The active tension-length curve of vascular smooth muscle related to its cellular components

The active and passive isometric tension-length (internal circumference) relation of vascular smooth muscle has been investigated using a 100-200-micron lumen diameter artery from the rat mesenteric bed. Conditions were established under which maximal activation was obtained at all lengths. Below L0 (the length at which maximum tension, delta T0, was developed) the active tension fell with decreasing length along a line which extrapolated to 0.38 L0; below 1.1 L0 the relation was reversible regardless of the protocol used. Above L0 the active tension fell linearly with increasing length along a line which extrapolated to zero tension at 1.82 L0. At the longer lengths investigated (up to 1.6 L0) the passive tension upon which the active responses were superimposed was as high as 4.4 delta T0. However, measurements of the dynamic characteristics of the preparation (with a time resolution of 2 ms) suggest that the active tension measured is nevertheless a measure of the active properties of the contractile apparatus. Direct light microscopic observation of the effect of length change on the cells within the walls of the preparation showed that changes in vessel length produced, on average, the same percentage change in cell length. Histological examination showed no signs of cell destruction following large extensions. The results suggest that the decrease in tension with extension above L0 is due to changes in the properties of the contractile apparatus, rather than to cellular damage.

[1]  B. Bressler,et al.  Cross bridges as the major source of compliance in contracting skeletal muscle , 1975, Nature.

[2]  R. Cherniack,et al.  Oxygen, carbon dioxide, H+ ion, and bronchial length-tension relationships , 1968 .

[3]  J. Lowy,et al.  The structure of the myosin elements in vertebrate smooth muscles. , 1973, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[4]  M. Mulvany,et al.  Mechanical properties of vascular smooth muscle cells in situ , 1976, Nature.

[5]  R. Meiss.  Dynamic stiffness of rabbit mesotubarium smooth muscle: effect of isometric length. , 1978, The American journal of physiology.

[6]  A. Huxley,et al.  Mechanical Transients and the Origin of Muscular Force , 1973 .

[7]  M. Mulvany.  The undamped and damped series elastic components of a vascular smooth muscle. , 1979, Biophysical journal.

[8]  M. J. Siegman,et al.  Mechanical properties of smooth muscle. I. Length-tension and force-velocity relations. , 1971, The American journal of physiology.

[9]  A. Somlyo,et al.  The contractile apparatus of vascular smooth muscle: intermediate high voltage stereo electron microscopy. , 1975, Journal of molecular biology.

[10]  J. Lowy,et al.  Tension-length behaviour of a molluscan smooth muscle related to filament organisation. , 1978, Acta physiologica Scandinavica.

[11]  P. Dobrin,et al.  Mechanical properties of arteries , 1978, Physiological reviews.

[12]  M. Mulvany,et al.  Mechanical properties of smooth muscle cells in the walls of arterial resistance vessels. , 1978, The Journal of physiology.

[13]  J. Lowy,et al.  Mechanical properties of guinea pig taenia coli muscles. , 1973, Acta physiologica Scandinavica.

[14]  B. Uvelius.  Isometric and isotonic length-tension relations and variaitonsin cell length in longitudinal smooth muscel from rabbit urinary bladder. , 1976, Acta physiologica Scandinavica.

[15]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[16]  Stuart R. Taylor,et al.  Striated Muscle Fibers: Facilitation of Contraction at Short Lengths by Caffeine , 1971, Science.

[17]  F. Fay.  Isometric contractile properties of single isolated smooth muscle cells , 1977, Nature.

[18]  J. Peterson,et al.  Effects of initial length and active shortening on vascular smooth muscle contractility. , 1974, The American journal of physiology.

[19]  B H Bressler,et al.  The compliance of contracting skeletal muscle , 1974, The Journal of physiology.

[20]  F. Julian,et al.  Sarcomere length non-uniformity in relation to tetanic responses of stretched skeletal muscle fibres , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[21]  J. Small.  Studies on isolated smooth muscle cells: The contractile apparatus. , 1977, Journal of cell science.

[22]  R. A. Murphy,et al.  Length‐Tension Relationship of Smooth Muscle of the Hog Carotid Artery , 1973, Circulation research.

[23]  M. Mulvany,et al.  Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. , 1977, Circulation research.

[24]  R. Speden.  The effect of initial strip length on the noradrenaline‐induced contraction of arterial strips , 1960, The Journal of physiology.

[25]  J. Peterson,et al.  Relation between length, isometric force, and O2 consumption rate in vascular smooth muscle. , 1975, The American journal of physiology.

[26]  M. Mulvany,et al.  Direct Evidence that the Greater Contractility of Resistance Vessels in Spontaneously Hypertensive Rats is Associated with a Narrowed Lumen, a Thickened Media, and an Increased Number of Smooth Muscle Cell Layers , 1978, Circulation research.

[27]  F. R. Winton.  The influence of length on the responses of unstriated muscle to electrical and chemical stimulation, and stretching , 1926, The Journal of physiology.