Literature DB >> 21767491

Productive cooperation among processive motors depends inversely on their mechanochemical efficiency.

Jonathan W Driver1, D Kenneth Jamison, Karthik Uppulury, Arthur R Rogers, Anatoly B Kolomeisky, Michael R Diehl.   

Abstract

Subcellular cargos are often transported by teams of processive molecular motors, which raises questions regarding the role of motor cooperation in intracellular transport. Although our ability to characterize the transport behaviors of multiple-motor systems has improved substantially, many aspects of multiple-motor dynamics are poorly understood. This work describes a transition rate model that predicts the load-dependent transport behaviors of multiple-motor complexes from detailed measurements of a single motor's elastic and mechanochemical properties. Transition rates are parameterized via analyses of single-motor stepping behaviors, load-rate-dependent motor-filament detachment kinetics, and strain-induced stiffening of motor-cargo linkages. The model reproduces key signatures found in optical trapping studies of structurally defined complexes composed of two kinesin motors, and predicts that multiple kinesins generally have difficulties in cooperating together. Although such behavior is influenced by the spatiotemporal dependence of the applied load, it appears to be directly linked to the efficiency of kinesin's stepping mechanism, and other types of less efficient and weaker processive motors are predicted to cooperate more productively. Thus, the mechanochemical efficiencies of different motor types may determine how effectively they cooperate together, and hence how motor copy number contributes to the regulation of cargo motion.
Copyright © 2011 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2011        PMID: 21767491      PMCID: PMC3136769          DOI: 10.1016/j.bpj.2011.05.067

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


  25 in total

Review 1.  Probing the relation between force--lifetime--and chemistry in single molecular bonds.

Authors:  E Evans
Journal:  Annu Rev Biophys Biomol Struct       Date:  2001

2.  Kinesin crouches to sprint but resists pushing.

Authors:  Michael E Fisher; Young C Kim
Journal:  Proc Natl Acad Sci U S A       Date:  2005-10-17       Impact factor: 11.205

3.  Finite-particle tracking reveals submicroscopic-size changes of mitochondria during transport in mitral cell dendrites.

Authors:  Arne Gennerich; Detlev Schild
Journal:  Phys Biol       Date:  2006-02-16       Impact factor: 2.583

4.  Stochastic simulations of cargo transport by processive molecular motors.

Authors:  Christian B Korn; Stefan Klumpp; Reinhard Lipowsky; Ulrich S Schwarz
Journal:  J Chem Phys       Date:  2009-12-28       Impact factor: 3.488

5.  On the origin of kinesin limping.

Authors:  Adrian N Fehr; Braulio Gutiérrez-Medina; Charles L Asbury; Steven M Block
Journal:  Biophys J       Date:  2009-09-16       Impact factor: 4.033

6.  Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes.

Authors:  Virupakshi Soppina; Arpan Kumar Rai; Avin Jayesh Ramaiya; Pradeep Barak; Roop Mallik
Journal:  Proc Natl Acad Sci U S A       Date:  2009-10-28       Impact factor: 11.205

7.  Directional loading of the kinesin motor molecule as it buckles a microtubule.

Authors:  F Gittes; E Meyhöfer; S Baek; J Howard
Journal:  Biophys J       Date:  1996-01       Impact factor: 4.033

8.  Processivity of the motor protein kinesin requires two heads.

Authors:  W O Hancock; J Howard
Journal:  J Cell Biol       Date:  1998-03-23       Impact factor: 10.539

9.  Force-induced bidirectional stepping of cytoplasmic dynein.

Authors:  Arne Gennerich; Andrew P Carter; Samara L Reck-Peterson; Ronald D Vale
Journal:  Cell       Date:  2007-11-30       Impact factor: 41.582

10.  A cytoplasmic dynein tail mutation impairs motor processivity.

Authors:  Kassandra M Ori-McKenney; Jing Xu; Steven P Gross; Richard B Vallee
Journal:  Nat Cell Biol       Date:  2010-11-21       Impact factor: 28.824

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  35 in total

1.  Cooperative responses of multiple kinesins to variable and constant loads.

Authors:  D Kenneth Jamison; Jonathan W Driver; Michael R Diehl
Journal:  J Biol Chem       Date:  2011-12-09       Impact factor: 5.157

2.  How the interplay between mechanical and nonmechanical interactions affects multiple kinesin dynamics.

Authors:  Karthik Uppulury; Artem K Efremov; Jonathan W Driver; D Kenneth Jamison; Michael R Diehl; Anatoly B Kolomeisky
Journal:  J Phys Chem B       Date:  2012-07-11       Impact factor: 2.991

3.  Cytoskeletal Network Morphology Regulates Intracellular Transport Dynamics.

Authors:  David Ando; Nickolay Korabel; Kerwyn Casey Huang; Ajay Gopinathan
Journal:  Biophys J       Date:  2015-10-20       Impact factor: 4.033

4.  Irrelevance of the power stroke for the directionality, stopping force, and optimal efficiency of chemically driven molecular machines.

Authors:  R Dean Astumian
Journal:  Biophys J       Date:  2015-01-20       Impact factor: 4.033

5.  Effective behavior of cooperative and nonidentical molecular motors.

Authors:  Joseph J Klobusicky; John Fricks; Peter R Kramer
Journal:  Res Math Sci       Date:  2020-09-21

6.  Cargo Transport by Two Coupled Myosin Va Motors on Actin Filaments and Bundles.

Authors:  M Yusuf Ali; Andrej Vilfan; Kathleen M Trybus; David M Warshaw
Journal:  Biophys J       Date:  2016-11-15       Impact factor: 4.033

7.  Mechanical coupling between myosin molecules causes differences between ensemble and single-molecule measurements.

Authors:  Sam Walcott; David M Warshaw; Edward P Debold
Journal:  Biophys J       Date:  2012-08-08       Impact factor: 4.033

8.  Spatial and temporal sensing limits of microtubule polarization in neuronal growth cones by intracellular gradients and forces.

Authors:  Saurabh Mahajan; Chaitanya A Athale
Journal:  Biophys J       Date:  2012-12-18       Impact factor: 4.033

9.  Bifurcation of velocity distributions in cooperative transport of filaments by fast and slow motors.

Authors:  Xin Li; Reinhard Lipowsky; Jan Kierfeld
Journal:  Biophys J       Date:  2013-02-05       Impact factor: 4.033

10.  The kinetics of mechanically coupled myosins exhibit group size-dependent regimes.

Authors:  Lennart Hilbert; Shivaram Cumarasamy; Nedjma B Zitouni; Michael C Mackey; Anne-Marie Lauzon
Journal:  Biophys J       Date:  2013-09-17       Impact factor: 4.033

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