Genome-wide identification of Ikaros targets elucidates its contribution to mouse B-cell lineage specification and pre-B-cell differentiation

Blood

Volumn 121, Issue 10, 2013, Pages 1769-1782

  Ferreir ́ os Vidal, Isabel ^a,b   Carroll, Thomas ^b   Taylor, Benjamin ^a,b   Terry, Anna ^a,b   Liang, Ziwei ^a,b   Bruno, Ludovica ^a,b   Dharmalingam, Gopuraja ^b   Khadayate, Sanjay ^b   Cobb, Bradley S ^a,b   Smale, Stephen T ^c   Spivakov, Mikhail ^d   Srivastava, Prashant ^b   Petretto, Enrico ^b   Fisher, Amanda G ^a,b   Merkenschlager, Matthias ^a,b  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

IKAROS TRANSCRIPTION FACTOR; LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CELL CYCLE PROGRESSION; CELL LINEAGE; DNA SEQUENCE; DOWN REGULATION; FLOW CYTOMETRY; GENE CONTROL; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; IMMUNOFLUORESCENCE; IN VIVO STUDY; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

EID: 84876532900     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-450114     Document Type: Article

References (45)

1. Georgopoulos K. Haematopoietic cell-fate decisions, chromatin regulation and ikaros. Nat Rev Immunol. 2002;2(3):162-174. (Pubitemid 37328763)
2. Wang JH, Nichogiannopoulou A, Wu L, et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity. 1996;5(6):537-549. (Pubitemid 27062064)
3. Yoshida T, Ng SY, Zuniga-Pflucker JC, et al. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol. 2006;7(4):382-391.
4. Winandy S, Wu P, Georgopoulos K. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell. 1995;83(2):289-299.
5. Papathanasiou P, Perkins AC, Cobb BS, et al. Widespread failure of hematolymphoid differentiation caused by a recessive niche-filling allele of the Ikaros transcription factor. Immunity. 2003;19(1):131-144. (Pubitemid 36859907)
6. Zhang Z, Swindle CS, Bates JT, et al. Expression of a non-DNA-binding isoform of Helios induces T-cell lymphoma in mice. Blood. 2007;109(5): 2190-2197. (Pubitemid 46350683)
7. Mullighan CG, Miller CB, Radtke I, et al. BCRABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature. 2008;453(7191): 110-114. (Pubitemid 351630327)
8. Mullighan CG, Su X, Zhang J, et al Children's Oncology Group. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med. 2009;360(5):470-480.
9. Melchers F, ten Boekel E, Seidl T, et al. Repertoire selection by pre-B-cell receptors and B-cell receptors, and genetic control of B-cell development from immature to mature B cells. Immunol Rev. 2000;175:33-46. (Pubitemid 30427154)
10. 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.
11. Hardy RR, Carmack CE, Shinton SA, et al. Resolution and characterization of pro-B and prepro-B cell stages in normal mouse bone marrow. J Exp Med. 1991;173(5):1213-1225.
12. Painter MW, Davis S, Hardy RR, et al Immunological Genome Project Consortium. Transcriptomes of the B and T lineages compared by multiplatform microarray profiling. J Immunol. 2011;186(5):3047-3057.
13. Thompson EC, Cobb BS, Sabbattini P, et al. Ikaros DNA-binding proteins as integral components of B cell developmental-stagespecific regulatory circuits. Immunity. 2007;26(3): 335-344. (Pubitemid 46413909)
14. Sun L, Liu A, Georgopoulos K. Zinc fingermediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J. 1996;15(19):5358-5369. (Pubitemid 26336218)
15. Trinh LA, Ferrini R, Cobb BS, et al. Downregulation of TDT transcription in CD4(1)CD8(1) thymocytes by Ikaros proteins in direct competition with an Ets activator. Genes Dev. 2001;15(14):1817-1832. (Pubitemid 32905639)
16. McCarty AS, Kleiger G, Eisenberg D, et al. Selective dimerization of a C2H2 zinc finger subfamily. Mol Cell. 2003;11(2):459-470. (Pubitemid 36297056)
17. Ma S, Pathak S, Trinh L, et al. 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. (Pubitemid 351213426)
18. Ma S, Pathak S, Mandal M, et al. Ikaros and Aiolos inhibit pre-B-cell proliferation by directly suppressing c-Myc expression. Mol Cell Biol. 2010;30(17):4149-4158.
19. Mandal M, Powers SE, Ochiai K, et al. Ras orchestrates exit from the cell cycle and lightchain recombination during early B cell development. Nat Immunol. 2009;10(10): 1110-1117.
20. Reynaud D, Demarco IA, Reddy KL, et al. Regulation of B cell fate commitment and immunoglobulin heavy-chain gene rearrangements by Ikaros. Nat Immunol. 2008; 9(8):927-936.
21. Trageser D, Iacobucci I, Nahar R, et al. Pre-B cell receptor-mediated cell cycle arrest in Philadelphia chromosome-positive acute lymphoblastic leukemia requires IKAROS function. J Exp Med. 2009;206(8):1739-1753.
22. Merkenschlager M. Ikaros in immune receptor signaling, lymphocyte differentiation, and function. FEBS Lett. 2010;584(24):4910-4914.
23. Novershtern N, Subramanian A, Lawton LN, et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell. 2011;144(2):296-309.
24. G'omez-del Arco P, Kashiwagi M, Jackson AF, et al. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity. 2010;33(5):685-698.
25. Zhang J, Jackson AF, Naito T, et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol. 2011; 13(1):86-94.
26. Moln'ar A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol. 1994;14(12): 8292-8303.
27. Cobb BS, Morales-Alcelay S, Kleiger G, et al. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 2000;14(17):2146-2160.
28. Ng SY, Yoshida T, Zhang J, et al. Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells. Immunity. 2009;30(4): 493-507.
29. G'omez-del Arco P, Maki K, Georgopoulos K. Phosphorylation controls Ikaros's ability to negatively regulate the G(1)-S transition. Mol Cell Biol. 2004;24(7):2797-2807. (Pubitemid 38381271)
30. Brown KE, Guest SS, Smale ST, et al. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell. 1997;91(6):845-854. (Pubitemid 28007740)
31. Hahm K, Cobb BS, McCarty AS, et al. Helios, a T cell-restricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev. 1998; 12(6):782-796. (Pubitemid 28150880)
32. Hu H, Wang B, Borde M, et al. Foxp1 is an essential transcriptional regulator of B cell development. Nat Immunol. 2006;7(8):819-826. (Pubitemid 44084088)
33. 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.
34. 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.
35. Treiber T, Mandel EM, Pott S, et al. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcriptionindependent poising of chromatin. Immunity. 2010;32(5):714-725.
36. Heinz S, Benner C, Spann N, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010; 38(4):576-589.
37. Wilson NK, Foster SD, Wang X, et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell. 2010;7(4):532-544.
38. Spooner CJ, Cheng JX, Pujadas E, et al. A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity. 2009;31(4): 576-586.
39. Schulz D, Vassen L, Chow KT, et al. Gfi1b negatively regulates Rag expression directly and via the repression of FoxO1. J Exp Med. 2012; 209(1):187-199.
40. Mangan S, Alon U. Structure and function of the feed-forward loop network motif. Proc Natl Acad Sci USA. 2003;100(21):11980-11985. (Pubitemid 37271501)
41. Karnowski A, Cao C, Matthias G, et al. Silencing and nuclear repositioning of the lambda5 gene locus at the pre-B cell stage requires Aiolos and OBF-1. PLoS ONE. 2008; 3(10):e3568.
42. Liu YY, Slotine JJ, Barab́ asi AL. Controllability of complex networks. Nature. 2011;473(7346): 167-173.
43. Whitehurst AW, Bodemann BO, Cardenas J, et al. Synthetic lethal screen identification of chemosensitizer loci in cancer cells. Nature. 2007; 446(7137):815-819. (Pubitemid 46582032)
44. Scholl C, Frǒhling S, Dunn IF, et al. Synthetic lethal interaction between oncogenic KRAS dependency and STK33 suppression in human cancer cells. Cell. 2009;137(5):821-834.
45. Alkhatib A, Werner M, Hug E, et al. FoxO1 induces Ikaros splicing to promote immunoglobulin gene recombination. J Exp Med. 2012;209(2):395-406.