STXBP1 promotes Weibel-Palade body exocytosis through its interaction with the Rab27A effector Slp4-a

Blood

Volumn 123, Issue 20, 2014, Pages 3185-3194

  Van Breevoort, Dorothee ^a   Snijders, Ambrosius P ^b   Hellen, Nicola ^c,d   Weckhuysen, Sarah ^e   Van Hooren, Kathinka W E M ^a   Eikenboom, Jeroen ^f   Valentijn, Karine ^f   Fernandez Borja, Mar ^g   Ceulemans, Berten ^h   De Jonghe, Peter ^e   Voorberg, Jan ^a   Hannah, Matthew ^c,i   Carter, Tom ^c,j   Bierings, Ruben ^a,c  

^a CENTRAL LABORATORY   (Netherlands)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^d NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^g ACADEMIC MEDICAL CENTER   (Netherlands)

^h ANTWERP UNIVERSITY HOSPITAL   (Belgium)

ⁱ PUBLIC HEALTH ENGLAND   (United Kingdom)

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

more..

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; SNARE PROTEIN; SYNAPTOTAGMIN; SYNAPTOTAGMIN LIKE PROTEIN 4 A; SYNTAXIN; SYNTAXIN 2; SYNTAXIN 3; SYNTAXIN 4; SYNTAXIN BINDING PROTEIN 1; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ARTICLE; CONTROLLED STUDY; EARLY INFANTILE EPILEPTIC ENCEPHALOPATHY; ENDOTHELIUM CELL; EPILEPSY; EXOCYTOSIS; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RNA INTERFERENCE; WEIBEL PALADE BODY;

CELLS, CULTURED; ENDOTHELIAL CELLS; EXOCYTOSIS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MUNC18 PROTEINS; PROTEIN INTERACTION MAPS; QA-SNARE PROTEINS; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SYNTAXIN 1; VESICULAR TRANSPORT PROTEINS; WEIBEL-PALADE BODIES;

EID: 84903201392     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-10-535831     Document Type: Article

References (60)

1. Lowenstein CJ, Morrell CN, Yamakuchi M. Regulation of Weibel-Palade body exocytosis. Trends Cardiovasc Med. 2005;15(8):302-308. (Pubitemid 41613876)
2. Michaux G, Cutler DF. How to roll an endothelial cigar: the biogenesis of Weibel-Palade bodies. Traffic. 2004;5(2):69-78. (Pubitemid 38196019)
3. Rondaij MG, Bierings R, Kragt A, van Mourik JA, Voorberg J. Dynamics and plasticity of Weibel-Palade bodies in endothelial cells. Arterioscler Thromb Vasc Biol. 2006;26(5):1002-1007. (Pubitemid 43732104)
4. Bonfanti R, Furie BC, Furie B, Wagner DD. PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells. Blood. 1989;73(5):1109-1112. (Pubitemid 19107409)
5. Knipe L, Meli A, Hewlett L, et al. A revised model for the secretion of tPA and cytokines from cultured endothelial cells. Blood. 2010;116(12):2183- 2191.
6. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest. 1989;84(1):92-99. (Pubitemid 19170099)
7. Utgaard JO, Jahnsen FL, Bakka A, Brandtzaeg P, Haraldsen G. Rapid secretion of prestored interleukin 8 from Weibel-Palade bodies of microvascular endothelial cells. J Exp Med. 1998;188(9):1751-1756. (Pubitemid 28516119)
8. Vischer UM, Wagner DD. CD63 is a component of Weibel-Palade bodies of human endothelial cells. Blood. 1993;82(4):1184-1191. (Pubitemid 23253992)
9. Wolff B, Burns AR, Middleton J, Rot A. Endothelial cell "memory" of inflammatory stimulation: human venular endothelial cells store interleukin 8 in Weibel-Palade bodies. J Exp Med. 1998;188(9):1757-1762. (Pubitemid 28516120)
10. Doyle EL, Ridger V, Ferraro F, Turmaine M, Saftig P, Cutler DF. CD63 is an essential cofactor to leukocyte recruitment by endothelial P-selectin. Blood. 2011;118(15):4265-4273.
11. Fiedler U, Scharpfenecker M, Koidl S, et al. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood. 2004;103(11):4150-4156. (Pubitemid 38685356)
12. Starke RD, Ferraro F, Paschalaki KE, et al. Endothelial von Willebrand factor regulates angiogenesis. Blood. 2011;117(3):1071-1080.
13. van Breevoort D, van Agtmaal EL, Dragt BS, et al. Proteomic screen identifies IGFBP7 as a novel component of endothelial cell-specific Weibel-Palade bodies. J Proteome Res. 2012;11(5): 2925-2936.
14. Bierings R, van den Biggelaar M, Kragt A, Mertens K, Voorberg J, van Mourik JA. Efficiency of von Willebrand factor-mediated targeting of interleukin-8 into Weibel-Palade bodies. J Thromb Haemost. 2007;5(12):2512-2519. (Pubitemid 350154363)
15. Øynebråten I, Bakke O, Brandtzaeg P, Johansen FE, Haraldsen G. Rapid chemokine secretion from endothelial cells originates from 2 distinct compartments. Blood. 2004;104(2):314-320. (Pubitemid 38900009)
16. van Agtmaal EL, Bierings R, Dragt BS, et al. The shear stress-induced transcription factor KLF2 affects dynamics and angiopoietin-2 content of Weibel-Palade bodies. PLoS ONE. 2012;7(6):e38399.
17. Kaufmann JE, Oksche A, Wollheim CB, Günther G, Rosenthal W, Vischer UM. Vasopressininduced von Willebrand factor secretion from endothelial cells involves V2 receptors and cAMP. J Clin Invest. 2000;106(1):107-116. (Pubitemid 30437246)
18. Loesberg C, Gonsalves MD, Zandbergen J, et al. The effect of calcium on the secretion of factor VIIIrelated antigen by cultured human endothelial cells. Biochim Biophys Acta. 1983;763(2):160-168. (Pubitemid 13012207)
19. van Hooren KW, van Agtmaal EL, Fernandez-Borja M, van Mourik JA, Voorberg J, Bierings R. The Epac-Rap1 signaling pathway controls cAMP-mediated exocytosis of Weibel-Palade bodies in endothelial cells. J Biol Chem. 2012; 287(29):24713-24720.
20. Vischer UM, Wollheim CB. Epinephrine induces von Willebrand factor release from cultured endothelial cells: involvement of cyclic AMPdependent signalling in exocytosis. Thromb Haemost. 1997;77(6):1182-1188. (Pubitemid 27311992)
21. de Leeuw HP, Fernandez-Borja M, Reits EA, et al. Small GTP-binding protein Ral modulates regulated exocytosis of von Willebrand factor by endothelial cells. Arterioscler Thromb Vasc Biol. 2001;21(6):899-904. (Pubitemid 34168643)
22. Hannah MJ, Hume AN, Arribas M, et al. Weibel-Palade bodies recruit Rab27 by a content-driven, maturation-dependent mechanism that is independent of cell type. J Cell Sci. 2003; 116(Pt 19):3939-3948. (Pubitemid 37279309)
23. Knop M, Aareskjold E, Bode G, Gerke V. Rab3D and annexin A2 play a role in regulated secretion of vWF, but not tPA, from endothelial cells. EMBO J. 2004;23(15):2982-2992. (Pubitemid 39093592)
24. Rondaij MG, Bierings R, van Agtmaal EL, et al. Guanine exchange factor RalGDS mediates exocytosis of Weibel-Palade bodies from endothelial cells. Blood. 2008;112(1):56-63.
25. Zografou S, Basagiannis D, Papafotika A, et al. A complete Rab screening reveals novel insights in Weibel-Palade body exocytosis. J Cell Sci. 2012;125(Pt 20):4780-4790.
26. Fukuda M. Rab27 effectors, pleiotropic regulators in secretory pathways. Traffic. 2013;14(9): 949-963.
27. Nightingale TD, Pattni K, Hume AN, Seabra MC, Cutler DF. Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood. 2009;113(20): 5010-5018.
28. Rojo Pulido I, Nightingale TD, Darchen F, Seabra MC, Cutler DF, Gerke V. Myosin Va acts in concert with Rab27a and MyRIP to regulate acute von-Willebrand factor release from endothelial cells. Traffic. 2011;12(10):1371-1382.
29. Bierings R, Hellen N, Kiskin N, et al. The interplay between the Rab27A effectors Slp4-a and MyRIP controls hormone-evoked Weibel-Palade body exocytosis. Blood. 2012;120(13):2757-2767.
30. Deprez L, Weckhuysen S, Holmgren P, et al. Clinical spectrum of early-onset epileptic encephalopathies associated with STXBP1 mutations. Neurology. 2010;75(13):1159-1165.
31. Saitsu H, Kato M, Mizuguchi T, et al. De novo mutations in the gene encoding STXBP1 (MUNC18-1) cause early infantile epileptic encephalopathy. Nat Genet. 2008;40(6):782-788. (Pubitemid 351748868)
32. Weckhuysen S, Holmgren P, Hendrickx R, et al. Reduction of seizure frequency after epilepsy surgery in a patient with STXBP1 encephalopathy and clinical description of six novel mutation carriers. Epilepsia. 2013;54(5):e74-e80.
33. Martin-Ramirez J, Hofman M, van den Biggelaar M, Hebbel RP, Voorberg J. Establishment of outgrowth endothelial cells from peripheral blood. Nat Protoc. 2012;7(9):1709-1715.
34. Dull T, Zufferey R, Kelly M, et al. A thirdgeneration lentivirus vector with a conditional packaging system. J Virol. 1998;72(11): 8463-8471. (Pubitemid 28471781)
35. Hannah MJ, Skehel P, Erent M, Knipe L, Ogden D, Carter T. Differential kinetics of cell surface loss of von Willebrand factor and its propolypeptide after secretion from Weibel- Palade bodies in living human endothelial cells. J Biol Chem. 2005;280(24):22827-22830. (Pubitemid 40853189)
36. Erent M, Meli A, Moisoi N, et al. Rate, extent and concentration dependence of histamine-evoked Weibel-Palade body exocytosis determined from individual fusion events in human endothelial cells. J Physiol. 2007;583(Pt 1):195-212. (Pubitemid 47244253)
37. Fukuda M. Slp4-a/granuphilin-a inhibits densecore vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12 cells. J Biol Chem. 2003;278(17):15390-15396. (Pubitemid 36799878)
38. Kuroda TS, Fukuda M, Ariga H, Mikoshiba K. The Slp homology domain of synaptotagmin-like proteins 1-4 and Slac2 functions as a novel Rab27A binding domain. J Biol Chem. 2002; 277(11):9212-9218. (Pubitemid 34953001)
39. van Hooren KW, van Breevoort D, Fernandez-Borja M, et al. Phosphatidylinositol-3,4,5- triphosphate-dependent Rac exchange factor 1 (PREX1) regulates epinephrine induced exocytosis of Weibel-Palade bodies. J Thromb Haemost. 2014;12(2):273-281.
40. Oh E, Kalwat MA, Kim MJ, Verhage M, Thurmond DC. Munc18-1 regulates first-phase insulin release by promoting granule docking to multiple syntaxin isoforms. J Biol Chem. 2012;287(31):25821-25833.
41. Tomas A, Meda P, Regazzi R, Pessin JE, Halban PA. Munc 18-1 and granuphilin collaborate during insulin granule exocytosis. Traffic. 2008;9(5):813-832. (Pubitemid 351494309)
42. Toonen RF, Wierda K, Sons MS, et al. Munc18-1 expression levels control synapse recovery by regulating readily releasable pool size. Proc Natl Acad Sci USA. 2006;103(48):18332-18337. (Pubitemid 44871658)
43. Verhage M, Maia AS, Plomp JJ, et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 2000;287(5454):864-869. (Pubitemid 30084331)
44. Voets T, Toonen RF, Brian EC, et al. Munc18-1 promotes large dense-core vesicle docking. Neuron. 2001;31(4):581-591. (Pubitemid 32835113)
45. Fukuda M, Imai A, Nashida T, Shimomura H. Slp4-a/granuphilin-a interacts with syntaxin-2/3 in a Munc18-2-dependent manner. J Biol Chem. 2005;280(47):39175-39184. (Pubitemid 41713869)
46. Fu J, Naren AP, Gao X, Ahmmed GU, Malik AB. Protease-activated 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. 2005;280(5):3178-3184. (Pubitemid 40223779)
47. Fukuda M, Kanno E, Saegusa C, Ogata Y, Kuroda TS. Slp4-a/granuphilin-a regulates densecore vesicle exocytosis in PC12 cells. J Biol Chem. 2002;277(42):39673-39678. (Pubitemid 35190949)
48. Michaux G, Dyer CE, Nightingale TD, Gallaud E, Nurrish S, Cutler DF. A role for Rab10 in von Willebrand factor release discovered by an AP-1 interactor screen in C. elegans. J Thromb Haemost. 2011;9(2):392-401.
49. Gálvez-Santisteban M, Rodriguez-Fraticelli AE, Bryant DM, et al. Synaptotagmin-like proteins control the formation of a single apical membrane domain in epithelial cells. Nat Cell Biol. 2012;14(8):838-849.
50. Hampson A, O'Connor A, Smolenski A. Synaptotagmin-like protein 4 and Rab8 interact and increase dense granule release in platelets. J Thromb Haemost. 2013;11(1):161-168.
51. Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature. 2012;490(7419):201-207.
52. Smith NL, Chen MH, Dehghan A, et al Wellcome Trust Case Control Consortium. Novel associations of multiple genetic loci with plasma levels of factor VII, factor VIII, and von Willebrand factor: the CHARGE (Cohorts for Heart and Aging Research in Genome Epidemiology) Consortium. Circulation. 2010;121(12):1382-1392.
53. Smith NL, Rice KM, Bovill EG, et al. Genetic variation associated with plasma von Willebrand factor levels and the risk of incident venous thrombosis. Blood. 2011;117(22):6007-6011.
54. van Loon JE, Leebeek FW, Deckers JW, et al. Effect of genetic variations in syntaxin-binding protein-5 and syntaxin-2 on von Willebrand factor concentration and cardiovascular risk. Circ Cardiovasc Genet. 2010;3(6):507-512.
55. van Loon JE, Sanders YV, de Wee EM, Kruip MJ, de Maat MP, Leebeek FW. Effect of genetic variation in STXBP5 and STX2 on von Willebrand factor and bleeding phenotype in type 1 von Willebrand disease patients. PLoS ONE. 2012; 7(7):e40624.
56. Sadler JE, Rodeghiero F; ISTH SSC Subcommittee on von Willebrand Factor. Provisional criteria for the diagnosis of VWD type1. J Thromb Haemost. 2005;3(4):775-777. (Pubitemid 41647892)
57. Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood. 2008;112(4):957-964.
58. Wang JW, Bouwens EA, Pintao MC, et al. Analysis of the storage and secretion of von Willebrand factor in blood outgrowth endothelial cells derived from patients with von Willebrand disease. Blood. 2013;121(14): 2762-2772.
59. Pulido IR, Jahn R, Gerke V. VAMP3 is associated with endothelial Weibel-Palade bodies and participates in their Ca(21)-dependent exocytosis. Biochim Biophys Acta. 2011;1813(5):1038-1044.
60. Cookson EA, Conte IL, Dempster J, Hannah MJ, Carter T. Characterisation of Weibel-Palade body fusion by amperometry in endothelial cells reveals fusion pore dynamics and the effect of cholesterol on exocytosis. J Cell Sci. 2013;126(Pt 23):5490-5499.