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E. Karampini et al.
Disclosures
No conflicts of interest to disclose.
Contributions
EK, PB, JO and AAM performed research and analyzed data; CRJ and DG contributed vital reagents and expertise; EK, JV and RB designed the research; EK, JV and RB wrote the paper.
Funding
This study was supported by grants from the Landsteiner Stichting voor Bloedtransfusie Research (LSBR-1517 and LSBR- 1707), the Netherlands Ministry of Health (PPOC-2015-24P) and the Dutch Thrombosis Foundation (TSN 2017-01).
References
1. Gomez-Navarro N, Miller E. Protein sorting at the ER-Golgi interface. J Cell Biol. 2016;215(6):769-778.
2. Araki K, Nagata K. Protein folding and qual- ity control in the ER. Cold Spring Harb Perspect Biol. 2011;3(11):1-25.
3.Kienzle C, von Blume J. Secretory cargo sorting at the trans-Golgi network. Trends Cell Biol. 2014;24(10):584-593.
4. Halban PA, Irminger JC. Sorting and pro- cessing of secretory proteins. Biochem J. 1994;299(1):1-18.
5. Huizing M, Helip-Wooley A, Westbroek W, Gunay-Aygun M, Gahl WA. Disorders of lysosome-related organelle biogenesis: clini- cal and molecular genetics. Annu Rev Genomics Hum Genet. 2008;9:359-386.
6. Weibel ER, Palade GE. New cytoplasmic components in arterial endothelia. J Cell Biol. 1964;23(1):101-112.
7. Schillemans M, Karampini E, Kat M, Bierings R. Exocytosis of Weibel–Palade bodies: how to unpack a vascular emer- gency kit. J Thromb Haemost. 2019;17(1):6- 18.
8. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem. 1998;67:395-424.
9. Wagner DD, Saffaripour S, Bonfanti R, et al. Induction of specific storage organelles by von Willebrand factor propolypeptide. Cell. 1991;64(2):403-413.
10. Voorberg J, Fontijn R, Calafat J, Janssen H, van Mourik JA, Pannekoek H. Biogenesis of von Willebrand factor-containing organelles in heterologous transfected CV-1 cells. EMBO J. 1993;12(2):749-758.
11. Groeneveld DJ, van Bekkum T, Dirven RJ, et al. Angiogenic characteristics of blood out- growth endothelial cells from patients with von Willebrand disease. J Thromb Haemost. 2015;13(10):1854-1866.
12. Schillemans M, Kat M, Westeneng J, et al. Alternative trafficking of Weibel-Palade body proteins in CRISPR/Cas9-engineered von Willebrand factor-deficient blood out- growth endothelial cells. Res Pract Thromb Haemost. 2019;3(4):718-732.
13. Michaux G, Abbitt KB, Collinson LM, Haberichter SL, Norman KE, Cutler DF. The physiological function of von Willebrand’s factor depends on its tubular storage in endothelial Weibel-Palade bodies. Dev Cell. 2006;10(2):223-232.
14. Huang R-H, Wang Y, Roth R, et al. Assembly of Weibel Palade body-like tubules from N-terminal domains of von Willebrand factor. Proc Natl Acad Sci U S A. 2008;105(2):482-487.
15. Berriman JA, Li S, Hewlett LJ, et al. Structural organization of Weibel-Palade bodies revealed by cryo-EM of vitrified endothelial cells. Proc Natl Acad Sci U S A. 2009;106(41):17407-17412.
16. Leebeek FWG, Eikenboom JCJ. Von Willebrand’s disease. N Engl J Med.
2016;375(21):2067-2080.
17. Valentijn KM, Eikenboom J. Weibel-Palade
bodies: a window to von Willebrand dis- ease. J Thromb Haemost. 2013;11(4):581- 592.
18. Conte IL, Cookson E, Hellen N, Bierings R, Mashanov G, Carter T. Is there more than one way to unpack a Weibel-Palade body? Blood. 2015;126(18):2165-2167.
19. Dong JF, Moake JL, Nolasco L, et al. ADAMTS-13 rapidly cleaves newly secret- ed ultralarge von Willebrand factor multi- mers on the endothelial surface under flowing conditions. Blood. 2002;100(12): 4033-4039.
20. Zheng Y, Chen J, López JA. Flow-driven assembly of VWF fibres and webs in in vitro microvessels. Nat Commun. 2015;6(1):7858.
21. De Ceunynck K, De Meyer SF, Vanhoorelbeke K. Unwinding the von Willebrand factor strings puzzle. Blood. 2013;121(2):270-277.
22. Sadler JE. von Willebrand factor assembly and secretion. J Thromb Haemost. 2009;7(Suppl 1):24-27.
23. Ferraro F, da Silva ML, Grimes W, et al. Weibel-Palade body size modulates the adhesive activity of its von Willebrand factor cargo in cultured endothelial cells. Sci Rep. 2016;6(1):32473.
24. Ferraro F, Kriston-Vizi J, Metcalf DJ, et al. A two-tier Golgi-based control of organelle size underpins the functional plasticity of endothelial cells. Dev Cell. 2014;29(3):292- 304.
25. Springer TA. von Willebrand factor, Jedi knight of the bloodstream. Blood. 2014;124(9):1412-1426.
26. Zhou Y-F, Eng ET, Nishida N, Lu C, Walz T, Springer TA. A pH-regulated dimeric bou- quet in the structure of von Willebrand fac- tor. EMBO J. 2011;30(19):4098-4111.
27. Purvis AR, Gross J, Dang LT, et al. Two Cys residues essential for von Willebrand factor multimer assembly in the Golgi. Proc Natl Acad Sci U S A. 2007;104(40):15647-15652.
28. Zenner HL, Collinson LM, Michaux G, Cutler DF. High-pressure freezing provides insights into Weibel-Palade body biogenesis. J Cell Sci. 2007;120(Pt 12):2117-2125.
29. Mourik MJ, Faas FGA, Zimmermann H, Voorberg J, Koster AJ, Eikenboom J. Content delivery to newly forming Weibel-Palade bodies is facilitated by multiple connections with the Golgi apparatus. Blood. 2015;125(22):3509-3516.
30. Jahn R, Scheller RH. SNAREs - engines for membrane fusion. Nat Rev Mol Cell Biol 2006;7(9):631-643.
31. Daste F, Galli T, Tareste D. Structure and function of longin SNAREs. J Cell Sci. 2015;128(23):4263-4272.
32. Lenzi C, Stevens J, Osborn D, Hannah MJ, Bierings R, Carter T. Synaptotagmin 5 regu- lates Ca 2+ -dependent Weibel–Palade body exocytosis in human endothelial cells. J Cell Sci. 2019;132(5):jcs221952.
33. Schillemans M, Karampini E, van den
Eshof BL, et al. Weibel-palade body local- ized syntaxin-3 modulates von Willebrand factor secretion from endothelial cells. Arterioscler Thromb Vasc Biol. 2018;38(7): 1549-1561.
34. Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11(8):783-784.
35. Haeussler M, Schönig K, Eckert H, et al. E- valuation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 2016;17(1):148.
36. van Breevoort D, Snijders AP, Hellen N, et al. STXBP1 promotes Weibel-Palade body exo- cytosis through its interaction with the Rab27A effector Slp4-a. Blood. 2014;123 (20):3185-3194.
37. Karampini E, Schillemans M, Hofman M, et al. Defective AP-3-dependent VAMP8 traf- ficking impairs Weibel-Palade body exocy- tosis in Hermansky-Pudlak syndrome type 2 blood outgrowth endothelial cells. Haematologica. 2019;104(10):2091-2099.
38. Vischer U, Wagner D. von Willebrand factor proteolytic processing and multimerization precede the formation of Weibel-Palade bodies. Blood. 1994;83(12):3536-3544.
39.Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood. 2008;112 (4):957-964.
40.
Lopes da Silva M, Cutler DF. von Willebrand factor multimerization and the polarity of secretory pathways in endothelial cells. Blood. 2016;128(2):277-285.
41.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.
42. 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.
43. Jani RA, Purushothaman LK, Rani S, Bergam P, Setty SRG. STX13 regulates cargo delivery from recycling endosomes during melanosome biogenesis. J Cell Sci. 2015;128(17):3263-3276.
44. Koseoglu S, Peters CG, Fitch-Tewfik JL, et al. VAMP-7 links granule exocytosis to actin reorganization during platelet activation. Blood. 2015;126(5):651-660.
45.
46.
47.
Kweon Y, Rothe A, Conibear E, Stevens TH. Ykt6p is a multifunctional yeast R-SNARE that is required for multiple membrane transport pathways to the vacuole. Mol Biol Cell. 2003;14(5):1868-1881.
Matsui T, Jiang P, Nakano S, Sakamaki Y, Yamamoto H, Mizushima N. Auto- phagosomal YKT6 is required for fusion with lysosomes independently of syntaxin 17. J Cell Biol. 2018;217(8):2633-2645.
Dai J, Lu Y, Wang C, et al. Vps33b regulates Vwf-positive vesicular trafficking in
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