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• W3043812980 abstract "Proteins from the tubulin and actin superfamilies self-assemble, forming dynamic filaments that are essential for DNA segregation, cell division, cytoplasmic organization, and motility. These filaments translocate (treadmill) fueled by nucleotide hydrolysis to perform their functions, even without motor proteins, growing from one end, whereas shortening from the other. Tubulin and bacterial FtsZ assembly machines adopt two main conformations: the free unassembled proteins are in a low self-association affinity relaxed (R) structure, whereas the subunits in polymers (microtubules and FtsZ filaments) are held in a high self-association affinity tense (T) form. Switching from the R to the T state is fundamentally coupled to the formation of a tight longitudinal association interface between consecutive subunits in the filament rather than to the nucleotide state. The assembly switch entails a rotation of the GTPase-activating domain with respect to the GTP-binding domain (FtsZ: open interdomain cleft = T vs. closed cleft = R; tubulin: straight subunits = T vs. curved subunits = R). The local interactions made by the nucleotide γ-phosphate chemically enhance the affinity of the longitudinal association interface rather than induce large structural changes. Tubulin makes additional lateral contacts with neighbor protofilaments in microtubules. The cooperative assembly of single-stranded FtsZ filaments and their treadmilling mechanism were puzzles, for which the solutions can also illuminate the dynamic mechanisms of more complex cytomotive filaments. Assembly models in which FtsZ monomers switch between low- and high-affinity conformations explain nucleated condensation polymerization of linear filaments (1Huecas S. Llorca O. Andreu J.M. et al.Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments.Biophys. J. 2008; 94: 1796-1806Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar,2Miraldi E.R. Thomas P.J. Romberg L. Allosteric models for cooperative polymerization of linear polymers.Biophys. J. 2008; 95: 2470-2486Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar) and the directional filament treadmilling upon GTP hydrolysis at the association interfaces (3Wagstaff J.M. Tsim M. Löwe J. et al.A polymerization-associated structural switch in FtsZ that enables treadmilling of model filaments.MBio. 2017; 8: e00254-17Crossref PubMed Scopus (44) Google Scholar). In this issue of Biophysical Journal, Corbin and Erickson present a timely numerical model of FtsZ filament assembly, nucleotide hydrolysis, and treadmilling employing Monte Carlo methods (4Corbin L. Erickson H.P. A unified model for treadmilling and nucleation of single-stranded FtsZ protofilaments.Biophys. J. 2020; 119: 792-805Abstract Full Text Full Text PDF Scopus (5) Google Scholar). Interestingly, the tubulin assembly switch possibly enables both microtubule treadmilling and dynamic instability. Actin filament treadmilling appears to involve an analogous mechanism, in which G-actin may be identified as an R state and F-actin as a T state. To analyze possible treadmilling mechanisms, let us first consider a GTP-hydrolyzing single-stranded protein filament (Fig. 1, Model A). A polar filament can, in principle, treadmill with nucleotide hydrolysis (5Wegner A. Head to tail polymerization of actin.J. Mol. Biol. 1976; 108: 139-150Crossref PubMed Scopus (438) Google Scholar). However, three problems can be identified that prevent the formation of a treadmilling single-stranded filament by this mechanism: 1) oligomers are formed, with a smaller proportion of larger species, rather than long filaments because the association affinity is constant at each association step; 2) oligomers fragment at the interfaces, where the nucleotide has been hydrolyzed at a rate similar to the dissociation rate at a diphosphate-containing end; and 3) the monomer association reactions at both oligomer ends are identical and thus have the same rate. For the association rates to be different at the top and bottom ends of a single-stranded filament, the association reactions at each end must have different initial, transition, or end states. Such differences might, in principle, be induced by the nucleotide γ-phosphate (in monomers or in polymer) or by the intermolecular protein contacts in the polymer. In the second model (Fig. 1, Model B), the protein monomers autosterically switch (6Caspar D.L. Movement and self-control in protein assemblies. Quasi-equivalence revisited.Biophys. J. 1980; 32: 103-138Abstract Full Text PDF PubMed Scopus (192) Google Scholar) between a state with low self-association affinity when unassembled (R) and a state with high-association affinity (T) when forming part of the polymer. Three main features can be identified in Model B: 1) the unfavorable switching from R to T subunits explains nucleated condensation polymerization of linear filaments with a cooperative behavior (1Huecas S. Llorca O. Andreu J.M. et al.Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments.Biophys. J. 2008; 94: 1796-1806Abstract Full Text Full Text PDF PubMed Scopus (81) Google Scholar,2Miraldi E.R. Thomas P.J. Romberg L. Allosteric models for cooperative polymerization of linear polymers.Biophys. J. 2008; 95: 2470-2486Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar,7Michie K.A. Löwe J. Dynamic filaments of the bacterial cytoskeleton.Annu. Rev. Biochem. 2006; 75: 467-492Crossref PubMed Scopus (169) Google Scholar, 8Dajkovic A. Lutkenhaus J. Z ring as executor of bacterial cell division.J. Mol. Microbiol. Biotechnol. 2006; 11: 140-151Crossref PubMed Scopus (88) Google Scholar, 9Lan G. Dajkovic A. Sun S.X. et al.Polymerization and bundling kinetics of FtsZ filaments.Biophys. J. 2008; 95: 4045-4056Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar) driven by the tight association contacts in the filament (10Matsui T. Han X. Tanaka I. et al.Structural change in FtsZ Induced by intermolecular interactions between bound GTP and the T7 loop.J. Biol. Chem. 2014; 289: 3501-3509Crossref PubMed Scopus (36) Google Scholar) rather than forming shorter oligomers as in model A. In support of this model, FtsZ T subunits relax to R subunits when isolated during atomistic molecular dynamics simulations starting from the crystal filament T structure ((11Ramírez-Aportela E. López-Blanco J.R. Chacón P. et al.Understanding nucleotide-regulated FtsZ filament dynamics and the monomer assembly switch with large-scale atomistic simulations.Biophys. J. 2014; 107: 2164-2176Abstract Full Text Full Text PDF PubMed Scopus (19) Google Scholar) and references therein) and also relax upon FtsZ disassembly during solution experiments, as monitored with fluorescent reporters (12Chen Y. Erickson H.P. Conformational changes of FtsZ reported by tryptophan mutants.Biochemistry. 2011; 50: 4675-4684Crossref PubMed Scopus (37) Google Scholar,13Artola M. Ruíz-Avila L.B. Huecas S. et al.The structural assembly switch of cell division protein FtsZ probed with fluorescent allosteric inhibitors.Chem. Sci. (Camb.). 2017; 8: 1525-1534Crossref PubMed Scopus (19) Google Scholar). Moreover, it has been possible to determine both T and R crystal structures from the same FtsZ protein (3Wagstaff J.M. Tsim M. Löwe J. et al.A polymerization-associated structural switch in FtsZ that enables treadmilling of model filaments.MBio. 2017; 8: e00254-17Crossref PubMed Scopus (44) Google Scholar,14Fujita J. Harada R. Matsumura H. et al.Identification of the key interactions in structural transition pathway of FtsZ from Staphylococcus aureus.J. Struct. Biol. 2017; 198: 65-73Crossref PubMed Scopus (17) Google Scholar). Notice that the structures of diverse unassembled FtsZ proteins correspond to the R state, irrespective of the bound nucleotide. On the other hand, the available crystal structures of T-FtsZ filaments contain GDP and are still missing a filament structure with a bound GTP analog. 2) A second feature is that the fragmentation rate is slower than dissociation from the end because an inner subunit is held in the T state by the contacts to the surrounding subunits along the filament. 3) Importantly, the structural switch between R and T makes both ends kinetically different. It creates different initial pairs of surfaces for association at each end so that the association rates become different, and the single filament can thus treadmill with nucleotide hydrolysis (3Wagstaff J.M. Tsim M. Löwe J. et al.A polymerization-associated structural switch in FtsZ that enables treadmilling of model filaments.MBio. 2017; 8: e00254-17Crossref PubMed Scopus (44) Google Scholar). This creates a translocating filament, a linear motor able to move and generate force when reversibly attached to a suitable stator. The end additions in Model B really encompass both switching and association reactions in a nonspecified kinetic pathway. Also, the kinetic growth (plus) and shrinkage (minus) ends can, in principle, be at the structural top (exposed nucleotide) and bottom ends, or vice versa, the growing end can be at the bottom, and the shrinking end can be at the top. This second possibility, with the filament treadmilling downward, has been chosen in Model B, according to the kinetic polarity deduced from the effects of top and bottom mutations in FtsZ (15Du S. Pichoff S. Lutkenhaus J. et al.FtsZ filaments have the opposite kinetic polarity of microtubules.Proc. Natl. Acad. Sci. USA. 2018; 115: 10768-10773Crossref PubMed Scopus (17) Google Scholar). Thanks to the Monte Carlo model of Corbin and Erickson (4Corbin L. Erickson H.P. A unified model for treadmilling and nucleation of single-stranded FtsZ protofilaments.Biophys. J. 2020; 119: 792-805Abstract Full Text Full Text PDF Scopus (5) Google Scholar), we can now quantitatively understand how treadmilling of single filaments works. The available MATLAB (The MathWorks, Natick, MA) code and user-friendly application permit testing of various values for the switch equilibrium constant, the rates of subunit addition, dissociation from plus and minus ends, and the GTP hydrolysis rate. We now know how both the structural switch and GTP hydrolysis are required for treadmilling. The model captures the birth and dynamic behavior of numerous simulated individual filaments. The bulk properties of simulated FtsZ solutions, including the monomer concentration, filament length distribution, GTP hydrolysis, and exchange of monomers between filaments, are in good agreement with experimental measurements from the Erickson lab on various FtsZ proteins. The model also incorporates sequestering and capping proteins. Interestingly, the treadmilling velocity depends on the GTPase activity, similar to FtsZ treadmilling in bacterial cells. Adding a reversible surface association feature to the model simulations might more closely simulate membrane-tethered FtsZ filaments in cells and in synthetic models systems. Let us now turn to multistranded polymers with nucleotide hydrolysis (Fig. 1, Model C). Bidimensional polymerization is typically cooperative, proceeding above a critical protein concentration for elongation (16Oosawa F. Asakura S. Thermodynamics of the Polymerization of Protein. Academic Press, London and New York1975Google Scholar). A multistranded polymer with nucleotide hydrolyzing subunits treadmills with a head-to-tail polymerization mechanism analytically demonstrated by Wegner in his landmark study (5Wegner A. Head to tail polymerization of actin.J. Mol. Biol. 1976; 108: 139-150Crossref PubMed Scopus (438) Google Scholar). Notice that the treadmilling direction in Model C has been drawn opposite to Model B to make it compatible with that of actin filaments and microtubules, which were previously thought to treadmill according to this type of mechanism. This model posits that the transition states, and therefore the rate constants of subunit addition and dissociation at the ends of a polar polymer, need not be equal, even in the absence of nucleotide hydrolysis, in which the equilibrium association constants are identical at both ends. Clearly, this is not the case for a single-stranded oligomer, in which the protein contacts are identical at both ends (Fig. 1, Model A), but in a multistranded polymer the association interfaces at each end may be somehow different. In Model C the longitudinal and lateral interactions made by one monomer at the top and bottom ends are similar, although with opposite handedness (see contacts marked by red dashes in Fig. 1, Model C). It might be debated whether this could be enough for different encounter kinetics at each filament end or whether a monomer structural switch is actually involved (6Caspar D.L. Movement and self-control in protein assemblies. Quasi-equivalence revisited.Biophys. J. 1980; 32: 103-138Abstract Full Text PDF PubMed Scopus (192) Google Scholar), similar to the case of single-stranded filaments. A key feature of this model is that different critical concentrations at each end are created by nucleotide hydrolysis. Notice that, in the model, the nucleotide forms part of the axial association interface, such as GTP/GDP in FtsZ and tubulin, and thus the association affinity may be directly reduced by hydrolysis at the shrinking end. However, in an actin-like filament, the ATP/ADP nucleotide binds into the monomer core rather than at an association interface. It may thus be argued that for a Wegner-type Model C to work for actin, it must contain some structural change transmitted from the association interfaces for internal nucleotide hydrolysis and that nucleotide hydrolysis has to allosterically reduce the association affinity at the shrinking end. A mechanism of multistranded polymerization with nucleotide hydrolysis and assembly switch (Fig. 1, Model D) may be proposed for actin and microtubule assembly, supported by current results. This model is a logical combination of Models B and C. It should treadmill as the single-stranded FtsZ filament B can, and it is further stabilized by the lateral interactions in the polymer lattice, similar to C. The concept of a polymerization-driven structural switch in microtubule assembly was proposed to explain the curved (R) structures of unassembled tubulins, irrespective of the bound nucleotide, in contrast with straight (T) tubulin in microtubules ((17Buey R.M. Díaz J.F. Andreu J.M. The nucleotide switch of tubulin and microtubule assembly: a polymerization-driven structural change.Biochemistry. 2006; 45: 5933-5938Crossref PubMed Scopus (74) Google Scholar,18Rice L.M. Montabana E.A. Agard D.A. The lattice as allosteric effector: structural studies of alphabeta- and gamma-tubulin clarify the role of GTP in microtubule assembly.Proc. Natl. Acad. Sci. USA. 2008; 105: 5378-5383Crossref PubMed Scopus (151) Google Scholar) and references therein); the tubulin assembly switch has been further supported by biochemical and structural studies. Indeed, recent cryo-EM structures of undecorated microtubules with different nucleotides have revealed similar tubulin subunit structures, with subtle structural changes mainly taking place at the longitudinal association interface (19Zhang R. LaFrance B. Nogales E. Separating the effects of nucleotide and EB binding on microtubule structure.Proc. Natl. Acad. Sci. USA. 2018; 115: E6191-E6200Crossref PubMed Scopus (50) Google Scholar). However, the exact role of the lateral interactions in microtubule assembly is still debated. Observations of individual curved protofilaments at growing microtubule ends (20McIntosh J.R. O’Toole E. Gudimchuk N. et al.Microtubules grow by the addition of bent guanosine triphosphate tubulin to the tips of curved protofilaments.J. Cell Biol. 2018; 217: 2691-2708Crossref PubMed Scopus (57) Google Scholar) suggest that the longitudinal interactions might primarily induce tubulin affinity switching or propagate from the lattice end, followed by protofilament straightening as the lateral interactions are formed. Extension of the numerical simulation model of Corbin and Erickson (4Corbin L. Erickson H.P. A unified model for treadmilling and nucleation of single-stranded FtsZ protofilaments.Biophys. J. 2020; 119: 792-805Abstract Full Text Full Text PDF Scopus (5) Google Scholar) to multistranded filaments should be helpful in analyzing the interplay of the structural switch, longitudinal and lateral interactions in microtubule treadmilling, and dynamic instability. Interestingly, actin appears to have converged to a conceptually similar assembly-switch mechanism, in which G-actin may be identified as an R state and F-actin as a T state. Indeed, recent cryo-EM structures of actin filaments with different bound nucleotides have confirmed a large structural change (monomer flattening) with interdomain rotation and translation that takes place upon actin monomer incorporation into filaments, rather than by the bound nucleotide, and have also revealed the small structural changes responsible for ATP hydrolysis and for subunit dissociation after phosphate release (21Merino F. Pospich S. Raunser S. et al.Structural transitions of F-actin upon ATP hydrolysis at near-atomic resolution revealed by cryo-EM.Nat. Struct. Mol. Biol. 2018; 25: 528-537Crossref PubMed Scopus (60) Google Scholar,22Chou S.Z. Pollard T.D. Mechanism of actin polymerization revealed by cryo-EM structures of actin filaments with three different bound nucleotides.Proc. Natl. Acad. Sci. USA. 2019; 116: 4265-4274Crossref PubMed Scopus (57) Google Scholar). Further investigation should reveal whether assembly switches are a constitutive feature of all treadmilling protein filaments. A Unified Model for Treadmilling and Nucleation of Single-Stranded FtsZ ProtofilamentsCorbin et al.Biophysical JournalJuly 16, 2020In BriefBacterial cell division is tightly coupled to the dynamic behavior of FtsZ, a tubulin homolog. Recent experimental work in vitro and in vivo has attributed FtsZ’s assembly dynamics to treadmilling, in which subunits add to the bottom and dissociate from the top of protofilaments. However, the molecular mechanisms producing treadmilling have yet to be characterized and quantified. We have developed a Monte Carlo model for FtsZ assembly that explains treadmilling, and also explains assembly nucleation by the same mechanisms. Full-Text PDF Open Archive" @default.
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• W3043812980 title "How Protein Filaments Treadmill" @default.
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