Gravitational Symmetry Breaking Leads to a Polar Liquid Crystal Phase of Microtubules In Vitro (original) (raw)

Models of spatial and orientational self-organization of microtubules under the influence of gravitational fields

Physical review. E, Statistical, nonlinear, and soft matter physics, 2003

Tabony and co-workers [C. Papaseit, N. Pochon, and J. Tabony, Proc. Natl. Acad. Sci. U.S.A. 97, 8364 (2000)] showed that the self-organization of microtubules from purified tubulin solutions is sensitive to gravitational conditions. In this paper, we propose two models of spatial and orientational self-organization of microtubules in a gravitational field. First, the spatial model is based on the dominant chemical kinetics. The pattern formation of microtubule concentration is obtained (1) in terms of a moving kink in the limit when the disassembly rate is negligible, and (2) for the case of no free tubulin and only assembled microtubules present. Second, the orientational pattern of striped microtubule domains is consistent with predictions from a phenomenological Landau-Ginzburg free energy expansion in terms of an orientational order parameter.

Biological Self-Organization by Way of Microtubule Reaction−Diffusion Processes †

Langmuir, 2002

This article addresses the physical chemical processes underlying biological self-organization by which a homogeneous solution of reacting chemicals spontaneously self-organizes. Theoreticians have predicted that self-organization can arise from a coupling of reactive processes with molecular diffusion. In addition, the presence of an external field such as gravity, at a critical moment early in the process may determine the morphology that subsequently develops. The formation, in vitro, of microtubules, a constituent of the cellular skeleton, shows this type of behavior. Preparations spontaneously self-organize by reactiondiffusion, and the morphology that develops depends on the presence of gravity at a critical bifurcation time early in the process. Numerical simulations of a population of microtubules involving only reactive and diffusive terms reproduce this behavior. Microtubules can grow from one end while shrinking from the other. The shrinking end leaves behind itself a chemical trail of high tubulin concentration. Neighboring microtubules preferentially grow into these regions, while avoiding regions of low concentration. The chemical trails produced by individual microtubules thus activate and inhibit the formation of their neighbors, and this progressively leads to self-organization. Gravity acts by way of its directional interaction with the macroscopic density fluctuations present in the solution arising from microtubule disassembly. Evidence is presented that similar processes might occur both during the cell cycle and the early stages of Drosophila fruit fly embryogenesis. † This article is part of the special issue of Langmuir devoted to the emerging field of self-assembled fibrillar networks.

Effect of weightlessness on colloidal particle transport and segregation in self-organising microtubule preparations

Biophysical Chemistry, 2007

Weightlessness is known to effect cellular functions by as yet undetermined processes. Many experiments indicate a role of the cytoskeleton and microtubules. Under appropriate conditions in vitro microtubule preparations behave as a complex system that self-organises by a combination of reaction and diffusion. This process also results in the collective transport and organisation of any colloidal particles present. In large centimetre-sized samples, selforganisation does not occur when samples are exposed to a brief early period of weightlessness. Here, we report both space-flight and ground-based (clinorotation) experiments on the effect of w eightlessness on the transport and segregation of colloidal particles and chromosomes. In centimetre-sized containers, both methods show that a brief initial period of weightlessness strongly inhibits particle transport. In miniature cell-sized containers under normal gravity conditions, the particle transport that self-organisation causes results in their accumulation into segregated regions of high and low particle density. The gravity dependence of this behaviour is strongly shape dependent. In square wells, neither self-organisation nor particle transport and segregation occur under conditions of weightlessness. On the contrary, in rectangular canals, both phenomena are largely unaffected by weightlessness. These observations suggest, depending on factors such as cell and embryo shape, that major biological functions associated with microtubule driven particle transport and organisation might be strongly perturbed by weightlessness.

Microtubule self-organisation by reaction–diffusion processes in miniature cell-sized containers and phospholipid vesicles

Biophysical Chemistry, 2006

Under appropriate conditions, in vitro microtubule preparations self-organise over macroscopic distances by a process of reaction and diffusion. To investigate whether such self-organisation can also occur in objects as small as a cell or an embryo we carried out experiments in miniature containers of cellular dimension. When assembled under self-organising conditions in wells of 120 -500 Am, microtubules developed organised structures. Self-organisation is strongly affected by shape, being highly favoured by elongated forms. In wells of more complex shape, geometrical factors may either oppose or strengthen one another and so inhibit or reinforce self-organisation. Microtubules were also assembled within phospholipid vesicles of 2 -5 Am diameter. Under self-organising conditions, we observed large shape changes from spheroids to long tubes (50 -100 Am) and intertwined coils. We conclude that self-organisation of microtubules by reaction -diffusion processes can occur in containers of cellular dimensions and is capable of strongly deforming the cellular membrane. D

Numerical simulations of microtubule self-organisation by reaction and diffusion

Acta biotheoretica, 2002

This article addresses the physical chemical processes underlying biological self-organisation by which a homogenous solution of reacting chemicals spontaneously self-organises. Theoreticians have predicted that self-organisation can arise from a coupling of reactive processes with molecular diffusion. In addition, the presence of an external field, such as gravity, at a critical moment early in the process may determine the morphology that subsequently develops. The formation, in-vitro, of microtubules, a constituent of the cellular skeleton, shows this type of behaviour. The preparations spontaneously self-organise by reaction-diffusion and the morphology that develops depends upon the presence of gravity at a critical bifurcation time early in the process. Here, we present numerical simulations of a population of microtubules that reproduce this behaviour. Microtubules can grow from one end whilst shrinking from the other. The shrinking end leaves behind a chemical trail of high ...

Selected Physical Issues in the Structure and Function of Microtubules

Journal of Structural Biology, 1997

The cytoskeleton consists of networks of protein polymers which structurally and dynamically organize interiors of living cells. Microtubules exhibit a complex array of self-organization phenomena which are very sensitive to various laboratory conditions. In this paper we discuss the main features of microtubules focusing our attention on a selection of their physical properties, i.e., the questions of assembly dynamics and energy transfer along their protofilaments, the possible dipolar phases which we predict to exist, and, finally, the hypothesis of current flows associated with the electric field lines produced by cytoskeletal components.

Structure of growing microtubule ends: two-dimensional sheets close into tubes at variable rates

The Journal of cell biology, 1995

Observation of microtubule growth at different rates by cryo-electron microscopy reveals that the ends range from blunt to long, gently curved sheets. The mean sheet length increases with the growth rate while the width of the distributions increases with the extent of assembly. The combination of a concentration dependent growth rate of the tubulin sheet with a variable closure rate of the microtubule cylinder, results in a model in which stochastic fluctuations in sheet length and tubulin conformation confine GTP-tubulins to microtubule ends. We propose that the variability of microtubule growth rate observed by video microscopy (Gildersleeve, R. F., A. R. Cross, K. E. Cullen, A. P. Fagen, and R. C. Williams. 1992. J. Biol. Chem. 267: 7995-8006, and this study) is due to the variation in the rate of cylinder closure. The curvature of the sheets at the end of growing microtubules and the small oligomeric structures observed at the end of disassembling microtubules, indicate that tu...

Microtubules: dissipative structures formed by self-assembly

Biosensors and Bioelectronics, 1994

Microtubules are hollow fibres that form the track upon which chromosomes or proteins, such as kinesins, are transported in the cell. They are formed by the self-assembly of the protein tubulin both in vitro and in vivo. In the cell, their appearance in time and space is strictly controlled by the presence of nucleation centres. Microtubules are very dynamic structures, a property that is obtained by coupling the self-assembly process to the hydrolysis of the nucleotide, guanosine 5'-triphosphate, (GTP). After assembly, GTP is hydrolysed and guanosine 5'-diphosphate, (GDP)-microtubule structure is formed which, although intrinsically very unstable, is stabilised by a small remaining tubulin-GTP-cap at both ends. As such, the ends of microtubules can be considered as gates for entry into the polymeric state. These gates can be blocked by sub-stoichiometric amounts of drugs such as colchicine. As biological devices, microtubules differ considerably from man-made devices: they are dynamic dissipative structures, made by spontaneous selfassembly. It has been suggested that microtubules could play a role in the conduction and dynamic storage of information. This implies the existence of different conformational states of tubulin.