The calcineurin-NFAT pathway negatively regulates megakaryopoiesis

Blood

Volumn 121, Issue 16, 2013, Pages 3205-3215

  Zaslavsky, Alexander ^a   Chou, Stella T ^b   Schadler, Keri ^a   Lieberman, Allyson ^a   Pimkin, Maxim ^b   Kim, Yeo Jung ^a   Baek, Kwan Hyuck ^a,c   Aird, William C ^d   Weiss, Mitchell J ^b   Ryeom, Sandra ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c Sungkyunkwan University School of Medicine   (South Korea)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CALCINEURIN; CYCLIN DEPENDENT KINASE 4; CYCLINE; CYCLOSPORIN A; DNA; FAS LIGAND; MESSENGER RNA; TRANSCRIPTION FACTOR NFAT; DSCR1 PROTEIN, MOUSE; MUSCLE PROTEIN; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA CONTENT; DOWN SYNDROME; GENE EXPRESSION; GENETIC PREDISPOSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MEGAKARYOBLAST; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THROMBOCYTE COUNT; THROMBOCYTOSIS; TRISOMY 21; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL CYCLE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; THROMBOCYTOPOIESIS; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CALCINEURIN; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; DOWN SYNDROME; FAS LIGAND PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEGAKARYOCYTE PROGENITOR CELLS; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE PROTEINS; NFATC TRANSCRIPTION FACTORS; PLATELET COUNT; SIGNAL TRANSDUCTION; THROMBOPOIESIS;

MLCS; MLOWN;

EID: 84879127872     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-04-421172     Document Type: Article

References (46)

1. Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA, Crabtree GR. Identification of a putative regulator of early T cell activation genes. Science. 1988;241(4862):202-205.
2. Müller MR, Rao A. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol. 2010;10(9):645-656.
3. Kiani A, Kuithan H, Kuithan F, et al. Expression analysis of nuclear factor of activated T cells (NFAT) during myeloid differentiation of CD341 cells: regulation of Fas ligand gene expression in megakaryocytes. Exp Hematol. 2007;35(5): 757-770.
4. Arabanian LS, Kujawski S, Habermann I, Ehninger G, Kiani A. Regulation of fas/fas ligand-mediated apoptosis by nuclear factor of activated T cells in megakaryocytes. Br J Haematol. 2012; 156(4):523-534.
5. Giraudier S, Chagraoui H, Komura E, et al. Overexpression of FKBP51 in idiopathic myelofibrosis regulates the growth factor independence of megakaryocyte progenitors. Blood. 2002;100(8):2932-2940.
6. Kyttälä S, Habermann I, Minami T, Ehninger G, Kiani A. Regulation of Down Syndrome Critical Region 1 expression by Nuclear Factor of Activated T cells in megakaryocytes. Br J Haematol. 2009;144(3):395-408.
7. Malinge S, Bliss-Moreau M, Kirsammer G, et al. Increased dosage of the chromosome 21 ortholog Dyrk1a promotes megakaryoblastic leukemia in a murine model of Down syndrome. J Clin Invest. 2012;122(3):948-962.
8. Latinis KM, Norian LA, Eliason SL, Koretzky GA. Two NFAT transcription factor binding sites participate in the regulation of CD95 (Fas) ligand expression in activated human T cells. J Biol Chem. 1997;272(50):31427-31434.
9. Baksh S, Widlund HR, Frazer-Abel AA, et al. NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol Cell. 2002;10(5): 1071-1081.
10. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell. 2008;132(2): 299-310.
11. Macian F. NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol. 2005;5(6):472-484.
12. Baek KH, Zaslavsky A, Lynch RC, et al. Down’s syndrome suppression of tumour growth and the role of the calcineurin inhibitor DSCR1. Nature. 2009;459(7250):1126-1130.
13. McCrann DJ, Ravid K. Survivin localization during endomitosis of high ploidy mouse megakaryocytes. Blood. 2010;116(12): 2192-2193.
14. Shibasaki F, Price ER, Milan D, McKeon F. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature. 1996;382(6589):370-373.
15. Clay D, Rubinstein E, Mishal Z, et al. CD9 and megakaryocyte differentiation. Blood. 2001;97(7): 1982-1989.
16. Nakorn TN, Miyamoto T, Weissman IL. Characterization of mouse clonogenic megakaryocyte progenitors. Proc Natl Acad Sci USA. 2003;100(1):205-210.
17. Pronk CJH, Rossi DJ, Månsson 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.
18. Ng AP, Kauppi M, Metcalf D, Di Rago L, Hyland CD, Alexander WS. Characterization of thrombopoietin (TPO)-responsive progenitor cells in adult mouse bone marrow with in vivo megakaryocyte and erythroid potential. Proc Natl Acad Sci USA. 2012;109(7):2364-2369.
19. Deutsch VR, Tomer A. Megakaryocyte development and platelet production. Br J Haematol. 2006;134(5):453-466.
20. Carvalho LD, Teixeira LK, Carrossini N, et al. The NFAT1 transcription factor is a repressor of cyclin A2 gene expression. Cell Cycle. 2007;6(14): 1789-1795.
21. Caetano MS, Vieira-de-Abreu A, Teixeira LK, Werneck MB, Barcinski MA, Viola JP. NFATC2 transcription factor regulates cell cycle progression during lymphocyte activation: evidence of its involvement in the control of cyclin gene expression. FASEB J. 2002;16(14): 1940-1942.
22. Chou ST, Opalinska JB, Yao Y, et al. Trisomy 21 enhances human fetal erythro-megakaryocytic development. Blood. 2008;112(12):4503-4506.
23. Clipstone NA, Crabtree GR. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature. 1992;357(6380): 695-697.
24. Crabtree GR, Olson EN. NFAT signaling: choreographing the social lives of cells. Cell. 2002;109(Suppl):S67-S79.
25. Gallo EM, Ho L, Winslow MM, Staton TL, Crabtree GR. Selective role of calcineurin in haematopoiesis and lymphopoiesis. EMBO Rep. 2008;9(11):1141-1148.
26. Crist SA, Sprague DL, Ratliff TL. Nuclear factor of activated T cells (NFAT) mediates CD154 expression in megakaryocytes. Blood. 2008; 111(7):3553-3561.
27. Görlach J, Fox DS, Cutler NS, Cox GM, Perfect JR, Heitman J. Identification and characterization of a highly conserved calcineurin binding protein, CBP1/calcipressin, in Cryptococcus neoformans. EMBO J. 2000;19(14):3618-3629.
28. Kingsbury TJ, Cunningham KW. A conserved family of calcineurin regulators. Genes Dev. 2000; 14(13):1595-1604.
29. Rothermel BA, Vega RB, Williams RS. The role of modulatory calcineurin-interacting proteins in calcineurin signaling. Trends Cardiovasc Med. 2003;13(1):15-21.
30. Yang J, Rothermel B, Vega RB, et al. Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles. Circ Res. 2000;87(12): E61-E68.
31. Ryeom S, Greenwald RJ, Sharpe AH, McKeon F. The threshold pattern of calcineurin-dependent gene expression is altered by loss of the endogenous inhibitor calcipressin. Nat Immunol. 2003;4(9):874-881.
32. Bock O, Neusch M, Büsche G, Mengel M, Kreipe H. Constitutive expression of the FK506 binding protein 51 (FKBP51) in bone marrow cells and megakaryocytes derived from idiopathic myelofibrosis and non-neoplastic haematopoiesis. Eur J Haematol. 2004;72(4):239-244.
33. Srivastava RK, Sasaki CY, Hardwick JM, Longo DL. Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fas ligand transcription. J Exp Med. 1999;190(2):253-265.
34. Zauli G, Valvassori L, Capitani S. Presence and characteristics of circulating megakaryocyte progenitor cells in human fetal blood. Blood. 1993; 81(2):385-390.
35. Yuan J, Nguyen CK, Liu X, Kanellopoulou C, Muljo SA. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science. 2012;335(6073): 1195-1200.
36. Wieland KC, Cantor AB. Gene expression differences between fetal liver-derived and adult bone marrow-derived murine megakaryocyte progenitors: implications for DS-TMD. ASH 2008 Abstract. Boston, MA: Children’s hospital Boston 2008.
37. Falcone A, Musto P, Carotenuto M. Effect of cyclosporin-A on anemia in idiopathic myelofibrosis. Haematologica. 1998;83(7): 665-666.
38. Novik Y, Oleksowicz L, Wiernik PH. Therapeutic effect of cyclosporine A in thrombocytopenia after myeloablative chemotherapy in acute myeloid leukaemia. Med Oncol. 1997;14(1):43-46.
39. Schultz KR, Strahlendorf C, Warrier I, Ravindranath Y. Cyclosporin A therapy of immune-mediated thrombocytopenia in children. Blood. 1995;85(5):1406-1408.
40. Tunstall-Pedoe O, Roy A, Karadimitris A, et al. Abnormalities in the myeloid progenitor compartment in Down syndrome fetal liver precede acquisition of GATA1 mutations. Blood. 2008;112(12):4507-4511.
41. Kivivuori SM, Rajantie J, Siimes MA. Peripheral blood cell counts in infants with Down’s syndrome. Clin Genet. 1996;49(1):15-19.
42. Matsubara K, Nigami H, Yura K, Inoue T, Isome K, Fukaya T. Serum thrombopoietin level and thrombocytopenia during the neonatal period in infants with Down’s syndrome. J Perinatol. 2010; 30(2):98-102.
43. Park ES, Kim SY, Yeom JS, Lim JY, Park CH, Youn HS. Extreme thrombocytosis associated with transient myeloproliferative disorder with Down Syndrome with t(11;17)(q13;q21). Pediatr Blood Cancer. 2008;50(3):643-644.
44. Henry E, Walker D, Wiedmeier SE, Christensen RD. Hematological abnormalities during the first week of life among neonates with Down syndrome: data from a multihospital healthcare system. Am J Med Genet A. 2007;143(1):42-50.
45. Arron JR, Winslow MM, Polleri A, et al. NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21. Nature. 2006; 441(7093):595-600.
46. Reynolds LE, Watson AR, Baker M, et al. Tumour angiogenesis is reduced in the Tc1 mouse model of Down’s syndrome. Nature. 2010;465(7299): 813-817.