ATP-induced reconfiguration of the micro-viscoelasticity of cardiac and skeletal myosin solutions

Abstract

We study the high-frequency, micro-mechanical response of suspensions composed of cardiac and skeletal muscle myosin by optical trapping interferometry. We observe that in low ionic strength solutions, upon the addition of magnesium adenosine triphosphate (MgATP^2-), myosin suspensions radically change their micro-mechanics properties, generating a viscoelastic fluid characterized by a complex modulus similar to a suspension of worm-like micelles. This transduction of energy, from chemical to mechanical, may be related to the relaxed states of myosin, which regulate muscle contractility and can be involved in the etiology of many myopathies. Within an analogous generic mechanical response, cardiac and skeletal myosin suspensions provide different stress relaxation times, elastic modulus values, and characteristic lengths. These discrepancies probably rely on the dissimilar physiological functions of cardiac and skeletal muscle, on the different MgATPase hydrolysis rates of cardiac and skeletal myosins, and on the observed distinct cooperative behavior of their myosin heads in the super-relaxed state. In vitro studies like these allow us to understand the foundations of muscle cell mechanics on the micro-scale, and may contribute to the engineering of biological materials whose micro-mechanics can be activated by energy regulators.

FIG. 1.

Log–log plots of the one-dimensional mean square displacements (MSD) for melamine resin trapped beads using the weakest optical strength available, immersed in myosin water solutions with a polymer concentration of 5 mg/ml, and 10 mM MgCl₂, and (a) porcine cardiac (PC) myosin (8 curves), (b) PC myosin with 10 mM ATP (6 curves), (c) rabbit skeletal (RS) myosin (12 curves), and d) RS myosin with 10 mM ATP (10 curves). The MSDs appear dispersed because we plot jointly all the curves obtained from different trapped probes.

FIG. 2.

Log–log plots of the averaged loss (○) and elastic ( $\square$) modulus of myosin solutions with 10 mM MgCl₂ in the absence of additional ATP when using (a) porcine cardiac (PC) myosin, or (b) rabbit skeletal (RS) myosin. All data have been blocked in 10 points per decade. Shades represent the standard deviations of the mean. Black lines show the linear regressions to $G^{″}(\omega )$. Dashed lines represent $G_k^{\prime }=k/6\pi a$, where $k=7\hspace{0.17em}\mu$m is the stiffness of the optical trap.

FIG. 3.

Log–log plots of the averaged loss (○) and elastic ( $\square$) modulus of myosin solutions with 10 mM MgCl₂, 10 mM ATP, and (a) porcine cardiac (PC) myosin, or (b) rabbit skeletal (RS) myosin. All data have been blocked in ten points per decade. Shades represent the standard deviations of the mean. Black lines show the linear regression to the experimental $G^{″}(\omega )$ data. Blue squares and circles represent the theoretical complex modulus by Eq. (1).