Literature DB >> 18577596

Force-generation and dynamic instability of microtubule bundles.

Liedewij Laan1, Julien Husson, E Laura Munteanu, Jacob W J Kerssemakers, Marileen Dogterom.   

Abstract

Individual dynamic microtubules can generate pushing or pulling forces when their growing or shrinking ends are in contact with cellular objects such as the cortex or chromosomes. These microtubules can operate in parallel bundles, for example when interacting with mitotic chromosomes. Here, we investigate the force-generating capabilities of a bundle of growing microtubules and study the effect that force has on the cooperative dynamics of such a bundle. We used an optical tweezers setup to study microtubule bundles growing against a microfabricated rigid barrier in vitro. We show that multiple microtubules can generate a pushing force that increases linearly with the number of microtubules present. In addition, the bundle can cooperatively switch to a shrinking state, due to a force-induced coupling of the dynamic instability of single microtubules. In the presence of GMPCPP, bundle catastrophes no longer occur, and high bundle forces are reached more effectively. We reproduce the observed behavior with a simple simulation of microtubule bundle dynamics that takes into account previously measured force effects on single microtubules. Using this simulation, we also show that a constant compressive force on a growing bundle leads to oscillations in bundle length that are of potential relevance for chromosome oscillations observed in living cells.

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Year:  2008        PMID: 18577596      PMCID: PMC2449340          DOI: 10.1073/pnas.0710311105

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


  34 in total

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Journal:  Eur Biophys J       Date:  2000       Impact factor: 1.733

2.  A simple, mechanistic model for directional instability during mitotic chromosome movements.

Authors:  Ajit P Joglekar; Alan J Hunt
Journal:  Biophys J       Date:  2002-07       Impact factor: 4.033

Review 3.  Chromosome-microtubule interactions during mitosis.

Authors:  J Richard McIntosh; Ekaterina L Grishchuk; Robert R West
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4.  Scaling of microtubule force-velocity curves obtained at different tubulin concentrations.

Authors:  Marcel E Janson; Marileen Dogterom
Journal:  Phys Rev Lett       Date:  2004-06-16       Impact factor: 9.161

5.  A mechanobiochemical mechanism for monooriented chromosome oscillation in mitosis.

Authors:  Jian Liu; Arshad Desai; José N Onuchic; Terence Hwa
Journal:  Proc Natl Acad Sci U S A       Date:  2007-10-02       Impact factor: 11.205

6.  A latent adenosine triphosphatase form of dynein 1 from sea urchin sperm flagella.

Authors:  I R Gibbons; E Fronk
Journal:  J Biol Chem       Date:  1979-01-10       Impact factor: 5.157

7.  Dynamic instability of microtubule growth.

Authors:  T Mitchison; M Kirschner
Journal:  Nature       Date:  1984 Nov 15-21       Impact factor: 49.962

Review 8.  Searching for the middle ground: mechanisms of chromosome alignment during mitosis.

Authors:  Tarun M Kapoor; Duane A Compton
Journal:  J Cell Biol       Date:  2002-05-13       Impact factor: 10.539

9.  The chromokinesin Kid is necessary for chromosome arm orientation and oscillation, but not congression, on mitotic spindles.

Authors:  A A Levesque; D A Compton
Journal:  J Cell Biol       Date:  2001-09-17       Impact factor: 10.539

10.  Dynamic instability of microtubules is regulated by force.

Authors:  Marcel E Janson; Mathilde E de Dood; Marileen Dogterom
Journal:  J Cell Biol       Date:  2003-06-23       Impact factor: 10.539

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  34 in total

1.  Minimal model for collective kinetochore-microtubule dynamics.

Authors:  Edward J Banigan; Kevin K Chiou; Edward R Ballister; Alyssa M Mayo; Michael A Lampson; Andrea J Liu
Journal:  Proc Natl Acad Sci U S A       Date:  2015-09-28       Impact factor: 11.205

2.  Buckling behavior of individual and bundled microtubules.

Authors:  Mohammad Soheilypour; Mohaddeseh Peyro; Stephen J Peter; Mohammad R K Mofrad
Journal:  Biophys J       Date:  2015-04-07       Impact factor: 4.033

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5.  Rapid assembly and collective behavior of microtubule bundles in the presence of polyamines.

Authors:  Loïc Hamon; Philippe Savarin; Patrick A Curmi; David Pastré
Journal:  Biophys J       Date:  2011-07-06       Impact factor: 4.033

Review 6.  Force probing of individual molecules inside the living cell is now a reality.

Authors:  Lene B Oddershede
Journal:  Nat Chem Biol       Date:  2012-11       Impact factor: 15.040

7.  Reconstitution of Basic Mitotic Spindles in Spherical Emulsion Droplets.

Authors:  Mathijs Vleugel; Sophie Roth; Celebrity F Groenendijk; Marileen Dogterom
Journal:  J Vis Exp       Date:  2016-08-13       Impact factor: 1.355

Review 8.  The molecular mechanisms underlying lens fiber elongation.

Authors:  Dylan S Audette; David A Scheiblin; Melinda K Duncan
Journal:  Exp Eye Res       Date:  2016-03-23       Impact factor: 3.467

Review 9.  Tension management in the kinetochore.

Authors:  Kerry Bloom; Elaine Yeh
Journal:  Curr Biol       Date:  2010-12-07       Impact factor: 10.834

10.  Clasp-mediated microtubule bundling regulates persistent motility and contact repulsion in Drosophila macrophages in vivo.

Authors:  Brian Stramer; Severina Moreira; Tom Millard; Iwan Evans; Chieh-Yin Huang; Ola Sabet; Martin Milner; Graham Dunn; Paul Martin; Will Wood
Journal:  J Cell Biol       Date:  2010-05-10       Impact factor: 10.539

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