Stimulation-dependent regulation of the pH, volume and quantal size of bovine land rodent secretory vesicles

Journal of Physiology

Volumn 542, Issue 2, 2002, Pages 453-476

  Pothos, Emmanuel N ^a   Mosharov, Eugene ^b   Liu, Kuo Peing ^c   Setlik, Wanda ^b   Haburcak, Marian ^a   Baldini, Giulia ^b   Gershon, Michael D ^b   Tamir, Hadassah ^b,c   Sulzer, David ^b,c,d  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b College of Physicians and Surgeons ^*  (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,1 DIMETHYL 4 PHENYLPIPERAZINIUM; BAFILOMYCIN; BOTULINUM TOXIN; CALCIUM ION; CATECHOLAMINE DERIVATIVE; CHLORIDE CHANNEL; LEVODOPA; NICOTINIC AGENT; POTASSIUM ION; PROTON PUMP; PROTON PUMP INHIBITOR; VERATRIDINE; 5 NITRO 2 (3 PHENYLPROPYLAMINO)BENZOIC ACID; BOTULINUM TOXIN E; CATECHOLAMINE; DOPA; POTASSIUM; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACIDIFICATION; ACIDITY; AMPEROMETRY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CATECHOLAMINE RELEASE; CATTLE; CELL CULTURE; CELL MEMBRANE; CELL PH; CELL SIZE; CELL STIMULATION; CELL VOLUME; CHLORIDE TRANSPORT; CHROMAFFIN CELL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOSOME; EXOCYTOSIS; HYPOTHESIS; IN VITRO STUDY; IN VIVO STUDY; INTESTINE INNERVATION; MALE; MEMBRANE MARKER; MOUSE; NERVE ENDING; NEUROBLASTOMA CELL; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SECRETORY VESICLE; STIMULUS RESPONSE; ANIMAL EXPERIMENT; ANION TRANSPORT; ENZYME INHIBITION; INTERNALIZATION; PH; STABLE EXPRESSION; SYNAPSE VESICLE;

ADRENAL MEDULLA; ANIMALS; ANTI-BACTERIAL AGENTS; CATTLE; CELL SIZE; CELLS, CULTURED; CHROMAFFIN CELLS; ELECTRIC STIMULATION; ELECTROCHEMISTRY; HOMEOSTASIS; HYDROGEN-ION CONCENTRATION; IMMUNOHISTOCHEMISTRY; MACROLIDES; MALE; MICROSCOPY, IMMUNOELECTRON; ORGANELLES; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0037101540     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2002.018630     Document Type: Article

References (74)

1. AGUADO, F., GOMBAU, L., MAJO, G., MARSAL, J., BLANCO, J. & BLASI, J. (1997). Regulated secretion is impaired in AtT-20 endocrine cells stably transfected with botulinum neurotoxin type A light chain. Journal of Biological Chemistry 272, 26005-26008.
2. ANDERSON, R. G. W., FALCK, J. R., GOLDSTEIN, J. L. & BROWN, M. S. (1984). Visualization of acidic organelles in intact cells by electron microscopy. Proceeding of the National Academy of Sciences of the USA 81, 4838-4842.
3. ANDERSON, R. G. W. & PATHAK, R. K. (1985). Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell 40, 635-643.
4. 2+ on insulin secretion in pancreatic beta cells. Journal of Biological Chemistry 272, 31308-31314.
5. BAE, H.-R. & VERKMAN, A. S. (1990). Protein kinase A regulates chloride conductance in endocytic vesicles from proximal tubule. Nature 348, 637-639.
6. 2+-dependent exocytosis. Journal of Biological Chemistry 271, 20227-20230.
7. BARASCH, J., GERSHON, M. D., NUNEZ, E. A., TAMIR, H. & AL-AWQATI, Q. (1988). Thyrotropin induced the acidification of secretory granules of parafollicular cells by increasing the chloride conductance of the granular membrane. Journal of Cell Biology 107, 2137-2147.
8. -) uptake and acidification. Journal of Cell Science 114, 2145-2154.
9. BRODWICK, M. S., CURRAN, M. & EDWARDS, C. (1992). Effects of osmotic stress on mast cell vesicles of the beige mouse. Journal of Membrane Biology 126, 159-169.
10. BROWN, E. M. & MACLEOD, R. J. (2001). Extracellular calcium sensing and extracellular calcium signaling. Physiological Review 81, 239-297.
11. CHENG, I., QURESHI, I., CHATTOPADHYAY, N., QURESHI, A., BUTTERS, R., HALL, A., CIMA, R., ROGERS, K., HERBERT, S., GEIBEL, J., BROWN, E. & SOYBEL, D. (1999). Expression of an extracellular calcium-sensing receptor in rat stomach. Gastroenterology 116, 118-126.
12. CHEVRIER, D., FOURNIER, H., NAULT, C., ZOLLINGER, M., CRINE, P. & BOILEAU, G. (1991). Expression of porcine pro-opiomelanocortin in mouse neuroblastoma (Neuro2A) cells: targeting of the foreign neuropeptide to dense-core vesicles. Molecular and Cellular Endocrinology 79, 109-118.
13. CIDON, S. & NELSON, N. (1983). A novel ATPase in the chromaffin granule membrane. Journal of Biological Chemistry 258, 2892-2898.
14. CIDON, S., TAMIR, H., NUNEZ, E. A. & GERSHON, M. D. (1991). ATP dependent uptake of 5-hydroxytryptamine by secretory granules isolated from thyroid parafollicular cells. Journal of Biological Chemistry 266, 4392-4400.
15. COLLIVER, T., HESS, E., POTHOS, E. N., SULZER, D. & EWING, A. G. (1999). Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells. Journal of Neurochemistry 74, 1086-1097.
16. COLLIVER, T. L., PYOTT, S. J., ACHALABUN, M. & EWING, A. G. (2000). VMAT-mediated changes in quantal size and vesicular volume. Journal of Neuroscience 20, 5276-5282.
17. ELHAMDANI, A., PALFREY, H. C. & ARTALEJO, C. R. (2001). Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells. Neuron 31, 819-830.
18. ENGEL, J., PASTUSHENKO, V. F., RICHTER, W. & DONATH, E. (1991). On the interaction between chromaffin granule membranes and intragranular vesicles - theory and analysis of freeze-fracture micrographs. Biorheology 28, 75-87.
19. FARQUHAR, M. G. (1978). Recovery of surface membrane in anterior pituitary cells. Variations in traffic detected with anionic and cationic ferritin. Journal of Cell Biology 77, R35-42.
20. +-ATPase: a universal proton pump of eukaryotes. Biochemical Journal 324, 697-712.
21. +)-ATPases. Journal of Experimental Biology 203, 71-80.
22. FUJITA, T. (1987). Paraneurons. In Encyclopedia of Neuroscience, vol. II, ed. ADELMAN, G., pp. 921-923. Birkhaüser, Boston.
23. 4. Journal of Histochemistry and Cytochemistry 30, 769-773.
24. + antiport: dependence on the proton electrochemical gradient. Molecular Brain Research 71, 178-184.
25. GRABE, M., WANG, H. & OSTER, G. (2000). The mechanochemistry of V-ATPase proton pumps. Biophysical Journal 78, 2798-2813.
26. 2+-induced deprotonation of peptide hormones inside secretory vesicles in preparation for release. Journal of Neuroscience 19, 900-905.
27. HANNAH, M. J., SCHMIDT, A. A. & HUTTNER, W. B. (1999). Synaptic vesicle biogenesis. Annual Review of Cell and Developmental Biology 15, 733-798.
28. JANKOWSKI, J. A., FINNEGAN, J. M. & WIGHTMAN, R. M. (1994). Extracellular ionic composition alters kinetics of vesicular release of catecholamines and quantal size during exocytosis at adrenal medullary cells. Journal of Neurochemistry 63, 1739-1747.
29. JOHNSON, R. G. (1988). Accumulation of biological amines into chromaffin granules: a model for hormone and neurotransmitter transport. Physiological Review 68, 232-307.
30. JOHNSON, S. M. & BUTTRESS, N. (1973). The osmotic insensitivity of sonicated liposomes and the density of phospholipid-cholesterol mixtures. Biochimica et Biophysica Acta 307, 20-26.
31. KOZMINSKI, K. D., GUTMAN, D. A., DAVILA, V., SULZER, D. & EWING, A. G. (1998). Voltammetric and pharmacological characterization of dopamine released from single quantal events in PC12 cells. Analytical Chemistry 70, 3123-3130.
32. 2+ receptor-stimulated hormone release from sheep thyroid parafollicular cells. Journal of Physiology 502, 31-44.
33. MAECHLER, P. & WOLLHEIM, C. B. (1999). Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 402, 685-689.
34. MARTIN, T. F. (1994). The molecular machinery for fast and slow neurosecretion. Current Opinion in Neurobiology 4, 626-632.
35. MAWE, G. M. & GERSHON, M. D. (1986). Functional heterogeneity in the myenteric plexus: demonstration using cytochrome oxidase as a verified cytochemical probe ofthe activity of individual enteric neurons. Journal of Comparative Neurology 249, 381-391.
36. MICHAEL, D. J. & WIGHTMAN, R. M. (1999). Electrochemical monitoring of biogenic amine neurotransmission in real time. Journal of Pharmaceutical and Biomedical Analysis 19, 33-46.
37. MUNDORF, M. L., HOCHSTETLER, S. E. & WIGHTMAN, R. M. (1999). Amine weak bases disrupt vesicular storage and promote exocytosis in chromaffin cells. Journal of Neurochemistry 73, 2397-2405.
38. NAGAYAMA, T., MATSUMOTO, T., KUWAKUBO, F., FUKUSHIMA, Y., YOSHIDA, M., SUZUKI-KUSABA, M., HISA, H., KIMURA, T. & SATOH, S. (1999). Role of calcium channels in catecholamine secretion in the rat adrenal gland. Journal of Physiology 520, 503-512.
39. NELSON, N., PERZOV, N., COHEN, A., HAGAI, K., PADLER, V. & NELSON, H. (2000). The cellular biology of proton-motive force generation by V-ATPases. Journal of Experimental Biology 203, 89-95.
40. NJUS, D., KELLEY, P. M. & HARNADEK, G. J. (1986). Bioenergetics of secretory vesicles. Biochimica et Biophysica Acta 853, 237-265.
41. ORCI, L., HALBAN, P., PERRELET, A., AMHERDT, M., RAVAZZOLA, M. & ANDERSON, R. G. (1994). pH independent and dependent cleavage of proinsulin in the same secretory vesicle. Journal of Cell Biology 126, 1149-1156.
42. ORCI, L., RAVAZZOLA, M., AMHERDT, M., MADSEN, O., PERRELET, A., VASSALLI, J. D. & ANDERSON, R. G. (1986). Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. Journal of Cell Biology 103, 2273-2281.
43. ORNBERG, R. L., DUONG, L. T. & POLLARD, H. B. (1986). Intragranular vesicles: new organelles in the secretory granules of adrenal chromaffin cells. Cell and Tissue Research 245, 547-553.
44. ORNBERG, R. L., FURUYA, S., GOPING, G. & KUIJPERS, G. A. (1995). Granule swelling in stimulated bovine adrenal chromaffin cells: regulation by internal granule pH. Cell and Tissue Research 279, 85-92.
45. PAZOLES, C., CREUTZ, C., RAMU, A. & POLLARD, H. (1980). Permeant anion activation of MgATPase activity in chromaffin granules. Journal of Biological Chemistry 255, 7863-7869.
46. PENNER, R., NEHER, E. & DREYER, F. (1986). Intracellularly injected tetanus toxin inhibits exocytosis in bovine adrenal chromaffin cells. Nature 324, 76-78.
47. PETERS, C., BAYER, M. J., BUHLER, S., ANDERSEN, J. S., MANN, M. & MAYER, A. (2001). Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409, 581-588.
48. 31P nuclear magnetic resonance spectroscopy. Journal of Biological Chemistry 254, 1170-1177.
49. 2+ uptake by the smooth muscle sarcoplasmic reticulum. Biophysical Journal 75, 1759-1766.
50. POTHOS, E., DAVILA, V. & SULZER, D. (1998). Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. Journal of Neuroscience 18, 4106-4118.
51. POTHOS, E., DESMOND, M. & SULZER, D. (1996). L-3,4-Dihydroxyphenylalanine increases the quantal size of exocytic dopamine release in vitro. Journal of Neurochemistry 66, 629-636.
52. REIMER, R. J., FON, E. A. & EDWARDS, R. H. (1998). Vesicular neurotransmitter transport and the presynaptic regulation of quantal size. Current Opinion in Neurobiology 8, 405-412.
53. RORSMAN, P. & RENSTROM, E. (1999). Glutamate primes the pump. Nature 402, 595-596.
54. RYBAK, S., LANNI, F. & MURPHY, R. F. (1997). Theoretical considerations on the role of membrane potential in the regulation of endosomal pH. Biophysical Journal 73, 674-687.
55. SABBAN, E. L., SCHWARTZ, J. & MCMAHON, A. (1990). Effect of compounds which disrupt proton gradients on secretion of neurosecretory proteins from PC12 pheochromocytoma cells. Neuroscience 38, 561-570.
56. SCEPEK, S. & LINDAU, M. (1993). Focal exocytosis by eosinophils-compound exocytosis and cumulative fusion. EMBO Journal 12, 1811-1817.
57. SCHNEIDER, D. (1981). ATP-acidification of intact and disrupted lysosomes. Journal of Biological Chemistry 256, 3858-3864.
58. - accumulation during acidification. Journal of Biological Chemistry 7, 7.
59. STOBRAWA, S. M., BREIDERHOFF, T., TAKAMORI, S., ENGEL, D., SCHWEIZER, M., ZDEBIK, A. A., BOSL, M. R., RUETHER, K., JAHN, H., DRAGUHN, A., JAHN, R. & JENTSCH, T. J. (2001). Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29, 185-196.
60. SULZER, D., CHEN, T., LAU, Y., KRISTENSEN, H., RAYPORT, S. & EWING, A. (1995). Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. Journal of Neuroscience 15, 4102-4108.
61. SULZER, D. & HOLTZMAN, E. (1989). Acidification and endosome-like compartments in the presynaptic terminals of frog retinal photoreceptors. Journal of Neurocytology 18, 529-540.
62. SULZER, D. & POTHOS, E. N. (2000). Presynaptic mechanisms that regulate quantal size. Reviews in the Neurosciences 11, 159-212.
63. SULZER, D. & RAYPORT, S. (1990). Amphetamine and other psychostimulants reduce PH gradients in midbrain dopaminergic neurons and chromaffin granules: a mechanism of action. Neuron 5, 797-808.
64. TAKAMORI, S., RIEDEL, D. & JAHN, R. (2000). Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. Journal of Neuroscience 20, 4904-4911.
65. TAMIR, H., LIU, K. P., ADLERSBERG, M., HSUING, S. & GERSHON, M. D. (1996). Acidification of serotonin-containing secretory vesicles induced by a plasma membrane calcium receptor. Journal of Biological Chemistry 271, 6441-6450.
66. TAMIR, H., PISCOPO, I., LIU, K.-P., HSIUNG, S., ADLERSBERG, M., NICOLAIDES, M., AL-AWQATI, Q. & GERSHON, M. D. (1994). Secretogogue-induced gating of chloride channels in the secretory vesicles of a paraneuron. Endocrinology 135, 2045-2057.
67. UNGERMANN, C., WICKNER, W. & XU, Z. (1999). Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proceedings of the National Academy of Sciences of the USA 96, 11194-11199.
68. VAN DER KLOOT, W. (1987). Inhibition of packing of acetylcholine into quanta by ammonium. FASEB Journal 1, 298-302.
69. VAN DER KLOOT, W. & SPIELHOLZ, N. (1987). Effects of changes in tonicity of the extracellular solution on the size of vesicles in frog motor nerve terminals. Journal of Neurocytology 16, 77-84.
70. VAN DYKE, R. W. (1996). Acidification of lysosomes and endosomes. Sub-cellular Biochemistry 27, 331-360.
71. WADE, P. R., TAMIR, H., KIRCHGESSNER, A. L. & GERSHON, M. D. (1994). Analysis of the role of 5-HT in the enteric nervous system using anti-idiotopic antibodies to 5-HT receptors. American Journal of Physiology 266, G403-416.
72. WILLIAMS, R. M. & WEBB, W. W. (2000). Single granule pH cycling in antigen induced mast cell secretion. Journal of Cell Science 21, 3839-3850.
73. WINKLER, H. (1993). The adrenal chromaffin granule: a model for large dense core vesicles of endocrine and nervous tissue. Journal of Anatomy 183, 237-252.
74. ZHOU, Q., PETERSEN, C. C. & NICOLL, R. A. (2000). Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. Journal of Physiology 525, 195-206.