Literature DB >> 19921171

Kinesin velocity increases with the number of motors pulling against viscoelastic drag.

Jason Gagliano1, Matthew Walb, Brian Blaker, Jed C Macosko, George Holzwarth.   

Abstract

Although the properties of single kinesin molecular motors are well understood, it is not clear whether multiple motors pulling a single vesicle in a cell cooperate or interfere with one another. To learn how small numbers of motors interact, microtubule gliding assays were carried out with full-length Drosophila kinesin in a novel motility medium containing xanthan, a stiff, water-soluble polysaccharide. At 2 mg/ml xanthan, the zero-shear viscosity of this medium is 1,000 times the viscosity of water, similar to cellular viscosity. To mimic the rheological drag force on the motors when attached to a vesicle in a cell, we attached a 2 microm bead to one end of the microtubule (MT). During gliding assays in our novel medium, the moving bead exerted a drag force of 4-15 pN on the kinesins pulling the MT. The velocity of MTs with an attached bead increased with MT length and with kinesin concentration. The increase with MT length arose because the number of motors is directly proportional to MT length. Our results show that small numbers of kinesins cooperate constructively when pulling against a viscoelastic drag. In the absence of a bead but still in the viscous medium, MT velocity was independent of MT length and kinesin concentration because the thin MT, like a snake moving through grass, was able to move between xanthan molecules with little resistance. A minimal shared-load model in which the number of motors is proportional to MT length fits the observed dependence of gliding velocity on MT length and kinesin concentration.

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Year:  2009        PMID: 19921171     DOI: 10.1007/s00249-009-0560-8

Source DB:  PubMed          Journal:  Eur Biophys J        ISSN: 0175-7571            Impact factor:   1.733


  42 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.  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.  Fast vesicle transport in PC12 neurites: velocities and forces.

Authors:  D B Hill; M J Plaza; K Bonin; G Holzwarth
Journal:  Eur Biophys J       Date:  2004-04-08       Impact factor: 1.733

4.  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

5.  Fewer active motors per vesicle may explain slowed vesicle transport in chick motoneurons after three days in vitro.

Authors:  Jed C Macosko; Jason M Newbern; Jean Rockford; Ernest N Chisena; Charlotte M Brown; George M Holzwarth; Carol E Milligan
Journal:  Brain Res       Date:  2008-03-20       Impact factor: 3.252

6.  Bead movement by single kinesin molecules studied with optical tweezers.

Authors:  S M Block; L S Goldstein; B J Schnapp
Journal:  Nature       Date:  1990-11-22       Impact factor: 49.962

7.  Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics.

Authors:  M A Welte; S P Gross; M Postner; S M Block; E F Wieschaus
Journal:  Cell       Date:  1998-02-20       Impact factor: 41.582

8.  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

9.  Kinesin takes one 8-nm step for each ATP that it hydrolyzes.

Authors:  D L Coy; M Wagenbach; J Howard
Journal:  J Biol Chem       Date:  1999-02-05       Impact factor: 5.157

10.  Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies.

Authors:  R A Walker; E T O'Brien; N K Pryer; M F Soboeiro; W A Voter; H P Erickson; E D Salmon
Journal:  J Cell Biol       Date:  1988-10       Impact factor: 10.539

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  17 in total

1.  Magnet polepiece design for uniform magnetic force on superparamagnetic beads.

Authors:  Todd Fallesen; David B Hill; Matthew Steen; Jed C Macosko; Keith Bonin; George Holzwarth
Journal:  Rev Sci Instrum       Date:  2010-07       Impact factor: 1.523

2.  A nonequilibrium power balance relation for analyzing dissipative filament dynamics.

Authors:  Falko Ziebert; Hervé Mohrbach; Igor M Kulić
Journal:  Eur Phys J E Soft Matter       Date:  2015-12-22       Impact factor: 1.890

3.  Force-velocity relationship for multiple kinesin motors pulling a magnetic bead.

Authors:  Todd L Fallesen; Jed C Macosko; G Holzwarth
Journal:  Eur Biophys J       Date:  2011-07-07       Impact factor: 1.733

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.  Geometry of antiparallel microtubule bundles regulates relative sliding and stalling by PRC1 and Kif4A.

Authors:  Sithara Wijeratne; Radhika Subramanian
Journal:  Elife       Date:  2018-10-24       Impact factor: 8.140

6.  Microtubules are required for efficient epithelial tight junction homeostasis and restoration.

Authors:  Lila G Glotfelty; Anita Zahs; Catalin Iancu; Le Shen; Gail A Hecht
Journal:  Am J Physiol Cell Physiol       Date:  2014-06-11       Impact factor: 4.249

7.  Dual-Color Herpesvirus Capsids Discriminate Inoculum from Progeny and Reveal Axonal Transport Dynamics.

Authors:  Julian Scherer; Zachary A Yaffe; Michael Vershinin; Lynn W Enquist
Journal:  J Virol       Date:  2016-10-14       Impact factor: 5.103

Review 8.  Kinesin and Dynein Mechanics: Measurement Methods and Research Applications.

Authors:  Zachary Abraham; Emma Hawley; Daniel Hayosh; Victoria A Webster-Wood; Ozan Akkus
Journal:  J Biomech Eng       Date:  2018-02-01       Impact factor: 2.097

9.  Motor coupling through lipid membranes enhances transport velocities for ensembles of myosin Va.

Authors:  Shane R Nelson; Kathleen M Trybus; David M Warshaw
Journal:  Proc Natl Acad Sci U S A       Date:  2014-09-08       Impact factor: 11.205

10.  Effects of surface passivation on gliding motility assays.

Authors:  Andy Maloney; Lawrence J Herskowitz; Steven J Koch
Journal:  PLoS One       Date:  2011-06-03       Impact factor: 3.240

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