Early embryonic lethality due to targeted inactivation of DNA ligase III

Molecular and Cellular Biology

Volumn 26, Issue 10, 2006, Pages 3935-3941

  Puebla Osorio, Nahum ^a   Lacey, Devin B ^a   Alt, Frederick W ^b   Zhu, Chengming ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA LIGASE III; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DNA STRAND BREAKAGE; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENZYME ASSAY; ENZYME INACTIVATION; GENOTYPE; HELA CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA INTERFERENCE; SOUTHERN BLOTTING; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, SOUTHERN; BLOTTING, WESTERN; DNA LIGASES; ELECTROPORATION; EMBRYO; EXONS; FEMALE; GENE TARGETING; GENES, LETHAL; HELA CELLS; HOMOZYGOTE; HUMANS; MICE; MICE, MUTANT STRAINS; MUTATION; POLYMERASE CHAIN REACTION; PREGNANCY; RESTRICTION MAPPING; RNA INTERFERENCE; SISTER CHROMATID EXCHANGE; STEM CELLS;

MAMMALIA;

EID: 33646589977     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.10.3935-3941.2006     Document Type: Article

References (56)

1. Barnes, D. E., G. Stamp, I. Rosewell, A. Denzel, and T. Lindahl. 1998. Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol. 8:1395-1398.
2. Caldecott, K. W. 2001. Mammalian DNA single-strand break repair: an X-ra(y)ted affair. Bioessays 23:447-455.
3. Caldecott, K. W., S. Aoufouchi, P. Johnson, and S. Shall. 1996. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 24:4387-4394.
4. Caldecott, K. W., C. K. McKeown, J. D. Tucker, S. Ljungquist, and L. H. Thompson. 1994. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol. 14:68-76.
5. Caldecott, K. W., J. D. Tucker, L. H. Stanker, and L. H. Thompson. 1995. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res. 23:4836-4843.
6. Cappelli, E., R. Taylor, M. Cevasco, A. Abbondandolo, K. Caldecott, and G. Frosina. 1997. Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair. J. Biol. Chem. 272:23970-23975.
7. Chen, J., A. E. Tomkinson, W. Ramos, Z. B. Mackey, S. Danehower, C. A. Walter, R. A. Schultz, J. M. Besterman, and I. Husain. 1995. Mammalian DNA ligase III: molecular cloning, chromosomal localization, and expression in spermatocytes undergoing meiotic recombination. Mol. Cell. Biol. 15:5412-5422.
8. de Boer, J., I. Donker, J. de Wit, J. H. Hoeijmakers, and G. Weeda. 1998. Disruption of the mouse xeroderma pigmentosum group D DNA repair/basal transcription gene results in preimplantation lethality. Cancer Res. 58:89-94.
9. El-Khamisy, S. F., G. M. Saifi, M. Weinfeld, F. Johansson, T. Helleday, J. R. Lupski, and K. W. Caldecott. 2005. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 434:108-113.
10. Fan, J., M. Otterlei, H. K. Wong, A. E. Tomkinson, and D. M. Wilson, III. 2004. XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res. 32:2193-2201.
11. Fan, J., and D. M. Wilson, III. 2005. Protein-protein interactions and posttranslational modifications in mammalian base excision repair. Free Radic. Biol. Med. 38:1121-1138.
12. Frank, K. M., J. M. Sekiguchi, K. J. Seidl, W. Swat, G. A. Rathbun, H. L. Cheng, L. Davidson, L. Kangaloo, and F. W. Alt. 1998. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 396:173-177.
13. Grawunder, U., M. Wilm, X. Wu, P. Kulesza, T. E. Wilson, M. Mann, and M. R. Lieber. 1997. Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 388:492-495.
14. Grawunder, U., D. Zimmer, S. Fugmann, K. Schwarz, and M. R. Lieber. 1998. DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Mol. Cell 2:477-484.
15. Grawunder, U., D. Zimmer, P. Kulesza, and M. R. Lieber. 1998. Requirement for an interaction of XRCC4 with DNA ligase IV for wild-type V(D)J recombination and DNA double-strand break repair in vivo. J. Biol. Chem. 273:24708-24714.
16. Gryk, M. R., A. Marintchev, M. W. Maciejewski, A. Robertson, S. H. Wilson, and G. P. Mullen. 2002. Mapping of the interaction interface of DNA polymerase beta with XRCC1. Structure (Cambridge) 10:1709-1720.
17. Gu, H., J. D. Marth, P. C. Orban, H. Mossmann, and K. Rajewsky. 1994. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265:103-106.
18. Husain, I., A. E. Tomkinson, W. A. Burkhart, M. B. Moyer, W. Ramos, Z. B. Mackey, J. M. Besterman, and J. Chen. 1995. Purification and characterization of DNA ligase III from bovine testes. Homology with DNA ligase II and vaccinia DNA ligase. J. Biol. Chem. 270:9683-9690.
19. Ikejima, M., S. Noguchi, R. Yamashita, T. Ogura, T. Sugimura, D. M. Gill, and M. Miwa. 1990. The zinc fingers of human poly(ADP-ribose) polymerase are differentially required for the recognition of DNA breaks and nicks and the consequent enzyme activation. Other structures recognize intact DNA. J. Biol. Chem. 265:21907-21913.
20. Krishnan, V. V., K. H. Thornton, M. P. Thelen, and M. Cosman. 2001. Solution structure and backbone dynamics of the human DNA ligase IIIalpha BRCT domain. Biochemistry 40:13158-13166.
21. Kubota, Y., R. A. Nash, A. Klungland, P. Schar, D. E. Barnes, and T. Lindahl. 1996. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J. 15:6662-6670.
22. Lakshmipathy, U., and C. Campbell. 1999. The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell. Biol. 19:3869-3876.
23. Lakshmipathy, U., and C. Campbell. 2000. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res. 28:3880-3886.
24. Leppard, J. B., Z. Dong, Z. B. Mackey, and A. E. Tomkinson. 2003. Physical and functional interaction between DNA ligase IIIα and poly(ADP-ribose) polymerase 1 in DNA single-strand break repair. Mol. Cell. Biol. 23:5919-5927.
25. Levin, D. S., A. E. McKenna, T. A. Motycka, Y. Matsumoto, and A. E. Tomkinson. 2000. Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair. Curr. Biol. 10:919-922.
26. Lim, D. S., and P. Hasty. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133-7143.
27. Ljungquist, S., K. Kenne, L. Olsson, and M. Sandstrom. 1994. Altered DNA ligase III activity in the CHO EM9 mutant. Mutat. Res. 314:177-186.
28. Ludwig, D. L., M. A. MacInnes, Y. Takiguchi, P. E. Purtymun, M. Henrie, M. Flannery, J. Meneses, R. A. Pedersen, and D. J. Chen. 1998. A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity. Mutat. Res. 409:17-29.
29. Ludwig, T., D. L. Chapman, V. E. Papaioannou, and A. Efstratiadis. 1997. Targeted mutations of breast cancer susceptibility gene homologs in mice: lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev. 11:1226-1241.
30. Mackey, Z. B., C. Niedergang, J. M. Murcia, J. Leppard, K. Au, J. Chen, G. de Murcia, and A. E. Tomkinson. 1999. DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. Identification of two functionally distinct DNA binding regions within DNA ligase III. J. Biol. Chem. 274:21679-21687.
31. Mackey, Z. B., W. Ramos, D. S. Levin, C. A. Walter, J. R. McCarrey, and A. E. Tomkinson. 1997. An alternative splicing event which occurs in mouse pachytene spermatocytes generates a form of DNA ligase III with distinct biochemical properties that may function in meiotic recombination. Mol. Cell. Biol. 17:989-998.
32. Martin, I. V., and S. A. MacNeill. 2002. ATP-dependent DNA ligases. Genome Biol. 3:3005.1-3005.7.
33. Nash, R. A., K. W. Caldecott, D. E. Barnes, and T. Lindahl. 1997. XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry 36:5207-5211.
34. Perez-Jannotti, R. M., S. M. Klein, and D. F. Bogenhagen. 2001. Two forms of mitochondrial DNA ligase III are produced in Xenopus laevis oocytes. J. Biol. Chem. 276:48978-48987.
35. Schreiber, V., J. C. Ame, P. Dolle, I. Schultz, B. Rinaldi, V. Fraulob, J. Menissier-de Murcia, and G. de Murcia. 2002. Poly(ADP-ribose) polymerase-2 (PARP-2) is required for efficient base excision DNA repair in association with PARP-1 and XRCC1. J. Biol. Chem. 277:23028-23036.
36. Shuman, S., and B. Schwer. 1995. RNA capping enzyme and DNA ligase: a superfamily of covalent nucleotidyl transferases. Mol. Microbiol. 17:405-410.
37. Sibanda, B. L., S. E. Critchlow, J. Begun, X. Y. Pei, S. P. Jackson, T. L. Blundell, and L. Pellegrini. 2001. Crystal structure of an Xrcc4-DNA ligase IV complex. Nat. Struct. Biol. 8:1015-1019.
38. Taylor, R. M., D. J. Moore, J. Whitehouse, P. Johnson, and K. W. Caldecott. 2000. A cell cycle-specific requirement for the XRCC1 BRCT II domain during mammalian DNA strand break repair. Mol. Cell. Biol. 20:735-740.
39. Taylor, R. M., J. Whitehouse, E. Cappelli, G. Frosina, and K. W. Caldecott. 1998. Role of the DNA ligase III zinc finger in polynucleotide binding and ligation. Nucleic Acids Res. 26:4804-4810.
40. Tebbs, R. S., M. L. Flannery, J. J. Meneses, A. Hartmann, J. D. Tucker, L. H. Thompson, J. E. Cleaver, and R. A. Pedersen. 1999. Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol. 208:513-529.
41. Tebbs, R. S., L. H. Thompson, and J. E. Cleaver. 2003. Rescue of Xrcc1 knockout mouse embryo lethality by transgene-complementation. DNA Repair (Amsterdam) 2:1405-1417.
42. Teraoka, H., T. Sumikawa, and K. Tsukada. 1986. Purification of DNA ligase II from calf thymus and preparation of rabbit antibody against calf thymus DNA ligase II. J. Biol. Chem. 261:6888-6892.
43. Thompson, L. H., K. W. Brookman, N. J. Jones, S. A. Allen, and A. V. Carrano. 1990. Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol. Cell. Biol. 10:6160-6171.
44. Timson, D. J., M. R. Singleton, and D. B. Wigley. 2000. DNA ligases in the repair and replication of DNA. Mutat. Res. 460:301-318.
45. Tom, S., L. A. Henricksen, M. S. Park, and R. A. Bambara. 2001. DNA ligase I and proliferating cell nuclear antigen form a functional complex. J. Biol. Chem. 276:24817-24825.
46. Tomkinson, A. E., L. Chen, Z. Dong, J. B. Leppard, D. S. Levin, Z. B. Mackey, and T. A. Motycka. 2001. Completion of base excision repair by mammalian DNA ligases. Prog. Nucleic Acid Res. Mol. Biol. 68:151-164.
47. Tomkinson, A. E., and D. S. Levin. 1997. Mammalian DNA ligases. Bioessays 19:893-901.
48. Tomkinson, A. E., and Z. B. Mackey. 1998. Structure and function of mammalian DNA ligases. Mutat. Res. 407:1-9.
49. Vidal, A. E., S. Boiteux, I. D. Hickson, and J. P. Radicella. 2001. XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J. 20:6530-6539.
50. Wang, H., B. Rosidi, R. Perrault, M. Wang, L. Zhang, F. Windhofer, and G. Iliakis. 2005. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 65:4020-4030.
51. Wang, Y. C., W. A. Burkhart, Z. B. Mackey, M. B. Moyer, W. Ramos, I. Husain, J. Chen, J. M. Besterman, and A. E. Tomkinson. 1994. Mammalian DNA ligase II is highly homologous with vaccinia DNA ligase. Identification of the DNA ligase II active site for enzyme-adenylate formation. J. Biol. Chem. 269:31923-31928.
52. Wei, Y. F., P. Robins, K. Carter, K. Caldecott, D. J. Pappin, G. L. Yu, R. P. Wang, B. K. Shell, R. A. Nash, P. Schar, D. E. Barnes, W. A. Haseltine, and T. Lindahl. 1995. Molecular cloning and expression of human cDNAs encoding a novel DNA ligase IV and DNA ligase III, an enzyme active in DNA repair and recombination. Mol. Cell. Biol. 15:3206-3216.
53. Wnitehouse, C. J., R. M. Taylor, A. Thistlethwaite, H. Zhang, F. Karimi-Busheri, D. D. Lasko, M. Weinfeld, and K. W. Caldecott. 2001. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104:107-117.
54. Wilier, M., M. Rainey, T. Pullen, and C. J. Stirling. 1999. The yeast CDC9 gene encodes both a nuclear and a mitochondrial form of DNA ligase I. Curr. Biol. 9:1085-1094.
55. Xanthoudakis, S., R. J. Smeyne, J. D. Wallace, and T. Curran. 1996. The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl. Acad. Sci. USA 93:8919-8923.
56. Zhang, X., S. Morera, P. A. Bates, P. C. Whitehead, A. I. Coffer, K. Hainbucher, R. A. Nash, M. J. Sternberg, T. Lindahl, and P. S. Freemont. 1998. Structure of an XRCC1 BRCT domain: a new protein-protein interaction module. EMBO J. 17:6404-6411.