Ikaros fingers on lymphocyte differentiation

International Journal of Hematology

Volumn 100, Issue 3, 2014, Pages 220-229

  Yoshida, Toshimi ^a   Georgopoulos, Katia ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

B ALL; Epigenetic regulation; Ikaros; LMPP; Lymphocyte precursors; Mi 2 ; NuRD; T ALL

Indexed keywords

AUTOANTIGEN; CHD4 PROTEIN, HUMAN; HISTONE DEACETYLASE; IKAROS TRANSCRIPTION FACTOR; IKZF1 PROTEIN, HUMAN; ISOPROTEIN;

ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CYTOLOGY; GENETIC EPIGENESIS; GENETICS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOLOGY; LYMPHOPOIESIS; MOUSE; PRE B LYMPHOCYTE; PRE T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ANIMALS; AUTOANTIGENS; CELL DIFFERENTIATION; CELL LINEAGE; EPIGENESIS, GENETIC; HEMATOPOIETIC STEM CELLS; HUMANS; IKAROS TRANSCRIPTION FACTOR; LYMPHOPOIESIS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; PRECURSOR CELLS, B-LYMPHOID; PRECURSOR CELLS, T-LYMPHOID; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION;

EID: 84927172713     PISSN: 09255710     EISSN: 18653774     Source Type: Journal    
DOI: 10.1007/s12185-014-1644-5     Document Type: Article

References (69)

1. Georgopoulos K, Moore DD, Derfler B. Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science. 1992;258:808–12.
2. Hahm K, Ernst P, Lo K, Kim GS, Turck C, Smale ST. The lymphoid transcription factor LyF-1 is encoded by specific, alternatively spliced mRNAs derived from the Ikaros gene. Mol Cell Biol. 1994;14:7111–23.
3. Molnar A, Georgopoulos K. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol Cell Biol. 1994;14:8292–303.
4. Molnar A, Wu P, Largespada DA, Vortkamp A, Scherer S, Copeland NG, Jenkins NA, Bruns G, Georgopoulos K. The Ikaros gene encodes a family of lymphocyte-restricted zinc finger DNA binding proteins, highly conserved in human and mouse. J Immunol. 1996;156:585–92.
5. Koipally J, Heller EJ, Seavitt JR, Georgopoulos K. Unconventional potentiation of gene expression by Ikaros. J Biol Chem. 2002;277:13007–15.
6. Georgopoulos K, Bigby M, Wang JH, Molnar A, Wu P, Winandy S, Sharpe A. The Ikaros gene is required for the development of all lymphoid lineages. Cell. 1994;79:143–56.
7. Papathanasiou P, Perkins AC, Cobb BS, Ferrini R, Sridharan R, Hoyne GF, Nelms KA, Smale ST, Goodnow CC. Widespread failure of hematolymphoid differentiation caused by a recessive niche-filling allele of the Ikaros transcription factor. Immunity. 2003;19:131–44.
8. Joshi I, Yoshida T, Jena N, Qi X, Zhang J, Van Etten RA, Georgopoulos K. Loss of Ikaros DNA-binding function confers integrin-dependent survival on pre-B cells and progression to acute lymphoblastic leukemia. Nat Immunol. 2014;15:294–304.
9. Schjerven H, McLaughlin J, Arenzana TL, Frietze S, Cheng D, Wadsworth SE, Lawson GW, Bensinger SJ, Farnham PJ, Witte ON, et al. Selective regulation of lymphopoiesis and leukemogenesis by individual zinc fingers of Ikaros. Nat Immunol. 2013;14:1073–83.
10. Zhang J, Jackson AF, Naito T, Dose M, Seavitt J, Liu F, Heller EJ, Kashiwagi M, Yoshida T, Gounari F, et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol. 2011;13:86–94.
11. Cobb BS, Morales-Alcelay S, Kleiger G, Brown KE, Fisher AG, Smale ST. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA binding. Genes Dev. 2000;14:2146–60.
12. Hollenhorst PC, Shah AA, Hopkins C, Graves BJ. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 2007;21:1882–94.
13. Sun L, Liu A, Georgopoulos K. Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J. 1996;15:5358–69.
14. Morgan B, Sun L, Avitahl N, Andrikopoulos K, Ikeda T, Gonzales E, Wu P, Neben S, Georgopoulos K. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J. 1997;16:2004–13.
15. Kelley CM, Ikeda T, Koipally J, Avitahl N, Wu L, Georgopoulos K, Morgan BA. Helios, a novel dimerization partner of Ikaros expressed in the earliest hematopoietic progenitors. Curr Biol. 1998;8:508–15.
16. Honma Y, Kiyosawa H, Mori T, Oguri A, Nikaido T, Kanazawa K, Tojo M, Takeda J, Tanno Y, Yokoya S, et al. Eos: a novel member of the Ikaros gene family expressed predominantly in the developing nervous system. FEBS Lett. 1999;447:76–80.
17. Wang JH, Nichogiannopoulou A, Wu L, Sun L, Sharpe AH, Bigby M, Georgopoulos K. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity. 1996;5:537–49.
18. Kastner P, Dupuis A, Gaub MP, Herbrecht R, Lutz P, Chan S. Function of Ikaros as a tumor suppressor in B cell acute lymphoblastic leukemia. Am J Blood Res. 2013;3:1–13.
19. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature. 1998;395:917–21.
20. Wade PA, Jones PL, Vermaak D, Wolffe AP. A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr Biol. 1998;8:843–6.
21. Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell. 1998;2:851–61.
22. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet. 1999;23:62–6.
23. Kim J, Sif S, Jones B, Jackson A, Koipally J, Heller E, Winandy S, Viel A, Sawyer A, Ikeda T, et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity. 1999;10:345–55.
24. O’Neill DW, Schoetz SS, Lopez RA, Castle M, Rabinowitz L, Shor E, Krawchuk D, Goll MG, Renz M, Seelig HP, et al. An ikaros-containing chromatin-remodeling complex in adult-type erythroid cells. Mol Cell Biol. 2000;20:7572–82.
25. Sridharan R, Smale ST. Predominant interaction of both Ikaros and Helios with the NuRD complex in immature thymocytes. J Biol Chem. 2007;282:30227–38.
26. Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell. 1998;95:279–89.
27. Becker PB, Horz W. ATP-dependent nucleosome remodeling. Annu Rev Biochem. 2002;71:247–73.
28. Shimono Y, Murakami H, Kawai K, Wade PA, Shimokata K, Takahashi M. Mi-2 beta associates with BRG1 and RET finger protein at the distinct regions with transcriptional activating and repressing abilities. J Biol Chem. 2003;278:51638–45.
29. Williams CJ, Naito T, Arco PG, Seavitt JR, Cashman SM, De Souza B, Qi X, Keables P, Von Andrian UH, Georgopoulos K. The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development. Immunity. 2004;20:719–33.
30. Naito T, Gomez-Del Arco P, Williams CJ, Georgopoulos K. Antagonistic interactions between Ikaros and the chromatin remodeler Mi-2beta determine silencer activity and Cd4 gene expression. Immunity. 2007;27:723–34.
31. Yoshida T, Hazan I, Zhang J, Ng SY, Naito T, Snippert HJ, Heller EJ, Qi X, Lawton LN, Williams CJ, et al. The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev. 2008;22:1174–89.
32. Gomez-del Arco P, Kashiwagi M, Jackson AF, Naito T, Zhang J, Liu F, Kee B, Vooijs M, Radtke F, Redondo JM, et al. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity. 2010;33:685–98.
33. Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K, Jensen CT, Bryder D, Yang L, Borge OJ, Thoren LA, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121:295–306.
34. Yoshida T, Ng SY, Zuniga-Pflucker JC, Georgopoulos K. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol. 2006;7:382–91.
35. Lai AY, Kondo M. Asymmetrical lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. J Exp Med. 2006;203:1867–73.
36. Igarashi H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity. 2002;17:117–30.
37. Yokota T, Sudo T, Ishibashi T, Doi Y, Ichii M, Orirani K, Kanakura Y. Complementary regulation of early B-lymphoid differentiation by genetic and epigenetic mechanisms. Int J Hematol. 2013;98:382–9.
38. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell. 1997;91:661–72.
39. Allman D, Sambandam A, Kim S, Miller JP, Pagan A, Well D, Meraz A, Bhandoola A. Thymopoiesis independent of common lymphoid progenitors. Nat Immunol. 2003;4:168–74.
40. Doulatov S, Notta F, Eppert K, Nguyen LT, Ohashi PS, Dick JE. Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat Immunol. 2010;11:585–94.
41. Goardon N, Marchi E, Atzberger A, Quek L, Schuh A, Soneji S, Woll P, Mead A, Alford KA, Rout R, et al. Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia. Cancer Cell. 2011; 138–152.
42. Laurenti E, Doulatov S, Zandi S, Plumb I, Chen J, April C, Fan JB, Dick JE. The transcriptional architecture of early human hematopoiesis identifies multilevel control of lymphoid commitment. Nat Immunol. 2013;14:756–63.
43. Dias S, Mansson R, Gurbuxani S, Sigvardsson M, Kee BL. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity. 2008;29:217–27.
44. Ng SY, Yoshida T, Zhang J, Georgopoulos K: Genome-wide Lineage-Specific Transcriptional Networks Underscore Ikaros-Dependent Lymphoid Priming in Hematopoietic Stem Cells. Immunity. 2009.
45. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404:193–7.
46. Rumfelt LL, Zhou Y, Rowley BM, Shinton SA, Hardy RR. Lineage specification and plasticity in CD19- early B cell precursors. J Exp Med. 2006;203:675–87.
47. Mansson R, Zandi S, Anderson K, Martensson IL, Jacobsen SE, Bryder D, Sigvardsson M. B-lineage commitment prior to surface expression of B220 and CD19 on hematopoietic progenitor cells. Blood. 2008;112:1048–55.
48. Wada H, Masuda K, Satoh R, Kakugawa K, Ikawa T, Katsura Y, Kawamoto H. Adult T-cell progenitors retain myeloid potential. Nature. 2008;452:768–72.
49. Bell JJ, Bhandoola A. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature. 2008;452:764–7.
50. Kawamoto H, Ikawa T, Masuda K, Wada H, Katsura Y. A map for lineage restriction of progenitors during hematopoiesis: the essence of the myeloid-based model. Immunol Rev. 2010;238:23–36.
51. Winandy S, Wu P, Georgopoulos K. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell. 1995;83:289–99.
52. Winandy S, Wu L, Wang JH, Georgopoulos K. Pre-T cell receptor (TCR) and TCR-controlled checkpoints in T cell differentiation are set by Ikaros. J Exp Med. 1999;190:1039–48.
53. Jeannet R, Mastio J, Macias-Garcia A, Oravecz A, Ashworth T, Geimer Le Lay AS, Jost B, Le Gras S, Ghysdael J, Gridley T, et al. Oncogenic activation of the Notch1 gene by deletion of its promoter in Ikaros-deficient T-ALL. Blood. 2010;116:5443–54.
54. Ashworth TD, Pear WS, Chiang MY, Blacklow SC, Mastio J, Xu L, Kelliher M, Kastner P, Chan S, Aster JC. Deletion-based mechanisms of Notch1 activation in T-ALL: key roles for RAG recombinase and a conserved internal translational start site in Notch1. Blood. 2010;116:5455–64.
55. Urayama KY, Chokkalingam AP, Manabe A, Mizutani S. Current evidence for an inherited genetic basis of childhood acute lymphoblastic leukemia. Int J Hematol. 2013;97:3–19.
56. Mullighan CG, Goorha S, Radtke I, Miller CB, Coustan-Smith E, Dalton JD, Girtman K, Mathew S, Ma J, Pounds SB, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature. 2007;446:758–64.
57. Mullighan CG, Miller CB, Radtke I, Phillips LA, Dalton J, Ma J, White D, Hughes TP, Le Beau MM, Pui CH, et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature. 2008;453:110–4.
58. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D, Easton J, Chen X, Wang J, Rusch M, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012;481:157–63.
59. Schwickert TA, Tagoh H, Gultekin S, Dakic A, Axelsson E, Minnich M, Ebert A, Werner B, Roth M, Cimmino L, et al. Stage-specific control of early B cell development by the transcription factor Ikaros. Nat Immunol. 2014;15:283–93.
60. Dupuis A, Gaub MP, Legrain M, Drenou B, Mauvieux L, Lutz P, Herbrecht R, Chan S, Kastner P. Biclonal and biallelic deletions occur in 20% of B-ALL cases with IKZF1 mutations. Leukemia. 2013;27:503–7.
61. Marcais A, Jeannet R, Hernandez L, Soulier J, Sigaux F, Chan S, Kastner P. Genetic inactivation of Ikaros is a rare event in human T-ALL. Leuk Res. 2010;34:426–9.
62. Kaufmann C, Yoshida T, Perotti EA, Landhuis E, Wu P, Georgopoulos K. A complex network of regulatory elements in Ikaros and their activity during hemo-lymphopoiesis. EMBO J. 2003;22:2211–23.
63. Yoshida T, Landhuis E, Dose M, Hazan I, Zhang J, Naito T, Jackson AF, Wu J, Perroti EA, Kaufmann C, et al.: Transcriptional regulation of the Ikzf1 locus. Blood 2013.
64. Gandhi AK, Kang J, Havens CG, Conklin T, Ning Y, Wu L, Ito T, Ando H, Waldman MF, Thakurta A, et al. Immunomodulatory agents lenalidomide and pomalidomide co-stimulate T cells by inducing degradation of T cell repressors Ikaros and Aiolos via modulation of the E3 ubiquitin ligase complex CRL4(CRBN.). Br J Haematol. 2014;164:811–21.
65. Lu G, Middleton RE, Sun H, Naniong M, Ott CJ, Mitsiades CS, Wong KK, Bradner JE, Kaelin WG Jr. The myeloma drug lenalidomide promotes the cereblon-dependent destruction of Ikaros proteins. Science. 2014;343:305–9.
66. Watanabe R, Tokuhira M, Kizaki M. Current approaches for the treatment of multiple myeloma. Int J Hematol. 2013;97:333–44.
67. Cortes M, Georgopoulos K. Aiolos is required for the generation of high affinity bone marrow plasma cells responsible for long-term immunity. J Exp Med. 2004;199:209–19.
68. Anderson KC, Carrasco RD. Pathogenesis of myeloma. Annu Rev Pathol. 2011;6:249–74.
69. Hosen N. Multiple myeloma-initiating cells. Int J Hematol. 2013;97:306–12.