Behaviors of individual microtubules and microtubule populations relative to critical concentrations: dynamic instability occurs when critical concentrations are driven apart by nucleotide hydrolysis

Jonasson, Erin M.; Mauro, Ava J.; Li, Chunlei; Labuz, Ellen C.; Mahserejian, Shant; Scripture, Jared P.; Gregoretti, Ivan V.; Alber, Mark; Goodson, Holly V.

doi:10.1091/mbc.e19-02-0101

Cited by 17 publications

(37 citation statements)

References 70 publications

(219 reference statements)

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“…Then, as seen from the J General equation (Equation 1), V g and J are different from each other (Figure 3). CC Elongation and CC NetAssembly are therefore distinguishable from each other (Jonasson et al, 2019); this is the case depicted in the schematics in Figures 2 to 4, and that will be examined in this paper.…”

Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 92%

“…The relationship between J and V g in the J equation can be useful in understanding two critical concentrations (CC NetAssembly and CC Elongation in Figure 4) that are relevant to the behaviors of DI polymers (e.g., (Jonasson et al, 2019)).…”

Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 99%

“…CC Elongation is the [free tubulin] above which the individual growth velocity is positive (V g > 0), as determined by extrapolation to V g = 0 from a plot of V g versus [free tubulin]. At [free tubulin] above CC Elongation , individual MTs can exhibit the transient growth phases that are part of dynamic instability, though for [free tubulin] near CC Elongation , few MTs will exceed experimentally relevant detection thresholds (i.e., most seeds will appear to be unoccupied at any given time) (Jonasson et al, 2019). CC Elongation was called c 1 in (Hill & Chen, 1984) and "the critical concentration for elongation (S c e )" in (Walker et al, 1988).…”

Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 99%

“…Even if there is no threshold on the displacement per time step, the size of the time step will still affect the measured values of V g and V s because it will affect how the length changes are categorized into growth or shortening (Figure 9; see also Supplemental Information of (Jonasson et al, 2019)). For example, if the time step is small (e.g., t i < ~1 s), V g may be overestimated due to brief rapid upward fluctuations, and the magnitude of V s may be underestimated due to brief shallow negative displacements that are within longer segments of overall growth.…”

Section: Effect Of Time-step Size On V G and V S As Measured In The Tmentioning

confidence: 99%

“…If measurements are performed after J has reached its steady-state value in dilution experiments and in constant [free tubulin] experiments, then J from the two types of experiments will be superimposed for [free tubulin] > CC NetAssembly (Jonasson et al, 2019). This is relevant, for example, in recognizing the relationship between critical concentrations as measured in dilution experiments or in constant [free tubulin] experiments ( Figure 4A-B).…”

Section: Timing Of Measurements In Constant [Free Tubulin] Systemsmentioning

confidence: 99%

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Relationship between dynamic instability of individual microtubules and flux of subunits into and out of polymer

2019

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Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 92%

Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 99%

Section: Role Of Flux and Dynamic Instability In Defining Critical Comentioning

confidence: 99%

Section: Effect Of Time-step Size On V G and V S As Measured In The Tmentioning

confidence: 99%

Section: Timing Of Measurements In Constant [Free Tubulin] Systemsmentioning

confidence: 99%

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Relationship between dynamic instability of individual microtubules and flux of subunits into and out of polymer

2019

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The gamma‐tubulin ring complex: Deciphering the molecular organization and assembly mechanism of a major vertebrate microtubule nucleator

et al. 2021

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Microtubules are protein cylinders with functions in cell motility, signal sensing, cell organization, intracellular transport, and chromosome segregation. One of the key properties of microtubules is their dynamic architecture, allowing them to grow and shrink in length by adding or removing copies of their basic subunit, the heterodimer αβ-tubulin. In higher eukaryotes, de novo assembly of microtubules from αβ-tubulin is initiated by a 2 MDa multi-subunit complex, the gamma-tubulin ring complex (γ-TuRC). For many years, the structure of the γ-TuRC and the function of its subunits remained enigmatic, although structural data from the much simpler yeast counterpart, the γ-tubulin small complex (γ-TuSC), were available. Two recent breakthroughs in the field, high-resolution structural analysis and recombinant reconstitution of the complex, have revolutionized our knowledge about the architecture and function of the γ-TuRC and will form the basis for addressing outstanding questions about biogenesis and regulation of this essential microtubule organizer. K E Y W O R D Sgamma-tubulin ring complex, gamma-tubulin small complex, gamma-tubulin, microtubule nucleation, microtubules, recombinant gamma-tubulin ring complex Abbreviations: AAA+, adenosine triphosphatases associated with various cellular activities;Arps, actin-related proteins; CDK5RAP2, CDK5 regulatory subunit-associated protein 2; CEP192, centrosomal protein of 192 kDa; ch-TOG, colonic hepatic tumor-overexpressed gene; CM1, centrosomin motif 1; GCP, γ-TuC component protein; γ-TuCs, γ-tubulin complexes; γ-TuRC, γ-tubulin ring complex; γ-TuSC, γ-tubulin small complex; GRIP1/2, γ-tubulin ring protein 1/2; HSP90, heat shock protein 90; INO80, inositol-requiring mutant 80 complex; MZT1/2, mitotic spindle organizing protein 1/2; NEDD1, neural precursor cell expressed, developmentally down-regulated 1; NME7, nucleotide diphosphate kinase 7; PCM, pericentriolar material; PIH1D1, PIH1 domain containing 1; R2TP, Rvb1-Rvb2-Tah1-Pih1; RPAP3, RNA polymerase II associated protein 3; RUVBL1/2, RuvB-like 1/2; SPB, spindle pole body; SWR1, SWI2/SNF2-related 1 complex; XMAP215, Xenopus microtubule assembly protein with 215 kDThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Polymerization kinetics of tubulin from mung seedlings modeled as a competition between nucleation and GTP‐hydrolysis rates

et al. 2021

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Microtubules (MTs) form physiologically important cytoskeletal structures that are assembled by tubulin polymerization in nucleation‐ and guanosine triphosphate (GTP)‐dependent manner. GTP hydrolysis competes with the addition of monomers, to determine the GTP‐cap size, and the onset of shrinkage, which alternates with growth. Multiple theoretical models of MT polymerization dynamics have been reconciled to the kinetics of animal brain tubulins, but more recently, rapid kinetics seen in Arabidopsis tubulin polymerization suggest the need to sample a wider diversity in tubulin polymerization kinetics and reconcile it to theory. Here, we isolated tubulin from seedlings of Vigna sp. (mung bean), compared polymerization kinetics to animal brain tubulin, and used a computational model to understand the differences. We find that activity‐isolated mung tubulin polymerizes in a nucleation‐dependent manner, based on turbidimetry, qualitatively similar to brain tubulin, but with a 10‐fold smaller critical concentration. GTP‐dependent polymerization kinetics also appear to be transient, indicative of high rates of GTP hydrolysis. Computational modeling of tubulin nucleation and vectorial GTP hydrolysis to examine the effects of high nucleation and GTP‐hydrolysis rates predicts a dominance of the latter in determining MT lengths and numbers. Microscopy of mung tubulin filaments stabilized by GMPCPP or taxol results in few and short MTs, compared to the many long MTs arising from goat tubulin, qualitatively matching the model predictions. We find GTP‐hydrolysis outcompetes nucleation rates in determining MT lengths and numbers.

show abstract

Behaviors of individual microtubules and microtubule populations relative to critical concentrations: dynamic instability occurs when critical concentrations are driven apart by nucleotide hydrolysis

Cited by 17 publications

References 70 publications

Relationship between dynamic instability of individual microtubules and flux of subunits into and out of polymer

Relationship between dynamic instability of individual microtubules and flux of subunits into and out of polymer

The gamma‐tubulin ring complex: Deciphering the molecular organization and assembly mechanism of a major vertebrate microtubule nucleator

Polymerization kinetics of tubulin from mung seedlings modeled as a competition between nucleation and GTP‐hydrolysis rates

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