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Originally published In Press as doi:10.1074/jbc.M106944200 on August 10, 2001

J. Biol. Chem., Vol. 276, Issue 43, 40210-40214, October 26, 2001
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RyR3 Amplifies RyR1-mediated Ca2+-induced Ca2+ Release in Neonatal Mammalian Skeletal Muscle*

Dongmei YangDagger §, Zui Pan, Hiroshi Takeshima||, Caihong Wu§, Ramakrishnan Y. Nagaraj**, Jianjie MaDagger Dagger , and Heping ChengDagger

From the Dagger  Laboratory of Cardiovascular Science, Gerontology Research Center, NIA National Institutes of Health, Baltimore, Maryland 21224, the  Department of Physiology and Biophysics, Case Western Reserve University, Cleveland, Ohio 44106, the § National Laboratory of Biomembrane and Membrane Biotechnology College of Life Sciences, Peking University, Beijing 100871, China, and the || Division of Cell Biology, Institute of Life Sciences Kurume University, Fukuoka 839-0861, Japan

The neonatal mammalian skeletal muscle contains both type 1 and type 3 ryanodine receptors (RyR1 and RyR3) located in the sarcoplasmic reticulum membrane. An allosteric interaction between RyR1 and dihydropyridine receptors located in the plasma membrane mediates voltage-induced Ca2+ release (VICR) from the sarcoplasmic reticulum. RyR3, which disappears in adult muscle, is not involved in VICR, and the role of the transiently expressed RyR3 remains elusive. Here we demonstrate that RyR1 participates in both VICR and Ca2+-induced Ca2+ release (CICR) and that RyR3 amplifies RyR1-mediated CICR in neonatal skeletal muscle. Confocal measurements of intracellular Ca2+ in primary cultured mouse skeletal myotubes reveal active sites of Ca2+ release caused by peripheral coupling between dihydropyridine receptors and RyR1. In myotubes lacking RyR3, the peripheral VICR component is unaffected, and RyR1s alone are able to support inward CICR propagation in most cells at an average speed of ~190 µm/s. With the co-presence of RyR1 and RyR3 in wild-type cells, unmitigated radial CICR propagates at 2,440 µm/s. Because neonatal skeletal muscle lacks a well developed transverse tubule system, the RyR3 reinforcement of CICR seems to ensure a robust, uniform, and synchronous activation of Ca2+ release throughout the cell body. Such functional interplay between RyR1 and RyR3 can serve important roles in Ca2+ signaling of cell differentiation and muscle contraction.

* This work was supported by National Institutes of Health extramural grants RO1-AG15556 and RO1-CA95739 (to J. M.) and intramural grants (to H. C.) and by grants from the Major State Basic Research Development Program of China (to H. C.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

** Supported by a postdoctoral fellowship from the American Heart Association.

Dagger Dagger To whom correspondence should be addressed: Dept. of Physiology and Biophysics, University of Medicine and Dentistry of New Jersey-Robert Wood Johnson Medical School, 675 Hoes Lane, Piscataway, NJ 08854. Tel.: 732-235-4550; Fax: 732-235-5038; E-mail: maj2@umdnj.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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