E and ID proteins branch out

Nature Reviews Immunology

Volumn 9, Issue 3, 2009, Pages 175-184

  Kee, Barbara L ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; INHIBITOR OF DIFFERENTIATION PROTEIN; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR E2A;

B LYMPHOCYTE; CELL DEGENERATION; CELL LINEAGE; CELL MATURATION; CELL MEMBRANE PERMEABILITY; CELL MOTION; DENDRITIC CELL; DNA BINDING; DRUG BINDING; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; INVERTEBRATE; LYMPHOCYTE DIFFERENTIATION; LYMPHOID PROGENITOR CELL; LYMPHOPOIESIS; MENTAL FUNCTION; NATURAL KILLER CELL; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN TARGETING; REVIEW; STEM CELL; T LYMPHOCYTE;

ANIMALS; B-LYMPHOCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINEAGE; DENDRITIC CELLS; DNA-BINDING PROTEINS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; KILLER CELLS, NATURAL; LYMPHOPOIESIS; T-LYMPHOCYTES;

EID: 61349152914     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2507     Document Type: Review

References (103)

1. Alt, F. W., Blackwell, T. K., DePinho, R. A., Reth, M. G. & Yancopoulos, G. D. Regulation of genome rearrangement events during lymphocyte differentiation. Immunol. Rev. 89, 5-30 (1986).
2. Kincade, P. W. Molecular signals for the production of lymphocytes in bone marrow. Braz. J. Med. Biol. Res. 27, 2533-2538 (1994).
3. Whitlock, C. A., Robertson, D. & Witte, O. N. Murine B cell lymphopoiesis in long term culture. J. Immunol. Methods 67, 353-369 (1984).
4. Nutt, S. L. & Kee, B. L. The transcriptional regulation of B cell lineage commitment. Immunity 26, 715-725 (2007).
5. Di Santo, J. P. Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24, 257-286 (2006).
6. Rothenberg, E. V. Negotiation of the T lineage fate decision by transcription-factor interplay and microenvironmental signals. Immunity 26, 690-702 (2007).
7. Wu, L. & Liu, Y. J. Development of dendritic-cell lineages. Immunity 26, 741-750 (2007).
8. Engel, I. & Murre, C. The function of E- and ID proteins in lymphocyte development. Nature Rev. Immunol. 1, 193-199 (2001).
9. Mullighan, C. G. et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 446, 758-764 (2007).
10. Wang, D. et al. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J. Immunol. 177, 109-119 (2006).
11. Massari, M. E. & Murre, C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20, 429-440 (2000).
12. Murre, C. Helix-loop-helix proteins and lymphocyte development. Nature Immunol. 6, 1079-1086 (2005).
13. Singh, H., Medina, K. L. & Pongubala, J. M. Contingent gene regulatory networks and B cell fate specification. Proc. Natl Acad. Sci. USA 102, 4949-4953 (2005).
14. Inlay, M. A., Tian, H., Lin, T. & Xu, Y. Important roles for E protein binding sites within the immunoglobulin k chain intronic enhancer in activating VκJκ rearrangement. J. Exp. Med. 200, 1205-1211 (2004). This paper establishes the importance of the E protein binding sites in the Igκ intronic enhancer for Igκ rearrangement using site-directed mutagenesis.
15. H recombination. J. Immunol. 176, 2439-2447 (2006).
16. Schlissel, M. S. Regulation of activation and recombination of the murine Igκ locus. Immunol. Rev. 200, 215-223 (2004).
17. Lazorchak, A. S., Schlissel, M. S. & Zhuang, Y. E2A and IRF-4/Pip promote chromatin modification and transcription of the immunoglobulin κ locus in pre-B cells. Mol. Cell. Biol. 26, 810-821 (2006).
18. Nagulapalli, S. & Atchison, M. L. Transcription factor Pip can enhance DNA binding by E47, leading to transcriptional synergy involving multiple protein domains. Mol. Cell. Biol. 18, 4639-4650 (1998).
19. Romanow, W. J. et al. E2A and EBF act in synergy with the V(D)J recombinase to generate a diverse immunoglobulin repertoire in nonlymphoid cells. Mol. Cell 5, 343-53 (2000). This paper establishes that E2A proteins, in combination with RAG1 and RAG2, are sufficient to initiate recombination at the Igκ loci in non-lymphoid cells.
20. Goebel, P. et al. Localized gene-specific induction of accessibility to V(D)J recombination induced by E2A and early B cell factor in nonlymphoid cells. J. Exp. Med. 194, 645-656 (2001).
21. -/- haematopoietic progenitors.
22. Kee, B. L. & Murre, C. Induction of early B cell factor (EBF) and multiple B lineage genes by the basic helix-loop-helix transcription factor E12. J. Exp. Med. 188, 699-713 (1998).
23. Kee, B. L., Rivera, R. R. & Murre, C. Id3 inhibits B lymphocyte progenitor growth and survival in response to TGF-β. Nature Immunol. 2, 242-247 (2001).
24. Hsu, L. Y. et al. A conserved transcriptional enhancer regulates RAG gene expression in developing B cells. Immunity 19, 105-117 (2003). This paper shows a role for E proteins in the regulation of a B-cell-specific enhancer of Rag1 and Rag2.
25. Borghesi, L. et al. B lineage-specific regulation of V(D)J recombinase activity is established in common lymphoid progenitors. J. Exp. Med. 199, 491-502 (2004).
26. Bain, G. et al. Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nature Immunol. 2, 165-171 (2001).
27. Zhuang, Y., Cheng, P. & Weintraub, H. B-lymphocyte development is regulated by the combined dosage of three basic helix-loop-helix genes, E2A, E2-2, and HEB. Mol. Cell. Biol. 16, 2898-2905 (1996).
28. Sun, X. H. & Baltimore, D. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 64, 459-470 (1991).
29. Roessler, S. et al. Distinct promoters mediate the regulation of Ebf1 gene expression by interleukin-7 and Pax5. Mol. Cell. Biol. 27, 579-594 (2007).
30. Kwon, K. et al. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 28, 751-762 (2008).
31. Kee, B. L., Quong, M. W. & Murre, C. E2A proteins: essential regulators at multiple stages of B-cell development. Immunol. Rev. 175, 138-149 (2000).
32. Ikawa, T., Kawamoto, H., Wright, L. Y. & Murre, C. Long-term cultured E2A-deficient hematopoietic progenitor cells are pluripotent. Immunity 20, 349-360 (2004).
33. Maier, H. et al. Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nature Immunol. 5, 1069-1077 (2004).
34. Sigvardsson, M. et al. Early B-cell factor, E2A, and Pax-5 cooperate to activate the early B cell-specific mb-1 promoter. Mol. Cell. Biol. 22, 8539-8551 (2002).
35. Zhuang, Y., Barndt, R. J., Pan, L., Kelley, R. & Dai, M. Functional replacement of the mouse E2A gene with a human HEB cDNA. Mol. Cell. Biol. 18, 3340-3349 (1998). This paper shows the redundancy between E proteins. In this case, expression of HEB under control of the E2A loci was sufficient to substantially rescue B-cell development.
36. Lazorchak, A. S., Wojciechowski, J., Dai, M. & Zhuang, Y. E2A promotes the survival of precursor and mature B lymphocytes. J. Immunol. 177, 2495-2504 (2006).
37. Kee, B. L. Id3 induces growth arrest and caspase-2-dependent apoptosis in B lymphocyte progenitors. J. Immunol. 175, 4518-4527 (2005).
38. Nutt, S. L., Morrison, A. M., Dorfler, P., Rolink, A. & Busslinger, M. Identification of BSAP (Pax-5) target genes in early B-cell development by loss- and gain-of-function experiments. EMBO J. 17, 2319-2333 (1998).
39. Bain, G. et al. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17, 4782-4791 (1997).
40. Bain, G., Gruenwald, S. & Murre, C. E2A and E2-2 are subunits of B-cell-specific E2-box DNA-binding proteins. Mol. Cell. Biol. 13, 3522-3529 (1993).
41. Barndt, R. J., Dai, M. & Zhuang, Y. Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Mol. Cell. Biol. 20, 6677-6685 (2000).
42. Pear, W. S. & Radtke, F. Notch signaling in lymphopoiesis. Semin. Immunol. 15, 69-79 (2003).
43. Hozumi, K. et al. Delta-like 4 is indispensable in thymic environment specific for T cell development. J. Exp. Med. 205, 2507-2513 (2008).
44. Koch, U. et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205, 2515-2523 (2008).
45. Tanigaki, K. & Honjo, T. Regulation of lymphocyte development by Notch signaling. Nature Immunol. 8, 451-456 (2007).
46. Pui, J. C. et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11, 299-308 (1999).
47. Huang, Z., Nie, L., Xu, M. & Sun, X. H. Notch-induced E2A degradation requires CHIP and Hsc70 as novel facilitators of ubiquitination. Mol. Cell. Biol. 24, 8951-8962 (2004).
48. Nie, L., Xu, M., Vladimirova, A. & Sun, X. H. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22, 5780-5792 (2003).
49. Nie, L. et al. Regulation of lymphocyte development by cell-type-specific interpretation of Notch signals. Mol. Cell. Biol. 28, 2078-2090 (2008). This paper shows that a series of MAPK phosphorylation sites in E2A proteins are not essential to allow Notch-dependent T-cell development, but function to decrease B-cell development in the presence of Notch signals.
50. Dias, S., Mansson, R., Gurbuxani, S., Sigvardsson, M. & Kee, B. L. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 29, 217-227 (2008). This paper reveals a role for E2A proteins in the generation of LMPPs and in lymphoid priming in these cells. A role for E2A proteins in suppressing proliferation of HSCs and LMPPs is also shown.
51. Ikawa, T., Kawamoto, H., Goldrath, A. W. & Murre, C. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J. Exp. Med. 203, 1329-1342 (2006). This paper demonstrates that E2A proteins are required for optimal expression of Notch1 and Notch3 and that they synergize with Notch signalling to activate multiple downstream target genes and to suppress NK-cell and myeloid-cell development.
52. Besseyrias, V. et al. Hierarchy of Notch-Delta interactions promoting T cell lineage commitment and maturation. J. Exp. Med. 204, 331-343 (2007).
53. Bergqvist, I. et al. The basic helix-loop-helix transcription factor E2-2 is involved in T lymphocyte development. Eur. J. Immunol. 30, 2857-2863 (2000).
54. Wikstrom, I., Forssell, J., Penha-Goncalves, M. N., Bergqvist, I. & Holmberg, D. A role for E2-2 at the DN3 stage of early thymopoiesis. Mol. Immunol. 45, 3302-3311 (2008).
55. Tremblay, M., Herblot, S., Lecuyer, E. & Hoang, T. Regulation of pTa gene expression by a dosage of E2A, HEB, and SCL. J. Biol. Chem. 278, 12680-12687 (2003).
56. Schwartz, R., Engel, I., Fallahi-Sichani, M., Petrie, H. T. & Murre, C. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc. Natl Acad. Sci. USA 103, 9976-9981 (2006).
57. Xu, W. & Kee, B. L. Growth factor independent 1B (Gfi1b) is an E2A target gene that modulates Gata3 in T-cell lymphomas. Blood 109, 4406-4414 (2007).
58. Fiolka, K. et al. Gfi1 and Gfi1b act equivalently in haematopoiesis, but have distinct, non-overlapping functions in inner ear development. EMBO Rep. 7, 326-333 (2006).
59. + T cell progenitors and CD4/CD8 lineage decision in the thymus. J. Exp. Med. 197, 831-844 (2003).
60. Agata, Y. et al. Regulation of T cell receptor β gene rearrangements and allelic exclusion by the helix-loop-helix protein, E47. Immunity 27, 871-884 (2007). This paper provides a mechanism by which E2A proteins regulate Tcrb gene expression and are targeted by pre-TCR signalling to mediate allelic exclusion.
61. Engel, I., Johns, C., Bain, G., Rivera, R. R. & Murre, C. Early thymocyte development is regulated by modulation of E2A protein activity. J. Exp. Med. 194, 733-745 (2001).
62. Bain, G., Romanow, W. J., Albers, K., Havran, W. L. & Murre, C. Positive and negative regulation of V(D)J recombination by the E2A proteins. J. Exp. Med. 189, 289-300 (1999).
63. Xiong, N. & Raulet, D. H. Development and selection of γδ T cells. Immunol. Rev. 215, 15-31 (2007).
64. Wojciechowski, J., Lai, A., Kondo, M. & Zhuang, Y. E2A and HEB are required to block thymocyte proliferation prior to pre-TCR expression. J. Immunol. 178, 5717-5726 (2007).
65. +/- mice and patients with Pitt-Hopkins syndrome, who have a haploinsufficiency of E2-2.
66. Nagasawa, M., Schmidlin, H., Hazekamp, M. G., Schotte, R. & Blom, B. Development of human plasmacytoid dendritic cells depends on the combined action of the basic helix-loop-helix factor E2-2 and the Ets factor Spi-B. Eur. J. Immunol. 38, 2389-2400 (2008). This paper demonstrates a role for E2-2 in pDC development through the use of ectopic expression and RNA interference-mediated inhibition of E2-2 expression in pDC progenitors. This study also indicates that E2-2 and SPIB may function together to promote pDC development.
67. + plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nature Immunol. 8, 1207-1216 (2007).
68. Harman, B. C., Miller, J. P., Nikbakht, N., Gerstein, R. & Allman, D. Mouse plasmacytoid dendritic cells derive exclusively from estrogen-resistant myeloid progenitors. Blood 108, 878-885 (2006).
69. Naik, S. H. et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nature Immunol. 8, 1217-1226 (2007).
70. Hacker, C. et al. Transcriptional profiling identifies Id2 function in dendritic cell development. Nature Immunol. 4, 380-386 (2003).
71. + stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J. Exp. Med. 192, 1775-1784 (2000).
72. Schotte, R., Nagasawa, M., Weijer, K., Spits, H. & Blom, B. The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J. Exp. Med. 200, 1503-1509 (2004).
73. Ji, M. et al. Id2 intrinsically regulates lymphoid and erythroid development via interaction with different target proteins. Blood 112, 1068-1077 (2008).
74. Haks, M. C. et al. Attenuation of γδTCR signaling efficiently diverts thymocytes to the αβ lineage. Immunity 22, 595-606 (2005).
75. Yokota, Y. et al. Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397, 702-706 (1999). This paper shows an essential role for ID2 in the development of mature NK cells and lymphoid-tissue inducer (LTi) cells.
76. Kee, B. L. Helix-loop-helix proteins in lymphocyte lineage determination. Curr. Top. Microbiol Immunol. 290, 15-27 (2005).
77. Ikawa, T., Fujimoto, S., Kawamoto, H., Katsura, Y. & Yokota, Y. Commitment to natural killer cells requires the helix-loop-helix inhibitor Id2. Proc. Natl Acad. Sci. USA 98, 5164-5169 (2001).
78. Boos, M. D., Yokota, Y., Eberl, G. & Kee, B. L. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204, 1119-1130 (2007). This paper reveals that ID2 functions in NK-cell and LTi-cell development to repress E protein activity and that ID2 is not required for NK-cell development in adult bone marrow until a mature NK-cell stage. This paper raises the issue of ID protein redundancy at early stages of NK-cell development.
79. Vosshenrich, C. A. et al. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nature Immunol. 7, 1217-1224 (2006).
80. Stewart, C. A. et al. Germ-line and rearranged Tcrd transcription distinguish bona fide NK cells and NK-like γδ T cells. Eur. J. Immunol. 37, 1442-1452 (2007).
81. + lymphomyeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121, 295-306 (2005).
82. Arinobu, Y. et al. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 1, 416-427 (2007).
83. Cochrane, S. W., Zhao, Y., Welner, R. S. & Sun, X. H. Balance between Id and E proteins regulates myeloid versus lymphoid lineage decisions. Blood 21 Sep 2008 (doi:10.1182/blood-2008-06-164996).
84. Dias, S., Xu, W., McGregor, S. & Kee, B. Transcriptional regulation of lymphocyte development. Curr. Opin. Genet. Dev. 18, 441-448 (2008).
85. Yoshida, T. et al. The role of the chromatin remodeler Mi-2β in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev. 22, 1174-1189 (2008).
86. Yang, Q. et al. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J. Immunol. 181, 5885-5894 (2008). This paper shows that E2A proteins are required to prevent the proliferation of HSCs as well as their exhaustion after treatment with 5-fluoruracil.
87. Jankovic, V. et al. Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells. Proc. Natl Acad. Sci. USA 104, 1260-1265 (2007).
88. Perry, S. S. et al. Id1, but not Id3, directs long-term repopulating hematopoietic stem-cell maintenance. Blood 110, 2351-2360 (2007).
89. Leeanansaksiri, W. et al. IL-3 induces inhibitor of DNA-binding protein-1 in hemopoietic progenitor cells and promotes myeloid cell development. J. Immunol. 174, 7014-7021 (2005).
90. Aspland, S. E., Bendall, H. H. & Murre, C. The role of E2A-PBX1 in leukemogenesis. Oncogene 20, 5708-5717 (2001).
91. LeBrun, D. P. E2A basic helix-loop-helix transcription factors in human leukemia. Front. Biosci. 8, s206-s222 (2003).
92. Ferrando, A. A. & Look, A. T. Gene expression profiling in T-cell acute lymphoblastic leukemia. Semin. Hematol. 40, 274-280 (2003).
93. Sun, X. H. Multitasking of helix-loop-helix proteins in lymphopoiesis. Adv. Immunol. 84, 43-77 (2004).
94. Reschly, E. J. et al. Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and -independent mechanisms. Blood 107, 4115-4121 (2006).
95. Zhang, J., Kalkum, M., Yamamura, S., Chait, B. T. & Roeder, R. G. E protein silencing by the leukemogenic AML1-ETO fusion protein. Science 305, 1286-1289 (2004).
96. Porcher, C. et al. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86, 47-57 (1996).
97. Shivdasani, R. A., Mayer, E. L. & Orkin, S. H. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373, 432-434 (1995).
98. Mikkola, H. K. et al. Haematopoietic stem cells retain long-term repopulating activity and multipotency in the absence of stem-cell leukaemia SCL/tal-1 gene. Nature 421, 547-551 (2003).
99. Curtis, D. J. et al. SCL is required for normal function of short-term repopulating hematopoietic stem cells. Blood 103, 3342-3348 (2004).
100. Capron, C. et al. The SCL relative LYL-1 is required for fetal and adult hematopoietic stem cell function and B-cell differentiation. Blood 107, 4678-4686 (2006).
101. Bayly, R. et al. Critical role for a single leucine residue in leukemia induction by E2A-PBX1. Mol. Cell. Biol. 26, 6442-6452 (2006).
102. Huggins, G. S. et al. Characterization of the mUBC9-binding sites required for E2A protein degradation. J. Biol. Chem. 274, 28690-28696 (1999).
103. Lasorella, A. et al. Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442, 471-474 (2006).