Essential control of early B-cell development by Mef2 transcription factors

Blood

Volumn 127, Issue 5, 2016, Pages 572-581

  Herglotz, Julia ^a   Unrau, Ludmilla ^a   Hauschildt, Friderike ^a   Fischer, Meike ^a   Kriebitzsch, Neele ^a   Alawi, Malik ^b,c   Indenbirken, Daniela ^b   Spohn, Michael ^b   Müller, Ursula ^a   Ziegler, Marion ^a   Schuh, Wolfgang ^d   Jäck, Hans Martin ^d   Stocking, Carol ^a  

^a Retroviral Pathogenesis   (Germany)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; EARLY GROWTH RESPONSE FACTOR 2; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 9; IMMUNOGLOBULIN HEAVY CHAIN; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 7; KRUPPEL LIKE FACTOR 2; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE 7; MYOCYTE ENHANCER FACTOR 2; MYOCYTE ENHANCER FACTOR 2C; MYOCYTE ENHANCER FACTOR 2D; PRE B CELL RECEPTOR; PROTEIN C JUN; SYNAPTOPHYSIN; TRANSCRIPTION FACTOR AIOLOS; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR EBF 1; TRANSCRIPTION FACTOR EGR 1; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR RUNX1; TRISTETRAPROLIN; UNCLASSIFIED DRUG; MEF2C PROTEIN, MOUSE; MEF2D PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING SITE; CELL ADHESION; CELL CYCLE CHECKPOINT; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENHANCER REGION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE ACTIVATION; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC CODE; GENETIC TRANSCRIPTION; HALF LIFE TIME; INTRACELLULAR SIGNALING; LYMPH NODE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTOPOIESIS; MITOSIS; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE REGULATORY NETWORK; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; TRANSCRIPTION INITIATION;

ANIMALS; B-LYMPHOCYTES; CELL LINE; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; GENE REGULATORY NETWORKS; MEF2 TRANSCRIPTION FACTORS; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 7; PHOSPHORYLATION; PRECURSOR CELLS, B-LYMPHOID; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84958211716     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2015-04-643270     Document Type: Article

References (76)

1. Busslinger M. Transcriptional control of early B cell development. Annu Rev Immunol. 2004;22:55-79.
2. Lin YC, Jhunjhunwala S, Benner C, et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat Immunol. 2010;11(7):635-643.
3. Mandel EM, Grosschedl R. Transcription control of early B cell differentiation. Curr Opin Immunol. 2010;22(2):161-167.
4. Barneda-Zahonero B, Roman-Gonzalez L, Collazo O, Mahmoudi T, Parra M. Epigenetic regulation of B lymphocyte differentiation, transdifferentiation, and reprogramming. Comp Funct Genomics. 2012;2012:564381.
5. Niebuhr B, Kriebitzsch N, Fischer M, et al. Runx1 is essential at two stages of early murine B-cell development. Blood. 2013;122(3): 413-423.
6. Rolink AG, Schaniel C, Andersson J, Melchers F. Selection events operating at various stages in B cell development. Curr Opin Immunol. 2001; 13(2):202-207.
7. Herzog S, Reth M, Jumaa H. Regulation of B-cell proliferation and differentiation by pre-B-cell receptor signalling. Nat Rev Immunol. 2009;9(3):195-205.
8. Vettermann C, Jack HM. The pre-B cell receptor: Turning autoreactivity into self-defense. Trends Immunol. 2010;31(5):176-183.
9. Clark MR, Mandal M, Ochiai K, Singh H. Orchestrating B cell lymphopoiesis through interplay of IL-7 receptor and pre-B cell receptor signalling. Nat Rev Immunol. 2014; 14(2):69-80.
10. Ma S, Pathak S, Trinh L, Lu R. Interferon regulatory factors 4 and 8 induce the expression of Ikaros and Aiolos to down-regulate pre-B-cell receptor and promote cell-cycle withdrawal in pre-B-cell development. Blood. 2008;111(3):1396-1403.
11. Thompson EC, Cobb BS, Sabbattini P, et al. Ikaros DNA-binding proteins as integral components of B cell developmental-stage-specific regulatory circuits. Immunity. 2007;26(3):335-344.
12. Murre C. Helix-loop-helix proteins and lymphocyte development. Nat Immunol. 2005;6(11): 1079-1086.
13. Dent AL, Shaffer AL, Yu X, Allman D, Staudt LM. Control of inflammation, cytokine expression, and germinal center formation by BCL-6. Science. 1997;276(5312):589-592.
14. Muto A, Ochiai K, Kimura Y, et al. Bach2 represses plasma cell gene regulatory network in B cells to promote antibody class switch. EMBO J. 2010;29(23):4048-4061.
15. Nutt SL, Taubenheim N, Hasbold J, Corcoran LM, Hodgkin PD. The genetic network controlling plasma cell differentiation. Semin Immunol. 2011; 23(5):341-349.
16. Debnath I, Roundy KM, Pioli PD, Weis JJ, Weis JH. Bone marrow-induced Mef2c deficiency delays B-cell development and alters the expression of key B-cell regulatory proteins. Int Immunol. 2013;25(2):99-115.
17. Gekas C, Rhodes KE, Gereige LM, et al. Mef2C is a lineage-restricted target of Scl/Tal1 and regulates megakaryopoiesis and B-cell homeostasis. Blood. 2009;113(15):3461-3471.
18. Wilker PR, Kohyama M, Sandau MM, et al. Transcription factor Mef2c is required for B cell proliferation and survival after antigen receptor stimulation. Nat Immunol. 2008;9(6):603-612.
19. Shore P, Sharrocks AD. The MADS-box family of transcription factors. Eur J Biochem. 1995;229(1):1-13.
20. Potthoff MJ, Olson EN. MEF2: A central regulator of diverse developmental programs. Development. 2007;134(23):4131-4140.
21. Heng TS, Painter MW; Immunological Genome Project Consortium. The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol. 2008;9(10):1091-1094.
22. Seita J, Sahoo D, Rossi DJ, et al. Gene Expression Commons: An open platform for absolute gene expression profiling. PLoS One. 2012;7(7):e40321.
23. Mullighan CG. Genomic analysis of acute leukemia. Int J Lab Hematol. 2009;31(4):384-397.
24. Prima V, Gore L, Caires A, et al. Cloning and functional characterization of MEF2D/DAZAP1 and DAZAP1/MEF2D fusion proteins created by a variant t(1;19)(q23;p13.3) in acute lymphoblastic leukemia. Leukemia. 2005;19(5):806-813.
25. Yuki Y, Imoto I, Imaizumi M, et al. Identification of a novel fusion gene in a pre-B acute lymphoblastic leukemia with t(1;19)(q23;p13). Cancer Sci. 2004; 95(6):503-507.
26. Lin Q, Schwarz J, Bucana C, Olson EN. Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. Science. 1997; 276(5317):1404-1407.
27. Kim Y, Phan D, van Rooij E, et al. The MEF2D transcription factor mediates stress-dependent cardiac remodeling in mice. J Clin Invest. 2008; 118(1):124-132.
28. Hobeika E, Thiemann S, Storch B, et al. Testing gene function early in the B cell lineage in mb1-cre mice. Proc Natl Acad Sci USA. 2006; 103(37):13789-13794.
29. Winkelmann R, Sandrock L, Porstner M, et al. B cell homeostasis and plasma cell homing controlled by Krüppel-like factor 2. Proc Natl Acad Sci USA. 2011;108(2):710-715.
30. Jumaa H, Wollscheid B, Mitterer M, Wienands J, Reth M, Nielsen PJ. Abnormal development and function of B lymphocytes in mice deficient for the signaling adaptor protein SLP-65. Immunity. 1999;11(5):547-554.
31. Meixlsperger S, Kohler F, Wossning T, Reppel M, Muschen M, Jumaa H. Conventional light chains inhibit the autonomous signaling capacity of the B cell receptor. Immunity. 2007;26(3):323-333.
32. Herglotz J, Kuvardina ON, Kolodziej S, et al. Histone arginine methylation keeps RUNX1 target genes in an intermediate state. Oncogene. 2013; 32(20):2565-2575.
33. Szklarczyk D, Franceschini A, Wyder S, et al. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43(Database issue):D447-D452.
34. Schuh W, Meister S, Herrmann K, Bradl H, Jäck HM. Transcriptome analysis in primary B lymphoid precursors following induction of the pre-B cell receptor. Mol Immunol. 2008;45(2): 362-375.
35. Swaminathan S, Duy C, Müschen M. BACH2-BCL6 balance regulates selection at the pre-B cell receptor checkpoint. Trends Immunol. 2014;35(3):131-137.
36. Schwickert TA, Tagoh H, Gultekin S, et al. Stagespecific control of early B cell development by the transcription factor Ikaros. Nat Immunol. 2014; 15(3):283-293.
37. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics. 2011;27(7):1017-1018.
38. Ochiai K, Maienschein-Cline M, Mandal M, et al. A self-reinforcing regulatory network triggered by limiting IL-7 activates pre-BCR signaling and differentiation. Nat Immunol. 2012;13(3):300-307.
39. Ferreiros-Vidal I, Carroll T, Taylor B, et al. Genome-wide identification of Ikaros targets elucidates its contribution to mouse B-cell lineage specification and pre-B-cell differentiation. Blood. 2013;121(10):1769-1782.
40. ENCODE Project Consortium. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011;9(4):e1001046.
41. Gould J. GENE.E: Interact with GENE-E from R. Vol. R package version 1.6.0. Cambridge, MA: Broad Institute; 2013.
42. Zhu LJ, Gazin C, Lawson ND, et al. ChIPpeakAnno: A Bioconductor package to annotate ChIP-seq and ChIP-chip data. BMC Bioinformatics. 2010;11:237.
43. McKinsey TA, Zhang CL, Olson EN. MEF2: A calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci. 2002;27(1):40-47.
44. Molkentin JD, Black BL, Martin JF, Olson EN. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 1995;83(7):1125-1136.
45. Morin S, Charron F, Robitaille L, Nemer M. GATAdependent recruitment of MEF2 proteins to target promoters. EMBO J. 2000;19(9):2046-2055.
46. Yang XJ, Gŕegoire S. Class II histone deacetylases: from sequence to function, regulation, and clinical implication. Mol Cell Biol. 2005;25(8):2873-2884.
47. Yasuda T, Sanjo H, Pages G, et al. Erk kinases link pre-B cell receptor signaling to transcriptional events required for early B cell expansion. Immunity. 2008;28(4):499-508.
48. Han J, Jiang Y, Li Z, Kravchenko VV, Ulevitch RJ. Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature. 1997;386(6622):296-299.
49. Kato Y, Zhao M, Morikawa A, et al. Big mitogenactivated kinase regulates multiple members of the MEF2 protein family. J Biol Chem. 2000; 275(24):18534-18540.
50. Cox DM, Du M, Marback M, et al. Phosphorylation motifs regulating the stability and function of myocyte enhancer factor 2A. J Biol Chem. 2003; 278(17):15297-15303.
51. Ji H, Wang J, Nika H, et al. EGF-induced ERK activation promotes CK2-mediated disassociation of alpha-Catenin from beta-Catenin and transactivation of beta-Catenin. Mol Cell. 2009;36(4):547-559.
52. Molkentin JD, Li L, Olson EN. Phosphorylation of the MADS-Box transcription factor MEF2C enhances its DNA binding activity. J Biol Chem. 1996;271(29):17199-17204.
53. Zhao M, New L, Kravchenko VV, et al. Regulation of the MEF2 family of transcription factors by p38. Mol Cell Biol. 1999;19(1):21-30.
54. Amit I, Citri A, Shay T, et al. A module of negative feedback regulators defines growth factor signaling. Nat Genet. 2007;39(4):503-512.
55. Corfe SA, Paige CJ. The many roles of IL-7 in B cell development; mediator of survival, proliferation and differentiation. Semin Immunol. 2012;24(3):198-208.
56. Fleming HE, Paige CJ. Pre-B cell receptor signaling mediates selective response to IL-7 at the pro-B to pre-B cell transition via an ERK/MAP kinase-dependent pathway. Immunity. 2001; 15(4):521-531.
57. Mandal M, Powers SE, Ochiai K, et al. Ras orchestrates exit from the cell cycle and light-chain recombination during early B cell development. Nat Immunol. 2009;10(10):1110-1117.
58. Nishimoto S, Nishida E. MAPK signalling: ERK5 versus ERK1/2. EMBO Rep. 2006;7(8):782-786.
59. Plotnikov A, Zehorai E, Procaccia S, Seger R. The MAPK cascades: signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim Biophys Acta. 2011;1813(9):1619-1633.
60. Dodou E, Treisman R. The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-Activated protein kinase pathway. Mol Cell Biol. 1997;17(4):1848-1859.
61. Posern G, Treisman R. Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 2006;16(11):588-596.
62. Fleige A, Alberti S, Gröbe L, et al. Serum response factor contributes selectively to lymphocyte development. J Biol Chem. 2007;282(33): 24320-24328.
63. Mylona A, Nicolas R, Maurice D, et al. The essential function for serum response factor in T-cell development reflects its specific coupling to extracellular signal-regulated kinase signaling. Mol Cell Biol. 2011;31(2):267-276.
64. Kato Y, Kravchenko VV, Tapping RI, Han J, Ulevitch RJ, Lee JD. BMK1/ERK5 regulates serum-induced early gene expression through transcription factor MEF2C. EMBO J. 1997; 16(23):7054-7066.
65. Sharrocks AD, Yang SH, Galanis A. Docking domains and substrate-specificity determination for MAP kinases. Trends Biochem Sci. 2000; 25(9):448-453.
66. Yang SH, Galanis A, Sharrocks AD. Targeting of p38 mitogen-Activated protein kinases to MEF2 transcription factors. Mol Cell Biol. 1999;19(6): 4028-4038.
67. Di Giorgio E, Gagliostro E, Clocchiatti A, Brancolini C. The control operated by the cell cycle machinery on MEF2 stability contributes to the downregulation of CDKN1A and entry into S phase. Mol Cell Biol. 2015;35(9):1633-1647.
68. Black BL, Lu J, Olson EN. The MEF2A 39 untranslated region functions as a cis-Acting translational repressor. Mol Cell Biol. 1997;17(5): 2756-2763.
69. Alon U. Network motifs: Theory and experimental approaches. Nat Rev Genet. 2007;8(6):450-461.
70. Shaulian E, Karin M. AP-1 as a regulator of cell life and death. Nat Cell Biol. 2002;4(5):E131-E136.
71. Thiel G, Cibelli G. Regulation of life and death by the zinc finger transcription factor Egr-1. J Cell Physiol. 2002;193(3):287-292.
72. Sanduja S, Blanco FF, Young LE, Kaza V, Dixon DA. The role of tristetraprolin in cancer and inflammation. Front Biosci. 2012;17:174-188.
73. Hart GT, Hogquist KA, Jameson SC. Kruppel-like factors in lymphocyte biology. J Immunol. 2012; 188(2):521-526.
74. Winkelmann R, Sandrock L, Kirberg J, Jäck HM, Schuh W. KLF2-A negative regulator of pre-B cell clonal expansion and B cell activation. PLoS One. 2014;9(5):e97953.
75. Buchner M, Swaminathan S, Chen Z, Müschen M. Mechanisms of pre-B-cell receptor checkpoint control and its oncogenic subversion in acute lymphoblastic leukemia. Immunol Rev. 2015; 263(1):192-209.
76. Rickert RC. New insights into pre-BCR and BCR signalling with relevance to B cell malignancies. Nat Rev Immunol. 2013;13(8):578-591.