Quantitative analysis of actin turnover in listeria comet tails: Evidence for catastrophic filament turnover

Biophysical Journal

Volumn 99, Issue 7, 2010, Pages 2153-2162

  Kueh, Hao Yuan ^a,b   Brieher, William M ^c   Mitchison, Timothy J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LISTERIA;

EID: 77958507493     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.07.038     Document Type: Article

References (38)

1. Pollard, T. D., and G. G. Borisy. 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 112:453-465.
2. Kueh, H. Y., and T. J. Mitchison. 2009. Structural plasticity in actin and tubulin polymer dynamics. Science. 325:960-963.
3. Bear, J. E., T. M. Svitkina, F. B. Gertler. 2002. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell. 109:509-521.
4. Kueh, H. Y., G. T. Charras, W. M. Brieher. 2008. Actin disassembly by cofilin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers. J. Cell Biol. 182:341-353.
5. Carlier, M. F., V. Laurent, D. Pantaloni. 1997. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136:1307-1322.
6. Andrianantoandro, E., and T. D. Pollard. 2006. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell. 24:13-23.
7. 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.
8. Theriot, J. A., and T. J. Mitchison. 1991. Actin microfilament dynamics in locomoting cells. Nature. 352:126-131.
9. Watanabe, N., and T. J. Mitchison. 2002. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science. 295:1083-1086.
10. Ponti, A., M. Machacek, G. Danuser. 2004. Two distinct actin networks drive the protrusion of migrating cells. Science. 305:1782-1786.
11. Diez, S., G. Gerisch, T. Bretschneider. 2005. Subsecond reorganization of the actin network in cell motility and chemotaxis. Proc. Natl. Acad. Sci. USA. 102:7601-7606.
12. Staiger, C. J., M. B. Sheahan, L. Blanchoin. 2009. Actin filament dynamics are dominated by rapid growth and severing activity in the Arabidopsis cortical array. J. Cell Biol. 184:269-280.
13. Dabiri, G. A., J. M. Sanger, F. S. Southwick. 1990. Listeria monocytogenes moves rapidly through the host-cell cytoplasm by inducing directional actin assembly. Proc. Natl. Acad. Sci. USA. 87:6068-6072.
14. Theriot, J. A., T. J. Mitchison, D. A. Portnoy. 1992. The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature. 357:257-260.
15. Theriot, J. A., J. Rosenblatt, T. J. Mitchison. 1994. Involvement of profilin in the actin-based motility of L. monocytogenes in cells and in cell-free extracts. Cell. 76:505-517.
16. Rosenblatt, J., B. J. Agnew, T. J. Mitchison. 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.
17. Gillespie, D. 1977. Exact stochastic simulation of coupled chemical reactions. J. Phys. Chem. 81:2340-2361.
18. Pardee, J., and J. Spudich. 1982. Purification of muscle actin. Methods Enzymol. 85:164-181.
19. Brieher, W. M., H. Y. Kueh, T. J. Mitchison. 2006. Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J. Cell Biol. 175:315-324.
20. Wang, K. 1977. Filamin, a new high-molecular-weight protein found in smooth muscle and nonmuscle cells. Purification and properties of chicken gizzard filamin. Biochemistry. 16:1857-1865.
21. Wegner, A. 1976. Head to tail polymerization of actin. J. Mol. Biol. 108:139-150.
22. Pantaloni, D., C. Le Clainche, and M. F. Carlier. 2001. Mechanism of actin-based motility. Science. 292:1502-1506.
23. Marchand, J. B., P. Moreau, D. Pantaloni. 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.
24. Cameron, L. A., T. M. Svitkina, G. G. Borisy. 2001. Dendritic organization of actin comet tails. Curr. Biol. 11:130-135.
25. Coughlin, M., W. M. Brieher, and R. Ohi. 2007. Cell-free extract systems and the cytoskeleton: preparation of biochemical experiments for transmission electron microscopy. Methods Mol. Biol. 369:199-212.
26. Le Clainche, C., D. Pantaloni, and M. F. Carlier. 2003. ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays. Proc. Natl. Acad. Sci. USA. 100:6337-6342.
27. Martin, A. C., M. D. Welch, and D. G. Drubin. 2006. Arp2/3 ATP hydrolysis-catalyzed branch dissociation is critical for endocytic force generation. Nat. Cell Biol. 8:826-833.
28. Maciver, S. K., D. H. Wachsstock, T. D. Pollard. 1991. The actin filament severing protein actophorin promotes the formation of rigid bundles of actin filaments crosslinked with a-actinin. J. Cell Biol. 115:1621-1628.
29. Silacci, P., L. Mazzolai, D. Hayoz. 2004. Gelsolin superfamily proteins: key regulators of cellular functions. Cell. Mol. Life Sci. 61:2614-2623.
30. Carlier, M. F., D. Pantaloni, and E. D. Korn. 1985. Polymerization of ADP-actin and ATP-actin under sonication and characteristics of the ATP-actin equilibrium polymer. J. Biol. Chem. 260:6565-6571.
31. Edelstein-Keshet, L., and G. B. Ermentrout. 1998. Models for the length distributions of actin filaments. I. Simple polymerization and fragmentation. Bull. Math. Biol. 60:449-475.
32. Carlsson, A. E. 2006. Stimulation of actin polymerization by filament severing. Biophys. J. 90:413-422.
33. Tilney, L. G., D. J. DeRosier, and M. S. Tilney. 1992. How Listeria exploits host cell actin to form its own cytoskeleton. I. Formation of a tail and how that tail might be involved in movement. J. Cell Biol. 118:71-81.
34. Kueh, H. Y., W. M. Brieher, and T. J. Mitchison. 2008. Dynamic stabilization of actin filaments. Proc. Natl. Acad. Sci. USA. 105: 16531-16536.
35. Needleman, D. J., A. Groen, T. Mitchison. 2010. Fast microtubule dynamics in meiotic spindles measured by single molecule imaging: evidence that the spindle environment does not stabilize microtubules. Mol. Biol. Cell. 21:323-333.
36. Kim, S. Y., Z. Gitai, W. E. Moerner. 2006. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA. 103:10929-10934.
37. Zaner, K. S., andJ. H. Hartwig. 1988. The effect of filament shortening on the mechanical properties of gel-filtered actin. J. Biol. Chem. 263:4532-4536.
38. Doi, M., and S. Edwards. 1999. The Theory of Polymer Dynamics. Clarendon Press, London, UK.