Classical and Alternative End-Joining Pathways for Repair of Lymphocyte-Specific and General DNA Double-Strand Breaks

Advances in Immunology

Volumn 116, Issue , 2012, Pages 1-49

  Boboila, Cristian ^a,b   Alt, Frederick W ^a,b   Schwer, Bjoern ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Alternative end joining; Chromosomal translocations; DNA breaks; DNA damage; DNA repair; IgH class switch recombination; Nonhomologous end joining; V(D)J recombination

Indexed keywords

ATM PROTEIN; DNA; IMMUNOGLOBULIN HEAVY CHAIN; UNCLASSIFIED DRUG; XRCC4 LIKE FACTOR; XRCC4 PROTEIN;

ALTERNATIVE END JOINING; ARTICLE; B LYMPHOCYTE; CELLULAR IMMUNITY; CHROMOSOME TRANSLOCATION; CLASS SWITCH RECOMBINATION; CLASSICAL NONHOMOLOGOUS DNA END JOINING; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENOMIC INSTABILITY; HUMAN; IMMUNE SYSTEM; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; VDJ RECOMBINATION;

EID: 84867386682     PISSN: 00652776     EISSN: 15578445     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394300-2.00001-6     Document Type: Chapter

References (236)

1. Ahnesorg P., Smith P., Jackson S.P. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 2006, 124:301-313.
2. Alt F.W., Baltimore D. Joining of immunoglobulin heavy chain gene segments: Implications from a chromosome with evidence of three D-JH fusions. Proceedings of the National Academy of Sciences of the United States of America 1982, 79:4118-4122.
3. Alt F.W., Rosenberg N., Casanova R.J., Thomas E., Baltimore D. Immunoglobulin heavy-chain expression and class switching in a murine leukaemia cell line. Nature 1982, 296:325-331.
4. Alt F.W., Yancopoulos G.D., Blackwell T.K., Wood C., Thomas E., Boss M., et al. Ordered rearrangement of immunoglobulin heavy chain variable region segments. The EMBO Journal 1984, 3:1209-1219.
5. Audebert M., Salles B., Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. The Journal of Biological Chemistry 2004, 279:55117-55126.
6. Barlow C., Hirotsune S., Paylor R., Liyanage M., Eckhaus M., Collins F., et al. Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
7. Bassing C.H., Alt F.W. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst) 2004, 3:781-796.
8. Bassing C.H., Chua K.F., Sekiguchi J., Suh H., Whitlow S.R., Fleming J.C., et al. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:8173-8178.
9. Bassing C.H., Suh H., Ferguson D.O., Chua K.F., Manis J., Eckersdorff M., et al. Histone H2AX: A dosage-dependent suppressor of oncogenic translocations and tumors. Cell 2003, 114:359-370.
10. Basu U., Chaudhuri J., Alpert C., Dutt S., Ranganath S., Li G., et al. The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation. Nature 2005, 438:508-511.
11. Basu U., Meng F.L., Keim C., Grinstein V., Pefanis E., Eccleston J., et al. The RNA exosome targets the AID cytidine deaminase to both strands of transcribed duplex DNA substrates. Cell 2011, 144:353-363.
12. Bennardo N., Cheng A., Huang N., Stark J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genetics 2008, 4:e1000110.
13. Bentley J., Diggle C.P., Harnden P., Knowles M.A., Kiltie A.E. DNA double strand break repair in human bladder cancer is error prone and involves microhomology-associated end-joining. Nucleic Acids Research 2004, 32:5249-5259.
14. Bentley D.J., Harrison C., Ketchen A.M., Redhead N.J., Samuel K., Waterfall M., et al. DNA ligase I null mouse cells show normal DNA repair activity but altered DNA replication and reduced genome stability. Journal of Cell Science 2002, 115:1551-1561.
15. Bentley D., Selfridge J., Millar J.K., Samuel K., Hole N., Ansell J.D., et al. DNA ligase I is required for fetal liver erythropoiesis but is not essential for mammalian cell viability. Nature Genetics 1996, 13:489-491.
16. Blackwell T.K., Malynn B.A., Pollock R.R., Ferrier P., Covey L.R., Fulop G.M., et al. Isolation of scid pre-B cells that rearrange kappa light chain genes: Formation of normal signal and abnormal coding joins. The EMBO Journal 1989, 8:735-742.
17. Boboila C., Jankovic M., Yan C.T., Wang J.H., Wesemann D.R., Zhang T., et al. Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3034-3039.
18. Boboila C., Oksenych V., Gostissa M., Wang J.H., Zha S., Zhang Y., et al. Robust chromosomal DNA repair via alternative end-joining in the absence of X-ray repair cross-complementing protein 1 (XRCC1). Proceedings of the National Academy of Sciences of the United States of America 2012, 109:2473-2478.
19. Boboila C., Yan C., Wesemann D.R., Jankovic M., Wang J.H., Manis J., et al. Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. The Journal of Experimental Medicine 2010, 207:417-427.
20. Borghesani P.R., Alt F.W., Bottaro A., Davidson L., Aksoy S., Rathbun G.A., et al. Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:3336-3341.
21. Bosma M.J. B and T cell leakiness in the scid mouse mutant. Immunodeficiency Reviews 1992, 3:261-276.
22. Bosma G.C., Custer R.P., Bosma M.J. A severe combined immunodeficiency mutation in the mouse. Nature 1983, 301:527-530.
23. Bosma G.C., Kim J., Urich T., Fath D.M., Cotticelli M.G., Ruetsch N.R., et al. DNA-dependent protein kinase activity is not required for immunoglobulin class switching. The Journal of Experimental Medicine 2002, 196:1483-1495.
24. Bothmer A., Robbiani D.F., Di Virgilio M., Bunting S.F., Klein I.A., Feldhahn N., et al. Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Molecular Cell 2011, 42:319-329.
25. Bothmer A., Robbiani D.F., Feldhahn N., Gazumyan A., Nussenzweig A., Nussenzweig M.C. 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination. The Journal of Experimental Medicine 2010, 207:855-865.
26. Boulton S.J., Jackson S.P. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. The EMBO Journal 1996, 15:5093-5103.
27. Bredemeyer A.L., Sharma G.G., Huang C.-Y., Helmink B.A., Walker L.M., Khor K.C., et al. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 2006, 442:466-470.
28. Buck D., Malivert L., de Chasseval R., Barraud A., Fondanèche M.-C., Sanal O., et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006, 124:287-299.
29. Buck D., Moshous D., de Chasseval R., Ma Y., Le Deist F., Cavazzana-Calvo M., et al. Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV. European Journal of Immunology 2006, 36:224-235.
30. Bunting S.F., Callen E., Wong N., Chen H.-T., Polato F., Gunn A., et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010, 141:243-254.
31. Caldecott K.W. XRCC1 and DNA strand break repair. DNA Repair (Amst) 2003, 2:955-969.
32. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Molecular and Cellular Biology 1994, 14:68-76.
33. Callebaut I., Malivert L., Fischer A., Mornon J.P., Revy P., de Villartay J.P. Cernunnos interacts with the XRCC4 x DNA-ligase IV complex and is homologous to the yeast nonhomologous end-joining factor Nej1. The Journal of Biological Chemistry 2006, 281:13857-13860.
34. Callén E., Jankovic M., Difilippantonio S., Daniel J.A., Chen H.-T., Celeste A., et al. ATM prevents the persistence and propagation of chromosome breaks in lymphocytes. Cell 2007, 130:63-75.
35. Callen E., Jankovic M., Wong N., Zha S., Chen H.-T., Difilippantonio S., et al. Essential role for DNA-PKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Molecular Cell 2009, 34:285-297.
36. Casellas R., Nussenzweig A., Wuerffel R., Pelanda R., Reichlin A., Suh H., et al. Ku80 is required for immunoglobulin isotype switching. The EMBO Journal 1998, 17:2404-2411.
37. Catalan N., Selz F., Imai K., Revy P., Fischer A., Durandy A. The block in immunoglobulin class switch recombination caused by activation-induced cytidine deaminase deficiency occurs prior to the generation of DNA double strand breaks in switch mu region. Journal of Immunology 2003, 171:2504-2509.
38. Celeste A., Difilippantonio S., Difilippantonio M.J., Fernandez-Capetillo O., Pilch D.R., Sedelnikova O.A., et al. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 2003, 114:371-383.
39. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., et al. Genomic instability in mice lacking histone H2AX. Science 2002, 296:922-927.
40. Charbonnel C., Gallego M.E., White C.I. Xrcc1-dependent and Ku-dependent DNA double-strand break repair kinetics in Arabidopsis plants. The Plant Journal 2010, 64:280-290.
41. Chaudhuri J., Alt F.W. Class-switch recombination: Interplay of transcription, DNA deamination and DNA repair. Nature Reviews. Immunology 2004, 4:541-552.
42. Chaudhuri J., Basu U., Zarrin A., Yan C., Franco S., Perlot T., et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Advances in Immunology 2007, 94:157-214.
43. Chaudhuri J., Tian M., Khuong C., Chua K., Pinaud E., Alt F.W. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 2003, 422:726-730.
44. Cheng H.L., Vuong B.Q., Basu U., Franklin A., Schwer B., Astarita J., et al. Integrity of the AID serine-38 phosphorylation site is critical for class switch recombination and somatic hypermutation in mice. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:2717-2722.
45. Chiarle R., Zhang Y., Frock R.L., Lewis S.M., Molinie B., Ho Y.J., et al. Genome-wide translocation sequencing reveals mechanisms of chromosome breaks and rearrangements in B cells. Cell 2011, 147:107-119.
46. Ciccia A., Elledge S.J. The DNA damage response: Making it safe to play with knives. Molecular Cell 2010, 40:179-204.
47. Corneo B., Wendland R.L., Deriano L., Cui X., Klein I.A., Wong S.-Y., et al. Rag mutations reveal robust alternative end joining. Nature 2007, 449:483-486.
48. Cui X., Meek K. Linking double-stranded DNA breaks to the recombination activating gene complex directs repair to the nonhomologous end-joining pathway. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:17046-17051.
49. Custer R.P., Bosma G.C., Bosma M.J. Severe combined immunodeficiency (SCID) in the mouse. Pathology, reconstitution, neoplasms. The American Journal of Pathology 1985, 120:464-477.
50. Daley J.M., Wilson T.E. Rejoining of DNA double-strand breaks as a function of overhang length. Molecular and Cellular Biology 2005, 25:896-906.
51. Di Noia J.M., Neuberger M.S. Molecular mechanisms of antibody somatic hypermutation. Annual Review of Biochemistry 2007, 76:1-22.
52. Difilippantonio S., Gapud E., Wong N., Huang C.-Y., Mahowald G., Chen H.T., et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 2008, 456:529-533.
53. Difilippantonio M.J., Petersen S., Chen H.T., Johnson R., Jasin M., Kanaar R., et al. Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. The Journal of Experimental Medicine 2002, 196:469-480.
54. Difilippantonio M.J., Zhu J., Chen H.T., Meffre E., Nussenzweig M.C., Max E.E., et al. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 2000, 404:510-514.
55. Dinkelmann M., Spehalski E., Stoneham T., Buis J., Wu Y., Sekiguchi J.M., et al. Multiple functions of MRN in end-joining pathways during isotype class switching. Nature Structural & Molecular Biology 2009, 16:808-813.
56. Downs J.A., Nussenzweig M.C., Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 2007, 447:951-958.
57. Du L., Peng R., Bjorkman A., Filipe de Miranda N., Rosner C., Kotnis A., et al. Cernunnos influences human immunoglobulin class switch recombination and may be associated with B cell lymphomagenesis. The Journal of Experimental Medicine 2012, 209:291-305.
58. Dudley D.D., Chaudhuri J., Bassing C.H., Alt F.W. Mechanism and control of V(D)J recombination versus class switch recombination: Similarities and differences. Advances in Immunology 2005, 86:43-112.
59. Dudley D.D., Manis J.P., Zarrin A.A., Kaylor L., Tian M., Alt F.W. Internal IgH class switch region deletions are position-independent and enhanced by AID expression. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:9984-9989.
60. Dunnick W., Hertz G.Z., Scappino L., Gritzmacher C. DNA sequences at immunoglobulin switch region recombination sites. Nucleic Acids Research 1993, 21:365-372.
61. Elliott B., Richardson C., Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Molecular Cell 2005, 17:885-894.
62. Errami A., He D.M., Friedl A.A., Overkamp W.J., Morolli B., Hendrickson E.A., et al. XR-C1, a new CHO cell mutant which is defective in DNA-PKcs, is impaired in both V(D)J coding and signal joint formation. Nucleic Acids Research 1998, 26:3146-3153.
63. Ferguson D.O., Alt F.W. DNA double strand break repair and chromosomal translocation: Lessons from animal models. Oncogene 2001, 20:5572-5579.
64. Ferguson D.O., Sekiguchi J.M., Chang S., Frank K.M., Gao Y., DePinho R.A., et al. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:6630-6633.
65. Franco S., Alt F.W., Manis J.P. Pathways that suppress programmed DNA breaks from progressing to chromosomal breaks and translocations. DNA Repair (Amst) 2006, 5:1030-1041.
66. Franco S., Gostissa M., Zha S., Lombard D.B., Murphy M.M., Zarrin A.A., et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Molecular Cell 2006, 21:201-214.
67. Franco S., Murphy M.M., Li G., Borjeson T., Boboila C., Alt F.W. DNA-PKcs and Artemis function in the end-joining phase of immunoglobulin heavy chain class switch recombination. The Journal of Experimental Medicine 2008, 205:557-564.
68. Frank K.M., Sekiguchi J.M., Seidl K.J., Swat W., Rathbun G.A., Cheng H.L., et al. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 1998, 396:173-177.
69. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Ferguson D.O., Zhu C., et al. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Molecular Cell 2000, 5:993-1002.
70. Fukumura R., Araki R., Fujimori A., Mori M., Saito T., Watanabe F., et al. Murine cell line SX9 bearing a mutation in the dna-pkcs gene exhibits aberrant V(D)J recombination not only in the coding joint but also in the signal joint. The Journal of Biological Chemistry 1998, 273:13058-13064.
71. Fukumura R., Araki R., Fujimori A., Tsutsumi Y., Kurimasa A., Li G.C., et al. Signal joint formation is also impaired in DNA-dependent protein kinase catalytic subunit knockout cells. Journal of Immunology 2000, 165:3883-3889.
72. Gao Y., Chaudhuri J., Zhu C., Davidson L., Weaver D.T., Alt F.W. A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity 1998, 9:367-376.
73. Gao Y., Ferguson D.O., Xie W., Manis J.P., Sekiguchi J., Frank K.M., et al. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 2000, 404:897-900.
74. Gao Y., Katyal S., Lee Y., Zhao J., Rehg J.E., Russell H.R., et al. DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 2011, 471:240-244.
75. Gao Y., Sun Y., Frank K.M., Dikkes P., Fujiwara Y., Seidl K.J., et al. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 1998, 95:891-902.
76. Gapud E.J., Dorsett Y., Yin B., Callen E., Bredemeyer A., Mahowald G.K., et al. Ataxia telangiectasia mutated (Atm) and DNA-PKcs kinases have overlapping activities during chromosomal signal joint formation. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:2022-2027.
77. Gilfillan S., Dierich A., Lemeur M., Benoist C., Mathis D. Mice lacking TdT: Mature animals with an immature lymphocyte repertoire. Science 1993, 261:1175-1178.
78. Gostissa M., Alt F.W., Chiarle R. Mechanisms that promote and suppress chromosomal translocations in lymphocytes. Annual Review of Immunology 2011, 29:319-350.
79. Gostissa M., Ranganath S., Bianco J., Alt F. Chromosomal location targets different MYC family gene members for oncogenic translocations. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:2265-2270.
80. Gu J., Lu H., Tippin B., Shimazaki N., Goodman M.F., Lieber M.R. XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. The EMBO Journal 2007, 26:1010-1023.
81. Gu J., Lu H., Tsai A.G., Schwarz K., Lieber M.R. Single-stranded DNA ligation and XLF-stimulated incompatible DNA end ligation by the XRCC4-DNA ligase IV complex: Influence of terminal DNA sequence. Nucleic Acids Research 2007, 35:5755-5762.
82. Gu Y., Seidl K.J., Rathbun G.A., Zhu C., Manis J.P., van der Stoep N., et al. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 1997, 7:653-665.
83. Gu H., Zou Y.R., Rajewsky K. Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 1993, 73:1155-1164.
84. Guirouilh-Barbat J., Huck S., Bertrand P., Pirzio L., Desmaze C., Sabatier L., et al. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Molecular Cell 2004, 14:611-623.
85. Guirouilh-Barbat J., Rass E., Plo I., Bertrand P., Lopez B.S. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:20902-20907.
86. Haber J.E. Alternative endings. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:405-406.
87. Han L., Mao W., Yu K. X-ray repair cross-complementing protein 1 (XRCC1) deficiency enhances class switch recombination and is permissive for alternative end joining. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:4604-4608.
88. Han L., Yu K. Altered kinetics of nonhomologous end joining and class switch recombination in ligase IV-deficient B cells. The Journal of Experimental Medicine 2008, 205:2745-2753.
89. Helmink B.A., Sleckman B.P. The response to and repair of RAG-mediated DNA double-strand breaks. Annual Review of Immunology 2012, 30:175-202.
90. Helmink B.A., Tubbs A.T., Dorsett Y., Bednarski J.J., Walker L.M., Feng Z., et al. H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature 2011, 469:245-249.
91. Heyer W.D., Ehmsen K.T., Liu J. Regulation of homologous recombination in eukaryotes. Annual Review of Genetics 2010, 44:113-139.
92. Hill D.A., Wang S.S., Cerhan J.R., Davis S., Cozen W., Severson R.K., et al. Risk of non-Hodgkin lymphoma (NHL) in relation to germline variation in DNA repair and related genes. Blood 2006, 108:3161-3167.
93. Honjo T., Alt F.W., Neuberger M. Molecular biology of B cells 2004, Elsevier Academic Press, London, UK.
94. Hopkins B.B., Paull T.T. The P. furiosus mre11/rad50 complex promotes 5' strand resection at a DNA double-strand break. Cell 2008, 135:250-260.
95. Huber A., Bai P., de Murcia J.M., de Murcia G. PARP-1, PARP-2 and ATM in the DNA damage response: Functional synergy in mouse development. DNA Repair (Amst) 2004, 3:1103-1108.
96. Iwasato T., Shimizu A., Honjo T., Yamagishi H. Circular DNA is excised by immunoglobulin class switch recombination. Cell 1990, 62:143-149.
97. Jung D., Giallourakis C., Mostoslavsky R., Alt F.W. Mechanism and control of V(D)J recombination at the immunoglobulin heavy chain locus. Annual Review of Immunology 2006, 24:541-570.
98. Kabotyanski E.B., Gomelsky L., Han J.O., Stamato T.D., Roth D.B. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Research 1998, 26:5333-5342.
99. Kiefer K., Oshinsky J., Kim J., Nakajima P.B., Bosma G.C., Bosma M.J. The catalytic subunit of DNA-protein kinase (DNA-PKcs) is not required for Ig class-switch recombination. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:2843-2848.
100. Kitada K., Yamasaki T. The MDR1/ABCB1 regional amplification in large inverted repeats with asymmetric sequences and microhomologies at the junction sites. Cancer Genetics and Cytogenetics 2007, 178:120-127.
101. Kitagawa R., Bakkenist C.J., McKinnon P.J., Kastan M.B. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes & Development 2004, 18:1423-1438.
102. Kohl N.E., Kanda N., Schreck R.R., Bruns G., Latt S.A., Gilbert F., et al. Transposition and amplification of oncogene-related sequences in human neuroblastomas. Cell 1983, 35:359-367.
103. Komori T., Okada A., Stewart V., Alt F.W. Lack of N regions in antigen receptor variable region genes of TdT-deficient lymphocytes. Science 1993, 261:1171-1175.
104. Komori T., Pricop L., Hatakeyama A., Bona C.A., Alt F.W. Repertoires of antigen receptors in Tdt congenitally deficient mice. International Reviews of Immunology 1996, 13:317-325.
105. Kuehl W.M., Bergsagel P.L. Multiple myeloma: Evolving genetic events and host interactions. Nature Reviews. Cancer 2002, 2:175-187.
106. Küppers R., Dalla-Favera R. Mechanisms of chromosomal translocations in B cell lymphomas. Oncogene 2001, 20:5580-5594.
107. Kurimasa A., Kumano S., Boubnov N.V., Story M.D., Tung C.S., Peterson S.R., et al. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Molecular and Cellular Biology 1999, 19:3877-3884.
108. Kurimasa A., Ouyang H., Dong L.J., Wang S., Li X., Cordon-Cardo C., et al. Catalytic subunit of DNA-dependent protein kinase: Impact on lymphocyte development and tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:1403-1408.
109. Lakshmipathy U., Campbell C. The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Molecular and Cellular Biology 1999, 19:3869-3876.
110. Lakshmipathy U., Campbell C. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Research 2000, 28:3880-3886.
111. Lavin M.F. Ataxia-telangiectasia: From a rare disorder to a paradigm for cell signalling and cancer. Nature Reviews. Molecular Cell Biology 2008, 9:759-769.
112. Lee Y., Katyal S., Li Y., El-Khamisy S.F., Russell H.R., Caldecott K.W., et al. The genesis of cerebellar interneurons and the prevention of neural DNA damage require XRCC1. Nature Neuroscience 2009, 12:973-980.
113. Lee G.S., Neiditch M.B., Salus S.S., Roth D.B. RAG proteins shepherd double-strand breaks to a specific pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 2004, 117:171-184.
114. Lee-Theilen M., Matthews A.J., Kelly D., Zheng S., Chaudhuri J. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nature Structural & Molecular Biology 2011, 18:75-79.
115. Li G., Alt F.W., Cheng H.-L., Brush J.W., Goff P.H., Murphy M.M., et al. Lymphocyte-specific compensation for XLF/cernunnos end-joining functions in V(D)J recombination. Molecular Cell 2008, 31:631-640.
116. Li Z., Otevrel T., Gao Y., Cheng H.L., Seed B., Stamato T.D., et al. The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell 1995, 83:1079-1089.
117. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annual Review of Biochemistry 2010, 79:181-211.
118. Lieber M.R., Hesse J.E., Lewis S., Bosma G.C., Rosenberg N., Mizuuchi K., et al. The defect in murine severe combined immune deficiency: Joining of signal sequences but not coding segments in V(D)J recombination. Cell 1988, 55:7-16.
119. Lieber M.R., Lu H., Gu J., Schwarz K. Flexibility in the order of action and in the enzymology of the nuclease, polymerases, and ligase of vertebrate non-homologous DNA end joining: Relevance to cancer, aging, and the immune system. Cell Research 2008, 18:125-133.
120. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Molecular Cell 2007, 28:134-146.
121. Liu X., Jiang W., Dubois R.L., Yamamoto K., Wolner Z., Zha S. Overlapping functions between XLF repair protein and 53BP1 DNA damage response factor in end joining and lymphocyte development. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:3903-3908.
122. Lou Z., Minter-Dykhouse K., Franco S., Gostissa M., Rivera M.A., Celeste A., et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Molecular Cell 2006, 21:187-200.
123. Lumsden J.M., McCarty T., Petiniot L.K., Shen R., Barlow C., Wynn T.A., et al. Immunoglobulin class switch recombination is impaired in Atm-deficient mice. The Journal of Experimental Medicine 2004, 200:1111-1121.
124. Ma J.L., Kim E.M., Haber J.E., Lee S.E. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Molecular and Cellular Biology 2003, 23:8820-8828.
125. Ma Y., Pannicke U., Schwarz K., Lieber M.R. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 2002, 108:781-794.
126. Malynn B.A., Blackwell T.K., Fulop G.M., Rathbun G.A., Furley A.J., Ferrier P., et al. The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell 1988, 54:453-460.
127. Manis J.P., Dudley D., Kaylor L., Alt F.W. IgH class switch recombination to IgG1 in DNA-PKcs-deficient B cells. Immunity 2002, 16:607-617.
128. Manis J.P., Gu Y., Lansford R., Sonoda E., Ferrini R., Davidson L., et al. Ku70 is required for late B cell development and immunoglobulin heavy chain class switching. The Journal of Experimental Medicine 1998, 187:2081-2089.
129. Manis J.P., Morales J.C., Xia Z., Kutok J.L., Alt F.W., Carpenter P.B. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nature Immunology 2004, 5:481-487.
130. Mansour W.Y., Rhein T., Dahm-Daphi J. The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Research 2010, 38:6065-6077.
131. Martin-Subero J.I., Odero M.D., Hernandez R., Cigudosa J.C., Agirre X., Saez B., et al. Amplification of IGH/MYC fusion in clinically aggressive IGH/BCL2-positive germinal center B-cell lymphomas. Genes, Chromosomes & Cancer 2005, 43:414-423.
132. Mattarucchi E., Guerini V., Rambaldi A., Campiotti L., Venco A., Pasquali F., et al. Microhomologies and interspersed repeat elements at genomic breakpoints in chronic myeloid leukemia. Genes, Chromosomes & Cancer 2008, 47:625-632.
133. McBlane J.F., van Gent D.C., Ramsden D.A., Romeo C., Cuomo C.A., Gellert M., et al. Cleavage at a V(D)J recombination signal requires only RAG1 and RAG2 proteins and occurs in two steps. Cell 1995, 83:387-395.
134. McVey M., Lee S.E. MMEJ repair of double-strand breaks (director's cut): Deleted sequences and alternative endings. Trends in Genetics 2008, 24:529-538.
135. Menissier de Murcia J., Ricoul M., Tartier L., Niedergang C., Huber A., Dantzer F., et al. Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. The EMBO Journal 2003, 22:2255-2263.
136. Mills K.D., Ferguson D.O., Alt F.W. The role of DNA breaks in genomic instability and tumorigenesis. Immunological Reviews 2003, 194:77-95.
137. Mills K.D., Ferguson D.O., Essers J., Eckersdorff M., Kanaar R., Alt F.W. Rad54 and DNA ligase IV cooperate to maintain mammalian chromatid stability. Genes & Development 2004, 18:1283-1292.
138. Mladenov E., Iliakis G. Induction and repair of DNA double strand breaks: The increasing spectrum of non-homologous end joining pathways. Mutation Research 2011, 711:61-72.
139. Morales J.C., Franco S., Murphy M.M., Bassing C.H., Mills K.D., Adams M.M., et al. 53BP1 and p53 synergize to suppress genomic instability and lymphomagenesis. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:3310-3315.
140. Moshous D., Callebaut I., de Chasseval R., Corneo B., Cavazzana-Calvo M., Le Deist F., et al. Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001, 105:177-186.
141. Moshous D., Pannetier C., Chasseval Rd R., Deist Fl F., Cavazzana-Calvo M., Romana S., et al. Partial T and B lymphocyte immunodeficiency and predisposition to lymphoma in patients with hypomorphic mutations in Artemis. The Journal of Clinical Investigation 2003, 111:381-387.
142. Muramatsu M., Kinoshita K., Fagarasan S., Yamada S., Shinkai Y., Honjo T. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 2000, 102:553-563.
143. Neal J.A., Meek K. Choosing the right path: Does DNA-PK help make the decision?. Mutation Research 2011, 711:73-86.
144. Nussenzweig A., Chen C., da Costa Soares V., Sanchez M., Sokol K., Nussenzweig M.C., et al. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 1996, 382:551-555.
145. Nussenzweig A., Nussenzweig M.C. A backup DNA repair pathway moves to the forefront. Cell 2007, 131:223-225.
146. Oettinger M.A., Schatz D.G., Gorka C., Baltimore D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 1990, 248:1517-1523.
147. Oksenych V., Alt F.W., Kumar V., Schwer B., Wesemann D.R., Hansen E., et al. Functional redundancy between repair factor XLF and damage response mediator 53BP1 in V(D)J recombination and DNA repair. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:2455-2460.
148. Pan-Hammarstrom Q., Jones A.M., Lahdesmaki A., Zhou W., Gatti R.A., Hammarstrom L., et al. Impact of DNA ligase IV on nonhomologous end joining pathways during class switch recombination in human cells. The Journal of Experimental Medicine 2005, 201:189-194.
149. Paull T.T., Gellert M. The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Molecular Cell 1998, 1:969-979.
150. Paull T.T., Gellert M. A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:6409-6414.
151. Pavri R., Gazumyan A., Jankovic M., Di Virgilio M., Klein I., Ansarah-Sobrinho C., et al. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 2010, 143:122-133.
152. Perlot T., Alt F.W. Cis-regulatory elements and epigenetic changes control genomic rearrangements of the IgH locus. Advances in Immunology 2008, 99:1-32.
153. Petersen S., Casellas R., Reina-San-Martin B., Chen H.T., Difilippantonio M.J., Wilson P.C., et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 2001, 414:660-665.
154. Petrini J.H., Donovan J.W., Dimare C., Weaver D.T. Normal V(D)J coding junction formation in DNA ligase I deficiency syndromes. Journal of Immunology 1994, 152:176-183.
155. Petrini J.H., Xiao Y., Weaver D.T. DNA ligase I mediates essential functions in mammalian cells. Molecular and Cellular Biology 1995, 15:4303-4308.
156. Puebla-Osorio N., Lacey D.B., Alt F.W., Zhu C. Early embryonic lethality due to targeted inactivation of DNA ligase III. Molecular and Cellular Biology 2006, 26:3935-3941.
157. Ramiro A.R., Jankovic M., Callen E., Difilippantonio S., Chen H.-T., Mcbride K.M., et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 2006, 440:105-109.
158. Ramiro A.R., Jankovic M., Eisenreich T., Difilippantonio S., Chen-Kiang S., Muramatsu M., et al. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 2004, 118:431-438.
159. Reina-San-Martin B., Chen H.T., Nussenzweig A., Nussenzweig M.C. ATM is required for efficient recombination between immunoglobulin switch regions. The Journal of Experimental Medicine 2004, 200:1103-1110.
160. Reina-San-Martin B., Chen J., Nussenzweig A., Nussenzweig M.C. Enhanced intra-switch region recombination during immunoglobulin class switch recombination in 53BP1-/- B cells. European Journal of Immunology 2007, 37:235-239.
161. Reina-San-Martin B., Difilippantonio S., Hanitsch L., Masilamani R.F., Nussenzweig A., Nussenzweig M.C. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. The Journal of Experimental Medicine 2003, 197:1767-1778.
162. Riballo E., Kuhne M., Rief N., Doherty A., Smith G.C., Recio M.J., et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Molecular Cell 2004, 16:715-724.
163. Rivera-Munoz P., Soulas-Sprauel P., Le Guyader G., Abramowski V., Bruneau S., Fischer A., et al. Reduced immunoglobulin class switch recombination in the absence of Artemis. Blood 2009, 114:3601-3609.
164. Robert I., Dantzer F., Reina-San-Martin B. Parp1 facilitates alternative NHEJ, whereas Parp2 suppresses IgH/c-myc translocations during immunoglobulin class switch recombination. The Journal of Experimental Medicine 2009, 206:1047-1056.
165. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. The Journal of Cell Biology 1999, 146:905-916.
166. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. The Journal of Biological Chemistry 1998, 273:5858-5868.
167. Rooney S., Alt F.W., Lombard D., Whitlow S., Eckersdorff M., Fleming J., et al. Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. The Journal of Experimental Medicine 2003, 197:553-565.
168. Rooney S., Alt F.W., Sekiguchi J., Manis J.P. Artemis-independent functions of DNA-dependent protein kinase in Ig heavy chain class switch recombination and development. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:2471-2475.
169. Rooney S., Chaudhuri J., Alt F.W. The role of the non-homologous end-joining pathway in lymphocyte development. Immunology Reviews 2004, 200:115-131.
170. Rooney S., Sekiguchi J., Whitlow S., Eckersdorff M., Manis J.P., Lee C., et al. Artemis and p53 cooperate to suppress oncogenic N-myc amplification in progenitor B cells. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:2410-2415.
171. Rooney S., Sekiguchi J., Zhu C., Cheng H.L., Manis J., Whitlow S., et al. Leaky SCID phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Molecular Cell 2002, 10:1379-1390.
172. Rucci F., Notarangelo L.D., Fazeli A., Patrizi L., Hickernell T., Paganini T., et al. Homozygous DNA ligase IV R278H mutation in mice leads to leaky SCID and represents a model for human LIG4 syndrome. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:3024-3029.
173. Saribasak H., Maul R.W., Cao Z., McClure R.L., Yang W., McNeill D.R., et al. XRCC1 suppresses somatic hypermutation and promotes alternative nonhomologous end joining in Igh genes. The Journal of Experimental Medicine 2011, 208:2209-2216.
174. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., et al. Human CtIP promotes DNA end resection. Nature 2007, 450:509-514.
175. Schatz D.G., Oettinger M.A., Baltimore D. The V(D)J recombination activating gene, RAG-1. Cell 1989, 59:1035-1048.
176. Schatz D.G., Swanson P.C. V(D)J recombination: Mechanisms of initiation. Annual Review of Genetics 2011, 45:167-202.
177. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nature Reviews. Cancer 2003, 3:155-168.
178. Shockett P., Stavnezer J. Inhibitors of poly(ADP-ribose) polymerase increase antibody class switching. Journal of Immunology 1993, 151:6962-6976.
179. Simsek D., Brunet E., Wong S.Y., Katyal S., Gao Y., McKinnon P.J., et al. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genetics 2011, 7:e1002080.
180. Simsek D., Furda A., Gao Y., Artus J., Brunet E., Hadjantonakis A.K., et al. Crucial role for DNA ligase III in mitochondria but not in Xrcc1-dependent repair. Nature 2011, 471:245-248.
181. Simsek D., Jasin M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nature Structural & Molecular Biology 2010, 17:410-416.
182. Stavnezer J., Bjorkman A., Du L., Cagigi A., Pan-Hammarstrom Q. Mapping of switch recombination junctions, a tool for studying DNA repair pathways during immunoglobulin class switching. Advances in Immunology 2010, 108:45-109.
183. Stracker T.H., Petrini J.H. The MRE11 complex: Starting from the ends. Nature Reviews. Molecular Cell Biology 2011, 12:90-103.
184. Sugawara N., Ira G., Haber J.E. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Molecular and Cellular Biology 2000, 20:5300-5309.
185. Taccioli G.E., Amatucci A.G., Beamish H.J., Gell D., Xiang X.H., Torres Arzayus M.I., et al. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity 1998, 9:355-366.
186. Taccioli G.E., Cheng H.L., Varghese A.J., Whitmore G., Alt F.W. A DNA repair defect in Chinese hamster ovary cells affects V(D)J recombination similarly to the murine scid mutation. The Journal of Biological Chemistry 1994, 269:7439-7442.
187. Taccioli G.E., Gottlieb T.M., Blunt T., Priestley A., Demengeot J., Mizuta R., et al. Ku80: Product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 1994, 265:1442-1445.
188. Taccioli G.E., Rathbun G., Oltz E., Stamato T., Jeggo P.A., Alt F.W. Impairment of V(D)J recombination in double-strand break repair mutants. Science 1993, 260:207-210.
189. Takeda S., Nakamura K., Taniguchi Y., Paull T.T. Ctp1/CtIP and the MRN complex collaborate in the initial steps of homologous recombination. Molecular Cell 2007, 28:351-352.
190. Tebbs R.S., Flannery M.L., Meneses J.J., Hartmann A., Tucker J.D., Thompson L.H., et al. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Developmental Biology 1999, 208:513-529.
191. Tian M., Alt F.W. Transcription-induced cleavage of immunoglobulin switch regions by nucleotide excision repair nucleases in vitro. The Journal of Biological Chemistry 2000, 275:24163-24172.
192. Timson D.J., Singleton M.R., Wigley D.B. DNA ligases in the repair and replication of DNA. Mutation Research 2000, 460:301-318.
193. Tobin L.A., Robert C., Nagaria P., Chumsri S., Twaddell W., Ioffe O.B., et al. Targeting abnormal DNA repair in therapy-resistant breast cancers. Molecular Cancer Research 2012, 10:96-107.
194. Tobin L.A., Robert C., Rapoport A.P., Gojo I., Baer M.R., Tomkinson A.E., et al. Targeting abnormal DNA double-strand break repair in tyrosine kinase inhibitor-resistant chronic myeloid leukemias. Oncogene 2012, 10.1038/onc.2012.203.
195. Tomimatsu N., Mukherjee B., Burma S. Distinct roles of ATR and DNA-PKcs in triggering DNA damage responses in ATM-deficient cells. EMBO Reports 2009, 10:629-635.
196. Tomkinson A.E., Vijayakumar S., Pascal J.M., Ellenberger T. DNA ligases: Structure, reaction mechanism, and function. Chemical Reviews 2006, 106:687-699.
197. Tonegawa S. Somatic generation of antibody diversity. Nature 1983, 302:575-581.
198. Tonegawa S., Brack C., Hozumi N., Pirrotta V. Organization of immunoglobulin genes. Cold Spring Harbor Symposia on Quantitative Biology 1978, 42(Pt 2):921-931.
199. Tsai C.J., Kim S.A., Chu G. Cernunnos/XLF promotes the ligation of mismatched and noncohesive DNA ends. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7851-7856.
200. van den Bosch M., Bree R.T., Lowndes N.F. The MRN complex: Coordinating and mediating the response to broken chromosomes. EMBO Reports 2003, 4:844-849.
201. Verkaik N.S., Esveldt-van Lange R.E.E., van Heemst D., Brüggenwirth H.T., Hoeijmakers J.H.J., Zdzienicka M.Z., et al. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. European Journal of Immunology 2002, 32:701-709.
202. Wang J.H., Alt F.W., Gostissa M., Datta A., Murphy M., Alimzhanov M.B., et al. Oncogenic transformation in the absence of Xrcc4 targets peripheral B cells that have undergone editing and switching. The Journal of Experimental Medicine 2008, 205:3079-3090.
203. Wang Y., Ghosh G., Hendrickson E.A. Ku86 represses lethal telomere deletion events in human somatic cells. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:12430-12435.
204. Wang J.H., Gostissa M., Yan C.T., Goff P., Hickernell T., Hansen E., et al. Mechanisms promoting translocations in editing and switching peripheral B cells. Nature 2009, 460:231-236.
205. Wang H., Perrault A.R., Takeda Y., Qin W., Wang H., Iliakis G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Research 2003, 31:5377-5388.
206. Wang H., Rosidi B., Perrault R., Wang M., Zhang L., Windhofer F., et al. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Research 2005, 65:4020-4030.
207. Wang M., Wu W., Wu W., Rosidi B., Zhang L., Wang H., et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Research 2006, 34:6170-6182.
208. Ward I.M., Minn K., van Deursen J., Chen J. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Molecular and Cellular Biology 2003, 23:2556-2563.
209. Ward I.M., Reina-San-Martin B., Olaru A., Minn K., Tamada K., Lau J.S., et al. 53BP1 is required for class switch recombination. The Journal of Cell Biology 2004, 165:459-464.
210. Weinstock D.M., Richardson C.A., Elliott B., Jasin M. Modeling oncogenic translocations: Distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amst) 2006, 5:1065-1074.
211. Weterings E., Chen D.J. DNA-dependent protein kinase in nonhomologous end joining: A lock with multiple keys?. The Journal of Cell Biology 2007, 179:183-186.
212. Windhofer F., Krause S., Hader C., Schulz W.A., Florl A.R. Distinctive differences in DNA double-strand break repair between normal urothelial and urothelial carcinoma cells. Mutation Research 2008, 638:56-65.
213. Xie A., Hartlerode A., Stucki M., Odate S., Puget N., Kwok A., et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Molecular Cell 2007, 28:1045-1057.
214. Xie A., Kwok A., Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nature Structural & Molecular Biology 2009, 16:814-818.
215. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes & Development 1996, 10:2411-2422.
216. Yan C.T., Boboila C., Souza E.K., Franco S., Hickernell T.R., Murphy M., et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007, 449:478-482.
217. Yan C.T., Kaushal D., Murphy M., Zhang Y., Datta A., Chen C., et al. XRCC4 suppresses medulloblastomas with recurrent translocations in p53-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:7378-7383.
218. Yancopoulos G.D., Alt F.W. Developmentally controlled and tissue-specific expression of unrearranged VH gene segments. Cell 1985, 40:271-281.
219. Yancopoulos G.D., DePinho R.A., Zimmerman K.A., Lutzker S.G., Rosenberg N., Alt F.W. Secondary genomic rearrangement events in pre-B cells: VHDJH replacement by a LINE-1 sequence and directed class switching. The EMBO Journal 1986, 5:3259-3266.
220. Yu K., Chedin F., Hsieh C.-L., Wilson T.E., Lieber M.R. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nature Immunology 2003, 4:442-451.
221. Yun M.H., Hiom K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 2009, 459:460-463.
222. Zarrin A.A., Alt F.W., Chaudhuri J., Stokes N., Kaushal D., Du Pasquier L., et al. An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nature Immunology 2004, 5:1275-1281.
223. Zarrin A.A., Del Vecchio C., Tseng E., Gleason M., Zarin P., Tian M., et al. Antibody class switching mediated by yeast endonuclease-generated DNA breaks. Science 2007, 315:377-381.
224. Zha S., Alt F.W., Cheng H.L., Brush J.W., Li G. Defective DNA repair and increased genomic instability in Cernunnos-XLF-deficient murine ES cells. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4518-4523.
225. Zha S., Bassing C.H., Sanda T., Brush J.W., Patel H., Goff P.H., et al. ATM-deficient thymic lymphoma is associated with aberrant tcrd rearrangement and gene amplification. The Journal of Experimental Medicine 2010, 207:1369-1380.
226. Zha S., Boboila C., Alt F.W. Mre11: Roles in DNA repair beyond homologous recombination. Nature Structural & Molecular Biology 2009, 16:798-800.
227. Zha S., Guo C., Boboila C., Oksenych V., Cheng H.L., Zhang Y., et al. ATM damage response and XLF repair factor are functionally redundant in joining DNA breaks. Nature 2011, 469:250-254.
228. Zha S., Jiang W., Fujiwara Y., Patel H., Goff P.H., Brush J.W., et al. Ataxia telangiectasia-mutated protein and DNA-dependent protein kinase have complementary V(D)J recombination functions. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:2028-2033.
229. Zha S., Sekiguchi J., Brush J.W., Bassing C.H., Alt F.W. Complementary functions of ATM and H2AX in development and suppression of genomic instability. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:9302-9306.
230. Zhang Y., Gostissa M., Hildebrand D.G., Becker M.S., Boboila C., Chiarle R., et al. The role of mechanistic factors in promoting chromosomal translocations found in lymphoid and other cancers. Advances in Immunology 2010, 106:93-133.
231. Zhang Y., Jasin M. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nature Structural & Molecular Biology 2011, 18:80-84.
232. Zhang Y., McCord R.P., Ho Y.J., Lajoie B.R., Hildebrand D.G., Simon A.C., et al. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 2012, 148:908-921.
233. Zhang Y., Rowley J.D. Chromatin structural elements and chromosomal translocations in leukemia. DNA Repair (Amst) 2006, 5:1282-1297.
234. Zhu C., Bogue M.A., Lim D.S., Hasty P., Roth D.B. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 1996, 86:379-389.
235. Zhu C., Mills K.D., Ferguson D.O., Lee C., Manis J., Fleming J., et al. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002, 109:811-821.
236. Ziv Y., Bielopolski D., Galanty Y., Lukas C., Taya Y., Schultz D.C., et al. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nature Cell Biology 2006, 8:870-876.