Chemomechanical Coupling and Motor Cycles of Myosin V

Bierbaum, Veronika; Lipowsky, Reinhard

doi:10.1016/j.bpj.2011.02.012

Cited by 38 publications

(65 citation statements)

References 38 publications

(90 reference statements)

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“…[38] consists of chemomechanical forward cycle F, dissipative cycle E, and pure mechanical cycle M ( SI for details and Fig. S11) reveals no local minimum in this condition.…”

Section: Comparison Of Q Among Different Types Of Motorsmentioning

confidence: 99%

Energetic costs, precision, and efficiency of a biological motor in cargo transport

Hwang

Hyeon

2017

Preprint

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Molecular motors play key roles in organizing the interior of cells. An efficient motor in cargo transport would travel with a high speed and a minimal error in transport time (or distance) while consuming minimal amount of energy. The travel distance and its variance of motor are, however, physically constrained by energy consumption, the principle of which has recently been formulated into the thermodynamic uncertainty relation. Here, we reinterpret the uncertainty measure (Q) defined in the thermodynamic uncertainty relation such that a motor efficient in cargo transport is characterized with a small Q. Analyses on the motility data from several types of molecular motors show that Q is a nonmonotic function of ATP concentration and load (f ). For kinesin-1, Q is locally minimized at [ATP] ≈ 200 µM and f ≈ 4 pN. Remarkably, for the mutant with a longer neck-linker this local minimum vanishes, and the energetic cost to achieve the same precision as the wild-type increases significantly, which underscores the importance of molecular structure in transport properties. For the biological motors studied here, their value of Q is semi-optimized under the cellular condition ([ATP] ≈ 1 mM, f = 0 − 1 pN). We find that among the motors, kinesin-1 at single molecule level is the most efficient in cargo transport.Biological systems are in nonequilibrium steady states (NESS) in which the energy and material currents flow constantly in and out of the system. Subjected to incessant thermal and nonequilibrium fluctuations, cellular processes are inherently stochastic and error-prone. To minimize detrimentaion effects, cells are equipped with a plethora of energy-consuming error-correction mechanisms. Trade-off relations between the energetic cost and information processing are ubiquitous in cellular processes, and have been a recurring theme in biology for many decades [1? ? -4].A recent study by Barato and Seifert [5] has formulated a concise inequality known as the thermodynamic uncertainty relation, the trade-off between energy consumption and precision of an observable from dissipative processes in NESS. To be more explicit, the uncertainty measure Q, defined as a product between the energy consumption (heat dissipation, Q(t)) from an energy-driven process in the steady state and the squared relative error of an output observable X(t), 2 X (t) = δX 2 / X 2 , is constant. It has been further conjectured that for an arbitrary chemical network formulated by Markov jump processes Q cannot be smaller than 2k B T ,The measure Q quantifies the uncertainty of a dynamic process. The smaller the value of Q, the more regular and predictable is the trajectory generated from the process, rendering the output observable more precise. The proof and physical significance of this inequality have been discussed [5][6][7][8][9][10]. In the presence of large fluctuations inherent to cellular processes, harnessing energy into precise motion is critical for accuracy in cellular computation.The uncertainty measure Q can be used to assess the e...

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“…[38] consists of chemomechanical forward cycle F, dissipative cycle E, and pure mechanical cycle M ( SI for details and Fig. S11) reveals no local minimum in this condition.…”

Section: Comparison Of Q Among Different Types Of Motorsmentioning

confidence: 99%

Energetic costs, precision, and efficiency of a biological motor in cargo transport

Hwang

Hyeon

2017

Preprint

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“…ForF ij = 0, the expression in (4) reduces to the force-dependent factors Φ ij (F ) as used in [8]. The parameterF ij represents a force threshold for the influence of the external force onto the corresponding chemical transition as in [43]. For the mechanical transitions, we take the exponential dependence…”

Section: Parametrization Of Transition Ratesmentioning

confidence: 99%

Network Complexity and Parametric Simplicity for Cargo Transport by Two Molecular Motors

et al. 2012

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Cargo transport by two molecular motors is studied by constructing a chemomechanical network for the whole transport system and analyzing the cargo and motor trajectories generated by this network. The theoretical description starts from the different nucleotide states of a single motor supplemented by chemical and mechanical transitions between these states. As an instructive example, we focus on kinesin-1, for which a detailed single-motor network has been developed previously. This network incorporates the chemical transitions arising from ATP hydrolysis on both motor heads. In addition, both the chemical and the mechanical transition rates of a single kinesin motor were found to depend on the load force experienced by the motor. When two such motors are attached via their stalks to a cargo particle, they become elastically coupled. This coupling can be effectively described by an elastic spring between the two motors. The spring extension, which is given by the deviation of the actual spring length from its rest length, determines the mutual interaction force between the motors and, thus, affects all chemical and mechanical transition rates of both motors. As a result, cargo transport by two motors leads to a combined chemomechanical network, which is quite complex and contains a large number of motor cycles. However, apart from the single motor parameters, this complex network involves only two additional parameters: (i) the spring constant of the elastic coupling between the motors and (ii) the rebinding rate for an unbound motor. We show that these two parameters can be determined directly from cargo trajectories and/or trajectories of individual motors. Both types of trajectories are accessible to experiment and, thus, can be used to obtain a complete set of parameters for cargo transport by two motors.

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“…Therefore, the fraction of time the myosin remains attached to actin can be affected by this equilibrium with consequences for processivity and motile activity [19], [20], [21]. While the kinetic properties and the mechanism of myosin-5 movement are well established [22], [23], [24], only little information regarding the energetics of the individual steps in the ATPase cycle of the motor is available [25]. An ultimate goal for a complete and detailed description of the myosin-5 mechanism of energy transduction should thus include the determination of the energetics of the individual steps in the acto-myosin ATPase cycle.…”

Section: Introductionmentioning

confidence: 99%

Global Fit Analysis of Myosin-5b Motility Reveals Thermodynamics of Mg2+-Sensitive Acto-Myosin-ADP States

et al. 2013

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Kinetic and thermodynamic studies of the mechanochemical cycle of myosin motors are essential for understanding the mechanism of energy conversion. Here, we report our investigation of temperature and free Mg2+-ion dependencies of sliding velocities of a high duty ratio class-5 myosin motor, myosin-5b from D. discoideum using in vitro motility assays. Previous studies have shown that the sliding velocity of class-5 myosins obeys modulation by free Mg2+-ions. Free Mg2+-ions affect ADP release kinetics and the dwell time of actin-attached states. The latter determines the maximal velocity of actin translocation in the sliding filament assay. We measured the temperature dependence of sliding velocity in the range from 5 to 55°C at two limiting free Mg2+-ion concentrations. Arrhenius plots demonstrated non-linear behavior. Based on this observation we propose a kinetic model, which explains both sensitivity towards free Mg2+-ions and non-linearity of the temperature dependence of sliding velocity. According to this model, velocity is represented as a simple analytical function of temperature and free Mg2+-ion concentrations. This function has been applied to global non-linear fit analysis of three data sets including temperature and magnesium (at 20°C) dependence of sliding velocity. As a result we obtain thermodynamic parameters (ΔHMg and ΔSMg) of a fast equilibrium between magnesium free (AM·D) and magnesium bound acto-myosin-ADP (AM· Mg2+D) states and the corresponding enthalpic barriers associated with ADP release (ΔH1 ‡ and ΔH2 ‡). The herein presented integrative approach of data analysis based on global fitting can be applied to the remaining steps of the acto-myosin ATPase cycle facilitating the determination of energetic parameters and thermodynamics of acto-myosin interactions.

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Chemomechanical Coupling and Motor Cycles of Myosin V

Cited by 38 publications

References 38 publications

Energetic costs, precision, and efficiency of a biological motor in cargo transport

Energetic costs, precision, and efficiency of a biological motor in cargo transport

Network Complexity and Parametric Simplicity for Cargo Transport by Two Molecular Motors

Global Fit Analysis of Myosin-5b Motility Reveals Thermodynamics of Mg2+-Sensitive Acto-Myosin-ADP States

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