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. 1999 Jun;76(6):3261–3266. doi: 10.1016/S0006-3495(99)77478-3

Water in actin polymerization.

N Fuller 1, R P Rand 1
PMCID: PMC1300295  PMID: 10354451

Abstract

We have addressed the question whether water is part of the G- to F-actin polymerization reaction. Under osmotic stress, the critical concentration for G-Ca-ATP actin was reduced for six different osmolytes. These results are interpreted as showing that reducing water activity favored the polymerized state. The magnitude of the effect correlated, then saturated, with increasing MW of the osmolyte and suggested that up to 10-12 fewer water molecules were associated with actin when it polymerized. By contrast, osmotic effects were insignificant for Mg-ATP actin. The nucleotide binding site of the Mg conformation is more closed than the Ca and more closely resembles the closed actin conformation in the polymerized state. These results suggest that the water may come from the cleft of the nucleotide binding site.

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Selected References

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  1. Bezrukov S. M., Vodyanoy I., Parsegian V. A. Counting polymers moving through a single ion channel. Nature. 1994 Jul 28;370(6487):279–281. doi: 10.1038/370279a0. [DOI] [PubMed] [Google Scholar]
  2. Bezrukov S. M., Vodyanoy I. Probing alamethicin channels with water-soluble polymers. Effect on conductance of channel states. Biophys J. 1993 Jan;64(1):16–25. doi: 10.1016/S0006-3495(93)81336-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bhat T. N., Bentley G. A., Boulot G., Greene M. I., Tello D., Dall'Acqua W., Souchon H., Schwarz F. P., Mariuzza R. A., Poljak R. J. Bound water molecules and conformational stabilization help mediate an antigen-antibody association. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):1089–1093. doi: 10.1073/pnas.91.3.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brenner S. L., Korn E. D. On the mechanism of actin monomer-polymer subunit exchange at steady state. J Biol Chem. 1983 Apr 25;258(8):5013–5020. [PubMed] [Google Scholar]
  5. Carlier M. F. Actin: protein structure and filament dynamics. J Biol Chem. 1991 Jan 5;266(1):1–4. [PubMed] [Google Scholar]
  6. Chik J. K., Lindberg U., Schutt C. E. The structure of an open state of beta-actin at 2.65 A resolution. J Mol Biol. 1996 Nov 8;263(4):607–623. doi: 10.1006/jmbi.1996.0602. [DOI] [PubMed] [Google Scholar]
  7. Colombo M. F., Rau D. C., Parsegian V. A. Protein solvation in allosteric regulation: a water effect on hemoglobin. Science. 1992 May 1;256(5057):655–659. doi: 10.1126/science.1585178. [DOI] [PubMed] [Google Scholar]
  8. De La Cruz E. M., Pollard T. D. Nucleotide-free actin: stabilization by sucrose and nucleotide binding kinetics. Biochemistry. 1995 Apr 25;34(16):5452–5461. doi: 10.1021/bi00016a016. [DOI] [PubMed] [Google Scholar]
  9. Detmers P., Weber A., Elzinga M., Stephens R. E. 7-Chloro-4-nitrobenzeno-2-oxa-1,3-diazole actin as a probe for actin polymerization. J Biol Chem. 1981 Jan 10;256(1):99–105. [PubMed] [Google Scholar]
  10. Drenckhahn D., 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 Sep 25;261(27):12754–12758. [PubMed] [Google Scholar]
  11. Gaertner A., Mayr G. W., Wegner A. Binding of sugar phosphates, inositol phosphates and phosphorylated amino acids to actin. Eur J Biochem. 1991 May 23;198(1):67–71. doi: 10.1111/j.1432-1033.1991.tb15987.x. [DOI] [PubMed] [Google Scholar]
  12. Garner M. M., Rau D. C. Water release associated with specific binding of gal repressor. EMBO J. 1995 Mar 15;14(6):1257–1263. doi: 10.1002/j.1460-2075.1995.tb07109.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gershman L. C., Selden L. A., Kinosian H. J., Estes J. E. Actin-bound nucleotide/divalent cation interactions. Adv Exp Med Biol. 1994;358:35–49. doi: 10.1007/978-1-4615-2578-3_4. [DOI] [PubMed] [Google Scholar]
  14. KASAI M., NAKANO E., OOSAWA F. POLYMERIZATION OF ACTIN FREE FROM NUCLEOTIDES AND DIVALENT CATIONS. Biochim Biophys Acta. 1965 Mar 29;94:494–503. doi: 10.1016/0926-6585(65)90058-0. [DOI] [PubMed] [Google Scholar]
  15. Kabsch W., Holmes K. C. The actin fold. FASEB J. 1995 Feb;9(2):167–174. doi: 10.1096/fasebj.9.2.7781919. [DOI] [PubMed] [Google Scholar]
  16. Kabsch W., Mannherz H. G., Suck D., Pai E. F., Holmes K. C. Atomic structure of the actin:DNase I complex. Nature. 1990 Sep 6;347(6288):37–44. doi: 10.1038/347037a0. [DOI] [PubMed] [Google Scholar]
  17. Korn E. D., Carlier M. F., Pantaloni D. Actin polymerization and ATP hydrolysis. Science. 1987 Oct 30;238(4827):638–644. doi: 10.1126/science.3672117. [DOI] [PubMed] [Google Scholar]
  18. Kornblatt J. A., Kornblatt M. J., Hoa G. H., Mauk A. G. Responses of two protein-protein complexes to solvent stress: does water play a role at the interface? Biophys J. 1993 Sep;65(3):1059–1065. doi: 10.1016/S0006-3495(93)81168-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kouyama T., Mihashi K. Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur J Biochem. 1981;114(1):33–38. [PubMed] [Google Scholar]
  20. Leikin S., Parsegian V. A., Rau D. C., Rand R. P. Hydration forces. Annu Rev Phys Chem. 1993;44:369–395. doi: 10.1146/annurev.pc.44.100193.002101. [DOI] [PubMed] [Google Scholar]
  21. LiCata V. J., Allewell N. M. Functionally linked hydration changes in Escherichia coli aspartate transcarbamylase and its catalytic subunit. Biochemistry. 1997 Aug 19;36(33):10161–10167. doi: 10.1021/bi970669r. [DOI] [PubMed] [Google Scholar]
  22. Lorenz M., Popp D., Holmes K. C. Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J Mol Biol. 1993 Dec 5;234(3):826–836. doi: 10.1006/jmbi.1993.1628. [DOI] [PubMed] [Google Scholar]
  23. Na G. C., Butz L. J., Bailey D. G., Carroll R. J. In vitro collagen fibril assembly in glycerol solution: evidence for a helical cooperative mechanism involving microfibrils. Biochemistry. 1986 Mar 11;25(5):958–966. doi: 10.1021/bi00353a003. [DOI] [PubMed] [Google Scholar]
  24. Na G. C. Interaction of calf skin collagen with glycerol: linked function analysis. Biochemistry. 1986 Mar 11;25(5):967–973. doi: 10.1021/bi00353a004. [DOI] [PubMed] [Google Scholar]
  25. Na G. C., Timasheff S. N. Interaction of calf brain tubulin with glycerol. J Mol Biol. 1981 Sep 5;151(1):165–178. doi: 10.1016/0022-2836(81)90226-6. [DOI] [PubMed] [Google Scholar]
  26. Orlova A., Chen X., Rubenstein P. A., Egelman E. H. Modulation of yeast F-actin structure by a mutation in the nucleotide-binding cleft. J Mol Biol. 1997 Aug 15;271(2):235–243. doi: 10.1006/jmbi.1997.1163. [DOI] [PubMed] [Google Scholar]
  27. Pantaloni D., Carlier M. F., Coué M., Lal A. A., Brenner S. L., Korn E. D. The critical concentration of actin in the presence of ATP increases with the number concentration of filaments and approaches the critical concentration of actin.ADP. J Biol Chem. 1984 May 25;259(10):6274–6283. [PubMed] [Google Scholar]
  28. Pardee J. D., Spudich J. A. Purification of muscle actin. Methods Cell Biol. 1982;24:271–289. doi: 10.1016/s0091-679x(08)60661-5. [DOI] [PubMed] [Google Scholar]
  29. Parsegian V. A., Rand R. P., Rau D. C. Macromolecules and water: probing with osmotic stress. Methods Enzymol. 1995;259:43–94. doi: 10.1016/0076-6879(95)59039-0. [DOI] [PubMed] [Google Scholar]
  30. Reid C., Rand R. P. Probing protein hydration and conformational states in solution. Biophys J. 1997 Mar;72(3):1022–1030. doi: 10.1016/S0006-3495(97)78754-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Timasheff S. N. The control of protein stability and association by weak interactions with water: how do solvents affect these processes? Annu Rev Biophys Biomol Struct. 1993;22:67–97. doi: 10.1146/annurev.bb.22.060193.000435. [DOI] [PubMed] [Google Scholar]
  32. Tobacman L. S., Korn E. D. The regulation of actin polymerization and the inhibition of monomeric actin ATPase activity by Acanthamoeba profilin. J Biol Chem. 1982 Apr 25;257(8):4166–4170. [PubMed] [Google Scholar]
  33. Valentin-Ranc C., Carlier M. F. Role of ATP-bound divalent metal ion in the conformation and function of actin. Comparison of Mg-ATP, Ca-ATP, and metal ion-free ATP-actin. J Biol Chem. 1991 Apr 25;266(12):7668–7675. [PubMed] [Google Scholar]
  34. Vodyanoy I., Bezrukov S. M., Parsegian V. A. Probing alamethicin channels with water-soluble polymers. Size-modulated osmotic action. Biophys J. 1993 Nov;65(5):2097–2105. doi: 10.1016/S0006-3495(93)81245-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wriggers W., Schulten K. Stability and dynamics of G-actin: back-door water diffusion and behavior of a subdomain 3/4 loop. Biophys J. 1997 Aug;73(2):624–639. doi: 10.1016/S0006-3495(97)78098-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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