Abstract
Intracellular Ca2+ ([Ca2+]i) was measured in single isolated human umbilical vein smooth muscle cells. Stimulation with histamine, in the absence of external Ca2+, mobilised Ca2+ from intracellular stores. When repeated brief applications of agonist were used, the time to onset, amplitude and rate of rise of the Ca2+ transients were found to change. Two components could often be discerned in the rising phase of the transients, an initial slow “pacemaker” and a second faster and larger component. Following the first histamine-activated transient the basal level of [Ca2+]i was invariably lower than that prior to stimulation. This lower value was maintained whilst the cell remained in Ca2+-free solution, but could be returned to a higher level if the cell was exposed to external Ca2+. When the mobilisation of the intracellular store was reduced to undetectable levels, re-exposure to Ca2+-containing medium reactivated responses. In the absence of external Ca2+, continuous application of histamine activated a series of transient increases in intracellular Ca2+, which decreased progressively in amplitude and rate of rise. The interval between transients also increased. These findings are discussed in terms of the activation of inositol trisphosphate-sensitive intracellular Ca2+ stores and their sensitivity to cytoplasmic Ca2+ and intrasarcoplasmic reticulum Ca2+.
Similar content being viewed by others
References
Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361: 315–325
Bian J, Ghosh TK, Wang J-C, Gill DL (1991) Identification of intracellular calcium pools. J Biol Chem 266: 8801–8806
Bootman MD, Berridge MJ, Taylor CW (1992) All or nothing Ca2+ mobilization from the intracellular stores of single histamine-stimulated HeLa cells. J Physiol (Lond) 450: 163–178
Cobbold PH, Rink TJ (1987) Fluorescence and bioluminescence measurement of cytoplasmic free calcium. Biochem J 248: 313–328
Dartsch PC, Weiss H-D, Betz E (1990) Human vascular smooth muscle cells in culture: growth characteristics and protein pattern by use of serum-free media supplements. Eur J Cell Biol 51: 285–294
Endo M (1977) Calcium release from the sarcoplasmic reticulum. Physiol Rev 57: 71–109
Endo M (1985) Calcium release from sarcoplasmic reticulum. Curr Top Membr Transp 25: 181–230
Finch EA, Turner TJ, Goldin SM (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 25: 443–446
Ghosh TK, Mullaney JM, Fahmy TI, Gill DL (1989) GTP-activated communication between distinct inositol 1,4,5-trisphosphate-sensitive and -insensitive calcium pools. Nature 340: 236–239
Giannini G, Clementi E, Ceci R, Marziali G, Sorrentino V (1992) Expression of a ryanodine receptor-Ca2+ channel that is regulated by TGF-β. Science 257: 91–94
Gill DL (1989) Receptor kinships revealed. Nature 342: 16–18
Gillespie JI, Greenwell JR (1988) Changes in intracellular pH regulating mechanisms in somitic cells of the early chick embryo. A study using fluorescent pH-sensitive dye. J Physiol (Lond) 405: 385–395
Greenwell JR, Nicholls JA, Harvey I, Gillespie JI (1992) The application of slow scan cooled integrating charge coupled devices (CCD) to the measurement of intracellular free calcium (Ca2+)i in single mammalian cells. J Physiol (Lond) 452:265P
Hill SJ (1990) Distribution, properties and functional characteristics of three classes of histamine receptor. Pharmacol Rev 42: 45–84
Iino M (1989) Calcium-induced calcium release mechanism in guinea pig tenia caeci. J Gen Physiol 94: 363–383
Iino M (1990) Biphasic Ca2+ dependence of inositol 1,4,5- trisphosphate-induced Ca release in smooth muscle cells of the guinea pig tenia caeci. J Gen Physiol 95: 1103–1122
Iino M (1991) Effects of adenine nucleotides on inositol 1,4,5- trisphosphate-induced calcium release in vascular smooth muscle cells. J Gen Physiol 98: 681–698
Iino M, Endo M (1992) Calcium-dependent immediate feedback control of inositol 1,4,5-trisphosphate-induced Ca2+ release. Nature 360: 76–78
Missiaen L, Declerk I, Droogmans G, Plessers L, De Smedt H, Raeymaekers L, Casteels R (1990) Agonist-dependent Ca2+ and Mn2+ entry dependent on state of filling of Ca2+ stores in aortic smooth muscle cells of the rat. J Physiol (Lond) 427: 171–186
Missiaen I, Taylor CW, Berridge MJ (1991) Spontaneous calcium release from inositol trisphosphate-sensitive calcium stores. Nature 352: 241–244
Missiaen L, De Smedt H, Droogmans G, Casteels R (1992) Ca2+ release induced by inositol 1,4,5-trisphosphate is a steady state phenomenon controlled by lumenal Ca2+ in permeabilized cells. Nature 357: 599–602
Neylon CB, Mason WT, Irvine RF (1991) Histamine-induced calcium oscillations in human vascular smooth muscle: temporal sequence and spatial organisation in single cells. Clin Exp Pharmacol Physiol 18: 299–302
Peres A (1990) InsP 3- and Ca2+-induced Ca2+ release in single mouse oocytes. FEBS Lett 275: 213–216
Roe MW, Lemasters JJ, Herman B (1990) Assessment of fura-2 for measurements of cytosolic free calcium. Cell Calcium 11: 63–73
Rousseau E, Meissner G (1989) Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine. Am J Physiol 256: H328-H333
Sharma RV, Bhalla RC (1989) Regulation of cytosolic free Ca2+ concentration in vascular smooth muscle cells by A- and C-kinase. Hypertension 13: 845–850
Somlyo AP, Walker JW, Goldman YE, Trentham DR, Kobayashi S, Kitazawa T, Somlyo AV (1988) Inositol trisphosphate, calcium and muscle contraction. Philos Trans R Soc Lond [Biol] 320: 399–414
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nicholls, J.A., Gillespie, J.I. & Greenwell, J.R. The time course of intracellular calcium movements in single human umbilical vein smooth muscle cells. Pflügers Arch 425, 225–232 (1993). https://doi.org/10.1007/BF00374171
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00374171