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J. Biol. Chem., Vol. 281, Issue 40, 30143-30151, October 6, 2006

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Excitation-Contraction Coupling in Airway Smooth Muscle^*

Wanglei Du, Timothy J. McMahon, Zhu-Shan Zhang, Jonathan A. Stiber, Gerhard Meissner^¶, and Jerry P. Eu¹

From the Division of Pulmonary, Allergy and Critical Care Medicine and Division of Cardiology, Duke University, Medical Center, Durham, North Carolina, 27710 and the ^¶Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, North Carolina 27599-7260

Excitation-contraction (EC) coupling in striated muscles is mediated by the cardiac or skeletal muscle isoform of voltage-dependent L-type Ca²⁺ channel (Ca_v1.2 and Ca_v1.1, respectively) that senses a depolarization of the cell membrane, and in response, activates its corresponding isoform of intracellular Ca²⁺ release channel/ryanodine receptor (RyR) to release stored Ca²⁺, thereby initiating muscle contraction. Specifically, in cardiac muscle following cell membrane depolarization, Ca_v1.2 activates cardiac RyR (RyR2) through an influx of extracellular Ca²⁺. In contrast, in skeletal muscle, Ca_v1.1 activates skeletal muscle RyR (RyR1) through a direct physical coupling that negates the need for extracellular Ca²⁺. Since airway smooth muscle (ASM) expresses Ca_v1.2 and all three RyR isoforms, we examined whether a cardiac muscle type of EC coupling also mediates contraction in this tissue. We found that the sustained contractions of rat ASM preparations induced by depolarization with KCl were indeed partially reversed (40%) by 200 µM ryanodine, thus indicating a functional coupling of L-type channels and RyRs in ASM. However, KCl still caused transient ASM contractions and stored Ca²⁺ release in cultured ASM cells without extracellular Ca²⁺. Further analyses of rat ASM indicated that this tissue expresses as many as four L-type channel isoforms, including Ca_v1.1. Moreover, Ca_v1.1 and RyR1 in rat ASM cells have a similar distribution near the cell membrane in rat ASM cells and thus may be directly coupled as in skeletal muscle. Collectively, our data implicate that EC-coupling mechanisms in striated muscles may also broadly transduce diverse smooth muscle functions.

Received for publication, July 10, 2006

^* This work was supported by a departmental fund and by grants from the American Lung Association (North Carolina Chapter) and the American Heart Association (Mid-Atlantic Affiliate) (to J. P. E.) and National Institutes of Health Grant AR18687 (to G. M.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Division of Pulmonary, Allergy and Critical Care Medicine, MSRB 241, Research Dr., Duke University Medical Center, Durham, NC 27710. Tel.: 919-668-3832; Fax: 919-684-3067; E-mail: eu000001{at}duke.edu.

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