Long-range cooperative binding of kinesin to a microtubule in the presence of ATP

Interaction of kinesin-coated latex beads with a single microtubule (MT) was directly observed by fluorescence microscopy. In the presence of ATP, binding of a kinesin bead to the MT facilitated the subsequent binding of other kinesin beads to an adjacent region on the MT that extended for micrometers in length. This cooperative binding was not observed in the presence of ADP or 5′-adenylylimidodiphosphate (AMP-PNP), where binding along the MT was random. Cooperative binding also was induced by an engineered, heterodimeric kinesin, WT/E236A, that could hydrolyze ATP, yet remained fixed on the MT in the presence of ATP. Relative to the stationary WT/E236A kinesin on a MT, wild-type kinesin bound preferentially in close proximity, but was biased to the plus-end direction. These results suggest that kinesin binding and ATP hydrolysis may cause a long-range state transition in the MT, increasing its affinity for kinesin toward its plus end. Thus, our study highlights the active involvement of MTs in kinesin motility.

• Publication year

  2005

• Venue

  Journal of Cell Biology

• Publication date

  2005-02-28

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.1083/jcb.200409035PMID 15738263PMCID 2171822
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Complex formation with kinesin motor domains affects the structure of microtubules.

  2004cited by this paper
• Alternate fast and slow stepping of a heterodimeric kinesin molecule

  2003cited by this paper
• Coordination of kinesin's two heads studied with mutant heterodimers

  2002cited by this paper
• Dynamics and cooperativity of microtubule decoration by the motor protein kinesin.

  2001influential reference
• A processive single-headed motor: kinesin superfamily protein KIF1A.

  1999cited by this paper
• A structural change in the kinesin motor protein that drives motility

  1999cited by this paper
• Intrastrand cross-linked actin between Gln-41 and Cys-374. III. Inhibition of motion and force generation with myosin.

  1998cited by this paper
• Direct inhibition of microtubule-based kinesin motility by local anesthetics.

  1998cited by this paper
• Intrastrand cross-linked actin between Gln-41 and Cys-374. II. Properties of cross-linked oligomers.

  1998cited by this paper
• Mechanics of single kinesin molecules measured by optical trapping nanometry.

  1997cited by this paper
• Motor domains of kinesin and ncd interact with microtubule protofilaments with the same binding geometry.

  1997cited by this paper
• The movement of kinesin along microtubules.

  1996cited by this paper
• Weak and strong states of kinesin and ncd.

  1996cited by this paper
• Evidence for alternating head catalysis by kinesin during microtubule-stimulated ATP hydrolysis.

  1994cited by this paper
• Motion of actin filaments in the presence of myosin heads and ATP.

  1992cited by this paper
• Bead movement by single kinesin molecules studied with optical tweezers

  1990influential reference
• Delayed start-up of kinesin-driven microtubule gliding following inhibition by adenosine 5'-[beta,gamma-imido]triphosphate.

  1990cited by this paper
• Movement of microtubules by single kinesin molecules

  1989cited by this paper
• Preferred microtubules for vesicle transport in lobster axons.

  1987cited by this paper
• The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate.

  1986cited by this paper
• Direct observation of motion of single F-actin filaments in the presence of myosin

  1984cited by this paper
• Protein measurement with the Folin phenol reagent.

  1951cited by this paper

• Accessibility of the unstructured α-tubulin C-terminal tail is controlled by microtubule lattice conformation

  2026cites this paper
• Accessibility of the unstructured α-tubulin C-terminal tail is controlled by microtubule lattice conformation

  2025cites this paper
• Structural switching of tubulin in the microtubule lattice

  2025cites this paper
• An Overview of Contrasting Experimental Results on Dynamics of Kinesin-1 Molecular Motors: Insight into the Underlying Mechanism

  2025cites this paper
• Tubulin CFEOM mutations both inhibit or activate kinesin motor activity

  2024cites this paper
• A model for cooperativity of kinesin-4 motors by communicating through the microtubule track

  2024cites this paper
• Cooperative ligand binding to a double-stranded Ising lattice—Application to cofilin binding to actin filaments

  2023cites this paper
• Manipulation of force geometry using optical tweezers reveals novel features of biomolecular interactions

  2023cites this paper
• Causes, costs and consequences of kinesin motors communicating through the microtubule lattice

  2023cites this paper
• Mechanical communication within the microtubule through network-based analysis of tubulin dynamics

  2023cites this paper
• Structural model of microtubule dynamics inhibition by kinesin-4 from the crystal structure of KLP-12 –tubulin complex

  2022cites this paper
• Motor guidance by long-range communication on the microtubule highway

  2022cites this paper
• Plus and minus ends of microtubules respond asymmetrically to kinesin binding by a long-range directionally driven allosteric mechanism

  2021influential citation
• Modeling spatiotemporally varying protein–protein interactions in CyLaKS, the Cytoskeleton Lattice-based Kinetic Simulator

  2021cites this paper
• CyLaKS: the Cytoskeleton Lattice-based Kinetic Simulator

  2021influential citation
• Motor usage imprints microtubule stability in the shaft

  2021cites this paper
• Micron-scale geometrical features of microtubules as regulators of microtubule organization

  2021cites this paper
• The role of extended range of interactions in the dynamics of interacting molecular motors

  2021cites this paper
• Design of Active Nanosystems Incorporating Biomolecular Motors

  2021cites this paper
• A kinesin-1 variant reveals motor-induced microtubule damage in cells

  2021cites this paper
• Motor usage imprints microtubule stability along the shaft.

  2021cites this paper
• Motor guidance by long-range communication through the microtubule highway

  2020cites this paper
• Single depolymerizing and transport kinesins stabilize microtubule ends

  2020cites this paper
• Long-Range and Directional Allostery of Actin Filaments Plays Important Roles in Various Cellular Activities

  2020cites this paper
• The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology

  2019cites this paper
• Microtubule lattice plasticity.

  2019cites this paper
• Generation and regulation of microtubule network asymmetry to drive cell polarity.

  2019cites this paper
• Cellular Logistics: Unraveling the Interplay Between Microtubule Organization and Intracellular Transport.

  2019cites this paper
• Modulation of Kinesin’s Load-Bearing Capacity by Force Geometry and the Microtubule Track

  2019cites this paper
• Mechanical Model of Nuclei Ordering in Drosophila Embryos Reveals Dilution of Stochastic Forces.

  2018cites this paper
• GMPCPP-microtubule complexed with nucleotide-free KIF5C

  2018cites this paper
• Kinesin expands and stabilises the GDP-microtubule lattice 2 3

  2018cites this paper
• Kinesin-binding–triggered conformation switching of microtubules contributes to polarized transport

  2018cites this paper
• Crowding and Pausing Strongly Affect Dynamics of Kinesin-1 Motors along Microtubules

  2018cites this paper
• Processive Kinesin-14 HSET Exhibits Directional Flexibility Depending on Motor Traffic.

  2018cites this paper
• Kinesin expands and stabilises the GDP-microtubule lattice

  2018cites this paper
• Mechanism of Catalytic Microtubule Depolymerization via KIF2-Tubulin Transitional Conformation.

  2017cites this paper
• Correlation imaging reveals specific crowding dynamics of kinesin motor proteins

  2017cites this paper
• Structural-mechanical remodelling of GDP-microtubules by kinesin

  2017cites this paper
• 1 1 Structural-mechanical remodelling of GDP-microtubules by kinesin 2 3

  2017cites this paper
• The +TIP coordinating protein EB1 is highly dynamic and diffusive on microtubules, sensitive to GTP analog, ionic strength, and EB1 concentration

  2016cites this paper
• Elastic Anisotropy Scenario for Cooperative Binding of Kinesin-Coated Beads on Microtubules.

  2016cites this paper
• Totally Asymmetric Simple Exclusion Process on an Open Lattice with Langmuir Kinetics Depending on the Occupancy of the Forward Neighboring Site

  2016cites this paper
• Semiflexible Chains at Surfaces: Worm-Like Chains and beyond

  2016cites this paper
• Mechanosensitive kinetic preference of actin-binding protein to actin filament.

  2016cites this paper
• Transport in complex driven systems

  2015cites this paper
• Driven diffusive systems with mutually interactive Langmuir kinetics.

  2015cites this paper
• Intracellular transport driven by cytoskeletal motors: General mechanisms and defects

  2015cites this paper
• Measuring transport of motor cargos.

  2014cites this paper
• Tau Proteins Harboring Neurodegeneration-Linked Mutations Impair Kinesin Translocation in vitro

  2014cites this paper
• Kar3Vik1 Uses a Minus-End Directed Powerstroke for Movement along Microtubules

  2013cites this paper
• Global transcriptomic profiling of aspen trees under elevated [CO2] to identify potential molecular mechanisms responsible for enhanced radial growth

  2013influential citation
• Functional asymmetry in kinesin and dynein dimers

  2013cites this paper
• 4.17 Kinesin Structure and Biochemistry

  2012cites this paper
• A fluorescent GTP analog as a specific, high-precision label of microtubules.

  2011cites this paper
• Particle interactions and lattice dynamics: scenarios for efficient bidirectional stochastic transport?

  2011cites this paper
• New insights into the mechanisms of cytomotive actin and tubulin filaments.

  2011cites this paper
• Cooperative lattice dynamics and anomalous fluctuations of microtubules

  2011cites this paper
• Alphaherpesviruses and the Cytoskeleton in Neuronal Infections

  2011cites this paper
• Preferential binding of a kinesin-1 motor to GTP-tubulin–rich microtubules underlies polarized vesicle transport

  2011cites this paper
• One-dimensional Brownian motion of charged nanoparticles along microtubules: a model system for weak binding interactions.

  2010cites this paper
• Stochastic modeling of intracellular processes : bidirectional transport and microtubule dynamics

  2010cites this paper
• Tau isoform‐specific modulation of kinesin‐driven microtubule gliding rates and trajectories as determined with tau‐stabilized microtubules

  2010cites this paper
• Cooperative behavior of molecular motors: Cargo transport and traffic phenomena

  2010cites this paper
• Small-molecule inhibitors reveal multiple strategies for Hedgehog pathway blockade

  2009cites this paper
• ACTIVE BIO-SYSTEMS: FROM SINGLE MOTOR MOLECULES TO COOPERATIVE CARGO TRANSPORT

  2009cites this paper
• Novel mode of cooperative binding between myosin and Mg2+ -actin filaments in the presence of low concentrations of ATP.

  2009cites this paper
• Kinesin-1 Regulates Microtubule Dynamics via a c-Jun N-terminal Kinase-dependent Mechanism*♦

  2009cites this paper
• Diameters of microtubules change during rotation of the lipotubuloids of Ornithogalum umbellatum stipule epidermis as a result of varying protofilament monomers sizes and distance between them

  2009cites this paper
• The role of microtubules in processive kinesin movement.

  2008cites this paper
• Dynamic kinesin-1 clustering on microtubules due to mutually attractive interactions

  2008cites this paper
• Temperature dependence of the flexural rigidity of single microtubules.

  2008cites this paper
• Energetics of kinesin‐1 stepping mechanism

  2008cites this paper
• How single molecule detection measures the dynamic actions of life

  2007cites this paper
• The Kinetic Characterization of the Marginally Processive Motor, Dimeric Eg5/KSP

  2007cites this paper
• Subunits interactions in kinesin motors.

  2007cites this paper
• Studying molecular motor-based cargo transport: what is real and what is noise?

  2007cites this paper
• Back on track – On the role of the microtubule for kinesin motility and cellular function

  2006cites this paper
• Probing and using the dielectric properties of microtubules within microsystems integrating Indium-Tin oxide microelectrodes

  2006cites this paper
• A structural model for monastrol inhibition of dimeric kinesin Eg5

  2006cites this paper
• Molecular motor traffic: From biological nanomachines to macroscopic transport

  2006cites this paper
• Assay of Rab4-dependent trafficking on microtubules.

  2005cites this paper
• Kinesin-driven sorting machine on large-scale microtubule arrays

  2005cites this paper