Vesicle size determines unitary exocytic properties and their sensitivity to sphingosine

Molecular and Cellular Endocrinology

Volumn 376, Issue 1-2, 2013, Pages 136-147

  Flašker, Ajda ^a,b   Jorgačevski, Jernej ^a,c   Calejo, Ana I ^d   Kreft, Marko ^a,b,c,e   Zorec, Robert ^a,b,c  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins   (Slovenia)

^c Celica Biomedical Sciences Center   (Slovenia)

^d UNIVERSITY OF AVEIRO   (Portugal)

^e UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Exocytosis; Fusion pore; Lactotrophs; Prolactin; Sphingosine

Indexed keywords

PROLACTIN; SPHINGOSINE; SYNAPTOBREVIN 2;

ANIMAL CELL; ANTIBODY LABELING; ARTICLE; CELL DENSITY; CELL FUSION; CELL MEMBRANE; CELL SIZE; CELL VACUOLE; CONTROLLED STUDY; EXOCYTOSIS; EXTRACELLULAR SPACE; MALE; MICROSCOPY; NONHUMAN; POROSITY; PRIORITY JOURNAL; PROLACTIN SECRETING CELL; RAT; SENSITIVITY ANALYSIS;

C(M); EXOCYTOSIS; FULL WIDTH AT HALF MAXIMUM; FUSION PORE; FWHM; G(P); IM; IMAGINARY AND REAL (RE) PARTS OF THE ADMITTANCE SIGNAL; LACTOTROPHS; LARGE DENSE CORE VESICLES; LDCVS; MEMBRANE CAPACITANCE; PORE CONDUCTANCE; PRL; PROLACTIN; SIM; SNARE; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FUSION FACTOR ATTACHMENT PROTEIN RECEPTOR; SPHINGOSINE; STRUCTURED ILLUMINATION MICROSCOPY; VAMP2; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2; VOCCS; VOLTAGE ACTIVATED CALCIUM CHANNELS;

ANIMALS; CELL MEMBRANE; ELECTRIC CAPACITANCE; EXOCYTOSIS; GENE EXPRESSION; LACTOTROPHS; MALE; MEMBRANE FUSION; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; PROLACTIN; RATS; RATS, WISTAR; SECRETORY VESICLES; SNARE PROTEINS; SPHINGOSINE; VESICLE-ASSOCIATED MEMBRANE PROTEIN 2;

EID: 84880163583     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.06.012     Document Type: Article

References (57)

1. Alvarez de Toledo G., Fernandez-Chacon R., Fernandez J.M. Release of secretory products during transient vesicle fusion. Nature 1993, 363:554-558.
2. An S.J., Grabner C.P., Zenisek D. Real-time visualization of complexin during single exocytic events. Nat. Neurosci. 2010, 13:577-583.
3. Angleson J.K., Cochilla A.J., Kilic G., Nussinovitch I., Betz W.J. Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events. Nat. Neurosci. 1999, 2:440-446.
4. Ben-Tabou S., Keller E., Nussinovitch I. Mechanosensitivity of voltage-gated calcium currents in rat anterior pituitary cells. J. Physiol. 1994, 476:29-39.
5. Blom T., Bergelin N., Slotte J.P., Tornquist K. Sphingosine kinase regulates voltage operated calcium channels in GH(4)C(1) rat pituitary cells. Cell. Signal. 2006, 18:1366-1375.
6. Breckenridge L.J., Almers W. Final steps in exocytosis observed in a cell with giant secretory granules. Proc. Nat. Acad. Sci. USA 1987, 84:1945-1949.
7. Camoletto P.G., Vara H., Morando L., Connell E., Marletto F.P., Giustetto M., Sassoe-Pognetto M., Van Veldhoven P.P., Ledesma M.D. Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18. PLoS ONE 2009, 4:e5310.
8. Ceccarelli B., Hurlbut W.P., Mauro A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 1973, 57:499-524.
9. Chen X.K., Wang L.C., Zhou Y., Zheng L.H., Zhou Z. "Kiss-and-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J. Neurosci. 2005, 25:9236-9243.
10. Cochilla A.J., Angleson J.K., Betz W.J. Differential regulation of granule-to-granule and granule-to-plasma membrane fusion during secretion from rat pituitary lactotrophs. J. Cell Biol. 2000, 150:839-848.
11. Coorssen J.R., Zorec R. Regulated exocytosis per partes. Cell Calcium 2012, 52:191-195.
12. Dannies P.S. Mechanisms for storage of prolactin and growth hormone in secretory granules. Mol. Genet. Metab. 2002, 76:6-13.
13. Darios F., Wasser C., Shakirzyanova A., Giniatullin A., Goodman K., Munoz-Bravo J.L., Raingo J., Jorgačevski J., Kreft M., Zorec R., Rosa J.M., Gandia L., Gutierrez L.M., Binz T., Giniatullin R., Kavalali E.T., Davletov B. Sphingosine facilitates SNARE complex assembly and activates synaptic vesicle exocytosis. Neuron 2009, 62:683-694.
14. Dasgupta S., Adams J.A., Hogan E.L. Maternal alcohol consumption increases sphingosine levels in the brains of progeny mice. Neurochem. Res. 2007, 32:2217-2224.
15. Debus K., Lindau M. Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys. J. 2000, 78:2983-2997.
16. Gandhi S.P., Stevens C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 2003, 423:607-613.
17. Gonçalves P.P., Stenovec M., Chowdhury H.H., Grilc S., Kreft M., Zorec R. Prolactin secretion sites contain syntaxin-1 and differ from ganglioside monosialic acid rafts in rat lactotrophs. Endocrinology 2008, 149:4948-4957.
18. Gustafsson M.G.L. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc.-Oxford 2000, 198:82-87.
19. Hanna S.T., Pigeau G.M., Galvanovskis J., Clark A., Rorsman P., MacDonald P.E. Kiss-and-run exocytosis and fusion pores of secretory vesicles in human beta-cells. Pflugers Arch. 2009, 457:1343-1350.
20. Hannun Y.A., Obeid L.M. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell Biol. 2008, 9:139-150.
21. He X.X., Huang Y., Li B., Gong C.X., Schuchman E.H. Deregulation of sphingolipid metabolism in Alzheimer's disease. Neurobiol. Aging 2010, 31:398-408.
22. Heuser J.E., Reese T.S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 1973, 57:315-344.
23. Huerta-Ocampo I., Christian H.C., Thompson N.M., El Kasti M.M., Wells T. The intermediate lactotroph: a morphologically distinct, ghrelin-responsive pituitary cell in the dwarf (dw/dw) rat. Endocrinology 2005, 146:5012-5023.
24. Jahn R., Lang T., Sudhof T.C. Membrane fusion. Cell 2003, 112:519-533.
25. Jena B.P. Exocytotic fusion: total or transient?. Cell Biol. Int. 1997, 21:257-259.
26. Jorgačevski J. Munc18-1 tuning of vesicle merger and fusion pore properties. J. Neurosci. 2011, 9055-9066.
27. Jorgačevski J., Stenovec M., Kreft M., Bajic A., Rituper B., Vardjan N., Stojilkovic S., Zorec R. Hypotonicity and peptide discharge from a single vesicle. Cell Physiol.: Am. J. Physiol. 2008, 295:624-631.
28. Jorgačevski J., Fosnaric M., Vardjan N., Stenovec M., Potokar M., Kreft M., Kralj-Iglic V., Iglic A., Zorec R. Fusion pore stability of peptidergic vesicles. Mol. Membr. Biol. 2010, 27:65-80.
29. Jorgačevski J., Fosnaric M., Vardjan N., Stenovec M., Potokar M., Kreft M., Kralj-Iglic V., Iglic A., Zorec R. Fusion pore stability of peptidergic vesicles. Mol. Membr. Biol. 2010, 27:65-80.
30. Jorgačevski J., Potokar M., Grilc S., Kreft M., Liu W., Barclay J.W., Buckers J., Medda R., Hell S.W., Parpura V., Burgoyne R.D., Zorec R. Munc18-1 tuning of vesicle merger and fusion pore properties. J. Neurosci. 2011, 31:9055-9066.
31. Kabaso D., Jorgačevski J., Calejo A.I., Flašker A., Guček A., Kreft M., Zorec R. Comparison of unitary exocytic events in pituitary lactotrophs and in astrocytes: modeling the discrete open fusion-pore states. Front. Cell. Neurosci. 2013, 7(33):1-6.
32. Katz B. The Sherrington Lectures X (The release of neural transmitter substances 1969, Thomas, C. C., Springfield, Illinois.
33. Klyachko V.A., Jackson M.B. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 2002, 418:89-92.
34. Kreft M., Zorec R. Cell-attached measurements of attofarad capacitance steps in rat melanotrophs. Pflügers Archiv 1997, 434:212-214.
35. Lollike K., Lindau M. Membrane capacitance techniques to monitor granule exocytosis in neutrophils. J. Immunol. Methods 1999, 232:111-120.
36. Mathes C., Fleig A., Penner R. Calcium release-activated calcium current (I-CRAC) is a direct target for sphingosine. J. Biol. Chem. 1998, 273:25020-25030.
37. Mohrmann R., de Wit H., Verhage M., Neher E., Sorensen J.B. Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 2010, 330:502-505.
38. Neher E., Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc. Nat. Acad. Sci. USA 1982, 79:6712-6716.
39. Riddle O., Bates R., Dykshorn S. The preparation, identification and assay of prolactin - a hormone of the anterior pituitary. Am. J. Physiol. 1933, 105:191-216.
40. Rituper B., Guček A., Jorgačevski J., Flašker A., Kreft M., Zorec R. High-resolution membrane capacitance measurements for the study of exocytosis and endocytosis. Nat. Protoc. 2013, 8:1169-1183.
41. Rosa J.M., Gandia L., Garcia A.G. Permissive role of sphingosine on calcium-dependent endocytosis in chromaffin cells. Pflugers Arch. 2010, 460:901-914.
42. Segovia M., Ales E., Montes M.A., Bonifas I., Jemal I., Lindau M., Maximov A., Sudhof T.C., de Toledo G.A. Push-and-pull regulation of the fusion pore by synaptotagmin-7. Proc. Nat. Acad. Sci. USA 2010, 107:19032-19037.
43. Sinha R., Ahmed S., Jahn R., Klingauf J. Two synaptobrevin molecules are sufficient for vesicle fusion in central nervous system synapses. Proc. Nat. Acad. Sci. USA 2011, 108:14318-14323.
44. Smets G., Velkeniers B., Finne E., Baldys A., Gepts W., Vanhaelst L. Postnatal development of growth hormone and prolactin cells in male and female rat pituitary. An immunocytochemical light and electron microscopic study. J. Histochem. Cytochem. 1987, 35:335-341.
45. Spruce A.E., Breckenridge L.J., Lee A.K., Almers W. Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 1990, 4:643-654.
46. Stenovec M., Kreft M., Poberaj I., Betz W.J., Zorec R. Slow spontaneous secretion from single large dense-core vesicles monitored in neuroendocrine cells. FASEB J. 2004, 18:1270-1272.
47. Stenovec M., Gonçalves P.P., Zorec R. Peptide hormone release monitored from single vesicles in membrane lawns of differentiated pituitary cells: SNAREs and fusion pore widening. Endocrinology 2013, 154:1235-1246.
48. Tani M., Sano T., Ito M., Igarashi Y. Mechanisms of sphingosine and sphingosine 1-phosphate generation in human platelets. J. Lipid Res. 2005, 46:2458-2467.
49. Titievsky A., Titievskaya I., Pasternack M., Kaila K., Tornquist K. Sphingosine inhibits voltage-operated calcium channels in GH4C1 cells. J. Biol. Chem. 1998, 273:242-247.
50. van den Bogaart G., Holt M.G., Bunt G., Riedel D., Wouters F.S., Jahn R. One SNARE complex is sufficient for membrane fusion. Nat. Struct. Mol. Biol. 2010, 17. 358-U129.
51. Vardjan N., Stenovec M., Jorgačevski J., Kreft M., Zorec R. Subnanometer fusion pores in spontaneous exocytosis of peptidergic vesicles. J. Neurosci. 2007, 27:4737-4746.
52. Vardjan N., Jorgačevski J., Stenovec M., Kreft M., Zorec R. Compound exocytosis in pituitary cells. Ann. N. Y. Acad. Sci. 2009, 1152:63-75.
53. Williams D., Vicogne J., Zaitseva I., McLaughlin S., Pessin J.E. Evidence that electrostatic interactions between vesicle-associated membrane protein 2 and acidic phospholipids may modulate the fusion of transport vesicles with the plasma membrane. Mol. Biol. Cell 2009, 20:4910-4919.
54. Zhang Z., Jackson M.B. Synaptotagmin IV modulation of vesicle size and fusion pores in PC12 cells. Biophys. J. 2010, 98:968-978.
55. Zhang Z., Wu Y., Wang Z., Dunning F.M., Rehfuss J., Ramanan D., Chapman E.R., Jackson M.B. Release mode of large and small dense-core vesicles specified by different synaptotagmin isoforms in PC12 cells. Mol. Biol. Cell 2011, 22:2324-2336.
56. Zorec, R., Henigman, F., Mason, W.T., Kordaš, M. (1991a) Electrophysiological study of hormone secretion by single adenohypophyseal cells. In: Methods in Neurosciences, pp. 194-210.
57. Zorec R., Sikdar S.K., Mason W.T. Increased cytosolic calcium stimulates exocytosis in bovine lactotrophs. Direct evidence from changes in membrane capacitance. J. Gen. Physiol. 1991, 97:473-497.