Chromatin remodeling complex NURF regulates thymocyte maturation

Genes and Development

Volumn 25, Issue 3, 2011, Pages 275-286

  Landry, Joseph W ^a,b   Banerjee, Subhadra ^a   Taylor, Barbara ^a   Aplan, Peter D ^a   Singer, Alfred ^a   Wu, Carl ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AP 1; Bptf; Chromatin remodeling; NURF; Positive selection; SRF

Indexed keywords

NUCLEOSOME REMODELING FACTOR; PROTEIN DERIVATIVE; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR EGR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MATURATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA BINDING; GENE CONTROL; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; THYMOCYTE;

ANIMALS; ANTIGENS, NUCLEAR; CELL DIFFERENTIATION; CHROMATIN; DNA; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; NERVE TISSUE PROTEINS; PROTEIN BINDING; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 79551611723     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.2007311     Document Type: Article

References (61)

1. Aicher WK, Sakamoto KM, Hack A, Eibel H. 1999. Analysis of functional elements in the human Egr-1 gene promoter. Rheumatol Int 18: 207-214.
2. Allen PM. 2009. Themis imposes new law and order on positive selection. Nat Immunol 10: 805-806.
3. Andersen EC, Lu X, Horvitz HR. 2006. C. elegans ISWI and NURF301 antagonize an Rb-like pathway in the determination of multiple cell fates. Development 133: 2695-2704.
4. Attema JL, Reeves R, Murray V, Levichkin I, Temple MD, Tremethick DJ, Shannon MF. 2002. The human IL-2 gene promoter can assemble a positioned nucleosome that becomes remodeled upon T cell activation. J Immunol 169: 2466-2476.
5. Badenhorst P, Xiao H, Cherbas L, Kwon SY, Voas M, Rebay I, Cherbas P, Wu C. 2005. The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev 19: 2540-2545.
6. Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, Shiekhattar R. 2003. Isolation of human NURF: A regulator of Engrailed gene expression. EMBO J 22: 6089-6100.
7. Bettini M, Xi H, Milbrandt J, Kersh GJ. 2002. Thymocyte development in early growth response gene 1-deficient mice. J Immunol 169: 1713-1720.
8. + thymocytes initially terminate CD8 transcription even when differentiating into CD8+ T cells. Immunity 13: 59-71.
9. Chen D, Rothenberg EV. 1993. Molecular basis for developmental changes in interleukin-2 gene inducibility. Mol Cell Biol 13: 228-237.
10. Chi TH, Wan M, Zhao K, Taniuchi I, Chen L, Littman DR, Crabtree GR. 2002. Reciprocal regulation of CD4/CD8 expression by SWI/SNF-like BAF complexes. Nature 418: 195-199.
11. Chi TH, Wan M, Lee PP, Akashi K, Metzger D, Chambon P, Wilson CB, Crabtree GR. 2003. Sequential roles of Brg, the ATPase subunit of BAF chromatin remodeling complexes, in thymocyte development. Immunity 19: 169-182.
12. Choudhary P, Varga-Weisz P. 2007. ATP-dependent chromatin remodelling: Action and reaction. Subcell Biochem 41: 29-43.
13. Clapier CR, Cairns BR. 2009. The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
14. Costello PS, Nicolas RH, Watanabe Y, Rosewell I, Treisman R. 2004. Ternary complex factor SAP-1 is required for Erkmediated thymocyte positive selection. Nat Immunol 5: 289-298.
15. Costello P, Nicolas R, Willoughby J, Wasylyk B, Nordheim A, Treisman R. 2010. Ternary complex factors SAP-1 and Elk-1, but not net, are functionally equivalent in thymocyte development. J Immunol 185: 1082-1092.
16. Croom HA, Izon DJ, Chong MM, Curtis DJ, Roberts AW, Kay TW, Hilton DJ, Alexander WS, Starr R. 2008. Perturbed thymopoiesis in vitro in the absence of suppressor of cytokine signalling 1 and 3. Mol Immunol 45: 2888-2896.
17. DeFranco C, Damon DH, Endoh M, Wagner JA. 1993. Nerve growth factor induces transcription of NGFIA through complex regulatory elements that are also sensitive to serum and phorbol 12-myristate 13-acetate. Mol Endocrinol 7: 365-379.
18. Dorschner MO, Hawrylycz M, Humbert R, Wallace JC, Shafer A, Kawamoto J, Mack J, Hall R, Goldy J, Sabo PJ, et al. 2004. High-throughput localization of functional elements by quantitative chromatin profiling. Nat Methods 1: 219-225.
19. Engel I, Murre C. 2001. The function of E- and Id proteins in lymphocyte development. Nat Rev Immunol 1: 193-199.
20. Fazzio TG, Tsukiyama T. 2003. Chromatin remodeling in vivo: Evidence for a nucleosome sliding mechanism. Mol Cell 12: 1333-1340.
21. Fleige A, Alberti S, Grobe L, Frischmann U, Geffers R, Muller W, Nordheim A, Schippers A. 2007. Serum response factor contributes selectively to lymphocyte development. J Biol Chem 282: 24320-24328.
22. Gebuhr TC, Kovalev GI, Bultman S, Godfrey V, Su L, Magnuson T. 2003. The role of Brg1, a catalytic subunit of mammalian chromatin-remodeling complexes, in T cell development. J Exp Med 198: 1937-1949. (Pubitemid 38032125)
23. Goldberg AD, Allis CD, Bernstein E. 2007. Epigenetics: A landscape takes shape. Cell 128: 635-638.
24. Goller T, Vauti F, Ramasamy S, Arnold HH. 2008. Transcriptional regulator BPTF/FAC1 is essential for trophoblast differentiation during early mouse development. Mol Cell Biol 28: 6819-6827.
25. Gross DS, Garrard WT. 1988. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem 57: 159-197.
26. Hamiche A, Sandaltzopoulos R, Gdula DA, Wu C. 1999. ATP-dependent histone octamer sliding mediated by the chromatin remodeling complex NURF. Cell 97: 833-842. (Pubitemid 29375043)
27. Hennet T, Hagen FK, Tabak LA, Marth JD. 1995. T-cell-specific deletion of a polypeptide N-acetylgalactosaminyl-transferase gene by site-directed recombination. Proc Natl Acad Sci 92: 12070-12074.
28. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463: 474-484.
29. Huang YH, Li D, Winoto A, Robey EA. 2004. Distinct transcriptional programs in thymocytes responding to T cell receptor, Notch, and positive selection signals. Proc Natl Acad Sci 101: 4936-4941. (Pubitemid 38469181)
30. Jani A, Wan M, Zhang J, Cui K, Wu J, Preston-Hurlburt P, Khatri R, Zhao K, Chi T. 2008. A novel genetic strategy reveals unexpected roles of the Swi-Snf-like chromatin-remodeling BAF complex in thymocyte development. J Exp Med 205: 2813-2825.
31. Kang JG, Hamiche A, Wu C. 2002. GAL4 directs nucleosome sliding induced by NURF. EMBO J 21: 1406-1413.
32. Kwon SY, Xiao H, Glover BP, Tjian R, Wu C, Badenhorst P. 2008. The nucleosome remodeling factor (NURF) regulates genes involved in Drosophila innate immunity. Dev Biol 316: 538-547.
33. Landry J, Sharov AA, Piao Y, Sharova LV, Xiao H, Southon E, Matta J, Tessarollo L, Zhang YE, Ko MS, et al. 2008. Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet 4: e1000241. doi: 10.1371/journal.pgen.1000241.
34. Lawson VJ, Weston K, Maurice D. 2010. Early growth response 2 regulates the survival of thymocytes during positive selection. Eur J Immunol 40: 232-241.
35. Lesourne R, Uehara S, Lee J, Song KD, Li L, Pinkhasov J, Zhang Y, Weng NP, Wildt KF, Wang L, et al. 2009. Themis, a T cellspecific protein important for late thymocyte development. Nat Immunol 10: 840-847.
36. Li H, Ilin S, Wang W, Duncan EM, Wysocka J, Allis CD, Patel DJ. 2006. Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442: 91-95.
37. Merkenschlager M, Wilson CB. 2008. RNAi and chromatin in T cell development and function. Curr Opin Immunol 20: 131-138.
38. Mick VE, Starr TK, McCaughtry TM, McNeil LK, Hogquist KA. 2004. The regulated expression of a diverse set of genes during thymocyte positive selection in vivo. J Immunol 173: 5434-5444.
39. + distinguished in the early growth response (Egr)-1 transgenic mice with a recombinase- activating gene-deficient background. J Exp Med 186: 877-885.
40. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68: 869-877.
41. Park JH, Adoro S, Lucas PJ, Sarafova SD, Alag AS, Doan LL, Erman B, Liu X, Ellmeier W, Bosselut R, et al. 2007. 'Coreceptor tuning': Cytokine signals transcriptionally tailor CD8 coreceptor expression to the self-specificity of the TCR. Nat Immunol 8: 1049-1059.
42. Park JH, Adoro S, Guinter T, Erman B, Alag AS, Catalfamo M, Kimura MY, Cui Y, Lucas PJ, Gress RE, et al. 2010. Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat Immunol 11: 257-264.
43. Rando OJ, Chang HY. 2009. Genome-wide views of chromatin structure. Annu Rev Biochem 78: 245-271.
44. Reya T, Bassiri H, Biancaniello R, Carding SR. 1998. Thymic stromal-cell abnormalities and dysregulated T-cell development in IL-2-deficient mice. Dev Immunol 5: 287-302. (Pubitemid 29145960)
45. Rothenberg EV, Taghon T. 2005. Molecular genetics of T cell development. Annu Rev Immunol 23: 601-649.
46. Shao H, Kono DH, Chen LY, Rubin EM, Kaye J. 1997. Induction of the early growth response (Egr) family of transcription factors during thymic selection. J Exp Med 185: 731-744.
47. Siebenlist U, Durand DB, Bressler P, Holbrook NJ, Norris CA, Kamoun M, Kant JA, Crabtree GR. 1986. Promoter region of interleukin-2 gene undergoes chromatin structure changes and confers inducibility on chloramphenicol acetyltransferase gene during activation of T cells. Mol Cell Biol 6: 3042-3049.
48. Song H, Spichiger-Haeusermann C, Basler K. 2009. The ISWI-containing NURF complex regulates the output of the canonical Wingless pathway. EMBO Rep 10: 1140-1146.
49. Starr TK, Jameson SC, Hogquist KA. 2003. Positive and negative selection of T cells. Annu Rev Immunol 21: 139-176.
50. Taghon T, Yui MA, Pant R, Diamond RA, Rothenberg EV. 2006. Developmental and molecular characterization of emerging b- and gd-selected pre-T cells in the adult mouse thymus. Immunity 24: 53-64.
51. Tsukiyama T, Wu C. 1995. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83: 1011-1020.
52. Tur G, Georgieva EI, Gagete A, Lopez-Rodas G, Rodriguez JL, Franco L. 2010. Factor binding and chromatin modification in the promoter of murine Egr1 gene upon induction. Cell Mol Life Sci 67: 4065-4077.
53. Ueno T, Saito F, Gray DH, Kuse S, Hieshima K, Nakano H, Kakiuchi T, Lipp M, Boyd RL, Takahama Y. 2004. CCR7 signals are essential for cortex-medulla migration of developing thymocytes. J Exp Med 200: 493-505.
54. Wan M, Zhang J, Lai D, Jani A, Prestone-Hurlburt P, Zhao L, Ramachandran A, Schnitzler GR, Chi T. 2009. Molecular basis of CD4 repression by the Swi/Snf-like BAF chromatin remodeling complex. Eur J Immunol 39: 580-588.
55. Wang L, Xiong Y, Bosselut R. 2010. Tenuous paths in unexplored territory: From T cell receptor signaling to effector gene expression during thymocyte selection. Semin Immunol 22: 294-302.
56. Ward SB, Hernandez-Hoyos G, Chen F, Waterman M, Reeves R, Rothenberg EV. 1998. Chromatin remodeling of the interleukin- 2 gene: Distinct alterations in the proximal versus distal enhancer regions. Nucleic Acids Res 26: 2923-2934.
57. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T. 2007. Chromatin remodelling at promoters suppresses antisense transcription. Nature 450: 1031-1035.
58. Williams CJ, Naito T, Arco PG, Seavitt JR, Cashman SM, De Souza B, Qi X, Keables P, Von Andrian UH, Georgopoulos K. 2004. The chromatin remodeler Mi-2b is required for CD4 expression and T cell development. Immunity 20: 719-733.
59. Xi H, Kersh GJ. 2003. Induction of the early growth response gene 1 promoter by TCR agonists and partial agonists: Ligand potency is related to sustained phosphorylation of extracellular signal-related kinase substrates. J Immunol 170: 315-324.
60. Xiao H, Sandaltzopoulos R, Wang HM, Hamiche A, Ranallo R, Lee KM, Fu D, Wu C. 2001. Dual functions of largest NURF subunit NURF301 in nucleosome sliding and transcription factor interactions. Mol Cell 8: 531-543.
61. Yui MA, Hernandez-Hoyos G, Rothenberg EV. 2001. A new regulatory region of the IL-2 locus that confers position-independent transgene expression. J Immunol 166: 1730-1739.