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Translesion DNA polymerases Pol ζ, Pol η, Pol ι, Pol κ and Rev1 are not essential for repeat-induced point mutation inNeurospora crassa

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Abstract

Pol ζ, Pol η, Pol ι, Pol κ and Rev1 are specialized DNA polymerases that are able to synthesize DNA across a damaged template. DNA synthesis by such translesion polymerases can be mutagenic due to the miscoding nature of most damaged nucleotides. In fact, many mutational and hypermutational processes in systems ranging from yeast to mammals have been traced to the activity of such polymerases. We show however, that the translesion polymerases are dispensable for repeat-induced point mutation (RIP) inNeurospora crassa. Additionally, we demonstrate that theupr-1 gene, which encodes the catalytic subunit of Pol ζ, is a highly polymorphic locus in Neurospora.

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Abbreviations

NER:

Nucleotide excision repair

ORF:

open reading frame

RIP:

repeat-induced print mutation

uORFs:

upstream out-of-frame ORFs

References

  • Bhat A, Tamuli R and Kasbekar D P 2004 Genetic transformation ofNeurospora tetrasperma, demonstration of repeat-induced point mutation (RIP) in self-crosses and a screen for recessive RIP-defective mutants;Genetics 167 1155–1164

    Article  CAS  Google Scholar 

  • Bhat A, Noubissi F K, Vyas M and Kasbekar D P 2003 Genetic analysis of wild-isolatedNeurospora crassa strains identified as dominant suppressors of repeat-induced point mutation;Genetics 164 947–961

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bebenek K, Tissier A, Frank E G, McDonald J P, Prasad R, Wilson S H, Woodgate R and Kunkel T A 2001 5’-deoxyribose phosphate lyase activity of human DNA polymerase ι in vitro;Science 291 2156–2158

    Article  CAS  Google Scholar 

  • Borkovich K A, Alex L A, Yarden O, Freitag M, Turner G Eet al 2004 Lessons from the genome sequence ofNeurospora crassa: Tracing the path from genetic blueprint to multicellular organism;Microbiol. Mol. Biol. Rev. 68 1–108

    Article  CAS  Google Scholar 

  • Bruchez J J P, Eberli J. and Russo V E A 1993 Regulatory sequences involved in the translation ofNeurospora crassa mRNA: Kozak sequences and stop codons;Fungal Genet. Newslett 40 85–88

    Google Scholar 

  • Cambareri E B, Hensen B C, Schabtach E and Selker E U 1989 Repeat-induced G-C to A-T mutations in Neurospora;Science 244 1571–1575

    Article  CAS  Google Scholar 

  • Datta A and Jinks-Robertson S 1995 Association of increased spontaneous mutation rates with high levels of transcription in yeast;Science 268 1616–1619

    Article  CAS  Google Scholar 

  • Davis R H and De Serres F J 1970 Genetic and microbiological research techniques forNeurospora crassa;Methods Enzymol 17 79–143

    Article  Google Scholar 

  • Diaz M, Watson N B, Turkington G, Verkoczy L K, Klinman N R and McGregor W G 2003 Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in thehprt gene of mouse fibroblasts expressing antisense RNA to DNA polymerase ζ;Mol. Cancer Res. 1 836–847

    CAS  PubMed  Google Scholar 

  • Galagan J E, Calvo S E, Borkovich K A, Selker E U, Read N Det al 2003 The genome sequence of the filamentous fungusNeurospora crassa;Nature (London) 422 859–868

    Article  CAS  Google Scholar 

  • Galagan J E and Selker E U 2004 RIP: the evolutionary cost of genome defense;Trends Genet. 20 417–423

    Article  CAS  Google Scholar 

  • Gibbs P E M, McGregor W G, Maher V M, Nisson P and Lawrence C W 1998 A human homolog of theSaccharomyces cerevisiae REV3 gene, which encodes the catalytic subunit of DNA polymerase ζ;Proc. Natl. Acad. Sci. USA 95 6876–6880

    Article  CAS  Google Scholar 

  • Gibbs P E M, McDonald J, Woodgate R and Lawrence C W 2005 The relative rolesin vivo ofSaccharomyces cerevisiae Pol η, Pol ζ, Rev1 protein and Pol 32 in the bypass and mutation induction of an abasic site, T-T (6–4) photoadduct and T-T cis-syn cyclobutane dimmer;Genetics 169 575–582

    Article  CAS  Google Scholar 

  • Haracska L, Prakash L and Prakash S 2002 Role of human DNA polymerase κ as an extender in translesion synthesis;Proc. Natl. Acad. Sci. USA 99 16000–16005

    Article  CAS  Google Scholar 

  • Haracska L, Prakash S and Prakash L 2003 Yeast DNA polymerase ζ is an efficient extender of primer ends opposite from 7,8-dihydro-8-oxoguanine and O6 -methylguanine;Mol. Cell. Biol. 23 1453–1459

    Article  CAS  Google Scholar 

  • Holbeck S L and Strathern J N 1997 A role for REV3 in mutagenesis during double-strand break repair inSaccharomyces cerevisiae;Genetics 147 1017–1024

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson R E, Washington M T, Haracska L, Prakash S and Prakash L. 2000 Eucaryotic polymerases ι and ζ act sequentially to bypass DNA lesions;Nature (London) 406 1015–1019

    Article  CAS  Google Scholar 

  • Kozmin S G, Pavlov Y I, Kunkel T A and Sage E 2003 Roles ofSaccharomyces cerevisiae DNA polymerases Pol η and Pol ζ in response to simulated sunlight;Nucleic Acids Res. 31 4541–4552

    Article  CAS  Google Scholar 

  • Lawrence C W 2002 Cellular roles of DNA polymerase ζ and Rev 1 protein;DNA Repair 1 425–435

    Article  CAS  Google Scholar 

  • Lemontt J F 1971 Mutants of yeast defective in mutation induced by ultraviolet light;Genetics 68 21–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livneh Z 2001 DNA damage control by novel DNA polymerases: translesion replication and mutagenesis;J. Biol. Chem. 276 25639–25642

    Article  CAS  Google Scholar 

  • McDonald J P, Tissier A, Frank E G, Iwai S, Hanaoka F and Woodgate R 2001 DNA polymerase iota and related Rad30-like enzymes;Philos. Trans. R. Soc. London B 356 53–60

    Article  Google Scholar 

  • Morris D R and Geballe A P 2000 Upstream open reading frames as regulators of mRNA translation;Mol. Cell. Biol. 20 8635–8642

    Article  CAS  Google Scholar 

  • Murakumo Y 2002 The property of DNA polymerase ζ: REV7 is a putative protein involved in translesion DNA synthesis and cell cycle control;Mutat. Res. 510 37–44

    Article  CAS  Google Scholar 

  • Noubissi F K, McCluskey K and Kasbekar D P 2000 Repeat-induced point mutation (RIP) in crosses with wild-isolated strains ofNeurospora crassa: evidence for dominant reduction of RIP;Fungal Genet. Biol. 31 91–97

    Article  CAS  Google Scholar 

  • Ogi T and Lehmann A R 2006 The Y-family DNA polymerase kappa (pol κ) functions in mammalian nucleotide-excision repair;Nat. Cell Biol. 8 640–642

    Article  CAS  Google Scholar 

  • Prakash A, Sengupta S, Aparna K and Kasbekar D P 1999 Theerg-3 (sterol δ14, 15 reductase) gene ofNeurospora crassa: generation of null mutants by repeat-induced point mutation and complementation by proteins chimeric for human lamin B receptor sequences;Microbiology 145 1443–1451

    Article  CAS  Google Scholar 

  • Quah S-K, Von Borstel R C and Hastings P J 1980 The origin of spontaneous mutation inSaccharomyces cerevisiae;Genetics 96 819–839

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sabbioneda S, Minesinger B K, Giannattasio M, Plevani P, Muzi- Falconi M and Jinks-Robertson S 2005 The 9-1-1 checkpoint clamp physically interacts with Polζ and is partially required for spontaneous Pol ζ-dependent mutagenesis inSaccharomyces cerevisiae;J. Biol. Chem. 280 38657–38665

    Article  CAS  Google Scholar 

  • Sakai W, Ishii C and Inoue H 2002 Theupr-1 gene encodes a catalytic subunit of the DNA polymerase ζ which is involved in damage-induced mutagenesis inNeurospora crassa;Mol. Genet. Genomics 267 401–408

    Article  CAS  Google Scholar 

  • Sakai W, Wada Y, Naoi Y, Ishii C and Inoue H. 2003 Isolation and genetic characterization of theNeurospora crassa REV1 andREV7 homologs: evidence for involvement in damage-induced mutagenesis;DNA Repair 2 337–346

    Article  CAS  Google Scholar 

  • Selker E U 1990 Premeiotic instability of repeated sequences inNeurospora crassa;Annu. Rev. Genet. 24 579–613

    Article  CAS  Google Scholar 

  • Singer M J, Kuzminova E A, Tharp A, Margolin B S and Selker E U 1995 Different frequencies of RIP among early vs. late ascosporesof Neurospora crassa;Fungal Genet. Newslett. 42 74–75

    Google Scholar 

  • Washington M T, Johnson R E, Prakash L and Prakash S 2002 Human DINB1-encoded polymerase κ is a promiscuous extender of mispaired primer termini;Proc. Natl. Acad. Sci. USA 99 1910–1914

    Article  CAS  Google Scholar 

  • Zan H, Komori A, Li Z, Cerutti A, Schaffer A, Flajnik M F, Diaz M and Casali P 2001 The translesion DNA polymerase ζ plays a major role in Ig andbcl-6 somatic hypermutation;Immunity 14 643–653

    Article  CAS  Google Scholar 

  • Zhang H, Chatterjee A and Singh K K 2006Saccharomyces cerevisiae polymerase ζ functions in mitochondria;Genetics 172 2683–2688

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Centre for Cellular and Molecular Biology, 500 007, Hyderabad, India

    Ranjan Tamuli, C. Ravindran & Durgadas P. Kasbekar

Authors
  1. Ranjan Tamuli
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  2. C. Ravindran
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  3. Durgadas P. Kasbekar
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Corresponding author

Correspondence to Durgadas P. Kasbekar.

Additional information

Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession Nos DQ 231523, DQ 231524, DQ 235021, DQ 235525-DQ 235541, DQ 240287, DQ 240288, DQ 354228, DQ 354235-DQ 354237, DQ 386416-DQ 386422, DQ 387872, DQ494492-DQ494503 and DQ417211-DQ417220.

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Tamuli, R., Ravindran, C. & Kasbekar, D.P. Translesion DNA polymerases Pol ζ, Pol η, Pol ι, Pol κ and Rev1 are not essential for repeat-induced point mutation inNeurospora crassa . J. Biosci. 31, 557–564 (2006). https://doi.org/10.1007/BF02708407

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