Effect of Active Lengthening and Shortening on Small-Angle X-ray Reflections in Skinned Skeletal Muscle Fibres.

Venus Joumaa,Timothy R Leonard,Thomas C Irving,Walter Herzog,Ian C Smith,Weikang Ma,Srboljub M Mijailovich,Atsuki Fukutani

doi:10.3390/ijms22168526

Abstract

Our purpose was to use small-angle X-ray diffraction to investigate the structural changes within sarcomeres at steady-state isometric contraction following active lengthening and shortening, compared to purely isometric contractions performed at the same final lengths. We examined force, stiffness, and the 1,0 and 1,1 equatorial and M3 and M6 meridional reflections in skinned rabbit psoas bundles, at steady-state isometric contraction following active lengthening to a sarcomere length of 3.0 µm (15.4% initial bundle length at 7.7% bundle length/s), and active shortening to a sarcomere length of 2.6 µm (15.4% bundle length at 7.7% bundle length/s), and during purely isometric reference contractions at the corresponding sarcomere lengths. Compared to the reference contraction, the isometric contraction after active lengthening was associated with an increase in force (i.e., residual force enhancement) and M3 spacing, no change in stiffness and the intensity ratio I1,1/I1,0, and decreased lattice spacing and M3 intensity. Compared to the reference contraction, the isometric contraction after active shortening resulted in decreased force, stiffness, I1,1/I1,0, M3 and M6 spacings, and M3 intensity. This suggests that residual force enhancement is achieved without an increase in the proportion of attached cross-bridges, and that force depression is accompanied by a decrease in the proportion of attached cross-bridges. Furthermore, the steady-state isometric contraction following active lengthening and shortening is accompanied by an increase in cross-bridge dispersion and/or a change in the cross-bridge conformation compared to the reference contractions.

Highlights

When a skeletal muscle is actively lengthened or shortened, the resulting isometric steady-state force is frequently greater or smaller, respectively, than the purely isometric contraction performed at the final muscle length without prior lengthening or shortening
Active lengthening and shortening experiments performed in single myofibrils, in which force and individual sarcomere lengths were measured [5,6,7,20,21], have demonstrated that residual force enhancement and force depression occur in the absence of increased sarcomere length non-uniformities and are likely intra-sarcomeric properties
M3 and M6 spacings, and M3 intensity. These results suggest that residual force enhanceM3 and spacings, and M3an intensity. These results suggest that residual force enhance- and ment is M6 achieved without increase in the proportion of attached cross-bridges, ment is achieved without an increase in the proportion of attached cross-bridges, and that that force depression is accompanied by a decrease in the proportion of attached crossforce depression is accompanied by a decrease in the proportion of attached cross-bridges

Summary

Introduction

When a skeletal muscle is actively lengthened or shortened, the resulting isometric steady-state force (after the transient effects of the length change are gone) is frequently greater or smaller, respectively, than the purely isometric contraction performed at the final muscle length without prior lengthening or shortening These well-documented properties of skeletal muscle, termed residual force enhancement and force depression, respectively, have been observed consistently in muscle preparations ranging from single myofibrils to human muscles in vivo [1,2,3,4,5,6,7,8,9]. Active lengthening and shortening experiments performed in single myofibrils, in which force and individual sarcomere lengths were measured [5,6,7,20,21], have demonstrated that residual force enhancement and force depression occur in the absence of increased sarcomere length non-uniformities and are likely intra-sarcomeric properties. This result is further supported by studies that showed residual force enhancement properties in single, mechanically isolated sarcomeres [22]

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Discussion

Conclusion