Nonhomologous DNA end joining in cell-free extracts

Journal of Nucleic Acids

Volumn 2010, Issue , 2010, Pages

  Sharma, Sheetal ^a   Raghavan, Sathees C ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; AMMONIUM SULFATE; BUFFER; CHLOROFORM; DNA; GLYCOGEN; HYPOTONIC SOLUTION; KU ANTIGEN; PHENOL; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; XRCC4 PROTEIN;

CELL FREE SYSTEM; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; DNA END JOINING REPAIR; DNA STRAND BREAKAGE; DNA SYNTHESIS; ENZYME ACTIVITY; HUMAN; IN VITRO STUDY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOLVENT EXTRACTION;

EID: 79960607271     PISSN: 20900201     EISSN: 2090021X     Source Type: Journal    
DOI: 10.4061/2010/389129     Document Type: Review

References (102)

1. Lieber M. R., Yu K., Raghavan S. C., Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. DNA Repair 2006 5 9-10 1234 1245 2-s2.0-33748138991 10.1016/j.dnarep.2006.05.013 (Pubitemid 44308464)
2. Ferguson D. O., Alt F. W., DNA double strand break repair and chromosomal translocation: lessons from animal models. Oncogene 2001 20 40 5572 5579 2-s2.0-0035839840 10.1038/sj.onc.1204767 (Pubitemid 32928098)
3. 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
4. Hefferin M. L., Tomkinson A. E., Mechanism of DNA double-strand break repair by non-homologous end joining. DNA Repair 2005 4 6 639 648 2-s2.0-19344370467 10.1016/j.dnarep.2004.12.005 (Pubitemid 40720306)
5. Weterings E., Chen D. J., The endless tale of non-homologous end-joining. Cell Research 2008 18 1 114 124 2-s2.0-38049125555 10.1038/cr.2008.3
6. Wyman C., Kanaar R., DNA double-strand break repair: all's well that ends well. Annual Review of Genetics 2006 40 363 383 2-s2.0-33845604556 10.1146/annurev.genet.40.110405.090451 (Pubitemid 44956790)
7. Jackson S. P., Sensing and repairing DNA double-strand breaks. Carcinogenesis 2002 23 5 687 696 2-s2.0-0036261707 (Pubitemid 34567505)
8. Takata M., Sasaki M. S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S., Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO Journal 1998 17 18 5497 5508 2-s2.0-0032530658 10.1093/emboj/17.18. 5497 (Pubitemid 28427063)
9. Sonoda E., Sasaki M. S., Buerstedde J.-M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., Takeda S., Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO Journal 1998 17 2 598 608 2-s2.0-0032518657 10.1093/emboj/17.2.598 (Pubitemid 28045499)
10. Lieber M. R., Ma Y., Pannicke U., Schwarz K., Mechanism and regulation of human non-homologous DNA end-joining. Nature Reviews Molecular Cell Biology 2003 4 9 712 720 2-s2.0-0042839614 10.1038/nrm1202 (Pubitemid 37082186)
11. Hartlerode A. J., Scully R., Mechanisms of double-strand break repair in somatic mammalian cells. Biochemical Journal 2009 423 2 157 168 2-s2.0-70350088548 10.1042/BJ20090942
12. West S. C., Molecular views of recombination proteins and their control. Nature Reviews Molecular Cell Biology 2003 4 6 435 445 2-s2.0-0038700698 10.1038/nrm1127 (Pubitemid 36648589)
13. Chiruvella K. K., Sankaran S. K., Singh M., Nambiar M., Raghavan S. C., Mechanism of DNA Double-Strand Break Repair. The ICFAI Journal of Biotechnology 2007 1 7 22
14. Reeves W. H., Use of monoclonal antibodies for the characterization of novel DNA-binding proteins recognized by human autoimmune sera. Journal of Experimental Medicine 1985 161 1 18 39 2-s2.0-0022000813 (Pubitemid 15169718)
15. Mimori T., Hardin J. A., Steitz J. A., Characterization of the DNA-binding protein antigen Ku recognized by autoantibodies from patients with rheumatic disorders. Journal of Biological Chemistry 1986 261 5 2274 2278 2-s2.0-0023018810 (Pubitemid 17205158)
16. Dynan W. S., Yoo S., Interaction of Ku protein and DNA-dependent protein kinase catalytic subunit with nucleic acids. Nucleic Acids Research 1998 26 7 1551 1559 2-s2.0-0032052815 10.1093/nar/26.7.1551 (Pubitemid 28291787)
17. Walker A. I., Hunt T., Jackson R. J., Anderson C. W., Double-stranded DNA induces the phosphorylation of several proteins including the 90 000 mol. wt. heat-shock protein in animal cell extracts. EMBO Journal 1985 4 1 139 145 2-s2.0-0021980039
18. Smider V., Rathmell W. K., Lieber M. R., Chu G., Restoration of X-ray resistance and V(D)J recombination in mutant cells by Ku cDNA. Science 1994 266 5183 288 291 2-s2.0-0028112944 (Pubitemid 24343516)
19. Taccioli G. E., Gottlieb T. M., Blunt T., Priestley A., Demengeot J., Mizuta R., Lehmann A. R., Alt F. W., Jackson S. P., Jeggo P. A., Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 1994 265 5177 1442 1445 2-s2.0-0028025020 (Pubitemid 24306796)
20. Rathmell W. K., Chu G., Involvement of the Ku autoantigen in the cellular response to DNA double-strand breaks. Proceedings of the National Academy of Sciences of the United States of America 1994 91 16 7623 7627 2-s2.0-0027966126 10.1073/pnas.91.16.7623 (Pubitemid 24238237)
21. Jeggo P. A., DNA-PK: at the cross-roads of biochemistry and genetics. Mutation Research 1997 384 1 1 14 2-s2.0-0030922250 10.1016/S0921-8777(97)00009- 8 (Pubitemid 27248612)
22. Gu Y., Jin S., Gao Y., Weaver D. T., Alt F. W., Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proceedings of the National Academy of Sciences of the United States of America 1997 94 15 8076 8081 2-s2.0-0030858967 10.1073/pnas.94.15.8076 (Pubitemid 27343779)
23. Lees-Miller S. P., Godbout R., Chan D. W., Weinfeld M., Day R. S. III, Barron G. M., Allalunis-Turner J., Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 1995 267 5201 1183 1185 2-s2.0-0028937877
24. Chan D. W., Lees-Miller S. P., The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. Journal of Biological Chemistry 1996 271 15 8936 8941 2-s2.0-0030009738 10.1074/jbc.271.15.8936 (Pubitemid 26123320)
25. Rooney S., Sekiguchi J., Zhu C., Cheng H.-L., Manis J., Whitlow S., DeVido J., Foy D., Chaudhuri J., Lombard D., Alt F. W., Leaky Scid phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Molecular Cell 2002 10 6 1379 1390 2-s2.0-0036932453 10.1016/S1097-2765(02) 00755-4 (Pubitemid 36050879)
26. Blunt T., Finnie N. J., Taccioli G. E., Smith G. C. M., Demengeot J., Gottlieb T. M., Mizuta R., Varghese A. J., Ait F. W., Jeggo P. A., Jackson S. P., Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 1995 80 5 813 823 2-s2.0-0028960511
27. Karanjawala Z. E., Adachi N., Irvine R. A., Oh E. K., Shibata D., Schwarz K., Hsieh C.-L., Lieber M. R., The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Repair 2002 1 12 1017 1026 2-s2.0-0037027853 10.1016/S1568-7864(02)00151-9 (Pubitemid 35335827)
28. 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 3 379 389 2-s2.0-0030576534 10.1016/S0092-8674(00)80111-7 (Pubitemid 26272078)
29. Frank K. M., Sharpless N. E., Gao Y., Sekiguchi J. M., Ferguson D. O., Zhu C., Manis J. P., Horner J., DePinho R. A., Alt F. W., DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Molecular Cell 2000 5 6 993 1002 2-s2.0-0033634973
30. Robins P., Lindahl T., DNA ligase IV from HeLa cell nuclei. Journal of Biological Chemistry 1996 271 39 24257 24261 2-s2.0-0029817836 10.1074/jbc.271.39.24257 (Pubitemid 26327414)
31. Wilson T. E., Grawunder U., Lieber M. R., Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 1997 388 6641 495 498 2-s2.0-0030811523 10.1038/41365 (Pubitemid 27328930)
32. Grawunder U., Wilm M., Wu X., Kulesza P., Wilson T. E., Mann M., Lieber M. R., Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 1997 388 6641 492 495 2-s2.0-0030743386 10.1038/41358 (Pubitemid 27328929)
33. Critchlow S. E., Bowater R. P., Jackson S. P., Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Current Biology 1997 7 8 588 598 2-s2.0-0031214080 (Pubitemid 27335654)
34. Thompson L. H., Jeggo P. A., Nomenclature of human genes involved in ionizing radiation sensitivity. Mutation Research 1995 337 2 131 134 2-s2.0-0029121551 10.1016/0921-8777(95)00018-F
35. Jeggo P. A., Tesmer J., Chen D. J., Genetic analysis of ionising radiation sensitive mutants of cultured mammalian cell lines. Mutation Research 1991 254 2 125 133 2-s2.0-0025971104 10.1016/0921-8777(91)90003-8
36. Thacker J., Wilkinson R. E., The genetic basis of resistance to ionising radiation damage in cultured mammalian cells. Mutation Research 1991 254 2 135 142 2-s2.0-0026081668 10.1016/0921-8777(91)90004-9
37. 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 2 301 313 2-s2.0-31044432090 10.1016/j.cell.2005.12.031 (Pubitemid 43121979)
38. Buck D., Malivert L., de Chasseval R., Barraud A., Fondanèche M.-C., Sanal O., Plebani A., Stéphan J.-L., Hufnagel M., Le Deist F., Fischer A., Durandy A., De Villartay J.-P., Revy P., Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006 124 2 287 299 2-s2.0-31044440630 10.1016/j.cell.2005.12. 030 (Pubitemid 43121978)
39. Moshous D., Callebaut I., de Chasseval R., Corneo B., Cavazzana-Calvo M., Le Deist F., Tezcan I., Sanal O., Bertrand Y., Philippe N., Fischer A., De Villartay J.-P., Artemis, a novel DNA double-strand break repair/V(D)J recombination protein, is mutated in human severe combined immune deficiency. Cell 2001 105 2 177 186 2-s2.0-0035917489 10.1016/S0092-8674(01)00309-9 (Pubitemid 32429508)
40. 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 6 781 794 2-s2.0-0037155703 10.1016/S0092-8674(02)00671-2 (Pubitemid 34327530)
41. Ma Y., Lu H., Tippin B., Goodman M. F., Shimazaki N., Koiwai O., Hsieh C.-L., Schwarz K., Lieber M. R., A biochemically defined system for mammalian nonhomologous DNA end joining. Molecular Cell 2004 16 5 701 713 2-s2.0-9744241712 10.1016/j.molcel.2004.11.017 (Pubitemid 39586529)
42. Ma Y., Schwarz K., Lieber M. R., The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair 2005 4 7 845 851 2-s2.0-20644463916 10.1016/j.dnarep.2005.04.013 (Pubitemid 40835856)
43. Yannone S. M., Khan I. S., Zhou R.-Z., Zhou T., Valerie K., Povirk L. F., Coordinate 5' and 3' endonucleolytic trimming of terminally blocked blunt DNA double-strand break ends by Artemis nuclease and DNA-dependent protein kinase. Nucleic Acids Research 2008 36 10 3354 3365 2-s2.0-45549099011 10.1093/nar/gkn205 (Pubitemid 351859004)
44. Tseng H.-M., Tomkinson A. E., A physical and functional interaction between yeast Pol4 and Dnl4-Lif1 links DNA synthesis and ligation in nonhomologous end joining. Journal of Biological Chemistry 2002 277 47 45630 45637 2-s2.0-0037160145 10.1074/jbc.M206861200 (Pubitemid 36159174)
45. Mahajan K. N., Nick McElhinny S. A., Mitchell B. S., Ramsden D. A., Association of DNA polymerase μ (pol μ) with Ku and ligase IV: Role for pol μ in end-joining double-strand break repair. Molecular and Cellular Biology 2002 22 14 5194 5202 2-s2.0-0036293744 10.1128/MCB.22.14.5194-5202.2002 (Pubitemid 34700708)
46. 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 1 125 133 2-s2.0-38049144085 10.1038/cr.2007.108
47. West R. B., Yaneva M., Lieber M. R., Productive and nonproductive complexes of Ku and DNA-dependent protein kinase at DNA termini. Molecular and Cellular Biology 1998 18 10 5908 5920 2-s2.0-0031708232 (Pubitemid 28450542)
48. Falzon M., Fewell J. W., Kuff E. L., EBP-80, a transcription factor closely resembling the human autoantigen Ku, recognizes single- to double-strand transitions in DNA. Journal of Biological Chemistry 1993 268 14 10546 10552 2-s2.0-0027156140 (Pubitemid 23150243)
49. Mimori T., Hardin J. A., Mechanism of interaction between Ku protein and DNA. Journal of Biological Chemistry 1986 261 22 10375 10379 2-s2.0-0022827675 (Pubitemid 17221977)
50. Zhu C., Mills K. D., Ferguson D. O., Lee C., Manis J., Fleming J., Gao Y., Morton C. C., Alt F. W., Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002 109 7 811 821 2-s2.0-0037188898 10.1016/S0092-8674(02)00770-5 (Pubitemid 34785997)
51. 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., Rajewsky K., Alt F. W., IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007 449 7161 478 482 2-s2.0-34748863465 10.1038/nature06020 (Pubitemid 47509538)
52. 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., Shah S., Brandt V. L., Meek K., Roth D. B., Rag mutations reveal robust alternative end joining. Nature 2007 449 7161 483 486 2-s2.0-34848843525 10.1038/nature06168 (Pubitemid 47509551)
53. 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 52 20902 20907 2-s2.0-38049187905 10.1073/pnas.0708541104
54. Dinkelmann M., Spehalski E., Stoneham T., Buis J., Wu Y., Sekiguchi J. M., Ferguson D. O., Multiple functions of MRN in end-joining pathways during isotype class switching. Nature Structural and Molecular Biology 2009 16 8 808 813 2-s2.0-68249135624 10.1038/nsmb.1639
55. Deriano L., Stracker T. H., Baker A., Petrini J. H. J., Roth D. B., Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Molecular Cell 2009 34 1 13 25 2-s2.0-63649110740 10.1016/j.molcel.2009.03.009
56. Robert I., Dantzer F., Reina-San-Martin B., Parp1 facilitates alternative NHEJ, whereas Parp2 suppresses IgH/c-myc translocations during immunoglobulin class switch recombination. Journal of Experimental Medicine 2009 206 5 1047 1056 2-s2.0-66049143898 10.1084/jem.20082468
57. Sallmyr A., Tomkinson A. E., Rassool F. V., Up-regulation of WRN and DNA ligase lll{alpha} in chronic myeloid leukemia: consequences for the repair of DNA double-strand breaks. Blood 2008 112 4 1413 1423 2-s2.0-51649128895 10.1182/blood-2007-07-104257
58. Simsek D., Jasin M., m-jasin@ski.mskcc.org Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nature Structural and Molecular Biology 2010 17 4 410 416 2-s2.0-0032535036 10.1038/nsmb.1773
59. Boboila C., Jankovic M., Yan C. T., Wang J. H., Wesemann D. R., Zhang T., Fazeli A., Feldman L., Nussenzweig A., Nussenzweig M., Alt F. W., alt@enders.tch.harvard.edu 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 7 3034 3039 2-s2.0-0032522564 10.1073/pnas.0915067107
60. Roth D. B., Wilson J. H., Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Molecular and Cellular Biology 1986 6 12 4295 4304 2-s2.0-0022976432 (Pubitemid 17217374)
61. Roth D. B., Wilson J. H., Relative rates of homologous and nonhomologous recombination in transfected DNA. Proceedings of the National Academy of Sciences of the United States of America 1985 82 10 3355 3359 2-s2.0-0021827069 (Pubitemid 15033181)
62. Grawunder U., Zimmer D., Fugmann S., Schwarz K., Lieber M. R., DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Molecular Cell 1998 2 4 477 484 2-s2.0-0032185230 (Pubitemid 128381300)
63. Roth D. B., Porter T. N., Wilson J. H., Mechanisms of nonhomologous recombination in mammalian cells. Molecular and Cellular Biology 1985 5 10 2599 2607 2-s2.0-0022256461 (Pubitemid 15249545)
64. Honma M., Sakuraba M., Koizumi T., Takashima Y., Sakamoto H., Hayashi M., Non-homologous end-joining for repairing I-SceI-induced DNA double strand breaks in human cells. DNA Repair 2007 6 6 781 788 2-s2.0-34247601575 10.1016/j.dnarep.2007.01.004 (Pubitemid 46670087)
65. Willers H., Husson J., Lee L. W., Hubbe P., Gazemeier F., Powell S. N., Dahm-Daphi J., Distinct mechanisms of nonhomologous end joining in the repair of site-directed chromosomal breaks with noncomplementary and complementary ends. Radiation Research 2006 166 4 567 574 2-s2.0-33749183858 10.1667/RR0524.1 (Pubitemid 44477709)
66. Thacker J., The role of homologous recombination processes in the repair of severe forms of DNA damage in mammalian cells. Biochimie 1999 81 1-2 77 85 2-s2.0-0032694294 10.1016/S0300-9084(99)80041-8
67. North P., Ganesh A., Thacker J., The rejoining of double-strand breaks in DNA by human cell extracts. Nucleic Acids Research 1990 18 21 6205 6210 2-s2.0-0025151450
68. Sathees C. R., Raman M. J., Mouse testicular extracts process DNA double-strand breaks efficiently by DNA end-to-end joining. Mutation Research 1999 433 1 1 13 2-s2.0-0033046569 10.1016/S0921-8777(98)00055-X (Pubitemid 29073665)
69. Nicolas A. L., Young C. S. H., Characterization of DNA end joining in a mammalian cell nuclear extract: junction formation is accompanied by nucleotide loss, which is limited and uniform but not site specific. Molecular and Cellular Biology 1994 14 1 170 180 2-s2.0-0028144408
70. Pont-Kingdon G., Dawson R. J., Carroll D., Intermediates in extrachromosomal homologous recombination in Xenopus laevis oocytes: characterization by electron microscopy. EMBO Journal 1993 12 1 23 34 2-s2.0-0027397089 (Pubitemid 23042379)
71. Pfeiffer P., Vielmetter W., Joining of nonhomologous DNA double strand breaks in vitro. Nucleic Acids Research 1988 16 3 907 924 2-s2.0-0024284051
72. Derbyshire M. K., Epstein L. H., Young C. S. H., Munz P. L., Fishel R., Nonhomologous recombination in human cells. Molecular and Cellular Biology 1994 14 1 156 169 2-s2.0-0028153704
73. Boe S.-O., Sodroski J., Helland D. E., Farnet C. M., DNA end-joining in extracts from human cells. Biochemical and Biophysical Research Communications 1995 215 3 987 993 2-s2.0-0028872822 10.1006/bbrc.1995.2561
74. Baumann P., West S. C., DNA end-joining catalyzed by human cell-free extracts. Proceedings of the National Academy of Sciences of the United States of America 1998 95 24 14066 14070 2-s2.0-0032564469 10.1073/pnas.95.24.14066 (Pubitemid 28549321)
75. Budman J., Chu G., Processing of DNA for nonhomologous end-joining by cell-free extract. EMBO Journal 2005 24 4 849 860 2-s2.0-15444370124 10.1038/sj.emboj.7600563 (Pubitemid 40396113)
76. 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. EMBO Journal 2007 26 4 1010 1023 2-s2.0-33847193121 10.1038/sj.emboj.7601559
77. Labhart P., Nonhomologous DNA end joining in cell-free systems. European Journal of Biochemistry 1999 265 3 849 861 2-s2.0-0033231221 10.1046/j.1432-1327.1999.00805.x (Pubitemid 29507796)
78. Manova V., Gecheff K., Stoilov L., Efficient repair of bleomycin-induced double-strand breaks in barley ribosomal genes. Mutation Research 2006 601 1-2 179 190 2-s2.0-33749534669 10.1016/j.mrfmmm.2006.07.004 (Pubitemid 44528603)
79. Pastwa E., Neumann R. D., Winters T. A., In vitro repair of complex unligatable oxidatively induced DNA double-strand breaks by human cell extracts. Nucleic Acids Research 2001 29 16 E78 2-s2.0-0035882894
80. Sharma S., Choudhary B., Raghavan S.C., Efficiency of nonhomologous DNA end joining varies among somatic tissues, despite similarity in mechanism. Cellular and Molecular Life Sciences. In press
81. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L., DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proceedings of the National Academy of Sciences of the United States of America 1980 77 7 3855 3859 2-s2.0-0242689439 (Pubitemid 10015480)
82. Coudoré F., Calsou P., Salles B., DNA repair activity in protein extracts from rat tissues. FEBS Letters 1997 414 3 581 584 2-s2.0-0030804284 10.1016/S0014-5793(97)01077-6 (Pubitemid 27390672)
83. Wood R. D., Robins P., Lindahl T., Complementation of the xeroderma pigmentosum DNA repair defect in cell-free extracts. Cell 1988 53 1 97 106 2-s2.0-0023878893
84. Raghavan S. C., Raman M. J., Nonhomologous end joining of complementary and noncomplementary DNA termini in mouse testicular extracts. DNA Repair 2004 3 10 1297 1310 2-s2.0-4444340631 10.1016/j.dnarep.2004.04.007 (Pubitemid 39164593)
85. Diggle C. P., Bentley J., Kiltie A. E., Development of a rapid, small-scale DNA repair assay for use on clinical samples. Nucleic Acids Research 2003 31 15 e83 2-s2.0-0042161806
86. Thode S., Schafer A., Pfeiffer P., Vielmetter W., A novel pathway of DNA end-to-end joining. Cell 1990 60 6 921 928 2-s2.0-0025274315 10.1016/0092-8674(90)90340-K (Pubitemid 20103874)
87. Lehman C. W., Clemens M., Worthylake D. K., Trautman J. K., Carroll D., Homologous and illegitimate recombination in developing Xenopus oocytes and eggs. Molecular and Cellular Biology 1993 13 11 6897 6906 2-s2.0-0027375231 (Pubitemid 23321143)
88. Thacker J., Chalk J., Ganesh A., North P., A mechanism for deletion formation in DNA by human cell extracts: the involvement of short sequence repeats. Nucleic Acids Research 1992 20 23 6183 6188 2-s2.0-0027074470 (Pubitemid 23039143)
89. Daza P., Reichenberger S., Göttlich B., Hagmann M., Feldmann E., Pfeiffer P., Mechanisms of nonhomologous DNA end-joining in frogs, mice and men. Biological Chemistry 1996 377 12 775 786 2-s2.0-0030475586 (Pubitemid 27025973)
90. Odersky A., Panyutin I. V., Panyutin I. G., Schunckl C., Feldmann E., Goedecke W., Neumann R. D., Obe G., Pfeiffer P., Repair of sequence-specific 125I-induced double-strand breaks by nonhomologous DNA end joining in mammalian cell-free extracts. Journal of Biological Chemistry 2002 277 14 11756 11764 2-s2.0-0037023694 10.1074/jbc.M111304200 (Pubitemid 34952730)
91. Mérel P., Prieur A., Pfeiffer P., Delattre O., Absence of major defects in non-homologous DNA end joining in human breast cancer cell lines. Oncogene 2002 21 36 5654 5659 2-s2.0-0037104045 10.1038/sj.onc.1205742 (Pubitemid 34983556)
92. Ren K., Pea de Ortiz S., Non-homologous DNA end joining in the mature rat brain. Journal of Neurochemistry 2002 80 6 949 959 2-s2.0-0036326014 10.1046/j.0022-3042.2002.00776.x (Pubitemid 34809947)
93. Vyjayanti V. N., Rao K. S., DNA double strand break repair in brain: reduced NHEJ activity in aging rat neurons. Neuroscience Letters 2006 393 1 18 22 2-s2.0-28444474288 10.1016/j.neulet.2005.09.053 (Pubitemid 41739646)
94. Shackelford D. A., DNA end joining activity is reduced in Alzheimer's disease. Neurobiology of Aging 2006 27 4 596 605 2-s2.0-33344463678 10.1016/j.neurobiolaging.2005.03.009 (Pubitemid 43290528)
95. Roth D. B., Wilson J. H., Genetic Recombination 1988 Washington, DC, USA American Society for Microbiology
96. Mason R. M., Thacker J., Fairman M. P., The joining of non-complementary DNA double-strand breaks by mammalian extracts. Nucleic Acids Research 1996 24 24 4946 4953 2-s2.0-0030471390 10.1093/nar/24.24.4946 (Pubitemid 27007899)
97. McVey M., Lee S. E., MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends in Genetics 2008 24 11 529 538 2-s2.0-54849404458 10.1016/j.tig.2008.08.007
98. Short S. C., Martindale C., Bourne S., Brand G., Woodcock M., Johnston P., DNA repair after irradiation in glioma cells and normal human astrocytes. Neuro-Oncology 2007 9 4 404 411 2-s2.0-36949025036 10.1215/15228517-2007-030
99. Carlomagno F., Burnet N. G., Turesson I., Nyman J., Peacock J. H., Dunning A. M., Ponder B. A. J., Jackson S. P., Comparison of DNA repair protein expression and activities between human fibroblast cell lines with different radiosensitivities. International Journal of Cancer 2000 85 6 845 849 2-s2.0-0034109911 10.1002/(SICI)1097-0215(20000315)85:6845::AID-IJC18>3.0. CO;2-C (Pubitemid 30131476)
100. Sandberg R., Ernberg I., Assessment of tumor characteristic gene expression in cell lines using a tissue similarity index (TSI). Proceedings of the National Academy of Sciences of the United States of America 2005 102 6 2052 2057 2-s2.0-13844312493 10.1073/pnas.0408105102 (Pubitemid 40262010)
101. Bentzen S. M., Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nature Reviews Cancer 2006 6 9 702 713 2-s2.0-33747826874 10.1038/nrc1950 (Pubitemid 44286002)
102. Hall E. J., Giacca A. J., Clinical Responses of Normal Tissues 2005 Lippincott, Williams and Wilkins