A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining

Molecular Cell

Volumn 19, Issue 3, 2005, Pages 357-366

  McElhinny, Stephanie A Nick ^a,b   Havener, Jody M ^b   Garcia Diaz, Miguel ^c   Juárez, Raquel ^d   Bebenek, Katarzyna ^c   Kee, Barbara L ^e   Blanco, Luis ^d   Kunkel, Thomas A ^c   Ramsden, Dale A ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE;

ACCURACY; ANIMAL CELL; ARTICLE; CORRELATION ANALYSIS; DNA TEMPLATE; ENZYME ACTIVITY; IMMUNITY; IN VIVO STUDY; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PROTEIN SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; B-LYMPHOCYTES; CELL LINE; DNA; DNA NUCLEOTIDYLEXOTRANSFERASE; DNA POLYMERASE BETA; DNA REPAIR; DNA-DIRECTED DNA POLYMERASE; GENE EXPRESSION; GENE REARRANGEMENT; HUMANS; IMMUNOGLOBULIN JOINING REGION; IMMUNOGLOBULIN KAPPA-CHAINS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; RECOMBINATION, GENETIC; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; TEMPLATES, GENETIC; TRANSFECTION;

MAMMALIA;

EID: 23044453811     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.06.012     Document Type: Article

References (44)

1. S. Aoufouchi, E. Flatter, A. Dahan, A. Faili, B. Bertocci, S. Storck, F. Delbos, L. Cocea, N. Gupta, J.C. Weill, and C.A. Reynaud Two novel human and mouse DNA polymerases of the polX family Nucleic Acids Res. 28 2000 3684 3693
2. K. Bebenek, M. Garcia-Diaz, L. Blanco, and T.A. Kunkel The frameshift infidelity of human DNA polymerase lambda. Implications for function J. Biol. Chem. 278 2003 34685 34690
3. K. Bebenek, and T.A. Kunkel DNA repair and replication W. Yang Advances in Protein Chemistry 2004 Elsevier Press San Diego 137 159
4. B. Bertocci, A. De Smet, E. Flatter, A. Dahan, J.C. Bories, C. Landreau, J.C. Weill, and C.A. Reynaud Cutting edge: DNA polymerases mu and lambda are dispensable for Ig gene hypermutation J. Immunol. 168 2002 3702 3706
5. B. Bertocci, A. De Smet, C. Berek, J.C. Weill, and C.A. Reynaud Immunoglobulin kappa light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu Immunity 19 2003 203 211
6. J. Budman, and G. Chu Processing of DNA for nonhomologous end-joining by cell-free extract EMBO J. 24 2005 849 860
7. P.M. Burgers, E.V. Koonin, E. Bruford, L. Blanco, K.C. Burtis, M.F. Christman, W.C. Copeland, E.C. Friedberg, F. Hanaoka, and D.C. Hinkle Eukaryotic DNA polymerases: proposal for a revised nomenclature J. Biol. Chem. 276 2001 43487 43490
8. Y. Chang, and M.L. Brown Formation of coding joints in V(D)J recombination-inducible severe combined immune deficient pre-B cell lines Proc. Natl. Acad. Sci. USA 96 1999 191 196
9. Y.Y. Chen, L.C. Wang, M.S. Huang, and N. Rosenberg An active v-abl protein tyrosine kinase blocks immunoglobulin light-chain gene rearrangement Genes Dev. 8 1994 688 697
10. S. Covo, L. Blanco, and Z. Livneh Lesion bypass by human DNA polymerase mu reveals a template-dependent, sequence-independent nucleotidyl transferase activity J. Biol. Chem. 279 2004 859 865
11. M. Delarue, J.B. Boule, J. Lescar, N. Expert-Bezancon, N. Jourdan, N. Sukumar, F. Rougeon, and C. Papanicolaou Crystal structures of a template-independent DNA polymerase: murine terminal deoxynucleotidyltransferase EMBO J. 21 2002 427 439
12. M. Della, P.L. Palmbos, H.M. Tseng, L.M. Tonkin, J.M. Daley, L.M. Topper, R.S. Pitcher, A.E. Tomkinson, T.E. Wilson, and A.J. Doherty Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine Science 306 2004 683 685
13. O. Dominguez, J.F. Ruiz, T. Lain de Lera, M. Garcia-Diaz, M.A. Gonzalez, T. Kirchhoff, A.C. Martinez, A. Bernad, and L. Blanco DNA polymerase mu (Pol mu), homologous to TdT, could act as a DNA mutator in eukaryotic cells EMBO J. 19 2000 1731 1742
14. J.B. Duvauchelle, L. Blanco, R.P. Fuchs, and A.M. Cordonnier Human DNA polymerase mu (Pol mu) exhibits an unusual replication slippage ability at AAF lesion Nucleic Acids Res. 30 2002 2061 2067
15. W. Fan, and X. Wu 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 2004 1328 1333
16. M. Garcia-Diaz, O. Dominguez, L.A. Lopez-Fernandez, L.T. de Lera, M.L. Saniger, J.F. Ruiz, M. Parraga, M.J. Garcia-Ortiz, T. Kirchhoff, and J. del Mazo DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis J. Mol. Biol. 301 2000 851 867
17. M. Garcia-Diaz, K. Bebenek, R. Sabariegos, O. Dominguez, J. Rodriguez, T. Kirchhoff, E. Garcia-Palomero, A.J. Picher, R. Juarez, and J.F. Ruiz DNA polymerase lambda, a novel DNA repair enzyme in human cells J. Biol. Chem. 277 2002 13184 13191
18. M. Garcia-Diaz, K. Bebenek, J.M. Krahn, L. Blanco, T.A. Kunkel, and L.C. Pedersen A structural solution for the DNA polymerase lambda-dependent repair of DNA gaps with minimal homology Mol. Cell 13 2004 561 572
19. S. Gilfillan, C. Benoist, and D. Mathis Mice lacking terminal deoxynucleotidyl transferase: adult mice with a fetal antigen receptor repertoire Immunol. Rev. 148 1995 201 219
20. Y. Kobayashi, M. Watanabe, Y. Okada, H. Sawa, H. Takai, M. Nakanishi, Y. Kawase, H. Suzuki, K. Nagashima, K. Ikeda, and N. Motoyama Hydrocephalus, situs inversus, chronic sinusitis, and male infertility in DNA polymerase lambda-deficient mice: possible implication for the pathogenesis of immotile cilia syndrome Mol. Cell. Biol. 22 2002 2769 2776
21. K.M. Kramer, J.A. Brock, K. Bloom, J.K. Moore, and J.E. Haber Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events Mol. Cell. Biol. 14 1994 1293 1301
22. P.J. Kraulis MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24 1991 946 950
23. J.W. Lee, L. Blanco, T. Zhou, M. Garcia-Diaz, K. Bebenek, T.A. Kunkel, Z. Wang, and L.F. Povirk Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts J. Biol. Chem. 279 2004 805 811
24. Y. Ma, U. Pannicke, K. Schwarz, and M.R. Lieber Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination Cell 108 2002 781 794
25. Y. Ma, H. Lu, B. Tippin, M.F. Goodman, N. Shimazaki, O. Koiwai, C.L. Hsieh, K. Schwarz, and M.R. Lieber A biochemically defined system for mammalian nonhomologous DNA end joining Mol. Cell 16 2004 701 713
26. K.N. Mahajan, S.A Nick McElhinny, B.S. Mitchell, and D.A. Ramsden Association of DNA polymerase μ (pol μ) with ku and ligase IV: role for pol μ in end-joining double-strand break repair Mol. Cell Biol. 22 2002 5194 5202
27. E.A. Merritt, and D.J. Bacon Raster3D: photorealistic molecular graphics Methods Enzymol. 277 1997 505 524
28. J.P. Morgenstern, and H. Land Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line Nucleic Acids Res. 18 1990 3587 3596
29. S.A. Nick McElhinny, and D.A. Ramsden Polymerase mu is a DNA-directed DNA/RNA polymerase Mol. Cell. Biol. 23 2003 2309 2315
30. S.A. Nick McElhinny, C.M. Snowden, J. McCarville, and D.A. Ramsden Ku recruits the XRCC4-ligase IV complex to DNA ends Mol. Cell. Biol. 20 2000 2996 3003
31. E.J. Perkins, A. Nair, D.O. Cowley, T. Van Dyke, Y. Chang, and D.A. Ramsden Sensing of intermediates in V(D)J recombination by ATM Genes Dev. 16 2000 159 164
32. R. Prasad, A. Kumar, S.G. Widen, J.R. Casas-Finet, and S.H. Wilson Identification of residues in the single-stranded DNA-binding site of the 8-kDa domain of rat DNA polymerase beta by UV cross-linking J. Biol. Chem. 268 1993 22746 22755
33. D.A. Ramsden, and M. Gellert Formation and resolution of double-strand break intermediates in V(D)J rearrangement Genes Dev. 9 1995 2409 2420
34. D.A. Ramsden, C.J. Paige, and G.E. Wu Kappa light chain rearrangement in mouse fetal liver J. Immunol. 153 1994 1150 1160
35. S. Rooney, J. Chaudhuri, and F.W. Alt The role of the non-homologous end-joining pathway in lymphocyte development Immunol. Rev. 200 2004 115 131
36. D.B. Roth, and J.H. Wilson Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction Mol. Cell. Biol. 6 1986 4295 4304
37. M.S. Schlissel Structure of nonhairpin coding-end DNA breaks in cells undergoing V(D)J recombination Mol. Cell. Biol. 18 1998 2029 2037
38. T. Schwede, J. Kopp, N. Guex, and M.C. Peitsch SWISS-MODEL: an automated protein homology-modeling server Nucleic Acids Res. 31 2003 3381 3385
39. S. Thode, A. Schafer, P. Pfeiffer, and W. Vielmetter A novel pathway of DNA end-to-end joining Cell 60 1990 921 928
40. B. Tippin, S. Kobayashi, J.G. Bertram, and M.F. Goodman To slip or skip, visualizing frameshift mutation dynamics for error-prone DNA polymerases J. Biol. Chem. 279 2004 45360 45368
41. H.M. Tseng, and A.E. Tomkinson A physical and functional interaction between yeast Pol4 and Dnl4-Lif1 links DNA synthesis and ligation in nonhomologous end joining J. Biol. Chem. 277 2002 45630 45637
42. T.E. Wilson, and M.R. Lieber Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway J. Biol. Chem. 274 1999 23599 23609
43. Y. Zhang, X. Wu, F. Yuan, Z. Xie, and Z. Wang Highly frequent frameshift DNA synthesis by human DNA polymerase mu Mol. Cell. Biol. 21 2001 7995 8006
44. Y. Zhang, X. Wu, D. Guo, O. Rechkoblit, J.S. Taylor, N.E. Geacintov, and Z. Wang Lesion bypass activities of human DNA polymerase mu J. Biol. Chem. 277 2002 44582 44587