Abstract
Spontaneous transient inward currents (STICs) were recorded in canine and guinea-pig tracheal myocytes held at negative membrane potentials. STICs were Cl− selective since their reversal potential was dependent on the Cl− gradient and they were blocked by the Cl− channel blocker niflumic acid. STICs were insensitive to Cs+, charybdotoxin, and nifedipine. Ca2+-activated K+ currents often preceded STICs, suggesting that the STICs are Ca2+ dependent. In support of this suggestion, we found the Cl− currents were: (1) abolished by depleting intracellular Ca2+ stores using caffeine, acetylcholine, histamine, or substance P; (2) enhanced by increasing external concentrations of Ca2+; (3) evoked by voltage-dependent Ca2+ influx. The channels responsible for this Cl− current are of small unitary conductance (<20 pS). Decay of the STICs was described by a single exponential with a time constant of 94±9 ms at −70 mV; the time constant increased considerably at more positive potentials. Using Ca2+-dependent Cl− currents and contractions as indices of internal levels of Ca2+, we found that isolated tracheal cells are capable of exhibiting rhythmic behaviour: bursts of currents and contractions with a periodicity of less than 0.1 Hz and which continued for more than 20 min. These rhythmic events were recorded at negative membrane potentials, suggesting that cyclical release of internally sequestered Ca2+ is responsible. We conclude that spontaneous release of Ca2+ from intracellular stores in tracheal muscle cells leads to transient currents in some cases accompanied by rhythmic contractions. Our studies provide evidence for a cellular mechanism that could underly myogenic oscillations of membrane potential in smooth muscle.
Similar content being viewed by others
References
Amédée T, Large WA, Wang Q (1990) Characteristics of chloride currents activated by noradrenaline in rabbit ear artery cells. J Physiol (Lond) 428:501–516
Arkett SA, Dixon SJ, Sims SM (1992) Substrate influences rat osteoclast morphology and expression of potassium conductances. J Physiol (Lond) 458:633–653
Benham CD, Bolton TB (1986) Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol (Lond) 381:385–406
Benham CD, Bolton TB, Lang RJ (1985) Acetylcholine activates an inward current in single mammalian smooth muscle cells. Nature 316:345–347
Coleman HA, Parkington HC (1987) Single channel Cl− and K+ currents from cells of uterus not treated with enzymes. Pflügers Arch 410:560–562
Evans MG, Marty A (1986) Calcium-dependent chloride currents in isolated cells from rat lacrimal glands. J Physiol (Lond) 378:437–460
Hogg RC, Wang Q, Large WA (1993) Time course of spontaneous calcium-activated chloride currents in smooth muscle cells from the rabbit portal vein. J Physiol (Lond) 464:15–31
Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145–159
Janssen LJ, Daniel EE (1991) Depolarizing agents induce oscillations in canine bronchial smooth muscle membrane potential: possible mechanisms. J Pharmacol Exp Ther 259:110–117
Janssen LJ, Sims SM (1992) Acetylcholine activates nonselective cation and chloride conductances in canine and guinea-pig tracheal myocytes. J Physiol (Lond) 453:197–218
Janssen LJ, Sims SM (1993) Histamine activates Cl− and K+ currents in guinea-pig tracheal myocytes: convergence with muscarinic signalling pathway. J Physiol (Lond) 465:661–677
Janssen LJ, Sims SM (1993) Emptying and refilling of Ca2+ store in canine tracheal myocytes as indicated by ACh-evoked currents and contraction. Am J Physiol 265:C877-C886
Kolb HA, Brown CDA, Murer H (1985) Identification of a voltage-dependent anion channel in the apical membrane of a Cl−-secretory epithelium (MDCK). Pflügers Arch 403:262–265
Kondo T, Tamura K, Onoe K, Takahara H, Ohta Y, Yamabayashi H (1992) In vivo recording of electrical activity of canine tracheal smooth muscle. J Appl Physiol 72:135–142
Marty A, Tan YP, Trautman A (1984) Three types of calcium-dependent channel in rat lacrimal glands. J Physiol (Lond) 357:297–325
Mayer ML (1985) A calcium-activated chloride current generates the after-depolarization of rat sensory neurons in culture. J Physiol (Lond) 364:217–239
Nelson DJ, Tang JM, Palmer LG (1984) Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells. J Membr Biol 80:81–89
Pacaud P, Loirand G, Lavie JL, Mironneau C, Mironneau J (1989) Calcium-activated chloride current in rat vascular smooth muscle cells in short-term primary culture. Pflügers Arch 413:629–636
Petersen OH, Wakui M (1990) Oscillating intracellular Ca2+ signals evoked by activation of receptors linked to inositol lipid hydrolysis: mechanism of generation. J Membr Biol 118:93–105
Post JM, Hume JR (1992) Ionic basis for spontaneous depolarizations in isolated smooth muscle cells of canine colon. Am J Physiol 263:C691-C699
Sanders KM (1992) Ionic mechanisms of electrical rhythmicity in gastrointestinal smooth muscles. Annu Rev Physiol 54:439–453
Schwarze W, Kolb H-A (1984) Voltage-dependent kinetics of an anionic channel of large unit conductance in macrophages and myotube membranes. Pflügers Arch 402:281–291
Soejima M, Kokubun S (1988) Single anion-selective channel and its ion selectivity in the vascular smooth muscle cell. Pflügers Arch 411:304–311
Sun XP, Supplisson S, Torres R, Sachs G, Mayer E (1992) Characterization of large conductance chloride channels in rabbit colonic smooth muscle. J Physiol (Lond) 448:355–382
Tsien RW, Tsien RY (1990) Calcium channels, stores, and oscillations. Annu Rev Cell Biol 6:715–760
van Helden DF (1991) Spontaneous and noradrenaline-induced transient depolarizations in the smooth muscle of guinea-pig mesenteric vein. J Physiol (Lond) 437:511–541
Wang Q, Hogg RC, Large WA (1992) Properties of spontaneous inward currents recorded in smooth muscle cells isolated from the rabbit portal vein. J Physiol (Lond) 451:525–537
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Janssen, L.J., Sims, S.M. Spontaneous transient inward currents and rhythmicity in canine and guinea-pig tracheal smooth muscle cells. Pflügers Arch. 427, 473–480 (1994). https://doi.org/10.1007/BF00374263
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00374263