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Mechanical and Structural Plasticity

Chun Y. Seow, Julian Solway

10.1002/cphy.c100024

Source: Volume 1, Issue 1, January 2011

Published online: November 2010

Full Article on Wiley Online Library



Abstract

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. © 2011 American Physiological Society. Compr Physiol 1:283‐293, 2011.

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Figure 1. Figure 1.

Length‐force relationship of tracheal smooth muscle (black circles and fitted line) superimposed on the same relationship of striated muscle (gray). Smooth muscle data replotted from Herrera et al. 27. The in situ length of the smooth muscle was taken as a reference length (Lref); the muscle was fully adapted at Lref before other forces at different length were measured. The force values were normalized to the maximal isometric force (Fmax) produced at Lref.
Figure 2. Figure 2.

Schematics illustrating the structure of a smooth muscle contractile unit and the predicted relationship between length and force based on the assumption that the extent of overlap between thick and thin filaments determines the amount of force produced. (A) A contractile unit consists of a thick filament sandwiched by two thin filaments of opposite polarity; the thin filaments are anchored by Z‐disk equivalent bodies (Z bodies) that define the boundary of a contractile unit. The thick filaments are assumed to be side polar and do not possess a central bare (cross‐bridge free) zone. (B) Illustration of diminishing overlap (black portion of the thick filament) between the thick and thin filaments as the muscle shortens. (C) Because the active force produced by the muscle is assumed to be directly proportional to the extent of filament overlap, and that the extent of overlap is directly proportional to the amount of shortening (or muscle length), the model predicts that the force‐length relationship is linear.
Figure 3. Figure 3.

Length‐force relationship of tracheal smooth muscle. In the absence of length adaptation, the final length the muscle shortens to is independent of the initial muscle length. A quick stretch of 10% (red) and 30% (blue) from Lref increases the amount of shortening but does not alter the final shortened length. In this test, a load equivalent to 30% Fmax was used in the isotonic contractions. Modified from Herrera et al. 27.
Figure 4. Figure 4.

Length‐force relationship of tracheal smooth muscle at different adapted lengths. The curve in the middle is the same as that shown in Figure 1 and is obtained after the muscle has been adapted to Lref. The curve to the right of this reference curve is obtained from the same muscle after it has been stretched to 1.5 Lref and fully adapted to the stretched length. Full adaptation is indicated by full recovery of isometric force to the level before length change. The curve to the left of the reference curve is obtained after the muscle has been shortened to 0.75 Lref and fully adapted to the shortened length.

Modified from Herrera et al. 27
Figure 5. Figure 5.

Schematic of shifts in length vs. passive tension relationship in smooth muscle. The reference curve is plotted in black, representing the relationship obtained from a muscle adapted to Lref. By adapting the same muscle at a shorter (red dotted line) or longer (blue dotted line) length, the curve can be shifted to the left (red) or right (blue) with respective to the reference curve (black).
Figure 6. Figure 6.

Force‐velocity and force‐power relationships in airway smooth muscle adapted to long (1.5 Lref) and short (0.75 Lref) lengths. Circles on the hyperbolic force‐velocity curves are experiment data from Herrera et al. 27. The power curves are obtained from the velocity curves based on the relationship: Power = force × velocity.
Figure 7. Figure 7.

Linear relationships between muscle length and shortening velocity, and between muscle length and power output. Data from Kuo et al. 33. Black line: a linear fit to combined data of velocity and power. Reference velocity and power are values obtained at Lref.
Figure 8. Figure 8.

Schematic of a smooth muscle cell adapted to two lengths, Lref and 2 × Lref. Doubling the length causes the number of contractile units to increase by two‐third, approximately matching the data presented in Figure 7. The thick filaments are assumed to be side polar and do not possess a central bare (cross‐bridge free) zone. The Z‐bodies are assumed to serve the same function as the Z‐disks in striated muscle.
Figure 9. Figure 9.

Cartoon illustration of thick filament (red) distribution inside smooth muscle cells adapted at different lengths. Black arrows indicate transverse cuts across the cells. Assuming that the cell volume is constant at different cell lengths and that the thick filaments are evenly distributed, the thick filament density measured in transverse sections (blue circles) should reflect the thick filament mass inside the cell. In this illustration, it is assumed that the thick filament number remains constant at any cell length.
Figure 10. Figure 10.

Linear relationships between muscle length and metabolic rate (rate of ATP utilization) and between muscle length and myosin (thick) filament mass. Data from Kuo et al. 33. Data for metabolic rate are available only for lengths at 1.0 and 1.5 Lref. The black line is not a linear best fit for the data on this figure but replotted from Figure 7.
Figure 11. Figure 11.

Force fluctuations promote relengthening of acetylcholine (ACh)‐contracted canine tracheal smooth muscle but have little effect on initial shortening. In this experiment, Dowell et al. 11 contracted canine trachealis first against a fixed load of 32% of maximal active force (by exposure to high concentration of [ACh]) and then again against an oscillating load with the same mean value (32% + 16% Fmax). Initial shortening was similar in both instances, but subsequent relengthening was markedly accentuated by the force fluctuations.

Adapted from Dowell et al. 11
Figure 12. Figure 12.

Force fluctuations promote relengthening of acetylcholine (ACh)‐contracted bovine tracheal smooth muscle in a fluctuation magnitude‐dependent fashion, and p38 MAPK inhibition potentiates force fluctuation‐induced relengthening. In this experiment, Lakser et al. 35 exposed bovine trachealis in “control” experiments against a fixed load of 32% of maximal active force (by exposure to high concentration of [ACh]) and then superimposed progressively increasing force fluctuations and found fluctuation magnitude‐dependent relengthening, which was potentiated in the presence of a p38 MAPK inhibitor. Relengthening was maintained even after reducing the magnitude of force fluctuations (dotted lines) to 8% Fmax from their greatest intensity (32% Fmax), suggesting that a plastic reconfiguration of the contractile apparatus had occurred. Additional experiments (not shown here) demonstrated that p38 MAPK is active in the “control” condition.

Adapted from Lakser et al. 35
Figure 13. Figure 13.

Conceptual model illustrating a hypothesized interaction between actin (thin) filament length and influence of a stretch of contracted airway smooth muscle. Stretching of smooth muscle with short actin filaments (upper panel) could break the connections between actin filaments by interposed myosin (thick) filaments; for contraction to occur subsequently, the actin and myosin filaments would have to undergo plastic rearrangement from a parallel to a series configuration, which while longer would generate less force. In contrast, stretching of smooth muscle with long actin filaments (lower panel) might not break the connections between actin filaments through myosin filaments. In this circumstance, stretching the muscle does not result in plastic elongation.

Adapted from Dulin et al. 13
Figure 14. Figure 14.

Force‐fluctuation‐induced relengthening of airway smooth muscle before and during exposure to latrunculin B (LatB). In this experiment, Dowell et al. 11 contracted canine trachealis against a fixed load of 32% of maximal active force (by exposure to high concentration of acetylcholine [ACh]) and then without delay superimposed load oscillations around the same mean value (32% ± 16% Fmax), thereby inducing relengthening of the still contracting muscle strip. Incubation with latrunculin B had little effect on initial shortening against a fixed load but markedly potentiated force fluctuation‐induced relengthening.

Adapted from Dowell et al. 11
Figure 15. Figure 15.

Markedly different initial responses to force fluctuation in acetylcholine (Ach)‐contracted vs. KCl‐contracted canine trachealis strips. Acetylcholine‐contracted airway smooth muscle strips exhibit only minor immediate relengthening upon initiation of force fluctuations, whereas KCl‐contracted strips relengthen very rapidly.

Adapted from Lavoie et al. 37


Figure 1.

Length‐force relationship of tracheal smooth muscle (black circles and fitted line) superimposed on the same relationship of striated muscle (gray). Smooth muscle data replotted from Herrera et al. 27. The in situ length of the smooth muscle was taken as a reference length (Lref); the muscle was fully adapted at Lref before other forces at different length were measured. The force values were normalized to the maximal isometric force (Fmax) produced at Lref.



Figure 2.

Schematics illustrating the structure of a smooth muscle contractile unit and the predicted relationship between length and force based on the assumption that the extent of overlap between thick and thin filaments determines the amount of force produced. (A) A contractile unit consists of a thick filament sandwiched by two thin filaments of opposite polarity; the thin filaments are anchored by Z‐disk equivalent bodies (Z bodies) that define the boundary of a contractile unit. The thick filaments are assumed to be side polar and do not possess a central bare (cross‐bridge free) zone. (B) Illustration of diminishing overlap (black portion of the thick filament) between the thick and thin filaments as the muscle shortens. (C) Because the active force produced by the muscle is assumed to be directly proportional to the extent of filament overlap, and that the extent of overlap is directly proportional to the amount of shortening (or muscle length), the model predicts that the force‐length relationship is linear.



Figure 3.

Length‐force relationship of tracheal smooth muscle. In the absence of length adaptation, the final length the muscle shortens to is independent of the initial muscle length. A quick stretch of 10% (red) and 30% (blue) from Lref increases the amount of shortening but does not alter the final shortened length. In this test, a load equivalent to 30% Fmax was used in the isotonic contractions. Modified from Herrera et al. 27.



Figure 4.

Length‐force relationship of tracheal smooth muscle at different adapted lengths. The curve in the middle is the same as that shown in Figure 1 and is obtained after the muscle has been adapted to Lref. The curve to the right of this reference curve is obtained from the same muscle after it has been stretched to 1.5 Lref and fully adapted to the stretched length. Full adaptation is indicated by full recovery of isometric force to the level before length change. The curve to the left of the reference curve is obtained after the muscle has been shortened to 0.75 Lref and fully adapted to the shortened length.

Modified from Herrera et al. 27


Figure 5.

Schematic of shifts in length vs. passive tension relationship in smooth muscle. The reference curve is plotted in black, representing the relationship obtained from a muscle adapted to Lref. By adapting the same muscle at a shorter (red dotted line) or longer (blue dotted line) length, the curve can be shifted to the left (red) or right (blue) with respective to the reference curve (black).



Figure 6.

Force‐velocity and force‐power relationships in airway smooth muscle adapted to long (1.5 Lref) and short (0.75 Lref) lengths. Circles on the hyperbolic force‐velocity curves are experiment data from Herrera et al. 27. The power curves are obtained from the velocity curves based on the relationship: Power = force × velocity.



Figure 7.

Linear relationships between muscle length and shortening velocity, and between muscle length and power output. Data from Kuo et al. 33. Black line: a linear fit to combined data of velocity and power. Reference velocity and power are values obtained at Lref.



Figure 8.

Schematic of a smooth muscle cell adapted to two lengths, Lref and 2 × Lref. Doubling the length causes the number of contractile units to increase by two‐third, approximately matching the data presented in Figure 7. The thick filaments are assumed to be side polar and do not possess a central bare (cross‐bridge free) zone. The Z‐bodies are assumed to serve the same function as the Z‐disks in striated muscle.



Figure 9.

Cartoon illustration of thick filament (red) distribution inside smooth muscle cells adapted at different lengths. Black arrows indicate transverse cuts across the cells. Assuming that the cell volume is constant at different cell lengths and that the thick filaments are evenly distributed, the thick filament density measured in transverse sections (blue circles) should reflect the thick filament mass inside the cell. In this illustration, it is assumed that the thick filament number remains constant at any cell length.



Figure 10.

Linear relationships between muscle length and metabolic rate (rate of ATP utilization) and between muscle length and myosin (thick) filament mass. Data from Kuo et al. 33. Data for metabolic rate are available only for lengths at 1.0 and 1.5 Lref. The black line is not a linear best fit for the data on this figure but replotted from Figure 7.



Figure 11.

Force fluctuations promote relengthening of acetylcholine (ACh)‐contracted canine tracheal smooth muscle but have little effect on initial shortening. In this experiment, Dowell et al. 11 contracted canine trachealis first against a fixed load of 32% of maximal active force (by exposure to high concentration of [ACh]) and then again against an oscillating load with the same mean value (32% + 16% Fmax). Initial shortening was similar in both instances, but subsequent relengthening was markedly accentuated by the force fluctuations.

Adapted from Dowell et al. 11


Figure 12.

Force fluctuations promote relengthening of acetylcholine (ACh)‐contracted bovine tracheal smooth muscle in a fluctuation magnitude‐dependent fashion, and p38 MAPK inhibition potentiates force fluctuation‐induced relengthening. In this experiment, Lakser et al. 35 exposed bovine trachealis in “control” experiments against a fixed load of 32% of maximal active force (by exposure to high concentration of [ACh]) and then superimposed progressively increasing force fluctuations and found fluctuation magnitude‐dependent relengthening, which was potentiated in the presence of a p38 MAPK inhibitor. Relengthening was maintained even after reducing the magnitude of force fluctuations (dotted lines) to 8% Fmax from their greatest intensity (32% Fmax), suggesting that a plastic reconfiguration of the contractile apparatus had occurred. Additional experiments (not shown here) demonstrated that p38 MAPK is active in the “control” condition.

Adapted from Lakser et al. 35


Figure 13.

Conceptual model illustrating a hypothesized interaction between actin (thin) filament length and influence of a stretch of contracted airway smooth muscle. Stretching of smooth muscle with short actin filaments (upper panel) could break the connections between actin filaments by interposed myosin (thick) filaments; for contraction to occur subsequently, the actin and myosin filaments would have to undergo plastic rearrangement from a parallel to a series configuration, which while longer would generate less force. In contrast, stretching of smooth muscle with long actin filaments (lower panel) might not break the connections between actin filaments through myosin filaments. In this circumstance, stretching the muscle does not result in plastic elongation.

Adapted from Dulin et al. 13


Figure 14.

Force‐fluctuation‐induced relengthening of airway smooth muscle before and during exposure to latrunculin B (LatB). In this experiment, Dowell et al. 11 contracted canine trachealis against a fixed load of 32% of maximal active force (by exposure to high concentration of acetylcholine [ACh]) and then without delay superimposed load oscillations around the same mean value (32% ± 16% Fmax), thereby inducing relengthening of the still contracting muscle strip. Incubation with latrunculin B had little effect on initial shortening against a fixed load but markedly potentiated force fluctuation‐induced relengthening.

Adapted from Dowell et al. 11


Figure 15.

Markedly different initial responses to force fluctuation in acetylcholine (Ach)‐contracted vs. KCl‐contracted canine trachealis strips. Acetylcholine‐contracted airway smooth muscle strips exhibit only minor immediate relengthening upon initiation of force fluctuations, whereas KCl‐contracted strips relengthen very rapidly.

Adapted from Lavoie et al. 37
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Article Title: Mechanical and Structural Plasticity
 

How to Cite

Chun Y. Seow, Julian Solway. Mechanical and Structural Plasticity. Compr Physiol 2010, 1: 283-293. doi: 10.1002/cphy.c100024