Activation of 12/23-RSS-Dependent RAG Cleavage by hSWI/SNF Complex in the Absence of Transcription

Molecular Cell

Volumn 31, Issue 5, 2008, Pages 641-649

  Du, Hansen ^a   Ishii, Haruhiko ^b   Pazin, Michael J ^a   Sen, Ranjan ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NONE

Author keywords

DNA

Indexed keywords

CHOLECYSTOKININ OCTAPEPTIDE[28,31 N METHYLNORLEUCINE]; HISTONE; PROTEIN SWI; RAG1 PROTEIN; RAG2 PROTEIN; RNA POLYMERASE II; SIGNAL PEPTIDE;

ARTICLE; CHROMATIN STRUCTURE; GENETIC TRANSCRIPTION; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE;

ANIMALS; BASE SEQUENCE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; GENE REARRANGEMENT; HOMEODOMAIN PROTEINS; NUCLEAR PROTEINS; NUCLEOSOMES; PLASMIDS; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 50249154114     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2008.08.012     Document Type: Article

References (65)

1. Abarrategui I., and Krangel M.S. Regulation of T cell receptor-alpha gene recombination by transcription. Nat. Immunol. 7 (2006) 1109-1115
2. Akamatsu Y., Monroe R., Dudley D.D., Elkin S.K., Gartner F., Talukder S.R., Takahama Y., Alt F.W., Bassing C.H., and Oettinger M.A. Deletion of the RAG2 C terminus leads to impaired lymphoid development in mice. Proc. Natl. Acad. Sci. USA 100 (2003) 1209-1214
3. Angelin-Duclos C., and Calame K. Evidence that immunoglobulin VH-DJ recombination does not require germ line transcription of the recombining variable gene segment. Mol. Cell. Biol. 18 (1998) 6253-6264
4. Bassing C.H., Swat W., and Alt F.W. The mechanism and regulation of chromosomal V(D)J recombination. Cell 109 Suppl (2002) S45-S55
5. Baumann M., Mamais A., McBlane F., Xiao H., and Boyes J. Regulation of V(D)J recombination by nucleosome positioning at recombination signal sequences. EMBO J. 22 (2003) 5197-5207
6. Bouvier G., Watrin F., Naspetti M., Verthuy C., Naquet P., and Ferrier P. Deletion of the mouse T-cell receptor beta gene enhancer blocks alphabeta T-cell development. Proc. Natl. Acad. Sci. USA 93 (1996) 7877-7881
7. Capone M., Watrin F., Fernex C., Horvat B., Krippl B., Wu L., Scollay R., and Ferrier P. TCR beta and TCR alpha gene enhancers confer tissue- and stage-specificity on V(D)J recombination events. EMBO J. 12 (1993) 4335-4346
8. Chi T., Lieberman P., Ellwood K., and Carey M. A general mechanism for transcriptional synergy by eukaryotic activators. Nature 377 (1995) 254-257
9. Cobb R.M., Oestreich K.J., Osipovich O.A., and Oltz E.M. Accessibility control of V(D)J recombination. Adv. Immunol. 91 (2006) 45-109
10. Curry J.D., Geier J.K., and Schlissel M.S. Single-strand recombination signal sequence nicks in vivo: evidence for a capture model of synapsis. Nat. Immunol. 6 (2005) 1272-1279
11. Dudley D.D., Sekiguchi J., Zhu C., Sadofsky M.J., Whitlow S., DeVido J., Monroe R.J., Bassing C.H., and Alt F.W. Impaired V(D)J recombination and lymphocyte development in core RAG1-expressing mice. J. Exp. Med. 198 (2003) 1439-1450
12. Dudley D.D., Chaudhuri J., Bassing C.H., and Alt F.W. Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv. Immunol. 86 (2005) 43-112
13. Eastman Q.M., Villey I.J., and Schatz D.G. Detection of RAG protein-V(D)J recombination signal interactions near the site of DNA cleavage by UV cross-linking. Mol. Cell. Biol. 19 (1999) 3788-3797
14. Elkin S.K., Ivanov D., Ewalt M., Ferguson C.G., Hyberts S.G., Sun Z.Y., Prestwich G.D., Yuan J., Wagner G., Oettinger M.A., and Gozani O.P. A PHD finger motif in the C terminus of RAG2 modulates recombination activity. J. Biol. Chem. 280 (2005) 28701-28710
15. Fernex C., Capone M., and Ferrier P. The V(D)J recombinational and transcriptional activities of the immunoglobulin heavy-chain intronic enhancer can be mediated through distinct protein-binding sites in a transgenic substrate. Mol. Cell. Biol. 15 (1995) 3217-3226
16. Fyodorov D.V., and Kadonaga J.T. Chromatin assembly in vitro with purified recombinant ACF and NAP-1. Methods Enzymol. 371 (2003) 499-515
17. Golding A., Chandler S., Ballestar E., Wolffe A.P., and Schlissel M.S. Nucleosome structure completely inhibits in vitro cleavage by the V(D)J recombinase. EMBO J. 18 (1999) 3712-3723
18. Gutierrez J.L., Chandy M., Carrozza M.J., and Workman J.L. Activation domains drive nucleosome eviction by SWI/SNF. EMBO J. 26 (2007) 730-740
19. Hsieh C.L., and Lieber M.R. CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. EMBO J. 11 (1992) 315-325
20. Hsieh C.L., McCloskey R.P., and Lieber M.R. V(D)J recombination on minichromosomes is not affected by transcription. J. Biol. Chem. 267 (1992) 15613-15619
21. Ishii H., Sen R., and Pazin M.J. Combinatorial control of DNase I-hypersensitive site formation and erasure by immunoglobulin heavy chain enhancer-binding proteins. J. Biol. Chem. 279 (2004) 7331-7338
22. Johnson K., Pflugh D.L., Yu D., Hesslein D.G., Lin K.I., Bothwell A.L., Thomas-Tikhonenko A., Schatz D.G., and Calame K. B cell-specific loss of histone 3 lysine 9 methylation in the V(H) locus depends on Pax5. Nat. Immunol. 5 (2004) 853-861
23. Jones J.M., and Gellert M. Ordered assembly of the V(D)J synaptic complex ensures accurate recombination. EMBO J. 21 (2002) 4162-4171
24. Kamakaka R.T., Bulger M., and Kadonaga J.T. Potentiation of RNA polymerase II transcription by Gal4-VP16 during but not after DNA replication and chromatin assembly. Genes Dev. 7 (1993) 1779-1795
25. Kassabov S.R., Zhang B., Persinger J., and Bartholomew B. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol. Cell 11 (2003) 391-403
26. Krangel M.S. Gene segment selection in V(D)J recombination: accessibility and beyond. Nat. Immunol. 4 (2003) 624-630
27. Kwon H., Imbalzano A.N., Khavari P.A., Kingston R.E., and Green M.R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370 (1994) 477-481
28. Kwon J., Imbalzano A.N., Matthews A., and Oettinger M.A. Accessibility of nucleosomal DNA to V(D)J cleavage is modulated by RSS positioning and HMG1. Mol. Cell 2 (1998) 829-839
29. Kwon J., Morshead K.B., Guyon J.R., Kingston R.E., and Oettinger M.A. Histone acetylation and hSWI/SNF remodeling act in concert to stimulate V(D)J cleavage of nucleosomal DNA. Mol. Cell 6 (2000) 1037-1048
30. Lauzurica P., and Krangel M.S. Temporal and lineage-specific control of T cell receptor alpha/delta gene rearrangement by T cell receptor alpha and delta enhancers. J. Exp. Med. 179 (1994) 1913-1921
31. Liang H.E., Hsu L.Y., Cado D., Cowell L.G., Kelsoe G., and Schlissel M.S. The "dispensable" portion of RAG2 is necessary for efficient V-to-DJ rearrangement during B and T cell development. Immunity 17 (2002) 639-651
32. Liu Y., Subrahmanyam R., Chakraborty T., Sen R., and Desiderio S. A plant homeodomain in RAG-2 that binds Hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement. Immunity 27 (2007) 561-571
33. Luger K., Rechsteiner T.J., Flaus A.J., Waye M.M., and Richmond T.J. Characterization of nucleosome core particles containing histone proteins made in bacteria. J. Mol. Biol. 272 (1997) 301-311
34. Marmorstein R., and Roth S.Y. Histone acetyltransferases: function, structure, and catalysis. Curr. Opin. Genet. Dev. 11 (2001) 155-161
35. Martens J.A., and Winston F. Recent advances in understanding chromatin remodeling by Swi/Snf complexes. Curr. Opin. Genet. Dev. 13 (2003) 136-142
36. Matthews A.G., Kuo A.J., Ramon-Maiques S., Han S., Champagne K.S., Ivanov D., Gallardo M., Carney D., Cheung P., Ciccone D.N., et al. RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature 450 (2007) 1106-1110
37. McBlane F., and Boyes J. Stimulation of V(D)J recombination by histone acetylation. Curr. Biol. 10 (2000) 483-486
38. Mohrmann L., and Verrijzer C.P. Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes. Biochim. Biophys. Acta 1681 (2005) 59-73
39. Morshead K.B., Ciccone D.N., Taverna S.D., Allis C.D., and Oettinger M.A. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl. Acad. Sci. USA 100 (2003) 11577-11582
40. Neely K.E., Hassan A.H., Wallberg A.E., Steger D.J., Cairns B.R., Wright A.P., and Workman J.L. Activation domain-mediated targeting of the SWI/SNF complex to promoters stimulates transcription from nucleosome arrays. Mol. Cell 4 (1999) 649-655
41. Nightingale K.P., Baumann M., Eberharter A., Mamais A., Becker P.B., and Boyes J. Acetylation increases access of remodelling complexes to their nucleosome targets to enhance initiation of V(D)J recombination. Nucleic Acids Res. 35 (2007) 6311-6321
42. Okada A., Mendelsohn M., and Alt F. Differential activation of transcription versus recombination of transgenic T cell receptor beta variable region gene segments in B and T lineage cells. J. Exp. Med. 180 (1994) 261-272
43. Osipovich O., Milley R., Meade A., Tachibana M., Shinkai Y., Krangel M.S., and Oltz E.M. Targeted inhibition of V(D)J recombination by a histone methyltransferase. Nat. Immunol. 5 (2004) 309-316
44. Osipovich O., Milley Cobb R., Oestreich K.J., Pierce S., Ferrier P., and Oltz E.M. Essential function for SWI-SNF chromatin-remodeling complexes in the promoter-directed assembly of Tcrb genes. Nat. Immunol. 8 (2007) 809-816
45. Patenge N., Elkin S.K., and Oettinger M.A. ATP-dependent remodeling by SWI/SNF and ISWI proteins stimulates V(D)J cleavage of 5 S arrays. J. Biol. Chem. 279 (2004) 35360-35367
46. Reece R.J., Rickles R.J., and Ptashne M. Overproduction and single-step purification of GAL4 fusion proteins from Escherichia coli. Gene 126 (1993) 105-107
47. Roberts S.G., and Green M.R. Activator-induced conformational change in general transcription factor TFIIB. Nature 371 (1994) 717-720
48. Rodgers K.K., Villey I.J., Ptaszek L., Corbett E., Schatz D.G., and Coleman J.E. A dimer of the lymphoid protein RAG1 recognizes the recombination signal sequence and the complex stably incorporates the high mobility group protein HMG2. Nucleic Acids Res. 27 (1999) 2938-2946
49. Roth D.B. Restraining the V(D)J recombinase. Nat. Rev. Immunol. 3 (2003) 656-666
50. Sadofsky M.J. Recombination-activating gene proteins: more regulation, please. Immunol. Rev. 200 (2004) 83-89
51. Schatz D.G. V(D)J recombination. Immunol. Rev. 200 (2004) 5-11
52. Schnitzler G., Sif S., and Kingston R.E. Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell 94 (1998) 17-27
53. Sen R., and Oltz E. Genetic and epigenetic regulation of IgH gene assembly. Curr. Opin. Immunol. 18 (2006) 237-242
54. Sif S., Stukenberg P.T., Kirschner M.W., and Kingston R.E. Mitotic inactivation of a human SWI/SNF chromatin remodeling complex. Genes Dev. 12 (1998) 2842-2851
55. Sikes M.L., Suarez C.C., and Oltz E.M. Regulation of V(D)J recombination by transcriptional promoters. Mol. Cell. Biol. 19 (1999) 2773-2781
56. Sikes M.L., Meade A., Tripathi R., Krangel M.S., and Oltz E.M. Regulation of V(D)J recombination: a dominant role for promoter positioning in gene segment accessibility. Proc. Natl. Acad. Sci. USA 99 (2002) 12309-12314
57. Sleckman B.P., Bardon C.G., Ferrini R., Davidson L., and Alt F.W. Function of the TCR alpha enhancer in alphabeta and gammadelta T cells. Immunity 7 (1997) 505-515
58. Spanopoulou E., Zaitseva F., Wang F.H., Santagata S., Baltimore D., and Panayotou G. The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 87 (1996) 263-276
59. Vignali M., Steger D.J., Neely K.E., and Workman J.L. Distribution of acetylated histones resulting from Gal4-VP16 recruitment of SAGA and NuA4 complexes. EMBO J. 19 (2000) 2629-2640
60. Villey I., Caillol D., Selz F., Ferrier P., and de Villartay J.P. Defect in rearrangement of the most 5′ TCR-J alpha following targeted deletion of T early alpha (TEA): implications for TCR alpha locus accessibility. Immunity 5 (1996) 331-342
61. West K.L., Singha N.C., De Ioannes P., Lacomis L., Erdjument-Bromage H., Tempst P., and Cortes P. A direct interaction between the RAG2 C terminus and the core histones is required for efficient V(D)J recombination. Immunity 23 (2005) 203-212
62. Whitehurst C.E., Schlissel M.S., and Chen J. Deletion of germline promoter PD beta 1 from the TCR beta locus causes hypermethylation that impairs D beta 1 recombination by multiple mechanisms. Immunity 13 (2000) 703-714
63. Xue Y., Canman J.C., Lee C.S., Nie Z., Yang D., Moreno G.T., Young M.K., Salmon E.D., and Wang W. The human SWI/SNF-B chromatin-remodeling complex is related to yeast rsc and localizes at kinetochores of mitotic chromosomes. Proc. Natl. Acad. Sci. USA 97 (2000) 13015-13020
64. Yancopoulos G.D., and Alt F.W. Developmentally controlled and tissue-specific expression of unrearranged VH gene segments. Cell 40 (1985) 271-281
65. Yancopoulos G.D., Blackwell T.K., Suh H., Hood L., and Alt F.W. Introduced T cell receptor variable region gene segments recombine in pre-B cells: evidence that B and T cells use a common recombinase. Cell 44 (1986) 251-259