Contractile filament architecture and force transmission in swine airway smooth muscle.

Kuo-Hsing Kuo,Chun Y Seow

doi:10.1242/jcs.00996

Kuo-Hsing Kuo, Chun Y Seow

Open Access

https://doi.org/10.1242/jcs.00996

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Abstract

It is well known that the cyclic interaction of myosin cross bridges with actin filaments is responsible for force and shortening generation in smooth muscle. The intracellular organization of contractile filaments, however, is still poorly understood. Here, we show electron microscopic and functional evidence that contractile filaments in airway smooth muscle lie parallel to the longitudinal axis of the cell bundle, in contrast to the obliquely arranged filaments depicted in conventional models. The parallel arrangement of contractile filaments is maintained despite the fact that individual cells are spindle-shaped. This is accomplished through filament attachment to membrane-associated dense plaques that are in turn connected to similar structures on neighboring cells. Intracellularly, the parallel arrangement is maintained despite the centrally located nucleus. This is accomplished by attachment of actin filaments to the nuclear envelope and making the nucleus a force transmitting structure. The results suggest that smooth muscle cells in tissue form a mechanical syncytium and are able to function properly only as a group.

Highlights

Force generation in smooth muscle is achieved through cyclic interaction of myosin cross bridges with actin filaments, similar to the contraction mechanism found in striated muscle (Guilford et al, 1998)
Through intercellular mechanical couplings the contractile filaments might be organized into a transcellular mechanical syncytium in which force can be generated and transmitted in contractile filaments that lie parallel to the longitudinal axis of the muscle bundle and the coincidental axis of force transmission, even at the tapered ends of the cells
To see the filament orientation with respect to the cell’s long axis, longitudinal sections were obtained; an example is shown in Fig. 2, for which a section was obtained by cutting the muscle bundle at a 15° angle to the longitudinal axis

Summary

Introduction

Force generation in smooth muscle is achieved through cyclic interaction of myosin cross bridges with actin filaments, similar to the contraction mechanism found in striated muscle (Guilford et al, 1998). The lack of precise knowledge about the contractile filament architecture within intact smooth muscle cells in tissue has hindered our efforts to understand the mechanisms and structures responsible for force transmission in situ. It has been recognized for some time that most smooth muscle cells in situ function electrically as a syncytium in a so-called ‘effector muscle bundle’ (Burnstock and Prosser, 1960; Burnstock, 1970). Through intercellular mechanical couplings (presumably intermediate junctions) the contractile filaments might be organized into a transcellular mechanical syncytium in which force can be generated and transmitted in contractile filaments that lie parallel to the longitudinal axis of the muscle bundle and the coincidental axis of force transmission, even at the tapered ends of the cells. Studies of filament organization in smooth muscle cells might be more appropriately carried out in a bundle of cells in which intercellular connections are intact

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