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First published online May 28, 2004
doi: 10.1242/10.1242/jcs.01136

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Requirement of ryanodine receptors for pacemaker Ca²⁺ activity in ICC and HEK293 cells

Masahiro Aoyama^1,*, Aki Yamada^4,*, Jing Wang², Susumu Ohya⁴, Shinji Furuzono⁴, Takayo Goto⁴, Shingo Hotta⁴, Yasushi Ito¹, Tatsuaki Matsubara³, Kaoru Shimokata¹, S. R. Wayne Chen⁵, Yuji Imaizumi^4, and Shinsuke Nakayama^2,

¹ Department of Physiological Medicine, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
² Department of Cell Physiology, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
³ Department of Metabolic Diseases, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan
⁴ Department of Molecular and Cellular Pharmacology, Graduate School of Pharmaceutical Sciences, Nagoya City University, Nagoya 467-8603, Japan
⁵ Department of Physiology and Biophysics, Faculty of Medicine, University of Calgary, Calgary, Alberta T2N 4N1, Canada

Authors for correspondence (e-mail: h44673a{at}nucc.cc.nagoya-u.ac.jp; yimaizum{at}phar.ngaoya-cu.ac.jp)

Accepted 2 February 2004

Intracellular Ca²⁺ ([Ca²⁺]_i) oscillations seen in interstitial cells of Cajal (ICCs) are considered to be the primary pacemaker activity in the gut. Here, we show evidence that periodic Ca²⁺ release from intracellular Ca²⁺ stores produces [Ca²⁺]_i oscillations in ICCs, using cell cluster preparations isolated from mouse ileum. The pacemaker [Ca²⁺]_i oscillations in ICCs are preserved in the presence of dihydropyridine Ca²⁺ antagonists, which suppress Ca²⁺ activity in smooth muscle cells. However, applications of drugs affecting either ryanodine receptors or inositol 1,4,5-trisphosphate receptors terminated [Ca²⁺]_i oscillations at relatively low concentrations. RT-PCR analyses revealed a predominant expression of type 3 RyR (RyR3) in isolated c-Kit-immunopositive cells (ICCs). Furthermore, we demonstrate that pacemaker-like global [Ca²⁺]_i oscillation activity is endowed by introducing RyR3 into HEK293 cells, which originally express only IP₃Rs. The reconstituted [Ca²⁺]_i oscillations in HEK293 cells possess essentially the same pharmacological characteristics as seen in ICCs. The results support the functional role of RyR3 in ICCs.

Key words: Ryanodine receptor, Pacemaker, Calcium oscillation, c-Kit-immunopositive cells, Interstitial cells of Cajal

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