Defining a core set of actin cytoskeletal proteins critical for actin-based motility of Rickettsia

Cell Host and Microbe

Volumn 7, Issue 5, 2010, Pages 388-398

  Serio, Alisa W ^a   Jeng, Robert L ^a,b   Haglund, Cat M ^a   Reed, Shawna C ^a   Welch, Matthew D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN CAPPING PROTEIN; COFILIN; CYTOSKELETON PROTEIN; FIMBRIA PROTEIN; PROFILIN; ACTIN BINDING PROTEIN; ACTIN DEPOLYMERIZING FACTOR; MEMBRANE PROTEIN; PLASTIN; SMALL INTERFERING RNA;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL MOTILITY; CONTROLLED STUDY; DROSOPHILA; EVOLUTIONARY ADAPTATION; LISTERIA MONOCYTOGENES; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; RICKETTSIA; RNA INTERFERENCE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CERCOPITHECUS; DRUG ANTAGONISM; GENE SILENCING; GENETICS; METABOLISM; MOTION; PATHOGENICITY;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES; MAMMALIA; RICKETTSIA; RICKETTSIA PARKERI;

ACTIN CAPPING PROTEINS; ACTIN DEPOLYMERIZING FACTORS; ANIMALS; CELL LINE; CERCOPITHECUS AETHIOPS; DROSOPHILA; GENE SILENCING; MEMBRANE GLYCOPROTEINS; MICROFILAMENT PROTEINS; MODELS, BIOLOGICAL; MOTION; PROFILINS; RICKETTSIA; RNA, SMALL INTERFERING;

EID: 77955284566     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2010.04.008     Document Type: Article

References (56)

1. Akin, O., and Mullins, R. D. (2008). Capping protein increases the rate of actinbased motility by promoting filament nucleation by the Arp2/3 complex. Cell 133, 841-851.
2. Anacker, R. L., Mann, R. E., and Gonzales, C. (1987). Reactivity of monoclonal antibodies to Rickettsia rickettsii with spotted fever and typhus group rickettsiae. J. Clin. Microbiol. 25, 167-171.
3. Andrianantoandro, E., and Pollard, T. D. (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 24, 13-23.
4. Balraj, P., El Karkouri, K., Vestris, G., Espinosa, L., Raoult, D., and Renesto, P. (2008). RickA expression is not sufficient to promote actin-based motility of Rickettsia raoultii. PLoS ONE 3, e2582. 10.1371/journal.pone. 0002582.
5. Bishop, D. K., and Hinrichs, D. J. (1987). Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J. Immunol. 139, 2005-2009.
6. Boujemaa-Paterski, R., Gouin, E., Hansen, G., Samarin, S., Le Clainche, C., Didry, D., Dehoux, P., Cossart, P., Kocks, C., Carlier, M. F., et al. (2001). Listeria protein ActA mimics WASp family proteins: it activates filament barbed end branching by Arp2/3 complex. Biochemistry 40, 11390-11404.
7. Brieher, W. M., Coughlin, M., and Mitchison, T. J. (2004). Fascin-mediated propulsion of Listeria monocytogenes independent of frequent nucleation by the Arp2/3 complex. J. Cell Biol. 165, 233-242.
8. Cameron, L. A., Svitkina, T. M., Vignjevic, D., Theriot, J. A., and Borisy, G. G. (2001). Dendritic organization of actin comet tails. Curr. Biol. 11, 130-135.
9. Campellone, K. G., and Welch, M. D. (2010). A nucleator arms race: cellular control of actin assembly. Natl. Rev. 11, 237-251.
10. Carlier, M. F., and Pantaloni, D. (1997). Control of actin dynamics in cell motility. J. Mol. Biol. 269, 459-467.
11. Carlier, M. F., Laurent, V., Santolini, J., Melki, R., Didry, D., Xia, G. X., Hong, Y., Chua, N. H., and Pantaloni, D. (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136, 1307-1322.
12. Delanote, V., Vandekerckhove, J., and Gettemans, J. (2005). Plastins: versatile modulators of actin organization in (patho) physiological cellular processes. Acta Pharmacol. Sin. 26, 769-779.
13. Egile, C., Loisel, T. P., Laurent, V., Li, R., Pantaloni, D., Sansonetti, P. J., and Carlier, M. F. (1999). Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. J. Cell Biol. 146, 1319-1332.
14. Field, C. M., and Alberts, B. M. (1995). Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J. Cell Biol. 131, 165-178.
15. Geese, M., Schluter, K., Rothkegel, M., Jockusch, B. M., Wehland, J., and Sechi, A. S. (2000). Accumulation of profilin II at the surface of Listeria is concomitant with the onset of motility and correlates with bacterial speed. J. Cell Sci. 113, 1415-1426.
16. Geese, M., Loureiro, J. J., Bear, J. E., Wehland, J., Gertler, F. B., and Sechi, A. S. (2002). Contribution of Ena/VASP proteins to intracellular motility of listeria requires phosphorylation and proline-rich core but not F-actin binding or multimerization. Mol. Biol. Cell 13, 2383-2396.
17. Giganti, A., Plastino, J., Janji, B., Van Troys, M., Lentz, D., Ampe, C., Sykes, C., and Friederich, E. (2005). Actin-filament cross-linking protein T-plastin increases Arp2/3-mediated actin-based movement. J. Cell Sci. 118, 1255-1265.
18. Gouin, E., Gantelet, H., Egile, C., Lasa, I., Ohayon, H., Villiers, V., Gounon, P., Sansonetti, P. J., and Cossart, P. (1999). A comparative study of the actinbased motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J. Cell Sci. 112, 1697-1708.
19. Gouin, E., Egile, C., Dehoux, P., Villiers, V., Adams, J., Gertler, F., Li, R., and Cossart, P. (2004). The RickA protein of Rickettsia conorii activates the Arp2/3 complex. Nature 427, 457-461.
20. Gouin, E., Welch, M. D., and Cossart, P. (2005). Actin-based motility of intracellular pathogens. Curr. Opin. Microbiol. 8, 35-45.
21. Grenklo, S., Geese, M., Lindberg, U., Wehland, J., Karlsson, R., and Sechi, A. S. (2003). A crucial role for profilin-actin in the intracellular motility of Listeria monocytogenes. EMBO Rep. 4, 523-529.
22. Hackstadt, T., Messer, R., Cieplak, W., and Peacock, M. G. (1992). Evidence for proteolytic cleavage of the 120-kilodalton outer membrane protein of rickettsiae: identification of an avirulent mutant deficient in processing. Infect. Immun. 60, 159-165.
23. Harlander, R. S., Way, M., Ren, Q., Howe, D., Grieshaber, S. S., and Heinzen, R. A. (2003). Effects of ectopically expressed neuronal Wiskott-Aldrich syndrome protein domains on Rickettsia rickettsii actin-based motility. Infect. Immun. 71, 1551-1556.
24. Heinzen, R. A. (2003). Rickettsial actin-based motility: behavior and involvement of cytoskeletal regulators. Ann. N Y Acad. Sci. 990, 535-547.
25. Heinzen, R. A., Hayes, S. F., Peacock, M. G., and Hackstadt, T. (1993). Directional actin polymerization associated with spotted fever group Rickettsia infection of Vero cells. Infect. Immun. 61, 1926-1935.
26. Hudson, A. M., and Cooley, L. (2002). A subset of dynamic actin rearrangements in Drosophila requires the Arp2/3 complex. J. Cell Biol. 156, 677-687.
27. Jeng, R. L., Goley, E. D., D'Alessio, J. A., Chaga, O. Y., Svitkina, T. M., Borisy, G. G., Heinzen, R. A., and Welch, M. D. (2004). A Rickettsia WASP-like protein activates the Arp2/3 complex and mediates actin-based motility. Cell. Microbiol. 6, 761-769.
28. Jockusch, B. M., Murk, K., and Rothkegel, M. (2007). The profile of profilins. Rev. Physiol. Biochem. Pharmacol. 159, 131-149.
29. Kang, F., Laine, R. O., Bubb, M. R., Southwick, F. S., and Purich, D. L. (1997). Profilin interacts with the Gly-Pro-Pro-Pro-Pro-Pro sequences of vasodilatorstimulated phosphoprotein (VASP): implications for actin-based Listeria motility. Biochemistry 36, 8384-8392.
30. Kleba, B., Clark, T. R., Lutter, E. I., Ellison, D. W., and Hackstadt, T. (2010). Disruption of the Rickettsia rickettsii Sca2 autotransporter inhibits actin based motility. Infect. Immun. 78, 2240-2247.
31. 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.
32. Mannherz, H. G., Gonsior, S. M., Gremm, D., Wu, X., Pope, B. J., and Weeds, A. G. (2005). Activated cofilin colocalises with Arp2/3 complex in apoptotic blebs during programmed cell death. Eur. J. Cell Biol. 84, 503-515.
33. Marchand, J. B., Moreau, P., Paoletti, A., Cossart, P., Carlier, M. F., and Pantaloni, D. (1995). Actin-based movement of Listeria monocytogenes: actin assembly results from the local maintenance of uncapped filament barbed ends at the bacterium surface. J. Cell Biol. 130, 331-343.
34. Martinez, J. J., and Cossart, P. (2004). Early signaling events involved in the entry of Rickettsia conorii into mammalian cells. J. Cell Sci. 117, 5097-5106.
35. Ogata, H., Audic, S., Renesto-Audiffren, P., Fournier, P. E., Barbe, V., Samson, D., Roux, V., Cossart, P., Weissenbach, J., Claverie, J. M., et al. (2001). Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293, 2093-2098.
36. Paddock, C. D., Sumner, J. W., Comer, J. A., Zaki, S. R., Goldsmith, C. S., Goddard, J., McLellan, S. L., Tamminga, C. L., and Ohl, C. A. (2004). Rickettsia parkeri: a newly recognized cause of spotted fever rickettsiosis in the United States. Clin. Infect. Dis. 38, 805-811.
37. Paddock, C. D., Finley, R. W., Wright, C. S., Robinson, H. N., Schrodt, B. J., Lane, C. C., Ekenna, O., Blass, M. A., Tamminga, C. L., Ohl, C. A., et al. (2008). Rickettsia parkeri rickettsiosis and its clinical distinction from Rocky Mountain spotted fever. Clin. Infect. Dis. 47, 1188-1196.
38. Policastro, P. F., Munderloh, U. G., Fischer, E. R., and Hackstadt, T. (1997). Rickettsia rickettsii growth and temperature-inducible protein expression in embryonic tick cell lines. J. Med. Microbiol. 46, 839-845.
39. Riedl, J., Crevenna, A. H., Kessenbrock, K., Yu, J. H., Neukirchen, D., Bista, M., Bradke, F., Jenne, D., Holak, T. A., Werb, Z., et al. (2008). Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5, 605-607.
40. Rogers, S. L., Wiedemann, U., Stuurman, N., and Vale, R. D. (2003). Molecular requirements for actin-based lamella formation in Drosophila S2 cells. J. Cell Biol. 162, 1079-1088.
41. Rosenblatt, J., Agnew, B. J., Abe, H., Bamburg, J. R., and Mitchison, T. J. (1997). Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J. Cell Biol. 136, 1323-1332.
42. Schafer, D. A., Welch, M. D., Machesky, L. M., Bridgman, P. C., Meyer, S. M., and Cooper, J. A. (1998). Visualization and molecular analysis of actin assembly in living cells. J. Cell Biol. 143, 1919-1930.
43. 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.
44. Skoble, J., Auerbuch, V., Goley, E. D., Welch, M. D., and Portnoy, D. A. (2001). Pivotal role of VASP in Arp2/3 complex-mediated actin nucleation, actin branch-formation, and Listeria monocytogenes motility. J. Cell Biol. 155, 89-100.
45. Suzuki, T., Miki, H., Takenawa, T., and Sasakawa, C. (1998). Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J. 17, 2767-2776. (Pubitemid 28227123)
46. Svitkina, T. M., and Borisy, G. G. (1999). Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145, 1009-1026.
47. Teysseire, N., Chiche-Portiche, C., and Raoult, D. (1992). Intracellular movements of Rickettsia conorii and R. typhi based on actin polymerization. Res. Microbiol. 143, 821-829.
48. 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.
49. Theriot, J. A., Rosenblatt, J., Portnoy, D. A., Goldschmidt-Clermont, P. J., and Mitchison, T. J. (1994). Involvement of profilin in the actin-based motility of L. monocytogenes in cells and in cell-free extracts. Cell 76, 505-517. (Pubitemid 24064171)
50. Timmers, A. C., Niebel, A., Balague, C., and Dagkesamanskaya, A. (2002). Differential localisation of GFP fusions to cytoskeleton-binding proteins in animal, plant, and yeast cells. Protoplasma 220, 69-78.
51. Van Kirk, L. S., Hayes, S. F., and Heinzen, R. A. (2000). Ultrastructure of Rickettsia rickettsii actin tails and localization of cytoskeletal proteins. Infect. Immun. 68, 4706-4713.
52. Van Troys, M., Huyck, L., Leyman, S., Dhaese, S., Vandekerkhove, J., and Ampe, C. (2008). Ins and outs of ADF/cofilin activity and regulation. Eur. J. Cell Biol. 87, 649-667.
53. Walker, D. H., and Ismail, N. (2008). Emerging and re-emerging rickettsioses: endothelial cell infection and early disease events. Nat. Rev. Microbiol. 6, 375-386.
54. Welch, M. D., DePace, A. H., Verma, S., Iwamatsu, A., and Mitchison, T. J. (1997). The human Arp2/3 complex is composed of evolutionarily conserved subunits and is localized to cellular regions of dynamic actin filament assembly. J. Cell Biol. 138, 375-384.
55. Yarmola, E. G., and Bubb, M. R. (2006). Profilin: emerging concepts and lingering misconceptions. Trends Biochem. Sci. 31, 197-205.
56. Zallen, J. A., Cohen, Y., Hudson, A. M., Cooley, L., Wieschaus, E., and Schejter, E. D. (2002). SCAR is a primary regulator of Arp2/3-dependent morphological events in Drosophila. J. Cell Biol. 156, 689-701.