Actin network disassembly powers dissemination of Listeria monocytogenes

Journal of Cell Science

Volumn 127, Issue 1, 2014, Pages 240-249

  Talman, Arthur M ^a   Chong, Ryan ^a   Chia, Jonathan ^b   Svitkina, Tatyana ^b   Agaisse, Hervé ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Actin assembly; Actin network disassembly; AIP1; ARP2 3; CFL1; GMFB; Listeria; WDR1

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2-3 COMPLEX; BACTERIAL PROTEIN; BACTERIAL PROTEIN AIP1; BACTERIAL PROTEIN CFL1; BACTERIAL PROTEIN GMBF; HOST FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CELL MOTILITY; CELL SPREADING; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; CYTOSOL; HUMAN; HUMAN CELL; LISTERIA MONOCYTOGENES; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; TURNOVER TIME; VELOCITY;

ACTIN ASSEMBLY; ACTIN NETWORK DISASSEMBLY; AIP1; ARP2/3; CFL1; GMFB; LISTERIA; WDR1;

ACTIN CYTOSKELETON; ACTINS; CELL MEMBRANE; COFILIN 1; CYTOSOL; GENE EXPRESSION REGULATION; GLIA MATURATION FACTOR; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; LISTERIA MONOCYTOGENES; MICROFILAMENT PROTEINS; MICROSCOPY, CONFOCAL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VACUOLES;

EID: 84891430173     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.140038     Document Type: Article

References (32)

1. Andersen, J. B., Roldgaard, B. B., Lindner, A. B., Christensen, B. B. and Licht, T. R. (2006). Construction of a multiple fluorescence labelling system for use in co-invasion studies of Listeria monocytogenes. BMC Microbiol. 6, 86
2. Brieher, W. M., Kueh, H. Y., Ballif, B. A. and Mitchison, T. J. (2006). Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J. Cell Biol. 175, 315-324
3. Chaudhry, F., Breitsprecher, D., Little, K., Sharov, G., Sokolova, O. and Goode, B. L. (2013). Srv2/cyclase-associated protein forms hexameric shurikens that directly catalyze actin filament severing by cofilin. Mol. Biol Cell 24, 31-41
4. Chong, R., Squires, R., Swiss, R. and Agaisse, H. (2011). RNAi screen reveals host cell kinases specifically involved in Listeria monocytogenes spread from cell to cell. PLoS ONE 6, e23399
5. Domann, E., Wehland, J., Rohde, M., Pistor, S., Hartl, M., Goebel, W., Leimeister-Wächter, M., Wuenscher, M. and Chakraborty, T. (1992). A novel bacterial virulence gene in Listeria monocytogenes required for host cell microfilament interaction with homology to the proline-rich region of vinculin EMBO J. 11, 1981-1990
6. Forscher, P. and Smith, S. J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516
7. Gandhi, M., Smith, B. A., Bovellan, M., Paavilainen, V., Daugherty-Clarke, K., Gelles, J., Lappalainen, P. and Goode, B. L. (2010). GMF is a cofilin homolog that binds Arp2/3 complex to stimulate filament debranching and inhibit actin nucleation. Curr. Biol. 20, 861-867
8. Haglund, C. M. and Welch, M. D. (2011). Pathogens and polymers: microbe-host interactions illuminate the cytoskeleton. J. Cell Biol. 195, 7-17
9. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H. and Cossart, P (1992). L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68, 521-531
10. Lambrechts, A., Gevaert, K., Cossart, P., Vandekerckhove, J. and Van Troys, M. (2008). Listeria comet tails: the actin-based motility machinery at work Trends Cell Biol. 18, 220-227
11. Lasa, I., Gouin, E., Goethals, M., Vancompernolle, K., David, V., Vandekerckhove, J. and Cossart, P. (1997). Identification of two regions in the N-terminal domain of ActA involved in the actin comet tail formation by Listeria monocytogenes. EMBO J. 16, 1531-1540
12. Loisel, T. P., Boujemaa, R., Pantaloni, D. and Carlier, M.-F. (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401, 613-616
13. Mattila, P. K., Quintero-Monzon, O., Kugler, J., Moseley, J. B., Almo, S. C., Lappalainen, P. and Goode, B. L. (2004). A high-affinity interaction with ADPactin monomers underlies the mechanism and in vivo function of Srv2/cyclaseassociated protein. Mol. Biol. Cell 15, 5158-5171
14. Mohri, K., Ono, K., Yu, R., Yamashiro, S. and Ono, S. (2006). Enhancement of actin-depolymerizing factor/cofilin-dependent actin disassembly by actininteracting protein 1 is required for organized actin filament assembly in the Caenorhabditis elegans body wall muscle. Mol. Biol. Cell 17, 2190-2199
15. Nakano, K., Kuwayama, H., Kawasaki, M., Numata, O. and Takaine, M. (2010) GMF is an evolutionarily developed Adf/cofilin-super family protein involved in the Arp2/3 complex-mediated organization of the actin cytoskeleton Cytoskeleton 67, 373-382
16. Normoyle, K. P. M. and Brieher, W. M. (2012). Cyclase-associated protein (CAP) acts directly on F-actin to accelerate cofilin-mediated actin severing across the range of physiological pH. J. Biol. Chem. 287, 35722-35732
17. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465
18. Poukkula, M., Kremneva, E., Serlachius, M. and Lappalainen, P. (2011). Actindepolymerizing factor homology domain: a conserved fold performing diverse roles in cytoskeletal dynamics. Cytoskeleton 68, 471-490
19. Robbins, J. R., Barth, A. I., Marquis, H., de Hostos, E. L., Nelson, W. J. and Theriot, J. A. (1999). Listeria monocytogenes exploits normal host cell processes to spread from cell to cell. J. Cell Biol. 146, 1333-1350
20. Rolls, M. M., Stein, P. A., Taylor, S. S., Ha, E., McKeon, F. and Rapoport, T. A (1999). A visual screen of a GFP-fusion library identifies a new type of nuclear envelope membrane protein. J. Cell Biol. 146, 29-44
21. Sechi, A. S., Wehland, J. and Small, J. V. (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
22. Siripala, A. D. and Welch, M. D. (2007). SnapShot: actin regulators I. Cell 128, 626.e1-626.e2
23. Skoble, J., Portnoy, D. A. and Welch, M. D. (2000). Three regions within ActA promote Arp2/3 complex-mediated actin nucleation and Listeria monocytogenes motility. J. Cell Biol. 150, 527-538
24. Stevens, J. M., Galyov, E. E. and Stevens, M. P. (2006). Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol. 4, 91-101
25. Svitkina, T. (2007). Electron microscopic analysis of the leading edge in migrating cells. Methods Cell Biol. 79, 295-319
26. Svitkina, T. M. and Borisy, G. G. (2006). Correlative light and electron microscopy of the cytoskeleton. In Cell Biology, 3rd edn (ed. E. C. Julio), pp. 277-285 Burlington, MA: Academic Press
27. Theriot, J. A., Mitchison, T. J., Tilney, L. G. and Portnoy, D. A. (1992). The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357, 257-260
28. Wang, Y. L. (1985). Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J. Cell Biol. 101, 597-602
29. Welch, M. D., Iwamatsu, A. and Mitchison, T. J. (1997). Actin polymerization is induced by Arp2/3 protein complex at the surface of Listeria monocytogenes Nature 385, 265-269
30. Welch, M. D., Rosenblatt, J., Skoble, J., Portnoy, D. A. and Mitchison, T. J (1998). Interaction of human Arp2/3 complex and the Listeria monocytogenes ActA protein in actin filament nucleation. Science 281, 105-108
31. Welman, A., Serrels, A., Brunton, V. G., Ditzel, M. and Frame, M. C. (2010) Two-color photoactivatable probe for selective tracking of proteins and cells. J Biol. Chem. 285, 11607-11616
32. Ydenberg, C. A., Padrick, S. B., Sweeney, M. O., Gandhi, M., Sokolova, O. and Goode, B. L. (2013). GMF severs actin-Arp2/3 complex branch junctions by a cofilin-like mechanism. Curr. Biol. 23, 1037-1045