Strontium-induced repetitive calcium spikes in a unicellular green alga

The divalent cation Sr2+ induced repetitive transient spikes of the cytosolic Ca2+ activity [Ca2+]cy and parallel repetitive transient hyperpolarizations of the plasma membrane in the unicellular green alga Eremosphaera viridis. [Ca2+]cy measurements, membrane potential measurements, and cation analysis of the cells were used to elucidate the mechanism of Sr2+-induced [Ca2+]cy oscillations. Sr2+ was effectively and rapidly compartmentalized within the cell, probably into the vacuole. The [Ca2+]cy oscillations cause membrane potential oscillations, and not the reverse. The endoplasmic reticulum (ER) Ca2+-ATPase blockers 2,5-di-tert-butylhydroquinone and cyclopiazonic acid inhibited Sr2+-induced repetitive [Ca2+]cy spikes, whereas the compartmentalization of Sr2+ was not influenced. A repetitive Ca2+ release and Ca2+ re-uptake by the ER probably generated repetitive [Ca2+]cy spikes in E. viridis in the presence of Sr2+. The inhibitory effect of ruthenium red and ryanodine indicated that the Sr2+-induced Ca2+ release from the ER was mediated by a ryanodine/cyclic ADP-ribose type of Ca2+ channel. The blockage of Sr2+-induced repetitive [Ca2+]cy spikes by La3+ or Gd3+ indicated the necessity of a certain influx of divalent cations for sustained [Ca2+]cy oscillations. Based on these data we present a mathematical model that describes the baseline spiking [Ca2+]cy oscillations in E. viridis.

[1]  G. Schönknecht,et al.  Light-Dependent Changes of the Cytoplasmic H and Cl Activity in the Green Alga Eremosphaera viridis. , 1992, Plant physiology.

[2]  G. Schonknecht.  Review article. Light-dependent signal transduction and transient changes in cytosolic Ca2+ in a unicellular green alga , 1998 .

[3]  Z. Rengel.  Effects of Al, Rare Earth Elements, and Other Metals on Net 45Ca2+ Uptake by Amaranthus Protoplasts , 1994 .

[4]  P. De Koninck,et al.  Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. , 1998, Science.

[5]  R. Tsien,et al.  A new generation of Ca2+ indicators with greatly improved fluorescence properties. , 1985, The Journal of biological chemistry.

[6]  J. Taylor,et al.  Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium. , 1995, The Plant cell.

[7]  D. Sanders,et al.  Release of Ca2+ from individual plant vacuoles by both InsP3 and cyclic ADP-ribose , 1995, Science.

[8]  A. Campbell,et al.  Transduction of Ca2+ signals in plant cells and compartmentalization of the Ca2+ signal. , 1996, Biochemical Society transactions.

[9]  R Y Tsien,et al.  Calcium channels, stores, and oscillations. , 1990, Annual review of cell biology.

[10]  Martin D. Bootman,et al.  The elemental principles of calcium signaling , 1995, Cell.

[11]  D. Ehrhardt,et al.  Calcium Spiking in Plant Root Hairs Responding to Rhizobium Nodulation Signals , 1996, Cell.

[12]  J. Putney,et al.  Uptake and intracellular sequestration of divalent cations in resting and methacholine-stimulated mouse lacrimal acinar cells. Dissociation by Sr2+ and Ba2+ of agonist-stimulated divalent cation entry from the refilling of the agonist-sensitive intracellular pool. , 1990, The Journal of biological chemistry.

[13]  K. Campbell,et al.  Purified ryanodine receptor from rabbit skeletal muscle is the calcium- release channel of sarcoplasmic reticulum , 1988, The Journal of general physiology.

[14]  P. Masson,et al.  Circadian oscillations of cytosolic and chloroplastic free calcium in plants. , 1995, Science.

[15]  I. Bezprozvanny,et al.  The pharmacology of intracellular Ca2+-release channels , 1994 .

[16]  M. Berridge.  The AM and FM of calcium signalling , 1997, Nature.

[17]  J. E. Melvin,et al.  Inhibitors of the intracellular Ca2+ release mechanism prevent muscarinicinduced Ca2+ influx in rat sublingual mucous acini , 1993, FEBS letters.

[18]  B. Fredholm,et al.  Oscillations in KATP channel activity promote oscillations in cytoplasmic free Ca2+ concentration in the pancreatic beta cell. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  D. S. Bush.  Calcium Regulation in Plant Cells and its Role in Signaling , 1995 .

[20]  S. Hagiwara,et al.  Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Eckberg,et al.  Human autonomic rhythms: vagal cardiac mechanisms in tetraplegic subjects. , 1994, The Journal of physiology.

[22]  L. Kochian,et al.  Voltage-dependent Ca2+ influx into right-side-out plasma membrane vesicles isolated from wheat roots: characterization of a putative Ca2+ channel. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G Boheim,et al.  Gadolinium‐sensitive, voltage‐dependent calcium release channels in the endoplasmic reticulum of a higher plant mechanoreceptor organ. , 1995, The EMBO journal.

[24]  G. Schönknecht,et al.  An Inwardly Rectifying Cation Current across the Plasma Membrane of the Green Alga Eremosphaera viridis , 1993 .

[25]  C. Petersen,et al.  Calcium and hormone action. , 1994, Annual review of physiology.

[26]  R. Somogyi,et al.  A dialogue on Ca2+ oscillations: an attempt to understand the essentials of mechanisms leading to hormone-induced intracellular Ca2+ oscillations in various kinds of cell on a theoretical level. , 1994, Biochimica et biophysica acta.

[27]  G. Schönknecht,et al.  Light-dependent signal transduction and transient changes in cytosolic Ca2+ in a unicellular green alga , 1998 .

[28]  C. Fewtrell.  Ca2+ oscillations in non-excitable cells. , 1993, Annual review of physiology.

[29]  G. Meissner,et al.  Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. , 1994, Annual review of physiology.

[30]  B. Förster.  Injected inositol 1,4,5‐trisphosphate activates Ca2+ ‐sensitive K + channels in the plasmalemma of Eremosphaera viridis , 1990, FEBS letters.

[31]  A. Webb,et al.  Calcium Ions as Intracellular Second Messengers in Higher Plants. , 1996 .

[32]  S. Mironov,et al.  Sr and Ba transients in isolated snail neurones studied with fura-2. The recovery from depolarization induced load and modulation of Ca release from intracellular stores , 1990, Neuroscience Letters.

[33]  J. Putney,et al.  Spatial and temporal aspects of cellular calcium signaling , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[34]  P. Thorn,et al.  Ca2+ signalling in rat chromaffin cells: interplay between Ca2+ release from intracellular stores and membrane potential. , 1996, Cell calcium.

[35]  E. Blumwald,et al.  Voltage-Dependent Calcium Channels in Plant Vacuoles , 1992, Science.

[36]  P. Pacaud,et al.  Ca2+ and Sr2+ entry induced Ca2+ release from the intracellular Ca2+ store in smooth muscle cells of rat portal vein. , 1993, The Journal of physiology.

[37]  U. Hansen,et al.  Repetitive Ca2+ spikes in a unicellular green alga , 1997, FEBS letters.

[38]  R. Graeff,et al.  Sensitization of Calcium-induced Calcium Release by Cyclic ADP-ribose and Calmodulin (*) , 1995, The Journal of Biological Chemistry.

[39]  Divalent cation and anion currents are activated during the dark-induced transient hyperpolarization of the plasma membrane of the green alga Eremosphaera viridis , 1994 .

[40]  K. Cunningham,et al.  ECA1 complements yeast mutants defective in Ca2+ pumps and encodes an endoplasmic reticulum-type Ca2+-ATPase in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[41]  K. Krause,et al.  Cyclopiazonic acid depletes intracellular Ca2+ stores and activates an influx pathway for divalent cations in HL-60 cells. , 1992, The Journal of biological chemistry.

[42]  A. Campbell,et al.  Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium , 1991, Nature.

[43]  W. Simonis,et al.  Calcium activation of potassium channels in the plasmalemma of Eremosphaera viridis , 1989 .

[44]  K. Swann,et al.  Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes , 1995, Molecular reproduction and development.

[45]  J Rinzel,et al.  Ca2+ excitability of the ER membrane: an explanation for IP3-induced Ca2+ oscillations. , 1995, The American journal of physiology.

[46]  I. Hwang,et al.  Distinction between Endoplasmic Reticulum-Type and Plasma Membrane-Type Ca2+ Pumps (Partial Purification of a 120-Kilodalton Ca2+-ATPase from Endomembranes) , 1997, Plant physiology.

[47]  A. Trewavas,et al.  Wind-induced plant motion immediately increases cytosolic calcium. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[48]  E. Johannes,et al.  Parallel pathways for intracellular Ca2+ release from the vacuole of higher plants , 1992 .

[49]  György Hajnóczky,et al.  Decoding of cytosolic calcium oscillations in the mitochondria , 1995, Cell.

[50]  D. Logan,et al.  Characterisation and Immunological Identification of a Calmodulin-Stimulated Ca2+-ATPase from Maize Shoots , 1995 .

[51]  U. Hansen,et al.  Methodological aspects of pressure loading of Fura-2 into Characean cells , 1996 .

[52]  J. Bailey-Serres,et al.  Nucleotide Sequence of a cDNA for the Maize Protein Synthesis Initiation Factor 4A , 1995, Plant physiology.

[53]  K. Schumaker,et al.  Inositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. , 1987, The Journal of biological chemistry.

[54]  M. Berridge.  Inositol trisphosphate and calcium signalling , 1993, Nature.

[55]  D. Sanders,et al.  Pharmacology of Ca2+ release from red beet microsomes suggests the presence of ryanodine receptor homologs in higher plants , 1996, FEBS letters.

[56]  W. Simonis,et al.  Electrochemical Potential Gradients of H+, K+, Ca2+, and Cl- across the Tonoplast of the Green Alga Eremosphaera Viridis , 1995, Plant physiology.

[57]  S. Orrenius,et al.  2,5-Di-(tert-butyl)-1,4-benzohydroquinone rapidly elevates cytosolic Ca2+ concentration by mobilizing the inositol 1,4,5-trisphosphate-sensitive Ca2+ pool. , 1989, The Journal of biological chemistry.

[58]  R. Leigh,et al.  Membrane potential‐dependent calcium transport in right‐side‐out plasma membrane vesicles from Zea mays L. roots , 1994 .

[59]  J. Ma,et al.  Block by ruthenium red of the ryanodine-activated calcium release channel of skeletal muscle , 1993, The Journal of general physiology.

[60]  J Rinzel,et al.  Spontaneous electrical and calcium oscillations in unstimulated pituitary gonadotrophs. , 1995, Biophysical journal.

[61]  U. Hansen,et al.  The action potential in Chara: Ca2+ release from internal stores visualized by Mn2+‐induced quenching of fura‐dextran , 1998 .