X-ray diffraction study on mammalian visceral smooth muscles in resting and activated states

American Journal of Physiology-Cell Physiology

2005

111

Seow, Chun Y. Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle. Am J Physiol Cell Physiol 289: C1363-C1368, 2005; doi:10.1152/ajpcell.00329.2005.-A major development in smooth muscle research in recent years is the recognition that the myofilament lattice of the muscle is malleable. The malleability appears to stem from plastic rearrangement of contractile and cytoskeletal filaments in response to stress and strain exerted on the muscle cell, and it allows the muscle to adapt to a wide range of cell lengths and maintain optimal contractility. Although much is still poorly understood, we have begun to comprehend some of the basic mechanisms underlying the assembly and disassembly of contractile and cytoskeletal filaments in smooth muscle during the process of adaptation to large changes in cell geometry. One factor that likely facilitates the plastic length adaptation is the ability of myosin filaments to form and dissolve at the right place and the right time within the myofilament lattice. It is proposed herein that formation of myosin filaments in vivo is aided by the various filament-stabilizing proteins, such as caldesmon, and that the thick filament length is determined by the dimension of the actin filament lattice. It is still an open question as to how the dimension of the dynamic filament lattice is regulated. In light of the new perspective of malleable myofilament lattice in smooth muscle, the roles of many smooth muscle proteins could be assigned or reassigned in the context of plastic reorganization of the contractile apparatus and cytoskeleton. contraction mechanism; length adaptation; thick filament; plasticity; contractile unit THE PRIMARY FUNCTION of smooth muscle in our bodies is to control and regulate the physical dimension and mechanical function of hollow organs. The large volume change in some organs requires that smooth muscle cells lining the organ wall have a large working length range. The length range over which a striated muscle can generate maximal or near maximal force is quite limited (19), between 10% and 20% of the resting muscle length. If smooth muscle were to have the same working length range, the corresponding volume change of the smooth muscle organ would be ϳ30 -70%, which is not adequate for organ functions such as emptying a urinary bladder or pushing a fetus through the birth canal.A broad plateau in the length-force relationship can be observed in many types of smooth muscle. It has been recognized recently that the plateau can become even broader if the muscle is allowed to adapt at each of the lengths at which force measurements are made (48, 69). Different extents of length adaptation in smooth muscle can be induced, at a fixed length, by a single contraction (21, 54), a series of brief activations (48, 55), or a continuous submaximal activation (42) over a period of tens of minutes. Adaptation can also occur in a relaxed muscle set at a fixed length over a period of hours (41, 69) or days (2, 44, 74). In isolated single cells from ...

mentioning

confidence: 73%

Section: Early Observations Of Myosin Filament Evanescencementioning

confidence: 99%

Myosin filament assembly in an ever-changing myofilament lattice of smooth muscle

American Journal of Physiology-Cell Physiology

2005

111

“…Lability of myosin thick filaments has been demonstrated in some intact smooth muscle preparations (2,3,14,15), including that of airway smooth muscle (5). The labile nature can be seen in the variation of the thick filament density in cross sections of cells fixed under different experimental conditions (2,5,15).…”

Section: Discussionmentioning

confidence: 99%

“…The results suggest that in airway smooth muscle, filamentous myosins exist in equilibrium with monomeric myosins; muscle activation favors filament formation, and the resting calcium level is crucial for preservation of the filaments in the relaxed state. electron microscopy; muscle contraction; ethylene glycolbis(␤-aminoethyl ether)-N,N,NЈ,NЈ-tetraacetic acid; muscle plasticity IT HAS BEEN SUGGESTED that myosin thick filaments in relaxed smooth muscle are partially dissolved and reaggregate upon activation (2,3,14,15). Functional studies of airway smooth muscle have shown that thick filament lengthening could account for the increase in isometric force and the decrease in shortening velocity during the sustained phase of contraction (9).…”

mentioning

confidence: 99%

“…electron microscopy; muscle contraction; ethylene glycolbis(␤-aminoethyl ether)-N,N,NЈ,NЈ-tetraacetic acid; muscle plasticity IT HAS BEEN SUGGESTED that myosin thick filaments in relaxed smooth muscle are partially dissolved and reaggregate upon activation (2,3,14,15). Functional studies of airway smooth muscle have shown that thick filament lengthening could account for the increase in isometric force and the decrease in shortening velocity during the sustained phase of contraction (9).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Influence of calcium on myosin thick filament formation in intact airway smooth muscle

Herrera

Kuo

American Journal of Physiology-Cell Physiology

2002

Myosin thick filaments have been shown to be structurally labile in intact smooth muscles. Although the mechanism of thick filament assembly/disassembly for purified myosins in solution has been well described, regulation of thick filament formation in intact muscle is still poorly understood. The present study investigates the effect of resting calcium level on thick filament maintenance in intact airway smooth muscle and on thick filament formation during activation. Cross-sectional density of the thick filaments measured electron microscopically showed that the density increased substantially (144%) when the muscle was activated. The abundance of filamentous myosins in relaxed muscle was calcium sensitive; in the absence of calcium (with EGTA), the filament density deceased by 35%. Length oscillation imposed on the muscle under zero-calcium conditions produced no further reduction in the density. Isometric force and filament density recovered fully after reincubation of the muscle in normal physiological saline. The results suggest that in airway smooth muscle, filamentous myosins exist in equilibrium with monomeric myosins; muscle activation favors filament formation, and the resting calcium level is crucial for preservation of the filaments in the relaxed state. electron microscopy; muscle contraction; ethylene glycolbis(␤-aminoethyl ether)-N,N,NЈ,NЈ-tetraacetic acid; muscle plasticity IT HAS BEEN SUGGESTED that myosin thick filaments in relaxed smooth muscle are partially dissolved and reaggregate upon activation (2,3,14,15). Functional studies of airway smooth muscle have shown that thick filament lengthening could account for the increase in isometric force and the decrease in shortening velocity during the sustained phase of contraction (9). It was observed in airway smooth muscle that within at least a threefold length range and when the muscle was allowed to adapt to the lengths at which it was studied, isometric force was independent of muscle length, and shortening velocity and power output were positively correlated to muscle length (7). The observations suggest that the number of in-series contractile units (of which myosin thick filaments are an essential component) could be variable. We observed in a recent study that the thick filaments in intact airway smooth muscle dissolved partially when subjected to mechanical perturbation (5). There are, therefore, many lines of evidence supporting a notion that myosin thick filaments in smooth muscle are labile; partial disassembly/reassembly of the thick filaments could allow the muscle to quickly adapt to externally imposed mechanical strains that reshape the cell. As a first step toward understanding what regulates cellular plasticity in terms of thick filament formation, the present study was carried out to examine myosin evanescence during activation and to determine the stability of the thick filaments in relaxed airway smooth muscle depleted of calcium and subjected to mechanical perturbation. METHODS Tissue PreparationPorcine tracheal smooth musc...

Mechanical and Structural Plasticity

Comprehensive Physiology

Solway

2010

Excessive narrowing of the airways due to airway smooth muscle (ASM) contraction is a major cause of asthma exacerbation. ASM is therefore a direct target for many drugs used in asthma therapy. The contractile mechanism of smooth muscle is not entirely clear. A major advance in the field in the last decade was the recognition and appreciation of the unique properties of smooth muscle--mechanical and structural plasticity, characterized by the muscle's ability to rapidly alter the structure of its contractile apparatus and cytoskeleton and adapt to the mechanically dynamic environment of the lung. This article describes a possible mechanism for smooth muscle to adapt and function over a large length range by adding or subtracting contractile units in series spanning the cell length; it also describes a mechanism by which actin-myosin-actin connectivity might be influenced by thin and thick filament lengths, thus altering the muscle response to mechanical perturbation. The new knowledge is extremely useful for our understanding of ASM behavior in the lung and could provide new and more effective targets for drugs aimed at relaxing the muscle or keeping the muscle from excessive shortening in the asthmatic airways.