Mechanism of actin filament nucleation by Vibrio VopL and implications for tandem W domain nucleation

Nature Structural and Molecular Biology

Volumn 18, Issue 9, 2011, Pages 1060-1067

  Namgoong, Suk ^a   Boczkowska, Malgorzata ^a   Glista, Michael J ^b   Winkelman, Jonathan D ^b   Rebowski, Grzegorz ^a   Kovar, David R ^b   Dominguez, Roberto ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; CELL PROTEIN; HYBRID PROTEIN; PROFILIN; PROTEIN SPIRE; PROTEIN VOPL; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; BINDING COMPETITION; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CYTOSKELETON; DIMERIZATION; EUKARYOTE; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TARGETING; VIBRIO PARAHAEMOLYTICUS;

ACTINS; BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; MICROFILAMENT PROTEINS; MICROFILAMENTS; PROFILINS; PROTEIN STRUCTURE, TERTIARY; VIBRIO PARAHAEMOLYTICUS;

EUKARYOTA; VIBRIO; VIBRIO PARAHAEMOLYTICUS;

EID: 80052471118     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2109     Document Type: Article

References (45)

1. Dominguez, R. Structural insights into de novo actin polymerization. Curr. Opin. Struct. Biol. 20, 217-225 (2010).
2. Pollard, T.D. Regulation of actin filament assembly by Arp2/3 complex and formins. Annu. Rev. Biophys. Biomol. Struct. 36, 451-477 (2007). (Pubitemid 47007562)
3. Goode, B.L. & Eck, M.J. Mechanism and function of formins in the control of actin assembly. Annu. Rev. Biochem. 76, 593-627 (2007).
4. Higgs, H.N. Formin proteins: a domain-based approach. Trends Biochem. Sci. 30, 342-353 (2005). (Pubitemid 40799053)
5. 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)
6. Ahuja, R. et al. Cordon-bleu is an actin nucleation factor and controls neuronal morphology. Cell 131, 337-350 (2007). (Pubitemid 47592919)
7. Chereau, D. et al. Leiomodin is an actin filament nucleator in muscle cells. Science 320, 239-243 (2008). (Pubitemid 351521421)
8. Morris, J.G. Jr. Cholera and other types of vibriosis: a story of human pandemics and oysters on the half shell. Clin. Infect. Dis. 37, 272-280 (2003). (Pubitemid 36930358)
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. 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)
11. Tam, V.C. et al. Functional analysis of VopF activity required for colonization in Vibrio cholerae. MBio 1 pii: e00289-10 (2010).
12. 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).
13. Jewett, T.J., Fischer, E.R., Mead, D.J. & Hackstadt, T. Chlamydial TARP is a bacterial nucleator of actin. Proc. Natl. Acad. Sci. USA 103, 15599-15604 (2006). (Pubitemid 44625638)
14. 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)
15. Quinlan, M.E., Hilgert, S., Bedrossian, A., Mullins, R.D. & Kerkhoff, E. Regulatory interactions between two actin nucleators, Spire and Cappuccino. J. Cell Biol. 179, 117-128 (2007). (Pubitemid 47606688)
16. Harris, E.S. & Higgs, H.N. Biochemical analysis of mammalian formin effects on actin dynamics. Methods Enzymol. 406, 190-214 (2006). (Pubitemid 43207441)
17. Kuhn, J.R. & Pollard, T.D. Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys. J. 88, 1387-1402 (2005). (Pubitemid 40975966)
18. Neidt, E.M., Skau, C.T. & Kovar, D.R. The cytokinesis formins from the nematode worm and fission yeast differentially mediate actin filament assembly. J. Biol. Chem. 283, 23872-23883 (2008).
19. Kovar, D.R., Harris, E.S., Mahaffy, R., Higgs, H.N. & Pollard, T.D. Control of the assembly of ATP-and ADP-actin by formins and profilin. Cell 124, 423-435 (2006). (Pubitemid 43121988)
20. Kovar, D.R. & Pollard, T.D. Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces. Proc. Natl. Acad. Sci. USA 101, 14725-14730 (2004). (Pubitemid 39410742)
21. Rebowski, G. et al. Structure of a longitudinal actin dimer assembled by tandem w domains: implications for actin filament nucleation. J. Mol. Biol. 403, 11-23 (2010).
22. Breitsprecher, D. et al. Clustering of VASP actively drives processive, WH2 domain-mediated actin filament elongation. EMBO J. 27, 2943-2954 (2008).
23. Franke, D. & Svergun, D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346 (2009).
24. Ferron, F., Rebowski, G., Lee, S.H. & Dominguez, R. Structural basis for the recruitment of profilin-actin complexes during filament elongation by Ena/VASP. EMBO J. 26, 4597-4606 (2007). (Pubitemid 350036631)
25. 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)
26. Perelroizen, I., Marchand, J.B., Blanchoin, L., Didry, D. & Carlier, M.F. Interaction of profilin with G-actin and poly(l-proline). Biochemistry 33, 8472-8478 (1994). (Pubitemid 24242684)
27. Marchand, J.B., Kaiser, D.A., Pollard, T.D. & Higgs, H.N. Interaction of WASP/Scar proteins with actin and vertebrate Arp2/3 complex. Nat. Cell Biol. 3, 76-82 (2001). (Pubitemid 32114835)
28. Pollard, T.D. & Borisy, G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465 (2003). (Pubitemid 36263079)
29. Paul, A.S. & Pollard, T.D. The role of the FH1 domain and profilin in formin-mediated actin-filament elongation and nucleation. Curr. Biol. 18, 9-19 (2008).
30. Zuchero, J.B., Coutts, A.S., Quinlan, M.E., Thangue, N.B. & Mullins, R.D. p53-cofactor JMY is a multifunctional actin nucleation factor. Nat. Cell Biol. 11, 451-459 (2009).
31. Oda, T., Iwasa, M., Aihara, T., Maeda, Y. & Narita, A. The nature of the globular-to fibrous-actin transition. Nature 457, 441-445 (2009).
32. Fujii, T., Iwane, A.H., Yanagida, T. & Namba, K. Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467, 724-728 (2010).
33. Pechlivanis, M., Samol, A. & Kerkhoff, E. Identification of a short Spir interaction sequence at the C-terminal end of formin subgroup proteins. J. Biol. Chem. 284, 25324-25333 (2009).
34. Dahlgaard, K., Raposo, A.A., Niccoli, T. & St. Johnston, D. Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev. Cell 13, 539-553 (2007). (Pubitemid 47500810)
35. Okada, K. et al. Adenomatous polyposis coli protein nucleates actin assembly and synergizes with the formin mDia1. J. Cell Biol. 189, 1087-1096 (2010).
36. Svergun, D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 (1992). (Pubitemid 23564996)
37. Boczkowska, M. et al. X-ray scattering study of activated Arp2/3 complex with bound actin-WCA. Structure 16, 695-704 (2008). (Pubitemid 351626898)
38. Beckett, D., Kovaleva, E. & Schatz, P.J. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8, 921-929 (1999). (Pubitemid 29165423)
39. Smith, P.A. et al. A plasmid expression system for quantitative in vivo biotinylation of thioredoxin fusion proteins in Escherichia coli. Nucleic Acids Res. 26, 1414-1420 (1998). (Pubitemid 28291615)
40. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
41. Sheldrick, G.M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
42. Cowtan, K. Recent developments in classical density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 470-478 (2010).
43. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
44. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
45. Volkov, V.V. & Svergun, D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).