Promiscuous DNA synthesis by human DNA polymerase θ

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2611-2622

  Hogg, Matthew ^a   Sauer Eriksson, A Elisabeth ^a   Johansson, Erik ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE THETA; DOUBLE STRANDED DNA; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; DNA SYNTHESIS; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME SUBSTRATE; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEADY STATE;

BASE PAIR MISMATCH; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA-DIRECTED DNA POLYMERASE; HUMANS; OLIGONUCLEOTIDES;

EID: 84859313681     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1102     Document Type: Article

References (47)

1. Seki, M., Marini, F. and Wood, R.D. (2003) POLQ (Pol theta), a DNA polymerase and DNA-dependent ATPase in human cells. Nucleic Acids Res., 31, 6117-6126 (Pubitemid 37442339)
2. Bebenek, K., Joyce, C.M., Fitzgerald, M.P. and Kunkel, T.A. (1990) The fidelity of DNA synthesis catalyzed by derivatives of Escherichia coli DNA polymerase I. J. Biol. Chem., 265, 13878-13887
3. Arana, M.E., Seki, M., Wood, R.D., Rogozin, I.B. and Kunkel, T.A. (2008) Low-fidelity DNA synthesis by human DNA polymerase theta. Nucleic Acids Res., 36, 3847-3856 (Pubitemid 351917544)
4. Seki, M. and Wood, R.D. (2008) DNA polymerase theta (POLQ) can extend from mismatches and from bases opposite a (6-4) photoproduct. DNA Repair, 7, 119-127 (Pubitemid 350184409)
5. Hogg, M., Seki, M., Wood, R.D., Doublié , S. and Wallace, S.S. (2011) Lesion bypass activity of DNA polymerase theta (POLQ) is an intrinsic property of the pol domain and depends on unique sequence inserts. J. Mol. Biol., 405, 642-652
6. Seki, M., Masutani, C., Yang, L.W., Schuffert, A., Iwai, S., Bahar, I. and Wood, R.D. (2004) High-efficiency bypass of DNA damage by human DNA polymerase Q. EMBO J., 23, 4484-4494 (Pubitemid 39601973)
7. Prasad, R., Longley, M.J., Sharief, F.S., Hou, E.W., Copeland, W.C. and Wilson, S.H. (2009) Human DNA polymerase theta possesses 50-dRP lyase activity and functions in single-nucleotide base excision repair in vitro. Nucleic Acids Res., 37, 1868-1877
8. Masuda, K., Ouchida, R., Takeuchi, A., Saito, T., Koseki, H., Kawamura, K., Tagawa, M., Tokuhisa, T., Azuma, T. and OWang, J. (2005) DNA polymerase theta contributes to the generation of C/G mutations during somatic hypermutation of Ig genes. Proc. Natl Acad. Sci. USA, 102, 13986-13991 (Pubitemid 41377690)
9. Masuda, K., Ouchida, R., Hikida, M., Kurosaki, T., Yokoi, M., Masutani, C., Seki, M., Wood, R.D., Hanaoka, F. and O-Wang, J. (2007) DNA polymerases eta and theta function in the same genetic pathway to generate mutations at A/T during somatic hypermutation of Ig genes. J. Biol. Chem., 282, 17387-17394 (Pubitemid 47100269)
10. Masuda, K., Ouchida, R., Hikida, M., Nakayama, M., Ohara, O., Kurosaki, T. and O-Wang, J. (2006) Absence of DNA polymerase theta results in decreased somatic hypermutation frequency and altered mutation patterns in Ig genes. DNA Repair, 5, 1384-1391 (Pubitemid 44573934)
11. Zan, H., Shima, N., Xu, Z., Al-Qahtani, A., Evinger Iii, A.J., Zhong, Y., Schimenti, J.C. and Casali, P. (2005) The translesion DNA polymerase theta plays a dominant role in immunoglobulin gene somatic hypermutation. EMBO J., 24, 3757-3769 (Pubitemid 41581692)
12. Seki, M., Gearhart, P.J. and Wood, R.D. (2005) DNA polymerases and somatic hypermutation of immunoglobulin genes. EMBO Rep., 6, 1143-1148 (Pubitemid 41741697)
13. Martomo, S.A., Saribasak, H., Yokoi, M., Hanaoka, F. and Gearhart, P.J. (2008) Reevaluation of the role of DNA polymerase theta in somatic hypermutation of immunoglobulin genes. DNA Repair, 7, 1603-1608
14. Yoshimura, M., Kohzaki, M., Nakamura, J., Asagoshi, K., Sonoda, E., Hou, E., Prasad, R., Wilson, S.H., Tano, K., Yasui, A. et al. (2006) Vertebrate POLQ and POL beta cooperate in base excision repair of oxidative DNA damage. Mol. Cell, 24, 115-125 (Pubitemid 44488583)
15. Garcia-Diaz, M., Bebenek, K., Kunkel, T.A. and Blanco, L. (2001) Identification of an intrinsic 50-deoxyribose-5-phosphate lyase activity in human DNA polymerase lambda: a possible role in base excision repair. J. Biol. Chem., 276, 34659-34663
16. Blanca, G., Villani, G., Shevelev, I., Ramadan, K., Spadari, S., Hubscher, U. and Maga, G. (2004) Human DNA polymerases lambda and beta show different efficiencies of translesion DNA synthesis past abasic sites and alternative mechanisms for frameshift generation. Biochemistry, 43, 11605-11615 (Pubitemid 39186982)
17. Goff, J.P., Shields, D.S., Seki, M., Choi, S., Epperly, M.W., Dixon, T., Wang, H., Bakkenist, C.J., Dertinger, S.D., Torous, D.K. et al. (2009) Lack of DNA polymerase theta (POLQ) radiosensitizes bone marrow stromal cells in vitro and increases reticulocyte micronuclei after total-body irradiation. Radiat. Res., 172, 165-174
18. Higgins, G.S., Prevo, R., Lee, Y.F., Helleday, T., Muschel, R.J., Taylor, S., Yoshimura, M., Hickson, I.D., Bernhard, E.J. and McKenna, W.G. (2010) A small interfering RNA screen of genes involved in DNA repair identifies tumor-specific radiosensitization by POLQ knockdown. Cancer Res., 70, 2984-2993
19. Ukai, A., Maruyama, T., Mochizuki, S., Ouchida, R., Masuda, K., Kawamura, K., Tagawa, M., Kinoshita, K., Sakamoto, A., Tokuhisa, T. et al. (2006) Role of DNA polymerase theta in tolerance of endogenous and exogenous DNA damage in mouse B cells. Genes Cells, 11, 111-121
20. Shima, N., Hartford, S.A., Duffy, T., Wilson, L.A., Schimenti, K.J. and Schimenti, J.C. (2003) Phenotype-based identification of mouse chromosome instability mutants. Genetics, 163, 1031-1040 (Pubitemid 36417944)
21. Shima, N., Munroe, R.J. and Schimenti, J.C. (2004) The mouse genomic instability mutation chaos1 is an allele of Polq that exhibits genetic interaction with Atm. Mol. Cell Biol., 24, 10381-10389 (Pubitemid 39507874)
22. Lee, J.H. and Paull, T.T. (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene, 26, 7741-7748 (Pubitemid 350242454)
23. Muzzini, D.M., Plevani, P., Boulton, S.J., Cassata, G. and Marini, F. (2008) Caenorhabditis elegans POLQ-1 and HEL-308 function in two distinct DNA interstrand cross-link repair pathways. DNA Repair, 7, 941-950
24. Hogg, M., Wallace, S.S. and Doublié , S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site. EMBO J., 23, 1483-1493 (Pubitemid 38579509)
25. Hogg, M., Aller, P., Konigsberg, W., Wallace, S.S. and Doublié , S. (2007) Structural and biochemical investigation of the role in proofreading of a beta hairpin loop found in the exonuclease domain of a replicative DNA polymerase of the B family. J. Biol. Chem., 282, 1432-1444 (Pubitemid 47076520)
26. Clark, J.M. (1988) Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res., 16, 9677-9686
27. Just, A., Butter, F., Trenkmann, M., Heitkam, T., Morl, M. and Betat, H. (2008) A comparative analysis of two conserved motifs in bacterial poly(A) polymerase and CCA-adding enzyme. Nucleic Acids Res., 36, 5212-5220
28. Gilfillan, S., Benoist, C. and Mathis, D. (1995) Mice lacking terminal deoxynucleotidyl transferase: adult mice with a fetal antigen receptor repertoire. Immunol. Rev., 148, 201-219 (Pubitemid 26010548)
29. Davis, B.J., Havener, J.M. and Ramsden, D.A. (2008) End-bridging is required for pol mu to efficiently promote repair of noncomplementary ends by nonhomologous end joining. Nucleic Acids Res., 36, 3085-3094 (Pubitemid 351737200)
30. 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 (Pubitemid 41074891)
31. Juarez, R., Ruiz, J.F., Nick McElhinny, S.A., Ramsden, D. and Blanco, L. (2006) A specific loop in human DNA polymerase mu allows switching between creative and DNA-instructed synthesis. Nucleic Acids Res., 34, 4572-4582 (Pubitemid 44574152)
32. Kato, K.I., Goncalves, J.M., Houts, G.E. and Bollum, F.J. (1967) Deoxynucleotide-polymerizing enzymes of calf thymus gland. II. Properties of the terminal deoxynucleotidyltransferase. J. Biol. Chem., 242, 2780-2789
33. Boule, J.B., Rougeon, F. and Papanicolaou, C. (2001) Terminal deoxynucleotidyl transferase indiscriminately incorporates ribonucleotides and deoxyribonucleotides. J. Biol. Chem., 276, 31388-31393 (Pubitemid 37385010)
34. Nick McElhinny, S.A. and Ramsden, D.A. (2003) Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol. Cell. Biol., 23, 2309-2315 (Pubitemid 36351014)
35. Covo, S., Blanco, L. and Livneh, Z. (2004) Lesion bypass by human DNA polymerase mu reveals a template-dependent, sequence-independent nucleotidyl transferase activity. J. Biol. Chem., 279, 859-865 (Pubitemid 38082605)
36. Ramsden, D.A. (2011) Polymerases in Nonhomologous End Joining: building a Bridge over Broken Chromosomes. Antioxid. Redox Signal., 14, 2509-2519
37. Kawamura, K., Bahar, R., Seimiya, M., Chiyo, M., Wada, A., Okada, S., Hatano, M., Tokuhisa, T., Kimura, H., Watanabe, S. et al. (2004) DNA polymerase theta is preferentially expressed in lymphoid tissues and upregulated in human cancers. Int. J. Cancer, 109, 9-16 (Pubitemid 38160656)
38. Gilfillan, S., Benoist, C. and Mathis, D. (1995) Mice lacking terminal deoxynucleotidyl transferase: adult mice with a fetal antigen receptor repertoire. Immunol. Rev., 148, 201-219 (Pubitemid 26010548)
39. Cabaniols, J.P., Fazilleau, N., Casrouge, A., Kourilsky, P. and Kanellopoulos, J.M. (2001) Most alpha/beta T cell receptor diversity is due to terminal deoxynucleotidyl transferase. J. Exp. Med., 194, 1385-1390 (Pubitemid 33055055)
40. Lieber, M.R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem., 79, 181-211
41. McVey, M. and Lee, S.E. (2008) MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet., 24, 529-538
42. Chan, S.H., Yu, A.M. and McVey, M. (2010) Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLoS Genet., 6, e1001005
43. Zuo, Z., Lin, H.K. and Trakselis, M.A. (2011) Strand Annealing and Terminal Transferase Activities of a B-family DNA Polymerase. Biochemistry, 50, 5379-5390
44. Lemé e, F., Bergoglio, V., Fernandez-Vidal, A., Machado-Silva, A., Pillaire, M.-J., Bieth, A., Gentil, C., Baker, L., Martin, A.-L., Leduc, C. et al. (2010) DNA polymeraseup-regulation is associated with poor survival in breast cancer, perturbs DNA replication and promotes genetic instability Proc. Natl Acad. Sci. USA, 107, 13390-13395
45. Pillaire, M.J., Selves, J., Gordien, K., Gourraud, P.A., Gentil, C., Danjoux, M., Do, C., Negre, V., Bieth, A., Guimbaud, R. et al. (2010) A 'DNA replication' signature of progression and negative outcome in colorectal cancer. Oncogene, 29, 876-887
46. Higgins, G.S., Harris, A.L., Prevo, R., Helleday, T., McKenna, W.G. and Buffa, F.M. (2010) Overexpression of POLQ confers a poor prognosis in early breast cancer patients. Oncotarget., 1, 175-184
47. Lange, S.S., Takata, K. and Wood, R.D. (2011) DNA polymerases and cancer. Nat. Rev. Cancer, 11, 96-110.