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Relationship between asynchronous Ca²⁺ waves and force development in intact smooth muscle bundles of the porcine trachea

St. Paul's Hospital, The iCAPTURE Center, University of British Columbia, Vancouver, British Columbia V6Z 1Y6, Canada

Submitted 10 February 2003 ; accepted in final form 19 August 2003

Fluctuations in intracellular calcium concentration ([Ca²⁺]_i) constitute the main link in excitation-contraction coupling (E-C coupling) in airway smooth muscle cells (ASMC). It has recently been reported that ACh induces asynchronous recurring Ca²⁺ waves in intact ASMC of murine bronchioles. With the use of a novel technique allowing us to simultaneously measure subcellular [Ca²⁺]_i and force generation in ASMC located within an intact tracheal muscle bundle, we examined a similar pattern of Ca²⁺ signaling in the trachea. We found that application of ACh resulted in the generation of recurring intracellular Ca²⁺ waves progressing along the longitudinal axis of the ribbon-shaped intact ASMC. These Ca²⁺ waves were not synchronized between neighboring cells, and induction of wave-like [Ca²⁺]_i oscillations was temporally associated with development of force by the tracheal muscle bundle. By comparing the concentration dependence of force generation and the parameters characterizing the [Ca²⁺]_i oscillations, we found that the concentration-dependent increase in ACh-induced force development by the tracheal smooth muscle bundle is achieved by differential recruitment of intact ASMC to initiate Ca²⁺ waves and by enhancement in the frequency of [Ca²⁺]_i oscillations and elevation of interspike [Ca²⁺]_i once the cells are recruited. Our findings demonstrate that asynchronous recurring Ca²⁺ waves underlie E-C coupling in ACh-induced contraction of the intact tracheal smooth muscle bundle. Furthermore, in contrast to what was reported in enzymatically dissociated ASMC, Ca²⁺ influx through the L-type voltage-gated Ca²⁺ channel was not an obligatory requirement for the generation of [Ca²⁺]_i oscillations and development of force in ACh-stimulated intact ASMC.

excitation-contraction coupling

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