Structural organization of Weibel-Palade bodies revealed by cryo-EM of vitrified endothelial cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 41, 2009, Pages 17407-17412

  Berriman, John A ^a,c   Li, Sam ^a,d   Hewlett, Lindsay J ^b   Wasilewski, Sebastian ^a   Kiskin, Fedir N ^a   Carter, Tom ^b   Hannah, Matthew J ^b   Rosenthal, Peter B ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c University of California at San Francisco ^*  (United Kingdom)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Electron cryomicroscopy; Paracrystal; Tomography; Von Willebrand factor

Indexed keywords

VON WILLEBRAND FACTOR;

ARTICLE; CELL GRANULE; CELL INTERACTION; CELL ORGANELLE; CRYOELECTRON MICROSCOPY; ENDOTHELIUM CELL; FOURIER ANALYSIS; HUMAN; HUMAN CELL; IMAGE RECONSTRUCTION; MODEL; PRIORITY JOURNAL; TOMOGRAPHY; UMBILICAL VEIN; VITRIFICATION; WEIBEL PALADE BODY;

CARRIER PROTEINS; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; ENDOTHELIAL CELLS; FACTOR VIII; HUMANS; MODELS, MOLECULAR; UMBILICAL VEINS; VON WILLEBRAND FACTOR; WEIBEL-PALADE BODIES;

EID: 70350445710     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902977106     Document Type: Article

References (51)

1. Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67:395-424. (Pubitemid 28411134)
2. Purvis AR, et al. (2007) Two Cys residues essential for Von Willebrand factor multimer assembly in the Golgi. Proc Natl Acad Sci USA 104:15647-15652.
3. Purvis AR, Sadler JE (2004) A covalent oxidoreductase intermediate in propeptide-dependent von Willebrand factor multimerization. J Biol Chem 279:49982-49988. (Pubitemid 39577807)
4. Weibel ER, Palade GE (1964) New cytoplasmic components in arterial endothelia. J Cell Biol 23:101-112.
5. Babich V, et al. (2008) Selective release of molecules from Weibel-Palade bodies during a lingering kiss. Blood 111:5282-5290.
6. Ewenstein BM, Warhol MJ, Handin RI, Pober JS (1987) Composition of the Von Willebrand-factor storage organelle (Weibel-Palade body) isolated from cultured human umbilical vein endothelial cells. J Cell Biol 104:1423-1433.
7. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA (2009) Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science 324:1330-1334.
8. Harrison-Lavoie KJ, et al. (2006) P-selectin and CD63 use different mechanisms for delivery to Weibel-Palade bodies. Traffic 7:647-662.
9. Hannah MJ, et al. (2003) Weibel-Palade bodies recruit Rab27 by a content-driven, maturation-dependent mechanism that is independent of cell type. J Cell Sci 116:3939-3948.
10. Knop M, Aareskjold E, Bode G, Gerke V (2004) Rab3D and annexin A2 play a role in regulated secretion of vWF, but not tPA, from endothelial cells. EMBO J 23:2982-2992. (Pubitemid 39093592)
11. Kobayashi T, et al. (2000) The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol Biol Cell 11:1829-1843. (Pubitemid 30307916)
12. Wagner DD, et al. (1991) Induction of specific storage organelles by von Willebrand factor propolypeptide. Cell 64:403-413. (Pubitemid 121001264)
13. Hoenger A, McIntosh JR (2009) Probing the macromolecular organization of cells by electron tomography. Curr Opin Cell Biol 21:89-96.
14. Leis A, Rockel B, Andrees L, Baumeister W (2009) Visualizing cells at the nanoscale. Trends Biochem Sci 34:60-70.
15. McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: An introduction to electron tomography. Trends Cell Biol 15:43-51. (Pubitemid 40094680)
16. Comolli LR, Downing KH (2005) Dose tolerance at helium and nitrogen temperatures for whole cell electron tomography. J Struct Biol 152:149-156.
17. Henderson GP, Gan L, Jensen GJ (2007) 3-D ultrastructure of O. tauri: Electron cryotomography of an entire eukaryotic cell. PLoS One 2:e749. (Pubitemid 351338867)
18. Grunewald K, Medalia O, Gross A, Steven AC, Baumeister W (2003) Prospects of electron cryotomography to visualize macromolecular complexes inside cellular compartments: Implications of crowding. Biophys Chem 100:577-591. (Pubitemid 36338067)
19. Koning RI, et al. (2008) Cryo electron tomography of vitrified fibroblasts: Microtubule plus ends in situ. J Struct Biol 161:459-468.
20. Medalia O, et al. (2002) Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298:1209-1213. (Pubitemid 35285482)
21. Al-Amoudi A, et al. (2004) Cryo-electron microscopy of vitreous sections. EMBO J 23:3583-3588.
22. Gruska M, Medalia O, Baumeister W, Leis A (2008) Electron tomography of vitreous sections from cultured mammalian cells. J Struct Biol 161:384-392.
23. Valentijn KM, Valentijn JA, Jansen KA, Koster AJ (2008) A new look at Weibel-Palade body structure in endothelial cells using electron tomography. J Struct Biol 161:447-458.
24. Zenner HL, Collinson LM, Michaux G, Cutler DF (2007) High-pressure freezing provides insights into Weibel-Palade body biogenesis. J Cell Sci 120:2117-2125. (Pubitemid 47010006)
25. Huang RH, et al. (2008) Assembly of Weibel-Palade body-like tubules from N-terminal domains of von Willebrand factor. Proc Natl Acad Sci USA 105:482-487.
26. Henderson R (1995) The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. Q Rev Biophys 28:171-193.
27. Grimm R, et al. (1998) Electron tomography of ice-embedded prokaryotic cells. Biophys J 74:1031-1042. (Pubitemid 28345298)
28. Koster AJ, et al. (1997) Perspectives of molecular and cellular electron tomography. J Struct Biol 120:276-308.
29. Dubochet J, Lepault J, Freeman R, Berriman JA, Homo J-C (1982) Electron microscopy of frozen water and aqueous solutions. J Microsc 128:219-237.
30. Matsui T, Titani K, Mizuochi T (1992) Structures of the asparagine-linked oligosaccharide chains of human Von Willebrand factor-occurrence of blood group A, Group B, and group H(O) structures. J Biol Chem 267:8723-8731.
31. Lui-Roberts WW, Collinson LM, Hewlett LJ, Michaux G, Cutler DF (2005) An AP-1/clathrin coat plays a novel and essential role in forming the Weibel-Palade bodies of endothelial cells. J Cell Biol 170:627-636. (Pubitemid 41186937)
32. Nightingale TD, Pattni K, Hume AN, Seabra MC, Cutler DF (2009) Rab27a and MyRIP regulate the amount and multimeric state of VWF released from endothelial cells. Blood 113:5010-5018.
33. Murk JL, et al. (2003) Influence of aldehyde fixation on the morphology of endosomes and lysosomes: Quantitative analysis and electron tomography. J Microsc 212:81-90. (Pubitemid 37267054)
34. Futter CE, Pearse A, Hewlett LJ, Hopkins CR (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J Cell Biol 132:1011-1023. (Pubitemid 26105491)
35. Eskelinen EL (2008) Fine structure of the autophagosome. Methods Mol Biol 445:11-28.
36. Michaux G, et al. (2006) The physiological function of von Willebrand's factor depends on its tubular storage in endothelial Weibel-Palade bodies. Dev Cell 10:223-232. (Pubitemid 43174955)
37. Fowler WE, Fretto LJ, Hamilton KK, Erickson HP, McKee PA (1985) Substructure of human von Willebrand factor. J Clin Invest 76:1491-1500.
38. Michaux G, Pullen TJ, Haberichter SL, Cutler DF (2006) P-selectin binds to the D'-D3 domains of von Willebrand factor in Weibel-Palade bodies. Blood 107:3922-3924. (Pubitemid 43726797)
39. Cohen AE, Mahadevan L (2003) Kinks, rings, and rackets in filamentous structures. Proc Natl Acad Sci USA 100:12141-12146.
40. Erent M, et al. (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. (Pubitemid 47244253)
41. Arvan P, Castle D (1998) Sorting and storage during secretory granule biogenesis: Looking backward and looking forward. Biochem J 332:593-610. (Pubitemid 28306683)
42. Thiele C, Huttner WB (1998) Protein and lipid sorting from the trans-Golgi network to secretory granules-recent developments. Semin Cell Dev Biol 9:511-516. (Pubitemid 128353016)
43. Arribas M, Cutler DF (2000) Weibel-Palade body membrane proteins exhibit differential trafficking after exocytosis in endothelial cells. Traffic 1:783-793.
44. Mastronarde DN (1997) Dual-axis tomography: An approach with alignment methods that preserve resolution. J Struct Biol 120:343-352.
45. Heymann JB, Cardone G, Winkler DC, Steven AC (2008) Computational resources for cryo-electron tomography in Bsoft. J Struct Biol 161:232-242.
46. Chen H, Hughes DD, Chan TA, Sedat JW, Agard DA (1996) IVE (Image Visualization Environment): A software platform for all three-dimensional microscopy applications. J Struct Biol 116:56-60. (Pubitemid 26093123)
47. Crowther RA, Henderson R, Smith JM (1996) MRC image processing programs. J Struct Biol 116:9-16.
48. Frank J, et al. (1996) SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116:190-199. (Pubitemid 26093143)
49. Egelman EH (2000) A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy 85:225-234.
50. Egelman EH (2007) The iterative helical real space reconstruction method: Surmounting the problems posed by real polymers. J Struct Biol 157:83-94.
51. Hannah MJ, et al. (2005) 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 280:22827-22830.