How depolymerization can promote polymerization: The case of actin and profilin

BioEssays

Volumn 31, Issue 11, 2009, Pages 1150-1160

  Yarmola, Elena G ^a,b   Bubb, Michael R ^a,b  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b N Florida/S Georgia Veterans Health System   (United States)

Author keywords

Actin; ATP hydrolysis; Exchange diffusion; Fluctuations; Profilin

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROFILIN;

BINDING AFFINITY; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); DEPOLYMERIZATION; HYDROLYSIS; MOLECULAR MECHANICS; NUCLEIC ACID TRANSPORT; POLYMERIZATION; PROTEIN BINDING; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; THERMODYNAMICS; TRANSPORT KINETICS;

ACTINS; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; BIOCHEMISTRY; CYTOSKELETON; DIFFUSION; HOT TEMPERATURE; HUMANS; HYDROLYSIS; KINETICS; MODELS, BIOLOGICAL; PROFILINS; STOCHASTIC PROCESSES; THERMODYNAMICS;

EID: 70549106122     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.200900049     Document Type: Review

References (82)

1. Birbach, R., Profilin, a multi-modal regulator of neuronal plasticity. BioEssays 2008. 30: 994-1002.
2. Witke, W., The role of profilin complexes in cell motility and other cellular processes. Trends Cell Biol 2004. 14: 461-469. (Pubitemid 39092704)
3. Pollard, T. D. and Borisy, G. G., Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003. 112: 453-465.
4. Haugwitz, M., Noegel, A. A., Karakesisoglou, J. and Schleicher, M., Dictyostelium amoebae that lack G-actin-sequestering profilins show defects in F-actin content, cytokinesis, and development. Cell 1994. 79: 303-314. (Pubitemid 24324920)
5. Magdole, V., Oechsner, U., Muller, G. and Bandlow, W., The introncontaining gene for yeast profilin (PFY) encodes a vital function. Mol Cell Biol 1988. 8: 5108-5115.
6. Verheyen, E. M. and Cooley, L., Profilin mutations disrupt multiple actindependent processes during Drosophila development. Development 1994. 120: 717-728. (Pubitemid 24111539)
7. Witke, W., Sharpe, A. H. and Kwiatkowski, D. J., Profilin deficient mice are not viable. Mol Biol Cell 1993. 4: 149a.
8. Witke, W., Sutherland, J. D., Sharpe, A., Arai, M. and Kwiatkowski, D. J., Profilin I is essential for cell survival and cell division in early mouse development. Proc Natl Acad Sci USA 2001. 98: 3832-3836. (Pubitemid 32249857)
9. Staiger, C. J. and Blanchoin, L., Actin dynamics: old friends with new stories. Curr Opin Plant Biol 2006. 9: 554-562. (Pubitemid 44559756)
10. Pantaloni, D., Le Clainche, C. and Carlier, M. F., Mechanism of actinbased motility. Science 2001. 292: 1502-1506.
11. Carlier, M. F. and Pantaloni, D., Control of actin dynamics in cell motility. J Mol Biol 1997. 269: 459-467. (Pubitemid 27267859)
12. Pollard, T. D., Blanchoin, L. and Mullins, R. D., Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu Rev Biophys Biomol Struct 2000. 29: 545-576. (Pubitemid 30599604)
13. Weber, A., Actin binding proteins that change extent and rate of actin monomer-polymer distribution by different mechanisms. Mol Cell Biochem 1999. 190: 67-74. (Pubitemid 29094989)
14. Mockrin, S. C. and Korn, E. D., Acanthamoeba profilin interacts with G-actin to increase the rate of exchange of actin-bound adenosine 5′-triphosphate. Biochemistry 1980. 19: 5359-5362.
15. Carlsson, L., Nystrom, L. E., Lindberg, U., Kannan, K. K., Cid-Dresdner, H. and Lovgren, S., Crystallization of a non-muscle actin. J Mol Biol 1976. 105: 353-366.
16. Tilney, L. G., Bonder, E. M., Coluccio, L. M. and Mooseker, M. S., Actin from Thyone sperm assembles on only one end of an actin filament: a behavior regulated by profilin. J Cell Biol 1983. 97: 112-124.
17. Pollard, T. D. and Cooper, J. A., Quantitative analysis of the effect of Acanthamoeba profilin on actin filament nucleation and elongation. Biochemistry 1984. 23: 6631-6641.
18. Kaiser, D. A., Sato, M., Ebert, R. F. and Pollard, T. D., Purification and characterization of two isoforms of acanthamoeba profilin. J Cell Biol 1986. 102: 221-226. (Pubitemid 16155570)
19. Pantaloni, D. and Carlier, M. F., How profilin promotes actin filament assembly in the presence of thymosin beta 4. Cell 1993. 75: 1007-1014. (Pubitemid 24014557)
20. Theriot, J. A. and Mitchison, T. J., The three faces of profilin. Cell 1993. 75: 835-838.
21. Kinosian, H. J., Selden, L. A., Gershman, L. C. and Estes, J. E., Actin filament barbed end elongation with nonmuscle MgATP-actin and MgADP-actin in the presence of profilin. Biochemistry 2002. 41: 6734-6743.
22. Kovar, D. R., Molecular details of formin-mediated actin assembly. Cur Opin Cell Biol 2005. 18: 11-17.
23. Pring, M., Weber, A. and Bubb, M. R., Profilin-actin complexes directly elongate actin filaments at the barbed end. Biochemistry 1992. 31: 1827-1836.
24. Bubb, M. R., Yarmola, E. G., Gibson, B. G. and Southwick, F. S., Depolymerization of actin filaments by profilin. Effects of profilin on capping protein function. J Biol Chem 2003. 278: 24629-24635. (Pubitemid 37548617)
25. Kang, F., Purich, D. L. and Southwick, F. S., Profilin promotes barbed-end actin filament assembly without lowering the critical concentration. J Biol Chem 1999. 274: 36963-36972. (Pubitemid 30016765)
26. 4 on the critical concentration of actin demonstrated in vitro and in cell extracts with a novel direct assay. J Biol Chem 2004. 279: 33519-33527.
27. Yarmola, E. G. and Bubb, M. R., Profilin: emerging concepts and lingering misconceptions. Trends Biochem Sci 2006. 31: 197-205.
28. Yarmola, E. G., Dranishnikov, D. A. and Bubb, M. R., Effect of profilin on actin critical concentration: a theoretical analysis. Biophys J 2008. 95: 5544-5573.
29. Kuhn, J. R. and Pollard, T. D., Real-time measurements of actin filament polymerization by total internal reflection fluorescence microscopy. Biophys J 2005. 88: 1387-1402. (Pubitemid 40975966)
30. Pollard, T. D., Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J Cell Biol 1986. 103: 2747-2754. (Pubitemid 17008020)
31. Oosawa, F. and Asakura, S., Thermodynamics of the polymerization of proteins. New York, Academic Press, 1975.
32. Wegner, A., Head to tail polymerization of actin. J Mol Biol 1976. 108: 139-150.
33. DiNubile, M. J. and Huang, S., Capping of the barbed ends of actin filaments by a high affinity profilin-actin complex. Cell Motil Cytoskeleton 1997. 37: 211-225. (Pubitemid 27287681)
34. Nyman, T., Page, R., Schutt, C. E., Karlsson, R. and Lindberg, U., A cross-linked profilin-actin heterodimer interferes with elongation at the fast-growing end of F-actin. J Biol Chem 2002. 277: 15828-15833. (Pubitemid 34967861)
35. Blanchoin, L. and Pollard, T. D., Hydrolysis of ATP by polymerized actin depends on the bound divalent cation but not profilin. Biochemistry 2002. 41: 597-602. (Pubitemid 34062030)
36. Romero, S., Didry, D., Larquet, E., Boisset, N., Pantaloni, D. and Carlier, M. F., How ATP hydrolysis controls filament assembly from profilin-actin: implication for formin processivity. J Biol Chem 2007. 282: 8435-8445. (Pubitemid 47093625)
37. Dickinson, R. B., Southwick, F. S. and Purich, D. L., A direct-transfer polymerization model explains how themultiple profilin-binding sites in the actoclampin motor promote rapid actin-based motility. Arch Biochem Biophys 2002. 406: 296-301.
38. Bindschadler, M., Osborn, E. A., Dewey, C. F., Jr. and McGrath, J. L., A mechanistic model of the actin cycle. Biophys J 2004. 86: 2720-2739.
39. Vavylonis, D., Kovar, D. R., O'Shaughnessy, B. and Pollard, T. D., Model of formin-associated actin filament elongation. Mol Cell 2006. 21: 455-466. (Pubitemid 43228002)
40. Gutsche-Perelroizen, I., Lepault, J., Ott, A. and Carlier, M. F., Filament assembly from profilin-actin. J Biol Chem 1999. 274: 6234-6243.
41. Carlier, M. F. and Pantaloni, D., Direct evidence for ADP-Pi-F-actin as the major intermediate in ATP-actin polymerization. Rate of dissociation of Pi from actin filaments. Biochemistry 1986. 25: 7789-7792.
42. Romero, S., Le Clainche, C., Didry, D., Egile, C., Pantaloni, D. and Carlier, M. F., Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 2004. 119: 419-429. (Pubitemid 39423843)
43. Dickinson, R. B., Caro, L. and Purich, D. L., Force generation by cytoskeletal filament end-tracking proteins. Biophys J 2004. 87: 2838-2854.
44. Vinson, V. K., De La Cruz, E. M., Higgs, H. N. and Pollard, T. D., Interactions of Acanthamoeba profilin with actin and nucleotides bound to actin. Biochemistry 1998. 37: 10871-10880. (Pubitemid 28368911)
45. Fujiwara, I., Vavylonis, D. and Pollard, T. D., Polymerization kinetics of ADP- and ADP-Pi-actin determined by fluorescence microscopy. Proc Natl Acad Sci USA 2007. 104: 8827-8832. (Pubitemid 47175396)
46. Perelroizen, I., Didry, D., Christensen, H., Chua, N. H. and Carlier, M. F., Role of nucleotide exchange and hydrolysis in the function of profilin in action assembly. J Biol Chem 1996. 271: 12302-12309. (Pubitemid 26160894)
47. Selden, L. A., Kinosian, H. J., Estes, J. E. and Gershman, L. C., Impact of profilin on actin-bound nucleotide exchange and actin polymerization dynamics. Biochemistry 1999. 38: 2769-2778. (Pubitemid 129502919)
48. Kovar, D. R., Yang, P., Sale, W. S., Drobak, B. K. and Staiger, C. J., Chlamydomonas reinhardtii produces a profilin with unique biochemical properties. J Cell Sci 2001. 114: 4293-4305. (Pubitemid 33138666)
49. Perelroizen, I., Didry, D., Christensen, H., Chua, N.-H. and Carlier, M.-F., Role of nucleotide exchange and hydrolysis in the function of profilin in actin assembly. J Biol Chem 1996. 271: 12302-12309. (Pubitemid 26160894)
50. Astumian, R. D., Making molecules into motors. Sci Am 2001. 285: 56-64.
51. Vologodskii, A., Energy transformation in biological molecular motors. Phys Life Rev 2006. 3: 119-132.
52. Astumian, R. D., Thermodynamics and kinetics of a Brownian motor. Science 1997. 276: 917-922.
53. Ait-Haddou, R. and Herzog, W., Brownian ratchet models of molecular motors. Cell Biochem Biophys 2003. 38: 191-214. (Pubitemid 41270817)
54. Tomkiewicz, D., Nouwen, N. and Driessen, A. J., Pushing, pulling and trapping - modes of motor protein supported protein translocation. FEBS Lett 2007. 581: 2820-2828. (Pubitemid 46874386)
55. Simon, S. M., Peskin, C. S. and Oster, G. F., What drives the translocation of proteins? Proc Natl Acad Sci USA 1992. 89: 3770-3774.
56. Konevega, A. L., Fischer, N., Semenkov, Y. P., Stark, H., Wintermeyer, W. and Rodnina, M. V., Spontaneous reverse movement of mRNA-bound tRNA through the ribosome. Nature Struct Mol Biol 2007. 14: 318-324. (Pubitemid 46608346)
57. Lizunov, V. and Zimmerberg, J., Cellular biophysics: bacterial endospore, membranes and random fluctuation. Curr Biol 2006. 16: R1025-R1028. (Pubitemid 44894915)
58. Broder, D. H. and Pogliano, K., Forespore engulfment mediated by a ratchet-like mechanism. Cell 2006. 126: 917-928. (Pubitemid 44310773)
59. Saffarian, S., Qian, H., Collier, I., Elson, E. and Goldberg, G., Powering a burnt bridges Brownian ratchet: a model for an extracellular motor driven by proteolysis of collagen. Phys Rev E 2006. 73: 041909.
60. Hinrichsen, L., Meyerholz, A., Groos, S. and Ungewickell, E. J., Bending a membrane: how clathrin affects budding. Proc Natl Acad Sci USA 2006. 103: 8715-8720. (Pubitemid 43878085)
61. Raj, A. and Peskin, C. S., The influence of chromosome flexibility on chromosome transport during anaphase A. Proc Natl Acad Sci USA 2006. 103: 5349-5354.
62. Abbondanzieri, E. A.,Greenleaf,W. J., Shaevitz, J. W., Landick, R. and Block, S. M., Direct observation of base-pair stepping by RNA polymerase. Nature 2005. 438: 460-465. (Pubitemid 41742012)
63. Park, S., Koch, D., Cardenas, R., Kas, J. and Shih, C. K., Cell motility and local viscoelasticity of fibroblasts. Biophys J 2005. 89: 4330-4342. (Pubitemid 41725651)
64. Qian, H., A stochastic analysis of a Brownian ratchet model for actin-based motility. Mech Chem Biosyst 2004. 1: 267-278.
65. Burroughs, N. J. and Marenduzzo, D., Three-dimensional dynamic Monte Carlo simulations of elastic actin-like ratchets. J Chem Phys 2005. 123: 174908.
66. van Oudenaarden, A. and Theriot, J. A., Cooperative symmetry-breaking by actin polymerization in a model for cell motility. Nat Cell Biol 1999. 1: 493-499.
67. Mogilner, A. and Oster, G., Cell motility driven by actin polymerization. Biophys J 1996. 71: 3030-3045. (Pubitemid 26422346)
68. Astumian, R. D., The role of thermal activation in motion and force generation by molecular motors. Philos Trans R Soc Lond B Biol Sci 2000. 355: 511-522.
69. Astumian, R. D. and Derenyi, I., Fluctuation driven transport and models of molecular motors and pumps. Eur Biophys J 1998. 27: 474-489. (Pubitemid 28414888)
70. Astumian, R. D., Protein conformational fluctuations and free-energy transduction. Appl Phys A 2002. 75: 193-206.
71. Brenner, S. L. and Korn, E. D., On the mechanism of actin monomerpolymer subunit exchange at steady state. J Biol Chem 1983. 258: 5013-45563.
72. Vavylonis, D., Yang, Q. and O'Shaughnessy, B., Actin polymerization kinetics, cap structure, fluctuations. 2005. Proc Natl Acad Sci USA 102: 8543-8548. (Pubitemid 40862772)
73. Stukalin, E. B. and Kolomeisky, A. B., ATP hydrolysis stimulates large length fluctuations in single actin filaments. Biophys J 2006. 90: 2673-2685.
74. Paul, A. S. and Pollard, T. D., Energetic requirements for processive elongation of actin filaments by FH1FH2-formins. J Biol Chem 2009. 284: 12533-12540.
75. Weisswange, I., Newsome, T. P., Schleich, S. and Way, M., The rate of N-WASP exchange limits the extent of ARP2/3-complex-dependent actinbased motility. Nature 2009. 458: 87-91.
76. Sablin, E. P., Dawson, J. F., VanLoock, M. S., Spudich, J. A., Egelman, E. H. and Fletterick, R. J., How does ATP hydrolysis control actin's associations? Proc Natl Acad Sci USA 2002. 99: 10945-10947.
77. Drenckhahn, D. and Pollard, T. D., Elongation of actin filaments is a diffusion-limited reaction at the barbed end and is accelerated by inert macromolecules. J Biol Chem 1986. 261: 12754-12758. (Pubitemid 17204237)
78. Frederick, K. B., Sept, D. and De La Cruz, E. M., Effects of solution crowding on actin polymerization reveal the energetic basis for nucleotide- dependent filament stability. J Mol Biol 2008. 378: 540-550.
79. Yarmola, E. G., Parikh, S. and Bubb, M. R., Formation and implications of a ternary complex of profilin, thymosin b4, and actin. J Biol Chem 2001. 276: 45555-45563. (Pubitemid 37370788)
80. Yarmola, E. G., Klimenko, E. S., Fujita, G. and Bubb, M. R., Thymosin b4: actin regulation and more. Ann NY Acad Sci 2007. 1112: 76-85.
81. Kinosian, H. J., Selden, L. A., Lewis, C., Gershman, L. C. and Estes, J. E., Interdependence of profilin, cation, and nucleotide binding to vertebrate non-muscle actin. Biochemistry 2000. 39: 13176-13188.
82. Kovar, D. R., Harris, E. S., Mahaffy, R., Higgs, H. N. and Pollard, T. D., Control of the assembly of ATP- and ADP-actin by formins and profilin. Cell 2006. 124: 423-435. (Pubitemid 43121988)