Peptide-induced Ca(2+) movements in a tonic insect muscle: effects of proctolin and periviscerokinin-2.
Although most of the characterized insect neuropeptides have been detected by their actions on muscle contractions, not much is known about the mechanisms underlying excitation-contraction coupling. Thus we initiated a pharmacological study on the myotropic action of the peptides periviscerokinin-2 (PVK-2) and proctolin on the hyperneural muscle of the cockroach Periplaneta americana. Both peptides required extracellular Ca(2+) to induce muscle contraction, and a blockage of sarcolemmal Ca(2+) channels by Mn(2+) or La(3+) inhibited myotropic effects. The peptides were able to induce contractions in dependence on the extracellular Ca(2+) concentration in muscles depolarized with high K(+) saline. A reduction of extracellular Na(+), K(+), or Cl(-) did not effect peptide action. Nifedipine, an L-type Ca(2+)-channel blocker, partially blocked the response to both peptides but to a much lesser extent than contractions evoked by elevated K(+). Using calcium imaging with fluo-3, we show that proctolin induces an increase of the intracellular Ca(2+) concentration. In calcium-free saline, no increase of the intracellular Ca(2+) concentration could be detected. The inhibiting effect of ryanodine, thapsigargin, and TMB-8 on peptide-induced contractions suggests that Ca(2+) release from the sarcoplasmic reticulum plays a major role during peptide-induced contractions. Preliminary experiments suggest that the peptides do not employ cyclic nucleotides as second messengers, but may activate protein kinase C. Our results indicate that the peptides induce Ca(2+) influx by an activation or modulation of dihydropyridine-sensitive and voltage-independent sarcolemmal Ca(2+) channels. Ca(2+)-induced Ca(2+) release from intracellular stores, but not inositol trisphosphate-induced Ca(2+) release, seems to account for most of the observed increase in intracellular Ca(2+). Additionally, both peptides were able to potentiate glutamate-induced contractions at threshold concentrations.
Wegener
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Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden.
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D000818:Animals; D002118:Calcium / Q000378:metabolism* / Q000494:pharmacology; D002121:Calcium Channel Blockers / Q000494:pharmacology; D002712:Chlorides / Q000378:metabolism; D005110:Extracellular Space / Q000378:metabolism; D018698:Glutamic Acid / Q000378:metabolism / Q000494:pharmacology; D066298:In Vitro Techniques; D007811:Lanthanum / Q000494:pharmacology; D008345:Manganese / Q000494:pharmacology; D009119:Muscle Contraction / Q000187:drug effects / Q000502:physiology; D009129:Muscle Tonus / Q000187:drug effects / Q000502:physiology*; D009132:Muscles / Q000187:drug effects / Q000378:metabolism*; D009479:Neuropeptides / Q000302:isolation & purification / Q000378:metabolism* / Q000494:pharmacology; D018377:Neurotransmitter Agents / Q000378:metabolism* / Q000494:pharmacology; D009712:Nucleotides, Cyclic / Q000378:metabolism; D009842:Oligopeptides / Q000378:metabolism* / Q000494:pharmacology; D010526:Periplaneta; D011188:Potassium / Q000378:metabolism; D026902:Potassium Channel Blockers; D019837:Ryanodine Receptor Calcium Release Channel / Q000378:metabolism; D012508:Sarcolemma / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects / Q000502:physiology; D012964:Sodium / Q000378:metabolism; D019831:Sodium-Calcium Exchanger / Q000378:metabolism; D010738:Type C Phospholipases / Q000378:metabolism
D002121:Calcium Channel Blockers; D002712:Chlorides; D009479:Neuropeptides; D018377:Neurotransmitter Agents; D009712:Nucleotides, Cyclic; D009842:Oligopeptides; D026902:Potassium Channel Blockers; D019837:Ryanodine Receptor Calcium Release Channel; D019831:Sodium-Calcium Exchanger; C417775:periviscerokinin-2; D018698:Glutamic Acid; D008345:Manganese; C011536:proctolin; D007811:Lanthanum; D012964:Sodium; D010738:Type C Phospholipases; D011188:Potassium; D002118:Calcium