Kinetics of the interaction of myo1c with phosphoinositides
Jennine M Dawicki McKenna1, E Michael Ostap
1Department of Physiology, Pennsylvania Muscle Institute, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6085, USA.
Insights
Myosin 1c (myo1c) dynamically links membranes to the actin cytoskeleton. Its binding kinetics to membranes were quantified, revealing that while anionic phospholipids stabilize myo1c binding, soluble inositol phosphates can induce dissociation.
Area of Science:
- Cell Biology
- Biochemistry
- Molecular Motors
Background:
- Myosin 1c (myo1c) is a single-headed myosin crucial for linking membranes to the actin cytoskeleton.
- A pleckstrin homology domain in myo1c's tail binds phosphoinositides and inositol phosphates.
- The kinetics of myo1c binding and the influence of phospholipid composition were previously undetermined.
Purpose of the Study:
- To kinetically characterize the association and dissociation of myo1c with membranes.
- To investigate the impact of phospholipid composition on myo1c binding kinetics.
- To explore the role of soluble inositol phosphates in modulating myo1c-membrane interactions.
Main Methods:
- Stopped-flow spectroscopy was employed to measure binding and dissociation rates.
- Recombinant myo1c construct (myo1c(IQ-tail)) was used.
- Large unilamellar vesicles (LUVs) with varying lipid compositions were utilized.
Main Results:
- Myo1c(IQ-tail) association with phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P(2))-containing LUVs followed a two-exponential time course, with a diffusion-limited fast phase.
- Increasing anionic phospholipid content enhanced association rates but stabilized dissociation.
- Soluble inositol phosphates induced myo1c(IQ-tail) dissociation from LUVs.
Conclusions:
- Myo1c's membrane binding is influenced by lipid composition, with anionic phospholipids promoting stable interactions.
- Myo1c exhibits distinct dissociation kinetics compared to other pleckstrin homology domains, indicating unique stabilization mechanisms.
- Soluble inositol phosphates can dynamically regulate myo1c-membrane association, suggesting a role in membrane-cytoskeleton crosstalk.
Abstract:
myo1c is a single-headed myosin that dynamically links membranes to the actin cytoskeleton. A putative pleckstrin homology domain has been identified in the myo1c tail that binds phosphoinositides and soluble inositol phosphates with high affinity. However, the kinetics of association and dissociation and the influence of phospholipid composition on the kinetics have not been determined. Stopped-flow spectroscopy was used to measure the binding and dissociation of a recombinant myo1c construct containing the tail and regulatory domains (myo1c(IQ-tail)) to and from 100-nm diameter large unilamellar vesicles (LUVs). We found the time course of association of myo1c(IQ-tail) with LUVs containing 2% phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P(2)) followed a two-exponential time course, and the rate of the predominant fast phase depended linearly upon the total lipid concentration. The apparent second-order rate constant was approximately diffusion-limited. Increasing the molar ratio of anionic phospholipid by adding phosphatidylserine, additional PtdIns(4,5)P(2), or by situating PtdIns(4,5)P(2) in a more physiologically relevant lipid background increased the apparent association rate constant less than 2-fold. myo1c(IQ-tail) dissociated from PtdIns(4,5)P(2) at a slower rate (2.0 s(-1)) than the pleckstrin homology domain of phospholipase C-delta (13 s(-1)). The presence of additional anionic phospholipid reduced the myo1c(IQ-tail) dissociation rate constant >50-fold but marginally changed the dissociation rate of phospholipase C-delta, suggesting that additional electrostatic interactions in myo1c(IQ-tail) help to stabilize binding. Remarkably, high concentrations of soluble inositol phosphates induce dissociation of myo1c(IQ-tail) from LUVs, suggesting that phosphoinositides are able to bind to and dissociate from myo1c(IQ-tail) as it remains bound to the membrane.
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