An oscillatory mode for microtubule assembly.

Pirollet, Fabienne; Job, Didier; Margolis, Robert L.; Garel, Jean‐Renaud

doi:10.1002/j.1460-2075.1987.tb02642.x

Cited by 71 publications

(70 citation statements)

References 17 publications

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“…The present results also allow us to propose a comprehensive interpretation of the recent observations of Pirollet et al (1987) within our model. These authors reported oscillations of microtubules in the presence of a GTP-regenerating system; total absence of free GTP was an absolute requisite to the observation of oscillations.…”

Section: T-gtp < Isupporting

confidence: 71%

“…Oscillatory polymerization kinetics have also been reported under similar ionic conditions (Pirollet et al, 1987) except that the absence of free GTP was strictly required and the restoration of tubulin bound GTP had to be ensured by a GTP-regenerating system. In the same medium conditions as Carlier et al (1987a), the existence of oscillations has recently been confirmed using synchrotron radiation (Mandelkow et al, 1988).…”

Section: Introductionmentioning

confidence: 86%

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Oscillations in microtubule polymerization: the rate of GTP regeneration on tubulin controls the period.

1988

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The essential reactions involved in the oscillatory kinetics of microtubule polymerization have been investigated. The rate of GDP dissociation from tubulin decreased cooperatively upon increasing tubulin concentration above 20 /M, consistent with the formation of GDP oligomers whose dissociation is rate limiting in nucleotide exchange. The apparent rate constant for nucleotide exchange at high tubulin concentration was 0.02 s-1 at 37°C, which is the exact value needed in previous theoretical sinulations to obtain oscillations with the real period of 70-80 s. A glass filter assay separating microtubules from oligomers and tubulin allowed nucleotide bound to non-microtubular tubulin during the oscillations to be monitored. In agreement with nucleotide exchange data, tubulin-bound GDP was found to oscillate in antiphase with microtubules. By varying the concentration of an enzymatic GTP-regenerating system, we could demonstrate that the period of the oscillations is directly controlled by the rate at which GTP is regenerated on tubulin, and oscillations can be observed under conditions where the dissociation of oligomers is no longer rate limiting. The possible physiological significance of GTPregenerating systems in establishing synchrony in a microtubule population is evoked. The present data confirm and extend the model that we previously proposed to account for the oscillations.

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Section: T-gtp < Isupporting

confidence: 71%

Section: Introductionmentioning

confidence: 86%

Oscillations in microtubule polymerization: the rate of GTP regeneration on tubulin controls the period.

1988

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“…Pirollet et al [14] have observed oscillations with ultraviolet light scattering, using a GTP-regenerating system. They do not specify a reaction model, but in our view their observations belong to the class of internally forced oscillations.…”

Section: Comparison With Other Published Results On Oscillationsmentioning

confidence: 99%

“…This leads to slow oscillations, with phases of assembly followed by nearly complete breakdown of microtubules. Another example is the experiment of Pirollet et al [14] who use acetate kinase, as discussed later. A computer simulation of this type of oscillation is shown in Fig.…”

Section: Computer Simulation Of Oscillationsmentioning

confidence: 99%

Tubulin oligomers and microtubule oscillations

Lange

Mandelkow

Jagla

et al. 1988

European Journal of Biochemistry

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Several types of non-equilibrium phenomena have been observed in microtubule polymerization, including dynamic instability, assembly overshoot and oscillations. They can be interpreted in terms of interactions between tubulin subunits ( = a, j heterodimers), microtubules, and a third state, oligomers, which represent intermediates between microtubule disassembly and the regeneration of assembly-competent subunits by GTP. Here we examine the role of oligomers by varying conditions that stabilize or destabilize microtubules and/or oligomers. By varying their ratio one can drive tubulin assembly either into steady-state microtubules or oligomers. These regimes of assembly conditions are separated by a region where microtubules oscillate. The oscillations can be simulated by computer modelling, based on a reaction scheme involving the three states of tubulin and nucleotide exchange on tubulin subunits, but not on microtubules or oligomers.The assembly of microtubules or other biopolymers is commonly thought to involve two interacting species, the polymer and the monomer. This suffices to explain the pseudo-first-order assembly kinetics that is frequently observed (reviewed in [l]). In the case of microtubules a third assembly state can be found, the oligomer. Its role in microtubule assembly has remained elusive. Initial electron microscope evidence suggested a role as nucleating centers (reviewed in [2]). Later X-ray studies called this view into question [3], leaving open the possibility that oligomers contributed to microtubule elongation [4]. The observation by cryo-electron microscopy of oligomers as primary breakdown products [5] suggested yet another function, namely that of a temporary storage form of nonpolymeric tubulin generated by disassembling microtubules. Whatever the role, it was clear that it must somehow be related to the assembly competence of tubulin which is activated by GTP but inactivated by GDP produced during microtubule assembly. Only the tubulin subunits are capable of quickly exchanging bound GDP by GTP [6], thus rendering them active, whereas GDP bound to microtubules is non-exchangeable.When studying microtubule assembly using synchroton X-ray scattering, we made two observations bearing on the role of oligomers. One was that the assembly of oligomers and microtubules had different physico-chemical properties but both aggregates drew on the pool of tubulin subunits [7, 81. The second was that in certain conditions the assembly kinetics deviated from the simple exponential approach to equilibrium. This could take the form of a short-lived assembly overshoot and decay, or of assembly overshoot, decay In a previous report [I 01 we have studied the dependence of microtubule oscillations in solution on various nucleotides and MAPs and we have proposed a reaction model which includes the disassembly of microtubules into oligomers that act as transient storage aggregates of nonpolymerizable tubulin. In the present study, we describe the structural transitions as seen by X-ray scattering and re...

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“…Oscillations during microtubule polymerization have been observed either when GTP is regenerated enzymatically from endogenous GDP (guanosine diphosphate) [5,7,9,11] or when some amount of GTP is provided at the beginning or during an experiment. In the latter case oscillations occur only as a transient, because GTP is either consumed or some reactions steps may be inhibited due to the accumulation of GDP [8].…”

Section: Introductionmentioning

confidence: 99%

Modeling oscillatory microtubule polymerization

Hammele

Zimmermann

2003

Phys. Rev. E

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Polymerization of microtubules is ubiquitous in biological cells and under certain conditions it becomes oscillatory in time. Here simple reaction models are analyzed that capture such oscillations as well as the length distribution of microtubules. We assume reaction conditions that are stationary over many oscillation periods, and it is a Hopf bifurcation that leads to a persistent oscillatory microtubule polymerization in these models. Analytical expressions are derived for the threshold of the bifurcation and the oscillation frequency in terms of reaction rates as well as typical trends of their parameter dependence are presented. Both, a catastrophe rate that depends on the density of guanosine triphosphate (GTP) liganded tubulin dimers and a delay reaction, such as the depolymerization of shrinking microtubules or the decay of oligomers, support oscillations. For a tubulin dimer concentration below the threshold oscillatory microtubule polymerization occurs transiently on the route to a stationary state, as shown by numerical solutions of the model equations. Close to threshold a so-called amplitude equation is derived and it is shown that the bifurcation to microtubule oscillations is supercritical.

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An oscillatory mode for microtubule assembly.

Cited by 71 publications

References 17 publications

Oscillations in microtubule polymerization: the rate of GTP regeneration on tubulin controls the period.

Oscillations in microtubule polymerization: the rate of GTP regeneration on tubulin controls the period.

Tubulin oligomers and microtubule oscillations

Modeling oscillatory microtubule polymerization

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