A specific N-terminal extension of the 8 kDa domain is required for DNA end-bridging by human Polμ and Polλ

Nucleic Acids Research

Volumn 41, Issue 19, 2013, Pages 9105-9116

  Martin, Maria Jose ^a,b   Garcia Ortiz, Maria Victoria ^a   Gomez Bedoya, Ana ^a   Esteban, Veronica ^a   Guerra, Susana ^a   Blanco, Luis ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE; DNA POLYMERASE; DNA POLYMERASE LAMBDA; DNA POLYMERASE MU; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL VIABILITY; CONTROLLED STUDY; CRYSTALLIZATION; DNA END JOINING REPAIR; HUMAN; IN VITRO STUDY; MUTATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SYNAPSE;

AMINO ACID SEQUENCE; CYCLIN-DEPENDENT KINASES; DNA; DNA END-JOINING REPAIR; DNA POLYMERASE BETA; DNA-DIRECTED DNA POLYMERASE; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84885974085     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt681     Document Type: Article

References (40)

1. Johnson, K.A. (2010) The kinetic and chemical mechanism of high-fidelity DNA polymerases. Biochim. Biophys. Acta, 1804, 1041-1048.
2. Sawaya, M.R., Prasad, R., Wilson, S.H., Kraut, J. and Pelletier, H. (1997) Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry, 36, 11205-11215.
3. Li, Y., Kong, Y., Korolev, S. and Waksman, G. (1998) Crystal structures of the Klenow fragment of Thermus aquaticus DNA polymerase I complexed with deoxyribonucleoside triphosphates. Protein Sci., 7, 1116-1123.
4. Doublie, S., Sawaya, M.R. and Ellenberger, T. (1999) An open and closed case for all polymerases. Structure, 7, R31-R35.
5. Holm, L. and Sander, C. (1995) DNA polymerase beta belongs to an ancient nucleotidyltransferase superfamily. Trends Biochem. Sci., 20, 345-347.
6. Brautigam, C.A. and Steitz, T.A. (1998) Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol., 8, 54-63.
7. Pelletier, H., Sawaya, M.R., Kumar, A., Wilson, S.H. and Kraut, J. (1994) Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP. Science, 264, 1891-1903.
8. Beard, W.A. and Wilson, S.H. (1998) Structural insights into DNA polymerase beta fidelity: hold tight if you want it right. Chem. Biol., 5, R7-R13.
9. Kunkel, T.A. and Bebenek, K. (2000) DNA replication fidelity. Annu. Rev. Biochem., 69, 497-529.
10. Beard, W.A., Shock, D.D. and Wilson, S.H. (2004) Influence of DNA structure on DNA polymerase beta active site function: extension of mutagenic DNA intermediates. J. Biol. Chem., 279, 31921-31929.
11. Garcia-Diaz, M., Bebenek, K., Krahn, J.M., Kunkel, T.A. and Pedersen, L.C. (2005) A closed conformation for the Pol lambda catalytic cycle. Nat. Struct. Mol. Biol., 12, 97-98.
12. Foley, M.C., Arora, K. and Schlick, T. (2006) Sequential side-chain residue motions transform the binary into the ternary state of DNA polymerase lambda. Biophys. J., 91, 3182-3195.
13. Moon, A.F., Garcia-Diaz, M., Bebenek, K., Davis, B.J., Zhong, X., Ramsden, D.A., Kunkel, T.A. and Pedersen, L.C. (2007) Structural insight into the substrate specificity of DNA Polymerase mu. Nat. Struct. Mol. Biol., 14, 45-53.
14. Li, Y. and Schlick, T. (2010) Modeling DNA polymerase mu motions: subtle transitions before chemistry. Biophys. J., 99, 3463-3472.
15. Ruiz, J.F., Dominguez, O., Lain de Lera, T., Garcia-Diaz, M., Bernad, A. and Blanco, L. (2001) DNA polymerase mu, a candidate hypermutase? Philos. Trans. R. Soc. Lond. B Biol. Sci., 356, 99-109.
16. Garcia-Diaz, M., Bebenek, K., Krahn, J.M., Blanco, L., Kunkel, T.A. and Pedersen, L.C. (2004) A structural solution for the DNA polymerase lambda-dependent repair of DNA gaps with minimal homology. Mol. Cell, 13, 561-572.
17. Garcia-Diaz, M., Bebenek, K., Gao, G., Pedersen, L.C., London, R.E. and Kunkel, T.A. (2005) Structure-function studies of DNA polymerase lambda. DNA Repair (Amst), 4, 1358-1367.
18. Martin, M.J., Juarez, R. and Blanco, L. (2012) DNA-binding determinants promoting NHEJ by human Polmu. Nucleic Acids Res., 40, 11389-11403.
19. Brissett, N.C., Pitcher, R.S., Juarez, R., Picher, A.J., Green, A.J., Dafforn, T.R., Fox, G.C., Blanco, L. and Doherty, A.J. (2007) Structure of a NHEJ polymerase-mediated DNA synaptic complex. Science, 318, 456-459.
20. Nick McElhinny, S.A., Havener, J.M., Garcia-Diaz, M., Juarez, R., Bebenek, K., Kee, B.L., Blanco, L., Kunkel, T.A. and Ramsden, D.A. (2005) A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining. Mol. Cell, 19, 357-366.
21. Garcia-Diaz, M., Bebenek, K., Sabariegos, R., Dominguez, O., Rodriguez, J., Kirchhoff, T., Garcia-Palomero, E., Picher, A.J., Juarez, R., Ruiz, J.F. et al. (2002) DNA polymerase lambda, a novel DNA repair enzyme in human cells. J. Biol. Chem., 277, 13184-13191.
22. Garcia-Diaz, M., Bebenek, K., Larrea, A.A., Havener, J.M., Perera, L., Krahn, J.M., Pedersen, L.C., Ramsden, D.A. and Kunkel, T.A. (2009) Template strand scrunching during DNA gap repair synthesis by human polymerase lambda. Nat. Struct. Mol. Biol., 16, 967-972.
23. Thode, S., Schafer, A., Pfeiffer, P. and Vielmetter, W. (1990) A novel pathway of DNA end-to-end joining. Cell, 60, 921-928.
24. Roth, D.B. and Wilson, J.H. (1986) Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell. Biol., 6, 4295-4304.
25. Kramer, K.M., Brock, J.A., Bloom, K., Moore, J.K. and Haber, J.E. (1994) Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52- independent, nonhomologous recombination events. Mol. Cell. Biol., 14, 1293-1301.
26. Ramsden, D.A. (2011) Polymerases in nonhomologous end joining: building a bridge over broken chromosomes. Antioxid. Redox Signal., 14, 2509-2519.
27. Mueller, G.A., Moon, A.F., Derose, E.F., Havener, J.M., Ramsden, D.A., Pedersen, L.C. and London, R.E. (2008) A comparison of BRCT domains involved in nonhomologous endjoining: introducing the solution structure of the BRCT domain of polymerase lambda. DNA Repair (Amst), 7, 1340-1351.
28. Matsumoto, T., Go, K., Hyodo, M., Koiwai, K., Maezawa, S., Hayano, T., Suzuki, M. and Koiwai, O. (2012) BRCT domain of DNA polymerase mu has DNA-binding activity and promotes the DNA polymerization activity. Genes Cells, 17, 790-806.
29. Martin, M.J., Juarez, R. and Blanco, L. (2012) DNA-binding determinants promoting NHEJ by human Polm. Nucleic Acids Res., 40, 11389-11403.
30. Fan, W. and Wu, X. (2004) DNA polymerase lambda can elongate on DNA substrates mimicking non-homologous end joining and interact with XRCC4-ligase IV complex. Biochem. Biophys. Res. Commun., 323, 1328-1333.
31. Fiala, K.A., Duym, W.W., Zhang, J. and Suo, Z. (2006) Upregulation of the fidelity of human DNA polymerase lambda by its non-enzymatic proline-rich domain. J. Biol. Chem., 281, 19038-19044.
32. Prasad, R., Beard, W.A., Strauss, P.R. and Wilson, S.H. (1998) Human DNA polymerase beta deoxyribose phosphate lyase. Substrate specificity and catalytic mechanism. J. Biol. Chem., 273, 15263-15270.
33. Garcia-Diaz, M., Bebenek, K., Kunkel, T.A. and Blanco, L. (2001) Identification of an intrinsic 5'-deoxyribose-5-phosphate lyase activity in human DNA polymerase lambda: a possible role in base excision repair. J. Biol. Chem., 276, 34659-34663.
34. Brissett, N.C., Martin, M.J., Pitcher, R.S., Bianchi, J., Juarez, R., Green, A.J., Fox, G.C., Blanco, L. and Doherty, A.J. (2011) Structure of a preternary complex involving a prokaryotic NHEJ DNA polymerase. Mol. Cell, 41, 221-231.
35. Boule, J.B., Rougeon, F. and Papanicolaou, C. (2001) Terminal deoxynucleotidyl transferase indiscriminately incorporates ribonucleotides and deoxyribonucleotides. J. Biol. Chem., 276, 31388-31393.
36. Nick McElhinny, S.A. and Ramsden, D.A. (2003) Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol. Cell. Biol., 23, 2309-2315.
37. Ruiz, J.F., Juarez, R., Garcia-Diaz, M., Terrados, G., Picher, A.J., Gonzalez-Barrera, S., Fernandez de Henestrosa, A.R. and Blanco, L. (2003) Lack of sugar discrimination by human Pol mu requires a single glycine residue. Nucleic Acids Res., 31, 4441-4449.
38. Martin, M.J., Garcia-Ortiz, M.V., Esteban, V. and Blanco, L. (2013) Ribonucleotides and manganese ions improve non-homologous end joining by human Polmu. Nucleic Acids Res., 41, 2428-2436.
39. Shevelev, I., Blanca, G., Villani, G., Ramadan, K., Spadari, S., Hubscher, U. and Maga, G. (2003) Mutagenesis of human DNA polymerase lambda: essential roles of Tyr505 and Phe506 for both DNA polymerase and terminal transferase activities. Nucleic Acids Res., 31, 6916-6925.
40. Matsuoka, S., Ballif, B.A., Smogorzewska, A., McDonald, E.R. 3rd, Hurov, K.E., Luo, J., Bakalarski, C.E., Zhao, Z., Solimini, N., Lerenthal, Y. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-1166.