Terminal deoxynucleotidyl transferase requires KU80 and XRCC4 to promote N-addition at non-V(D)J chromosomal breaks in non-lymphoid cells

Nucleic Acids Research

Volumn 40, Issue 17, 2012, Pages 8381-8391

  Boubakour Azzouz, Imenne ^a,b   Bertrand, Pascale ^c   Claes, Aurélie ^a   Lopez, Bernard S ^b,c   Rougeon, François ^a  

^a CNRS   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA NUCLEOTIDYLEXOTRANSFERASE; NUCLEASE; NUCLEOTIDE; PROTEIN I SCEL; PROTEIN KINASE; PROTEIN KU80; UNCLASSIFIED DRUG; XRCC4 PROTEIN;

ANIMAL CELL; ARTICLE; CHROMOSOME BREAKAGE; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; LYMPHOID CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS, NUCLEAR; CHO CELLS; CRICETINAE; CRICETULUS; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA NUCLEOTIDYLEXOTRANSFERASE; DNA-BINDING PROTEINS; NUCLEOTIDES; V(D)J RECOMBINATION;

EID: 84866893030     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks585     Document Type: Article

References (45)

1. Jung, D. and Alt, F.W. (2004) Unraveling V(D)J recombination; insights into gene regulation. Cell, 116, 299-311. (Pubitemid 38167319)
2. Rooney, S., Chaudhuri, J. and Alt, F.W. (2004) The role of the non-homologous end-joining pathway in lymphocyte development. Immunol. Rev., 200, 115-131. (Pubitemid 38998197)
3. Lieber, M.R., Ma, Y., Pannicke, U. and Schwarz, K. (2004) The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. DNA Repair, 3, 817-826. (Pubitemid 39004089)
4. 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.
5. Corneo, B., Wendland, R.L., Deriano, L., Cui, X., Klein, I.A., Wong, S.Y., Arnal, S., Holub, A.J., Weller, G.R., Pancake, B.A. et al. (2007) Rag mutations reveal robust alternative end joining. Nature, 449, 483-486. (Pubitemid 47509551)
6. Bennardo, N., Cheng, A., Huang, N. and Stark, J.M. (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet., 4, e1000110.
7. Guirouilh-Barbat, J., Huck, S., Bertrand, P., Pirzio, L., Desmaze, C., Sabatier, L. and Lopez, B.S. (2004) Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell., 14, 611-623. (Pubitemid 38744575)
8. Guirouilh-Barbat, J., Rass, E., Plo, I., Bertrand, P. and Lopez, B.S. (2007) Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl Acad. Sci. USA, 104, 20902-20907.
9. Rass, E., Grabarz, A., Plo, I., Gautier, J., Bertrand, P. and Lopez, B.S. (2009) Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat. Struct. Mol. Biol., 16, 819-824.
10. Soulas-Sprauel, P., Le Guyader, G., Rivera-Munoz, P., Abramowski, V., Olivier-Martin, C., Goujet-Zalc, C., Charneau, P. and de Villartay, J.P. (2007) Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med., 204, 1717-1727. (Pubitemid 47048036)
11. Yan, C.T., Boboila, C., Souza, E.K., Franco, S., Hickernell, T.R., Murphy, M., Gumaste, S., Geyer, M., Zarrin, A.A., Manis, J.P. et al. (2007) IgH class switching and translocations use a robust non-classical end-joining pathway. Nature, 449, 478-482. (Pubitemid 47509538)
12. Lewis, S.M. (1994) P nucleotide insertions and the resolution of hairpin DNA structures in mammalian cells. Proc. Natl Acad. Sci. USA, 91, 1332-1336. (Pubitemid 24059005)
13. Benedict, C.L., Gilfillan, S., Thai, T.H. and Kearney, J.F. (2000) Terminal deoxynucleotidyl transferase and repertoire development. Immunol. Rev., 175, 150-157. (Pubitemid 30427165)
14. Desiderio, S.V., Yancopoulos, G.D., Paskind, M., Thomas, E., Boss, M.A., Landau, N., Alt, F.W. and Baltimore, D. (1984) Insertion of N regions into heavy-chain genes is correlated with expression of terminal deoxytransferase in B cells. Nature, 311, 752-755. (Pubitemid 14008988)
15. Nick McElhinny, S.A. and Ramsden, D.A. (2004) Sibling rivalry: competition between Pol X family members in V(D)J recombination and general double strand break repair. Immunol. Rev., 200, 156-164. (Pubitemid 38998200)
16. Bollum, F.J. (1978) Terminal deoxynucleotidyl transferase: biological studies. Adv. Enzymol. Relat. Areas. Mol. Biol., 47, 347-374.
17. Kato, K.I., Goncalves, J.M., Houts, G.E. and Bollum, F.J. (1967) Deoxynucleotide-polymerizing enzymes of calf thymus gland. II. Properties of the terminal deoxynucleotidyltransferase. J. Biol. Chem., 242, 2780-2789.
18. Iwasato, T. and Yamagishi, H. (1992) Novel excision products of T cell receptor gamma gene rearrangements and developmental stage specificity implied by the frequency of nucleotide insertions at signal joints. Eur. J. Immunol., 22, 101-106.
19. Shimizu, T. and Yamagishi, H. (1992) Biased reading frames of pre-existing DH-JH coding joints and preferential nucleotide insertions at VH-DJH signal joints of excision products of immunoglobulin heavy chain gene rearrangements. EMBO. J., 11, 4869-4875. (Pubitemid 23023430)
20. Komori, T., Okada, A., Stewart, V. and Alt, F.W. (1993) Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science, 261, 1171-1175. (Pubitemid 23300884)
21. Bentolila, L.A., Wu, G.E., Nourrit, F., Fanton d'Andon, M., Rougeon, F. and Doyen, N. (1997) Constitutive expression of terminal deoxynucleotidyl transferase in transgenic mice is sufficient for N region diversity to occur at any Ig locus throughout B cell differentiation. J. Immunol., 158, 715-723. (Pubitemid 127492649)
22. Anderson, R.S., Bollum, F.J. and Beattie, K.L. (1999) Pyrophosphorolytic dismutation of oligodeoxy-nucleotides by terminal deoxynucleotidyltransferase. Nucleic Acids Res., 27, 3190-3196. (Pubitemid 29355735)
23. Repasky, J.A., Corbett, E., Boboila, C. and Schatz, D.G. (2004) Mutational analysis of terminal deoxynucleotidyltransferase-mediated N-nucleotide addition in V(D)J recombination. J. Immunol., 172, 5478-5488. (Pubitemid 38542048)
24. Motea, E.A. and Berdis, A.J. (2010) Terminal deoxynucleotidyl transferase: the story of a misguided DNA polymerase. Biochim. Biophys. Acta, 1804, 1151-1166.
25. Robbins, D.J. and Coleman, M.S. (1988) Initiator role of double stranded DNA in terminal transferase catalyzed polymerization reactions. Nucleic Acids Res., 16, 2943-2957.
26. 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. (Pubitemid 27357263)
27. Purugganan, M.M., Shah, S., Kearney, J.F. and Roth, D.B. (2001) Ku80 is required for addition of N nucleotides to V(D)J recombination junctions by terminal deoxynucleotidyl transferase. Nucleic Acids Res., 29, 1638-1646. (Pubitemid 32288514)
28. Sandor, Z., Calicchio, M.L., Sargent, R.G., Roth, D.B. and Wilson, J.H. (2004) Distinct requirements for Ku in N nucleotide addition at V(D)J-and non-V(D)J-generated double-strand breaks. Nucleic Acids Res., 32, 1866-1873. (Pubitemid 38842533)
29. Gao, Y., Ferguson, D.O., Xie, W., Manis, J.P., Sekiguchi, J., Frank, K.M., Chaudhuri, J., Horner, J., DePinho, R.A. and Alt, F.W. (2000) Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature, 404, 897-900. (Pubitemid 30230344)
30. Ma, Y., Lu, H., Tippin, B., Goodman, M.F., Shimazaki, N., Koiwai, O., Hsieh, C.L., Schwarz, K. and Lieber, M.R. (2004) A biochemically defined system for mammalian nonhomologous DNA end joining. Mol. Cell., 16, 701-713. (Pubitemid 39586529)
31. Mahajan, K.N., Nick McElhinny, S.A., Mitchell, B.S. and Ramsden, D.A. (2002) Association of DNA polymerase mu (pol mu) with Ku and ligase IV: role for pol mu in end-joining double-strand break repair. Mol. Cell. Biol., 22, 5194-5202. (Pubitemid 34700708)
32. Liang, F., Han, M., Romanienko, P.J. and Jasin, M. (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl Acad. Sci. USA, 95, 5172-5177. (Pubitemid 28208570)
33. Boule, J.B., Johnson, E., Rougeon, F. and Papanicolaou, C. (1998) High-level expression of murine terminal deoxynucleotidyl transferase in Escherichia coli grown at low temperature and overexpressing argU tRNA. Mol. Biotechnol., 10, 199-208. (Pubitemid 29084744)
34. Murray, J.M., O'Neill, J.P., Messier, T., Rivers, J., Walker, V.E., McGonagle, B., Trombley, L., Cowell, L.G., Kelsoe, G., McBlane, F. et al. (2006) V(D)J recombinase-mediated processing of coding junctions at cryptic recombination signal sequences in peripheral T cells during human development. J. Immunol., 177, 5393-5404. (Pubitemid 44527612)
35. Sale, J.E. and Neuberger, M.S. (1998) TdT-accessible breaks are scattered over the immunoglobulin V domain in a constitutively hypermutating B cell line. Immunity, 9, 859-869. (Pubitemid 29024465)
36. Kabotyanski, E.B., Gomelsky, L., Han, J.O., Stamato, T.D. and Roth, D.B. (1998) Double-strand break repair in Ku86-and XRCC4-deficient cells. Nucleic Acids Res., 26, 5333-5342. (Pubitemid 28542732)
37. Simsek, D. and Jasin, M. (2010) Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat. Struct. Mol. Biol., 17, 410-416.
38. Weinstock, D.M., Brunet, E. and Jasin, M. (2007) Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell. Biol., 9, 978-981. (Pubitemid 47190453)
39. Zhang, Y. and Jasin, M. (2011) An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat. Struct. Mol. Biol., 18, 80-84.
40. Carroll, D. (2011) Genome engineering with zinc-finger nucleases. Genetics, 188, 773-782.
41. Miller, J.C., Tan, S., Qiao, G., Barlow, K.A., Wang, J., Xia, D.F., Meng, X., Paschon, D.E., Leung, E., Hinkley, S.J. et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol., 29, 143-148.
42. Silva, G., Poirot, L., Galetto, R., Smith, J., Montoya, G., Duchateau, P. and Paques, F. (2011) Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr. Gene. Ther., 11, 11-27.
43. Boboila, C., Jankovic, M., Yan, C.T., Wang, J.H., Wesemann, D.R., Zhang, T., Fazeli, A., Feldman, L., Nussenzweig, A., Nussenzweig, M. et al. (2010) Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc. Natl Acad. Sci. USA, 107, 3034-3039.
44. Stephens, P.J., McBride, D.J., Lin, M.L., Varela, I., Pleasance, E.D., Simpson, J.T., Stebbings, L.A., Leroy, C., Edkins, S., Mudie, L.J. et al. (2009) Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature, 462, 1005-1010.
45. Zhang, Y., Gostissa, M., Hildebrand, D.G., Becker, M.S., Boboila, C., Chiarle, R., Lewis, S. and Alt, F.W. (2010) The role of mechanistic factors in promoting chromosomal translocations found in lymphoid and other cancers. Adv.Immunol., 106, 93-133.