Literature DB >> 16844776

Biophysical model of self-organized spindle formation patterns without centrosomes and kinetochores.

Stuart C Schaffner1, Jorge V José.   

Abstract

Eukaryotic cell division and chromosome segregation depend crucially on the mitotic spindle pattern formation. The usual pathway for spindle production involves microtubule polymerization from two centrosomes. However, experiments using Xenopus extracts with micrometer-sized chromatin-coated beads found, remarkably, that spindle patterns can form in the absence of centrosomes, kinetochores, and duplicated chromosomes. Here we introduce a previously undescribed biophysical model inspired by the heuristic interpretations of the experiments that provides a quantitative explanation and constraints for this type of experiment. The model involves plus-directed (chromokinesin and Eg5) and minus-directed (cytoplasmic dynein oligomers) motors walking on microtubules and the boundary conditions caused by the chromatin-coated spheres. This model combines the effects of the plus-directed cross-linking motor Eg5 and any chromokinesin on the chromatin-covered beads, reflecting current uncertainties in the division of function between the two kinds of motors. The model can nucleate dynamically a variety of self-organized spindle patterns over a wide range of biological parameter values. Our calculations show that spindles will form over a wide range of parameter values. Some parameter values cause a monaster to form instead of a bipolar spindle. Varying the processivity and the dynein microtubule attachment and detachment rates, we find stability parameters for spindle formations. These results not only constrain the possible parameter values, but they point toward the proper division of function between Eg5 and chromokinesin in this spindle formation pathway. The model results suggest experiments that would further enhance our understanding of the basic elements needed for spindle pattern formation in this pathway.

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Year:  2006        PMID: 16844776      PMCID: PMC1544059          DOI: 10.1073/pnas.0604721103

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  Requirement of a centrosomal activity for cell cycle progression through G1 into S phase.

Authors:  E H Hinchcliffe; F J Miller; M Cham; A Khodjakov; G Sluder
Journal:  Science       Date:  2001-02-23       Impact factor: 47.728

2.  A dynamical model of kinesin-microtubule motility assays.

Authors:  F Gibbons; J F Chauwin; M Despósito; J V José
Journal:  Biophys J       Date:  2001-06       Impact factor: 4.033

3.  Dynein structure and power stroke.

Authors:  Stan A Burgess; Matt L Walker; Hitoshi Sakakibara; Peter J Knight; Kazuhiro Oiwa
Journal:  Nature       Date:  2003-02-13       Impact factor: 49.962

4.  Cell division: burning the spindle at both ends.

Authors:  Rebecca W Heald
Journal:  Nature       Date:  2004-01-22       Impact factor: 49.962

5.  Nanometres and piconewtons: the macromolecular mechanics of kinesin.

Authors:  S M Block
Journal:  Trends Cell Biol       Date:  1995-04       Impact factor: 20.808

Review 6.  Self-organisation and forces in the microtubule cytoskeleton.

Authors:  François Nédélec; Thomas Surrey; Eric Karsenti
Journal:  Curr Opin Cell Biol       Date:  2003-02       Impact factor: 8.382

7.  Cytoplasmic dynein functions as a gear in response to load.

Authors:  Roop Mallik; Brian C Carter; Stephanie A Lex; Stephen J King; Steven P Gross
Journal:  Nature       Date:  2004-02-12       Impact factor: 49.962

8.  Assembly pathway of the anastral Drosophila oocyte meiosis I spindle.

Authors:  Helén Nilsson Sköld; Donald J Komma; Sharyn A Endow
Journal:  J Cell Sci       Date:  2005-03-29       Impact factor: 5.285

9.  Eg5 is static in bipolar spindles relative to tubulin: evidence for a static spindle matrix.

Authors:  T M Kapoor; T J Mitchison
Journal:  J Cell Biol       Date:  2001-09-17       Impact factor: 10.539

10.  Spindle assembly in Xenopus egg extracts: respective roles of centrosomes and microtubule self-organization.

Authors:  R Heald; R Tournebize; A Habermann; E Karsenti; A Hyman
Journal:  J Cell Biol       Date:  1997-08-11       Impact factor: 10.539

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  11 in total

Review 1.  Biophysics of mitosis.

Authors:  J Richard McIntosh; Maxim I Molodtsov; Fazly I Ataullakhanov
Journal:  Q Rev Biophys       Date:  2012-02-10       Impact factor: 5.318

2.  Mitotic membrane helps to focus and stabilize the mitotic spindle.

Authors:  Christopher C Poirier; Yixian Zheng; Pablo A Iglesias
Journal:  Biophys J       Date:  2010-11-17       Impact factor: 4.033

3.  Spatial regulation improves antiparallel microtubule overlap during mitotic spindle assembly.

Authors:  Wilbur E Channels; François J Nédélec; Yixian Zheng; Pablo A Iglesias
Journal:  Biophys J       Date:  2007-12-20       Impact factor: 4.033

4.  Anastral spindle assembly: a mathematical model.

Authors:  Mark A Hallen; Sharyn A Endow
Journal:  Biophys J       Date:  2009-10-21       Impact factor: 4.033

5.  50 ways to build a spindle: the complexity of microtubule generation during mitosis.

Authors:  Tommy Duncan; James G Wakefield
Journal:  Chromosome Res       Date:  2011-04       Impact factor: 5.239

6.  Proteomic Profiling of Microtubule Self-organization in M-phase.

Authors:  Miquel Rosas-Salvans; Tommaso Cavazza; Guadalupe Espadas; Eduard Sabido; Isabelle Vernos
Journal:  Mol Cell Proteomics       Date:  2018-07-03       Impact factor: 5.911

7.  The emergence of sarcomeric, graded-polarity and spindle-like patterns in bundles of short cytoskeletal polymers and two opposite molecular motors.

Authors:  E M Craig; S Dey; A Mogilner
Journal:  J Phys Condens Matter       Date:  2011-08-23       Impact factor: 2.333

8.  Centriole movements in mammalian epithelial cells during cytokinesis.

Authors:  Asta Björk Jonsdottir; Roeland W Dirks; Johannes Vrolijk; Helga M Ogmundsdottir; Hans J Tanke; Jorunn E Eyfjörd; Karoly Szuhai
Journal:  BMC Cell Biol       Date:  2010-05-21       Impact factor: 4.241

9.  A theoretical model of mitotic spindle elongation under experimental constraints.

Authors:  Thomas Surrey
Journal:  Mol Syst Biol       Date:  2008-05-06       Impact factor: 11.429

Review 10.  Mechanisms by Which Kinesin-5 Motors Perform Their Multiple Intracellular Functions.

Authors:  Himanshu Pandey; Mary Popov; Alina Goldstein-Levitin; Larisa Gheber
Journal:  Int J Mol Sci       Date:  2021-06-15       Impact factor: 5.923

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