Literature DB >> 18310242

Coordination of Kinesin motors pulling on fluid membranes.

Otger Campàs1, Cécile Leduc, Patricia Bassereau, Jaume Casademunt, Jean-François Joanny, Jacques Prost.   

Abstract

Intracellular transport relies on the action of motor proteins, which work collectively to either carry small vesicles or pull membranes tubes along cytoskeletal filaments. Although the individual properties of kinesin-1 motors have been extensively studied, little is known on how several motors coordinate their action and spatially organize on the microtubule when pulling on fluid membranes. Here we address these questions by studying, both experimentally and numerically, the growth of membrane tubes pulled by molecular motors. Our in vitro setup allows us to simultaneously control the parameters monitoring tube growth and measure its characteristics. We perform numerical simulations of membrane tube growth, using the experimentally measured values of all parameters, and analyze the growth properties of the tube considering various motor cooperation schemes. The comparison of the numerical results and the experimental data shows that motors use simultaneously several protofilaments of a microtubule to pull a single tube, as motors moving along a single protofilament cannot generate the forces required for tube extraction. In our experimental conditions, we estimate the average number of motors pulling the tube to be approximately nine, distributed over three contiguous protofilaments. Our results also indicate that the motors pulling the tube do not step synchronously.

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Year:  2008        PMID: 18310242      PMCID: PMC2397365          DOI: 10.1529/biophysj.107.118554

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  32 in total

1.  Single kinesin molecules studied with a molecular force clamp.

Authors:  K Visscher; M J Schnitzer; S M Block
Journal:  Nature       Date:  1999-07-08       Impact factor: 49.962

2.  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

3.  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

4.  Chemomechanical coupling of the forward and backward steps of single kinesin molecules.

Authors:  Masayoshi Nishiyama; Hideo Higuchi; Toshio Yanagida
Journal:  Nat Cell Biol       Date:  2002-10       Impact factor: 28.824

5.  Dynein-mediated cargo transport in vivo. A switch controls travel distance.

Authors:  S P Gross; M A Welte; S M Block; E F Wieschaus
Journal:  J Cell Biol       Date:  2000-03-06       Impact factor: 10.539

6.  Cooperative extraction of membrane nanotubes by molecular motors.

Authors:  Cécile Leduc; Otger Campàs; Konstantin B Zeldovich; Aurélien Roux; Pascale Jolimaitre; Line Bourel-Bonnet; Bruno Goud; Jean-François Joanny; Patricia Bassereau; Jacques Prost
Journal:  Proc Natl Acad Sci U S A       Date:  2004-11-29       Impact factor: 11.205

7.  Tracking melanosomes inside a cell to study molecular motors and their interaction.

Authors:  Comert Kural; Anna S Serpinskaya; Ying-Hao Chou; Robert D Goldman; Vladimir I Gelfand; Paul R Selvin
Journal:  Proc Natl Acad Sci U S A       Date:  2007-03-16       Impact factor: 11.205

8.  Kinesin and dynein move a peroxisome in vivo: a tug-of-war or coordinated movement?

Authors:  Comert Kural; Hwajin Kim; Sheyum Syed; Gohta Goshima; Vladimir I Gelfand; Paul R Selvin
Journal:  Science       Date:  2005-04-07       Impact factor: 47.728

9.  Direct observation of kinesin stepping by optical trapping interferometry.

Authors:  K Svoboda; C F Schmidt; B J Schnapp; S M Block
Journal:  Nature       Date:  1993-10-21       Impact factor: 49.962

10.  Coordination of opposite-polarity microtubule motors.

Authors:  Steven P Gross; Michael A Welte; Steven M Block; Eric F Wieschaus
Journal:  J Cell Biol       Date:  2002-02-28       Impact factor: 10.539

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  17 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.  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

4.  Transport efficiency of membrane-anchored kinesin-1 motors depends on motor density and diffusivity.

Authors:  Rahul Grover; Janine Fischer; Friedrich W Schwarz; Wilhelm J Walter; Petra Schwille; Stefan Diez
Journal:  Proc Natl Acad Sci U S A       Date:  2016-11-01       Impact factor: 11.205

5.  Calibration of optical tweezers for in vivo force measurements: how do different approaches compare?

Authors:  Yonggun Jun; Suvranta K Tripathy; Babu R J Narayanareddy; Michelle K Mattson-Hoss; Steven P Gross
Journal:  Biophys J       Date:  2014-09-16       Impact factor: 4.033

6.  Robust transport by multiple motors with nonlinear force-velocity relations and stochastic load sharing.

Authors:  Ambarish Kunwar; Alexander Mogilner
Journal:  Phys Biol       Date:  2010-02-10       Impact factor: 2.583

7.  Mechanical coupling of microtubule-dependent motor teams during peroxisome transport in Drosophila S2 cells.

Authors:  María Cecilia De Rossi; Diana E Wetzler; Lorena Benseñor; María Emilia De Rossi; Mariela Sued; Daniela Rodríguez; Vladimir Gelfand; Luciana Bruno; Valeria Levi
Journal:  Biochim Biophys Acta Gen Subj       Date:  2017-09-19       Impact factor: 3.770

Review 8.  Single-molecule fluorescence and in vivo optical traps: how multiple dyneins and kinesins interact.

Authors:  Benjamin H Blehm; Paul R Selvin
Journal:  Chem Rev       Date:  2014-01-23       Impact factor: 60.622

9.  How molecular motors are arranged on a cargo is important for vesicular transport.

Authors:  Robert P Erickson; Zhiyuan Jia; Steven P Gross; Clare C Yu
Journal:  PLoS Comput Biol       Date:  2011-05-05       Impact factor: 4.475

10.  Highly loaded behavior of kinesins increases the robustness of transport under high resisting loads.

Authors:  Woochul Nam; Bogdan I Epureanu
Journal:  PLoS Comput Biol       Date:  2015-03-03       Impact factor: 4.475

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