The roles of ATP in the dynamics of the actin filaments of the cytoskeleton
-
Erwin W. Becker
Abstract
In contrast to the actin filaments of muscle, which are stabilized by special proteins, actin filaments of the cytoskeleton are highly dynamic. In vitro observations at room temperature have led to the conclusion that the hydrolysis of ATP, which accompanies the polymerization of ATP-containing monomers, destabilizes the filaments of the actin skeleton. Many functions of this skeleton, such as signal transduction, the anchoring of cell adhesion complexes, and the transfer and generation of pulling forces, can obviously only be adequately performed by stable filaments. Here it is assumed that, at room temperature, the interaction of ADP-containing monomers is impaired by complexed water molecules that partly shield the binding surfaces. The possibility that, at higher temperatures, the interaction of the monomers is strong enough to prevent spontaneous filament depolymerization is explored. Using mechanical models that take into account binding forces and energies, the polymerization cycle expected under these conditions is described. It is shown that ATP serves primarily to prevent incorrect binding of the incoming monomer to the end of the filament (‘adjusted fit’). In addition, it provides the free energy needed for disassembly of the expected stable filaments.
References
Arber, S., Barbayannis, F.A., Hanser, H., Schneider, C., Stanyon C.A., Bernard, O., and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature393, 805–809.10.1038/31729Search in Google Scholar
Bagshaw, C.R. and Trentham, D.R. (1973). The reversibility of adenosine triphosphate cleavage by myosin. Biochem. J.133,323–328.10.1042/bj1330323Search in Google Scholar
Bear, J.E., Svitkina, T.M., Krause, M., Schafer, D.A., Loureiro, J.J., Strasser, G.A., Maly, I.V., Chaga, O.Y., Cooper, J.A., Borisy, G.G., and Gertler, F.B. (2002). Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell109, 509–521.10.1016/S0092-8674(02)00731-6Search in Google Scholar
Becker, E.W. (1992). Dynamics and kinetics of enzymes. Kinetic equilibrium of forces in Biochemistry. Z. Naturforsch.47c, 628–633.Search in Google Scholar
Becker, E.W. (2000). Kinetic equilibrium of forces and molecular events in muscle contraction. Proc. Natl. Acad. Sci. USA97, 157–161.10.1073/pnas.97.1.157Search in Google Scholar PubMed PubMed Central
Becker, E.W. (2004). Relevance of the kinetic equilibrium of forces to the control of the cell cycle by Ras proteins. Biol. Chem.385, 41–47.10.1515/BC.2004.006Search in Google Scholar PubMed
Bernheim-Groswasser, A., Wiesner, S., Golsteyr, R.M., Carlier, M.-F., and Sykes, C. (2002). The dynamics of actin-based motility depend on surface parameters. Nature417, 308–311.10.1038/417308aSearch in Google Scholar PubMed
Blanchoin, L. and Pollard, T.D. (1999). Mechanism of interaction of Acanthamoeba actophorin (ADF/Cofilin) with actin filaments. J. Biol. Chem.274,15538–15546.10.1074/jbc.274.22.15538Search in Google Scholar PubMed
Cooke, R. and Murdoch, L. (1973). Interaction of actin with analogs of adenosine triphosphate. Biochemistry12, 3927–3932.10.1021/bi00744a022Search in Google Scholar PubMed
De La Cruz, E.M., Mandinova, A., Steinmetz, M.O., Stoffler, D., Aebi, U., and Pollard, T.D. (2000). Polymerization and structure of nucleotide-free actin filaments. J. Mol. Biol.295, 517–526.10.1006/jmbi.1999.3390Search in Google Scholar PubMed
Frischknecht, F., Moreau, V., Röttger, S., Gonfloni, S., Reckmann, I., Superti-Furga, G., and Way, M. (1999). Actin-based motility of vaccinia virus mimics receptor tyrosine kinase signalling. Nature401, 926–929.10.1038/44860Search in Google Scholar PubMed
Giehl, K., Menke, A., Wedlich, D., Beil, M., and Seufferlein, T. (2005). From tumorigenesis to tumor progression: signaling pathways driving tumor invasion and metastasis. In: Cell Migration, D. Wedlich, ed. (Weinheim, Germany: Wiley-VCH), pp. 299–339.Search in Google Scholar
Hill, T.L. and Simmons, R.M. (1976). Free energy levels and entropy production associated with biochemical kinetic diagrams. Proc. Natl. Acad. Sci. USA73, 95–99.10.1073/pnas.73.1.95Search in Google Scholar
Holmes, K.C., Popp, D., Gebhard, W., and Kabsch, W. (1990). Atomic model of the actin filament. Nature347, 44–49.10.1038/347044a0Search in Google Scholar
Howard, J. (2001). Active polymerization. In: Mechanics of Motor Proteins and the Cytoskeleton (Sunderland, MA, USA: Sinauer Associates), pp. 179–193.Search in Google Scholar
Kodama, T. (1985). Thermodynamic analysis of muscle ATPase mechanisms. Physiol. Rev. 65,467–551.10.1152/physrev.1985.65.2.467Search in Google Scholar
Koshland, D.E. Jr. (1970). The molecular basis for enzyme regulation. In: The Enzymes, Vol. 1, P.D. Boyer, ed. (New York, USA: Academic Press).Search in Google Scholar
Kovac, L. (1987). Bioenergetics between chemistry, genetics, and physics. Curr. Top. Bioenerg.15, 331–372.Search in Google Scholar
Loisel, T.P., Boujemaa, R., Pantaloni, D., and Carlier, M.-F. (1999). Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature401, 613–616.10.1038/44183Search in Google Scholar
Machesky, L.M. and Cooper, J.A. (1999). Bare bones of the cytoskeleton. Nature401, 542–543.10.1038/44044Search in Google Scholar
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. USA96, 3739–3744.10.1073/pnas.96.7.3739Search in Google Scholar
Mitchison, T.J. and Cramer, L.P (1996). Actin-based cell motility and cell locomotion. Cell84, 371–379.10.1016/S0092-8674(00)81281-7Search in Google Scholar
Mogilner, A. and Oster, G. (1996). Cell motility driven by actin polymerization. Biophys. J.71, 3030–3045.10.1016/S0006-3495(96)79496-1Search in Google Scholar
Monod, J., Wyman, J., and Changeux, J.P. (1965). On the nature of allosteric transition: a plausible model. J. Mol. Biol.12, 88–118.10.1016/S0022-2836(65)80285-6Search in Google Scholar
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 filaments. Proc. Natl. Acad. Sci. USA95, 6181–6186.10.1073/pnas.95.11.6181Search in Google Scholar PubMed PubMed Central
Pantaloni, D., Le Clainche, C., and Carlier, M.-F. (2001). Mechanism of actin-based motility. Science292, 1502–1506.10.1126/science.1059975Search in Google Scholar
Pollard, T.D. (1986). Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J. Cell Biol.103, 2747–2754.10.1083/jcb.103.6.2747Search in Google Scholar
Pollard, T.D. and Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell112, 453–465.10.1016/S0092-8674(03)00120-XSearch in Google Scholar
Ponta, H., Sherman, L., and Herrlich, P.A. (2003). CD44: from adhesion molecules to signaling regulators. Nat. Rev. Mol. Cell Biol.4, 33–45.10.1038/nrm1004Search in Google Scholar
Schutt, C.E., Myslik, J.C., Rozycki, M.D., Goonesekere, N.C.W., and Lindberg, U. (1993). The structure of crystalline profilin-β-actin. Nature365,810–816.10.1038/365810a0Search in Google Scholar
Tsukita, S., Yonemura, S., and Tsukita, S. (1997). ERM proteins: head-to-tail regulation of actin-plasma membrane interaction. Trends Biochem. Sci.22, 53–58.10.1016/S0968-0004(96)10071-2Search in Google Scholar
Wanger, M. and Wegner, A. (1983). Similar affinities of ADP and ATP for G-actin at physiological salt concentrations. FEBS Lett.162, 112–116.10.1016/0014-5793(83)81059-XSearch in Google Scholar
Weber, A. (1999). Actin binding proteins that change extend and rate of actin monomer-polymer distribution by different mechanisms. Mol. Cell. Biochem.190, 67–74.10.1023/A:1006984010267Search in Google Scholar
Wyman, J. (1975). The turning wheel: a study in steady states. Proc. Natl. Acad. Sci. USA72, 3983–3987.10.1073/pnas.72.10.3983Search in Google Scholar PubMed PubMed Central
Yang, N., Higuchi, O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E., and Mizuno, K. (1998). Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature393, 809–812.10.1038/31735Search in Google Scholar PubMed
Zigmond, S.H. (2004). Beginning and ending an actin filament: control at the barbed end. Curr. Top. Dev. Biol.63, 145–188.10.1016/S0070-2153(04)63005-5Search in Google Scholar
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- Highlight: chronic oxidative stress and cancer
- Risk factors and mechanisms of hepatocarcinogenesis with special emphasis on alcohol and oxidative stress
- Does Helicobacter pylori cause gastric cancer via oxidative stress?
- Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis
- Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids
- Concomitant suppression of hyperlipidemia and intestinal polyp formation by increasing lipoprotein lipase activity in Apc-deficient mice
- Cancer-preventive anti-oxidants that attenuate free radical generation by inflammatory cells
- Evidence for attenuated cellular 8-oxo-7,8-dihydro-2′-deoxyguanosine removal in cancer patients
- The roles of ATP in the dynamics of the actin filaments of the cytoskeleton
- Chiral distinction between the enantiomers of bicyclic alcohols by UDP-glucuronosyltransferases 2B7 and 2B17
- A structural model of 20S immunoproteasomes: effect of LMP2 codon 60 polymorphism on expression, activity, intracellular localisation and insight into the regulatory mechanisms
- Role of the kinin B1 receptor in insulin homeostasis and pancreatic islet function
- Comparative proteomic analysis of neoplastic and non-neoplastic germ cell tissue
- BID, an interaction partner of protein kinase CK2α
- Monomeric and dimeric GDF-5 show equal type I receptor binding and oligomerization capability and have the same biological activity
- Novel ketomethylene inhibitors of angiotensin I-converting enzyme (ACE): inhibition and molecular modelling
- Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain
- A fluorescence assay for rapid detection of ligand binding affinity to HIV-1 gp41
Articles in the same Issue
- Highlight: chronic oxidative stress and cancer
- Risk factors and mechanisms of hepatocarcinogenesis with special emphasis on alcohol and oxidative stress
- Does Helicobacter pylori cause gastric cancer via oxidative stress?
- Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis
- Mutagenesis and carcinogenesis caused by the oxidation of nucleic acids
- Concomitant suppression of hyperlipidemia and intestinal polyp formation by increasing lipoprotein lipase activity in Apc-deficient mice
- Cancer-preventive anti-oxidants that attenuate free radical generation by inflammatory cells
- Evidence for attenuated cellular 8-oxo-7,8-dihydro-2′-deoxyguanosine removal in cancer patients
- The roles of ATP in the dynamics of the actin filaments of the cytoskeleton
- Chiral distinction between the enantiomers of bicyclic alcohols by UDP-glucuronosyltransferases 2B7 and 2B17
- A structural model of 20S immunoproteasomes: effect of LMP2 codon 60 polymorphism on expression, activity, intracellular localisation and insight into the regulatory mechanisms
- Role of the kinin B1 receptor in insulin homeostasis and pancreatic islet function
- Comparative proteomic analysis of neoplastic and non-neoplastic germ cell tissue
- BID, an interaction partner of protein kinase CK2α
- Monomeric and dimeric GDF-5 show equal type I receptor binding and oligomerization capability and have the same biological activity
- Novel ketomethylene inhibitors of angiotensin I-converting enzyme (ACE): inhibition and molecular modelling
- Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain
- A fluorescence assay for rapid detection of ligand binding affinity to HIV-1 gp41