The motor protein myosin-I produces its working stroke in two steps

Veigel, Claudia; Coluccio, Lynne M.; Jontes, James D.; Sparrow, John C.; Milligan, Ronald A.; Molloy, Justin E.

doi:10.1038/19104

Cited by 312 publications

(270 citation statements)

References 23 publications

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“…If d = 5.5 nm is an underestimate, and is equal to 10 nm under high calmodulin concentrations (21), the duty ratio is ∼0.5 at 1 pN and > 0.8 at 2 pN ( Figure 8). Although this simulation is a rough estimate of the force-dependence of the duty ratio, it supports the proposal that myo1b (and likely myo1a and myo1c) are motors well designed for tension maintenance and tension sensing (10,13,35,39). It is interesting to note that alternative splicing within the myo1b lever arm results in isoforms with four, five, or six IQ motifs, and thus may be a mechanism for tuning the strain-dependence of the myo1b duty ratio (21).…”

supporting

confidence: 77%

Temperature Dependence of Nucleotide Association and Kinetic Characterization of Myo1b

et al. 2006

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Myo1b is a widely expressed myosin-I isoform that concentrates on endosomal and ruffling membranes and is thought to play roles in membrane trafficking and dynamics. It is one of the best characterized myosin-I isoforms and appears to have unique biochemical properties tuned for tension sensing or tension maintenance. We determined the key biochemical rate constants that define the actomyo1b ATPase cycle at 37 °C and measured the temperature dependence of ATP binding, ADP release, and the transition from a nucleotide inaccessible state to a nucleotide accessible state (kalpha). The rate of ATP binding is highly temperature sensitive, with an Arrhenius activation energy 2-3 fold greater than other characterized myosins (e.g, myosin-II and myosin-V). ATP hydrolysis is fast, and phosphate release is slow and rate limiting with an actin dependence that is nearly identical to the steady-state ATPase parameters (V max and K ATPase ). ADP release is not as temperature dependent as ATP binding. The rates and temperature dependence of ADP release are similar to kalpha suggesting a similar structural change is responsible for both transitions. We calculate a duty ratio of 0.08 based on the biochemical kinetics. However, this duty ratio is likely to be highly sensitive to strain.Myosin-Is are the single-headed, low-molecular-weight members of the myosin superfamily that are proposed to link cellular membranes with the actin cytoskeleton. Myosin-I isoforms bind phosphoinositides directly (1) and function in several important cellular processes, including membrane retraction, macropinocytosis, phagocytosis, membrane trafficking, cellcell adhesion, and mechanical signal transduction (2-8).The biochemical mechanisms of long-tail and short-tail myosin-I isoforms have been studied (9-12), with myo1b being the best characterized short-tail isoform (13)(14)(15). The myo1b ATPase mechanism (Scheme 1) is notable in that (a) the maximum rate of ATP binding and population of the myo1b IQ weakly-bound states is > 30-fold slower than myosin-II, (b) nucleotide-free myo1b is in equilibrium between a state that binds nucleotide (AM′) and a state that does not bind nucleotide (AM), (c) the rate of transition between AM and AM′ (k +α ) states is similar to the rate of ADP release (k +5 ′), and (d) ADP release is slow and is accompanied by a rotation of the lever arm.We proposed that the strikingly slow actomyo1b ATPase rate constants are a property of all short-tail myosin-I isoforms (11,16). However, it has been shown recently that short-tailed Dictyostelium myosin-IE (not to be confused with vertebrate long-tail myo1e (11)) has kinetic rate constants that are substantially faster than vertebrate short-tail isoforms (12). Because of † EMO was supported by grants from the National Institutes of Health (GM57247 and AR051174). JHL was supported by a training grant from the National Institute of Arthritis and Musculoskeletal and Skin Diseases (AR053461). *Corresponding author: E. Michael Ostap, Department of Physiology, University of Pe...

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confidence: 77%

Temperature Dependence of Nucleotide Association and Kinetic Characterization of Myo1b

et al. 2006

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“…A group of myosins (similar to those with the ADP induced tail swing) have been shown in the elegant work of Veigel et al (1999Veigel et al ( , 2002Veigel et al ( , 2003, to exhibit a double step in the laser trap, single molecule displacement measurements. These two steps have been interpreted to reflect a displacement step associated with P i release and a second (usually smaller) displacement step associated with ADP release.…”

Section: Double Step In the Optical Trapmentioning

confidence: 99%

Adenosine diphosphate and strain sensitivity in myosin motors

Nyitrai

Geeves

2004

Phil. Trans. R. Soc. Lond. B

171

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The release of adenosine diphosphate (ADP) from the actomyosin cross-bridge plays an important role in the adenosine-triphosphate-driven cross-bridge cycle. In fast contracting muscle fibres, the rate at which ADP is released from the cross-bridge correlates with the maximum shortening velocity of the muscle fibre, and in some models the rate of ADP release defines the maximum shortening velocity. In addition, it has long been thought that the rate of ADP release could be sensitive to the load on the cross-bridge and thereby provide a molecular explanation of the Fenn effect. However, direct evidence of a strain-sensitive ADPrelease mechanism has been hard to come by for fast muscle myosins. The recently published evidence for a strain-sensing mechanism involving ADP release for slower muscle myosins, and in particular non-muscle myosins, is more compelling and can provide the mechanism of processivity for motors such as myosin V. It is therefore timely to examine the evidence for this strain-sensing mechanism. The evidence presented here will argue that a strain-sensitive mechanism of ADP release is universal for all myosins but the basic mechanism has evolved in different ways for different types of myosin. Furthermore, this strain-sensing mechanism provides a way of coordinating the action of multiple myosin motor domains in a single myosin molecule, or in complex assemblies of myosins over long distances without invoking a classic direct allosteric or cooperative communication between motors.

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“…Using a single-molecule technique, Veigel et al (1999) have recently found that the working stroke of certain slow, non-muscle myosins consists of two well-separated steps, each of about 5 nm. When they used subfragment S1 of skeletal muscle, they could not fully resolve two steps in the attachment but showed that it occupied some 5 ms as against 1ms for detachment, suggesting strongly that it too consists of more than one step.…”

Section: Number Of Attached Statesmentioning

confidence: 99%

Mechanics and models of the myosin motor

Huxley

2000

Phil. Trans. R. Soc. Lond. B

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In striated muscles, shortening comes about by the sliding movement of thick ¢laments, composed mostly of myosin, relative to thin ¢laments, composed mostly of actin. This is brought about by cyclic action of cross-bridges' composed of the heads of myosin molecules projecting from a thick ¢lament, which attach to an adjacent thin ¢lament, exert force for a limited time and detach, and then repeat this cycle further along the ¢lament. The requisite energy is provided by the hydrolysis of a molecule of adenosine triphosphate to the diphosphate and inorganic phosphate, the steps of this reaction being coupled to mechanical events within the cross-bridge. The nature of these events is discussed. There is good evidence that one of them is a change in the angle of tilt of a`lever arm' relative to the`catalytic domain' of the myosin head which binds to the actin ¢lament. It is suggested here that this event is superposed on a slower, temperature-sensitive change in the orientation of the catalytic domain on the actin ¢lament. Many uncertainties remain.

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The motor protein myosin-I produces its working stroke in two steps

Cited by 312 publications

References 23 publications

Temperature Dependence of Nucleotide Association and Kinetic Characterization of Myo1b

Temperature Dependence of Nucleotide Association and Kinetic Characterization of Myo1b

Adenosine diphosphate and strain sensitivity in myosin motors

Mechanics and models of the myosin motor

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