Functional redundancy between DNA ligases i and III in DNA replication in vertebrate cells

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2599-2610

  Arakawa, Hiroshi ^a,c   Bednar, Theresa ^b   Wang, Minli ^b,d   Paul, Katja ^b   Mladenov, Emil ^b   Bencsik Theilen, Alena A ^b   Iliakis, George ^b  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^c FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^d UNIVERSITIES SPACE RESEARCH ASSOCIATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA LIGASE I GENE; DNA LIGASE III GENE; DNA LIGASE IV GENE; DNA REPLICATION; EXCISION REPAIR; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENE FUNCTION; GENE INACTIVATION; GENE LOCUS; GENE OVEREXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GENETIC CONSERVATION; MITOCHONDRIAL RESPIRATION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRUCTURAL GENE; VERTEBRATE;

ANIMALS; CELL LINE; CELL SURVIVAL; CHICKENS; DNA LIGASES; DNA REPLICATION; GENE KNOCKOUT TECHNIQUES; GENE TARGETING; GENES, LETHAL; MITOCHONDRIA; MUTATION;

EUKARYOTA; VERTEBRATA;

EID: 84859336816     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1024     Document Type: Article

References (36)

1. Lindahl, T. and Barnes, D.E. (1992) Mammalian DNA ligases. Annu. Rev. Biochem., 61, 251-281
2. Ellenberger, T. and Tomkinson, A.E. (2008) Eukaryotic DNA ligases: structural and functional insights. Annu. Rev. Biochem., 77, 313-338
3. Cardoso, M.C., Joseph, C., Rahn, H.-P., Reusch, R., Nadal-Ginard, B. and Leonhardt, H. (1997) Mapping and use of a sequence that targets DNA ligase I to sites of DNA replication in vivo. J. Cell Biol., 139, 579-587 (Pubitemid 27485825)
4. Montecucco, A., Savini, E., Weighardt, F., Rossi, R., Ciarrocchi, G., Villa, A. and Biamonti, G. (1995) The N-terminal domain of human DNA ligase I contains the nuclear localization signal and directs the enzyme to sites of DNA replication. EMBO J., 14, 5379-5386
5. Montecucco, A., Rossi, R., Levin, D.S., Gary, R., Park, M.S., Motycka, T.A., Ciarrocchi, G., Villa, A., Biamonti, G. and Tomkinson, A.E. (1998) DNA ligase I is recruited to sites of DNA replication by an interaction with proliferating cell nuclear antigen: identification of a common targeting mechanism for the assembly of replication factories. EMBO J., 17, 3786-3795 (Pubitemid 28327396)
6. Barnes, D.E., Tomkinson, A.E., Lehmann, A.R., Webster, A.D.B. and Lindahl, T. (1992) Mutations in the DNA ligase 1 gene of an individual with immunodeficiencies and cellular hypersensitivity to DNA-damaging agents. Cell, 69, 495-503
7. Webster, A.D.B., Barnes, D.E., Arlett, C.F., Lehmann, A.R. and Lindahl, T. (1992) Growth retardation and immunodeficiency in a patient with mutations in the DNA ligase 1 gene. Lancet, 339, 1508-1509
8. Bentley, D.J., Selfridge, J., Millar, J.K., Samuel, K., Hole, N., Ansell, J.D. and Melton, D.W. (1996) DNA ligase I is required for fetal liver erythropoiesis but is not essential for mammlian cell viability. Nat. Genet., 13, 489-491 (Pubitemid 26256628)
9. Bentley, D.J., Harrison, C., Ketchen, A.-M., Redhead, N.J., Samuel, K., Waterfall, M., Ansell, J.D. and Melton, D.W. (2002) DNA ligase I null mouse cells show normal DNA repair activity but altered DNA replication and reduced genome stability. J. Cell Sci., 115, 1551-1561 (Pubitemid 34428711)
10. Critchlow, S.E., Bowater, R.P. and Jackson, S.P. (1997) Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol., 7, 588-598 (Pubitemid 27335654)
11. Grawunder, U., Wilm, M., Wu, X., Kulesza, P., Wilson, T.E., Mann, M. and Lieber, M.R. (1997) Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature, 388, 492-495 (Pubitemid 27328929)
12. Frank, K.M., Sekiguchi, J.M., Seidl, K.J., Swat, W., Rathbun, G.A., Cheng, H.-L., Davidson, L., Kangaloo, L. and Alt, F.W. (1998) Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature, 396, 173-177 (Pubitemid 28523619)
13. Barnes, D.E., Stamp, G., Rosewell, I., Denzel, A. and Lindahl, T. (1998) Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice. Curr. Biol., 8, 1395-1398 (Pubitemid 29020149)
14. Frank, K.M., Sharpless, N.E., Gao, Y., Sekiguchi, J.M., Fergson, D.O., Zhu, C., Manis, J.P., Horner, J., DePinho, R.A. and Alt, F.W. (2000) DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell, 5, 993-1002
15. Sekiguchi, J.M., Ferguson, D.O., Chen, H.T., Yang, E.M., Earle, J., Frank, K., Whitlow, S., Gu, Y., Xu, Y., Nussenzweig, A. et al. (2001) Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc. Natl Acad. Sci. USA, 98, 3243-3028
16. Lee, Y., Barnes, D.E., Lindahl, T. and McKinnon, P.J. (2000) Defective neurogenesis resulting from DNA ligase IV deficiency requires Atm. Genes Dev., 14, 2576-2580
17. Lakshmipathy, U. and Campbell, C. (1999) The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell Biol., 19, 3869-3876 (Pubitemid 29193846)
18. Perez-Jannotti, R.M., Klein, S.M. and Bogenhagen, D.F. (2001) Two forms of mitochondrial DNA ligase III are produced in Xenopus laevis oocytes. J. Biol. Chem., 276, 48978-48987
19. Mackey, Z.B., Ramos, W., Levin, D.S., Walter, C.A., McCarrey, J.R. and Tomkinson, A.E. (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 (Pubitemid 27044397)
20. Frosina, G., Fortini, P., Rossi, O., Carrozzino, F., Raspaglio, G., Cox, L.S., Lane, D.P., Abbondandolo, A. and Dogliotti, E. (1996) Two pathways for base excision repair in mammalian cells. J. Biol. Chem., 271, 9573-9578 (Pubitemid 26137362)
21. Okano, S., Lan, L., Caldecott, K.W., Mori, T. and Yasui, A. (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell Biol., 23, 3974-3981 (Pubitemid 36597475)
22. Okano, S., Lan, L., Tomkinson, A.E. and Yasui, A. (2005) Translocation of XRCC1 and DNA ligase IIIa from centrosomes to chromosomes in response to DNA damage in mitotic human cells. Nucleic Acids Res., 33, 422-429 (Pubitemid 40276962)
23. Moser, J., Kool, H., Giakzidis, I., Caldecott, K., Mullenders, L.H.F. and Fousteri, M.I. (2007) Sealing of chromosomal DNA nicks during nucleotide excision repair requires XRCC1 and DNA ligase III[alpha] in a cell-cycle-specific manner. Mol. Cell, 27, 311-323 (Pubitemid 47058307)
24. Wang, H., Rosidi, B., Perrault, R., Wang, M., Zhang, L., Windhofer, F. and Iliakis, G. (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res., 65, 4020-4030 (Pubitemid 40775638)
25. Simsek, D., Brunet, E., Wong, S.Y.-W., Katyal, S., Gao, Y., McKinnon, P.J., Lou, J., Zhang, L., Li, J., Rebar, E.J. et al. (2011) DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet., 7, e1002080
26. Puebla-Osorio, N., Lacey, D.B., Alt, F.W. and Zhu, C. (2006) Early embryonic lethality due to targeted inactivation of dna ligase III. Mol. Cell Biol., 26, 3935-3941 (Pubitemid 43726408)
27. Simsek, D., Furda, A., Gao, Y., Artus, J., Brunet, E., Hadjantonakis, A.-K., Van Houten, B., Shuman, S., McKinnon, P.J. and Jasin, M. (2011) Crucial role for DNA ligase III in mitochondria but not in Xrcc1-dependent repair. Nature, 471, 245-248
28. Gao, Y., Katyal, S., Lee, Y., Zhao, J., Rehg, J.E., Russell, H.R. and McKinnon, P.J. (2011) DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature, 471, 240-244
29. Arakawa, H., Hauschild, J. and Buerstedde, J.-M. (2002) Requirement of the activation-induced deaminase (AID) gene for immunoglobulin gene conversion. Science, 295, 1301-1306 (Pubitemid 34157623)
30. Arakawa, H., Lodygin, D. and Buerstedde, J.-M. (2001) Mutant lox P vectors for selectable marker recycle and conditional knockouts. BMC Biotechnol., 1, 7
31. Zhang, Y., Riesterer, C., Ayrall, A.M., Sablitzky, F., Littlewood, T.D. and Reth, M. (1996) Inducible site-directed recombination in mouse embryonic stem cells. Nucleic Acids Res., 24, 543-548 (Pubitemid 26085826)
32. Tomkinson, A.E. and Mackey, Z.B. (1998) Structure and function of mammalian DNA ligases. Mutat. Res., 407, 1-9 (Pubitemid 28157166)
33. Pascal, J.M., O'Brien, P.J., Tomkinson, A.E. and Ellenberger, T. (2004) Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature, 432, 473-478 (Pubitemid 39576523)
34. Mackenney, V.J., Barnes, D.E. and Lindahl, T. (1997) Specific function of DNA ligase I in simian virus 40 DNA replication by human cell-free extracts is mediated by the amino-terminal non-catalytic domain. J. Biol. Chem., 272, 11550-11556 (Pubitemid 27184166)
35. Freie, B.W., Ciccone, S.L.M., Li, X., Plett, A., Orschell, C.M., Srour, E.F., Hanenberg, H., Schindler, D., Lee, S.-H. and Clapp, D.W. (2004) A role for the Fanconi anemia C protein in maintaining the DNA damage-induced G2 checkpoint. J. Biol. Chem., 279, 50986-50993 (Pubitemid 40017839)
36. Wang, C. and Youle, R.J. (2009) The role of mitochondria in apoptosis. Annu. Rev. Genet., 43, 95-118.