The Structure of Ca2+ Release Units in Arthropod Body Muscle Indicates an Indirect Mechanism for Excitation-Contraction Coupling

Abstract

The relative disposition of ryanodine receptors (RyRs) and L-type Ca(2+) channels was examined in body muscles from three arthropods. In all muscles the disposition of ryanodine receptors in the junctional gap between apposed SR and T tubule elements is highly ordered. By contrast, the junctional membrane of the T tubule is occupied by distinctive large particles that are clustered within the small junctional domain, but show no order in their arrangement. We propose that the large particles of the junctional T tubules represent L-type Ca(2+) channels involved in excitation-contraction (e-c) coupling, based on their similarity in size and location with the L-type Ca(2+) channels or dihydropyridine receptors (DHPRs) of skeletal and cardiac muscle. The random arrangement of DHPRs in arthropod body muscles indicates that there is no close link between them and RyRs. This matches the architecture of vertebrate cardiac muscle and is in keeping with the similarity in e-c coupling mechanisms in cardiac and invertebrate striated muscles.

The quantal nature of Ca 2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells

“…Instances of local Ca 2ϩ release, in the form of ''Ca 2ϩ sparks'' or their equivalents, constitute the elementary Ca 2ϩ signaling events in heart, brain, and muscle cells (6)(7)(8)(9)(10)(11)(12). Intriguingly, RyRCs in intact cells are almost exclusively found at discrete spark-generating sites, where Ϸ100 channels are assembled into two-dimensional paracrystalline arrays (13)(14)(15). This pattern of RyRC organization seems to be highly conserved from crustaceans to vertebrates (13,15,16), suggesting that array formation is critical to RyRC-mediated Ca 2ϩ signaling in vivo.…”

Reduced L-type Ca2+ current and compromised excitability induce loss of skeletal muscle function during acute cooling in locust

“…-induced Ca 2+ -release mechanism that can be inhibited by ryanodine (Huddart and Oates, 1970;Takekura and Franzini-Armstrong, 2002;Collet, 2009). Finally, the released Ca 2+ binds to regulatory proteins on the contractile filaments, facilitating contraction of the fiber.…”

“…The depolarization during the AP is known in many insect species (honey bees, Drosophila, stick insect, dragonflies, damselflies) to be generated by the activation of L-type voltagegated Ca 2+ channels and not voltage-gated Na + channels as in insect nerves or mammalian skeletal muscle. The influx of Ca 2+ through the L-type Ca 2+ channels triggers release of Ca 2+ from the sarcoplasmic reticulum through a Ca 2+ -induced Ca 2+ -release mechanism (Huddart and Oates, 1970;Ashcroft and Stanfield, 1982;Takekura and Franzini-Armstrong, 2002;Collet and Belzunces, 2007;Collet, 2009;Frolov and Singh, 2013). The repolarizing current of the AP is primarily driven by two K + currents -an early (I A ) and a delayed (I K ) outward current (Ashcroft and Stanfield, 1982;Salkoff and Wyman, 1983;Gorczynska et al, 1996).…”

Quantitative relationship between insecticidal activity and Ca2+ pump stimulation by flubendiamide and its related compounds

“…In addition to its structural and pharmacological identity, the mediation of RyRs in muscle contraction has also been established for insect RyRs. [2][3][4][5] Because of their vital role in muscle contraction, several researchers view the insect RyRs as a promising target site for potent insecticides. [6][7][8][9] Flubendiamide, a new benzenedicarboxamide compound (Table 1), is the first synthetic insecticide that controls lepidopterous pests through functional modulation of the RyR.…”