IP₃-induced tension and IP₃-receptor expression in rat soleus muscle during postnatal development

Abstract

Talon, Sophie, Olivier Vallot, Corinne Huchet-Cadiou, Anne-Marie Lompré , and Claude Lé oty. IP3-induced tension and IP3-receptor expression in rat soleus muscle during postnatal development. Am J Physiol Regulatory Integrative Comp Physiol 282: R1164-R1173, 2002; 10.1152/ ajpregu.00073.2001.-The present study was designed to examine whether changes in Ca 2ϩ release by inositol-1,4,5-trisphosphate (IP 3) in 8-, 15-, and 30-day-old rat skeletal muscles could be associated with the expression of IP 3 receptors. Experiments were conducted in slow-twitch muscle in which both IP3-induced Ca 2ϩ release and IP3-receptor (IP3R) expression have been shown to be larger than in fast-twitch muscle. In saponin-skinned fibers, IP3 induced transient contractile responses in which the amplitude was dependent on the Ca 2ϩ -loading period with the maximal IP3 contracture being at 20 min of loading. The IP3 tension decreased during postnatal development, was partially inhibited by ryanodine (100 M), and was blocked by heparin (20-400 g/ml). Amplification of the DNA sequence encoding for IP3R isoforms (using the RT-PCR technique) showed that in slow-twitch muscle, the type 2 isoform is mainly expressed, and its level decreases during postnatal development in parallel with changes in IP3 responses in immature fibers. IP3-induced Ca 2ϩ release would then have greater participation in excitation-contraction coupling in developing fibers than in mature muscle. sarcoplasmic reticulum Ca 2ϩ release; inositol-1,4,5-trisphosphate; skinned slow-twitch fibers; mammalian muscles INCREASED INTRACELLULAR CA 2ϩ activity is an important factor in the contractile process of skeletal muscle, because Ca 2ϩ binds to contractile proteins and triggers contraction. In adult skeletal muscle, the major pathway for increasing intracellular Ca 2ϩ is the depolarization of transverse tubular system membranes, which induces the release of Ca 2ϩ from the sarcoplasmic reticulum by opening Ca 2ϩ channels/ryanodine receptors (RyR; see Ref. 8). The most accepted hypothesis for the coupling of Ca 2ϩ release and the contractile responses to excitation in skeletal muscle is a direct interaction between the "voltage sensor" dihydropyridine receptor of tubular membranes and the RyR of sarcoplasmic reticulum (15,35). It has also been suggested that an intracellular messenger, inositol-1,4,5-trisphosphate (IP 3 ), contributes to excitation-contraction coupling in skeletal muscle (44,45). Such chemical coupling is well established in smooth muscle (2, 39), but its role in skeletal muscle remains controversial. Although Posterino and Lamb (33) found that application of IP 3 failed to produce contractile force in fibers in which excitation-contraction coupling was functional, Lopez and Parra (25) have shown that local contraction can be induced by microinjection of IP 3 into intact skeletal fibers. Furthermore, recent experiments conducted on skinned skeletal muscle fibers have shown that IP 3 induces contractile responses (41, 42), which suggests that IP 3 may play a role...

Inositol Trisphosphate Receptor Ca2+Release Channels

“…The three channel isoforms have distinct and overlapping patterns of expression, with most cells outside the central nervous system expressing more than one type (68,104,105,340,345,418,451,460,493). InsP 3 R isoform expression levels can be modified during development and differentiation (129,242,340,394,419,450,460) and in response to various normal and pathological stimuli (20,61,70,218,226,250,305,403,418,460,502,526). Furthermore, InsP 3 R protein expression levels can be downregulated by a use-dependent mechanism that involves InsP 3 -and Ca 2ϩ -dependent channel ubiquitination, and subsequent degradation involving the proteasome (9,10,35,515).…”

No evidence for inositol 1,4,5-trisphosphate–dependent Ca2+ release in isolated fibers of adult mouse skeletal muscle

“…Most available data support the existence of a functional IP 3 -IP 3 R system in cultured skeletal muscle cells, and it has been suggested that IP 3 Rs regulate Ca 2+dependent gene transcription in these cells (Powell et al, 2001;Stiber et al, 2005). In cultured mouse muscle cells, high potassium-induced depolarization was reported to induce, in addition to the fast Ca 2+ transients associated with EC coupling, a slower calcium wave, mostly confined to the nuclear and perinuclear regions that were larger in slow compared with fast muscles but decreased during postnatal development (Talon et al, 1999(Talon et al, , 2002. On the contrary, muscle fibers isolated from the fast flexor digitorum brevis (FDB) but not from slow soleus muscle of young adult (5-7-wk-old) mice were found to respond to electrical stimulation with a fast calcium signal associated with muscle contraction, followed by a slower signal, which was inhibited by the IP 3 R inhibitors xestospongin B or C (Casas et al, 2010).…”