Intrinsic impaired proplatelet formation and microtubule coil assembly of megakaryocytes in a mouse model of Bernard-Soulier syndrome

Haematologica

Volumn 94, Issue 6, 2009, Pages 800-810

  Strassel, Catherine ^a   Eckly, Anita ^a   Léon, Catherine ^a   Petitjean, Claire ^a   Freund, Monique ^a   Cazenave, Jean Pierre ^a   Gachet, Christian ^a   Lanza, François ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

Author keywords

Bernar Soulier; GPIb V IX; Megakaryocyte; Microtubules; Platelet

Indexed keywords

GLYCOPROTEIN IB; PLATELET GLYCOPROTEIN IB BETA; TUBULIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BERNARD SOULIER DISEASE; BONE MARROW; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS; HUMAN; LIVER CELL; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MICROTUBULE ASSEMBLY; MOUSE; NONHUMAN; PROTEIN DEFICIENCY; THROMBOCYTOPOIESIS;

ADULT; ANIMALS; BERNARD-SOULIER SYNDROME; BLOOD PLATELETS; BONE MARROW CELLS; CELL SURVIVAL; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; HUMANS; KINETICS; MEGAKARYOCYTE PROGENITOR CELLS; MEGAKARYOCYTES; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MICROTUBULES; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; TIME FACTORS; YOUNG ADULT;

EID: 66749109857     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2008.001032     Document Type: Article

References (53)

1. Bernard J, Soulier JP. [Not Available.]. Sem Hop 1948;24:3217-3223
2. Nurden AT, Didry D, Rosa JP. Molecular defects of platelets in Bernard-Soulier syndrome. Blood Cells 1983;9:333-358 (Pubitemid 14248112)
3. Berndt MC, Du XP, Booth WJ. Ristocetin-dependent reconstitution of binding of von Willebrand factor to purified human platelet membrane glycoprotein Ib-IX complex. Biochemistry 1988;27:633-640 (Pubitemid 18043508)
4. Italiano JE Jr, Shivdasani RA. Megakaryocytes and beyond: the birth of platelets. J Thromb Haemost 2003;1:1174-1182
5. Schulze H, Shivdasani RA. Mechanisms of thrombopoiesis. J Thromb Haemost 2005;3:1717-1724 (Pubitemid 41716558)
6. Tomer A, Scharf RE, McMillan R, Ruggeri ZM, Harker LA. Bernard-Soulier syndrome: quantitative characterization of megakaryocytes and platelets by flow cytometric and platelet kinetic measurements. Eur J Haematol 1994;52:193-200. (Pubitemid 24205471)
7. Hourdille P, Benabdallah S, Belloc F, Nurden AT. Distribution of glycoprotein IIb-IIIa complexes in the surface membranes of human platelets and megakaryocytes. Br J Haematol 1985;59:171-182 (Pubitemid 15188832)
8. Nurden P, Nurden A. Giant platelets, megakaryocytes and the expression of glycoprotein Ib-IX complexes. C R Acad Sci III 1996;319:717-726 (Pubitemid 26315872)
9. Poujol C, Ware J, Nieswandt B, Nurden AT, Nurden P. Absence of GPIba is responsible for aberrant membrane development during megakaryocyte maturation: ultrastructural study using a transgenic model. Exp Hematol 2002;30:352-360 (Pubitemid 34286441)
10. Lepage A, Leboeuf M, Cazenave JP, de la Salle C, Lanza F, Uzan G. The a(IIb)b(3) integrin and GPIb-V-IX complex identify distinct stages in the maturation of CD34(+) cord blood cells to megakaryocytes. Blood 2000;96:4169-4177
11. Debili N, Kieffer N, Nakazawa M, Guichard J, Titeux M, Cramer E, et al. Expression of platelet glycoprotein Ib by cultured human megakaryocytes: ultrastructural localization and biosynthesis. Blood 1990;76:368-376 (Pubitemid 20225528)
12. Lopez JA, Andrews RK, Afshar-Kharghan V, Berndt MC. Bernard-Soulier syndrome. Blood 1998;91:4397-4418 (Pubitemid 28270285)
13. Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Culleré M, Hynes RO, Wagner DD. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci USA 1998;95:9524-9529 (Pubitemid 28506264)
14. Subramaniam M, Frenette PS, Saffaripour S, Johnson RC, Hynes RO, Wagner DD. Defects in hemostasis in P-selectin-deficient mice. Blood 1996;87:1238-1242 (Pubitemid 26056885)
15. Nurden P, Debili N, Vainchenker W, Bobe R, Bredoux R, Corvazier E, et al. Impaired megakaryocytopoiesis in type 2B von Willebrand disease with severe thrombocytopenia. Blood 2006;108:2587-2595 (Pubitemid 44776992)
16. Takahashi R, Sekine N, Nakatake T. Influence of monoclonal antiplatelet glycoprotein antibodies on in vitro human megakaryocyte colony formation and proplatelet formation. Blood 1999;93:1951-1958 (Pubitemid 29128497)
17. Feng S, Lu X, Kroll MH. Filamin A binding stabilizes nascent glycoprotein Ibalpha trafficking and thereby enhances its surface expression. J Biol Chem 2005;280:6709-6715 (Pubitemid 40341225)
18. Hartwig JH, Italiano JE Jr. Cytoskeletal mechanisms for platelet production. Blood Cells Mol Dis 2006;36:99-103.
19. Rojnuckarin P, Kaushansky K. Actin reorganization and proplatelet formation in murine megakaryocytes: the role of protein kinase c alpha. Blood 2001;97:154-161 (Pubitemid 32061255)
20. Kanaji T, Russell S, Cunningham J, Izuhara K, Fox JE, Ware J. Megakaryocyte proliferation and ploidy regulated by the cytoplasmic tail of glycoprotein Ibalpha. Blood 2004;104:3161-3168 (Pubitemid 39507130)
21. Lecine P, Villeval JL, Vyas P, Swencki B, Xu Y, Shivdasani RA. Mice lacking transcription factor NF-E2 provide in vivo validation of the proplatelet model of thrombocytopoiesis and show a platelet production defect that is intrinsic to megakaryocytes. Blood 1998;92:1608-1616 (Pubitemid 28406864)
22. Hartwig J, Italiano J Jr. The birth of the platelet. J Thromb Haemost 2003;1:1580-1586
23. Italiano JE Jr, Patel-Hett S, Hartwig JH. Mechanics of proplatelet elaboration. J Thromb Haemost 2007;5(Suppl 1):18-23. (Pubitemid 46958812)
24. Schulze H, Korpal M, Hurov J, Kim SW, Zhang J, Cantley LC, et al. Characterization of the megakaryocyte demarcation membrane system and its role in thrombopoiesis. Blood 2006;107:3868-3875 (Pubitemid 43726790)
25. Italiano JE Jr, Lecine P, Shivdasani RA, Hartwig JH. Blood platelets are assembled principally at the ends of proplatelet processes produced by differentiated megakaryocytes. J Cell Biol 1999;147:1299-1312 (Pubitemid 30012814)
26. Patel-Hett S, Richardson JL, Schulze H, Drabek K, Isaac NA, Hoffmeister K, et al. Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood 2008;111:4605-4616
27. Strassel C, Nonne C, Eckly A, David T, Leon C, Freund M, et al. Decreased thrombotic tendency in mouse models of the Bernard-Soulier syndrome. Arterioscler Thromb Vasc Biol 2007;27:241-247 (Pubitemid 46360405)
28. Peng J, Friese P, Heilmann E, George JN, Burstein SA, Dale GL. Aged platelets have an impaired response to thrombin as quantitated by P-selectin expression. Blood 1994;83:161-166 (Pubitemid 24016528)
29. Hartwig JH, DeSisto M. The cytoskeleton of the resting human blood platelet: structure of the membrane skeleton and its attachment to actin filaments. J Cell Biol 1991;112:407-425 (Pubitemid 21925996)
30. Cazenave JP, Ohlmann P, Cassel D, Eckly A, Hechler B, Gachet C. Preparation of washed platelet suspensions from human and rodent blood. Methods Mol Biol 2004;272:13-28.
31. Zucker-Franklin D. Megakaryocytes and platelets. In: Zucker-Franklin D, Grossi CE, eds. Atlas of Blood Cells. Vol.2 (ed Edi-Ermes). Milan;2003:788-791
32. Tablin F, Castro M, Leven RM. Blood platelet formation in vitro. The role of the cytoskeleton in megakaryocyte fragmentation. J Cell Sci 1990;97(Pt 1):59-70. (Pubitemid 120023246)
33. Heyns Adu P, Badenhorst PN, Wessels P, Pieters H, Lotter MG. Kinetics, in vivo redistribution and sites of sequestration of indium-111-labelled platelets in giant platelet syndromes. Br J Haematol 1985;60:323-330 (Pubitemid 15090182)
34. Tsakiris DA, Scudder L, Hodivala-Dilke K, Hynes RO, Coller BS. Hemostasis in the mouse (Mus musculus): a review. Thromb Haemost 1999;81:177-188 (Pubitemid 29078299)
35. Vainchenker W, Kieffer N. Human megakaryocytopoiesis: in vitro regulation and characterization of megakaryocytic precursor cells by differentiation markers. Blood Rev 1988;2:102-107 (Pubitemid 18162965)
36. Nieswandt B, Bergmeier W, Rackebrandt K, Gessner JE, Zirngibl H. Identification of critical antigen-specific mechanisms in the development of immune thrombocytopenic purpura in mice. Blood 2000;96:2520-2527
37. Kaushansky K. Thrombopoietin and the hematopoietic stem cell. Ann N Y Acad Sci 2005;1044:139-141
38. Battinelli EM, Hartwig JH, Italiano JE Jr. Delivering new insight into the biology of megakaryopoiesis and thrombopoiesis. Curr Opin Hematol 2007;14:419-426 (Pubitemid 47457630)
39. Cramer EM. Megakaryocyte structure and function. Curr Opin Hematol 1999;6:354-361
40. Zucker-Franklin D. Megakaryocyte and platelet structure in thrombocytopoiesis: the effect of cytokines. Stem Cells 1996;14(Suppl 1):1-17. (Pubitemid 126687186)
41. Ware J, Russell S, Ruggeri ZM. Generation and rescue of a murine model of platelet dysfunction: the Bernard-Soulier syndrome. Proc Natl Acad Sci USA 2000;97:2803-2808 (Pubitemid 30159252)
42. Eckly A, Strassel C, Freund M, Cazenave JP, Lanza F, Gachet C, Leon C. Abnormal megakaryocyte morphology and proplatelet formation in mice with megakaryocyte-restricted MYH9 inactivation. Blood 2009;113:3182-3189
43. Thiele J, Galle R, Sander C, Fischer R. Interactions between megakaryocytes and sinus wall. An ultrastructural study on bone marrow tissue in primary (essential) thrombocythemia. J Submicrosc Cytol Pathol 1991;23:595-603.
44. Williamson D, Pikovski I, Cranmer SL, Mangin P, Mistry N, Domagala T, et al. Interaction between platelet glycoprotein Ibalpha and filamin-1 is essential for glycoprotein Ib/IX receptor anchorage at high shear. J Biol Chem 2002;277:2151-2159 (Pubitemid 34968801)
45. White JG, Sauk JJ. The organization of microtubules and microtubule coils in giant platelet disorders. Am J Pathol 1984;116:514-522 (Pubitemid 14034019)
46. Schwer HD, Lecine P, Tiwari S, Italiano JE Jr, Hartwig JH, Shivdasani RA. A lineage-restricted and divergent beta-tubulin isoform is essential for the biogenesis, structure and function of blood platelets. Curr Biol 2001;11:579-586 (Pubitemid 32324760)
47. Schulze H, Dose M, Korpal M, Meyer I, Italiano JE Jr, Shivdasani RA. RanBP10 is a cytoplasmic guanine nucleotide exchange factor that modulates noncentrosomal microtubules. J Biol Chem 2008;283:14109-14119
48. Nurden P, Nurden AT. Congenital disorders associated with platelet dysfunctions. Thromb Haemost 2008;99:253-263
49. Kato K, Martinez C, Russell S, Nurden P, Nurden A, Fiering S, Ware J. Genetic deletion of mouse platelet glycoprotein Ibbeta produces a Bernard-Soulier phenotype with increased alpha-granule size. Blood 2004;104:2339-2344 (Pubitemid 39331831)
50. Sabri S, Jandrot-Perrus M, Bertoglio J, Farndale RW, Mas VM, Debili N, et al. Differential regulation of actin stress fiber assembly and proplatelet formation by α2β1 integrin and GPVI in human megakaryocytes. Blood 2004;104:3117-3125 (Pubitemid 39517011)
51. Balduini A, Pallotta I, Malara A, Lova P, Pecci A, Viarengo G, et al. Adhesive receptors, extracellular proteins and myosin IIA orchestrate proplatelet formation by human megakaryocytes. J Thromb Haemost 2008;6:1900-1907
52. Balduini A, Malara A, Pecci A, Badalucco S, Bozzi V, Pallotta I, et al. Proplatelet formation in heterozygous Bernard-Soulier syndrome type Bolzano. J Thromb Haemost 2009;7:478-484
53. Kanaji T, Russell S, Ware J. Amelioration of the macrothrombocytopenia associated with the murine Bernard-Soulier syndrome. Blood 2002;100:2102-2107 (Pubitemid 35001244)