Regulation of platelet myosin light chain (MYL9) by RUNX1: Implications for thrombocytopenia and platelet dysfunction in RUNX1 haplodeficiency

Blood

Volumn 116, Issue 26, 2010, Pages 6037-6045

  Jalagadugula, Gauthami ^a   Mao, Guangfen ^a   Kaur, Gurpreet ^a   Goldfinger, Lawrence E ^a   Dhanasekaran, Danny N ^a   Rao, A Koneti ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; FIBRINOGEN; MYOSIN IIA; MYOSIN LIGHT CHAIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX1;

ADULT; ARTICLE; BINDING SITE; CASE REPORT; CELL SPREADING; CHROMATIN IMMUNOPRECIPITATION; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; THROMBOCYTE DYSFUNCTION; THROMBOCYTOPENIA; THROMBOCYTOPOIESIS;

EID: 78650665647     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-289850     Document Type: Article

References (50)

1. Speck NA, Stacy T, Wang Q, et al. Core-binding factor: a central player in hematopoiesis and leukemia. Cancer Res. 1999;59(7 suppl): 1789s-1793s.
2. de Bruijn MF, Speck NA. Core-binding factors in hematopoiesis and immune function. Oncogene. 2004;23(24):4238-4248.
3. Mikhail FM, Sinha KK, Saunthararajah Y, Nucifora G. Normal and transforming functions of RUNX1: a perspective. J Cell Physiol. 2006;207(3):582-593.
4. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84(2):321-330.
5. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996;93(8):3444-3449.
6. Ichikawa M, Asai T, Saito T, et al. AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat Med. 2004;10(3):299-304.
7. Michaud J, Simpson KM, Escher R, et al. Integrative analysis of RUNX1 downstream pathways and target genes. BMC Genomics. 2008;9:363.
8. Otto F, Lubbert M, Stock M. Upstream and downstream targets of RUNX proteins. J Cell Biochem. 2003;89(1):9-18.
9. Song WJ, Sullivan MG, Legare RD, et al. Haploinsufficiency of CBFA2 causes familial thrombocytopenia with propensity to develop acute myelogenous leukaemia. Nat Genet. 1999;23(2):166-175.
10. Michaud J, Wu F, Osato M, et al. In vitro analyses of known and novel RUNX1/AML1 mutations in dominant familial platelet disorder with predisposition to acute myelogenous leukemia: implications for mechanisms of pathogenesis. Blood. 2002;99(4):1364-1372.
11. Ho CY, Otterud B, Legare RD, et al. Linkage of a familial platelet disorder with a propensity to develop myeloid malignancies to human chromosome 21q22.1-22.2. Blood. 1996;87(12):5218-5224.
12. Sun L, Mao G, Rao AK. Association of CBFA2 mutation with decreased platelet PKC-theta and impaired receptor-mediated activation of GPIIb-IIIa and pleckstrin phosphorylation: proteins regulated by CBFA2 play a role in GPIIb-IIIa activation. Blood. 2004;103(3):948-954.
13. Buijs A, Poddighe P, van Wijk R, et al. A novel CBFA2 single-nucleotide mutation in familial platelet disorder with propensity to develop myeloid malignancies. Blood. 2001;98(9):2856-2858.
14. Walker LC, Stevens J, Campbell H, et al. A novel inherited mutation of the transcription factor RUNX1 causes thrombocytopenia and may predispose to acute myeloid leukaemia. Br J Haematol. 2002;117(4):878-881.
15. Heller PG, Glembotsky AC, Gandhi MJ, et al. Low Mpl receptor expression in a pedigree with familial platelet disorder with predisposition to acute myelogenous leukemia and a novel AML1 mutation. Blood. 2005;105(12):4664-4670.
16. Matheny CJ, Speck ME, Cushing PR, et al. Disease mutations in RUNX1 and RUNX2 create nonfunctional, dominant-negative, or hypomorphic alleles. Embo J. 2007;26(4):1163-1175.
17. Gabbeta J, Yang X, Sun L, McLane MA, Niewiarowski S, Rao AK. Abnormal inside-out signal transduction-dependent activation of glycoprotein IIb-IIIa in a patient with impaired pleckstrin phosphorylation. Blood. 1996;87(4):1368-1376.
18. Sun L, Gorospe JR, Hoffman EP, Rao AK. Decreased platelet expression of myosin regulatory light chain polypeptide (MYL9) and other genes with platelet dysfunction and CBFA2/RUNX1 mutation: insights from platelet expression profiling. J Thromb Haemost 2007;5(1):146-154.
19. Aneja K, Jalagadugula G, Mao G, Rao AK. Mechanism of platelet factor (PF4) deficiency with RUNX1 mutations: RUNX1 is atranscriptional regulator of PF4 [abstract]. Blood. 2009;114:98-99. Abstract 227.
20. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Nonmuscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol. 2009;10(11):778-790.
21. Krendel M, Mooseker MS. Myosins: tails (and heads) of functional diversity. Physiology (Bethesda). 2005;20:239-251.
22. Marigo V, Nigro A, Pecci A, et al. Correlation between the clinical phenotype of MYH9-related disease and tissue distribution of class II nonmuscle myosin heavy chains. Genomics. 2004;83(6):1125-1133.
23. Hathaway DR, Eaton CR, Adelstein RS. Regulation of human platelet myosin light chain kinase by the catalytic subunit of cyclic AMP-dependent protein kinase. Nature. 1981;291(5812):252-256.
24. 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(40):28293-28300.
25. Bodie SL, Ford I, Greaves M, Nixon GF. Thrombininduced activation of RhoA in platelet shape change. Biochem Biophys Res Commun. 2001;287(1):71-76.
26. 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(5):1665-1672.
27. Nakai K, Suzuki Y, Kihira H, et al. Regulation of myosin phosphatase through phosphorylation of the myosin-binding subunit in platelet activation. Blood. 1997;90(10):3936-3942.
28. Johnson GJ, Leis LA, Krumwiede MD, White JG. The critical role of myosin IIA in platelet internal contraction. J Thromb Haemost. 2007;5(7):1516-1529.
29. Fox JE, Phillips DR. Role of phosphorylation in mediating the association of myosin with the cytoskeletal structures of human platelets. J Biol Chem. 1982;257(8):4120-4126.
30. 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(15):9826-9831.
31. Hartwig JH, Bokoch GM, Carpenter CL, et al. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell. 1995;82(4):643-653.
32. 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(12):3798-3805.
33. Nishikawa M, Tanaka T, Hidaka H. Ca2+- calmodulin-dependent phosphorylation and platelet secretion. Nature. 1980;287(5785):863-865.
34. Suzuki Y, Yamamoto M, Wada H, et al. Agonistinduced regulation of myosin phosphatase activity in human platelets through activation of Rhokinase. Blood. 1999;93(10):3408-3417.
35. Chen Z, Naveiras O, Balduini A, et al. The May-Hegglin anomaly gene MYH9 is a negative regulator of platelet biogenesis modulated by the Rho-ROCK pathway. Blood. 2007;110(1):171-179.
36. Chang Y, Aurade F, Larbret F, et al. Proplatelet formation is regulated by the Rho/ROCK pathway. Blood. 2007;109(10):4229-4236.
37. Balduini A, Pallotta I, Malara A, et al. Adhesive receptors, extracellular proteins and myosin IIAorchestrate proplatelet formation by human megakaryocytes. J Thromb Haemost. 2008;6(11):1900-1907.
38. Cupit LD, Schmidt VA, Gnatenko DV, Bahou WF Expression of protease activated receptor 3 (PAR3) is upregulated by induction of megakaryocyte phenotype in human erythroleukemia (HEL) cells. Exp Hematol. 2004;32(10):991-999.
39. Lavrrar JL, Farnham PJ. The use of transient chromatin immunoprecipitation assays to test models for E2F1-specific transcriptional activation. J Biol Chem. 2004;279:46343-46349.
40. Dignam JD, Lebovitz RM, Roeder RG. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983;11(5):1475-1489.
41. Goldfinger LE, Ptak C, Jeffery ED, Shabanowitz J, Hunt DF, Ginsberg MH. RLIP76 (RalBP1) is an R-Ras effector that mediates adhesiondependent Rac activation and cell migration. J Cell Biol. 2006;174(6):877-888.
42. Pecci A, Malara A, Badalucco S, et al. Megakaryocytes of patients with MYH9-related thrombocytopenia present an altered proplatelet formation. Thromb Haemost. 2009;102(1):90-96.
43. Arepally G, Rebbeck TR, Song W, Gilliland G, Maris JM, Poncz M. Evidence for genetic homogeneity in a familial platelet disorder with predisposition to acute myelogenous leukemia (FPD/AML) [letter]. Blood. 1998;92(7):2600-2602.
44. Jalagadugula GS, Mao G, Dhanasekaran DN, Kaur G, Rao AK. RUNX1 regulates platelet/megakaryocyte PKC-theta: decreased platelet PKC-0 expression in human RUNX1 haplodeficiency [abstract]. J Thromb Haemost. 2009; (suppl 2):95.
45. Kaur G, Jalagadugula G, Mao G, Rao AK. RUNX1/core binding factor A2 regulates platelet 12-Lipoxygenase gene (ALOX12): studies in human RUNX1 haplodeficiency. Blood. 2010;115:3128-3135.
46. Elagib KE, Racke FK, Mogass M, Khetawat R, Delehanty LL, Goldfarb A.N. RUNX1 and GATA-1 coexpression and cooperation in megakaryocytic differentiation. Blood. 2003;101(11):4333-4341.
47. Huang G, Zhang P, Hirai H, et al. PU. 1 is a major downstream target of AML1 (RUNX1) in adult mouse hematopoiesis. Nat Genet. 2008;40(1):51-60.
48. Hug BA, Ahmed N, Robbins JA, Lazar MA. A chromatin immunoprecipitation screen reveals protein kinase Cbetaas a direct RUNX1 target gene. J Biol Chem. 2004;279(2):825-830.
49. Javed A, Gutierrez S, Montecino M, et al. Multiple Cbfa/AML sites in the rat osteocalcin promoter are required for basal and vitamin D-responsive transcription and contribute to chromatin organization. Mol Cell Biol. 1999;19(11):7491-7500.
50. Li D, Sinha KK, Hay MA, Rinaldi CR, Saunthararajah Y, Nucifora G. RUNX1-RUNX1 homodimerization modulates RUNX1 activity and function. J Biol Chem. 2007;282(18):13542-13551.