Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Exocytosis in adrenal chromaffin cells is strongly influenced by the pattern of stimulation. To understand the dynamic and spatial properties of the underlying Ca2+ signal, we used pulsed laser Ca2+ imaging to capture Ca2+ gradients during stimulation by single and repetitive depolarizing stimuli. Short single pulses (10-100 ms) lead to the development of submembrane Ca2+ gradients, as previously described (F. D. Marengo and J. R. Monck, 2000, Biophysical Journal, 79:1800-1820). Repetitive stimulation with trains of multiple pulses (50 ms each, 2Hz) produce a pattern of intracellular Ca2+ increase that progressively changes from the typical Ca2+ gradient seen after a single pulse to a Ca 2+ increase throughout the cell that peaks at values 3-4 times higher than the maximum values obtained at the end of single pulses. After seven or more pulses, the fluorescence increase was typically larger in the interior of the cell than in the submembrane region. The pattern of Ca 2+ gradient was not modified by inhibitors of Ca2+- induced Ca2+ release (ryanodine), inhibitors of IP3- induced Ca2+ release (xestospongin), or treatments designed to deplete intracellular Ca2+ stores (thapsigargin). However, we found that the large fluorescence increase in the cell interior spatially colocalized with the nucleus. These results can be simulated using mathematical models of Ca2+ redistribution in which the nucleus takes up Ca2+ by active or passive transport mechanisms. These results show that chromaffin cells can respond to depolarizing stimuli with different dynamic Ca 2+ signals in the submembrane space, the cytosol, and the nucleus.

Registro:

Documento: Artículo
Título:Spatial Distribution of Ca2+ Signals during Repetitive Depolarizing Stimuli in Adrenal Chromaffin Cells
Autor:Marengo, F.D.; Monck, J.R.
Filiación:Department of Physiology, UCLA School of Medicine, Los Angeles, CA 90095, United States
Dept. of Physiology, Center for Health Sciences, UCLA School of Medicine, 10833 Le Conte Ave., Los Angeles, CA 90095, United States
Depto. de Fisiol./Biol. Molecular, Fac. de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:calcium antagonist; calcium ion; inositol 1,4,5 trisphosphate receptor; receptor blocking agent; ryanodine; thapsigargin; unclassified drug; xestospongin; animal cell; article; calcium cell level; calcium signaling; calcium transport; cattle; cell membrane; cell membrane depolarization; cell nucleus; cell stimulation; cell structure; chromaffin cell; controlled study; cytoplasm; exocytosis; fluorescence; mathematical model; nonhuman; Animalia; Bos taurus
Año:2003
Volumen:85
Número:5
Página de inicio:3397
Página de fin:3417
DOI: http://dx.doi.org/10.1016/S0006-3495(03)74759-6
Título revista:Biophysical Journal
Título revista abreviado:Biophys. J.
ISSN:00063495
CODEN:BIOJA
CAS:calcium ion, 14127-61-8; ryanodine, 15662-33-6; thapsigargin, 67526-95-8
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00063495_v85_n5_p3397_Marengo

Referencias:

  • Al-Mohanna, F.A., Caddy, K.W., Bolsover, S.R., The nucleus is insulated from large cytosolic calcium ion changes (1994) Nature, 367, pp. 745-750
  • Artalejo, C.R., Elhamdani, A., Palfrey, H.C., Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells (1996) Neuron, 16, pp. 195-205
  • Baylor, S.M., Hollingworth, S., Fura-2 calcium transients in frog skeletal muscle fibres (1988) J. Physiol., 403, pp. 151-192
  • Berridge, M.J., Lipp, P., Bootman, M.D., The versatility and universality of calcium signalling (2000) Nat. Rev. Mol. Cell Biol., 1, pp. 11-21
  • Brini, M., Carafoli, E., Calcium signalling: A historical account, recent developments and future perspectives (2000) Cell. Mol. Life Sci., 57, pp. 354-370
  • Burgoyne, R.D., Cheek, T.R., Morgan, A., O'Sullivan, A.J., Moreton, R.B., Berridge, M.J., Mata, A.M., East, J.M., Distribution of two distinct Ca2+-ATPase-like proteins and their relationships to the agonist-sensitive calcium store in adrenal chromaffin cells (1989) Nature, 342, pp. 72-74
  • Burgoyne, R.D., Geisow, M.J., The annexin family of calcium-binding proteins. Review article (1989) Cell Calcium, 10, pp. 1-10
  • Burgoyne, R.D., Morgan, A., O'Sullivan, A.J., A major role for protein kinase C in calcium-activated exocytosis in permeabilised adrenal chromaffin cells (1988) FEBS Lett., 238, pp. 151-155
  • Craske, M., Takeo, T., Gerasimenko, O., Vaillant, C., Torok, K., Petersen, O.H., Tepikin, A.V., Hormone-induced secretory and nuclear translocation of calmodulin: Oscillations of calmodulin concentration with the nucleus as an integrator (1999) Proc. Natl. Acad. Sci. USA, 96, pp. 4426-4431
  • Deisseroth, K., Bito, H., Tsien, R.W., Signaling from synapse to nucleus: Postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity (1996) Neuron, 16, pp. 89-101
  • Deisseroth, K., Heist, E.K., Tsien, R.W., Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons (1998) Nature, 392, pp. 198-202
  • DiFranco, M., Novo, D., Vergara, V.L., Characterization of the calcium release domains during excitation-contraction coupling in skeletal muscle fibres (2002) Pflugers Arch., 443, pp. 508-519
  • DiGregorio, D.A., Peskoff, A., Vergara, J.L., Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction (1999) J. Neurosci., 19, pp. 7846-7859
  • DiGregorio, D.A., Vergara, J.L., Localized detection of action potential-induced presynaptic calcium transients at a Xenopus neuromuscular junction (1997) J. Physiol. (Lond.), 505, pp. 585-592
  • Escobar, A.L., Monck, J.R., Fernandez, J.M., Vergara, J.L., Localization of the site of Ca2+ release at the level of a single sarcomere in skeletal muscle fibres (1994) Nature, 367, pp. 739-741
  • Escobar, A.L., Velez, P., Kim, A.M., Cifuentes, F., Fill, M., Vergara, J.L., Kinetic properties of DM-nitrophen and calcium indicators: Rapid transient response to flash photolysis (1997) Pflugers Arch., 434, pp. 615-631
  • Fink, C.C., Slepchenko, B., Moraru, I.I., Watras, J., Schaff, J.C., Loew, L.M., An image-based model of calcium waves in differentiated neuroblastoma cells (2000) Biophys. J., 79, pp. 163-183
  • Gabso, M., Neher, E., Spira, M.E., Low mobility of the Ca2+ buffers in axons of cultured Aplysia neurons (1997) Neuron, 18, pp. 473-481
  • Gerasimenko, O.V., Gerasimenko, J.V., Tepikin, A.V., Petersen, O.H., ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP- ribose-mediated release of Ca2+ from the nuclear envelope (1995) Cell, 80, pp. 439-444
  • Gerasimenko, O.V., Gerasimenko, J.V., Tepikin, A.V., Petersen, O.H., Calcium transport pathways in the nucleus (1996) Pflugers Arch., 432, pp. 1-6
  • Harkins, A.B., Kurebayashi, N., Baylor, S.M., Resting myoplasmic free calcium in frog skeletal muscle fibers estimated with fluo-3 (1993) Biophys. J., 65, pp. 865-881
  • Heinemann, C., Von Ruden, L., Chow, R.H., Neher, E., A two-step model of secretion control in neuroendocrine cells (1993) Pflugers Arch., 424, pp. 105-112
  • Heizmann, C.W., Calcium-binding proteins: Basic concepts and clinical implications (1992) Gen. Physiol. Biophys., 11, pp. 411-425
  • Hernández-Cruz, A., Sala, F., Adams, P.R., Subcellular calcium transients visualized by confocal microscopy in a voltage-clamped vertebrate neuron (1990) Science, 247, pp. 858-862
  • Herrington, J., Park, Y.B., Babcock, D.F., Hille, B., Dominant role of mitochondria in clearance of large Ca2+ loads from rat adrenal chromaffin cells (1996) Neuron, 16, pp. 219-228
  • Horrigan, F.T., Bookman, R.J., Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells (1994) Neuron, 13, pp. 1119-1129
  • Iida, S., Calcium binding to troponin C. II. A Ca2+ ion titration study with a Ca2+ ion sensitive electrode (1988) J. Biochem. (Tokyo), 103, pp. 482-486
  • Issa, N.P., Hudspeth, A.J., The entry and clearance of Ca2+ at individual presynaptic active zones of hair cells from the bullfrog's sacculus (1996) Proc. Natl. Acad. Sci. USA, 93, pp. 9527-9532
  • Klingauf, J., Neher, E., Modeling buffered Ca2+ diffusion near the membrane: Implications for secretion in neuroendocrine cells (1997) Biophys. J., 72, pp. 674-690
  • Konishi, M., Olson, A., Hollingworth, S., Baylor, S.M., Myoplasmic binding of fura-2 investigated by steady-state fluorescence and absorbance measurements (1988) Biophys. J., 54, pp. 1089-1104
  • Leathers, V.L., Linse, S., Forsén, S., Norman, A.W., Calbindin-D28K, a 1 α,25-dihydroxyvitamin D3-induced calcium-binding protein, binds five or six Ca2+ ions with high affinity (1990) J. Biol. Chem., 265, pp. 9838-9841
  • Marengo, F.D., Monck, J.R., Development and dissipation of Ca2+ gradients in adrenal chromaffin cells (2000) Biophys. J., 79, pp. 1800-1820
  • Minta, A., Kao, J.P., Tsien, R.Y., Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores (1989) J. Biol. Chem., 264, pp. 8171-8178
  • Monck, J.R., Oberhauser, A.F., Keating, T.J., Fernandez, J.M., Thin-section ratiometric Ca2+ images obtained by optical sectioning of fura-2 loaded mast cells (1992) J. Cell Biol., 116, pp. 745-759
  • Monck, J.R., Reynolds, E.E., Thomas, A.P., Williamson, J.R., Novel kinetics of single cell Ca2+ transients in stimulated hepatocytes and A10 cells measured using fura-2 and fluorescent videomicroscopy (1988) J. Biol. Chem., 263, pp. 4569-4575
  • Monck, J.R., Robinson, I.M., Escobar, A.L., Vergara, J.L., Fernandez, J.M., Pulsed laser imaging of rapid Ca2+ gradients in excitable cells (1994) Biophys. J., 67, pp. 505-514
  • Morimoto, S., Ohtsuki, I., Ca2+ binding to cardiac troponin C in the myofilament lattice and its relation to the myofibrillar ATPase activity (1994) Eur. J. Biochem., 226, pp. 597-602
  • Neher, E., Correction for liquid junction potentials in patch clamp experiments (1992) Methods Enzymol., 207, pp. 123-131
  • Nicotera, P., McConkey, D.J., Jones, D.P., Orrenius, S., ATP stimulates Ca2+ uptake and increases the free Ca2 + concentration in isolated rat liver nuclei (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 453-457
  • Nohmi, M., Hua, S.Y., Kuba, K., Intracellular calcium dynamics in response to action potentials in bullfrog sympathetic ganglion cells (1992) J. Physiol., 458, pp. 171-190
  • Nowycky, M.C., Pinter, M.J., Time courses of calcium and calcium-bound buffers following calcium influx in a model cell (1993) Biophys. J., 64, pp. 77-91
  • Olwin, B.B., Storm, D.R., Calcium binding to complexes of calmodulin and calmodulin binding proteins (1985) Biochemistry, 24, pp. 8081-8086
  • O'Sullivan, A.J., Cheek, T.R., Moreton, R.B., Berridge, M.J., Burgoyne, R.D., Localization and heterogeneity of agonist-induced changes in cytosolic calcium concentration in single bovine adrenal chromaffin cells from video imaging of fura-2 (1989) EMBO J., 8, pp. 401-411
  • Pan, C.Y., Kao, L.S., Catecholamine secretion from bovine adrenal chromaffin cells: The role of the Na+/Ca2+ exchanger and the intracellular Ca2 + pool (1997) J. Neurochem., 69, pp. 1085-1092
  • Pusch, M., Neher, E., Rates of diffusional exchange between small cells and a measuring patch pipette (1988) Pflugers Arch., 411, pp. 204-211
  • Sala, F., Hernández-Cruz, A., Calcium diffusion modeling in a spherical neuron. Relevance of buffering properties (1990) Biophys. J., 57, pp. 313-324
  • Segal, M., Manor, D., Confocal microscopic imaging of [Ca2+]i in cultured rat hippocampal neurons following exposure to N-methyl-D-aspartate (1992) J. Physiol., 448, pp. 655-676
  • Smith, G.D., Keizer, J.E., Stern, M.D., Lederer, W.J., Cheng, H., A simple numerical model of calcium spark formation and detection in cardiac myocytes (1998) Biophys. J., 75, pp. 15-32
  • Stehno-Bittel, L., Perez-Terzic, C., Clapham, D.E., Diffusion across the nuclear envelope inhibited by depletion of the nuclear Ca2+ store (1995) Science, 270, pp. 1835-1838
  • Tang, Y.M., Travis, E.R., Wightman, R.M., Schneider, A.S., Sodium-calcium exchange affects local calcium signal decay and the rate of exocytotic secretion in single chromaffin cells (2000) J. Neurochem., 74, pp. 702-710
  • Teleman, O., Drakenberg, T., Forsen, S., Thulin, E., Calcium and cadmium binding to troponin C. Evidence for cooperativity (1983) Eur. J. Biochem., 134, pp. 453-457
  • Thomas, D., Tovey, S.C., Collins, T.J., Bootman, M.D., Berridge, M.J., Lipp, P., A comparison of fluorescent Ca2+ indicator properties and their use in measuring elementary and global Ca2+ signals (2000) Cell Calcium, 28, pp. 213-223
  • Williams, D.A., Fogarty, K.E., Tsien, R.Y., Fay, F.S., Calcium gradients in single smooth muscle cells revealed by the digital imaging microscope using Fura-2 (1985) Nature, 318, pp. 558-561
  • Zhou, Z., Neher, E., Mobile and immobile calcium buffers in bovine adrenal chromaffin cells (1993) J. Physiol. (Lond.), 469, pp. 245-273

Citas:

---------- APA ----------
Marengo, F.D. & Monck, J.R. (2003) . Spatial Distribution of Ca2+ Signals during Repetitive Depolarizing Stimuli in Adrenal Chromaffin Cells. Biophysical Journal, 85(5), 3397-3417.
http://dx.doi.org/10.1016/S0006-3495(03)74759-6
---------- CHICAGO ----------
Marengo, F.D., Monck, J.R. "Spatial Distribution of Ca2+ Signals during Repetitive Depolarizing Stimuli in Adrenal Chromaffin Cells" . Biophysical Journal 85, no. 5 (2003) : 3397-3417.
http://dx.doi.org/10.1016/S0006-3495(03)74759-6
---------- MLA ----------
Marengo, F.D., Monck, J.R. "Spatial Distribution of Ca2+ Signals during Repetitive Depolarizing Stimuli in Adrenal Chromaffin Cells" . Biophysical Journal, vol. 85, no. 5, 2003, pp. 3397-3417.
http://dx.doi.org/10.1016/S0006-3495(03)74759-6
---------- VANCOUVER ----------
Marengo, F.D., Monck, J.R. Spatial Distribution of Ca2+ Signals during Repetitive Depolarizing Stimuli in Adrenal Chromaffin Cells. Biophys. J. 2003;85(5):3397-3417.
http://dx.doi.org/10.1016/S0006-3495(03)74759-6