Megakaryocyte-specific deletion of the protein-tyrosine phosphatases Shp1 and Shp2 causes abnormal megakaryocyte development, platelet production, and function

Blood

Volumn 121, Issue 20, 2013, Pages 4205-4220

  Mazharian, Alexandra ^a   Mori, Jun ^a   Wang, Ying Jie ^a,c   Heising, Silke ^a   Neel, Benjamin G ^b   Watson, Steve P ^a   Senis, Yotis A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRINOGEN; GLYCOPROTEIN IB ALPHA; INTEGRIN; INTEGRIN ALPHA2BETA3; PHOSPHOLIPASE C GAMMA2; PROTEIN; PROTEIN GPVI; PROTEIN KINASE SYK; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; THROMBOPOIETIN; UNCLASSIFIED DRUG; PROTEIN TYROSINE PHOSPHATASE; PTPN11 PROTEIN, MOUSE; PTPN6 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EX VIVO STUDY; GENE DELETION; HEMOSTASIS; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IN VIVO STUDY; MEGAKARYOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; THROMBOCYTE FUNCTION; THROMBOCYTE KINETICS; THROMBOCYTE MEMBRANE; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS; THROMBOSIS; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CELL CULTURE; GENETICS; MEGAKARYOBLAST; METABOLISM; PHYSIOLOGY; THROMBOCYTE; TRANSGENIC MOUSE;

ANIMALS; BLOOD PLATELETS; CELLS, CULTURED; GENE DELETION; MEGAKARYOCYTE PROGENITOR CELLS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ORGAN SPECIFICITY; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; PROTEIN TYROSINE PHOSPHATASES; THROMBOPOIESIS;

MLCS; MLOWN;

EID: 84881014317     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-449272     Document Type: Article

References (49)

1. Pao LI, Badour K, Siminovitch KA, Neel BG. Nonreceptor protein-tyrosine phosphatases in immune cell signaling. Annu Rev Immunol. 2007; 25:473-523.
2. Daëron M, Jaeger S, Du Pasquier L, Vivier E. Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol Rev. 2008;224:11-43.
3. Ivins Zito C, Kontaridis MI, Fornaro M, Feng GS, Bennett AM. SHP-2 regulates the phosphatidylinositide 39-kinase/Akt pathway and suppresses caspase 3-mediated apoptosis. J Cell Physiol. 2004;199(2):227-236.
4. Kontaridis MI, Eminaga S, Fornaro M, Zito CI, Sordella R, Settleman J, Bennett AM. SHP-2 positively regulates myogenesis by coupling to the Rho GTPase signaling pathway. Mol Cell Biol. 2004;24(12):5340-5352.
5. Yamashita T, Suzuki R, Backlund PS, Yamashita Y, Yergey AL, Rivera J. Differential dephosphorylation of the FcRgamma immunoreceptor tyrosine-based activation motif tyrosines with dissimilar potential for activating Syk. J Biol Chem. 2008;283(42):28584-28594.
6. Yusa S, Campbell KS. Src homology region 2-containing protein tyrosine phosphatase-2 (SHP-2) can play a direct role in the inhibitory function of killer cell Ig-like receptors in human NK cells. J Immunol. 2003;170(9):4539-4547.
7. Shultz LD, Schweitzer PA, Rajan TV, et al. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell. 1993;73(7): 1445-1454.
8. Wo, Tsui H, Siminovitch KA, de Souza L, Tsui FW. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat Genet. 1993;4(2):124-129.
9. Kozlowski M, Mlinaric-Rascan I, Feng GS, Shen R, Pawson T, Siminovitch KA. Expression and catalytic activity of the tyrosine phosphatase PTP1C is severely impaired in motheaten and viable motheaten mice. J Exp Med. 1993;178(6): 2157-2163.
10. Pasquet JM, Quek L, Pasquet S, Poole A, Matthews JR, Lowell C, Watson SP. Evidence of a role for SHP-1 in platelet activation by the collagen receptor glycoprotein VI. J Biol Chem. 2000;275(37):28526-28531.
11. Yang W, Klaman LD, Chen B, et al. An Shp2/SFK/ Ras/Erk signaling pathway controls trophoblast stem cell survival. Dev Cell. 2006;10(3):317-327.
12. Arrandale JM, Gore-Willse A, Rocks S, et al. Insulin signaling in mice expressing reduced levels of Syp. J Biol Chem. 1996;271(35): 21353-21358.
13. Qu CK, Shi ZQ, Shen R, Tsai FY, Orkin SH, Feng GS. A deletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development. Mol Cell Biol. 1997;17(9): 5499-5507.
14. Saxton TM, Ciruna BG, Holmyard D, et al. The SH2 tyrosine phosphatase shp2 is required for mammalian limb development. Nat Genet. 2000; 24(4):420-423.
15. Dhanjal TS, Pendaries C, Ross EA, et al. A novel role for PECAM-1 in megakaryocytokinesis and recovery of platelet counts in thrombocytopenic mice. Blood. 2007;109(10):4237-4244.
16. Wong C, Liu Y, Yip J, et al. CEACAM1 negatively regulates platelet-collagen interactions and thrombus growth in vitro and in vivo. Blood. 2009; 113(8):1818-1828.
17. Washington AV, Schubert RL, Quigley L, et al. A TREM family member, TLT-1, is found exclusively in the alpha-granules of megakaryocytes and platelets. Blood. 2004;104(4):1042-1047.
18. Xue J, Zhang X, Zhao H, et al. Leukocyte-associated immunoglobulin-like receptor-1 is expressed on human megakaryocytes and negatively regulates the maturation of primary megakaryocytic progenitors and cell line. Biochem Biophys Res Commun. 2011;405(1): 128-133.
19. Mazharian A, Wang YJ, Mori J, et al. Mice lacking the ITIM-containing receptor G6b-B exhibit macrothrombocytopenia and aberrant platelet function. Sci Signal. 2012;5(248):ra78.
20. Senis YA, Tomlinson MG, García A, et al. A comprehensive proteomics and genomics analysis reveals novel transmembrane proteins in human platelets and mouse megakaryocytes including G6b-B, a novel immunoreceptor tyrosine-based inhibitory motif protein. Mol Cell Proteomics. 2007;6(3):548-564.
21. Senis YA, Antrobus R, Severin S, et al. Proteomic analysis of integrin alphaIIbbeta3 outside-in signaling reveals Src-kinase-independent phosphorylation of Dok-1 and Dok-3 leading to SHIP-1 interactions. J Thromb Haemost. 2009; 7(10):1718-1726.
22. Barford D, Neel BG. Revealing mechanisms for SH2 domain mediated regulation of the protein tyrosine phosphatase SHP-2. Structure. 1998; 6(3):249-254.
23. Eck MJ, Pluskey S, Trüb T, Harrison SC, Shoelson SE. Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature. 1996;379(6562):277-280.
24. Hof P, Pluskey S, Dhe-Paganon S, Eck MJ, Shoelson SE. Crystal structure of the tyrosine phosphatase SHP-2. Cell. 1998;92(4):441-450.
25. Pluskey S, Wandless TJ, Walsh CT, Shoelson SE. Potent stimulation of SH-PTP2 phosphatase activity by simultaneous occupancy of both SH2 domains. J Biol Chem. 1995;270(7):2897-2900.
26. Yang J, Cheng Z, Niu T, Liang X, Zhao ZJ, Zhou GW. Structural basis for substrate specificity of protein-tyrosine phosphatase SHP-1. J Biol Chem. 2000;275(6):4066-4071.
27. Yang J, Liu L, He D, et al. Crystal structure of human protein-tyrosine phosphatase SHP-1. J Biol Chem. 2003;278(8):6516-6520.
28. Pao LI, Lam KP, Henderson JM, et al. B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity. 2007; 27(1):35-48.
29. Fornaro M, Burch PM, Yang W, et al. SHP-2 activates signaling of the nuclear factor of activated T cells to promote skeletal muscle growth. J Cell Biol. 2006;175(1):87-97.
30. Tiedt R, Schomber T, Hao-Shen H, Skoda RC. Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo. Blood. 2007;109(4):1503-1506.
31. Ault KA, Knowles C. In vivo biotinylation demonstrates that reticulated platelets are the youngest platelets in circulation. Exp Hematol. 1995;23(9):996-1001.
32. Mazharian A, Thomas SG, Dhanjal TS, Buckley CD, Watson SP. Critical role of Src-Syk-PLCg2 signaling in megakaryocyte migration and thrombopoiesis. Blood. 2010;116(5):793-800.
33. Senis YA, Atkinson BT, Pearce AC, et al. Role of the p110delta PI 3-kinase in integrin and ITAM receptor signalling in platelets. Platelets. 2005; 16(3-4):191-202.
34. Pearce AC, Senis YA, Billadeau DD, Turner M, Watson SP, Vigorito E. Vav1 and vav3 have critical but redundant roles in mediating platelet activation by collagen. J Biol Chem. 2004; 279(52):53955-53962.
35. 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(47):39474-39484.
36. Senis YA, Tomlinson MG, Ellison S, et al. The tyrosine phosphatase CD148 is an essential positive regulator of platelet activation and thrombosis. Blood. 2009;113(20):4942-4954.
37. Mazharian A, Watson SP, Severin S. Critical role for ERK1/2 in bone marrow and fetal liver-derived primary megakaryocyte differentiation, motility, and proplatelet formation. Exp Hematol. 2009; 37(10):1238-1249 e5.
38. Bender M, Hofmann S, Stegner D, et al. Differentially regulated GPVI ectodomain shedding by multiple platelet-expressed proteinases. Blood. 2010;116(17):3347-3355.
39. Kanaji S, Kanaji T, Furihata K, Kato K, Ware JL, Kunicki TJ. Convulxin binds to native, human glycoprotein Ib a. J Biol Chem. 2003;278(41): 39452-39460.
40. Shattil SJ, Newman PJ. Integrins: dynamic scaffolds for adhesion and signaling in platelets. Blood. 2004;104(6):1606-1615.
41. Auger JM, Kuijpers MJ, Senis YA, Watson SP, Heemskerk JW. Adhesion of human and mouse platelets to collagen under shear: a unifying model. FASEB J. 2005;19(7):825-827.
42. Thon JN, Montalvo A, Patel-Hett S, et al. Cytoskeletal mechanics of proplatelet maturation and platelet release. J Cell Biol. 2010;191(4):861-874.
43. Sabri S, Jandrot-Perrus M, Bertoglio J, et al. Differential regulation of actin stress fiber assembly and proplatelet formation by a2b1 integrin and GPVI in human megakaryocytes. Blood. 2004;104(10):3117-3125.
44. Mazharian A, Ghevaert C, Zhang L, Massberg S, Watson SP. Dasatinib enhances megakaryocyte differentiation but inhibits platelet formation. Blood. 2011;117(19):5198-5206.
45. Oh ES, Gu H, Saxton TM, et al. Regulation of early events in integrin signaling by protein tyrosine phosphatase SHP-2. Mol Cell Biol. 1999; 19(4):3205-3215.
46. Macaulay IC, Tijssen MR, Thijssen-Timmer DC, et al. Comparative gene expression profiling of in vitro differentiated megakaryocytes and erythroblasts identifies novel activatory and inhibitory platelet membrane proteins. Blood. 2007;109(8):3260-3269.
47. Cicmil M, Thomas JM, Leduc M, Bon C, Gibbins JM. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets. Blood. 2002;99(1):137-144.
48. Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-1 is a negative regulator of platelet-collagen interactions. Blood. 2001;98(5):1456-1463.
49. Bluteau D, Lordier L, Di Stefano A, et al. Regulation of megakaryocyte maturation and platelet formation. J Thromb Haemost. 2009; 7(Suppl 1):227-234.