Human polymerase kappa uses a template-slippage deletion mechanism, but can realign the slipped strands to favour base substitution mutations over deletions

Nucleic Acids Research

Volumn 41, Issue 9, 2013, Pages 5024-5035

  Mukherjee, Purba ^a,b   Lahiri, Indrajit ^a,b   Pata, Janice D ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE KAPPA; NUCLEOTIDE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARCHAEON; ARTICLE; BACTERIUM; BASE MISPAIRING; DNA SYNTHESIS; DNA TEMPLATE; FRAMESHIFT MUTATION; GENE DELETION; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

BASE SEQUENCE; DEOXYCYTOSINE NUCLEOTIDES; DNA; DNA-DIRECTED DNA POLYMERASE; HUMANS; MUTATION; NUCLEOTIDES; REPETITIVE SEQUENCES, NUCLEIC ACID; TEMPLATES, GENETIC;

EID: 84877247843     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt179     Document Type: Article

References (35)

1. Sale, J.E., Lehmann, A.R. and Woodgate, R. (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat. Rev. Mol. Cell Biol., 13, 141-152.
2. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., Kunkel, T.A., Lawrence, C.W., Livneh, Z., Nohmi, T. et al. (2001) The Y-family of DNA polymerases. Mol. Cell, 8, 7-8.
3. Jarosz, D.F., Godoy, V.G., Delaney, J.C., Essigmann, J.M. and Walker, G.C. (2006) A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature, 439, 225-228.
4. Kumari, A., Minko, I.G., Harbut, M.B., Finkel, S.E., Goodman, M.F. and Lloyd, R.S. (2008) Replication bypass of interstrand cross-link intermediates by Escherichia coli DNA polymerase IV. J. Biol. Chem., 283, 27433-27437.
5. Minko, I.G., Yamanaka, K., Kozekov, I.D., Kozekova, A., Indiani, C., O'Donnell, M.E., Jiang, Q., Goodman, M.F., Rizzo, C.J. and Lloyd, R.S. (2008) Replication bypass of the acrolein-mediated deoxyguanine DNA-peptide cross-links by DNA polymerases of the DinB family. Chem. Res. Toxicol., 21, 1983-1990.
6. Seo, K.Y., Nagalingam, A., Miri, S., Yin, J., Chandani, S., Kolbanovskiy, A., Shastry, A. and Loechler, E.L. (2006) Mirror image stereoisomers of the major benzo[a]pyrene N2-dG adduct are bypassed by different lesion-bypass DNA polymerases in E. coli. DNA Repair (Amst.), 5, 515-522.
7. Shen, X., Sayer, J.M., Kroth, H., Ponten, I., O'Donnell, M., Woodgate, R., Jerina, D.M. and Goodman, M.F. (2002) Efficiency and accuracy of SOS-induced DNA polymerases replicating benzo[a]pyrene-7, 8-diol 9, 10-epoxide A and G adducts. J. Biol. Chem., 277, 5265-5274.
8. Ogi, T., Shinkai, Y., Tanaka, K. and Ohmori, H. (2002) Polkappa protects mammalian cells against the lethal and mutagenic effects of benzo[a]pyrene. Proc. Natl Acad. Sci. USA, 99, 15548-15553.
9. Fiala, K.A. and Suo, Z. (2004) Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry, 43, 2106-2115.
10. Johnson, R.E., Prakash, S. and Prakash, L. (2000) The human DINB1 gene encodes the DNA polymerase Poltheta. Proc. Natl Acad. Sci. USA, 97, 3838-3843.
11. Potapova, O., Grindley, N.D. and Joyce, C.M. (2002) The mutational specificity of the Dbh lesion bypass polymerase and its implications. J. Biol. Chem., 277, 28157-28166.
12. Boudsocq, F., Kokoska, R.J., Plosky, B.S., Vaisman, A., Ling, H., Kunkel, T.A., Yang, W. and Woodgate, R. (2004) Investigating the role of the little finger domain of Y-family DNA polymerases in low fidelity synthesis and translesion replication. J. Biol. Chem., 279, 32932-32940.
13. Kim, S.R., Maenhaut-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., Nohmi, T. and Ohmori, H. (1997) Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc. Natl Acad. Sci. USA, 94, 13792-13797.
14. Kokoska, R.J., Bebenek, K., Boudsocq, F., Woodgate, R. and Kunkel, T.A. (2002) Low fidelity DNA synthesis by a y family DNA polymerase due to misalignment in the active site. J. Biol. Chem., 277, 19633-19638.
15. Ohashi, E., Bebenek, K., Matsuda, T., Feaver, W.J., Gerlach, V.L., Friedberg, E.C., Ohmori, H. and Kunkel, T.A. (2000) Fidelity and processivity of DNA synthesis by DNA polymerase kappa, the product of the human DINB1 gene. J. Biol. Chem., 275, 39678-39684.
16. Washington, M.T., Johnson, R.E., Prakash, L. and Prakash, S. (2002) Human DINB1-encoded DNA polymerase kappa is a promiscuous extender of mispaired primer termini. Proc. Natl Acad. Sci. USA, 99, 1910-1914.
17. Wolfle, W.T., Washington, M.T., Prakash, L. and Prakash, S. (2003) Human DNA polymerase kappa uses template-primer misalignment as a novel means for extending mispaired termini and for generating single-base deletions. Genes Dev., 17, 2191-2199.
18. Garcia-Diaz, M. and Kunkel, T.A. (2006) Mechanism of a genetic glissando: structural biology of indel mutations. Trends Biochem. Sci., 31, 206-214.
19. Streisinger, G., Okada, Y., Emrich, J., Newton, J., Tsugita, A., Terzaghi, E. and Inouye, M. (1966) Frameshift mutations and the genetic code. Cold Spring Harb. Symp. Quant. Biol., 31, 77-84.
20. Kunkel, T.A. and Soni, A. (1988) Mutagenesis by transient misalignment. J. Biol. Chem., 263, 14784-14789.
21. Bebenek, K. and Kunkel, T.A. (1990) Frameshift errors initiated by nucleotide misincorporation. Proc. Natl Acad. Sci. USA, 87, 4946-4950.
22. Bloom, L.B., Chen, X., Fygenson, D.K., Turner, J., O'Donnell, M. and Goodman, M.F. (1997) Fidelity of Escherichia coli DNA polymerase III holoenzyme. The effects of beta, gamma complex processivity proteins and epsilon proofreading exonuclease on nucleotide misincorporation efficiencies. J. Biol. Chem., 272, 27919-27930.
23. Efrati, E., Tocco, G., Eritja, R., Wilson, S.H. and Goodman, M.F. (1997) Abasic translesion synthesis by DNA polymerase beta violates the "A-rule" Novel types of nucleotide incorporation by human DNA polymerase beta at an abasic lesion in different sequence contexts. J. Biol. Chem., 272, 2559-2569.
24. Kunkel, T.A. (1986) Frameshift mutagenesis by eucaryotic DNA polymerases in vitro. J. Biol. Chem., 261, 13581-13587.
25. Lone, S., Townson, S.A., Uljon, S.N., Johnson, R.E., Brahma, A., Nair, D.T., Prakash, S., Prakash, L. and Aggarwal, A.K. (2007) Human DNA polymerase kappa encircles DNA: implications for mismatch extension and lesion bypass. Mol. cell, 25, 601-614.
26. Uljon, S.N., Johnson, R.E., Edwards, T.A., Prakash, S., Prakash, L. and Aggarwal, A.K. (2004) Crystal structure of the catalytic core of human DNA polymerase kappa. Structure, 12, 1395-1404.
27. Wilson, R.C. and Pata, J.D. (2008) Structural insights into the generation of single-base deletions by the Y family DNA polymerase dbh. Mol. Cell, 29, 767-779.
28. Wu, Y., Wilson, R.C. and Pata, J.D. (2011) The Y-family DNA polymerase Dpo4 uses a template slippage mechanism to create single-base deletions. J. Bacteriol., 193, 2630-2636.
29. Carlson, K.D., Johnson, R.E., Prakash, L., Prakash, S. and Washington, M.T. (2006) Human DNA polymerase kappa forms nonproductive complexes with matched primer termini but not with mismatched primer termini. Proc. Natl Acad. Sci. USA, 103, 15776-15781.
30. Foti, J.J. and Walker, G.C. (2011) Efficient extension of slipped DNA intermediates by DinB is required to escape primer template realignment by DnaQ. J. Bacteriol., 193, 2637-2641.
31. DeLucia, A.M., Grindley, N.D. and Joyce, C.M. (2007) Conformational changes during normal and error-prone incorporation of nucleotides by a Y-family DNA polymerase detected by 2-aminopurine fluorescence. Biochemistry, 46, 10790-10803.
32. Foti, J.J., Delucia, A.M., Joyce, C.M. and Walker, G.C. (2010) UmuD(2) inhibits a non-covalent step during DinB-mediated template slippage on homopolymeric nucleotide runs. J. Biol. Chem., 285, 23086-23095.
33. Ling, H., Boudsocq, F., Woodgate, R. and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: a mechanism for error-prone and lesion-bypass replication. Cell, 107, 91-102.
34. Vasquez-Del Carpio, R., Silverstein, T.D., Lone, S., Swan, M.K., Choudhury, J.R., Johnson, R.E., Prakash, S., Prakash, L. and Aggarwal, A.K. (2009) Structure of human DNA polymerase kappa inserting dATP opposite an 8-OxoG DNA lesion. PLoS One, 4, e5766.
35. Wilson, R.C., Jackson, M.A. and Pata, J.D. (2013) Y-family polymerase conformation is a major determinant of fidelity and translesion specificity. Structure, 21, 20-31.