Actin polymerization overshoots and ATP hydrolysis as assayed by pyrene fluorescence

Biophysical Journal

Volumn 95, Issue 3, 2008, Pages 1050-1062

  Brooks, F J ^a   Carlsson, A E ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; PYRENE; PYRENE DERIVATIVE;

ARTICLE; CHEMICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; DIMERIZATION; HYDROLYSIS; METHODOLOGY; SENSITIVITY AND SPECIFICITY; SPECTROFLUOROMETRY;

ACTINS; ADENOSINE TRIPHOSPHATE; COMPUTER SIMULATION; DIMERIZATION; HYDROLYSIS; MODELS, CHEMICAL; PYRENES; SENSITIVITY AND SPECIFICITY; SPECTROMETRY, FLUORESCENCE;

EID: 51049093826     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.123125     Document Type: Article

References (54)

1. Alberts, B. 2002. Molecular Biology of the Cell, 4th Ed. Garland Science, New York.
2. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
3. dos Remedios, C. G., D. Chhabra, M. Kekic, I. V. Dedova, M. Tsubakihara, D. A. Berry, and N. J. Nosworthy. 2003. Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol. Rev. 83:433-473.
4. Bray, D. 2001. Cell Movements: from Molecules to Motility, 2nd Ed. Garland Publications, New York.
5. Rafelski, S. M., and J. A. Theriot. 2004. Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics. Annu. Rev. Biochem. 73:209-239.
6. Korn, E. D. 1982. Actin polymerization and its regulation by proteins from nonmuscle cells. Physiol. Rev. 62:672-737.
7. Kouyama, T., and K. Mihashi. 1981. Fluorimetry study of n-(1-pyrenyl)iodoacetamide-labeled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur. J. Biochem. 114:33-38.
8. Haugland, R. P., M. T. Z. Spence, I. D. Johnson, and A. Basey. 2005. The Handbook: a Guide to Fluorescent Probes and Labeling Technologies, 10th Ed. Molecular Probes, Eugene, OR.
9. Cooper, J. A., S. B. Walker, and T. D. Pollard. 1983. Pyrene actin: documentation of the validity of a sensitive assay for actin polymerization. J. Muscle Res. Cell Motil. 4:253-262.
10. Halasi, S., G. Papp, B. Bugyi, S. Barko, J. Orban, Z. Ujfalusi, and B. Visegrady. 2006. The effect of pyrene labeling on the thermal stability of actin filaments. Thermochim. Acta. 445:185-189.
11. Lodish, H. F. 2007. Molecular Cell Biology, 6th Ed. W. H. Freeman, New York.
12. i from actin filaments. Biochemistry. 25:7789-7792.
13. Carlier, M. F., D. Pantaloni, and E. D. Korn. 1984. Evidence for an ATP cap at the ends of actin filaments and its regulation of the F-actin steady state. J. Biol. Chem. 259:9983-9986.
14. Grazi, E. 1985. Polymerization of n-(1-pyrenyl) iodoacetamide-labeled actin: the fluorescence signal is not directly proportional to the incorporation of the monomer into the polymer. Biochem. Biophys. Res. Commun. 128:1058-1063.
15. Siegel, D. L., and D. Branton. 1985. Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J. Cell Biol. 100:775-785.
16. Buzan, J. M., and C. Frieden. 1996. Yeast actin: polymerization kinetic studies of wild type and a poorly polymerizing mutant. Proc. Natl. Acad. Sci. USA. 93:91-95.
17. Du, J. Y., and C. Frieden. 1998. Kinetic studies on the effect of yeast cofilin on yeast actin polymerization. Biochemistry. 37:13276-13284.
18. Ohmi, K., S. Enosawa, Y. Nonomura, T. Tatsuno, and Y. Ueno. 2001. Acceleration of actin polymerization and rapid microfilament reorganization in cultured hepatocytes by cyclochlorotin, a hepatotoxic cyclic peptide. Toxicon. 39:303-308.
19. Amann, K. J., and T. D. Pollard. 2001. The Arp2/3 complex nucleates actin filament branches from the sides of pre-existing filaments. Nat. Cell Biol. 3:306-310.
20. Amann, K. J., and T. D. Pollard. 2001. Direct real-time observation of actin filament branching mediated by Arp2/3 complex using total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. USA. 98:15009-15013.
21. Uruno, T., J. Liu, P. Zhang, C. Egile, R. Li, S. C. Mueller, and X. Zhan. 2001. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3:259-266.
22. Weaver, A. M., A. V. Karginov, A. W. Kinley, S. A. Weed, Y. Li, J. T. Parsons, and J. A. Cooper. 2001. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. 11:370-374.
23. Kumar, N., P. Zhao, A. Tomar, C. A. Galea, and S. Khurana. 2004. Association of villin with phosphatidylinositol 4,5-bisphosphate regulates the actin cytoskeleton. J. Biol. Chem. 279:3096-3110.
24. Carlsson, A. E., M. A. Wear, and J. A. Cooper. 2004. End versus side branching by Arp2/3 complex. Biophys. J. 86:1074-1081.
25. Kim, K., A. Yamashita, M. A. Wear, Y. Maeda, and J. A. Cooper. 2004. Capping protein binding to actin in yeast: biochemical mechanism and physiological relevance. J. Cell Biol. 164:567-580.
26. Leng, Y., J. Zhang, K. Badour, E. Arpaia, S. Freeman, P. Cheung, M. Siu, and K. Siminovitch. 2005. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl. Acad. Sci. USA. 102:1098-1103.
27. Goley, E. D., T. Ohkawa, J. Mancuso, J. B. Woodruff, J. A. D'Alessio, W. Z. Cande, L. E. Volkman, and M. D. Welch. 2006. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science. 314:464-467.
28. Tehrani, S., N. Tomasevic, S. Weed, R. Sakowicz, and J. Cooper. 2007. SRC phosphorylation of cortactin enhances actin assembly. Proc. Natl. Acad. Sci. USA. 104:11933-11938.
29. i-actin determined by fluorescence microscopy. Proc. Natl. Acad. Sci. USA. 104:8827-8832.
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. Coue, M., and E. D. Korn. 1986. ATP hydrolysis by the gelsolin-actin complex and at the pointed ends of gelsolin-capped filaments. J. Biol. Chem. 261:1588-1593.
32. Debye, P. 1947. Molecular weight determination by light scattering. J. Phys. Chem. 51:18-32.
33. Masai, J., S. Ishiwata, and S. Fujime. 1986. Dynamic light-scattering study on polymerization process of muscle actin. Biophys. Chem. 25:253-269.
34. Zimm, B. H., R. S. Stein, and P. Doty. 1945. Classical theory of light scattering from solutions - a review. Polym. Bull. 1:90-119.
35. Kroy, K., and E. Frey. 1997. Dynamic scattering from solutions of semiflexible polymers. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics. 55:3092-3101.
36. Harnau, L., R. G. Winkler, and P. Reineker. 1996. Dynamic structure factor of semiflexible macromolecules in dilute solution. J. Chem. Phys. 104:6355-6368.
37. Gotter, R., K. Kroy, E. Frey, M. Barmann, and E. Sackmann. 1996. Dynamic light scattering from semidilute actin solutions: a study of hydrodynamic screening, filament bending stiffness, and the effect of tropomyosin/troponin- binding. Macromolecules. 29:30-36.
38. Carlsson, A. E. 2004. Structure of autocatalytically branched actin solutions. Phys. Rev. Lett. 92:238102.
39. Carlsson, A. E. 2006. Stimulation of actin polymerization by filament severing. Biophys. J. 90:413-422.
40. Alberts, J. B., and G. M. Odell. 2004. In silico reconstitution of Listeria propulsion exhibits nano-saltation. PLoS Biol. 2:e412.
41. Bindschadler, M., E. A. Osborn, C. F. J. Dewey, and J. L. McGrath. 2004. A mechanistic model of the actin cycle. Biophys. J. 86:2720-2739.
42. Rickard, J. E., and P. Sheterline. 1986. Cytoplasmic concentrations of inorganic phosphate affect the critical concentration for assembly of actin in the presence of cytochalasin D or ADP. J. Mol. Biol. 191:273-280.
43. Otterbein, L. R., P. Graceffa, and R. Dominguez. 2001. The crystal structure of uncomplexed actin in the ADP state. Science. 293:708-711.
44. i release following nucleotide hydrolysis in actin or tubulin assembly using 2-amino-6-mercapto-7-methylpurine ribonucleoside and purine-nucleoside phosphorylase as an enzyme-linked assay. Biochemistry. 35:12038-12045.
45. Selden, L. A., H. J. Kinosian, J. E. Estes, and L. C. Gershman. 1999. Impact of profilin on actin-bound nucleotide exchange and actin polymerization dynamics. Biochemistry. 38:2769-2778.
46. Mahaffy, R. E., and T. D. Pollard. 2006. Kinetics of the formation and dissociation of actin filament branches mediated by Arp2/3 complex. Biophys. J. 91:3519-3528.
47. Goley, E. D., and M. D. Welch. 2006. The Arp2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol. 7:713-726.
48. Kovar, D. R. 2006. Arp2/3 ATP hydrolysis: to branch or to debranch? Nat. Cell Biol. 8:783-785.
49. Sept, D., J. Xu, T. D. Pollard, and J. A. McCammon. 1999. Annealing accounts for the length of actin filaments formed by spontaneous polymerization. Biophys. J. 77:2911-2919.
50. Andrianantoandro, E., L. Blanchoin, D. Sept, J. A. McCammon, and T. D. Pollard. 2001. Kinetic mechanism of end-to-end annealing of actin filaments. J. Mol. Biol. 312:721-730.
51. Blanchoin, L., and T. D. Pollard. 2002. Hydrolysis of ATP by polymerized actin depends on the bound divalent cation but not profilin. Biochemistry. 41:597-602.
52. Carlier, M. F., V. Laurent, J. Santolini, R. Melki, D. Didry, G. X. Xia, Y. Hong, N. H. Chua, and 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.
53. Schuler, H., C. E. Schutt, U. Lindberg, and R. Karlsson. 2000. Covalent binding of ATPγS to the nucleotide-binding site in S14C-actin. FEBS Lett. 476:155-159.
54. Bryan, K. E., and P. A. Rubenstein. 2005. An intermediate form of ADP-F-actin. J. Biol. Chem. 280:1696-1703.