Cooperative recruitment of HMGB1 during V(D)J recombination through interactions with RAG1 and DNA

Nucleic Acids Research

Volumn 41, Issue 5, 2013, Pages 3289-3301

  Little, Alicia J ^a   Corbett, Elizabeth ^a,b   Ortega, Fabian ^a   Schatz, David G ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; HIGH MOBILITY GROUP B PROTEIN; HIGH MOBILITY GROUP B2 PROTEIN; OLIGONUCLEOTIDE; RAG1 PROTEIN; RAG2 PROTEIN;

ANISOTROPY; ARTICLE; BINDING AFFINITY; DNA BINDING; DNA RECOMBINATION; DNA SEQUENCE; GENE; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; RAG1 GENE; RAG2 GENE; VDJ RECOMBINATION;

AMINO ACID SUBSTITUTION; ANIMALS; CHROMATOGRAPHY, GEL; DNA; HEK293 CELLS; HMGB1 PROTEIN; HOMEODOMAIN PROTEINS; HUMANS; MICE; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; V(D)J RECOMBINATION;

EID: 84876381777     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1461     Document Type: Article

References (73)

1. Oettinger, M.A., Schatz, D.G., Gorka, C. and Baltimore, D. (1990) RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science, 248, 1517-1523.
2. Schatz, D.G., Oettinger, M.A. and Baltimore, D. (1989) The V(D)J recombination activating gene, RAG-1. Cell, 59, 1035-1048.
3. van Gent, D.C., Hiom, K., Paull, T.T. and Gellert, M. (1997) Stimulation of V(D)J cleavage by high mobility group proteins. EMBO J., 16, 2665-2670.
4. Schatz, D.G. and Swanson, P.C. (2011) V(D)J recombination: mechanisms of initiation. Annu. Rev. Genet., 45, 167-202.
5. McBlane, J.F., van Gent, D.C., Ramsden, D.A., Romeo, C., Cuomo, C.A., Gellert, M. and Oettinger, M.A. (1995) Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell, 83, 387-395.
6. van Gent, D.C., Mizuuchi, K. and Gellert, M. (1996) Similarities between initiation of V(D)J recombination and retroviral integration. Science, 271, 1592-1594.
7. Eastman, Q.M., Leu, T.M. and Schatz, D.G. (1996) Initiation of V(D)J recombination in vitro obeying the 12/23 rule. Nature, 380, 85-88.
8. Lieber, M.R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 79, 181-211.
9. Sadofsky, M.J., Hesse, J.E., McBlane, J.F. and Gellert, M. (1993) Expression and V(D)J recombination activity of mutated RAG-1 proteins. Nucleic Acids Res., 21, 5644-5650.
10. Spanopoulou, E., Zaitseva, F., Wang, F.H., Santagata, S., Baltimore, D. and Panayotou, G. (1996) The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell, 87, 263-276.
11. Yin, F.F., Bailey, S., Innis, C.A., Ciubotaru, M., Kamtekar, S., Steitz, T.A. and Schatz, D.G. (2009) Structure of the RAG1 nonamer binding domain with DNA reveals a dimer that mediates DNA synapsis. Nat. Struct. Mol. Biol., 16, 499-508.
12. Peak, M.M., Arbuckle, J.L. and Rodgers, K.K. (2003) The central domain of core RAG1 preferentially recognizes single-stranded recombination signal sequence heptamer. J. Biol. Chem., 278, 18235-18240.
13. Mo, X., Bailin, T. and Sadofsky, M.J. (2001) A C-terminal region of RAG1 contacts the coding DNA during V(D)J recombination. Mol. Cell. Biol., 21, 2038-2047.
14. Arbuckle, J.L., Fauss, L.A., Simpson, R., Ptaszek, L.M. and Rodgers, K.K. (2001) Identification of two topologically independent domains in RAG1 and their role in macromolecular interactions relevant to V(D)J recombination. J. Biol. Chem., 276, 37093-37101.
15. Kim, D.R., Dai, Y., Mundy, C.L., Yang, W. and Oettinger, M.A. (1999) Mutations of acidic residues in RAG1 define the active site of the V(D)J recombinase. Genes Dev., 13, 3070-3080.
16. Landree, M.A., Wibbenmeyer, J.A. and Roth, D.B. (1999) Mutational analysis of RAG1 and RAG2 identifies three catalytic amino acids in RAG1 critical for both cleavage steps of V(D)J recombination. Genes Dev., 13, 3059-3069.
17. Fugmann, S.D., Villey, I.J., Ptaszek, L.M. and Schatz, D.G. (2000) Identification of two catalytic residues in RAG1 that define a single active site within the RAG1/RAG2 protein complex. Mol. Cell, 5, 97-107.
18. Rodgers, K.K., Villey, I.J., Ptaszek, L., Corbett, E., Schatz, D.G. and Coleman, J.E. (1999) 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, 2938-2946.
19. Ciubotaru, M., Ptaszek, L.M., Baker, G.A., Baker, S.N., Bright, F.V. and Schatz, D.G. (2003) RAG1-DNA binding in V(D)J recombination. Specificity and DNA-induced conformational changes revealed by fluorescence and CD spectroscopy. J. Biol. Chem., 278, 5584-5596.
20. Zhao, S., Gwyn, L.M., De, P. and Rodgers, K.K. (2009) A non-sequence-specific DNA binding mode of RAG1 is inhibited by RAG2. J. Mol. Biol., 387, 744-758.
21. Mo, X., Bailin, T. and Sadofsky, M.J. (1999) RAG1 and RAG2 cooperate in specific binding to the recombination signal sequence in vitro. J. Biol. Chem., 274, 7025-7031.
22. Lin, W.C. and Desiderio, S. (1994) Cell cycle regulation of V(D)J recombination-activating protein RAG-2. Proc. Natl Acad. Sci. USA, 91, 2733-2737.
23. van Gent, D.C., Ramsden, D.A. and Gellert, M. (1996) The RAG1 and RAG2 proteins establish the 12/23 rule in V(D)J recombination. Cell, 85, 107-113.
24. Swanson, P.C. (2002) Fine structure and activity of discrete RAG-HMG complexes on V(D)J recombination signals. Mol. Cell. Biol., 22, 1340-1351.
25. Ronfani, L., Ferraguti, M., Croci, L., Ovitt, C.E., Scholer, H.R., Consalez, G.G. and Bianchi, M.E. (2001) Reduced fertility and spermatogenesis defects in mice lacking chromosomal protein Hmgb2. Development, 128, 1265-1273.
26. Watson, M., Stott, K. and Thomas, J.O. (2007) Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach. J. Mol. Biol., 374, 1286-1297.
27. Stott, K., Watson, M., Howe, F.S., Grossmann, J.G. and Thomas, J.O. (2010) Tail-mediated collapse of HMGB1 is dynamic and occurs via differential binding of the acidic tail to the A and B domains. J. Mol. Biol., 403, 706-722.
28. Stros, M. (2010) HMGB proteins: interactions with DNA and chromatin. Biochim. Biophys. Acta, 1799, 101-113.
29. Jayaraman, L., Moorthy, N.C., Murthy, K.G., Manley, J.L., Bustin, M. and Prives, C. (1998) High mobility group protein-1 (HMG-1) is a unique activator of p53. Genes Dev., 12, 462-472.
30. Sutrias-Grau, M., Bianchi, M.E. and Bernues, J. (1999) High mobility group protein 1 interacts specifically with the core domain of human TATA box-binding protein and interferes with transcription factor IIB within the pre-initiation complex. J. Biol. Chem., 274, 1628-1634.
31. Agresti, A., Scaffidi, P., Riva, A., Caiolfa, V.R. and Bianchi, M.E. (2005) GR and HMGB1 interact only within chromatin and influence each other's residence time. Mol. Cell, 18, 109-121.
32. Agresti, A. and Bianchi, M.E. (2003) HMGB proteins and gene expression. Curr. Opin. Genet. Dev., 13, 170-178.
33. Scaffidi, P., Misteli, T. and Bianchi, M.E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature, 418, 191-195.
34. Phair, R.D., Scaffidi, P., Elbi, C., Vecerova, J., Dey, A., Ozato, K., Brown, D.T., Hager, G., Bustin, M. and Misteli, T. (2004) Global nature of dynamic protein-chromatin interactions in vivo: three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol., 24, 6393-6402.
35. Agrawal, A. and Schatz, D.G. (1997) RAG1 and RAG2 form a stable postcleavage synaptic complex with DNA containing signal ends in V(D)J recombination. Cell, 89, 43-53.
36. Swanson, P.C. (2002) A RAG-1/RAG-2 tetramer supports 12/23-regulated synapsis, cleavage, and transposition of V(D)J recombination signals. Mol. Cell. Biol., 22, 7790-7801.
37. Grundy, G.J., Ramon-Maiques, S., Dimitriadis, E.K., Kotova, S., Biertumpfel, C., Heymann, J.B., Steven, A.C., Gellert, M. and Yang, W. (2009) Initial stages of V(D)J recombination: the organization of RAG1/2 and RSS DNA in the postcleavage complex. Mol. Cell, 35, 217-227.
38. Aidinis, V., Bonaldi, T., Beltrame, M., Santagata, S., Bianchi, M.E. and Spanopoulou, E. (1999) The RAG1 homeodomain recruits HMG1 and HMG2 to facilitate recombination signal sequence binding and to enhance the intrinsic DNA-bending activity of RAG1-RAG2. Mol. Cell. Biol., 19, 6532-6542.
39. Zappavigna, V., Falciola, L., Helmer-Citterich, M., Mavilio, F. and Bianchi, M.E. (1996) HMG1 interacts with HOX proteins and enhances their DNA binding and transcriptional activation. EMBO J., 15, 4981-4991.
40. Zwilling, S., Konig, H. and Wirth, T. (1995) High mobility group protein 2 functionally interacts with the POU domains of octamer transcription factors. EMBO J., 14, 1198-1208.
41. Ge, H. and Roeder, R.G. (1994) The high mobility group protein HMG1 can reversibly inhibit class II gene transcription by interaction with the TATA-binding protein. J. Biol. Chem., 269, 17136-17140.
42. Bergeron, S., Anderson, D.K. and Swanson, P.C. (2006) RAG and HMGB1 proteins: purification and biochemical analysis of recombination signal complexes. Methods Enzymol., 408, 511-528.
43. Cortajarena, A.L., Lois, G., Sherman, E., O'Hern, C.S., Regan, L. and Haran, G. (2008) Non-random-coil behavior as a consequence of extensive PPII structure in the denatured state. J. Mol. Biol., 382, 203-212.
44. Haugland, R.P., Spence, M.T.Z., Johnson, I.D. and Basey, A. (2005) The handbook: a guide to fluorescent probes and labeling technologies, 10th edn, Molecular Probes, Eugene, OR.
45. Gasteiger, E., Gattiker, A., Hoogland, C., Ivanyi, I., Appel, R.D. and Bairoch, A. (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res., 31, 3784-3788.
46. Ramsden, D.A., McBlane, J.F., van Gent, D.C. and Gellert, M. (1996) Distinct DNA sequence and structure requirements for the two steps of V(D)J recombination signal cleavage. EMBO J., 15, 3197-3206.
47. Subrahmanyam, R., Du, H., Ivanova, I., Chakraborty, T., Ji, Y., Zhang, Y., Alt, F.W., Schatz, D.G. and Sen, R. (2012) Localized epigenetic changes induced by dh recombination restricts recombinase to DJH junctions. Nat. Immunol., 13, 1205-1212.
48. Lakowicz, J.R. (2006) Principles of fluorescence spectroscopy, 3rd edn. Springer, New York.
49. McMahan, C.J., Sadofsky, M.J. and Schatz, D.G. (1997) Definition of a large region of RAG1 that is important for coimmunoprecipitation of RAG2. J. Immunol., 158, 2202-2210.
50. Aidinis, V., Dias, D.C., Gomez, C.A., Bhattacharyya, D., Spanopoulou, E. and Santagata, S. (2000) Definition of minimal domains of interaction within the recombination-activating genes 1 and 2 recombinase complex. J. Immunol., 164, 5826-5832.
51. Leu, T.M. and Schatz, D.G. (1995) rag-1 and rag-2 are components of a high-molecular-weight complex, and association of rag-2 with this complex is rag-1 dependent. Mol. Cell. Biol., 15, 5657-5670.
52. Godderz, L.J., Rahman, N.S., Risinger, G.M., Arbuckle, J.L. and Rodgers, K.K. (2003) Self-association and conformational properties of RAG1: implications for formation of the V(D)J recombinase. Nucleic Acids Res., 31, 2014-2023.
53. Rusinova, E., Tretyachenko-Ladokhina, V., Vele, O.E., Senear, D.F. and Alexander Ross, J.B. (2002) Alexa and Oregon Green dyes as fluorescence anisotropy probes for measuring protein-protein and protein-nucleic acid interactions. Anal. Biochem., 308, 18-25.
54. Akamatsu, Y. and Oettinger, M.A. (1998) Distinct roles of RAG1 and RAG2 in binding the V(D)J recombination signal sequences. Mol. Cell. Biol., 18, 4670-4678.
55. Wagner, J.P., Quill, D.M. and Pettijohn, D.E. (1995) Increased DNA-bending activity and higher affinity DNA binding of high mobility group protein HMG-1 prepared without acids. J. Biol. Chem., 270, 7394-7398.
56. Jung, Y. and Lippard, S.J. (2003) Nature of full-length HMGB1 binding to cisplatin-modified DNA. Biochemistry, 42, 2664-2671.
57. Butteroni, C., De Felici, M., Scholer, H.R. and Pesce, M. (2000) Phage display screening reveals an association between germline-specific transcription factor Oct-4 and multiple cellular proteins. J. Mol. Biol., 304, 529-540.
58. Boonyaratanakornkit, V., Melvin, V., Prendergast, P., Altmann, M., Ronfani, L., Bianchi, M.E., Taraseviciene, L., Nordeen, S.K., Allegretto, E.A. and Edwards, D.P. (1998) High-mobility group chromatin proteins 1 and 2 functionally interact with steroid hormone receptors to enhance their DNA binding in vitro and transcriptional activity in mammalian cells. Mol. Cell. Biol., 18, 4471-4487.
59. Melvin, V.S., Roemer, S.C., Churchill, M.E. and Edwards, D.P. (2002) The C-terminal extension (CTE) of the nuclear hormone receptor DNA binding domain determines interactions and functional response to the HMGB-1/-2 co-regulatory proteins. J. Biol. Chem., 277, 25115-25124.
60. Onate, S.A., Prendergast, P., Wagner, J.P., Nissen, M., Reeves, R., Pettijohn, D.E. and Edwards, D.P. (1994) The DNA-bending protein HMG-1 enhances progesterone receptor binding to its target DNA sequences. Mol. Cell. Biol., 14, 3376-3391.
61. Verrijdt, G., Haelens, A., Schoenmakers, E., Rombauts, W. and Claessens, F. (2002) Comparative analysis of the influence of the high-mobility group box 1 protein on DNA binding and transcriptional activation by the androgen, glucocorticoid, progesterone and mineralocorticoid receptors. Biochem. J., 361, 97-103.
62. Drejer-Teel, A.H., Fugmann, S.D. and Schatz, D.G. (2007) The beyond 12/23 restriction is imposed at the nicking and pairing steps of DNA cleavage during V(D)J recombination. Mol. Cell. Biol., 27, 6288-6299.
63. Brent, R. (2001) Analysis of protein-protein interactions. Curr. Protoc. Protein Sci., Chapter 19, Unit 19.11.
64. Pavlicek, J.W., Lyubchenko, Y.L. and Chang, Y. (2008) Quantitative analyses of RAG-RSS interactions and conformations revealed by atomic force microscopy. Biochemistry, 47, 11204-11211.
65. Ciubotaru, M., Trexler, A.J., Spiridon, L.N., Surleac, M.D., Rhoades, E., Petrescu, A.J. and Schatz, D.G. (2012) RAG and HMGB1 create a large bend in the 23RSS in the V(D)J recombination synaptic complex. Nucleic Acids Res., 41, 2437-2454.
66. Roemer, S.C., Adelman, J., Churchill, M.E. and Edwards, D.P. (2008) Mechanism of high-mobility group protein B enhancement of progesterone receptor sequence-specific DNA binding. Nucleic Acids Res., 36, 3655-3666.
67. McKinney, K. and Prives, C. (2002) Efficient specific DNA binding by p53 requires both its central and C-terminal domains as revealed by studies with high-mobility group 1 protein. Mol. Cell. Biol., 22, 6797-6808.
68. Jiang, H., Chang, F.C., Ross, A.E., Lee, J., Nakayama, K., Nakayama, K. and Desiderio, S. (2005) Ubiquitylation of RAG-2 by Skp2-SCF links destruction of the V(D)J recombinase to the cell cycle. Mol. Cell, 18, 699-709.
69. Ji, Y., Resch, W., Corbett, E., Yamane, A., Casellas, R. and Schatz, D.G. (2010) The in vivo pattern of binding of RAG1 and RAG2 to antigen receptor loci. Cell, 141, 419-431.
70. Swanson, P.C. and Desiderio, S. (1998) V(D)J recombination signal recognition: distinct, overlapping DNA-protein contacts in complexes containing RAG1 with and without RAG2. Immunity, 9, 115-125.
71. Xin, H., Taudte, S., Kallenbach, N.R., Limbach, M.P. and Zitomer, R.S. (2000) DNA binding by single HMG box model proteins. Nucleic Acids Res., 28, 4044-4050.
72. Pohler, J.R., Norman, D.G., Bramham, J., Bianchi, M.E. and Lilley, D.M. (1998) HMG box proteins bind to four-way DNA junctions in their open conformation. EMBO J., 17, 817-826.
73. Vitoc, C.I. and Mukerji, I. (2011) HU binding to a DNA four-way junction probed by Forster resonance energy transfer. Biochemistry, 50, 1432-1441.