Int. Rev. Cell. Mol. Biol. 290, 55-85 (2011).
16. Quinlan, M.E., Heuser, J.E., Kerkhoff, E. & Mullins, R.D. Drosophila Spire is an actin nucleation factor. Nature 433, 382-388 (2005). (Pubitemid 40203312)
17. Ahuja, R. et al. Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 131, 337-350 (2007). (Pubitemid 47592919)
18. Bosch, M. et al. Analysis of the function of Spire in actin assembly and its synergy with formin and profilin. Mol. Cell 28, 555-568 (2007). (Pubitemid 350137795)
19. Husson, C., Renault, L., Didry, D., Pantaloni, D. & Carlier, M.F. Cordon-Bleu uses WH2 domains as multifunctional dynamizers of actin filament assembly. Mol. Cell 43, 464-477 (2011).
20. Namgoong, S. et al. Mechanism of actin filament nucleation by Vibrio VopL and implications for tandem W domain nucleation. Nat. Struct. Mol. Biol. 18, 1060-1067 (2011).
21. Yu, B., Cheng, H.C., Brautigam, C.A., Tomchick, D.R. & Rosen, M.K. Mechanism of actin filament nucleation by the bacterial effector VopL. Nat. Struct. Mol. Biol. 18, 1068-1074 (2011).
22. Carlier, M.F. A new twist in actin filament nucleation. Nat. Struct. Mol. Biol. 18, 967-969 (2011).
23. Van Troys, M. et al. The actin binding site of thymosin ?4 mapped by mutational analysis. EMBO J. 15, 201-210 (1996). (Pubitemid 26029199)
24. Co, C., Wong, D.T., Gierke, S., Chang, V. & Taunton, J. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128, 901-913 (2007). (Pubitemid 46341410)
25. Elzinga, M. & Phelan, J.J. F-actin is intermolecularly crosslinked by N,N ?-p-phenylenedimaleimide through lysine-191 and cysteine-374. Proc. Natl. Acad. Sci. USA 81, 6599-6602 (1984). (Pubitemid 15220967)
26. De La Cruz, E.M. et al. Thymosin-?4 changes the conformation and dynamics of actin monomers. Biophys. J. 78, 2516-2527 (2000). (Pubitemid 30313811)
27. Hertzog, M. et al. The ?-thymosin/WH2 domain; structural basis for the switch from inhibition to promotion of actin assembly. Cell 117, 611-623 (2004). (Pubitemid 38692527)
28. Cooper, J.A. & Sept, D. New insights into mechanism and regulation of actin capping protein. Int. Rev. Cell. Mol. Biol. 267, 183-206 (2008).
29. Narita, A., Takeda, S., Yamashita, A. & Maéda, Y. Structural basis of actin filament capping at the barbed-end: a cryo-electron microscopy study. EMBO J. 25, 5626-5633 (2006). (Pubitemid 44847202)
30. Kim, T., Cooper, J.A. & Sept, D. The interaction of capping protein with the barbed end of the actin filament. J. Mol. Biol. 404, 794-802 (2010).
31. Wear, M.A., Yamashita, A., Kim, K., Maéda, Y. & Cooper, J.A. How capping protein binds the barbed end of the actin filament. Curr. Biol. 13, 1531-1537 (2003). (Pubitemid 37078410)
32. Fujiwara, I., Remmert, K. & Hammer, J.A. III. Direct observation of the uncapping of capping protein-capped actin filaments by CARMIL homology domain 3. J. Biol. Chem. 285, 2707-2720 (2010).
33. Jégou, A. et al. Individual actin filaments in a microfluidic flow reveal the mechanism of ATP hydrolysis and give insight into the properties of profilin. PLoS Biol. 9, e1001161 (2011).
34. Oda, T., Iwasa, M., Aihara, T., Maéda, Y. & Narita, A. The nature of the globular-to fibrous-actin transition. Nature 457, 441-445 (2009).
35. Yamashita, A., Maeda, K. & Maéda, Y. Crystal structure of CapZ: structural basis for actin filament barbed end capping. EMBO J. 22, 1529-1538 (2003). (Pubitemid 36417402)
36. Gayathri, P. et al. A bipolar spindle of antiparallel ParM Filaments drives bacterial plasmid segregation. Science 338, 1334-1337 (2012).
37. Chereau, D. et al. Actin-bound structures of Wiskott-Aldrich syndrome protein (WASP)-homology domain 2 and the implications for filament assembly. Proc. Natl. Acad. Sci. USA 102, 16644-16649 (2005). (Pubitemid 41688830)
38. Breitsprecher, D. et al. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943-2954 (2008).
39. Hansen, S.D. & Mullins, R.D. VASP is a processive actin polymerase that requires monomeric actin for barbed end association. J. Cell Biol. 191, 571-584 (2010).
40. Tripathi, R., Kaithwas, V., Dureja, C. & Raychaudhuri, S. Alanine-scanning mutagenesis of WH2 domains of VopF reveals residues important for conferring lethality in a Saccharomyces cerevisiae model. Gene 525, 116-123 (2013).
41. Sept, D. & McCammon, J.A. Thermodynamics and kinetics of actin filament nucleation. Biophys. J. 81, 667-674 (2001). (Pubitemid 32721442)
42. Wiesner, S. et al. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J. Cell Biol. 160, 387-398 (2003). (Pubitemid 36182729)
43. Mejillano, M.R. et al. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363-373 (2004). (Pubitemid 39061116)
44. Walsh, T.P., Weber, A., Higgins, J., Bonder, E.M. & Mooseker, M.S. Effect of villin on the kinetics of actin polymerization. Biochemistry 23, 2613-2621 (1984). (Pubitemid 14122484)
45. Tam, V.C. et al. Functional analysis of VopF activity required for colonization in Vibrio cholerae. MBio. 1, e00289-10 (2010).
46. Hernandez-Valladares, M. et al. Structural characterization of a capping protein interaction motif defines a family of actin filament regulators. Nat. Struct. Mol. Biol. 17, 497-503 (2010).
47. Arnold, K., Bordoli, L., Kopp, J. & Schwede, T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (2006). (Pubitemid 43205406)
48. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004). (Pubitemid 41742764)