Hairpin coding end opening is mediated by RAG1 and RAG2 proteins

Molecular Cell

Volumn 2, Issue 6, 1998, Pages 817-828

  Besmer, Eva ^a   Mansilla Soto, Jorge ^a   Cassard, Sylvanie ^a   Sawchuk, Dennis J ^a   Brown, Greg ^b   Sadofsky, Moshe ^c   Lewis, Susanna M ^b   Nussenzweig, Michel C ^a   Cortes, Patricia ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DERIVATIVE; DNA; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; OLIGONUCLEOTIDE; RAG 1 PROTEIN; RAG-1 PROTEIN; V(D)J RECOMBINATION ACTIVATING PROTEIN 2;

ARTICLE; BASE PAIRING; CHEMISTRY; CONFORMATION; GENETICS; HYDROLYSIS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE;

ALCOHOLS; BASE PAIRING; BASE SEQUENCE; DNA; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES;

EID: 0032247578     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80296-8     Document Type: Article

References (87)

1. Agrawal, A., and Schatz, D. (1997). RAG1 and RAG2 form a stable postcleavage synaptic complex with DNA containing signal ends in V(D)J recombination. Cell 89, 43-53.
2. Agrawal, A., Eastman, Q.M., and Schatz, D. (1998). Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394, 744-751.
3. Blunt, T., Finnie, N., Taccioli, G., Smith, G., Demengeot, J., Gottlieb, T., Mizuta, R., Varghese, A., Alt, F., Jeggo, P., and Jackson, S. (1995). Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine seid mutation. Cell 80, 813-823.
4. Bogue, M., and Roth, D.B. (1996). Mechanism of V(D)J recombination. Curr. Opin. Immunol. 8, 175-180.
5. Bogue, M.A., Wang, C., Zhu, C., and Roth, D.B. (1997). V(D)J recombination in Ku86-deficient mice: distinct effects on coding, signal and hybrid joint formation. Immunity 7, 37-47.
6. Cortes, P., Weis-Garcia, F., Misulovin, Z., Nussenzweig, A., Lai, J.-S., Li, G., Nussenzweig, M.C., and Baltimore, D. (1996). In vitro V(D)J recombination: signal joint formation. Proc. Natl. Acad. Sci. USA 31, 14008-14013.
7. Critchlow, S.E., Bowater, R.P., and Jackson, S.P. (1997). Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol. 7, 588-598.
8. Cuomo, C.A., and Oettinger, M.A. (1994). Analysis of regions of RAG-2 important for V(D)J recombination. Nucleic Acids Res. 22, 1810-1814.
9. Difilippantonio, M.J., McMahan, C.J., Eastman, Q.M., Spanopoulou, E., and Schatz, D. (1996). RAG1 mediates signal sequence recognition and recruitment of RAG2 in V(D)J recombination. Cell 87, 253-262.
10. Dvir, A., Peterson, S.R., Knuth, M.W., Lu, H., and Dynan, W.S. (1992). Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc. Natl. Acad. Sci. USA 89, 11920-11924.
11. Dynan, W.S., and Yoo, S. (1998). Interaction of Ku protein and DNA-dependent protein kinase catalytic subunit with nucleic acids. Nucleic Acids Res. 26, 1551-1559.
12. Eastman, Q.M., Leu, T.M.L., and Schatz, D.G. (1996). Initiation of V(D)J recombination in vitro obeying 12/23 rule. Nature 380, 85-88.
13. Engelman, A., Mizuuchi, K., and Craigie, R. (1991). HIV-1 DNA integration: mechanism of viral DNA cleavage and DNA strand transfer. Cell 67, 1211-1221.
14. Fish, S.M., and Bosma, M.J. (1994) Abnormal deletions in the T cell receptor d locus of mouse thymocytes. Mol. Cell. Biol. 14, 4455-4464.
15. Gilfillan, S., Dierich, A., Lemeur, M., Benoist, C., and Mathis, D. (1993). Mice lacking TdT: mature animals with an immature lymphocyte repertoire. Science 261, 1175-1178.
16. Gottlieb, T., and Jackson, S.P. (1993). The DNA-dependent protein kinase: requirements for DNA ends and association with Ku antigen. Cell 72, 131-142.
17. Grawunder, U., Wilm, M., Wu, X., Kulesza, P., Wilson, T.E., Mann, M., and Lieber, M.R. (1997). Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 388, 492-495.
18. Gu, Y., Seidl, K.J., Rathbun, G.A., Zhu, C., Manis, J.P., van der Stoep, N., Davidson, L., Cheng, H-L., Sekiguchi, J.M., Frank, K., et al. (1997). Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7, 653-665.
19. Haniford, D.B., Benjamin, H.W., and Kleckner., N. (1991). Kinetic and structural analysis of a cleaved donor intermediate and a strand transfer intermediate in Tn10 transposition. Cell 64, 171-179.
20. Hendrickson, E.A., Qin, X.-Q., Bump, E.A., Schatz, D.G., Oettinger, M., and Weaver, D.T. (1991). A link between double-strand break-related repair and V(D)J recombination: the scid mutation. Proc. Natl. Acad. Sci. USA 88, 4061-4065.
21. Hiom, K., and Gellert, M. (1997). A stable RAG1-RAG-2-DNA complex that is active in V(D)J cleavage. Cell 88, 65-72.
22. Hiom, K., and Gellert, M. (1998). Assembly of a 12/23 paired signal complex: a critical control point in V(D)J recombination. Mol. Cell 1, 1011-1019.
23. Hiom, K., Melek, M., and Gellert, M. (1998). DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94, 463-470.
24. Jackson, S.P., and Jeggo, P.A. (1995). DNA double-strand break repair and V(D)J recombination-involvement of DNA-PK. Trends Biochem. Sci. 20, 412-415.
25. Kabotyanski, E.B., Zhu, C., Kallick, D.A., and Roth, D.B. (1995). Hairpin opening by single-strand-specific nucleases. Nucleic Acids Res. 23, 3872-3881.
26. Kallenbach, S., Doyen, N., Fanton d'Andon, M., and Reugeon, F. (1992). Three lymphold-specific factors account for all the junctional diversity characteristic of somatic assembly of T-cell receptor and immunoglobulins genes. Proc. Natl. Acad. Sci. USA 89, 2799-2803.
27. Kemp, L.M., Sedgwick, S.G., and Jeggo, P.A. (1984). X-ray sensitive mutants of Chinese hamster ovary cells defective in double-stranded break rejoining. Mutat. Res. 132, 189-196.
28. Kennedy, A.K., Guhathakurta, A., Kleckner, N., and Haniford, D.B. (1998). Tn10 Excision via a DNA Hairpin Intermediate. Cell 95, 125-134.
29. Kirchgessner, C.U., Patil, C.K., Evans, J.W., Cuomo, C.A., Fried, L.M., Carter, T., Oettinger, M.A., and Brown, J.M. (1995). DNA-dependent kinase (p350) as a candidate gene for the murine scid defect. Science 267, 1178-1183.
30. Komori, T., Okada, A., Stewart, V., and Alt, F.W. (1993). Lack of N regions of antigen receptor variable region genes of TdT-defiecient lymphocytes. Science 261, 1171-1175.
31. Lafaille, J.J., DeCloux, A., Bonneville, M., Takagaki, Y., and Tonegawa, S. (1989). Junctional sequences of T cell receptor gamma delta genes: implications for gamma delta T cell lineages and for a novel intermediate of V(D)J joining. Cell 59, 859-870.
32. Landau, N.R., Schatz, D.G., Rosa, M., and Baltimore, D. (1987). Increased frequency of N-region insertion in a murine pre-B-cell line infected with a terminal deoxynucleotidyl transferase retroviral expression vector. Mol. Cell. Biol. 7, 3237-3243.
33. Leu, T.M.J., Eastman, Q.M., and Schatz, D.G. (1997). Coding joint formation in a cell-free V(D)J recombination system. Immunity 7, 303-314.
34. Lewis, S.M. (1994a). The mechanism of V(D)J joining: lessons from molecular, immunological and comparative analysis. Adv. immunol. 56, 27-150.
35. Lewis, S.M. (1994b). P nucleotides insertions and the resolution of hairpin DNA structures in mammalian cells. Proc. Natl. Acad. Sci. USA 91, 1332-1336.
36. Lewis, S., and Wu, G. (1997). The origin of V(D)J recombination. Cell 88, 159-162.
37. Li, Z., Otevrel, T., Gao, Y., Cheng, H.-L., Seed, B., Stamoto, T.D., Taccioli, G.E., and Alt, F. (1995). The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 83, 1079-1089.
38. Li, W., Swason, P., and Desiderio, S. (1997). RAG1 and RAG2 dependent assembly of functional complexes with V(D)J recombination substrates in solution. Mol. Cell. Biol. 17, 6932-6939.
39. Lieber, M.R. (1991). The mechanism of V(D)J recombination: a balance of diversity, specificity and stability. Cell 70, 873-876.
40. Livak, F., and Schatz, D.G. (1997). Identification of V(D)J recombination coding ends intermediates in normal thymocytes. J. Mol. Biol. 267, 1-9.
41. 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.
42. McCormack, W.T. Tjoelker, L.W., Carlson, L.M., Petryniak, B., Barth, C.F., Humphries, E.H., and Thompson, C.B. (1989). Chicken IgL gene rearrangement involves deletions of a circular episome and addition of a single nonrandom nucleotides to both coding segments. Cell 56, 785-791.
43. Meier, J.T., and Lewis, S.M. (1993). P nucleotides in V(D)J recombination: a fine-structure analysis. Mol. Cell. Biol. 13, 1078-1092.
44. Melek, M., Gellert, M., and van Gent, D.C. (1998). Rejoining of DNA by the RAG1 and RAG2 proteins. Science 280, 301-303.
45. Mizushima, S., and Nagata, S. (1990). pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18, 5322.
46. Mizuuchi., K. (1997). Polynucleotidyl transfer reactions in site-specific DNA recombination. Genes to Cells 2, 1-12.
47. Mizuuchi, K., and Adzuma, K. (1991). Inversion of the phosphate chirality at the target site of Mu DNA strand transfer: evidence for one-step transesterification mechanism. Cell 66, 129-140.
48. Nadel, B., and Feeney, A.J. (1997). Nucleotide deletion and P addition in V(D)J recombination: a determinant role of the coding-end sequence. Mol. Cell. Biol. 17, 3768-3778.
49. Nagawa, F., Ishiguro, K.-I., Tsuboi, A., Yoshida, T., Ishikawa, A., Takemori, T., Otsuka, A. J., and Sakano, H. (1998). Footprint analysis of the RAG protein recombination signal sequence complex for V(D)J type recombination. Mol. Cell. Biol. 18, 655-663.
50. Nussenzweig, A., Chen, C., da Costa Soares, V., Sanchez, M., Sokol, K., Nussenzweig, M.C., and Li, G.C. (1996). Requirement for Ku80 in growth and V(D)J recombination. Nature 382, 551-555.
51. 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.
52. Pear, W., Nolan, G., Scott, M., and Baltimore, D. (1993). Purification of high titer helper free retrovirus by transient transfection. Proc. Natl. Acad. Sci. USA 90, 8392-8395.
53. Pergola, F., Zdzienicka, M.Z., and Lieber, M.R. (1993). V(D)J recombination in mammalian mutants defective in DNA double-strand break repair. Mol. Cell. Biol. 13, 3464-3471.
54. Peterson, S., Kurimasa, A., Oshimura, M., Dynan, W., Bradbury, E., and Chen, D. (1995). Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proc. Natl. Acad. Sci. USA 92, 3171-3174.
55. Ramsden, D.A., and Gellert, M. (1995). Formation and resolution of double-strand break intermediates in V(D)J rearrangement. Genes Dev. 9, 2409-2420.
56. Ramsden, D.A., Paull, T., and Gellert, M. (1997). Cell-free V(D)J recombination. Nature 388, 488-491.
57. Rathmell, W.K., and Chu, G. (1994). A DNA end-binding factor involved in double-strand break repair and V(D)J recombination. Mol. Cell. Biol 14, 4741-4748.
58. Roth, D.B., Menetski, J.P., Nakajima, P.B., Bosma, M.J., and Gellert, M. (1992). V(D)J recombination: broken DNA molecules with covalently sealed (hairpin) coding ends in seid mouse thymocytes. Cell 70, 983-991.
59. Roth, D.B., Nakajima, P.B., Menetski, J.P., Bosma, M.J., and Gellert, M. (1993). V(D)J Recombination in mouse Thymocytes: double-strand breaks near T cell receptor 5 rearrangement signals. Cell 69, 41-53.
60. Roth, D.B., Lindahl, T., and Gellert, M. (1995). Repair and recombination. How to make ends meet. Curr. Biol. 5, 496-499.
61. 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.
62. Sadofsky, M.J., Hesse, J.E., and Gellert, M. (1994). Definition of a core region of RAG-2 that is functional in V(D)J recombination. Nucleic Acids Res. 22, 1805-1809.
63. Sakano, H., Huppi, K., Heinrich, G., and Tonegawa, S. (1979). Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature 280, 288-294.
64. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning, a laboratory manual. 11.23.
65. Santagata, S., Aidinis, V., and Spanopoulou, E. (1998). The effect of Me2+ cofactors at the initial stages of V(D)J recombination. J. Biol. Chem. 273, 16325-16331.
66. Sawchuk, D.J., Weis-Garcia, F., Malik, S., Besmer, E.B.M., Nussenzweig, M., and Cortes, P. (1997). V(D)J recombination: modulation of RAG1 and RAG2 cleavage activity on 12/23 substrates by whole cell extract and DNA-bending proteins. J. Exp. Med. 185, 2025-2032.
67. Schlissel, M.S. (1998). Structure of nonhairpin coding-end DNA breaks in cells undergoing V(D)J recombination. Mol. Cell. Biol. 18, 2029-2037.
68. Schlissel, M.S., Constantinescu, A., Morrow, T., Baxter, M., and Peng, A. (1993). Double-strand signal sequence breaks in V(D)J recombination are blunt, 5′ phosphorylated, RAG-dependent and cell cycle regulated. Genes Dev. 7, 2520-2532.
69. Silver, D.P., Spanopoulou, E., Mulligan, R.C., and Baltimore, D. (1993). Dispensable sequence motifs in the RAG-1 and RAG-2 genes for plasmid V(D)J recombination. Proc. Natl. Acad. Sci. USA 90, 6100-6104.
70. Smider, V., and Chu, G. (1997). The end-joining reaction in V(D)J recombination. Semin. Immunol. 9, 189-197.
71. Spanopoulou, E., Cortes, P., Shih, C., Huang, E., Silver, D.P., Svec, P., and Baltimore, D. (1995). Localization, interaction and RNA binding properties of the V(D)J recombination activating proteins Rag-1 and Rag-2. Immunity 3, 715-726.
72. Spanopoulou, E., Zaitseta, 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.
73. Steen, S.B., Gomelsky, L., and Roth, D.B. (1996). The 12/23 rule is enforced at the cleavage step of V(D)J recombination in vivo. Genes to Cells 1, 543-553.
74. 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.
75. Taccioli, G.E., Rathbun, G., Oltz, E., Stamato, T., Jeggo, P.A., and Alt, F.W. (1993). Impairment of V(D)J recombination in double-strand break repair mutants. Science 260, 207-210.
76. Taccioli, G.E., Gottlieb, T.M., Blunt, T., Priestly, A., Demengeot, J., Mizuta, R., Lehmann, A.R., Alt, F.W., Jackson, S.P., and Jeggo, P.A. (1994). Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265, 1442-1445.
77. Thompson, C.B. (1995). New insights into V(D)J recombination and its role in the evolution of the immune system. Immunity 3, 531-539.
78. Tonegawa, S. (1983). Somatic generation of antibody diversity. Nature 302, 575-581.
79. van Gent, D.C., McBlane, J.F., Ramsden, D.A., Sadofsky, M.J., Hesse, J.A., and Gellert, M. (1995). Initiation of V(D)J recombination in a cell-free system. Cell 81, 825-934.
80. van Gent, D.C., Mizuuchi, K., and Gellert, M. (1996a). Similarities between initiation of V(D)J recombination and retroviral integration. Science 271, 1592-1594.
81. van Gent, D.C., Ramsden, D.A., and Gellert, M. (1996b). The RAG1 and RAG2 proteins establish the 12/23 rule in V(D)J recombination. Cell 85, 107-113.
82. van Gent, D.C., Hiom, K., Paul, T.T., and Gellert, M. (1997). Stimulation of V(D)J cleavage by high mobility group proteins. EMBO J. 16, 2665-2670.
83. Vink, C., Yeheskiely, E., van der Marel, G.A., van Boon, J.H., and Plasterk, H.A. (1991). Site-specific hydrolysis of human immunodeficiency virus DNA termini mediated by the viral integrase protein. Nucleic Acids Res. 24, 6691-6698.
84. Walker, A.I., Hunt, T., Jackson, R.J., and Anderson, C.W. (1985). Double-strand DNA induces the phosphorylation of several proteins including the 90000 mol. wt. heat shock protein in animal cell extracts. EMBO J. 4, 139-144.
85. Weaver, D.T., and Alt, F.W. (1997). V(D)J recombination. From RAGs to stitches. Nature 388, 428-429.
86. Weis-Garcia, F., Besmer, E., Sawchuk, D.J., Yu, W., Hu, Y., Cassard, S., Nussenzweig, M.C., and Cortes, P. (1997). V(D)J recombination: in vitro coding joint formation. Mol. Cell. Biol. 17, 6379-6385.
87. Zhu, C., Bogue, M.A., Lim, D.-S., and Hasty, P.R., Roth, D.B. (1996). Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86, 379-389.