Induction of megakaryocyte differentiation drives nuclear accumulation and transcriptional function of MKL1 via actin polymerization and RhoA activation

Blood

Volumn 121, Issue 7, 2013, Pages 1094-1101

  Smith, Elenoe C ^a   Teixeira, Alexandra M ^a   Chen, Rachel C ^a   Wang, Lin ^a   Gao, Yuan ^a   Hahn, Katherine L ^a   Krause, Diane S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 O METHYLPHORBOL 13 ACETATE 12 MYRISTATE; MKL1 PROTEIN; PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBOPOIETIN; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL TYPE; CYTOPLASM; FIBROBLAST; GENE TARGETING; HUMAN; HUMAN CELL; MEGAKARYOCYTE; NERVE CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SMOOTH MUSCLE FIBER;

EID: 84874088071     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-05-429993     Document Type: Article

References (36)

1. Ragu C, Boukour S, Elain G, et al. The serum response factor (SRF)/megakaryocytic acute leukemia (MAL) network participates in megakaryo-cyte development. Leukemia. 2010;24(6):1227-1230.
2. Gilles L, Bluteau D, Boukour S, et al. MAL/SRF complex is involved in platelet formation and megakaryocyte migration by regulating MYL9 (MLC2) and MMP9. Blood. 2009;114(19):4221-4232.
3. Cheng EC, Luo Q, Bruscia EM, et al. Role for MKL1 in megakaryocytic maturation. Blood. 2009;113(12):2826-2834.
4. Small EM, Thatcher JE, Sutherland LB, et al. Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ Res. 2010;107(2): 294-304.
5. Sun Y, Boyd K, Xu W, et al. Acute myeloid leukemia-associated Mkl1 (Mrtf-a) is a key regulator of mammary gland function. Mol Cell Biol. 2006;26(15):5809-5826. (Pubitemid 44134336)
6. Li S, Chang S, Qi X, Richardson JA, Olson EN. Requirement of a myocardin-related transcription factor for development of mammary myoepithelial cells. Mol Cell Biol. 2006;26(15):5797-5808. (Pubitemid 44134335)
7. Du KL, Chen M, Li J, Lepore JJ, Mericko P, Parmacek MS. Megakaryoblastic leukemia factor-1 transduces cytoskeletal signals and induces smooth muscle cell differentiation from un-differentiated embryonic stem cells. J Biol Chem. 2004;279(17):17578-17586. (Pubitemid 38560522)
8. Oh J, Richardson JA, Olson EN. Requirement of myocardin-related transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc Natl Acad Sci USA. 2005;102(42):15122-15127. (Pubitemid 41513345)
9. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science. 2007;316(5832):1749-1752. (Pubitemid 46988550)
10. Posern G, Sotiropoulos A, Treisman R. Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol Biol Cell. 2002;13(12):4167-4178. (Pubitemid 35471176)
11. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell. 2003;113(3):329-342. (Pubitemid 36556115)
12. Pawlowski R, Rajakyla EK, Vartiainen MK, Treisman R. An actin-regulated importin alpha/beta-dependent extended bipartite NLS directs nuclear import of MRTF-A. EMBO J. 2010;29(20): 3448-3458.
13. Wang D, Chang PS, Wang Z, et al. Activation of cardiac gene expression by myocardin, a tran-scriptional cofactor for serum response factor. Cell. 2001;105(7):851-862. (Pubitemid 32635087)
14. Kalita K, Kharebava G, Zheng JJ, Hetman M. Role of megakaryoblastic acute leukemia-1 in ERK1/2-dependent stimulation of serum response factor-driven transcription by BDNF or increased synaptic activity. J Neurosci. 2006; 26(39):10020-10032. (Pubitemid 44477163)
15. Evelyn CR, Bell JL, Ryu JG, et al. Design, synthesis and prostate cancer cell-based studies of analogs of the Rho/MKL1 transcriptional pathway inhibitor, CCG-1423. Bioorg Med Chem Lett. 2010;20(2):665-672.
16. Pronk CJ, Rossi DJ, Mansson R, et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell. 2007;1(4):428-442. (Pubitemid 47506534)
17. Gao Y, Smith E, Ker E, et al. Role of RhoA-specific guanine exchange factors in regulation of en-domitosis in megakaryocytes. Dev Cell. 2012; 22(3):573-584.
18. Pertz O, Hodgson L, Klemke RL, Hahn KM. Spa-tiotemporal dynamics of RhoA activity in migrating cells. Nature. 2006;440(7087):1069-1072.
19. Jin W, Goldfine AB, Boes T, et al. Increased SRF transcriptional activity in human and mouse skeletal muscle is a signature of insulin resistance. J Clin Invest. 2011;121(3):918-929.
20. Leon C, Eckly A, Hechler B, et al. Megakaryocyte-restricted MYH9 inactivation dramatically affects hemostasis while preserving platelet aggregation and secretion. Blood. 2007;110(9):3183-3191. (Pubitemid 350106310)
21. Chang Y, Aurade F, Larbret F, et al. Proplatelet formation is regulated by the Rho/ROCK pathway. Blood. 2007;109(10):4229-4236. (Pubitemid 46743387)
22. Burns JC, Friedmann T, Driever W, Burrascano M, Yee JK. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc Natl Acad Sci USA. 1993;90(17): 8033-8037. (Pubitemid 23260849)
23. Lu J, Guo S, Ebert BL, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14(6):843-853. (Pubitemid 351757199)
24. Smith EC, Thon JN, Devine MT, et al. MKL1 and MKL2 play redundant and crucial roles in mega-karyocyte maturation and platelet formation. Blood. 2012;120(11):2317-2329.
25. Murone M, Carpenter DA, de Sauvage FJ. Hema-topoietic deficiencies in c-mpl and TPO knockout mice. Stem Cells. 1998;16(1):1-6.
26. 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. (Pubitemid 47026832)
27. Malara A, Gruppi C, Pallotta I, et al. Extracellular matrix structure and nano-mechanics determine megakaryocyte function. Blood. 2011;118(16): 4449-4453.
28. Malara A, Gruppi C, Rebuzzini P, et al. Megakaryocyte-matrix interaction within bone marrow: new roles for fibronectin and factor XIII-A. Blood. 2011;117(8):2476-2483.
29. Descot A, Hoffmann R, Shaposhnikov D, Reschke M, Ullrich A, Posern G. Negative regulation of the EGFR-MAPK cascade by actin-MAL-mediated Mig6/Errfi-1 induction. Mol Cell. 2009; 35(3):291-304.
30. Huveneers S, Danen EH. Adhesion signaling-crosstalk between integrins, Src and Rho. J Cell Sci. 2009;122(Pt 8):1059-1069.
31. Busche S, Descot A, Julien S, Genth H, Posern G. Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J Cell Sci. 2008;121(Pt 7):1025-1035. (Pubitemid 351639421)
32. Fan L, Sebe A, Peterfi Z, et al. Cell contact-dependent regulation of epithelial-myofibroblast transition via the rho-rho kinase-phospho-myosin pathway. Mol Biol Cell. 2007;18(3):1083-1097. (Pubitemid 46399511)
33. Sebe A, Masszi A, Zulys M, et al. Rac, PAK and p38 regulate cell contact-dependent nuclear translocation of myocardin-related transcription factor. FEBS Lett. 2008;582(2):291-298.
34. McGee KM, Vartiainen MK, Khaw PT, Treisman R, Bailly M. Nuclear transport of the serum response factor coactivator MRTF-A is downregulated at tensional homeostasis. EMBO Rep. 2011;12(9): 963-970.
35. Ma Z, Morris SW, Valentine V, et al. Fusion of two novel genes, RBM15 and MKL1, in the t(1;22) (p13;q13) of acute megakaryoblastic leukemia. Nat Genet. 2001;28(3):220-221. (Pubitemid 32626023)
36. Mercher T, Coniat MB, Monni R, et al. Involvement of a human gene related to the Drosophila spen gene in the recurrent t(1;22) translocation of acute megakaryocytic leukemia. Proc Natl Acad Sci USA. 2001;98(10):5776-5779. (Pubitemid 32435718)