Literature DB >> 22304918

Cortical dynein controls microtubule dynamics to generate pulling forces that position microtubule asters.

Liedewij Laan1, Nenad Pavin, Julien Husson, Guillaume Romet-Lemonne, Martijn van Duijn, Magdalena Preciado López, Ronald D Vale, Frank Jülicher, Samara L Reck-Peterson, Marileen Dogterom.   

Abstract

Dynein at the cortex contributes to microtubule-based positioning processes such as spindle positioning during embryonic cell division and centrosome positioning during fibroblast migration. To investigate how cortical dynein interacts with microtubule ends to generate force and how this functional association impacts positioning, we have reconstituted the 'cortical' interaction between dynein and dynamic microtubule ends in an in vitro system using microfabricated barriers. We show that barrier-attached dynein captures microtubule ends, inhibits growth, and triggers microtubule catastrophes, thereby controlling microtubule length. The subsequent interaction with shrinking microtubule ends generates pulling forces up to several pN. By combining experiments in microchambers with a theoretical description of aster mechanics, we show that dynein-mediated pulling forces lead to the reliable centering of microtubule asters in simple confining geometries. Our results demonstrate the intrinsic ability of cortical microtubule-dynein interactions to regulate microtubule dynamics and drive positioning processes in living cells.
Copyright © 2012 Elsevier Inc. All rights reserved.

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Year:  2012        PMID: 22304918      PMCID: PMC3292199          DOI: 10.1016/j.cell.2012.01.007

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  51 in total

1.  Dynein motor regulation stabilizes interphase microtubule arrays and determines centrosome position.

Authors:  M P Koonce; J Köhler; R Neujahr; J M Schwartz; I Tikhonenko; G Gerisch
Journal:  EMBO J       Date:  1999-12-01       Impact factor: 11.598

2.  Centrosome polarization delivers secretory granules to the immunological synapse.

Authors:  Jane C Stinchcombe; Endre Majorovits; Giovanna Bossi; Stephen Fuller; Gillian M Griffiths
Journal:  Nature       Date:  2006-09-28       Impact factor: 49.962

3.  Establishing new sites of polarization by microtubules.

Authors:  Nicolas Minc; Scott V Bratman; Roshni Basu; Fred Chang
Journal:  Curr Biol       Date:  2009-01-15       Impact factor: 10.834

4.  Force production by disassembling microtubules.

Authors:  Ekaterina L Grishchuk; Maxim I Molodtsov; Fazly I Ataullakhanov; J Richard McIntosh
Journal:  Nature       Date:  2005-11-17       Impact factor: 49.962

5.  Tension directly stabilizes reconstituted kinetochore-microtubule attachments.

Authors:  Bungo Akiyoshi; Krishna K Sarangapani; Andrew F Powers; Christian R Nelson; Steve L Reichow; Hugo Arellano-Santoyo; Tamir Gonen; Jeffrey A Ranish; Charles L Asbury; Sue Biggins
Journal:  Nature       Date:  2010-11-25       Impact factor: 49.962

6.  Cortical microtubule contacts position the spindle in C. elegans embryos.

Authors:  Cleopatra Kozlowski; Martin Srayko; Francois Nedelec
Journal:  Cell       Date:  2007-05-04       Impact factor: 41.582

7.  Single-molecule analysis of dynein processivity and stepping behavior.

Authors:  Samara L Reck-Peterson; Ahmet Yildiz; Andrew P Carter; Arne Gennerich; Nan Zhang; Ronald D Vale
Journal:  Cell       Date:  2006-07-28       Impact factor: 41.582

8.  Finding the cell center by a balance of dynein and myosin pulling and microtubule pushing: a computational study.

Authors:  Jie Zhu; Anton Burakov; Vladimir Rodionov; Alex Mogilner
Journal:  Mol Biol Cell       Date:  2010-10-27       Impact factor: 4.138

9.  Direct role of dynein motor in stable kinetochore-microtubule attachment, orientation, and alignment.

Authors:  Dileep Varma; Pascale Monzo; Stephanie A Stehman; Richard B Vallee
Journal:  J Cell Biol       Date:  2008-09-22       Impact factor: 10.539

10.  Self-organization of dynein motors generates meiotic nuclear oscillations.

Authors:  Sven K Vogel; Nenad Pavin; Nicola Maghelli; Frank Jülicher; Iva M Tolić-Nørrelykke
Journal:  PLoS Biol       Date:  2009-04-21       Impact factor: 8.029

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  170 in total

Review 1.  Cell adhesion molecule control of planar spindle orientation.

Authors:  Hüseyin Tuncay; Klaus Ebnet
Journal:  Cell Mol Life Sci       Date:  2015-12-23       Impact factor: 9.261

2.  Chromosome misalignments induce spindle-positioning defects.

Authors:  Mihoko A Tame; Jonne A Raaijmakers; Pavel Afanasyev; René H Medema
Journal:  EMBO Rep       Date:  2016-02-04       Impact factor: 8.807

3.  Preparation of segmented microtubules to study motions driven by the disassembling microtubule ends.

Authors:  Vladimir A Volkov; Anatoly V Zaytsev; Ekaterina L Grishchuk
Journal:  J Vis Exp       Date:  2014-03-15       Impact factor: 1.355

Review 4.  End-on microtubule-dynein interactions and pulling-based positioning of microtubule organizing centers.

Authors:  Liedewij Laan; Sophie Roth; Marileen Dogterom
Journal:  Cell Cycle       Date:  2012-08-16       Impact factor: 4.534

Review 5.  The biology of boundary conditions: cellular reconstitution in one, two, and three dimensions.

Authors:  Michael D Vahey; Daniel A Fletcher
Journal:  Curr Opin Cell Biol       Date:  2013-11-12       Impact factor: 8.382

Review 6.  Microtubule catastrophe and rescue.

Authors:  Melissa K Gardner; Marija Zanic; Jonathon Howard
Journal:  Curr Opin Cell Biol       Date:  2012-10-22       Impact factor: 8.382

7.  Contributions of Microtubule Dynamic Instability and Rotational Diffusion to Kinetochore Capture.

Authors:  Robert Blackwell; Oliver Sweezy-Schindler; Christopher Edelmaier; Zachary R Gergely; Patrick J Flynn; Salvador Montes; Ammon Crapo; Alireza Doostan; J Richard McIntosh; Matthew A Glaser; Meredith D Betterton
Journal:  Biophys J       Date:  2016-09-28       Impact factor: 4.033

8.  CYLD regulates spindle orientation by stabilizing astral microtubules and promoting dishevelled-NuMA-dynein/dynactin complex formation.

Authors:  Yunfan Yang; Min Liu; Dengwen Li; Jie Ran; Jinmin Gao; Shaojun Suo; Shao-Cong Sun; Jun Zhou
Journal:  Proc Natl Acad Sci U S A       Date:  2014-01-27       Impact factor: 11.205

Review 9.  Microtubule-based force generation.

Authors:  Ian A Kent; Tanmay P Lele
Journal:  Wiley Interdiscip Rev Nanomed Nanobiotechnol       Date:  2016-08-25

Review 10.  Regulation of Microtubule Growth and Catastrophe: Unifying Theory and Experiment.

Authors:  Hugo Bowne-Anderson; Anneke Hibbel; Jonathon Howard
Journal:  Trends Cell Biol       Date:  2015-12       Impact factor: 20.808

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