Literature DB >> 18332438

Bidirectional membrane tube dynamics driven by nonprocessive motors.

Paige M Shaklee1, Timon Idema, Gerbrand Koster, Cornelis Storm, Thomas Schmidt, Marileen Dogterom.   

Abstract

In cells, membrane tubes are extracted by molecular motors. Although individual motors cannot provide enough force to pull a tube, clusters of such motors can. Here, we investigate, using a minimal in vitro model system, how the tube pulling process depends on fundamental properties of the motor species involved. Previously, it has been shown that processive motors can pull tubes by dynamic association at the tube tip. We demonstrate that, remarkably, nonprocessive motors can also cooperatively extract tubes. Moreover, the tubes pulled by nonprocessive motors exhibit rich dynamics as compared to those pulled by their processive counterparts. We report distinct phases of persistent growth, retraction, and an intermediate regime characterized by highly dynamic switching between the two. We interpret the different phases in the context of a single-species model. The model assumes only a simple motor clustering mechanism along the length of the entire tube and the presence of a length-dependent tube tension. The resulting dynamic distribution of motor clusters acts as both a velocity and distance regulator for the tube. We show the switching phase to be an attractor of the dynamics of this model, suggesting that the switching observed experimentally is a robust characteristic of nonprocessive motors. A similar system could regulate in vivo biological membrane networks.

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Year:  2008        PMID: 18332438      PMCID: PMC2786943          DOI: 10.1073/pnas.0709677105

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


  19 in total

1.  Probing the kinesin reaction cycle with a 2D optical force clamp.

Authors:  Steven M Block; Charles L Asbury; Joshua W Shaevitz; Matthew J Lang
Journal:  Proc Natl Acad Sci U S A       Date:  2003-02-18       Impact factor: 11.205

2.  Microscopic evidence for a minus-end-directed power stroke in the kinesin motor ncd.

Authors:  Thomas G Wendt; Niels Volkmann; Georgios Skiniotis; Kenneth N Goldie; Jens Müller; Eckhard Mandelkow; Andreas Hoenger
Journal:  EMBO J       Date:  2002-11-15       Impact factor: 11.598

3.  Working strokes by single molecules of the kinesin-related microtubule motor ncd.

Authors:  M J deCastro; R M Fondecave; L A Clarke; C F Schmidt; R J Stewart
Journal:  Nat Cell Biol       Date:  2000-10       Impact factor: 28.824

4.  Membrane tube formation from giant vesicles by dynamic association of motor proteins.

Authors:  Gerbrand Koster; Martijn VanDuijn; Bas Hofs; Marileen Dogterom
Journal:  Proc Natl Acad Sci U S A       Date:  2003-12-08       Impact factor: 11.205

5.  Formation and interaction of membrane tubes.

Authors:  Imre Derényi; Frank Jülicher; Jacques Prost
Journal:  Phys Rev Lett       Date:  2002-05-28       Impact factor: 9.161

Review 6.  Collective dynamics of interacting molecular motors.

Authors:  O Campàs; Y Kafri; K B Zeldovich; J Casademunt; J-F Joanny
Journal:  Phys Rev Lett       Date:  2006-07-19       Impact factor: 9.161

7.  The microtubule-dependent formation of a tubulovesicular network with characteristics of the ER from cultured cell extracts.

Authors:  S L Dabora; M P Sheetz
Journal:  Cell       Date:  1988-07-01       Impact factor: 41.582

8.  Movement of membrane tubules along microtubules in vitro: evidence for specialised sites of motor attachment.

Authors:  V Allan; R Vale
Journal:  J Cell Sci       Date:  1994-07       Impact factor: 5.285

9.  Formation of membrane networks in vitro by kinesin-driven microtubule movement.

Authors:  R D Vale; H Hotani
Journal:  J Cell Biol       Date:  1988-12       Impact factor: 10.539

10.  Microtubules and the endoplasmic reticulum are highly interdependent structures.

Authors:  M Terasaki; L B Chen; K Fujiwara
Journal:  J Cell Biol       Date:  1986-10       Impact factor: 10.539

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  16 in total

1.  Kinesin recycling in stationary membrane tubes.

Authors:  Paige M Shaklee; Timon Idema; Line Bourel-Bonnet; Marileen Dogterom; Thomas Schmidt
Journal:  Biophys J       Date:  2010-09-22       Impact factor: 4.033

2.  Nonprocessive motor dynamics at the microtubule membrane tube interface.

Authors:  Paige M Shaklee; Line Bourel-Bonnet; Marileen Dogterom; Thomas Schmidt
Journal:  Biophys J       Date:  2010-01-06       Impact factor: 4.033

3.  Analytical expressions for the shape of axisymmetric membranes with multiple domains.

Authors:  T Idema; C Storm
Journal:  Eur Phys J E Soft Matter       Date:  2011-07-14       Impact factor: 1.890

Review 4.  Building endocytic pits without clathrin.

Authors:  Ludger Johannes; Robert G Parton; Patricia Bassereau; Satyajit Mayor
Journal:  Nat Rev Mol Cell Biol       Date:  2015-04-10       Impact factor: 94.444

5.  Intracellular cargo transport by single-headed kinesin motors.

Authors:  Kristin I Schimert; Breane G Budaitis; Dana N Reinemann; Matthew J Lang; Kristen J Verhey
Journal:  Proc Natl Acad Sci U S A       Date:  2019-03-08       Impact factor: 11.205

6.  Measuring collective transport by defined numbers of processive and nonprocessive kinesin motors.

Authors:  Ken'ya Furuta; Akane Furuta; Yoko Y Toyoshima; Misako Amino; Kazuhiro Oiwa; Hiroaki Kojima
Journal:  Proc Natl Acad Sci U S A       Date:  2012-12-24       Impact factor: 11.205

7.  Reversible membrane pearling in live cells upon destruction of the actin cortex.

Authors:  Doris Heinrich; Mary Ecke; Marion Jasnin; Ulrike Engel; Günther Gerisch
Journal:  Biophys J       Date:  2014-03-04       Impact factor: 4.033

8.  Fluorescent quantification of size and lamellarity of membrane nanotubes.

Authors:  Younes F Baroji; Lene B Oddershede; Seyed Nader Seyed Reihani; Poul M Bendix
Journal:  Eur Biophys J       Date:  2014-09-26       Impact factor: 1.733

Review 9.  Lipid polymorphisms and membrane shape.

Authors:  Vadim A Frolov; Anna V Shnyrova; Joshua Zimmerberg
Journal:  Cold Spring Harb Perspect Biol       Date:  2011-11-01       Impact factor: 10.005

10.  Caveolin-1 induces formation of membrane tubules that sense actomyosin tension and are inhibited by polymerase I and transcript release factor/cavin-1.

Authors:  Prakhar Verma; Anne G Ostermeyer-Fay; Deborah A Brown
Journal:  Mol Biol Cell       Date:  2010-04-28       Impact factor: 4.138

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