Evidence for the Existence of a Minimum of Two Phases of Ordered Water in Skeletal Muscle

Hazlewood, Carlton F.; Nichols, Buford L.; Chamberlain, Nugent F.

doi:10.1038/222747a0

Cited by 312 publications

(110 citation statements)

References 14 publications

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“…The assumptions made in this paper are in accord with results of nuclear magnetic resonance measurements that indicate a reduced freedom of motion of water in muscle and an increase in freedom in contraction (9)(10)(11)(12). The theory is also in accord with my contention that muscle contraction is "contraction," that is, the shortening of elongated particles, fibers.…”

supporting

confidence: 77%

The Mechanism of Muscle Contraction

Szent‐Györgyi

1974

Proc. Natl. Acad. Sci. U.S.A.

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Muscular contraction is essentially the shortening of the S2 subunits of heavy meromyosin, integrated to macroscopic motion by the thick and thin filaments.According to our present knowledge the main contractile proteins of muscle are myosin and actin which, in vitro, form the complex actomyosin (AM). The actin filaments, in muscle, have attached to them tropomyosin and troponin. The slender myosin molecule is about 1400 A long and is built of two fragments, the "light" and "heavy" meromyosin (LMM and HMM). The latter consists of a long and thin "stalk" (subfragment 2, S2) and a globular "head" (subfragment 1, Si). The HMM S2 is actually a double spiral of two polypeptide fibers attached at one end to the LMM, each peptide carrying a globule, SIat the other (1).AM is strongly hydrophilic. Threads prepared from it contain 97% water. At a proper ionic concentration its micelles show two major changes under influence of ATP: they contract and become completely hydrophobic, anhydrous. Thus, under influence of ATP, suspensions of AM "superprecipitate," while threads contract. If the micelles within the threads have a random orientation, then their contraction causes the thread to contract in all directions, that is, shrink, become shorter and thinner. If the micelles are arranged parallel to the axis, then, under influence of ATP, the threads become shorter and thicker without losing volume, behaving thus similarly to contracting muscle.There are reasons to believe that these changes, shortening and dehydration, reflect the elementary changes taking place in contracting muscle. The analogy between muscle and AM was brought still closer by the development of glycerination and the introduction of the psoas fiber (2), and the demonstration that rigor mortis is essentially a lack of ATP (3). It was natural to expect that muscle would be found to be a bundle of AM threads built of micelles, ordered parallel to the axis.It came as a shock when the electron microscope revealed muscle to consist of "thick" myosin and "thin" actin filaments, which did not shorten on contraction, but only slid alongside one another. Initially no connection was seen between the two. Later, H. E. Huxley (4) showed them to be connected by "bridges." It is generally believed that these bridges are the HMM S2-s of the myosin molecules, which attach themselves, in contracting muscle, to the "actin" of the thin filaments. H. E. Huxley believes that the sliding and In all these studies the hydration and dehydration were completely disregarded. The first question on this line has to be: which of the components of muscle is responsible for the binding and release of the great quantities of water? Actin cannot be, because very little actin is needed to make AM hydrate and dehydrate under influence of ATP. Nor can LMM be made responsible, because it does not interact with actin or ATP, and it is this interaction that induces the changes in hydration. This leaves us with HMM, and within the HMM only the helical HMM S2 could be expected to bind a gr...

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supporting

confidence: 77%

The Mechanism of Muscle Contraction

Szent‐Györgyi

1974

Proc. Natl. Acad. Sci. U.S.A.

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“…The agarose gel network is built from fibrils, formed by lateral aggregation of six or more double helices (13). The dramatic broadening of the water-1 H resonance upon gelation of agarose was originally attributed to extensive perturbations of bulk water (14), and similar ideas regarding longrange ordering and slowing down of water motions have been invoked to explain water-1 H and 2 H relaxation enhancements in biological tissue (15,16). Subsequent more systematic studies attributed the relaxation enhancement to a small fraction of "bound" water molecules or exchanging hydroxyl protons (17,18).…”

mentioning

confidence: 99%

Molecular basis of water proton relaxation in gels and tissue

Chávez

Halle

2006

Magnetic Resonance in Med

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An extensive set of water-1 H magnetic relaxation dispersion (MRD) data are presented for aqueous agarose and gelatin gels. It is demonstrated that the EMOR model, which was developed in a companion paper to this study (see Halle, this issue), accounts for the dependence of the water-1 H spin-lattice relaxation rate on resonance frequency over more than four decades and on pH. The parameter values deduced from analysis of the 1 H MRD data are consistent with values derived from 2 H MRD profiles from the same gels and with small-molecule reference data. This agreement indicates that the water-1 H relaxation dispersion in aqueous biopolymer gels is produced directly by exchange-mediated orientational randomization of internal water molecules or labile biopolymer protons, with little or no role played by collective biopolymer vibrations or coherent spin diffusion. This ubiquitous mechanism is proposed to be the principal source of water-1 H spin-lattice relaxation at low magnetic fields in all aqueous systems with rotationally immobile biopolymers, including biological tissue. The same mechanism also contributes to transverse and rotating-frame relaxation and magnetization transfer at high fields. Intrinsic contrast in magnetic resonance images of soft tissue is generated largely by spatial variations in spin relaxation rates. Whereas the phenomenology of water-1 H relaxation in tissue is well documented (1-3), the underlying molecular mechanism remains controversial (4 -9). The task of elucidating the relaxation mechanism is complicated by incomplete knowledge about the chemical composition and supramolecular structure of most tissues. In addition, it is usually not possible to vary biopolymer composition, pH, or temperature in a controlled way while maintaining the integrity of the tissue. For these reasons, most mechanistic studies have been carried out on model systems, such as aqueous biopolymer gels, with relaxation characteristics similar to those of tissue. Here we report an extensive set of water-1 H relaxation data from two widely used tissue models: aqueous gels of agarose and gelatin.Detailed information about relaxation mechanisms in complex systems can be obtained from the magnetic relaxation dispersion (MRD) profile, that is, the field/frequency dependence of the spin-lattice relaxation rate, R 1 ϭ 1/T 1 . Ideally, the dispersion profile should be recorded from typical MRI frequencies of order 100 MHz down to the kHz range. The water-1 H MRD profiles reported here cover more than four frequency decades. The strong frequency dependence of R 1 at low fields, which is the focus of the present study, can be used to enhance image contrast in prepolarized MRI experiments (10). The low-field R 1 dispersion also yields information about the zero-frequency dipolar contributions to transverse relaxation and steadystate magnetization transfer and to the low-frequency dipolar contribution to rotating-frame spin-lattice relaxation.Agarose is a linear polysaccharide with a disaccharide repeat (agarobiose) composed...

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“…The few experimental techniques that can monitor the molecular properties of water in vivo have suffered from interpretational ambiguities, allowing widely discordant views about cell water structure and dynamics to coexist for a long time (5)(6)(7). NMR spectroscopy can provide information about cell water via the spin relaxation times of the dominant water-1 H signal (8,9). In fact, tissue-specific variations in water relaxation times provided the impetus for developing magnetic resonance imaging (10).…”

mentioning

confidence: 99%

Cell water dynamics on multiple time scales

Persson

Halle

2008

Proc. Natl. Acad. Sci. U.S.A.

186

165

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Water-biomolecule interactions have been extensively studied in dilute solutions, crystals, and rehydrated powders, but none of these model systems may capture the behavior of water in the highly organized intracellular milieu. Because of the experimental difficulty of selectively probing the structure and dynamics of water in intact cells, radically different views about the properties of cell water have proliferated. To resolve this long-standing controversy, we have measured the 2 H spin relaxation rate in living bacteria cultured in D2O. The relaxation data, acquired in a wide magnetic field range (0.2 mT-12 T) and analyzed in a modelindependent way, reveal water dynamics on a wide range of time scales. Contradicting the view that a substantial fraction of cell water is strongly perturbed, we find that Ϸ85% of cell water in Escherichia coli and in the extreme halophile Haloarcula marismortui has bulk-like dynamics. The remaining Ϸ15% of cell water interacts directly with biomolecular surfaces and is motionally retarded by a factor 15 ؎ 3 on average, corresponding to a rotational correlation time of 27 ps. This dynamic perturbation is three times larger than for small monomeric proteins in solution, a difference we attribute to secluded surface hydration sites in supramolecular assemblies. The relaxation data also show that a small fraction (Ϸ0.1%) of cell water exchanges from buried hydration sites on the microsecond time scale, consistent with the current understanding of protein hydration in solutions and crystals. biomolecular hydration ͉ buried water molecules ͉ Escherichia coli ͉ Haloarcula marismortui ͉ in vivo NMR W ater, the ubiquitous biosolvent, mediates or modulates the intermolecular forces that govern the self-assembly of biological cells, it controls the rates of substrate diffusion and conformational transitions, and it participates in molecular recognition and enzyme catalysis (1-4). It is therefore imperative to characterize and understand any differences between cell water and bulk water. Biopolymers and other solutes make up one-third of the mass of a typical cell, so this difference could be substantial. The few experimental techniques that can monitor the molecular properties of water in vivo have suffered from interpretational ambiguities, allowing widely discordant views about cell water structure and dynamics to coexist for a long time (5-7). NMR spectroscopy can provide information about cell water via the spin relaxation times of the dominant water-1 H signal (8, 9). In fact, tissue-specific variations in water relaxation times provided the impetus for developing magnetic resonance imaging (10). Unfortunately, the interpretation of water-1 H relaxation data from biological samples is confounded by crossrelaxation, intermolecular paramagnetic couplings, and protonexchange modulation of the nuclear shielding (11,12). Here, we circumvent these complications by measuring the relaxation rate of the longitudinal water-2 H magnetization from cells cultured in D 2 O. We have chosen to study...

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Evidence for the Existence of a Minimum of Two Phases of Ordered Water in Skeletal Muscle

Cited by 312 publications

References 14 publications

The Mechanism of Muscle Contraction

The Mechanism of Muscle Contraction

Molecular basis of water proton relaxation in gels and tissue

Cell water dynamics on multiple time scales

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