Biogenesis of Weibel-Palade bodies in von Willebrand's disease variants with impaired von Willebrand factor intrachain or interchain disulfide bond formation

Haematologica

Volumn 97, Issue 6, 2012, Pages 859-866

  Wang, Jiong Wei ^a   Groeneveld, Dafna J ^a   Cosemans, Guy ^a   Dirven, Richard J ^a   Valentijn, Karine M ^a   Voorberg, Jan ^b   Reitsma, Pieter H ^a   Eikenboom, Jeroen ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Cysteine mutations; Secretion; Storage; Von Willebrand factor; Von Willebrand's disease; Weibel Palade body

Indexed keywords

CYSTEINE; PHENYLALANINE; SERINE; TYROSINE; VON WILLEBRAND FACTOR;

ARTICLE; BIOGENESIS; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DISULFIDE BOND; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; MUTATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; TRANSIENT TRANSFECTION; TRANSMISSION ELECTRON MICROSCOPY; VON WILLEBRAND DISEASE; WEIBEL PALADE BODY; WESTERN BLOTTING;

CYSTEINE; DISULFIDES; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; MODELS, BIOLOGICAL; MUTATION; PLASMIDS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; SERINE; TRANSFECTION; TYROSINE; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR; WEIBEL-PALADE BODIES;

EID: 84862146869     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2011.057216     Document Type: Article

References (41)

1. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem. 1998;67:395-424.
2. Sporn LA, Marder VJ, Wagner DD. Inducible secretion of large, biologically potent von Willebrand factor multimers. Cell. 1986;46(2):185-90.
3. Giblin JP, Hewlett LJ, Hannah MJ. Basal secretion of von Willebrand factor from human endothelial cells. Blood. 2008;112 (4):957-64.
4. Wagner DD. Cell biology of von Willebrand factor. Annu Rev Cell Biol. 1990;6:217-46.
5. Valentijn KM, Sadler JE, Valentijn JA, Voorberg J, Eikenboom J. Functional architecture of Weibel-Palade bodies. Blood. 2011;117(19):5033-43.
6. Dang LT, Purvis AR, Huang RH, Westfield LA, Sadler JE. Phylogenetic and functional analysis of histidine residues essential for pH-dependent multimerization of von Willebrand factor. J Biol Chem. 2011;286 (29):25763-9.
7. Zhou YF, Eng ET, Nishida N, Lu C, Walz T, Springer TA. A pH-regulated dimeric bouquet in the structure of von Willebrand factor. EMBO J. 2011;30(19):4098-111.
8. Marti T, Rosselet SJ, Titani K, Walsh KA. Identification of disulfide-bridged substructures within human von Willebrand factor. Biochemistry. 1987;26(25):8099-109.
9. Tjernberg P, Vos HL, Castaman G, Bertina RM, Eikenboom JC. Dimerization and multimerization defects of von Willebrand factor due to mutated cysteine residues. J Thromb Haemost. 2004;2(2):257-65.
10. Eikenboom J, Hilbert L, Ribba AS, Hommais A, Habart D, Messenger S, et al. Expression of 14 von Willebrand factor mutations identified in patients with type 1 von Willebrand disease from the MCMDM-1VWD study. J Thromb Haemost. 2009;7(8):1304-12.
11. Tjernberg P, Castaman G, Vos HL, Bertina RM, Eikenboom JC. Homozygous C2362F von Willebrand factor induces intracellular retention of mutant von Willebrand factor resulting in autosomal recessive severe von Willebrand disease. Br J Haematol. 2006;133(4):409-18.
12. Hommais A, Stepanian A, Fressinaud E, Mazurier C, Meyer D, Girma JP, et al. Mutations C1157F and C1234W of von Willebrand factor cause intracellular retention with defective multimerization and secretion. J Thromb Haemost. 2006;4(1): 148-57.
13. Wang JW, Valentijn KM, de Boer HC, Dirven RJ, van Zonneveld AJ, Koster AJ, et al. Intracellular storage and regulated secretion of von Willebrand factor in quantitative von Willebrand disease. J Biol Chem. 2011;286(27):24180-8.
14. Katsumi A, Tuley EA, Bodo I, Sadler JE. Localization of disulfide bonds in the cystine knot domain of human von Willebrand factor. J Biol Chem. 2000;275(33):25585-94.
15. Enayat MS, Guilliatt AM, Surdhar GK, Jenkins PV, Pasi KJ, Toh CH, et al. Aberrant dimerization of von Willebrand factor as the result of mutations in the carboxy-terminal region: identification of 3 mutations in members of 3 different families with type 2A (phenotype IID) von Willebrand disease. Blood. 2001;98(3):674-80.
16. Schneppenheim R, Brassard J, Krey S, Budde U, Kunicki TJ, Holmberg L, et al. Defective dimerization of von Willebrand factor subunits due to a Cys-> Arg mutation in type IID von Willebrand disease. Proc Natl Acad Sci USA. 1996;93(8):3581-6.
17. Tjernberg P, Vos HL, Spaargaren-van Riel CC, Luken BM, Voorberg J, Bertina RM, et al. Differential effects of the loss of intrachain-versus interchain-disulfide bonds in the cystine-knot domain of von Willebrand factor on the clinical phenotype of von Willebrand disease. Thromb Haemost. 2006;96(6):717-24.
18. Eikenboom JC, Matsushita T, Reitsma PH, Tuley EA, Castaman G, Briet E, et al. Dominant type 1 von Willebrand disease caused by mutated cysteine residues in the D3 domain of von Willebrand factor. Blood. 1996;88(7):2433-41.
19. Goodeve A, Eikenboom J, Castaman G, Rodeghiero F, Federici AB, Batlle J, et al. Phenotype and genotype of a cohort of families historically diagnosed with type 1 von Willebrand disease in the European study, Molecular and Clinical Markers for the Diagnosis and Management of Type 1 von Willebrand Disease (MCMDM-1VWD). Blood. 2007;109(1):112-21.
20. Budde U, Schneppenheim R, Eikenboom J, Goodeve A, Will K, Drewke E, et al. Detailed von Willebrand factor multimer analysis in patients with von Willebrand disease in the European study, molecular and clinical markers for the diagnosis and management of type 1 von Willebrand disease (MCMDM-1VWD). J Thromb Haemost. 2008;6(5):762-71.
21. Schneppenheim R, Michiels JJ, Obser T, Oyen F, Pieconka A, Schneppenheim S, et al. A cluster of mutations in the D3 domain of von Willebrand factor correlates with a distinct subgroup of von Willebrand disease: type 2A/IIE. Blood. 2010;115(23): 4894-901.
22. Eikenboom JC, Castaman G, Vos HL, Bertina RM, Rodeghiero F. Characterization of the genetic defects in recessive type 1 and type 3 von Willebrand disease patients of Italian origin. Thromb Haemost. 1998;79(4):709-17.
23. Romani de WT, Rondaij MG, Hordijk PL, Voorberg J, van Mourik JA. Real-time imaging of the dynamics and secretory behavior of Weibel-Palade bodies. Arterioscler Thromb Vasc Biol. 2003;23(5):755-61.
24. Benham AM, Cabibbo A, Fassio A, Bulleid N, Sitia R, Braakman I. The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lalpha. EMBO J. 2000;19(17):4493-502.
25. Valentijn KM, Valentijn JA, Jansen KA, Koster AJ. A new look at Weibel-Palade body structure in endothelial cells using electron tomography. J Struct Biol. 2008; 161(3):447-58.
26. Wise RJ, Barr PJ, Wong PA, Kiefer MC, Brake AJ, Kaufman RJ. Expression of a human proprotein processing enzyme: correct cleavage of the von Willebrand factor precursor at a paired basic amino acid site. Proc Natl Acad Sci USA. 1990;87(23):9378-82.
27. Shapiro J, Sciaky N, Lee J, Bosshart H, Angeletti RH, Bonifacino JS. Localization of endogenous furin in cultured cell lines. J Histochem Cytochem. 1997;45(1):3-12.
28. van de Ven WJ, Voorberg J, Fontijn R, Pannekoek H, van den Ouweland AM, van Duijnhoven HL, et al. Furin is a subtilisinlike proprotein processing enzyme in higher eukaryotes. Mol Biol Rep. 1990;14(4): 265-75.
29. Schooten CJ, Tjernberg P, Westein E, Terraube V, Castaman G, Mourik JA, et al. Cysteine-mutations in von Willebrand factor associated with increased clearance. J Thromb Haemost. 2005;3(10):2228-37.
30. Castaman G, Lethagen S, Federici AB, Tosetto A, Goodeve A, Budde U, et al. Response to desmopressin is influenced by the genotype and phenotype in type 1 von Willebrand disease (VWD): results from the European Study MCMDM-1VWD. Blood. 2008;111(7):3531-9.
31. Purvis AR, Gross J, Dang LT, Huang RH, Kapadia M, Townsend RR, et al. Two Cys residues essential for von Willebrand factor multimer assembly in the Golgi. Proc Natl Acad Sci USA. 2007;104(40):15647-52.
32. Voorberg J, Fontijn R, Calafat J, Janssen H, van Mourik JA, Pannekoek H. Assembly and routing of von Willebrand factor variants: the requirements for disulfide-linked dimerization reside within the carboxy-terminal 151 amino acids. J Cell Biol. 1991;113(1):195-205.
33. Michaux G, Hewlett LJ, Messenger SL, Goodeve AC, Peake IR, Daly ME, et al. Analysis of intracellular storage and regulated secretion of 3 von Willebrand diseasecausing variants of von Willebrand factor. Blood. 2003;102(7):2452-8.
34. Ledford MR, Rabinowitz I, Sadler JE, Kent JW, Civantos F. New variant of von Willebrand disease type II with markedly increased levels of von Willebrand factor antigen and dominant mode of inheritance: von Willebrand disease type IIC Miami. Blood. 1993;82(1):169-75.
35. Schneppenheim R, Obser T, Drewke E, Ledford MR, Lavergne JM, Meyer D, et al. The first mutations in von Willebrand disease type IIC Miami. Thromb Haemost. 2001;(Suppl.):P1805.
36. Allen S, Goodeve AC, Peake IR, Daly ME. Endoplasmic reticulum retention and prolonged association of a von Willebrand's disease-causing von Willebrand factor variant with ERp57 and calnexin. Biochem Biophys Res Commun. 2001;280(2):448-53.
37. Bodo I, Katsumi A, Tuley EA, Eikenboom JC, Dong Z, Sadler JE. Type 1 von Willebrand disease mutation Cys1149Arg causes intracellular retention and degradation of heterodimers: a possible general mechanism for dominant mutations of oligomeric proteins. Blood. 2001;98(10): 2973-9.
38. Huang RH, Wang Y, Roth R, Yu X, Purvis AR, Heuser JE, et al. Assembly of Weibel-Palade body-like tubules from N-terminal domains of von Willebrand factor. Proc Natl Acad Sci USA. 2008;105(2):482-7.
39. Haberichter SL, Merricks EP, Fahs SA, Christopherson PA, Nichols TC, Montgomery RR. Re-establishment of VWF-dependent Weibel-Palade bodies in VWD endothelial cells. Blood. 2005;105(1): 145-52.
40. Springer TA. Biology and physics of von Willebrand factor concatamers. J Thromb Haemost. 2011;9(Suppl 1):130-43.
41. Berriman JA, Li S, Hewlett LJ, Wasilewski S, Kiskin FN, Carter T, et al. Structural organization of Weibel-Palade bodies revealed by cryo-EM of vitrified endothelial cells. Proc Natl Acad Sci USA. 2009;106 (41):17407-12.