Actin comet tails, endosomes and endosymbionts

Journal of Experimental Biology

Volumn 206, Issue 12, 2003, Pages 1977-1984

  Fehrenbacher, Kammy ^a   Huckaba, Thomas ^a   Yang, Hyeong Cheol ^a   Boldogh, Istvan ^a   Pon, Liza ^a  

^a Howard Hughes Medical Institute   (United States)

Author keywords

Actin; Cytoskeleton; Endocytosis; Mitochondria; Organelle movement; Pathogen

Indexed keywords

ACTIN;

CELL MOTION; CELL ORGANELLE; CYTOSKELETON; PHYSIOLOGY; REVIEW;

ACTINS; CELL MOVEMENT; CYTOSKELETON; ORGANELLES;

BACTERIA (MICROORGANISMS); SACCHAROMYCETALES;

EID: 0038270568     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00240     Document Type: Review

References (71)

1. Bernardini, M. L., Mounier, J., d'Hauteville, H., Coquis-Rondon, M. and Sansonetti, P. J. (1989). Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc. Natl. Acad. Sci. USA 86, 3867-3871.
2. Blanchoin, L., Amann, K. J., Higgs, H. N., Marchand, J. B., Kaiser, D. A. and Pollard, T. D. (2000). Direct observation of dendritic actin filament networks created by Arp2/3 complex and WASP/Scar proteins. Nature 404, 1007-1011.
3. Boldogh, I. R., Yang, H.-C., Nowakowski, W. D., Karmon, S. L., Hays, L. G., Yates, J. R., III and Pon, L. A. (2001). Arp2/3 complex and actin dynamics are required for actin-based mitochondrial motility in yeast. Proc. Natl. Acad. Sci. USA 98, 3162-3167.
4. Boldogh, I., Vojtov, N., Karmon S. and Pon, L. A. (1998). Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J. Cell Biol. 141, 1371-1381.
5. Cameron, L. A., Footer, M. J., Van Oudenaarden, A. and Theriot, J. (1999). Motility of ActA protein-coated microspheres driven by actin polymerization. Proc. Natl. Acad. Sci. USA 96, 4908-4913.
6. 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, 1307-1323.
7. Chakraborty, T., Ebel, F., Domann, E., Niebuhr, K., Gerstel, B., Pistor, S., Temm-Grove, C. J., Jockusch, B. M., Reinhard, M., Walter, U. and Wehland, J. (1995). A focal adhesion factor directly linking intracellularly motile Listeria monocytogenes and Listeria ivanovii to the actin-based cytoskeleton of mammalian cells. EMBO J. 14, 1314-1321.
8. Chang, F. S., Stefan, C. J. and Blumer, K. J. (2003). A WASp homolog powers actin polymerization-dependent motility of endosomes in vivo. Curr. Biol., in press.
9. Drubin, D. G., Jones, H. D. and Wertman, K. F. (1993). Actin structure and function: roles in mitochondrial organization and morphogenesis in budding yeast and identification of the phalloidin-binding site. Mol. Biol. Cell 4, 1277-1294.
10. Duncan, M. C., Cope, M. J., Goode, B. L., Wendland, B. and Drubin, D. G. (2001). Yeast Eps15-like endocytic protein, Pan1p, activates the Arp2/3 complex. Nat. Cell Biol. 3, 687-690.
11. 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.
12. Evangelista, M., Klebl, B. M., Tong, A. H., Webb, B. A., Leeuw, T., Leberer, E., Whiteway, M., Thomas, D. Y. and Boone, C. (2000). A role for myosin-I in actin assembly through interactions with Vrp1p, Bee1p, and the Arp2/3 complex. J. Cell Biol. 148, 353-362.
13. Fujimoto, L. M., Roth, R., Heuser, J. E. and Schmid, S. L. (2000). Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic 1, 161-171.
14. Gaidarov, L, Santini, F., Warren, R. A. and Keen, J. H. (1999). Spatial control of coated-pit dynamics in living cells. Nature Cell Biol. 1, 1-7.
15. Goldberg, M. A. (2001). Actin-based motility of intracellular microbial pathogens. Microbiol. Mol. Biol. Rev. 65, 595-626.
16. Goode, B. L., Rodal, A. A., Barnes, G. and Drubin, D. G. (2001). Activation of the Arp2/3 complex by the actin filament binding protein Abp1p. J. Cell Biol. 153, 627-634.
17. 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 actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri, and Rickettsia conorii. J. Cell Sci. 112, 1697-1708.
18. 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.
19. Heinzen, R. A., Grieshaber, S. S., Van Kirk, L. S. and Devin, C. J. (1999). Dynamics of actin-based movement by Rickettsia rickettsii in Vero cells. Infect. Immun. 67, 4201-4207.
20. Insall, R., Müller-Taubenberger, A., Machesky, L., Köhler, J., Simmeth, E., Atkinson, S. J., Weber, I. and Gerisch, G. (2001). Dynamics of the Dictyostelium Arp2/3 complex in endocytosis, cytokinesis, and chemotaxis. Cell Motil. Cytoskel. 50, 115-128.
21. Jung, G., Remmert, K., Wu, X., Volosky, J. M. and Hammer, J. A., III. (2001). The Dictystelium CARMIL protein links capping protein and the Arp2/3 complex to type I myosins through their SH3 domains. J. Cell Biol. 153, 1479-1497.
22. Kaksonen, M., Peng, B. and Rauvala, H. (2000). Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J. Cell Sci. 113, 4421-4426.
23. Kelleher, J. F., Atkinson, S. J. and Pollard, T. D. (1995). Sequences, structural models, and cellular localization of the actin-related protein Arp2 and Arp3 from Acanthamoeba. J. Cell Biol. 131, 385-397.
24. Kocks, C., Marchand, J. B., Gouin, E., d'Huateville, H., Sansonetti, P. J., Carlier, M. F. and Cossart, P. (1995). The unrelated surface proteins ActA of Listeria monocytogenes and IcsA of Shigella flexneri are sufficient to confer actin-based motility on Listeria innocua and Eschericia coli, respectively. Mol. Microbiol. 18, 413-423.
25. Laine, R. O., Zeile, W., Kang, F., Purch, D. L. and Southwick, F. S. (1997). Vinculin proteolysis unmasks an ActA homolog for actin-based Shigella motility. J. Cell Biol. 138, 1255-1264.
26. Lamaze, C., Fujimoto, L. M., Yin, L. H. and Schmid, S. L. (1997). The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272, 20332-20335.
27. Lazzarino, D. A., Boldogh, I., Smlth, M. G., Rosand, J. and Pon, L. A. (1994). Yeast mitochondria contain ATP-sensitive, reversible actin-binding activity. Mol. Biol. Cell 5, 807-818.
28. Lechler, T., Shevchenko, A. and Li, R. (2000). Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. J. Cell Biol. 148, 363-373.
29. Lee, W. L., Bezanilla, M. and Pollard, T. D. (2000). Fission yeast myosin-I, Myo1p, stimulates actin assembly by Arp2/3 complex and shares functions with WASp. J. Cell Biol. 151, 789-800.
30. Lett, M.-C., Sasakawa, C., Okada, N., Sakai, T., Makino, S., Yamada, M., Komatsu, K. and Yoshikawa, M. (1989). virG, a plasmid-coded virulence gene of Shigella flexneri: identification of the virG protein and determination of the complete coding sequence. J. Bacteriol. 171, 353-359.
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. Ma, L., Rohatgi, R. and Kirschner, M. W. (1998). The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc. Natl. Acad. Sci. USA 95, 15362-15367.
33. Machesky, L. M., Atkinson, S. J., Ampe, C., Vandekerckhove, J. and Pollard, T. D. (1994). Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin-agarose. J. Cell Biol. 127, 107-115.
34. Machesky, L. M., Mullins, R. D., Higgs, H. N., Kaiser, D. A., Blanchoin, L., May, R. C., Hall, M. E. and Pollard, T. D. (1999). Scar, a WASp-related protein, activates nucleation of actin filaments by the Arp2/3 complex. Proc. Natl. Acad. Sci. USA 96, 3739-3744.
35. May, R. C., Hall, M. E., Higgs, H. N., Pollard, T. D., Chakraborty, T., Wehland, J., Machesky, L. M. and Sechi, A. S. (1999). The Arp2/3 complex is essential for the actin-based motility of Listeria monocytogenes. Curr. Biol. 9, 759-762.
36. Merrifield, C. J., Moss, S. E., Ballestrem, C., Imhof, B. A., Giese, G., Wunderlich, I. and Almers, W. (1999). Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat. Cell Biol. 1, 71-74.
37. Moreau, V., Galan, J., Devilliers, G., Haguenauer-Tsapis, R. and Winsor, B. (1997). The yeast actin-related Arp2p is required for the internalization step of endocytosis. Mol. Biol. Cell 8, 1361-1375.
38. Moreau, V., Madania, A., Martin, R. P. and Winsor, B. (1996). The Saccharomyces cerevisiae actin-related Arp2 is involved in the actin cytoskeleton. J. Cell Biol. 134, 117-132.
39. Mullins, R. D., Heuser, J. A. and Pollard, T. D. (1998). The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of actin filaments. Proc. Natl. Acad. Sci. USA 95, 6181-6186.
40. Mullins, R. D. and Pollard, T. D. (1999). Rho-family GTPases require the Arp2/3 complex to stimulate actin polymerization in Acanthamoeba extracts. Curr. Biol. 9, 405-415.
41. Nunnari, J., Marshall, W. F., Straight, A., Murray, A., Sedat, J. W. and Walter, P. (1997). Mitochondrial transmission during mating in Saccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA. Mol. Biol. Cell 8, 1233-1242.
42. Pistor, S., Chakraborty, T., Niebuhr, K., Domann, E. and Wehland, J. (1994). The ActA protein of Listeria monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton. EMBO J. 13, 758-763.
43. Robinson, R. C., Turbedsky, K., Kaiser, D. A., Marchand, J. B., Higgs, H. N., Choe, S. and Pollard, T. D. (2001). Crystal structure of Arp2/3 complex. Science 294, 1679-1684.
44. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T. and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
45. Rosenblatt, J., Agnew, B. J., Abe, H., Bamburg, J. R. and Mitchison, T. J. (1997). Xenopus actin-depolymerizing factor (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J. Cell Biol. 136, 1323-1332.
46. Simon, V. R., Swayne, T. C. and Pon, L. A. (1995). Actin-dependent mitochondrial motility in mitotic yeast and cell-free system: identification of a motor activity on the mitochondrial surface. J. Cell Biol. 130, 345-354.
47. Simon, V. R., Karmon, S. L. and Pon, L. A. (1997). Mitochondrial inheritance: cell cycle and actin cable dependence of polarized mitochondrial movements in Saccharomyces cerevisiae. Cell Motil. Cytoskel. 37, 199-210.
48. Smith, G. A., Portnoy, D. A. and Theriot, J. A. (1995). Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Mol. Microbiol. 17, 945-951.
49. Smith, G. A., Theriot, J. A. and Portnoy, D. A. (1996). The tandem repeat domain in the Listeria monocytogenes ActA protein controls the rate of actin-based motility, the percentage of moving bacteria, and the localization of vasodilator-stimulated phosphoprotein and profilin. J. Cell Biol. 135, 647-660.
50. Snapper, S. B., Takeshima, F., Anton, I., Liu, C.-H., Thomas, S., Nguyen, D., Dudley, D., Fraser, H., Putich, D., Lopez-Ilasaca, M. et al. (2001). N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3, 897-904.
51. Stevens, B. J. (1977). Variation in number and volume of the mitochondria in yeast according to growth conditions. A study based on serial sectioning and computergraphics reconstruction. Biol. Cell 28, 37-56.
52. Suzuki, T., Miki, H., Takenawa, T. and Saskawa, C. (1998). Neural Wiskott-Aldrich syndrome protein is implicated in the actin-based motility of Shigella flexneri. EMBO J. 17, 2767-2776.
53. Svitkina, T. M. and Borisy, G. G. (1999). Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament arrays in lamellipodia. J. Cell Biol. 145, 1009-1026.
54. Taunton, J., Rowling, B. A., Coughlin, M. L., Wu, M., Moon, R. T., Mitchison, T. J. and Larabell, C. A. (2000). Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148, 519-530
55. 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.
56. Tilney, L. G. and Portnoy, D. A. (1989). Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite Listeria monocytogenes. J. Cell Biol. 109, 1597-1608.
57. Tilney, L. G., Connelly, P. S. and Portnoy, D. A. (1990). Actin filament nucleation by the bacterial pathogen, Listeria monocytogenes. J. Cell Biol. 111, 2979-2988.
58. Trifaró, J.-M. and Vitale, M. L. (1993). Cytoskeleton dynamics during neurotransmitter release. Trends Neurosci. 16, 466-472.
59. Uruno, T., Liu, J., Zhang, P., Fan, Y., Egile, C., Li, R., Mueller, S. C. and Zhan, X. (2001). Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3, 259-266.
60. 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.
61. Volkmann, N., Amann, K. J., Stoilova-McPhie, S., Egile, C., Winter, D. C., Hazelwood, L., Heuser, J. E., Li, R., Pollard, T. D. and Hanein, D. (2001). Structure of Arp2/3 complex in its activated state and in actin filament branch junctions. Science 293, 2456-2459.
62. Weaver, A. M., Karginov, A. V., Kinley, A. W., Weed, S. A., Li, Y., Parsons, J. T. and Cooper, J. A. (2001). Cortactin promotes and stabilizes Arp2/3-induced actin filaments network formation. Curr. Biol. 11, 370-374.
63. Weed, S. A., Karginov, A. V., Schafer, D. A., Weaver, A. M., Kinley, A. W., Cooper, J. A. and Parsons, J. T. (2000). Cortactin localization to sites of actin assembly in lamellipodia requires interactions with F-actin and the Arp2/3 complex. J. Cell Biol. 151, 29-40.
64. Welch, M. D., Iwamatsu, A. and Mitchison, T. J. (1997a). Actin polymerization is induced by the Arp2/3 protein complex at the surface of Listeria monocytogenes. Nature 385, 265-269.
65. Welch, M. D., DePace, A. H., Verma, S., Iwamatsu, A. and Mitchison, T. J. (1997b). 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.
66. 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.
67. Winter, D., Podtelejnikov, A. V., Mann, M. and Li, R. (1997). Purification and in vivo functional analysis of the yeast Arp2/3 complex. Curr. Biol. 7, 519-529.
68. Winter, D. C., Choe, E. Y. and Li, R. (1999a). Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc. Natl. Acad. Sci. USA 96, 7288-7293.
69. Winter, D., Lechler, T. and Li, R. (1999b). Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr. Biol. 9, 501-504.
70. Yang, H.-C., Palazzo, A., Swayne, T. C. and Pon, L. A. (1999). A retention mechanism for distribution of mitochondria during cell division in budding yeast. Curr. Biol. 9, 1111-1114.
71. Yarar, D., To, W., Abo, A. and Welch, M. D. (1999). The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr. Biol. 9, 555-558.