Rapid recovery of releasable vesicles and formation of nonreleasable endosomes follow intense exocytosis in chromaffin cells

Neurons and neuroendocrine cells must retrieve plasma membrane excess and refill vesicle pools depleted by exocytosis. To perform these tasks cells can use different endocytosis/recycling mechanisms whose selection will impact on vesicle recycling time and secretion performance. We used FM1-43 to ev...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autor principal: Bay, A.E.P
Otros Autores: Ibañez, L.I, Marengo, F.D
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: 2007
Materias:
Acceso en línea:Registro en Scopus
DOI
Handle
Registro en la Biblioteca Digital
Aporte de:Registro referencial: Solicitar el recurso aquí
Descripción
Sumario:Neurons and neuroendocrine cells must retrieve plasma membrane excess and refill vesicle pools depleted by exocytosis. To perform these tasks cells can use different endocytosis/recycling mechanisms whose selection will impact on vesicle recycling time and secretion performance. We used FM1-43 to evaluate in the same experiment exocytosis, endocytosis, and recovery of releasable vesicles on mouse chromaffin cells. Various exocytosis levels were induced by a variety of stimuli, and we discriminated the resultant endocytosis-recycling responses according to their ability to rapidly generate releasable vesicles. Exocytosis of ≤20% of plasma membrane (provoked by nicotine/acetylcholine) was followed by total recovery of releasable vesicles. If a stronger stimulus (50 mM K + and 2 mM Ca2+) provoking intense exocytosis (51 ± 7%) was applied, endocytosis still retrieved all the fused membrane, but only a fraction (19 ± 2%) was releasable by a second stimulus. Using ADVASEP-7 or bromophenol blue to quickly eliminate fluorescence from noninternalized FM1-43, we determined that this fraction became releasable in <2 min. The remaining nonreleasable fraction was distributed mainly as fluorescent spots (∼0.7 μm) selectively labeled by 40- to 70-kDa dextrans and was suppressed by a phosphatidylinositol-3-phosphate kinase inhibitor, suggesting that it had been formed by a bulk retrieval mechanism. We concluded that chromaffin cells can rapidly recycle significant fractions of their total vesicle population, and that this pathway prevails when cholinergic agonists are used as secretagogues. When exocytosis exceeded ∼20% of plasma membrane, an additional mechanism was activated, which was unable to produce secretory vesicles in our experimental time frame but appeared crucial to maintaining membrane surface homeostasis under extreme conditions. Copyright © 2007 the American Physiological Society.
Bibliografía:Ales, E., Tabares, L., Poyato, J.M., Valero, V., Lindau, M., Alvarez de Toledo, G., High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism (1999) Nat Cell Biol, 1, pp. 40-44
Araki, N., Johnson, M.T., Swanson, J.A., A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages (1996) J Cell Biol, 135, pp. 1249-1260
Artalejo, C.R., Elhamdani, A., Palfrey, H.C., Secretion: Dense-core vesicles can kiss-and-run too (1998) Curr Biol, 8, pp. R62-R65
Artalejo, C.R., Elhamdani, A., Palfrey, H.C., Sustained stimulation shifts the mechanism of endocytosis from dynamin-1-dependent rapid endocytosis to clathrin- and dynamin-2-mediated slow endocytosis in chromaffin cells (2002) Proc Natl Acad Sci USA, 99, pp. 6358-6363
Artalejo, C.R., Henley, J.R., McNiven, M.A., Palfrey, H.C., Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin but not clathrin (1995) Proc Natl Acad Sci USA, 92, pp. 8328-8332
Augustine, G.J., Neher, E., Calcium requirements for secretion in bovine chromaffin cells (1992) J Physiol, 450, pp. 247-271
Baartscheer, A., Schumacher, C.A., Opthof, T., Fiolet, J.W., The origin of increased cytoplasmic calcium upon reversal of the Na+/Ca 2+-exchanger in isolated rat ventricular myocytes (1996) J Mol Cell Cardiol, 28, pp. 1963-1973
Bauer, R.A., Khera, R.S., Lieber, J.L., Angleson, J.K., Recycling of intact dense core vesicles in neurites of NGF-treated PC12 cells (2004) FEBS Lett, 571, pp. 107-111
Bauer, R.A., Overlease, R.L., Lieber, J.L., Angleson, J.K., Retention and stimulus-dependent recycling of dense core vesicle content in neuroendocrine cells (2004) J Cell Sci, 117, pp. 2193-2202
Burgoyne, R.D., Control of exocytosis in adrenal chromaffin cells (1991) Biochim Biophys Acta, 1071, pp. 174-202
Burgoyne, R.D., Fast exocytosis and endocytosis triggered by depolarisation in single adrenal chromaffin cells before rapid Ca2+ current run-down (1995) Pflügers Arch, 430, pp. 213-219
Chan, S.A., Smith, C., Low frequency stimulation of mouse adrenal slices reveals a clathrin-independent, protein kinase C-mediated endocytic mechanism (2003) J Physiol, 553, pp. 707-717
Clague, M.J., Thorpe, C., Jones, A.T., Phosphatidylinositol 3-kinase regulation of fluid phase endocytosis (1995) FEBS Lett, 367, pp. 272-274
de Lange, R.P., de Roos, A.D., Borst, J.G., Two modes of vesicle recycling in the rat calyx of Held (2003) J Neurosci, 23, pp. 10164-10173
Dinkelacker, V., Voets, T., Neher, E., Moser, T., The readily releasable pool of vesicles in chromaffin cells is replenished in a temperature-dependent manner and transiently overfills at 37°C (2000) J Neurosci, 20, pp. 8377-8383
Elhamdani, A., Azizi, F., Artalejo, C.R., Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: High calcium shifts the mechanism from kiss-and-run to complete fusion (2006) J Neurosci, 26, pp. 3030-3036
Fulop, T., Radabaugh, S., Smith, C., Activity-dependent differential transmitter release in mouse adrenal chromaffin cells (2005) J Neurosci, 25, pp. 7324-7332
Harata, N.C., Aravanis, A.M., Tsien, R.W., Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion (2006) J Neurochem, 97, pp. 1546-1570
Harata, N.C., Choi, S., Pyle, J.L., Aravanis, A.M., Tsien, R.W., Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods (2006) Neuron, 49, pp. 243-256
Heinemann, C., von Ruden, L., Chow, R.H., Neher, E., A two-step model of secretion control in neuroendocrine cells (1993) Pflügers Arch, 424, pp. 105-112
Henkel, A.W., Horstmann, H., Henkel, M.K., Direct observation of membrane retrieval in chromaffin cells by capacitance measurements (2001) FEBS Lett, 505, pp. 414-418
Holt, M., Cooke, A., Wu, M.M., Lagnado, L., Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells (2003) J Neurosci, 23, pp. 1329-1339
Kay, A.R., Alfonso, A., Alford, S., Cline, H.T., Holgado, A.M., Sakmann, B., Snitsarev, V.A., Wu, L.G., Imaging synaptic activity in intact brain and slices with FM1-43 in C. elegans, lamprey, and rat (1999) Neuron, 24, pp. 809-817
Klingauf, J., Kavalali, E.T., Tsien, R.W., Kinetics and regulation of fast endocytosis at hippocampal synapses (1998) Nature, 394, pp. 581-585
Koval, L.M., Yavorskaya, E.N., Lukyanetz, E.A., Electron microscopic evidence for multiple types of secretory vesicles in bovine chromaffin cells (2001) Gen Comp Endocrinol, 121, pp. 261-277
Liu, P.S., Kao, L.S., Na+-dependent Ca2+ influx in bovine adrenal chromaffin cells (1990) Cell Calcium, 11, pp. 573-579
Maxfield, F.R., McGraw, T.E., Endocytic recycling (2004) Nat Rev Mol Cell Biol, 5, pp. 121-132
Moser, T., Neher, E., Estimation of mean exocytic vesicle capacitance in mouse adrenal chromaffin cells (1997) Proc Natl Acad Sci USA, 94, pp. 6735-6740
Pan, C.Y., Huang, C.H., Lee, C.H., Calcium elevation elicited by reverse mode Na+/Ca2+ exchange activity is facilitated by intracellular calcium stores in bovine chromaffin cells (2006) Biochem Biophys Res Commun, 342, pp. 589-595
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
Patzak, A., Winkler, H., Exocytotic exposure and recycling of membrane antigens of chromaffin granules: Ultrastructural evaluation after immunolabeling (1986) J Cell Biol, 102, pp. 510-515
Perrais, D., Kleppe, I.C., Taraska, J.W., Almers, W., Recapture after exocytosis causes differential retention of protein in granules of bovine chromaffin cells (2004) J Physiol, 560, pp. 413-428
Phillips, J.H., Burridge, K., Wilson, S.P., Kirshner, N., Visualization of the exocytosis/endocytosis secretory cycle in cultured adrenal chromaffin cells (1983) J Cell Biol, 97, pp. 1906-1917
Richards, D.A., Guatimosim, C., Betz, W.J., Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals (2000) Neuron, 27, pp. 551-559
Rizzoli, S.O., Betz, W.J., Synaptic vesicle pools (2005) Nat Rev Neurosci, 6, pp. 57-69
Smith, C.B., Betz, W.J., Simultaneous independent measurement of endocytosis and exocytosis (1996) Nature, 380, pp. 531-534
Taraska, J.W., Perrais, D., Ohara-Imaizumi, M., Nagamatsu, S., Almers, W., Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells (2003) Proc Natl Acad Sci USA, 100, pp. 2070-2075
Tomoda, H., Kishimoto, Y., Lee, Y.C., Temperature effect on endocytosis and exocytosis by rabbit alveolar macrophages (1989) J Biol Chem, 264, pp. 15445-15450
von Grafenstein, H., Knight, D.E., Membrane recapture and early triggered secretion from the newly formed endocytotic compartment in bovine chromaffin cells (1992) J Physiol, 453, pp. 15-31
Wick, P.F., Trenkle, J.M., Holz, R.W., Punctate appearance of dopamine-beta-hydroxylase on the chromaffin cell surface reflects the fusion of individual chromaffin granules upon exocytosis (1997) Neuroscience, 80, pp. 847-860
ISSN:03636143
DOI:10.1152/ajpcell.00632.2006