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Paired arrangement of kinetochores together with microtubule pivoting and dynamics drive kinetochore capture in meiosis I.

Cojoc G, Florescu AM, Krull A, Klemm AH, Pavin N, Jülicher F, Tolić IM - Sci Rep (2016)

Bottom Line: Our theory describes paired kinetochores on homologous chromosomes as a single object, as well as angular movement of microtubules and their dynamics.For the experimentally measured parameters, the model reproduces the measured capture kinetics and shows that the paired configuration of kinetochores accelerates capture, whereas microtubule pivoting and dynamics have a smaller contribution.Kinetochore pairing may be a general feature that increases capture efficiency in meiotic cells.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstr. 108, 01307 Dresden, Germany.

ABSTRACT
Kinetochores are protein complexes on the chromosomes, whose function as linkers between spindle microtubules and chromosomes is crucial for proper cell division. The mechanisms that facilitate kinetochore capture by microtubules are still unclear. In the present study, we combine experiments and theory to explore the mechanisms of kinetochore capture at the onset of meiosis I in fission yeast. We show that kinetochores on homologous chromosomes move together, microtubules are dynamic and pivot around the spindle pole, and the average capture time is 3-4 minutes. Our theory describes paired kinetochores on homologous chromosomes as a single object, as well as angular movement of microtubules and their dynamics. For the experimentally measured parameters, the model reproduces the measured capture kinetics and shows that the paired configuration of kinetochores accelerates capture, whereas microtubule pivoting and dynamics have a smaller contribution. Kinetochore pairing may be a general feature that increases capture efficiency in meiotic cells.

No MeSH data available.


Related in: MedlinePlus

Description of the model for simulating KC capture.(A) Geometry of the model. A MT is described as a stiff rod, which is freely jointed to the SPB and exhibits dynamic instability. A KC pair is described as a single sphere with a radius which is twice as large as that of a single KC. (B) Model equations: The first column shows the equations of motion for the KCs and the MTs, the length dependence of the MT diffusion coefficient and the equations for MT growth, shrinkage and catastrophe rate. The second column shows the boundary conditions for MTs and KCs and the condition defining a KC capture event. (C) Table of model parameters. The values of DKC , vg, vs, and the initial value of rKC were measured in this work. The value for C was obtained by fitting the measured values of the MT angular diffusion coefficient as a function of length to the expression of the angular diffusion coefficient of a rigid rod. The parameter α was computed by fitting the measured length dependence of the MT catastrophe rate with a straight line passing through the origin. The value for a was obtained by doubling the value for a single KC that is given in26 and the value for R is taken from33.
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f3: Description of the model for simulating KC capture.(A) Geometry of the model. A MT is described as a stiff rod, which is freely jointed to the SPB and exhibits dynamic instability. A KC pair is described as a single sphere with a radius which is twice as large as that of a single KC. (B) Model equations: The first column shows the equations of motion for the KCs and the MTs, the length dependence of the MT diffusion coefficient and the equations for MT growth, shrinkage and catastrophe rate. The second column shows the boundary conditions for MTs and KCs and the condition defining a KC capture event. (C) Table of model parameters. The values of DKC , vg, vs, and the initial value of rKC were measured in this work. The value for C was obtained by fitting the measured values of the MT angular diffusion coefficient as a function of length to the expression of the angular diffusion coefficient of a rigid rod. The parameter α was computed by fitting the measured length dependence of the MT catastrophe rate with a straight line passing through the origin. The value for a was obtained by doubling the value for a single KC that is given in26 and the value for R is taken from33.

Mentions: To understand the mechanisms that lead to the observed KC capture times we developed a stochastic model that takes into account MT pivoting around the SPB (as was described in our previous work9, MT dynamics and paired movement of the KCs. The nucleus is described as a sphere of radius 1.5 μm corresponding to the nuclear membrane9. We consider that the two SPBs are located together at one pole of the sphere and acting as a single MT nucleation source. This choice is based on our observation that two SPBs are close to each other during most of the capturing process. MTs are described as thin, rigid rods that can grow, shrink and perform angular diffusion while fixed with one end at the SPB (Fig. 3A). They can switch from growth to shrinkage (catastrophe) with a probability per unit time that increases linearly with MT length, as shown by our experiments (Fig. 2B) and as was observed previously in1722. The model does not include the possibility of switching from shrinkage to growth (rescue), since we did not observe this in our experiments. The simulations were performed using a constant number of MTs, so if one MT shrinks until its length equals zero it immediately starts growing again, with a new random orientation. A pair of KCs was described as a single rigid sphere that has a radius twice as large as that of a single KC. To check that this description can be used for studying capture we plotted the experimental fraction of free KC pairs as a function of time and observed that it obeys a kinetics that is very similar to that of the capture of single KCs.


Paired arrangement of kinetochores together with microtubule pivoting and dynamics drive kinetochore capture in meiosis I.

Cojoc G, Florescu AM, Krull A, Klemm AH, Pavin N, Jülicher F, Tolić IM - Sci Rep (2016)

Description of the model for simulating KC capture.(A) Geometry of the model. A MT is described as a stiff rod, which is freely jointed to the SPB and exhibits dynamic instability. A KC pair is described as a single sphere with a radius which is twice as large as that of a single KC. (B) Model equations: The first column shows the equations of motion for the KCs and the MTs, the length dependence of the MT diffusion coefficient and the equations for MT growth, shrinkage and catastrophe rate. The second column shows the boundary conditions for MTs and KCs and the condition defining a KC capture event. (C) Table of model parameters. The values of DKC , vg, vs, and the initial value of rKC were measured in this work. The value for C was obtained by fitting the measured values of the MT angular diffusion coefficient as a function of length to the expression of the angular diffusion coefficient of a rigid rod. The parameter α was computed by fitting the measured length dependence of the MT catastrophe rate with a straight line passing through the origin. The value for a was obtained by doubling the value for a single KC that is given in26 and the value for R is taken from33.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4863148&req=5

f3: Description of the model for simulating KC capture.(A) Geometry of the model. A MT is described as a stiff rod, which is freely jointed to the SPB and exhibits dynamic instability. A KC pair is described as a single sphere with a radius which is twice as large as that of a single KC. (B) Model equations: The first column shows the equations of motion for the KCs and the MTs, the length dependence of the MT diffusion coefficient and the equations for MT growth, shrinkage and catastrophe rate. The second column shows the boundary conditions for MTs and KCs and the condition defining a KC capture event. (C) Table of model parameters. The values of DKC , vg, vs, and the initial value of rKC were measured in this work. The value for C was obtained by fitting the measured values of the MT angular diffusion coefficient as a function of length to the expression of the angular diffusion coefficient of a rigid rod. The parameter α was computed by fitting the measured length dependence of the MT catastrophe rate with a straight line passing through the origin. The value for a was obtained by doubling the value for a single KC that is given in26 and the value for R is taken from33.
Mentions: To understand the mechanisms that lead to the observed KC capture times we developed a stochastic model that takes into account MT pivoting around the SPB (as was described in our previous work9, MT dynamics and paired movement of the KCs. The nucleus is described as a sphere of radius 1.5 μm corresponding to the nuclear membrane9. We consider that the two SPBs are located together at one pole of the sphere and acting as a single MT nucleation source. This choice is based on our observation that two SPBs are close to each other during most of the capturing process. MTs are described as thin, rigid rods that can grow, shrink and perform angular diffusion while fixed with one end at the SPB (Fig. 3A). They can switch from growth to shrinkage (catastrophe) with a probability per unit time that increases linearly with MT length, as shown by our experiments (Fig. 2B) and as was observed previously in1722. The model does not include the possibility of switching from shrinkage to growth (rescue), since we did not observe this in our experiments. The simulations were performed using a constant number of MTs, so if one MT shrinks until its length equals zero it immediately starts growing again, with a new random orientation. A pair of KCs was described as a single rigid sphere that has a radius twice as large as that of a single KC. To check that this description can be used for studying capture we plotted the experimental fraction of free KC pairs as a function of time and observed that it obeys a kinetics that is very similar to that of the capture of single KCs.

Bottom Line: Our theory describes paired kinetochores on homologous chromosomes as a single object, as well as angular movement of microtubules and their dynamics.For the experimentally measured parameters, the model reproduces the measured capture kinetics and shows that the paired configuration of kinetochores accelerates capture, whereas microtubule pivoting and dynamics have a smaller contribution.Kinetochore pairing may be a general feature that increases capture efficiency in meiotic cells.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Molecular Cell Biology and Genetics, Pfotenhauerstr. 108, 01307 Dresden, Germany.

ABSTRACT
Kinetochores are protein complexes on the chromosomes, whose function as linkers between spindle microtubules and chromosomes is crucial for proper cell division. The mechanisms that facilitate kinetochore capture by microtubules are still unclear. In the present study, we combine experiments and theory to explore the mechanisms of kinetochore capture at the onset of meiosis I in fission yeast. We show that kinetochores on homologous chromosomes move together, microtubules are dynamic and pivot around the spindle pole, and the average capture time is 3-4 minutes. Our theory describes paired kinetochores on homologous chromosomes as a single object, as well as angular movement of microtubules and their dynamics. For the experimentally measured parameters, the model reproduces the measured capture kinetics and shows that the paired configuration of kinetochores accelerates capture, whereas microtubule pivoting and dynamics have a smaller contribution. Kinetochore pairing may be a general feature that increases capture efficiency in meiotic cells.

No MeSH data available.


Related in: MedlinePlus