CoChat
Sign Up
Cited by 22DNA Repair MechanismsGenomics and Phylogenetic StudiesEnzyme Structure and Function

The DOI matches its Crossref record; the references it cites are not checked yet.

Characterization of Family D DNA polymerase from Thermococcus sp. 9°N

Open access
Greenough, Lucia, Menin, Julie F., Desai, Nirav S., Kelman, Zvi, Gardner, Andrew F.·2014·Extremophiles
DOI 10.1007/s00792-014-0646-9PMC PMC4065339
Open this paper in CoChat — free accountOpen PDF

Abstract

Accurate DNA replication is essential for maintenance of every genome. All archaeal genomes except Crenarchaea, encode for a member of Family B (polB) and Family D (polD) DNA polymerases. Gene deletion studies in Thermococcus kodakaraensis and Methanococcus maripaludis show that polD is the only essential DNA polymerase in these organisms. Thus, polD may be the primary replicative DNA polymerase for both leading and lagging strand synthesis. To understand this unique archaeal enzyme, we report the biochemical characterization of a heterodimeric polD from Thermococcus. PolD contains both DNA polymerase and proofreading 3'-5' exonuclease activities to ensure efficient and accurate genome duplication. The polD incorporation fidelity was determined for the first time. Despite containing 3'-5' exonuclease proofreading activity, polD has a relatively high error rate (95 × 10(-5)) compared to polB (19 × 10(-5)) and at least 10-fold higher than the polB DNA polymerases from yeast (polε and polδ) or Escherichia coli DNA polIII holoenzyme. The implications of polD fidelity and biochemical properties in leading and lagging strand synthesis are discussed.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1007/s00792-014-0646-9

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

The citation lists haven’t been fetched yet

References 54 · Cited by 22

Research works printed but not linked: 53

  1. Beese LS, Steitz TA (1991) Structural basis for the 3′–5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J 10(1):25–33 · DOI
  2. Berquist BR, DasSarma P, DasSarma S (2007) Essential and non-essential DNA replication genes in the model halophilic Archaeon, Halobacterium sp. NRC-1. BMC Genet 8:31 · DOI
  3. Braithwaite DK, Ito J (1993) Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res 21(4):787–802 · DOI
  4. Cann IK, Komori K, Toh H, Kanai S, Ishino Y (1998) A heterodimeric DNA polymerase: evidence that members of Euryarchaeota possess a distinct DNA polymerase. Proc Natl Acad Sci USA 95(24):14250–14255 · DOI
  5. Cubonova L, Richardson T, Burkhart BW, Kelman Z, Connolly BA, Reeve JN, Santangelo TJ (2013) Archaeal DNA polymerase D but not DNA polymerase B is required for genome replication in Thermococcus kodakarensis. J Bacteriol 195:2322–2328 · DOI
  6. Derbyshire V, Grindley ND, Joyce CM (1991) The 3′–5′ exonuclease of DNA polymerase I of Escherichia coli: contribution of each amino acid at the active site to the reaction. EMBO J 10(1):17–24 · DOI
  7. Dong Q, Copeland WC, Wang TS (1993) Mutational studies of human DNA polymerase alpha. Identification of residues critical for deoxynucleotide binding and misinsertion fidelity of DNA synthesis. J Biol Chem 268(32):24163–24174 · DOI
  8. Fijalkowska IJ, Jonczyk P, Tkaczyk MM, Bialoskorska M, Schaaper RM (1998) Unequal fidelity of leading strand and lagging strand DNA replication on the Escherichia coli chromosome. Proc Natl Acad Sci USA 95(17):10020–10025 · DOI
  9. Gibson DG (2011) Enzymatic assembly of overlapping DNA fragments. Methods Enzymol 498:349–361 · DOI
  10. Gueguen Y, Rolland JL, Lecompte O, Azam P, Le Romancer G, Flament D, Raffin JP, Dietrich J (2001) Characterization of two DNA polymerases from the hyperthermophilic euryarchaeon Pyrococcus abyssi. FEBS 268(22):5961–5969
  11. Henneke G (2012) In vitro reconstitution of RNA primer removal in Archaea reveals the existence of two pathways. Biochem J 447(2):271–280 · DOI
  12. Henneke G, Flament D, Hübscher U, Querellou J, Raffin J-P (2005) The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J Mol Biol 350(1):53–64 · DOI
  13. Indiani C, O’Donnell M (2006) The replication clamp-loading machine at work in the three domains of life. Nat Rev Mol Cell Biol 7(10):751–761 · DOI
  14. Ishino Y, Ishino S (2012) Rapid progress of DNA replication studies in Archaea, the third domain of life. Science China Life Sci 55(5):386–403. doi: 10.1007/s11427-012-4324-9 · DOI
  15. Ishino Y, Komori K, Cann IK, Koga Y (1998) A novel DNA polymerase family found in Archaea. J Bacteriol 180(8):2232–2236 · DOI
  16. Jokela M, Eskelinen A, Pospiech H, Rouvinen J, Syväoja JE (2004) Characterization of the 3′–5′ exonuclease subunit DP1 of Methanococcus jannaschii replicative DNA polymerase D. Nucleic Acids Res 32(8):2430–2440 · DOI
  17. Jokela M, Raki M, Heikkinen K, Sepponen K, Eskelinen A, Syväoja JE (2005) The screening of expression and purification conditions for replicative DNA polymerase associated B-subunits, assignment of the exonuclease activity to the C-terminus of archaeal pol D DP1 subunit. Protein Express Purif 43(1):73–84 · DOI
  18. Joyce CM, Steitz TA (1995) Polymerase structures and function: variations on a theme? J Bacteriol 177(22):6321–6329 · DOI
  19. Kermekchiev MB, Tzekov A, Barnes WM (2003) Cold-sensitive mutants of Taq DNA polymerase provide a hot start for PCR. Nucleic Acids Res 31(21):6139–6147 · DOI
  20. Kong H, Kucera RB, Jack WE (1993) Characterization of a DNA polymerase from the hyperthermophile archaea Thermococcus litoralis. Vent DNA polymerase, steady state kinetics, thermal stability, processivity, strand displacement, and exonuclease activities. J Biol Chem 268(3):1965–1975 · DOI
  21. Krokan H, Wist E, Krokan RH (1981) Aphidicolin inhibits DNA synthesis by DNA polymerase alpha and isolated nuclei by a similar mechanism. Nucleic Acids Res 9(18):4709–4719 · DOI
  22. Kuba Y, Ishino S, Yamagami T, Tokuhara M, Kanai T, Fujikane R, Daiyasu H, Atomi H, Ishino Y (2012) Comparative analyses of the two proliferating cell nuclear antigens from the hyperthermophilic archaeon, Thermococcus kodakarensis. Genes Cells 17(11):923–937 · DOI
  23. Kunkel TA (2009) Evolving views of DNA replication (in)fidelity. Cold Spring Harbor Symp Quant Biol 74:91–101 · DOI
  24. Ladner JE, Pan M, Hurwitz J, Kelman Z (2011) Crystal structures of two active proliferating cell nuclear antigens (PCNAs) encoded by Thermococcus kodakaraensis. Proc Natl Acad Sci USA 108(7):2711–2716 · DOI · Paper page
  25. Li Z, Santangelo TJ, Cuboňová L, Reeve JN, Kelman Z (2010) Affinity purification of an archaeal DNA replication protein network. mBio 1 (5). · DOI
  26. Li Z, Pan M, Santangelo TJ, Chemnitz W, Yuan W, Edwards JL, Hurwitz J, Reeve JN, Kelman Z (2011) A novel DNA nuclease is stimulated by association with the GINS complex. Nucleic Acids Res 39(14):6114–6123 · DOI
  27. Li Z, Kelman LM, Kelman Z (2013) Thermococcus kodakarensis DNA replication. Biochem Soc Trans 41(1):332–338 · DOI
  28. Matsui I, Urushibata Y, Shen Y, Matsui E, Yokoyama H (2011) Novel structure of an N-terminal domain that is crucial for the dimeric assembly and DNA-binding of an archaeal DNA polymerase D large subunit from Pyrococcus horikoshii. FEBS Lett 585(3):452–458 · DOI
  29. Mattila P, Korpela J, Tenkanen T, Pitkänen K (1991) Fidelity of DNA synthesis by the Thermococcus litoralis DNA polymerase-an extremely heat stable enzyme with proofreading activity. Nucleic Acids Res 19(18):4967–4973 · DOI
  30. Mayanagi K, Kiyonari S, Nishida H, Saito M, Kohda D, Ishino Y, Shirai T, Morikawa K (2011) Architecture of the DNA polymerase B-proliferating cell nuclear antigen (PCNA)-DNA ternary complex. Proc Natl Acad Sci USA 108(5):1845–1849 · DOI
  31. McHenry CS (2011) Bacterial replicases and related polymerases. Curr Opin Chem Biol 15(5):587–594 · DOI
  32. Motz M, Kober I, Girardot C, Loeser E, Bauer U, Albers M, Moeckel G, Minch E, Voss H, Kilger C, Koegl M (2002) Elucidation of an archaeal replication protein network to generate enhanced PCR enzymes. J Biol Chem 277(18):16179–16188 · DOI
  33. Myllykallio H, Lopez P, López-García P, Heilig R, Saurin W, Zivanovic Y, Philippe H, Forterre P (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288(5474):2212–2215 · DOI
  34. Pan M, Kelman LM, Kelman Z (2011) The archaeal PCNA proteins. Biochem Soc Trans 39(1):20–24 · DOI
  35. Perler FB (2002) InBase: the Intein Database. Nucleic Acids Res 30(1):383–384 · DOI
  36. Perler FB, Comb DG, Jack WE, Moran LS, Qiang B, Kucera RB, Benner J, Slatko BE, Nwankwo DO, Hempstead SK (1992) Intervening sequences in an Archaea DNA polymerase gene. Proc Natl Acad Sci USA 89(12):5577–5581 · DOI
  37. Pham PT, Olson MW, McHenry CS, Schaaper RM (1998) The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro. J Biol Chem 273(36):23575–23584 · DOI
  38. Reha-Krantz LJ (2010) DNA polymerase proofreading: multiple roles maintain genome stability. Biochim Biophys Acta 1804(5):1049–1063 · DOI
  39. Rodriguez A, Park H, Mao C, Beese L (2000) Crystal structure of a pol alpha family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9 degrees N-7. J Mol Biol 299(2):447–462 · DOI
  40. Rouillon C, Henneke G, Flament D, Querellou J, Raffin J-P (2007) DNA polymerase switching on homotrimeric PCNA at the replication fork of the euryarchaeota Pyrococcus abyssi. J Mol Biol 369(2):343–355 · DOI
  41. Sarmiento F, Mrazek J, Whitman WB (2013) Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proc Natl Acad Sci USA 110(12):4726–4731 · DOI
  42. Shcherbakova PV, Pavlov YI, Chilkova O, Rogozin IB, Johansson E, Kunkel TA (2003) Unique error signature of the four-subunit yeast DNA polymerase epsilon. J Biol Chem 278(44):43770–43780 · DOI
  43. Shen Y, Musti K, Hiramoto M, Kikuchi H, Kawarabayashi Y, Matsui I (2001) Invariant Asp-1122 and Asp-1124 are essential residues for polymerization catalysis of family D DNA polymerase from Pyrococcus horikoshii. J Biol Chem 276(29):27376–27383 · DOI
  44. Shen Y, Tang X-F, Matsui I (2003) Subunit interaction and regulation of activity through terminal domains of the family D DNA polymerase from Pyrococcus horikoshii. J Biol Chem 278(23):21247–21257 · DOI
  45. Shen Y, Tang X-F, Matsui E, Matsui I (2004a) Subunit interaction and regulation of activity through terminal domains of the family D DNA polymerase from Pyrococcus horikoshii. Biochem Soc Trans 32(Pt 2):245–249 · DOI
  46. Shen Y, Tang X-F, Yokoyama H, Matsui E, Matsui I (2004b) A 21-amino acid peptide from the cysteine cluster II of the family D DNA polymerase from Pyrococcus horikoshii stimulates its nuclease activity which is Mre11-like and prefers manganese ion as the cofactor. Nucleic Acids Res 32(1):158–168 · DOI
  47. Southworth MW, Kong H, Kucera RB, Ware J, Jannasch HW, Perler FB (1996) Cloning of thermostable DNA polymerases from hyperthermophilic marine Archaea with emphasis on Thermococcus sp. 9 degrees N-7 and mutations affecting 3′–5′ exonuclease activity. Proc Natl Acad Sci USA 93(11):5281–5285 · DOI
  48. Suzuki M, Avicola AK, Hood L, Loeb LA (1997) Low fidelity mutants in the O-helix of Thermus aquaticus DNA polymerase I. J Biol Chem 272(17):11228–11235 · DOI
  49. Tang X-F, Shen Y, Matsui E, Matsui I (2004) Domain topology of the DNA polymerase D complex from a hyperthermophilic archaeon Pyrococcus horikoshii. Biochemistry 43(37):11818–11827 · DOI
  50. Yamasaki K, Urushibata Y, Yamasaki T, Arisaka F, Matsui I (2010) Solution structure of the N-terminal domain of the archaeal D-family DNA polymerase small subunit reveals evolutionary relationship to eukaryotic B-family polymerases. FEBS Lett 584(15):3370–3375 · DOI
  51. Yamtich J, Sweasy JB (2010) DNA polymerase family X: function, structure, and cellular roles. Biochim Biophys Acta 1804(5):1136–1150 · DOI
  52. Zhang L, Brown JA, Newmister SA, Suo Z (2009) Polymerization fidelity of a replicative DNA polymerase from the hyperthermophilic archaeon Sulfolobus solfataricus P2. Biochemistry 48(31):7492–7501 · DOI
  53. Zhang L, Lou H, Guo L, Zhan Z, Duan Z, Guo X, Huang L (2010) Accurate DNA synthesis by Sulfolobus solfataricus DNA polymerase B1 at high temperature. Extremophiles 14(1):107–117 · DOI

Metadata

Authors
Greenough, L., Menin, J. F., Desai, N. S., Kelman, Z., & Gardner, A. F.
Affiliations
  • New England Biolabs (United States) (US)
  • National Institute of Standards and Technology (US)
Corresponding author
Gardner, Andrew F.
ORCID
Venue
Extremophiles
Publisher
Springer Science and Business Media LLC
Published
2014-05-03
Volume
18
Issue
4
Pages
653-664
ISSN
  • 1431-0651 (ISSN-L)
  • 1433-4909
DOI
10.1007/s00792-014-0646-9
PMC
PMC4065339
OpenAlex
W1970102978
Cited by
22
References
54
Citations by year
2026: 3 · 2023: 1 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 4 · 2014: 3
FWCI
1.64
Type
journal article
Language
en
Open access
Licence
Locations
  • Extremophiles (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Enzyme Structure and Function
Keywords
Thermococcus, archaeal DNA replication, error rate, POLB, Methanococcus maripaludis, Thermococcus kodakarensis
MeSH terms
Base Sequence, DNA Replication, Kinetics, Molecular Sequence Data, Mutation, Phylogeny, 4-Hydroxyphenylpyruvate Dioxygenase, Thermococcus, Archaeal Proteins

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review