A pH-regulated dimeric bouquet in the structure of von Willebrand factor

EMBO Journal

Volumn 30, Issue 19, 2011, Pages 4098-4111

  Zhou, Yan Feng ^a   Eng, Edward T ^a   Nishida, Noritaka ^b   Lu, Chafen ^a   Walz, Thomas ^c   Springer, Timothy A ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTINE; DIMER; RACEMASE; VON WILLEBRAND FACTOR;

ALKALINITY; AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CROSS LINKING; DISULFIDE BOND; EMBRYO; HEMOSTASIS; HUMAN; HUMAN CELL; MOLECULAR SIZE; PH; PLASMA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECRETION; PROTEIN STRUCTURE;

BLOOD FLOW VELOCITY; BLOOD PLATELETS; DIMERIZATION; DISULFIDES; ENDOTHELIUM, VASCULAR; HEK293 CELLS; HEMOSTASIS; HUMANS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, ELECTRON; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; VON WILLEBRAND FACTOR; WEIBEL-PALADE BODIES;

EID: 80053588028     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.297     Document Type: Article

References (46)

1. Berriman JA, Li S, Hewlett LJ, Wasilewski S, Kiskin FN, Carter T, Hannah MJ, Rosenthal PB (2009) Structural organization of Weibel-Palade bodies revealed by cryo-EM of vitrified endothelial cells. Proc Natl Acad Sci USA 106: 17407-17412
2. Bienkowska J, Cruz M, Atiemo A, Handin R, Liddington R (1997) The von Willebrand factor A3 domain does not contain a metal ion-dependent adhesion site motif. J Biol Chem 272: 25162-25167 (Pubitemid 27415701)
3. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, Behr J (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 92: 7297-7301
4. Celikel R, Varughese KI, Madhusudan, Yoshioka A, Ware J, Ruggeri ZM (1998) Crystal structure of the von Willebrand factor A1 domain in complex with the function blocking NMC-4 Fab. Nat Struct Biol 5: 189-194 (Pubitemid 28113749)
5. Chen X, Xie C, Nishida N, Li Z, Walz T, Springer TA (2010) Requirement of open headpiece conformation for activation of leukocyte integrin aXb2. Proc Natl Acad Sci USA 107 : 14727-14732
6. Cohen-Salmon M, El-Amraoui A, Leibovici M, Petit C (1997) Otogelin: a glycoprotein specific to the acellular membranes of the inner ear. Proc Natl Acad Sci USA 94: 14450-14455 (Pubitemid 28041394)
7. Emsley J, Cruz M, Handin R, Liddington R (1998) Crystal structure of the von Willebrand factor A1 domain and implications for the binding of platelet glycoprotein Ib. J Biol Chem 273: 10396-10401 (Pubitemid 28227648)
8. Erent M, Meli A, Moisoi N, Babich V, Hannah MJ, Skehel P, Knipe L, Zupancic G, Ogden D, 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 (Part 1): 195-212 (Pubitemid 47244253)
9. 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 (Pubitemid 17084500)
10. Fowler WE, Fretto LJ, Hamilton KK, Erickson HP, McKee PA (1985) Substructure of human von Willebrand factor. J Clin Invest 76: 1491-1500 (Pubitemid 16193699)
11. Girma JP, Chopek MW, Titani K, Davie EW (1986) Limited proteo-lysis of human von Willebrand factor by Staphylococcus aureus V-8 protease: isolation and partial characterization of a platelet-binding domain. Biochemistry 25: 3156-3163 (Pubitemid 16056958)
12. Goto A, Kumagai T, Kumagai C, Hirose J, Narita H, Mori H, Kadowaki T, Beck K, Kitagawa Y (2001) A Drosophila haemo-cyte-specific protein, hemolectin, similar to human von Willebrand factor. Biochem J 359(Part 1): 99-108 (Pubitemid 32939211)
13. Haberichter SL, Fahs SA, Montgomery RR (2000) von Willebrand factor storage and multimerization: 2 independent intracellular processes. Blood 96: 1808-1815 (Pubitemid 30661065)
14. Huang RH, Wang Y, Roth R, Yu X, Purvis AR, Heuser JE, Egelman EH, Sadler JE (2008) Assembly of Weibel-Palade body-like tubules from N-terminal domains of von Willebrand factor. Proc Natl Acad Sci USA 105 : 482-487 (Pubitemid 351171734)
15. Huizinga EG, Martijn van der Plas R, Kroon J, Sixma JJ (1997) Crystal structure of the A3 domain of human von Willebrand factor: imlications for collagen binding. Structure 5: 1147-1156
16. Katsumi A, Tuley EA, Bodo I, Sadler JE (2000) Localization of disulfide bonds in the cystine knot domain of human von Willebrand factor. J Biol Chem 275: 25585-25594
17. Li F, Erickson HP, James JA, Moore KL, Cummings RD, McEver RP (1996) Visualization of P-selectin glycoprotein ligand-1 as a highly extended molecule and mapping of protein epitopes for monoclonal antibodies. J Biol Chem 271: 6342-6348 (Pubitemid 26095442)
18. Marti T, Rosselet SJ, Titani K, Walsh KA (1987) Identification of disulfide-bridged substructures within human von Willebrand factor. Biochemistry 26: 8099-8109 (Pubitemid 18023058)
19. Matsushita T, Sadler JE (1995) Identification of amino acid residues essential for von Willebrand factor binding to platelet glyco-protein Ib. Charged-to-alanine scanning mutagenesis of the A1 domain of human von Willebrand factor. J Biol Chem 270: 13406-13414
20. Mi LZ, Grey MJ, Nishida N, Walz T, Lu C, Springer TA (2008) Functional and structural stability of the epidermal growth factor receptor in detergent micelles and phospholipid nanodiscs. Biochemistry 47: 10314-10323
21. Michaux G, Abbitt KB, Collinson LM, Haberichter SL, Norman KE, Cutler DF (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)
22. Ohi M, Li Y, Cheng Y, Walz T (2004) Negative staining and image classification-powerful tools in modern electron microscopy. Biol Proced Online 6: 23-34 (Pubitemid 38597695)
23. Perez-Vilar J (2007) Mucin granule intraluminal organization. Am J Respir Cell Mol Biol 36: 183-190 (Pubitemid 46233471)
24. Reeves PJ, Callewaert N, Contreras R, Khorana HG (2002) Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracy-cline-inducible N- acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci USA 99: 13419-13424 (Pubitemid 35215396)
25. Rosenberg JB, Haberichter SL, Jozwiak MA, Vokac EA, Kroner PA, Fahs SA, Kawai Y, Montgomery RR (2002) The role of the D1 domain of the von Willebrand factor propeptide in multimeriza-tion of VWF. Blood 100: 1699-1706 (Pubitemid 34925147)
26. Rudenko G, Henry L, Henderson K, Ichtchenko K, Brown MS, Goldstein JL, Deisenhofer J (2002) Structure of the LDL receptor extracellular domain at endosomal pH. Science 298: 2353-2358 (Pubitemid 36014201)
27. Ruggeri ZM, Mendolicchio GL (2007) Adhesion mechanisms in platelet function. Circ Res 100: 1673-1685 (Pubitemid 46987859)
28. Sadler JE (1998) Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem 67: 395-424 (Pubitemid 28411134)
29. Sadler JE (2005) New concepts in von Willebrand disease. Annu Rev Med 56: 173-191 (Pubitemid 40299779)
30. Sadler JE, Shelton-Inloes BB, Sorace JM, Harlan JM, Titani K, Davie EW (1985) Cloning and characterization of two cDNAs coding for human von Willebrand factor. Proc Natl Acad Sci USA 82: 6394-6398 (Pubitemid 16230519)
31. Schneider SW, Nuschele S, Wixforth A, Gorzelanny C, Alexander-Katz A, Netz RR, Schneider MF (2007) Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci USA 104: 7899-7903 (Pubitemid 47185848)
32. Seksek O, Biwersi J, Verkman AS (1995) Direct measurement of trans-Golgi pH in living cells and regulation by second messengers. J Biol Chem 270: 4967-4970
33. Siedlecki CA, Lestini BJ, Kottke-Marchant KK, Eppell SJ, Wilson DL, Marchant RE (1996) Shear-dependent changes in the three-dimensional structure of human von Willebrand factor. Blood 88: 2939-2950 (Pubitemid 26357374)
34. Sing CE, Alexander-Katz A (2010) Elongational flow induces the unfolding of von Willebrand factor at physiological flow rates. Biophys J 98: L35-L37.
35. Slayter H, Loscalzo J, Bockenstedt P, Handin RI (1985) Native conformation of human von Willebrand protein. J Biol Chem 260: 8559-8563
36. Tirado M, Garcia de la Torre J (1979) Translational friction coefficients of rigid, symmetric top macromolecules. Application to circular cylinders. J Chem Phys 71 : 2581-2588
37. Titani K, Kumar S, Takio K, Ericsson LH, Wade RD, Ashida K, Walsh KA, Chopek MW, Sadler JE, Fujikawa K (1986) Amino acid sequence of human von Willebrand factor. Biochemistry 25: 3171-3184 (Pubitemid 16056960)
38. 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 (Pubitemid 351375090)
39. Van den Steen P, Rudd PM, Dwek RA, Opdenakker G (1998) Concepts and principles of O-linked glycosylation. Crit Revs Biochem Mol Biol 33: 151-208 (Pubitemid 28334620)
40. Vischer UM, Wagner DD (1994) von Willebrand factor proteolytic processing and multimerization precede the formation of Weibel-Palade bodies. Blood 83: 3536-3544 (Pubitemid 24175543)
41. Voorberg J, Fontijn R, van Mourik JA, Pannekoek H (1990) Domains involved in multimer assembly of von willebrand factor (vWF): multimerization is independent of dimerization. EMBO J 9: 797-803
42. Wagner DD (1990) Cell biology of von Willebrand factor. Annu Rev Cell Biol 6: 217-246
43. Wagner DD, Saffaripour S, Bonfanti R, Sadler JE, Cramer EM, Chapman B, Mayadas TN (1991) Induction of specific storage organelles by von Willebrand factor propolypeptide. Cell 64: 403-413 (Pubitemid 121001264)
44. Zenner HL, Collinson LM, Michaux G, Cutler DF (2007) High-pressure freezing provides insights into Weibel-Palade body biogenesis. J Cell Sci 120(Part 12): 2117-2125 (Pubitemid 47010006)
45. Zhang Q, Zhou Y-F, Zhang C-Z, Springer TA (2009a) Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc Natl Acad Sci USA 106: 9226-9231
46. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA (2009b) Mechanoenzymatic cleavage of the ultralarge vascular protein, von Willebrand factor. Science 324: 1330-1334