Collective dynamics of processive cytoskeletal motors.

Major cellular processes are supported by various biomolecular motors that usually operate together as teams. We present an overview of the collective dynamics of processive cytokeletal motor proteins based on recent experimental and theoretical investigations. Experimental studies show that multiple motors function with different degrees of cooperativity, ranging from negative to positive. This effect depends on the mechanical properties of individual motors, the geometry of their connections, and the surrounding cellular environment. Theoretical models based on stochastic approaches underline the importance of intermolecular interactions, the properties of single motors, and couplings with cellular medium in predicting the collective dynamics. We discuss several features that specify the cooperativity in motor proteins. Based on this approach a general picture of collective dynamics of motor proteins is formulated, and the future directions and challenges are discussed.

[1]  E. Landahl,et al.  Mechanism of cooperative behaviour in systems of slow and fast molecular motors. , 2009, Physical chemistry chemical physics : PCCP.

[2]  Sivaraj Sivaramakrishnan,et al.  Myosin lever arm directs collective motion on cellular actin network , 2014, Proceedings of the National Academy of Sciences.

[3]  Anatoly B Kolomeisky,et al.  Motor proteins and molecular motors: how to operate machines at the nanoscale , 2013, Journal of physics. Condensed matter : an Institute of Physics journal.

[4]  Erkan Tüzel,et al.  Transport by populations of fast and slow kinesins uncovers novel family-dependent motor characteristics important for in vivo function. , 2014, Biophysical journal.

[5]  S. Gross,et al.  Building Complexity: An In Vitro Study of Cytoplasmic Dynein with In Vivo Implications , 2005, Current Biology.

[6]  Hamid Teimouri,et al.  Theoretical analysis of dynamic processes for interacting molecular motors , 2014, Journal of physics. A, Mathematical and theoretical.

[7]  S. Gross,et al.  Cargo Transport: Two Motors Are Sometimes Better Than One , 2007, Current Biology.

[8]  L. Christophorou Science , 2018, Emerging Dynamics: Science, Energy, Society and Values.

[9]  Melanie J. I. Müller,et al.  Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors , 2008, Proceedings of the National Academy of Sciences.

[10]  Cécile Leduc,et al.  Collective behavior of antagonistically acting kinesin-1 motors. , 2010, Physical review letters.

[11]  Eric A. Kumar,et al.  Building cells for quantitative, live-cell analyses of collective motor protein functions. , 2015, Methods in cell biology.

[12]  R. Vale,et al.  Regulation of microtubule motors by tubulin isotypes and posttranslational modifications , 2014, Nature Cell Biology.

[13]  M. Schuster,et al.  Kinesin-3 and dynein cooperate in long-range retrograde endosome motility along a nonuniform microtubule array , 2011, Molecular biology of the cell.

[14]  D. Chowdhury Stochastic mechano-chemical kinetics of molecular motors: A multidisciplinary enterprise from a physicist’s perspective , 2012, 1207.6070.

[15]  A. Kolomeisky,et al.  How the interplay between mechanical and nonmechanical interactions affects multiple kinesin dynamics. , 2012, The journal of physical chemistry. B.

[16]  Frank Jülicher,et al.  Multimotor transport in a system of active and inactive kinesin-1 motors. , 2014, Biophysical journal.

[17]  Karthik Uppulury,et al.  Productive cooperation among processive motors depends inversely on their mechanochemical efficiency. , 2011, Biophysical journal.

[18]  D. Helbing,et al.  Molecular crowding creates traffic jams of kinesin motors on microtubules , 2012, Proceedings of the National Academy of Sciences.

[19]  Jacek Gaertig,et al.  The Tubulin Code , 2007, Cell cycle.

[20]  Matthias Rief,et al.  Force-dependent stepping kinetics of myosin-V. , 2005, Biophysical journal.

[21]  N. Hirokawa,et al.  Brain dynein (MAP1C) localizes on both anterogradely and retrogradely transported membranous organelles in vivo , 1990, The Journal of cell biology.

[22]  Steven M. Block,et al.  A universal pathway for kinesin stepping , 2011, Nature Structural &Molecular Biology.

[23]  Samara L. Reck-Peterson,et al.  Tug-of-War in Motor Protein Ensembles Revealed with a Programmable DNA Origami Scaffold , 2012, Science.

[24]  Mark J. Schnitzer,et al.  Single kinesin molecules studied with a molecular force clamp , 1999, Nature.

[25]  Zeynep Ökten,et al.  Myosin VI walks hand-over-hand along actin , 2004, Nature Structural &Molecular Biology.

[26]  H. Sweeney,et al.  Myosin Va and myosin VI coordinate their steps while engaged in an in vitro tug of war during cargo transport , 2011, Proceedings of the National Academy of Sciences.

[27]  Suvranu De,et al.  Multiscale Modeling in Biomechanics and Mechanobiology , 2015 .

[28]  R. Lipowsky,et al.  Cooperative cargo transport by several molecular motors. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Paul R. Selvin,et al.  The role of microtubule movement in bidirectional organelle transport , 2008, Proceedings of the National Academy of Sciences.

[30]  Barry J Dickson,et al.  Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. , 2008, Molecular biology of the cell.

[31]  Fernando Falo,et al.  The influence of direct motor–motor interaction in models for cargo transport by a single team of motors , 2010, Physical biology.

[32]  R. Mallik,et al.  Molecular Adaptations Allow Dynein to Generate Large Collective Forces inside Cells , 2013, Cell.

[33]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[34]  Christoph F. Schmidt,et al.  Moving into the cell: single-molecule studies of molecular motors in complex environments , 2011, Nature Reviews Molecular Cell Biology.

[35]  Ken’ya Furuta,et al.  Measuring collective transport by defined numbers of processive and nonprocessive kinesin motors , 2012, Proceedings of the National Academy of Sciences.

[36]  R. Cross,et al.  Prime movers: the mechanochemistry of mitotic kinesins , 2014, Nature Reviews Molecular Cell Biology.

[37]  M. Diehl Templating a Molecular Tug-of-War , 2012, Science.

[38]  R. Vale,et al.  Directional instability of microtubule transport in the presence of kinesin and dynein, two opposite polarity motor proteins , 1992, The Journal of cell biology.

[39]  S. Gross,et al.  Stepping, Strain Gating, and an Unexpected Force-Velocity Curve for Multiple-Motor-Based Transport , 2008, Current Biology.

[40]  Michael R Diehl,et al.  Cooperative Responses of Multiple Kinesins to Variable and Constant Loads* , 2011, The Journal of Biological Chemistry.

[41]  R. Lipowsky,et al.  Elastic Coupling Effects in Cooperative Transport by a Pair of Molecular Motors , 2013 .

[42]  Anatoly B. Kolomeisky,et al.  Correlations and symmetry of interactions influence collective dynamics of molecular motors , 2015, 1503.00633.

[43]  Steven P. Gross,et al.  Consequences of Motor Copy Number on the Intracellular Transport of Kinesin-1-Driven Lipid Droplets , 2008, Cell.

[44]  B. C. Carter,et al.  Cytoplasmic dynein functions as a gear in response to load , 2004, Nature.

[45]  Reinhard Lipowsky,et al.  Transport of Beads by Several Kinesin Motors , 2007, Biophysical journal.

[46]  Yale E Goldman,et al.  Coordination of molecular motors: from in vitro assays to intracellular dynamics. , 2010, Current opinion in cell biology.

[47]  W. Greenleaf,et al.  High-resolution, single-molecule measurements of biomolecular motion. , 2007, Annual review of biophysics and biomolecular structure.

[48]  Ronald D Vale,et al.  The Molecular Motor Toolbox for Intracellular Transport , 2003, Cell.

[49]  P. Wolynes,et al.  Communication: Effective temperature and glassy dynamics of active matter. , 2011, The Journal of chemical physics.

[50]  Peter G Wolynes,et al.  On the spontaneous collective motion of active matter , 2011, Proceedings of the National Academy of Sciences.

[51]  Vladimir Gelfand,et al.  Opposite-polarity motors activate one another to trigger cargo transport in live cells , 2009, The Journal of cell biology.

[52]  K. Trybus,et al.  Delineating cooperative responses of processive motors in living cells , 2014, Proceedings of the National Academy of Sciences.

[53]  A. Kolomeisky,et al.  Analysis of Cooperative Behavior in Multiple Kinesins Motor Protein Transport by Varying Structural and Chemical Properties , 2013, Cellular and molecular bioengineering.

[54]  N. Hirokawa,et al.  Charcot-Marie-Tooth Disease Type 2A Caused by Mutation in a Microtubule Motor KIF1Bβ , 2001, Cell.

[55]  Paul R Selvin,et al.  Single-molecule fluorescence and in vivo optical traps: how multiple dyneins and kinesins interact. , 2014, Chemical reviews.

[56]  B. C. Carter,et al.  Multiple-motor based transport and its regulation by Tau , 2007, Proceedings of the National Academy of Sciences.

[57]  Steven M Block,et al.  Kinesin motor mechanics: binding, stepping, tracking, gating, and limping. , 2007, Biophysical journal.

[58]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[59]  Ambarish Kunwar,et al.  Teamwork in microtubule motors. , 2013, Trends in cell biology.

[60]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[61]  G. Yarrington Molecular Cell Biology , 1987, The Yale Journal of Biology and Medicine.

[62]  Paul R Selvin,et al.  In vivo optical trapping indicates kinesin’s stall force is reduced by dynein during intracellular transport , 2013, Proceedings of the National Academy of Sciences.

[63]  Steven P Gross,et al.  Developmental Regulation of Vesicle Transport in Drosophila Embryos: Forces and Kinetics , 1998, Cell.

[64]  A. Mogilner,et al.  Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors , 2006, The Journal of cell biology.

[65]  C. Leidel,et al.  Measuring molecular motor forces in vivo: implications for tug-of-war models of bidirectional transport. , 2012, Biophysical journal.

[66]  Clare C. Yu,et al.  Mechanical stochastic tug-of-war models cannot explain bidirectional lipid-droplet transport , 2011, Proceedings of the National Academy of Sciences.

[67]  Traffic , 2004 .

[68]  Štefan Bálint,et al.  Correlative live-cell and superresolution microscopy reveals cargo transport dynamics at microtubule intersections , 2013, Proceedings of the National Academy of Sciences.

[69]  Adam G. Hendricks,et al.  Motor Coordination via a Tug-of-War Mechanism Drives Bidirectional Vesicle Transport , 2010, Current Biology.

[70]  Y. Goldman,et al.  Motor Number Controls Cargo Switching at Actin-Microtubule Intersections In Vitro , 2010, Current Biology.

[71]  Allison L. Zajac,et al.  Local Cytoskeletal and Organelle Interactions Impact Molecular-Motor-Driven Early Endosomal Trafficking , 2013, Current Biology.

[72]  R. Cross,et al.  Mechanics of the kinesin step , 2005, Nature.

[73]  Yosuke Tanaka,et al.  Molecular Motors in Neurons: Transport Mechanisms and Roles in Brain Function, Development, and Disease , 2010, Neuron.

[74]  Adam G. Hendricks,et al.  Intracellular Transport: New Tools Provide Insights into Multi-motor Transport , 2012, Current Biology.

[75]  Matthias Rief,et al.  Myosin-V is a processive actin-based motor , 1999, Nature.

[76]  Samara L. Reck-Peterson,et al.  Force-Induced Bidirectional Stepping of Cytoplasmic Dynein , 2007, Cell.

[77]  Ram Dixit,et al.  Differential Regulation of Dynein and Kinesin Motor Proteins by Tau , 2008, Science.

[78]  P. Bieling,et al.  Microtubule Motility on Reconstituted Meiotic Chromatin , 2010, Current Biology.

[79]  Samara L. Reck-Peterson,et al.  Single-Molecule Analysis of Dynein Processivity and Stepping Behavior , 2006, Cell.

[80]  Roop Mallik,et al.  Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes , 2009, Proceedings of the National Academy of Sciences.

[81]  V. Hu The Cell Cycle , 1994, GWUMC Department of Biochemistry Annual Spring Symposia.

[82]  Oliver Rath,et al.  Kinesins and cancer , 2012, Nature Reviews Cancer.

[83]  J. Joanny,et al.  Collective dynamics of interacting molecular motors. , 2006, Physical review letters.

[84]  Pamela E. Constantinou,et al.  Two kinesins transport cargo primarily via the action of one motor: implications for intracellular transport. , 2010, Biophysical journal.

[85]  Amber L. Wells,et al.  Myosin VI is a processive motor with a large step size , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Paul R. Selvin,et al.  Kinesin and Dynein Move a Peroxisome in Vivo: A Tug-of-War or Coordinated Movement? , 2005, Science.

[87]  M. Fisher,et al.  Molecular motors: a theorist's perspective. , 2007, Annual review of physical chemistry.

[88]  Eric F. Wieschaus,et al.  Coordination of opposite-polarity microtubule motors , 2002, The Journal of cell biology.

[89]  K. Trybus,et al.  Motor coupling through lipid membranes enhances transport velocities for ensembles of myosin Va , 2014, Proceedings of the National Academy of Sciences.

[90]  A. Yildiz,et al.  Processive cytoskeletal motors studied with single‐molecule fluorescence techniques , 2014, FEBS letters.

[91]  K. Tamura,et al.  Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci U S A , 2001 .

[92]  Anatoly B Kolomeisky,et al.  Coupling between motor proteins determines dynamic behaviors of motor protein assemblies. , 2010, Physical chemistry chemical physics : PCCP.

[93]  Robert A Cross,et al.  Transport and self-organization across different length scales powered by motor proteins and programmed by DNA , 2013, Nature nanotechnology.

[94]  Melanie J. I. Müller,et al.  Bidirectional transport by molecular motors: enhanced processivity and response to external forces. , 2010, Biophysical journal.

[95]  Shin'ichi Ishiwata,et al.  Kinesin–microtubule binding depends on both nucleotide state and loading direction , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[96]  K. Trybus Intracellular Transport: The Causes for Pauses , 2013, Current Biology.

[97]  J. Howard,et al.  Mechanics of Motor Proteins and the Cytoskeleton , 2001 .

[98]  Kechun Zhang,et al.  Engineering Cooperativity in Biomotor-Protein Assemblies , 2006, Science.

[99]  W. Saxton,et al.  Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. , 1999, Molecular biology of the cell.

[100]  Adam G. Hendricks,et al.  Force measurements on cargoes in living cells reveal collective dynamics of microtubule motors , 2012, Proceedings of the National Academy of Sciences.

[101]  Carsten Janke,et al.  Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions , 2011, Nature Reviews Molecular Cell Biology.

[102]  Anatoly B. Kolomeisky,et al.  Motor Proteins and Molecular Motors , 2015 .

[103]  Hailong Lu,et al.  Collective Dynamics of Elastically Coupled Myosin V Motors* , 2012, The Journal of Biological Chemistry.

[104]  Tuning Multiple Motor Travel via Single Motor Velocity , 2012, Traffic.

[105]  William O. Hancock,et al.  Bidirectional cargo transport: moving beyond tug of war , 2014, Nature Reviews Molecular Cell Biology.

[106]  Reinhard Lipowsky,et al.  Bifurcation of velocity distributions in cooperative transport of filaments by fast and slow motors. , 2013, Biophysical journal.

[107]  Lukas C. Kapitein,et al.  Optogenetic control of organelle transport and positioning , 2015, Nature.

[108]  Stephen R. Norris,et al.  A method for multiprotein assembly in cells reveals independent action of kinesins in complex , 2014, The Journal of cell biology.

[109]  Pamela E. Constantinou,et al.  Negative interference dominates collective transport of kinesin motors in the absence of load. , 2009, Physical chemistry chemical physics : PCCP.