Electron Tomography and Simulation of Baculovirus Actin Comet Tails Support a Tethered Filament Model of Pathogen Propulsion

PLoS Biology

Volumn 12, Issue 1, 2014, Pages

  Mueller, Jan ^a   Pfanzelter, Julia ^a   Winkler, Christoph ^a,b   Narita, Akihiro ^c,d   Le Clainche, Christophe ^e   Nemethova, Maria ^a   Carlier, Marie France ^e   Maeda, Yuichiro ^c   Welch, Matthew D ^f   Ohkawa, Taro ^f   Schmeiser, Christian ^a,b   Resch, Guenter P ^g   Small, J Victor ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

^c NAGOYA UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g University of California ^*  (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ANIMALS; BACULOVIRIDAE; COMET ASSAY; ELECTRON MICROSCOPE TOMOGRAPHY; GENE EXPRESSION; GENES, REPORTER; GOLDFISH; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; LUMINESCENT PROTEINS; MELANOMA, EXPERIMENTAL; MODELS, STATISTICAL; SF9 CELLS; SPODOPTERA;

EID: 84893790336     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001765     Document Type: Article

References (38)

1. Tilney LG, Portnoy DA, (1989) Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J Cell Biol 109: 1597-1608.
2. Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD, (1994) Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J Cell Biol 127: 107-115.
3. Welch MD, Iwamatsu A, Mitchison TJ, (1997) Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385: 265-269.
4. Loisel TP, Boujemaa R, Pantaloni D, Carlier MF, (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401: 613-616.
5. Wiesner S, Helfer E, Didry D, Ducouret G, Lafuma F, et al. (2003) A biomimetic motility assay provides insight into the mechanism of actin-based motility. J Cell Biol 160: 387-398.
6. Goley ED, Welch MD, (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7: 713-726.
7. Dodding MP, Way M, (2009) Nck- and N-WASP-dependent actin-based motility is conserved in divergent vertebrate poxviruses. Cell Host Microbe 6: 536-550.
8. Haglund CM, Welch MD, (2011) Pathogens and polymers: microbe-host interactions illuminate the cytoskeleton. J Cell Biol 195: 7-17.
9. Sechi AS, Wehland J, Small JV, (1997) The isolated comet tail pseudopodium of Listeria monocytogenes: a tail of two actin filament populations, long and axial and short and random. J Cell Biol 137: 155-167.
10. Cameron LA, Svitkina TM, Vignjevic D, Theriot JA, Borisy GG, (2001) Dendritic organization of actin comet tails. Curr Biol 11: 130-135.
11. Gouin E, Welch MD, Cossart P, (2005) Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8: 35-45.
12. Vinzenz M, Nemethova M, Schur F, Mueller J, Narita A, et al. (2012) Actin branching in the initiation and maintenance of lamellipodia. J Cell Sci 125: 2775-2785.
13. Goley ED, Ohkawa T, Mancuso J, Woodruff JB, D'Alessio JA, et al. (2006) Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314: 464-467.
14. Ohkawa T, Volkman LE, Welch MD, (2010) Actin-based motility drives baculovirus transit to the nucleus and cell surface. J Cell Biol 190: 187-195.
15. Machesky LM, Insall RH, Volkman LE, (2001) WASP homology sequences in baculoviruses. Trends Cell Biol 11: 286-287.
16. Mogilner A, (2009) Mathematics of cell motility: have we got its number? J Math Biol 58: 105-134.
17. Dickinson RB, (2009) Models for actin polymerization motors. J Math Biol 58: 81-103.
18. Urban E, Jacob S, Nemethova M, Resch GP, Small JV, (2010) Electron tomography reveals unbranched networks of actin filaments in lamellipodia. Nat Cell Biol 12: 429-435.
19. Narita A, Maeda Y, (2007) Molecular determination by electron microscopy of the actin filament end structure. J Mol Biol 365: 480-501.
20. Narita A, Mueller J, Urban E, Vinzenz M, Small JV, et al. (2012) Direct determination of actin polarity in the cell. J Mol Biol 419: 359-368.
21. Lacayo CI, Soneral PA, Zhu J, Tsuchida MA, Footer MJ, et al. (2012) Choosing orientation: influence of cargo geometry and ActA polarization on actin comet tails. Mol Biol Cell 23: 614-629.
22. Dickinson RB, (2008) A multi-scale mechanistic model for actin-propelled bacteria. Cellular and Molecular Bioengineering 1: 110-121.
23. Plastino J, Sykes C, (2005) The actin slingshot. Curr Opin Cell Biol 17: 62-66.
24. Upadhyaya A, Chabot JR, Andreeva A, Samadani A, van Oudenaarden A, (2003) Probing polymerization forces by using actin-propelled lipid vesicles. Proc Natl Acad Sci U S A 100: 4521-4526.
25. Mogilner A, Oster G, (2003) Force generation by actin polymerization II: the elastic ratchet and tethered filaments. Biophys J 84: 1591-1605.
26. Dickinson RB, Purich DL, (2002) Clamped-filament elongation model for actin-based motors. Biophys J 82: 605-617.
27. Alberts JB, Odell GM, (2004) In silico reconstitution of Listeria propulsion exhibits nano-saltation. PLoS Biol 2: e412.
28. Breitsprecher D, Kiesewetter AK, Linkner J, Vinzenz M, Stradal TE, et al. (2011) Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J 30: 456-467.
29. Tsuchida MA, Theriot JA, (2007) Decoupling the coupling: surface attachment in actin-based motility. ACS Chem Biol 2: 221-224.
30. Risca VI, Wang EB, Chaudhuri O, Chia JJ, Geissler PL, et al. (2012) Actin filament curvature biases branching direction. Proc Natl Acad Sci U S A 109: 2913-2918.
31. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, et al. (1997) Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136: 1307-1322.
32. Cudmore S, Reckmann I, Griffiths G, Way M, (1996) Vaccinia virus: a model system for actin-membrane interactions. J Cell Sci 109 (Pt 7):: 1739-1747.
33. Nemethova M, Auinger S, Small JV, (2008) Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J Cell Biol 180: 1233-1244.
34. Lai FP, Szczodrak M, Block J, Faix J, Breitsprecher D, et al. (2008) Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27: 982-992.
35. Rottner K, Behrendt B, Small JV, Wehland J, (1999) VASP dynamics during lamellipodia protrusion. Nat Cell Biol 1: 321-322.
36. Schafer DA, Welch MD, Machesky LM, Bridgman PC, Meyer SM, et al. (1998) Visualization and molecular analysis of actin assembly in living cells. J Cell Biol 143: 1919-1930.
37. Breitsprecher D, Koestler SA, Chizhov I, Nemethova M, Mueller J, et al. (2011) Cofilin cooperates with fascin to disassemble filopodial actin filaments. J Cell Sci 124: 3305-3318.
38. Kremer JR, Mastronarde DN, McIntosh JR, (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.