Mi-2/NuRD chromatin remodeling complexes regulate B and T-lymphocyte development and function

Immunological Reviews

Volumn 261, Issue 1, 2014, Pages 126-140

  Dege, Carissa ^a   Hagman, James ^a  

^a DEPARTMENT OF MEDICINE   (United States)

Author keywords

B cells; Gene regulation; Hematopoiesis; Lineage commitment specification; T cells; Transcription factors

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD4 ANTIGEN; CD8 ANTIGEN; HISTONE DEACETYLASE; IKAROS TRANSCRIPTION FACTOR; PROTEIN MI 2; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FATE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; DEACETYLATION; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GERMINAL CENTER; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOREGULATION; LEUKEMOGENESIS; LYMPHOPOIESIS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; T LYMPHOCYTE; ANIMAL; CELL LINEAGE; CELLULAR IMMUNITY; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; IMMUNOLOGY; LYMPHOCYTE SUBPOPULATION; METABOLISM;

ANIMALS; B-LYMPHOCYTES; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, CELLULAR; LYMPHOCYTE SUBSETS; LYMPHOPOIESIS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; T-LYMPHOCYTES;

EID: 84905990739     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12209     Document Type: Article

References (122)

1. Tong JK, Hassig CA, Schnitzler GR, Kingston RE, Schreiber SL. Chromatin deacetylation by an ATP-dependent nucleosome remodelling complex. Nature 1998;395:917-921.
2. 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;2:851-861.
3. 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;95:279-289.
4. Zhang Y, Ng HH, Erdjument-Bromage H, Tempst P, Bird A, Reinberg D. Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation. Genes Dev 1999;13:1924-1935.
5. 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;23:62-66.
6. Nair SS, Li DQ, Kumar R. A core chromatin remodeling factor instructs global chromatin signaling through multivalent reading of nucleosome codes. Mol Cell 2013;49:704-718.
7. Watson AA, et al. The PHD and chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4. J Mol Biol 2012;422:3-17.
8. Morra R, Lee BM, Shaw H, Tuma R, Mancini EJ. Concerted action of the PHD, chromo and motor domains regulates the human chromatin remodelling ATPase CHD4. FEBS Lett 2012;586:2513-2521.
9. Moshkin YM, et al. Remodelers organize cellular chromatin by counteracting intrinsic histone-DNA sequence preferences in a class-specific manner. Mol Cell Biol 2012;32:675-688.
10. Morey L, et al. MBD3, a component of the NuRD complex, facilitates chromatin alteration and deposition of epigenetic marks. Mol Cell Biol 2008;28:5912-5923.
11. Sims JK, Wade PA. Mi-2/NuRD complex function is required for normal S phase progression and assembly of pericentric heterochromatin. Mol Biol Cell 2011;22:3094-3102.
12. Kwintkiewicz J, Padilla-Banks E, Jefferson WN, Jacobs IM, Wade PA, Williams CJ. Metastasis-associated protein 3 (MTA3) regulates G2/M progression in proliferating mouse granulosa cells. Biol Reprod 2012;86:1-8.
13. Helbling Chadwick L, Chadwick BP, Jaye DL, Wade PA. The Mi-2/NuRD complex associates with pericentromeric heterochromatin during S phase in rapidly proliferating lymphoid cells. Chromosoma 2009;118:445-457.
14. Wang Y, et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 2009;138:660-672.
15. Kolla V, Zhuang T, Higashi M, Naraparaju K, Brodeur GM. Role of CHD5 in human cancers: 10 years later. Cancer Res 2014;74:652-658.
16. Heng TS, Painter MW. The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 2008;9:1091-1094.
17. Williams CJ, et al. The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development. Immunity 2004;20:719-733.
18. Musselman CA, et al. Binding of the CHD4 PHD2 finger to histone H3 is modulated by covalent modifications. Biochem J 2009;423:179-187.
19. Musselman CA, et al. Bivalent recognition of nucleosomes by the tandem PHD fingers of the CHD4 ATPase is required for CHD4-mediated repression. Proc Natl Acad Sci USA 2012;109:787-792.
20. Ramirez J, Dege C, Kutateladze TG, Hagman J. MBD2 and multiple domains of CHD4 are required for transcriptional repression by Mi-2/NuRD complexes. Mol Cell Biol 2012;32:5078-5088.
21. Jones DO, Cowell IG, Singh PB. Mammalian chromodomain proteins: their role in genome organisation and expression. BioEssays 2000;22:124-137.
22. Bouazoune K, et al. The dMi-2 chromodomains are DNA binding modules important for ATP-dependent nucleosome mobilization. EMBO J 2002;21:2430-2440.
23. Hauk G, McKnight JN, Nodelman IM, Bowman GD. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell 2010;39:711-723.
24. Yao YL, Yang WM. The metastasis-associated proteins 1 and 2 form distinct protein complexes with histone deacetylase activity. J Biol Chem 2003;278:42560-42568.
25. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS, Wade PA. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 2003;113:207-219.
26. Oliver AW, Jones SA, Roe SM, Matthews S, Goodwin GH, Pearl LH. Crystal structure of the proximal BAH domain of the polybromo protein. Biochem J 2005;389:657-664.
27. Humphrey GW, et al. Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1. J Biol Chem 2001;276:6817-6824.
28. Roche AE, Bassett BJ, Samant SA, Hong W, Blobel GA, Svensson EC. The zinc finger and C-terminal domains of MTA proteins are required for FOG-2-mediated transcriptional repression via the NuRD complex. J Mol Cell Cardiol 2008;44:352-360.
29. Fujita N, et al. MTA3 and the Mi-2/NuRD complex regulate cell fate during B lymphocyte differentiation. Cell 2004;119:75-86.
30. Jaye DL, et al. The BCL6-associated transcriptional co-repressor, MTA3, is selectively expressed by germinal centre B cells and lymphomas of putative germinal centre derivation. J Pathol 2007;213:106-115.
31. Cismasiu VB, Adamo K, Gecewicz J, Duque J, Lin Q, Avram D. BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene 2005;24:6753-6764.
32. Wu M, Wang L, Li Q, Li J, Qin J, Wong J. The MTA family proteins as novel histone H3 binding proteins. Cell Biosci 2013;3:1-14.
33. Toh Y, et al. Molecular analysis of a candidate metastasis-associated gene, MTA1: possible interaction with histone deacetylase 1. J Exp Clin Cancer Res 2000;19:105-111.
34. Saito M, Ishikawa F. The mCpG-binding domain of human MBD3 does not bind to mCpG but interacts with NuRD/Mi2 components HDAC1 and MTA2. J Biol Chem 2002;277:35434-35439.
35. Luo J, Su F, Chen D, Shiloh A, Gu W. Deacetylation of p53 modulates its effect on cell growth and apoptosis. Nature 2000;408:377-381.
36. Li X, Jia S, Wang S, Wang Y, Meng A. Mta3-NuRD complex is a master regulator for initiation of primitive hematopoiesis in vertebrate embryos. Blood 2009;114:5464-5472.
37. Hong W, et al. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J 2005;24:2367-2378.
38. Ross J, Mavoungou L, Bresnick EH, Milot E. GATA-1 utilizes Ikaros and polycomb repressive complex 2 to suppress Hes1 and to promote erythropoiesis. Mol Cell Biol 2012;32:3624-3638.
39. Singh RR, Barnes CJ, Talukder AH, Fuqua SA, Kumar R. Negative regulation of estrogen receptor alpha transactivation functions by LIM domain only 4 protein. Cancer Res 2005;65:10594-10601.
40. Fournier A, Sasai N, Nakao M, Defossez PA. The role of methyl-binding proteins in chromatin organization and epigenome maintenance. Brief Funct Genomics 2012;11:251-264.
41. Hendrich B, Bird A. Identification and characterization of a family of mammalian methyl-CpG binding proteins. Mol Cell Biol 1998;18:6538-6547.
42. Le Guezennec X, et al. MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 2006;26:843-851.
43. Tan CP, Nakielny S. Control of the DNA methylation system component MBD2 by protein arginine methylation. Mol Cell Biol 2006;26:7224-7235.
44. Yildirim O, et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 2011;147:1498-1510.
45. Hendrich B, Guy J, Ramsahoye B, Wilson VA, Bird A. Closely related proteins MBD2 and MBD3 play distinctive but interacting roles in mouse development. Genes Dev 2001;15:710-723.
46. Baubec T, Ivanek R, Lienert F, Schubeler D. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 2013;153:480-492.
47. Gnanapragasam MN, et al. p66Alpha-MBD2 coiled-coil interaction and recruitment of Mi-2 are critical for globin gene silencing by the MBD2-NuRD complex. Proc Natl Acad Sci USA 2011;108:7487-7492.
48. Brackertz M, Gong Z, Leers J, Renkawitz R. p66alpha and p66beta of the Mi-2/NuRD complex mediate MBD2 and histone interaction. Nucleic Acids Res 2006;34:397-406.
49. Brackertz M, Boeke J, Zhang R, Renkawitz R. Two highly related p66 proteins comprise a new family of potent transcriptional repressors interacting with MBD2 and MBD3. J Biol Chem 2002;277:40958-40966.
50. Kaji K, Caballero IM, MacLeod R, Nichols J, Wilson VA, Hendrich B. The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat Cell Biol 2006;8:285-292.
51. Kaji K, Nichols J, Hendrich B. Mbd3, a component of the NuRD co-repressor complex, is required for development of pluripotent cells. Development 2007;134:1123-1132.
52. Luo M, et al. NuRD blocks reprogramming of mouse somatic cells into pluripotent stem cells. Stem Cells 2013;31:1278-1286.
53. Shimbo T, et al. MBD3 localizes at promoters, gene bodies and enhancers of active genes. PLoS Genet 2013;9:e1004028.
54. Gunther K, et al. Differential roles for MBD2 and MBD3 at methylated CpG islands, active promoters and binding to exon sequences. Nucleic Acids Res 2013;41:3010-3021.
55. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 2002;16:2893-2905.
56. Verreault A, Kaufman PD, Kobayashi R, Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 1996;87:95-104.
57. Lejon S, et al. Insights into association of the NuRD complex with FOG-1 from the crystal structure of an RbAp48.FOG-1 complex. J Biol Chem 2011;286:1196-1203.
58. Migliori V, et al. Symmetric dimethylation of H3R2 is a newly identified histone mark that supports euchromatin maintenance. Nat Struct Mol Biol 2012;19:136-144.
59. Murzina NV, et al. Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 2008;16:1077-1085.
60. Feng Q, Cao R, Xia L, Erdjument-Bromage H, Tempst P, Zhang Y. Identification and functional characterization of the p66/p68 components of the MeCP1 complex. Mol Cell Biol 2002;22:536-546.
61. Marino S, Nusse R. Mutants in the mouse NuRD/Mi2 component P66alpha are embryonic lethal. PLoS ONE 2007;2:e519.
62. Allen HF, Wade PA, Kutateladze TG. The NuRD architecture. Cell Mol Life Sci 2013;70:3513-3524.
63. Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann NY Acad Sci 2003;983:84-100.
64. Lee MG, Wynder C, Cooch N, Shiekhattar R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 2005;437:432-435.
65. Metzger E, et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005;437:436-439.
66. Shi Y, et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004;119:941-953.
67. Li Q, et al. Binding of the JmjC demethylase JARID1B to LSD1/NuRD suppresses angiogenesis and metastasis in breast cancer cells by repressing chemokine CCL14. Cancer Res 2011;71:6899-6908.
68. Whyte WA, et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 2012;482:221-225.
69. Kim J, et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 1999;10:345-355.
70. Yoshida T, et al. The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev 2008;22:1174-1189.
71. O'Neill DW, et al. An ikaros-containing chromatin-remodeling complex in adult-type erythroid cells. Mol Cell Biol 2000;20:7572-7582.
72. Sridharan R, Smale ST. Predominant interaction of both Ikaros and Helios with the NuRD complex in immature thymocytes. J Biol Chem 2007;282:30227-30238.
73. Rodriguez P, et al. GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J 2005;24:2354-2366.
74. Koipally J, Renold A, Kim J, Georgopoulos K. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J 1999;18:3090-3100.
75. Nichogiannopoulou A, Trevisan M, Neben S, Friedrich C, Georgopoulos K. Defects in hemopoietic stem cell activity in Ikaros mutant mice. J Exp Med 1999;190:1201-1214.
76. Yoshida T, Ng SY, Zuniga-Pflucker JC, Georgopoulos K. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol 2006;7:382-391.
77. Hardy RR, Kincade PW, Dorshkind K. The protean nature of cells in the B lymphocyte lineage. Immunity 2007;26:703-714.
78. Maier H, et al. Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat Immunol 2004;5:1069-1077.
79. Maier H, Colbert J, Fitzsimmons D, Clark DR, Hagman J. Activation of the early B-cell-specific mb-1 (Ig-alpha) gene by Pax-5 is dependent on an unmethylated Ets binding site. Mol Cell Biol 2003;23:1946-1960.
80. Gao H, Lukin K, Ramirez J, Fields S, Lopez D, Hagman J. Opposing effects of SWI/SNF and Mi-2/NuRD chromatin remodeling complexes on epigenetic reprogramming by EBF and Pax5. Proc Natl Acad Sci USA 2009;106:11258-11263.
81. Georgopoulos K, et al. The Ikaros gene is required for the development of all lymphoid lineages. Cell 1994;79:143-156.
82. Georgopoulos K, Moore DD, Derfler B. Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science 1992;258:808-812.
83. 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;14:7111-7123.
84. John LB, Ward AC. The Ikaros gene family: transcriptional regulators of hematopoiesis and immunity. Mol Immunol 2011;48:1272-1278.
85. Sun L, Liu A, Georgopoulos K. Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J 1996;15:5358-5369.
86. Wang JH, et al. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 1996;5:537-549.
87. Schwickert TA, et al. Stage-specific control of early B cell development by the transcription factor Ikaros. Nat Immunol 2014;15:283-293.
88. Zhang J, et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat Immunol 2012;13:86-94.
89. Koipally J, Georgopoulos K. Ikaros-CtIP interactions do not require C-terminal binding protein and participate in a deacetylase-independent mode of repression. J Biol Chem 2002;277:23143-23149.
90. Bereshchenko OR, Gu W, Dalla-Favera R. Acetylation inactivates the transcriptional repressor BCL6. Nat Genet 2002;32:606-613.
91. Shaffer AL, et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 2002;17:51-62.
92. Shapiro-Shelef M, Lin KI, McHeyzer-Williams LJ, Liao J, McHeyzer-Williams MG, Calame K. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 2003;19:607-620.
93. Shapiro-Shelef M, Calame K. Regulation of plasma-cell development. Nat Rev Immunol 2005;5:230-242.
94. Ancelin K, et al. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 2006;8:623-630.
95. Gyory I, Wu J, Fejer G, Seto E, Wright KL. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol 2004;5:299-308.
96. Yu J, Angelin-Duclos C, Greenwood J, Liao J, Calame K. Transcriptional repression by blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol Cell Biol 2000;20:2592-2603.
97. Su ST, Ying HY, Chiu YK, Lin FR, Chen MY, Lin KI. Involvement of histone demethylase LSD1 in Blimp-1-mediated gene repression during plasma cell differentiation. Mol Cell Biol 2009;29:1421-1431.
98. Germain RN. T-cell development and the CD4-CD8 lineage decision. Nat Rev Immunol 2002;2:309-322.
99. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008;8:523-532.
100. Brown KE, Guest SS, Smale ST, Hahm K, Merkenschlager M, Fisher AG. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997;91:845-854.
101. Avitahl N, Winandy S, Friedrich C, Jones B, Ge Y, Georgopoulos K. Ikaros sets thresholds for T cell activation and regulates chromosome propagation. Immunity 1999;10:333-343.
102. Koipally J, Georgopoulos K. Ikaros interactions with CtBP reveal a repression mechanism that is independent of histone deacetylase activity. J Biol Chem 2000;275:19594-19602.
103. 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;27:723-734.
104. Harker N, et al. Pre-TCR signaling and CD8 gene bivalent chromatin resolution during thymocyte development. J Immunol 2011;186:6368-6377.
105. Harker N, et al. The CD8alpha gene locus is regulated by the Ikaros family of proteins. Mol Cell 2002;10:1403-1415.
106. Collins B, et al. Ikaros promotes rearrangement of TCR alpha genes in an Ikaros null thymoma cell line. Eur J Immunol 2013;43:521-532.
107. Kathrein KL, Lorenz R, Innes AM, Griffiths E, Winandy S. Ikaros induces quiescence and T-cell differentiation in a leukemia cell line. Mol Cell Biol 2005;25:1645-1654.
108. Hosokawa H, et al. Functionally distinct Gata3/Chd4 complexes coordinately establish T helper 2 (Th2) cell identity. Proc Natl Acad Sci USA 2013;110:4691-4696.
109. Hutchins AS, Artis D, Hendrich BD, Bird AP, Scott P, Reiner SL. Cutting edge: a critical role for gene silencing in preventing excessive type 1 immunity. J Immunol 2005;175:5606-5610.
110. Hutchins AS, et al. Gene silencing quantitatively controls the function of a developmental trans-activator. Mol Cell 2002;10:81-91.
111. Lu X, et al. Inactivation of NuRD component Mta2 causes abnormal T cell activation and lupus-like autoimmune disease in mice. J Biol Chem 2008;283:13825-13833.
112. Lal G, et al. Epigenetic regulation of Foxp3 expression in regulatory T cells by DNA methylation. J Immunol 2009;182:259-273.
113. Lal G, Bromberg JS. Epigenetic mechanisms of regulation of Foxp3 expression. Blood 2009;114:3727-3735.
114. Wang L, et al. Mbd2 promotes foxp3 demethylation and T-regulatory-cell function. Mol Cell Biol 2013;33:4106-4115.
115. Kersh EN. Impaired memory CD8 T cell development in the absence of methyl-CpG-binding domain protein 2. J Immunol 2006;177:3821-3826.
116. Rothenberg EV. Transcriptional drivers of the T-cell lineage program. Curr Opin Immunol 2012;24:132-138.
117. Wakabayashi Y, et al. Bcl11b is required for differentiation and survival of αβ T lymphocytes. Nat Immunol 2003;4:533-539.
118. Albu DI, et al. BCL11B is required for positive selection and survival of double-positive thymocytes. J Exp Med 2007;204:3003-3015.
119. Ikawa T, et al. An essential developmental checkpoint for production of the T cell lineage. Science 2010;329:93-96.
120. Cismasiu VB, et al. BCL11B enhances TCR/CD28-triggered NF-kappaB activation through up-regulation of Cot kinase gene expression in T-lymphocytes. Biochem J 2009;417:457-466.
121. Cismasiu VB, et al. BCL11B participates in the activation of IL2 gene expression in CD4+ T lymphocytes. Blood 2006;108:2695-2702.
122. Cismasiu VB, Paskaleva E, Suman Daya S, Canki M, Duus K, Avram D. BCL11B is a general transcriptional repressor of the HIV-1 long terminal repeat in T lymphocytes through recruitment of the NuRD complex. Virology 2008;380:173-181.