Megakaryocyte-restricted MYH9 inactivation dramatically affects hemostasis while preserving platelet aggregation and secretion

Blood

Volumn 110, Issue 9, 2007, Pages 3183-3191

  Léon, Catherine ^a,b,c   Eckly, Anita ^a,b,c   Hechler, Béatrice ^a,b,c   Aleil, Boris ^a,b,c   Freund, Monique ^a,b,c   Ravanat, Catherine ^a,b,c   Jourdain, Marie ^a,b,c   Nonne, Christelle ^a,b,c   Weber, Josiane ^a,b,c   Tiedt, Ralph ^d   Gratacap, Marie Pierre ^a,e   Severin, Sonia ^a,e   Cazenave, Jean Pierre ^a,b,c   Lanza, François ^a,b,c   Skoda, Radek ^d   Gachet, Christian ^a,b,c  

^a INSERM   (France)

^b ETABLISSEMENT FRANÇAIS DU SANG   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA3 INTEGRIN; COLLAGEN; FERROUS CHLORIDE; FIBRINOGEN; MYOSIN IIA; PHOSPHATIDYLINOSITOL 3,4 BISPHOSPHATE;

AGONIST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; BLEEDING TIME; BLOOD; BLOOD CLOT; CAROTID ARTERY INJURY; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE DISRUPTION; HEMOSTASIS; LAMELLIPODIUM; MALE; MEGAKARYOCYTE; MOUSE; NONHUMAN; PERFUSION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRESS FIBER; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOCYTE FUNCTION; THROMBOCYTE RELEASE REACTION; THROMBOCYTOPENIA; THROMBUS;

EID: 36148955807     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-03-080184     Document Type: Article

References (59)

1. Barkalow KL, Falet H, Hartwig JH. Dynamics of the platelet cytoskeleton. In: Gresele P, Page C, Fuster V, Vermylen J, eds. Platelets in Thrombotic and Non-thrombotic Disorders. Cambridge, United Kingdom: Cambridge University Press; 2002:93-103.
2. Gear ARL, Polanowska-Grabowska Rk. The platelet shape change. In: Gresele P, Page C, Fuster V, Vermylen J, eds. Platelets in Thrombotic and Non-thrombotic Disorders. Cambridge, United Kingdom: Cambridge University Press; 2002:319-337.
3. Fox JE. The platelet cytoskeleton. Thromb Haemost. 1993;70:884-893.
4. Fox JE. Cytoskeletal proteins and platelet signaling. Thromb Haemost. 2001;86:198-213.
5. Suzuki Y, Yamamoto M, Wada H, et al. Agonist-induced regulation of myosin phosphatase activity in human platelets through activation of Rho-kinase. Blood. 1999;93:3408-3417.
6. Paul BZ, Daniel JL, Kunapuli SP. Platelet shape change is mediated by both calcium-dependent and -independent signaling pathways: role of p160 Rho-associated coiled-coil-containing protein kinase in platelet shape change. J Biol Chem. 1999;274:28293-28300.
7. Bauer M, Retzer M, Wilde JI, et al. Dichotomous regulation of myosin phosphorylation and shape change by Rho-kinase and calcium in intact human platelets. Blood. 1999;94:1665-1672.
8. Klages B, Brandt U, Simon MI, Schultz G, Offermanns S. Activation of G12/G13 results in shape change and Rho/Rho-kinase-mediated myosin light chain phosphorylation in mouse platelets. J Cell Biol. 1999;144:745-754.
9. Daniel JL, Molish IR, Rigmaiden M, Stewart G. Evidence for a role of myosin phosphorylation in the initiation of the platelet shape change response. J Biol Chem. 1984;259:9826-9831.
10. Nachmias VT, Kavaler J, Jacubowitz S. Reversible association of myosin with the platelet cytoskeleton. Nature. 1985;313:70-72.
11. Tanaka K, Itoh K. Reorganization of stress fiber-like structures in spreading platelets during surface activation. J Struct Biol. 1998;124:13-41.
12. Lokeshwar VB, Bourguignon LY. The involvement of Ca2+ and myosin light chain kinase in collagen-induced platelet activation. Cell Biol Int Rep. 1992;16:883-897.
13. Nishikawa M, Tanaka T, Hidaka H. Ca2+-calmodulin-dependent phosphorylation and platelet secretion. Nature. 1980;287:863-865.
14. Saitoh M, Naka M, Hidaka H. The modulatory role of myosin light chain phosphorylation in human platelet activation. Biochem Biophys Res Commun. 1986;140:280-287.
15. Watanabe Y, Ito M, Kataoka Y, et al. Protein kinase C-catalyzed phosphorylation of an inhibitory phosphoprotein of myosin phosphatase is involved in human platelet secretion. Blood. 2001;97:3798-3805.
16. Suzuki-Inoue K, Hughes CE, Inoue O, et al. Involvement of Src kinases and PLCgamma2 in clot retraction. Thromb Res. 2007;120:251-258.
17. Berg JS, Powell BC, Cheney RE. A millennial myosin census. Mol Biol Cell. 2001;12:780-794.
18. Noris P, Spedini P, Belletti S, Magrini U, Balduini CL. Thrombocytopenia, giant platelets, and leukocyte inclusion bodies (May-Hegglin anomaly): clinical and laboratory findings. Am J Med. 1998;104:355-360.
19. Seri M, Cusano R, Gangarossa S, et al. Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes: The May-Heggllin/Fechtner Syndrome Consortium. Nat Genet. 2000;26:103-105.
20. Heath KE, Campos-Barros A, Toren A, et al. Non-muscle myosin heavy chain IIA mutations define a spectrum of autosomal dominant macrothrombocytopenias: May-Hegglin anomaly and Fechtner, Sebastian, Epstein, and Alport-like syndromes. Am J Hum Genet. 2001;69:1033-1045.
21. Kunishima S, Matsushita T, Kojima T, et al. Immunofluorescence analysis of neutrophil nonmuscle myosin heavy chain-A in MYH9 disorders: association of subcellular localization with MYH9 mutations. Lab Invest. 2003;83:115-122.
22. Pujol-Moix N, Kelley MJ, Hernandez A, Muniz-Diaz E, Espanol I. Ultrastructural analysis of granulocyte inclusions in genetically confirmed MYH9-related disorders. Haematologica. 2004;89:330-337.
23. Canobbio I, Noris P, Pecci A, Balduini A, Balduini CL, Torti M. Altered cytoskeleton organization in platelets from patients with MYH9-related disease. J Thromb Haemost. 2005;3:1026-1035.
24. Heynen MJ, Blockmans D, Verwilghen RL, Vermylen J. Congenital macrothrombocytopenia, leucocyte inclusions, deafness and proteinuria: functional and electron microscopic observations on platelets and megakaryocytes. Br J Haematol. 1988;70:441-448.
25. Lusher JM, Barnhart MI. Congenital disorders affecting platelets. Semin Thromb Hemost. 1977;4:123-186.
26. Jantunen E. Inherited giant platelet disorders. Eur J Haematol. 1994;53:191-196.
27. D'Apolito M, Guarnieri V, Boncristiano M, Zelante L, Savoia A. Cloning of the murine non-muscle myosin heavy chain IIA gene ortholog of human MYH9 responsible for May-Hegglin, Sebastian, Fechtner, and Epstein syndromes. Gene. 2002;286:215-222.
28. Matsushita T, Hayashi H, Kunishima S, et al. Targeted disruption of mouse ortholog of the human MYH9 responsible for macrothrombocytopenia with different organ involvement: hematological, nephrological, and otological studies of heterozygous KO mice. Biochem Biophys Res Commun. 2004;325:1163-1171.
29. Franke JD, Dong F, Rickoll WL, Kelley MJ, Kiehart DP. Rod mutations associated with MYH9-related disorders disrupt nonmuscle myosin-IIA assembly. Blood. 2005;105:161-169.
30. Deutsch S, Rideau A, Bochaton-Piallat ML, et al. Asp1424Asn MYH9 mutation results in an unstable protein responsible for the phenotypes in May-Hegglin anomaly/Fechtner syndrome. Blood. 2003;102:529-534.
31. Pecci A, Noris P, Invernizzi R, et al. Immunocytochemistry for the heavy chain of the non-muscle myosin IIA as a diagnostic tool for MYH9-related disorders. Br J Haematol. 2002;117:164-167.
32. Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem. 2004;279:41263-41266.
33. Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-Cre transgenic mice allow generating lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood. 2007;109:1503-1506.
34. 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.
35. Leon C, Hechler B, Freund M, et al. Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y(1) receptor-null mice. J Clin Invest. 1999;104:1731-1737.
36. McCarty OJ, Larson MK, Auger JM, et al. Rac1 is essential for platelet lamellipodia formation and aggregate stability under flow. J Biol Chem. 2005;280:39474-39484.
37. Kauffenstein G, Bergmeier W, Eckly A, et al. The P2Y(12) receptor induces platelet aggregation through weak activation of the alpha(IIb)beta(3) integrin: a phosphoinositide 3-kinase-dependent mechanism. FEBS Lett. 2001;505:281-290.
38. Payrastre B. Phosphoinositides: lipid kinases and phosphatases. Methods Mol Biol. 2004;273:201-212.
39. Strassel C, Nonne C, Eckly A, et al. Decreased thrombotic tendency in mouse models of the Bernard-Soulier syndrome. Arterioscler Thromb Vasc Biol. 2007;27:241-247.
40. Gross S, Tilly P, Hentsch D, Vonesch JL, Fabre JE. Vascular wall-produced prostaglandin E2 exacerbates arterial thrombosis and atherothrombosis through platelet EP3 receptors. J Exp Med. 2007;204:311-320.
41. Franke JD, Boury AL, Gerald NJ, Kiehart DP. Native nonmuscle myosin II stability and light chain binding in Drosophila melanogaster. Cell Motil Cytoskeleton. 2006;63:604-622.
42. Knecht DA, Loomis WF. Developmental consequences of the lack of myosin heavy chain in Dictyostelium discoideum. Dev Biol. 1988;128:178-184.
43. Limouze J, Straight AF, Mitchison T, Sellers JR. Specificity of blebbistatin, an inhibitor of myosin II. J Muscle Res Cell Motil. 2004;25:337-341.
44. Straight AF, Cheung A, Limouze J, et al. Dissecting temporal and spatial control of cytokinesis with a myosin II inhibitor. Science. 2003;299:1743-1747.
45. Guinebault C, Payrastre B, Racaud-Sultan C, et al. Integrin-dependent translocation of phosphoinositide 3-kinase to the cytoskeleton of thrombin-activated platelets involves specific interactions of p85 alpha with actin filaments and focal adhesion kinase. J Cell Biol. 1995;129:831-842.
46. Payrastre B, Missy K, Trumel C, Bodin S, Plantavid M, Chap H. The integrin alpha IIb/beta 3 in human platelet signal transduction. Biochem Pharmacol. 2000;60:1069-1074.
47. Nonne C, Lenain N, Hechler B, et al. Importance of platelet phospholipase Cgamma2 signaling in arterial thrombosis as a function of lesion severity. Arterioscler Thromb Vasc Biol. 2005;25:1293-1298.
48. Bunting S, Widmer R, Lipari T, et al. Normal platelets and megakaryocytes are produced in vivo in the absence of thrombopoietin. Blood. 1997;90:3423-3429.
49. 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.
50. Goschnick MW, Lau LM, Wee JL, et al. Impaired "outside-in" integrin alphaIIbbeta3 signaling and thrombus stability in TSSC6-deficient mice. Blood. 2006;108:1911-1918.
51. Law DA, DeGuzman FR, Heiser P, Ministri-Madrid K, Killeen N, Phillips DR. Integrin cytoplasmic tyrosine motif is required for outside-in alphaIIbbeta3 signalling and platelet function. Nature. 1999;401:808-811.
52. Godwin HA, Ginsburg AD. May-Hegglin anomaly: a defect in megakaryocyte fragmentation? Br J Haematol. 1974;26:117-128.
53. Volpe E, Cuccurullo L, Valente A, Jori GP, Buonanno G. The May-Hegglin anomaly: further studies on leukocyte inclusions and platelet ultrastructure. Acta Haematol. 1974;52:238-247.
54. Painter RG, Ginsberg MH. Centripetal myosin redistribution in thrombin-stimulated platelets: relationship to platelet Factor 4 secretion. Exp Cell Res. 1984;155:198-212.
55. Gerrard JM, Israels SJ, Friesen LL. Protein phosphorylation and platelet secretion. Nouv Rev Fr Hematol. 1985;27:267-273.
56. White JG, Gerrard JM. Recent advances in platelet structural physiology. Suppl Thromb Haemost. 1978;63:49-60.
57. Phillips DR, Prasad KS, Manganello J, Bao M, Nannizzi-Alaimo L. Integrin tyrosine phosphorylation in platelet signaling. Curr Opin Cell Biol. 2001;13:546-554.
58. Chrzanowska-Wodnicka M, Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol. 1996;133:1403-1415.
59. Sandquist JC, Swenson KI, Demali KA, Burridge K, Means AR. Rho kinase differentially regulates phosphorylation of nonmuscle myosin II isoforms A and B during cell rounding and migration. J Biol Chem. 2006;281:35873-35883.