Chromosomal reinsertion of broken RSS ends during T cell development

Journal of Experimental Medicine

Volumn 204, Issue 10, 2007, Pages 2293-2303

  Curry, John D ^a   Schulz, Danae ^a   Guidos, Cynthia J ^b,c   Danska, Jayne S ^b,c   Nutter, Lauryl ^b,c   Nussenzweig, Andre ^d   Schlissel, Mark S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; RECOMBINASE;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL MATURATION; CHROMOSOME STRUCTURE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA REPAIR; DNA SEQUENCE; DNA TRANSPOSITION; ENZYME ACTIVITY; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC RECOMBINATION; GENOME; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THYMOCYTE;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELL LINE; CHROMOSOMES, MAMMALIAN; DNA; MICE; MICE, KNOCKOUT; MUTATION; RECOMBINATION, GENETIC; T-LYMPHOCYTES; THYMUS GLAND;

EID: 34948844963     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20070583     Document Type: Article

References (44)

1. Gellert, M. 2002. V(D)J recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 71:101-132.
2. Mills, K.D., D.O. Ferguson, and F.W. Alt. 2003. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 194:77-95.
3. Lewis, S.M., and G.E. Wu. 1997. The origins of V(D)J recombination. Cell. 88:159-162.
4. Oettinger, M.A., D.G. Schatz, C. Gorka, and D. Baltimore. 1990. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science. 248:1517-1523.
5. Jones, J.M., and M. Gellert. 2004. The taming of a transposon: V(D)J recombination and the immune system. Immunol. Rev. 200:233-248.
6. Lewis, S.M., J.E. Hesse, K. Mizuuchi, and M. Gellert. 1988. Novel strand exchanges in V(D)J recombination. Cell. 55:1099-1107.
7. Agrawal, A., Q.M. Eastman, and D.G. Schatz. 1998. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature. 394:744-751.
8. Hiom, K., M. Melek, and M. Gellert. 1998. DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell. 94:463-470.
9. Melek, M., and M. Gellert. 2000. RAG1/2-mediated resolution of transposition intermediates: two pathways and possible consequences. Cell. 101:625-633.
10. Tsai, C.L., and D.G. Schatz. 2003. Regulation of RAG1/RAG2-mediated transposition by GTP and the C-terminal region of RAG2. EMBO J. 22:1922-1930.
11. Swanson, P.C., D. Volkmer, and L. Wang. 2004. Full-length RAG-2, and not full-length RAG-1, specifically suppresses RAG-mediated transposition but not hybrid joint formation or disintegration. J. Biol. Chem. 279:4034-4044.
12. Elkin, S.K., A.G. Matthews, and M.A. Oettinger. 2003. The C-terminal portion of RAG2 protects against transposition in vitro. EMBO J. 22:1931-1938.
13. Sekiguchi, J.A., S. Whitlow, and F.W. Alt. 2001. Increased accumulation of hybrid V(D)J joins in cells expressing truncated versus full-length RAGs. Mol. Cell. 8:1383-1390.
14. Kuppers, R., and R. Dalla-Favera. 2001. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene. 20:5580-5594.
15. Roth, D.B. 2003. Restraining the V(D)J recombinase. Nat. Rev. Immunol. 3:656-666.
16. Schlissel, M.S., C.R. Kaffer, and J.D. Curry. 2006. Leukemia and lymphoma: a cost of doing business for adaptive immunity. Genes Dev. 20:1539-1544.
17. Raghavan, S.C., I.R. Kirsch, and M.R. Lieber. 2001. Analysis of the V(D)J recombination efficiency at lymphoid chromosomal translocation breakpoints. J. Biol. Chem. 276:29126-29133.
18. Raghavan, S.C., P.C. Swanson, X. Wu, C.L. Hsieh, and M.R. Lieber. 2004. A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Nature. 428:88-93.
19. Vanura, K., B. Montpellier, T. Le, S. Spicuglia, J.M. Navarro, O. Cabaud, S. Roulland, E. Vachez, I. Prinz, P. Ferrier, et al. 2007. In Vivo Reinsertion of Excised episomes by the V(D)J recombinase: a potential threat to genomic stability. PLoS Biol. 5:e43.
20. Messier, T.L., J.P. O'Neill, and B.A. Finette. 2006. V(D)J recombinase mediated inter-chromosomal HPRT alterations at cryptic recombination signal sequences in peripheral human T cells. Hum. Mutat. 27:829.
21. Messier, T.L., J.P. O'Neill, S.M. Hou, J.A. Nicklas, and B.A. Finette. 2003. In vivo transposition mediated by V(D)J recombinase in human T lymphocytes. EMBO J. 22:1381-1388.
22. Reddy, Y.V., E.J. Perkins, and D.A. Ramsden. 2006. Genomic instability due to V(D)J recombination-associated transposition. Genes Dev. 20:1575-1582.
23. Liang, H.E., L.Y. Hsu, D. Cado, L.G. Cowell, G. Kelsoe, and M.S. Schlissel. 2002. The "dispensable" portion of RAG2 is necessary for efficient V-to-DJ rearrangement during B and T cell development. Immunity. 17:639-651.
24. Celeste, A., S. Petersen, P.J. Romanienko, O. Fernandez-Capetillo, H.T. Chen, O.A. Sedelnikova, B. Reina-San-Martin, V. Coppola, E. Meffre, M.J. Difilippantonio, et al. 2002. Genomic instability in mice lacking histone H2AX. Science. 296:922-927.
25. Guidos, C.J., C.J. Williams, I. Grandal, G. Knowles, M.T. Huang, and J.S. Danska. 1996. V(D)J recombination activates a p53-dependent DNA damage checkpoint in scid lymphocyte precursors. Genes Dev. 10:2038-2054.
26. Ward, I.M., K. Minn, J. van Deursen, and J. Chen. 2003. p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23:2556-2563.
27. Xu, Y., T. Ashley, E.E. Brainerd, R.T. Bronson, M.S. Meyn, and D. Baltimore. 1996. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10:2411-2422.
28. Schuler, W., I. Weiler, A. Schuler, R. Phillips, N. Rosenberg, T.W. Mak, and M.J. Bosma. 1986. Rearrangement of antigen receptor genes is defective in mice with severe combined immune deficiency. Cell. 46:963-974.
29. Fukumura, R., R. Araki, A. Fujimori, Y. Tsutsumi, A. Kurimasa, G.C. Li, D.J. Chen, K. Tatsumi, and M. Abe. 2000. Signal joint formation is also impaired in DNA-dependent protein kinase catalytic subunit knockout cells. J. Immunol. 165:3883-3889.
30. Muljo, S.A., and M.S. Schlissel. 2003. A small molecule Abl kinase inhibitor induces differentiation of Abelson virus-transformed pre-B cell lines. Nat. Immunol. 4:31-37.
31. Neiditch, M.B., G.S. Lee, L.E. Huye, V.L. Brandt, and D.B. Roth. 2002. The V(D)J recombinase efficiently cleaves and transposes signal joints. Mol. Cell. 9:871-878.
32. Reddy, Y.V., E.J. Perkins, and D.A. Ramsden. 2006. Genomic instability due to V(D)J recombination-associated transposition. Genes Dev. 20:1575-1582.
33. Curry, J.D., L. Li, and M.S. Schlissel. 2005. Quantification of Jkappa signal end breaks in developing B cells by blunt-end linker ligation and qPCR. J. Immunol. Methods. 296:19-30.
34. Bredemeyer, A.L., G.G. Sharma, C.Y. Huang, B.A. Helmink, L.M. Walker, K.C. Khor, B. Nuskey, K.E. Sullivan, T.K. Pandita, C.H. Bassing, and B.P. Sleckman. 2006. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature. 442:466-470.
35. West, K.L., N.C. Singha, P. De Ioannes, L. Lacomis, H. Erdjument-Bromage, P. Tempst, and P. Cortes. 2005. A direct interaction between the RAG2 C terminus and the core histones is required for efficient V(D)J recombination. Immunity. 23:203-212.
36. Marculescu, R., K. Vanura, B. Montpellier, S. Roulland, T. Le, J.M. Navarro, U. Jager, F. McBlane, and B. Nadel. 2006. Recombinase, chromosomal translocations and lymphoid neoplasia: targeting mistakes and repair failures. DNA Repair (Amst.). 5:1246-1258.
37. Tillman, R.E., A.L. Wooley, M.M. Hughes, T.D. Wehrly, W. Swat, and B.P. Sleckman. 2002. Restrictions limiting the generation of DNA double strand breaks during chromosomal V(D)J recombination. J. Exp. Med. 195:309-316.
38. Sen, R., and E. Oltz. 2006. Genetic and epigenetic regulation of IgH gene assembly. Curr. Opin. Immunol. 18:237-242.
39. Roix, J.J., P.G. McQueen, P.J. Munson, L.A. Parada, and T. Misteli. 2003. Spatial proximity of translocation-prone gene loci in human lymphomas. Nat. Genet. 34:287-291.
40. Hill, D.A., S.S. Wang, J.R. Cerhan, S. Davis, W. Cozen, R.K. Severson, P. Hartge, S. Wacholder, M. Yeager, S.J. Chanock, and N. Rothman. 2006. Risk of non-Hodgkin lymphoma (NHL) in relation to germline variation in DNA repair and related genes. Blood. 108:3161-3167.
41. Shinkai, Y., G. Rathbun, K. Lam, E. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A.M. Stall, and F.W. Alt. 1992. RAG-2 deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell. 68:855-867.
42. Shinkai, Y., S. Koyasu, K. Nakayama, K.M. Murphy, D.Y. Loh, E.L. Reinherz, and F.W. Alt. 1993. Restoration of T cell development in RAG-2-deficient mice by functional TCR transgenes. Science. 259:822-825.
43. Luria, S.E., and M. Delbruck. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics. 28:491-511.
44. Cowell, L.G., M. Davila, K. Yang, T.B. Kepler, and G. Kelsoe. 2003. Prospective estimation of recombination signal efficiency and identification of functional cryptic signals in the genome by statistical modeling. J. Exp. Med. 197:207-220.