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

Volumn 18, Issue 1, 2008, Pages 125-133

  Lieber, Michael R ^a   Lu, Haihui ^a   Gu, Jiafeng ^a   Schwarz, Klaus ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b German Red Cross Blood Transfusion Service Baden Württemberg Hessen and University Hospital Ulm   (Germany)

Author keywords

Artemis; Cernunnos XLF; DNA PKcs; Ku; Ligase IV; Nonhomologous DNA end joining (NHEJ); Polymerase ; Polymerase ; XRCC4

Indexed keywords

DCLRE1C PROTEIN, HUMAN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; DNA DEPENDENT PROTEIN KINASE; DNA DIRECTED DNA POLYMERASE; NHEJ1 PROTEIN, HUMAN; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); PRKDC PROTEIN, HUMAN; UNCLASSIFIED DRUG; XRCC4 PROTEIN, HUMAN;

ADAPTATION; AGING; ANIMAL; BIOLOGICAL MODEL; DNA REPAIR; ENZYMOLOGY; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENETICS; HUMAN; IMMUNE SYSTEM; METABOLISM; NEOPLASM; PHYSIOLOGY; REVIEW; VDJ EXON; VERTEBRATE;

ADAPTATION, BIOLOGICAL; AGING; ANIMALS; DEOXYRIBONUCLEASES; DNA LIGASES; DNA REPAIR; DNA REPAIR ENZYMES; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; HUMANS; IMMUNE SYSTEM; IMMUNOGLOBULIN CLASS SWITCHING; MODELS, BIOLOGICAL; NEOPLASMS; NUCLEAR PROTEINS; RECOMBINATION, GENETIC; VDJ EXONS; VERTEBRATES;

EUKARYOTA; VERTEBRATA;

EID: 38049144085     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2007.108     Document Type: Review

References (59)

1. Roberts SA, Ramsden DA. Loading of the nonhomologous end joining factor, Ku, on protein-occluded DNA ends. J Biol Chem 2007; 282:10605- 10613.
2. Ma Y, Lu H, Tippin B, et al. A biochemically defined system for mammalian nonhomologous DNA end joining. Mol Cell 2004; 16:701-713.
3. Ma Y, Pannicke U, Schwarz K, Lieber MR. Hairpin opening and overhang processing by an Artemis:DNA-PKcs complex in V(D)J recombination and in nonhomologous end joining. Cell 2002; 108:781-794.
4. Zhang Y, Hefferin ML, Chen L, et al. Role of Dn14-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat Struct Mol Biol 2007; 14:639-646.
5. West RB, Yaneva M, Lieber MR. Productive and nonproductive complexes of Ku and DNA-PK at DNA termini. Mol Cell Biol 1998; 18:5908-5920.
6. Meek K, Douglas P, Cui X, Ding Q, Lees-Miller SP. trans Autophosphorylation at DNA-dependent protein kinase's two major autophosphorylation site clusters facilitates end processing but not end joining. Mol Cell Biol 2007; 27:3881-3890.
7. Ma Y, Pannicke U, Lu H, et al. The DNA-PKcs phosphorylation sites of human artemis. J Biol Chem 2005; 280:33839-33846.
8. Niewolik D, Pannicke U, Lu H, et al. DNA-PKcs dependence of artemis endonucleolytic activity: differences between hairpins and 5′ or 3′ overhangs. J Biol Chem 2006; 281:33900-33909.
9. Goodarzi AA, Yu Y, Riballo E, et al. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J 2006; 25:3880-3889.
10. Ma Y, Schwarz K, Lieber MR. The Artemis:DNA-PKcs endonuclease can cleave gaps, flaps, and loops. DNA Repair (Amst) 2005;4:845-851.
11. Povirk LF, Zhou T, Zhou R, Cowan MJ, Yannone SM. Processing of 30-phosphoglycolate-terminated DNA double strand breaks by Artemis nuclease. J Biol Chem 2007; 282:3547-3558.
12. Povirk LF. Biochemical mechanisms of chromosomal translocations resulting from DNA double-strand breaks. DNA Repair (Amst) 2006; 5:1199-1212.
13. Bertocci B, De Smet A, Weill JC, Reynaud CA. Nonoverlapping functions of DNA polymerases mu, lambda, and terminal deoxynucleotidyltransferase during immunoglobulin V(D)J recombination in vivo. Immunity 2006; 25:31-41.
14. Bertocci B, De Smet A, Berek C, Weill JC, Reynaud CA. Immunoglobulin kappa light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu. Immunity 2003; 19:203-211.
15. NickMcElhinny SA, Ramsden DA. Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol Cell Biol 2003; 23:2309-2315.
16. Tseng HM, Tomkinson AE. A physical and functional interaction between yeast Pol4 and Dn14-Lif1 links DNA synthesis and ligation in nonhomologous end joining. J Biol Chem 2002; 277:45630-45637.
17. Wilson TE, Lieber MR. Efficient processing of DNA ends during yeast nonhomologous end joining: evidence for a DNA polymerase beta (POL4)-dependent pathway. J Biol Chem 1999; 274:23599-23609.
18. Daley JM, Laan RLV, Suresh A, Wilson TE. DNA joint dependence of pol X family polymerase action in nonhomologous end joining. J Biol Chem 2005; 280:29030-29037.
19. Garcia-Diaz M, Bebenek K, Sabariegos R, et al. DNA polymerase lambda, a novel DNA repair enzyme in human cells. J Biol Chem 2002; 277:13184-13191.
20. Lee JW, Blanco L, Zhou T, et al. Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts. J Biol Chem 2003; 279:805-811.
21. NickMcElhinny SA, Havener JM, Garcia-Diaz M, et al. A gradient of template dependence defines distinct biological roles for family x polymerases in nonhomologous end joining. Mol Cell 2005; 19:357-366.
22. Gu J, Lu H, Tippin B, et al. XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. EMBO J 2007; 26:1010-1023.
23. Juarez R, Ruiz JF, NickMcElhinny SA, Ramsden D, Blanco L. A specific loop in human DNA polymerase mu allows switching between creative and DNA-insructed synthesis. Nucl Acids Res 2006; 34:4572-4582.
24. Moon AF, Garcia-Diaz M, Bebenek K, et al. Structural insight into the substrate specificity of DNA polymerase mu. Nat Struct Mol Biol 2007; 14:45-53.
25. Grawunder U, Wilm M, Wu X, et al. Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 1997; 388:492-495.
26. Wilson TE, Grawunder U, Lieber MR. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 1997; 388:495-498.
27. Teo SH, Jackson SP. Identification of S. cerevisiae DNA ligase IV: involvement in DNA double-strand break repair. EMBO J 1997; 16:4788-4795.
28. Schar P, Herrmann G, Daly G, Lindahl T. A newly identified DNA ligase of S. cerevisiae involved in RAD52-independent repair of DNA double-strand breaks. Genes Dev 1997; 11:1912-1924.
29. Modesti M, Hesse JE, Geliert M. DNA binding of XRCC4 is associated with V(D)J recombination but not with stimulation of DNA ligase IV activity. EMBO J 1999; 18:2008-2018.
30. Modesti M, Junop MS, Ghirlando R, et al. Tetramerization and DNA ligase IV interaction of the DNA double-strand break protein XRCC4 are mutually exclusive. J Mol Biol 2003; 334:215-228.
31. Tomkinson AE, Vijayakumar S, Pascal JM, Ellenberger T. DNA ligases: structure, reaction mechanism, and function. Chem Rev 2006; 106:687-699.
32. Robins P, Lindahl T. DNA ligase IV from HeLa cell nuclei. J Biol Chem 1996; 271:24257-24261.
33. Buck D, Malivert L, deChasseval R, et al. Cernunnos, a novel nonhomologous end-joining factor, is mutated in human immunodeficiency with microcephaly. Cell 2006; 124:287-299.
34. Ahnesorg P, Smith P, Jackson SP. XLF interacts with the XRCC4-DNA ligase IV complex to promote nonhomologous end-joining. Cell 2006; 124:301-313.
35. Callebaut I, Malivert L, Fischer A, et al. Cernunnos interacts with the XRCC4/DNA-ligase IV complex and is homologous to the yeast nonhomologous end-joining factor NEJ1. J Biol Chem 2006; 281:13857-13860.
36. Hentges P, Ahnesorg P, Pritcher RS, et al. Evolutionary and functional conservation of the DNA nonhomologous end joining protein, XLF/Cernunnos. J Biol Chem 2006; 281:36952-36959.
37. Lu H, Pannicke U, Schwarz K, Lieber MR. Length-dependent binding of human XLF to DNA and stimulation of XRCC4. DNA ligase IV activity. J Biol Chem 2007; 282:11155-11162.
38. Tsai CJ, Kim SA, Chu G. Cernunnos/XLF promotes the ligation of mismatched and noncohesive DNA ends. Proc Natl Acad Sci USA 2007; 104:7851-7856.
39. Gu J, Lu H, Tsai AG, Schwarz K, Lieber MR. 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 Res 2007; 35:5755-5762.
40. Daley JM, Wilson TE. Evidence that base stacking potential in annealed 3' overhangs determines polymerase utilization in yeast nonhomologous end joining. DNA Repair (Amst) 2007; doi:10.1016/j.dnarep.2007.07.018.
41. Deshpande RA, Wilson TE. Modes of interaction among yeast Nej1, Lif1 and Dn14 proteins and comparison to human XLF, XRCC4 and Lig4. DNA Repair (Amst) 2007; 6:1507-1516.
42. Walker JR, Corpina RA, Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001; 412:607-614.
43. Gellert M. V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 2002; 71:101-132.
44. Ferguson DO, Sekiguchi JM, Chang S, et al. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci USA 2000; 97:6630-6633.
45. Corneo B, Deriano L, Cui X, et al. A mutation in RAG2 reveals robust, error-prone alternative end joining. Nature 2007; 449:483-486.
46. Chaudhuri J, Basu U, Zarrin A, et al. Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv Immunol 2007; 94:157-214.
47. Yu K, Lieber MR. Nucleic acid structures and enzymes in the immunoglobulin class switch recombination mechanism. DNA Repair (Amst) 2003; 2:1163-1174.
48. Selsing E. Ig class switching: targeting the recombinational mechanism. Curr Opin Immunol 2006; 18:249-254.
49. Yu K, Chedin F, Hsieh C-L, Wilson TE, Lieber MR. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat Immunol 2003; 4:442-451.
50. Shinkura R, Tian M, Khuong C, et al. The influence of transcriptional orientation on endogenous switch region function. Nat Immunol 2003; 4:435-441.
51. Zarrin AA, Alt FW, Chaudhuri J, et al. An evolutionarily conserved target motif for immunoglobulin class-switch recombination. Nat Immunol 2004; 5:1275-1281.
52. Pham P, Bransteitter R, Petruska J, Goodman MF. Processive AID-catalyzed cytosine deamination on single-stranded DNA stimulates somatic hypermutation. Nature 2003; 424:103-107.
53. Rada C, Di Noia JM, Neuberger MS. Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 2004; 16:163-171.
54. Bardwell PD, Woo CJ, Wei K, et al. Altered somatic hypermutation and reduced class-switch recombination in exonuclease 1 -mutant mice. Nat Immunol 2004; 5:224-229.
55. Soulas-Sprauel P, Le Guyader G, Rivera-Munoz P, et al. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J Exp Med 2007; 204:1717-1727.
56. Yan CT, Boboila C, Souza EK, et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007; 449:478-482.
57. Ferguson DO, Alt FW. DNA double-strand break repair and chromosomal translocations: lessons from animal models. Oncogene 2001; 20:5572-5579.
58. Greenblatt MS, Grollman AP, Harris CC. Deletions and insertions in the p53 tumor suppressor gene in human cancers: confirmation of the DNA polymerase slippage/misalignment model. Cancer Res 1996; 56:2130-2136.
59. Murnane JP. Telomeres, chromosome instability, and cancer. DNA Repair (Amst) 2006; 5:1082-1092.