Characterisation of Weibel-Palade body fusion by amperometry in endothelial cells reveals fusion pore dynamics and the effect of cholesterol on exocytosis

Journal of Cell Science

Volumn 126, Issue 23, 2013, Pages 5490-5499

  Cookson, Emma A ^a   Conte, Ianina L ^a,d   Dempster, John ^b   Hannah, Matthew J ^c   Carter, Tom ^a,d  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Amperometry; Endothelial cell; Exocytosis; Serotonin; VMAT1; Weibel Palade bodies

Indexed keywords

CHOLESTEROL; SEROTONIN; VESICULAR MONOAMINE TRANSPORTER 1;

AMPEROMETRY; ARTICLE; CELL EXPANSION; CELL FUSION; CONTROLLED STUDY; DEPLETION; EXOCYTOSIS; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MODULATION; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY GRANULE; SUPPLEMENTATION; UMBILICAL VEIN ENDOTHELIAL CELL; WEIBEL PALADE BODY;

AMPEROMETRY; ENDOTHELIAL CELL; EXOCYTOSIS; SEROTONIN; VMAT1; WEIBEL-PALADE BODIES;

BETA-CYCLODEXTRINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CHOLESTEROL; ELECTROCHEMICAL TECHNIQUES; EVOKED POTENTIALS; EXOCYTOSIS; GENE EXPRESSION; HISTAMINE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; SEROTONIN; VESICULAR MONOAMINE TRANSPORT PROTEINS; WEIBEL-PALADE BODIES;

EID: 84890234927     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.138438     Document Type: Article

References (83)

1. Alvarez de Toledo, G., Fernández-Chacón, R. and Fernández, J. M. (1993). Release of secretory products during transient vesicle fusion. Nature 363, 554-558.
2. Amatore, C., Arbault, S., Bonifas, I., Bouret, Y., Erard, M., Ewing, A. G. and Sombers, L. A. (2005). Correlation between vesicle quantal size and fusion pore release in chromaffin cell exocytosis. Biophys. J. 88, 4411-4420.
3. Anantharam, A., Bittner, M. A., Aikman, R. L., Stuenkel, E. L., Schmid, S. L., Axelrod, D. and Holz, R. W. (2011). A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol. Biol. Cell 22, 1907-1918.
4. Babich, V., Meli, A., Knipe, L., Dempster, J. E., Skehel, P., Hannah, M. J. and Carter, T. (2008). Selective release of molecules from Weibel-Palade bodies during a lingering kiss. Blood 111, 5282-5290.
5. Barnes, K., Dobrzynski, H., Foppolo, S., Beal, P. R., Ismat, F., Scullion, E. R., Sun, L., Tellez, J., Ritzel, M. W., Claycomb, W. C. et al. (2006). Distribution and functional characterization of equilibrative nucleoside transporter-4, a novel cardiac adenosine transporter activated at acidic pH. Circ. Res. 99, 510-519.
6. Berberian, K., Torres, A. J., Fang, Q., Kisler, K. and Lindau, M. (2009). F-actin and myosin II accelerate catecholamine release from chromaffin granules. J. Neurosci. 29, 863-870.
7. Berger, M., Gray, J. A. and Roth, B. L. (2009). The expanded biology of serotonin. Annu. Rev. Med. 60, 355-366.
8. Bierings, R., Hellen, N., Kiskin, N., Knipe, L., Fonseca, A. V., Patel, B., Meli, A., Rose, M., Hannah, M. J. and Carter, T. (2012). The interplay between the Rab27A effectors Slp4-a and MyRIP controls hormone-evoked Weibel-Palade body exocytosis. Blood 120, 2757-2767.
9. Blann, A. D., Jackson, P., Bath, P. M. and Watts, G. F. (1995). von Willebrand factor, a possible indicator of endothelial cell damage, decreases during long-term compliance with a lipid-lowering diet. J. Intern. Med. 237, 557-561.
10. Braun, M., Wendt, A., Karanauskaite, J., Galvanovskis, J., Clark, A., MacDonald, P. E. and Rorsman, P. (2007). Corelease and differential exit via the fusion pore of GABA, serotonin, and ATP from LDCV in rat pancreatic beta cells. J. Gen. Physiol. 129, 221-231.
11. Brust, P., Friedrich, A., Krizbai, I. A., Bergmann, R., Roux, F., Ganapathy, V. and Johannsen, B. (2000). Functional expression of the serotonin transporter in immortalized rat brain microvessel endothelial cells. J. Neurochem. 74, 1241-1248.
12. Chang, J., Kim, S. A., Lu, X., Su, Z., Kim, S. K. and Shin, Y. K. (2009). Fusion stepspecific influence of cholesterol on SNARE-mediated membrane fusion. Biophys. J. 96, 1839-1846.
13. Chen, Z. and Rand, R. P. (1997). The influence of cholesterol on phospholipid membrane curvature and bending elasticity. Biophys. J. 73, 267-276.
14. Chow, R. H. and Von Ruden, L. (2009). Electrochemical detection of secretion from single cells. In Single-Channel Recording (ed. B. Sakmann and E. Neher). New York, NY: Springer.
15. Chow, R. H., von Rüden, L. and Neher, E. (1992). Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature 356, 60-63.
16. Churchward, M. A. and Coorssen, J. R. (2009). Cholesterol, regulated exocytosis and the physiological fusion machine. Biochem. J. 423, 1-14.
17. Churchward, M. A., Rogasevskaia, T., Brandman, D. M., Khosravani, H., Nava, P., Atkinson, J. K. and Coorssen, J. R. (2008). Specific lipids supply critical negative spontaneous curvature-an essential component of native Ca2+-triggered membrane fusion. Biophys. J. 94, 3976-3986.
18. Demer, L. L., Wortham, C. M., Dirksen, E. R. and Sanderson, M. J. (1993). Mechanical stimulation induces intercellular calcium signaling in bovine aortic endothelial cells. Am. J. Physiol. 264, H2094-H2102.
19. Dempsie, Y. and MacLean, M. R. (2008). Pulmonary hypertension: therapeutic targets within the serotonin system. Br. J. Pharmacol. 155, 455-462.
20. Diamond, S. L., Sachs, F. and Sigurdson, W. J. (1994). Mechanically induced calcium mobilization in cultured endothelial cells is dependent on actin and phospholipase. Arterioscler. Thromb. 14, 2000-2006.
21. Dibner, M. D. and Insel, P. A. (1981). Serum catecholamines desensitize betaadrenergic receptors of cultured C6 glioma cells. J. Biol. Chem. 256, 7343-7346.
22. Eiden, L. E., Schäfer, M. K., Weihe, E. and Schü tz, B. (2004). The vesicular amine transporter family (SLC18): amine/proton antiporters required for vesicular accumulation and regulated exocytotic secretion of monoamines and acetylcholine. Pflugers Arch. 447, 636-640.
23. Engel, K., Zhou, M. and Wang, J. (2004). Identification and characterization of a novel monoamine transporter in the human brain. J. Biol. Chem. 279, 50042-50049.
24. Erent, M., Meli, A., Moisoi, N., Babich, V., Hannah, M. J., Skehel, P., Knipe, L., Zupancic, G., Ogden, D. and Carter, T. (2007). Rate, extent and concentration dependence of histamine-evoked Weibel-Palade body exocytosis determined from individual fusion events in human endothelial cells. J. Physiol. 583, 195-212.
25. Erickson, J. D., Schafer, M. K., Bonner, T. I., Eiden, L. E. and Weihe, E. (1996). Distinct pharmacological properties and distribution in neurons and endocrine cells of two isoforms of the human vesicular monoamine transporter. Proc. Natl. Acad. Sci. USA 93, 5166-5171.
26. Essand, M., Vikman, S., Grawé, J., Gedda, L., Hellberg, C., Oberg, K., Totterman, T. H. and Giandomenico, V. (2005). Identification and characterization of a novel splicing variant of vesicular monoamine transporter 1. J. Mol. Endocrinol. 35, 489- 501.
27. Fang, Q., Berberian, K., Gong, L. W., Hafez, I., Sørensen, J. B. and Lindau, M. (2008). The role of the C terminus of the SNARE protein SNAP-25 in fusion pore opening and a model for fusion pore mechanics. Proc. Natl. Acad. Sci. USA 105, 15388-15392.
28. Ferk, P., Lipnik-S? tangelj, M., Krz?an, M. and C ? erne, K. (2012). Expression of organic cation transporter 3 (SLC22A3) and plasma membrane monoamine transporter (SLC29A4) in human umbilical vein endothelial cells and their elevance for histamine uptake. BMC Pharmacol. Toxicol. 13, Suppl. 1, A73.
29. Finnegan, J. M., Pihel, K., Cahill, P. S., Huang, L., Zerby, S. E., Ewing, A. G., Kennedy, R. T. and Wightman, R. M. (1996). Vesicular quantal size measured by amperometry at chromaffin, mast, pheochromocytoma, and pancreatic beta-cells. J. Neurochem. 66, 1914-1923.
30. Fu, J., Naren, A. P., Gao, X., Ahmmed, G. U. and Malik, A. B. (2005). Proteaseactivated receptor-1 activation of endothelial cells induces protein kinase Calphadependent phosphorylation of syntaxin 4 and Munc18c: role in signaling p-selectin expression. J. Biol. Chem. 280, 3178-3184.
31. Galbusera, M., Zoja, C., Donadelli, R., Paris, S., Morigi, M., Benigni, A., Figliuzzi, M., Remuzzi, G. and Remuzzi, A. (1997). Fluid shear stress modulates von Willebrand factor release from human vascular endothelium. Blood 90, 1558-1564.
32. Ge, S., Wittenberg, N. J. and Haynes, C. L. (2008). Quantitative and real-time detection of secretion of chemical messengers from individual platelets. Biochemistry 47, 7020-7024.
33. Ge, S., White, J. G. and Haynes, C. L. (2009). Quantal release of serotonin from platelets. Anal. Chem. 81, 2935-2943.
34. Ge, S., White, J. G. and Haynes, C. L. (2010). Critical role of membrane cholesterol in exocytosis revealed by single platelet study. ACS Chem. Biol. 5, 819-828.
35. Goligorsky, M. S. (1988). Mechanical stimulation induces Ca2+i transients and membrane depolarization in cultured endothelial cells. Effects on Ca2+i in coperfused smooth muscle cells. FEBS Lett. 240, 59-64.
36. Hamamori, Y., Hoshijima, M., Ohmori, T., Ueda, T. and Takai, Y. (1988). Serotonin as a major serum factor inducing the phospholipase C-mediated hydrolysis of phosphoinositides in normal rat kidney cells. Cancer Res. 48, 6697-6702.
37. Hewlett, L., Zupanc?ic?, G., Mashanov, G., Knipe, L., Ogden, D., Hannah, M. J. and Carter, T. (2011). Temperature-dependence of Weibel-Palade body exocytosis and cell surface dispersal of von Willebrand factor and its propolypeptide. PLoS ONE 6, e27314.
38. Huang, J., Motto, D. G., Bundle, D. R. and Sadler, J. E. (2010). Shiga toxin B subunits induce VWF secretion by human endothelial cells and thrombotic microangiopathy in ADAMTS13-deficient mice. Blood 116, 3653-3659.
39. Jackson, M. B. and Chapman, E. R. (2008). The fusion pores of Ca2+ -triggered exocytosis. Nat. Struct. Mol. Biol. 15, 684-689.
40. Jansson, J. H., Nilsson, T. K. and Johnson, O. (1991). von Willebrand factor in plasma: a novel risk factor for recurrent myocardial infarction and death. Br. Heart J. 66, 351-355.
41. Klein, U., Gimpl, G. and Fahrenholz, F. (1995). Alteration of the myometrial plasma membrane cholesterol content with beta-cyclodextrin modulates the binding affinity of the oxytocin receptor. Biochemistry 34, 13784-13793.
42. Knipe, L., Meli, A., Hewlett, L., Bierings, R., Dempster, J., Skehel, P., Hannah, M. J. and Carter, T. (2010). A revised model for the secretion of tPA and cytokines from cultured endothelial cells. Blood 116, 2183-2191.
43. König, J., Prenen, J., Nilius, B. and Gerke, V. (1998). The annexin II-p11 complex is involved in regulated exocytosis in bovine pulmonary artery endothelial cells. J. Biol. Chem. 273, 19679-19684.
44. Koseoglu, S., Love, S. A. and Haynes, C. L. (2011). Cholesterol effects on vesicle pools in chromaffin cells revealed by carbon-fiber microelectrode amperometry. Anal. Bioanal. Chem. 400, 2963-2971.
45. Lip, G. Y. and Blann, A. (1997). von Willebrand factor: a marker of endothelial dysfunction in vascular disorders? Cardiovasc. Res. 34, 255-265.
46. Little, K. Y., Elmer, L. W., Zhong, H., Scheys, J. O. and Zhang, L. (2002). Cocaine induction of dopamine transporter trafficking to the plasma membrane. Mol. Pharmacol. 61, 436-445.
47. Mann, G. E., Pearson, J. D., Sheriff, C. J. and Toothill, V. J. (1989). Expression of amino acid transport systems in cultured human umbilical vein endothelial cells. J. Physiol. 410, 325-339.
48. Marszalek, P. E., Farrell, B., Verdugo, P. and Fernandez, J. M. (1997). Kinetics of release of serotonin from isolated secretory granules. II. Ion exchange determines the diffusivity of serotonin. Biophys. J. 73, 1169-1183.
49. McEwan, M. and Parsons, P. G. (1987). Inhibition of melanization in human melanoma cells by a serotonin uptake inhibitor. J. Invest. Dermatol. 89, 82-86.
50. Mendoza, S. A., Fang, J., Gutterman, D. D., Wilcox, D. A., Bubolz, A. H., Li, R., Suzuki, M. and Zhang, D. X. (2010). TRPV4-mediated endothelial Ca2+ influx and vasodilation in response to shear stress. Am. J. Physiol. 298, H466-H476.
51. Mercado, C. P. and Kilic, F. (2010). Molecular mechanisms of SERT in platelets: regulation of plasma serotonin levels. Mol. Interv. 10, 231-241.
52. Mosharov, E. V. and Sulzer, D. (2005). Analysis of exocytotic events recorded by amperometry. Nat. Methods 2, 651-658.
53. Mothersill, C., Saroya, R., Smith, R. W., Singh, H. and Seymour, C. B. (2010). Serum serotonin levels determine the magnitude and type of bystander effects in medium transfer experiments. Radiat. Res. 174, 119-123.
54. Neco, P., Fernández-Peruchena, C., Navas, S., Gutiérrez, L. M., de Toledo, G. A. and Alés, E. (2008). Myosin II contributes to fusion pore expansion during exocytosis. J. Biol. Chem. 283, 10949-10957.
55. Ni, W. and Watts, S. W. (2006). 5-hydroxytryptamine in the cardiovascular system: focus on the serotonin transporter (SERT). Clin. Exp. Pharmacol. Physiol. 33, 575- 583.
56. Nightingale, T. D., Pattni, K., Hume, A. N., Seabra, M. C. and Cutler, D. F. (2009). Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 113, 5010-5018.
57. Nilius, B., Droogmans, G. and Wondergem, R. (2003). Transient receptor potential channels in endothelium: solving the calcium entry puzzle?. Endothelium 10, 5-15.
58. Obermü ller, S., Lindqvist, A., Karanauskaite, J., Galvanovskis, J., Rorsman, P. and Barg, S. (2005). Selective nucleotide-release from dense-core granules in insulinsecreting cells. J. Cell Sci. 118, 4271-4282.
59. Pérez-Jiménez, F., Castro, P., López-Miranda, J., Paz-Rojas, E., Blanco, A., López- Segura, F., Velasco, F., Marín, C., Fuentes, F. and Ordovás, J. M. (1999). Circulating levels of endothelial function are modulated by dietary monounsaturated fat. Atherosclerosis 145, 351-358.
60. Pike, C. M., Grabner, C. P. and Harkins, A. B. (2009). Fabrication of amperometric electrodes. J. Vis. Exp. 27, e1040.
61. Pulido, I. R., Jahn, R. and Gerke, V. (2011). VAMP3 is associated with endothelial weibel-palade bodies and participates in their Ca2+-dependent exocytosis. Biochim. Biophys. Acta 1813, 1038-1044.
62. Qizilbash, N., Duffy, S., Prentice, C. R., Boothby, M. and Warlow, C. (1997). Von Willebrand factor and risk of ischemic stroke. Neurology 49, 1552-1556.
63. Rojo Pulido, I., Nightingale, T. D., Darchen, F., Seabra, M. C., Cutler, D. F. and Gerke, V. (2011). Myosin Va acts in concert with Rab27a and MyRIP to regulate acute von-Willebrand factor release from endothelial cells. Traffic 12, 1371-1382.
64. Rondaij, M. G., Bierings, R., Kragt, A., van Mourik, J. A. and Voorberg, J. (2006). Dynamics and plasticity of Weibel-Palade bodies in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 26, 1002-1007.
65. Rothberg, K. G., Ying, Y. S., Kamen, B. A. and Anderson, R. G. (1990). Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5- methyltetrahydrofolate. J. Cell Biol. 111, 2931-2938.
66. Sadler, J. E. (1998). Biochemistry and genetics of von Willebrand factor. Annu. Rev. Biochem. 67, 395-424.
67. Schroeder, T. J., Borges, R., Finnegan, J. M., Pihel, K., Amatore, C. and Wightman, R. M. (1996). Temporally resolved, independent stages of individual exocytotic secretion events. Biophys. J. 70, 1061-1068.
68. Schulte, A. and Chow, R. H. (1996). A simple method for insulating carbon-fiber microelectrodes using anodic electrophoretic deposition of paint. Anal. Chem. 68, 3054-3058.
69. Segovia, M., Alés, E., Montes, M. A., Bonifas, I., Jemal, I., Lindau, M., Maximov, A., Sü dhof, T. C. and Alvarez de Toledo, G. (2010). Push-and-pull regulation of the fusion pore by synaptotagmin-7. Proc. Natl. Acad. Sci. USA 107, 19032-19037.
70. Sigurdson, W. J., Sachs, F. and Diamond, S. L. (1993). Mechanical perturbation of cultured human endothelial cells causes rapid increases of intracellular calcium. Am. J. Physiol. 264, H1745-H1752.
71. Soekmadji, C. and Thorn, P. (2010). Secretory control: evidence for agonist regulation of post-fusion vesicle behaviour. Clin. Exp. Pharmacol. Physiol. 37, 218-221.
72. Solbach, T. F., Grube, M., Fromm, M. F. and Zolk, O. (2011). Organic cation transporter 3: expression in failing and nonfailing human heart and functional characterization. J. Cardiovasc. Pharmacol. 58, 409-417.
73. Springer, T. A. (2011). Biology and physics of von Willebrand factor concatamers. J. Thromb. Haemost. 9 Suppl. 1, 130-143.
74. Starke, R. D., Ferraro, F., Paschalaki, K. E., Dryden, N. H., McKinnon, T. A., Sutton, R. E., Payne, E. M., Haskard, D. O., Hughes, A. D., Cutler, D. F. et al. (2011). Endothelial von Willebrand factor regulates angiogenesis. Blood 117, 1071- 1080.
75. Terraube, V., Marx, I. and Denis, C. V. (2007). Role of von Willebrand factor in tumor metastasis. Thromb. Res. 120 Suppl. 2, S64-S70.
76. van Breevoort, D., van Agtmaal, E. L., Dragt, B. S., Gebbinck, J. K., Dienava- Verdoold, I., Kragt, A., Bierings, R., Horrevoets, A. J., Valentijn, K. M., Eikenboom, J. C. et al. (2012). Proteomic screen identifies IGFBP7 as a novel component of endothelial cell-specific Weibel-Palade bodies. J. Proteome Res. 11, 2925-2936.
77. Vardjan, N., Stenovec, M., Jorgacevski, J., Kreft, M. and Zorec, R. (2007). Subnanometer fusion pores in spontaneous exocytosis of peptidergic vesicles. J. Neurosci. 27, 4737-4746.
78. Vardjan, N., Stenovec, M., Jorgacevski, J., Kreft, M., Grilc, S. and Zorec, R. (2009). The fusion pore and vesicle cargo discharge modulation. Ann. N. Y. Acad. Sci. 1152, 135-144.
79. Wagner, D. D. (1990). Cell biology of von Willebrand factor. Annu. Rev. Cell Biol. 6, 217-242.
80. Wang, N., Kwan, C., Gong, X., de Chaves, E. P., Tse, A. and Tse, F. W. (2010). Influence of cholesterol on catecholamine release from the fusion pore of large dense core chromaffin granules. J. Neurosci. 30, 3904-3911.
81. Zhang, J., Xue, R., Ong, W. Y. and Chen, P. (2009). Roles of cholesterol in vesicle fusion and motion. Biophys. J. 97, 1371-1380.
82. Zimmerberg, J. and Chernomordik, L. V. (2005). Neuroscience. Synaptic membranes bend to the will of a neurotoxin. Science 310, 1626-1627.
83. Zografou, S., Basagiannis, D., Papafotika, A., Shirakawa, R., Horiuchi, H., Auerbach, D., Fukuda, M. and Christoforidis, S. (2012). A complete Rab screening reveals novel insights in Weibel-Palade body exocytosis. J. Cell Sci. 125, 4780-4790.