Isometric and Isotonic Length‐Tension Relations and Variations in Cell Length in Longitudinal Smooth Muscle from Rabbit Urinary Bladder

Uvelius, Bengt

doi:10.1111/j.1748-1716.1976.tb10230.x

Cited by 116 publications

(95 citation statements)

References 18 publications

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“…Although there is always a danger in extrapolating interpretation on one smooth muscle type to another, it could, however, be speculated that the very long functional length range (up to 10-fold change in length) of rabbit urinary bladder muscle (18) and pedal retractor muscle of Mytilus edulis (blue mussel) (8) could be due to a similar plastic mechanism described above.…”

Section: Discussionmentioning

confidence: 99%

Structure-function correlation in airway smooth muscle adapted to different lengths

Kuo¹,

Herrera²,

Wang³

et al. 2003

American Journal of Physiology-Cell Physiology

110

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Airway smooth muscle is able to adapt and maintain a nearly constant maximal force generation over a large length range. This implies that a fixed filament lattice such as that found in striated muscle may not exist in this tissue and that plastic remodeling of its contractile and cytoskeletal filaments may be involved in the process of length adaptation that optimizes contractile filament overlap. Here, we show that isometric force produced by airway smooth muscle is independent of muscle length over a twofold length change; cell cross-sectional area was inversely proportional to cell length, implying that the cell volume was conserved at different lengths; shortening velocity and myosin filament density varied similarly to length change: increased by 69.4% Ϯ 5.7 (SE) and 76.0% Ϯ 9.8, respectively, for a 100% increase in cell length. Muscle power output, ATPase rate, and myosin filament density also have the same dependence on muscle cell length: increased by 35.4% Ϯ 6.7, 34.6% Ϯ 3.4, and 35.6% Ϯ 10.6, respectively, for a 50% increase in cell length. The data can be explained by a model in which additional contractile units containing myosin filaments are formed and placed in series with existing contractile units when the muscle is adapted at a longer length. muscle contraction; myosin filaments; ATPase activity; electron microscopy RECENT STUDIES HAVE DEMONSTRATED that the cycle of contraction and relaxation in airway smooth muscle involves polymerization and depolymerization of the actin (9, 13) and myosin (6) filaments. This lability of contractile filaments during muscle activation resembles that of nonmuscle motile cells that rely on impromptu assembly of contractile apparatus for motility. Oscillatory strains applied to single airway smooth muscle cells have revealed plastic deformation similar to that observed in soft glassy materials (3). Functional studies of airway smooth muscle indicate that the cells maintain maximal isometric force production (optimal contractile filament overlap) over a threefold length change by varying the number of contractile units in series (15). This newly emerged "plasticity" model of smooth muscle contraction is incompatible with the current concept of contraction based on the relatively restrictive model of striated muscle that possesses filament arrays in fixed lattice, which cannot accommodate large changes in cell length without compromising force production (4).The feasibility of the plasticity model can be tested experimentally based on the model predictions: the recruitment of additional contractile units in muscles adapted to longer lengths should result in an increase in thick filament content (or mass) in individual muscle cells, and as a consequence, the metabolic rate should increase with muscle length. In the present study, we tested the plasticity hypothesis through quantitative analysis of mechanical properties and ultrastructure, and measurement of the rate of ATP consumption in airway smooth muscles adapted to different lengths. MATERIALS AND METHODSMuscl...

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Section: Discussionmentioning

confidence: 99%

Structure-function correlation in airway smooth muscle adapted to different lengths

Kuo¹,

Herrera²,

Wang³

et al. 2003

American Journal of Physiology-Cell Physiology

110

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“…In a muscle that displays length adaptation of active tension, one might expect that the passive length-tension curve will also length adapt (i.e., shift along the length axis). This seems especially relevant in the urinary bladder, a hollow organ that can accommodate large volumes at low luminal pressures during filling by lengthening DSM cells over sevenfold (52), which is over twofold greater than in striated muscles (14).…”

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confidence: 99%

Evidence that actomyosin cross bridges contribute to “passive” tension in detrusor smooth muscle

Ratz

Speich

2010

American Journal of Physiology-Renal Physiology

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Ratz PH, Speich JE. Evidence that actomyosin cross bridges contribute to "passive" tension in detrusor smooth muscle. Am J Physiol Renal Physiol 298: F1424 -F1435, 2010. First published April 7, 2010 doi:10.1152/ajprenal.00635.2009.-Contraction of detrusor smooth muscle (DSM) at short muscle lengths generates a stiffness component we termed adjustable passive stiffness (APS) that is retained in tissues incubated in a Ca 2ϩ -free solution, shifts the DSM length-passive tension curve up and to the left, and is softened by muscle strain and release (strain softened). In the present study, we tested the hypothesis that APS is due to slowly cycling actomyosin cross bridges. APS and active tension produced by the stimulus, KCl, displayed similar length dependencies with identical optimum length values. The myosin II inhibitor blebbistatin relaxed active tension maintained during a KCl-induced contraction and the passive tension maintained during stress-relaxation induced by muscle stretch in a Ca 2ϩ -free solution. Passive tension was attributed to tension maintaining rather than tension developing cross bridges because tension did not recover after a rapid 10% stretch and release as it did during a KCl-induced contraction. APS generated by a KCl-induced contraction in intact tissues was preserved in tissues permeabilized with Triton X-100. Blebbistatin and the actin polymerization inhibitor latrunculin-B reduced the degree of APS generated by a KCl-induced contraction. The degree of APS generated by KCl was inhibited to a greater degree than was the peak KCl-induced tension by rhoA kinase and cyclooxygenase inhibitors. These data support the hypothesis that APS is due to slowly cycling actomyosin cross bridges and suggest that cross bridges may play a novel role in DSM that uniquely serves to ensure proper contractile function over an extreme working length range. urinary bladder; muscle mechanics; Triton X-100 permeabilization; Rho-kinase

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“…The ability of airway smooth muscle (Pratusevich et al, 1995;Gunst et al, 1995) and probably other smooth muscles (Uvelius, 1976;Gillis et al, 1988) to adapt to changes in length and maintain maximal force generation over a large length range appears to require plastic changes in subcellular structures that involves rearrangement of contractile units within the contractile apparatus and reshaping of the apparatus itself. Rearrangement of the contractile units due to length adaptation is modeled in the present study to account for the observed length-dependent changes in ultrastructure and mechanical properties.…”

mentioning

confidence: 99%

`Sarcomeres' of smooth muscle: functional characteristics and ultrastructural evidence

Herrera

McParland

Bienkowska

et al. 2005

Journal of Cell Science

103

123

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Smooth muscle cells line the walls of hollow organs and control the organ dimension and mechanical function by generating force and changing length. Although significant progress has been made in our understanding of the molecular mechanism of actomyosin interaction that produces sliding of actin (thin) and myosin (thick) filaments in smooth muscle, the sarcomeric structure akin to that in striated muscle, which allows the sliding of contractile filaments to be translated into cell shortening has yet to be elucidated. Here we show evidence from porcine airway smooth muscle that supports a model of malleable sarcomeric structure composed of contractile units assembled in series and in parallel. The geometric organization of the basic building blocks (contractile units) within the assembly and the dimension of individual contractile units can be altered when the muscle cells adapt to different lengths. These structural alterations can account for the different length-force relationships of the muscle obtained at different adapted cell lengths. The structural malleability necessary for length adaptation precludes formation of a permanent filament lattice and explains the lack of aligned filament arrays in registers, which also explains why smooth muscle is `smooth'.

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Isometric and Isotonic Length‐Tension Relations and Variations in Cell Length in Longitudinal Smooth Muscle from Rabbit Urinary Bladder

Cited by 116 publications

References 18 publications

Structure-function correlation in airway smooth muscle adapted to different lengths

Structure-function correlation in airway smooth muscle adapted to different lengths

Evidence that actomyosin cross bridges contribute to “passive” tension in detrusor smooth muscle

`Sarcomeres' of smooth muscle: functional characteristics and ultrastructural evidence

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