Skip to main content
Genetics logoLink to Genetics
. 1999 Aug;152(4):1249–1267. doi: 10.1093/genetics/152.4.1249

Archaeal DNA replication: identifying the pieces to solve a puzzle.

I K Cann 1, Y Ishino 1
PMCID: PMC1460685  PMID: 10430556

Abstract

Archaeal organisms are currently recognized as very exciting and useful experimental materials. A major challenge to molecular biologists studying the biology of Archaea is their DNA replication mechanism. Undoubtedly, a full understanding of DNA replication in Archaea requires the identification of all the proteins involved. In each of four completely sequenced genomes, only one DNA polymerase (Pol BI proposed in this review from family B enzyme) was reported. This observation suggested that either a single DNA polymerase performs the task of replicating the genome and repairing the mutations or these genomes contain other DNA polymerases that cannot be identified by amino acid sequence. Recently, a heterodimeric DNA polymerase (Pol II, or Pol D as proposed in this review) was discovered in the hyperthermophilic archaeon, Pyrococcus furiosus. The genes coding for DP1 and DP2, the subunits of this DNA polymerase, are highly conserved in the Euryarchaeota. Euryarchaeotic DP1, the small subunit of Pol II (Pol D), has sequence similarity with the small subunit of eukaryotic DNA polymerase delta. DP2 protein, the large subunit of Pol II (Pol D), seems to be a catalytic subunit. Despite possessing an excellent primer extension ability in vitro, Pol II (Pol D) may yet require accessory proteins to perform all of its functions in euryarchaeotic cells. This review summarizes our present knowledge about archaeal DNA polymerases and their relationship with those accessory proteins, which were predicted from the genome sequences.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Araki H., Hamatake R. K., Johnston L. H., Sugino A. DPB2, the gene encoding DNA polymerase II subunit B, is required for chromosome replication in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4601–4605. doi: 10.1073/pnas.88.11.4601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aravind L., Koonin E. V. Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res. 1998 Aug 15;26(16):3746–3752. doi: 10.1093/nar/26.16.3746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bauer G. A., Burgers P. M. The yeast analog of mammalian cyclin/proliferating-cell nuclear antigen interacts with mammalian DNA polymerase delta. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7506–7510. doi: 10.1073/pnas.85.20.7506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bernad A., Blanco L., Lázaro J. M., Martín G., Salas M. A conserved 3'----5' exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell. 1989 Oct 6;59(1):219–228. doi: 10.1016/0092-8674(89)90883-0. [DOI] [PubMed] [Google Scholar]
  6. Bernander R. Archaea and the cell cycle. Mol Microbiol. 1998 Aug;29(4):955–961. doi: 10.1046/j.1365-2958.1998.00956.x. [DOI] [PubMed] [Google Scholar]
  7. Blattner F. R., Plunkett G., 3rd, Bloch C. A., Perna N. T., Burland V., Riley M., Collado-Vides J., Glasner J. D., Rode C. K., Mayhew G. F. The complete genome sequence of Escherichia coli K-12. Science. 1997 Sep 5;277(5331):1453–1462. doi: 10.1126/science.277.5331.1453. [DOI] [PubMed] [Google Scholar]
  8. Bonner C. A., Stukenberg P. T., Rajagopalan M., Eritja R., O'Donnell M., McEntee K., Echols H., Goodman M. F. Processive DNA synthesis by DNA polymerase II mediated by DNA polymerase III accessory proteins. J Biol Chem. 1992 Jun 5;267(16):11431–11438. [PubMed] [Google Scholar]
  9. Brown J. R., Doolittle W. F. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2441–2445. doi: 10.1073/pnas.92.7.2441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bult C. J., White O., Olsen G. J., Zhou L., Fleischmann R. D., Sutton G. G., Blake J. A., FitzGerald L. M., Clayton R. A., Gocayne J. D. Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science. 1996 Aug 23;273(5278):1058–1073. doi: 10.1126/science.273.5278.1058. [DOI] [PubMed] [Google Scholar]
  11. Cann I. K., Kanai S., Toh H., Ishino Y. Adenylosuccinate synthetase genes: molecular cloning and phylogenetic analysis of a highly conserved archaeal gene. Syst Appl Microbiol. 1998 Dec;21(4):478–486. doi: 10.1016/S0723-2020(98)80059-3. [DOI] [PubMed] [Google Scholar]
  12. Cann I. K., Komori K., Toh H., Kanai S., Ishino Y. A heterodimeric DNA polymerase: evidence that members of Euryarchaeota possess a distinct DNA polymerase. Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14250–14255. doi: 10.1073/pnas.95.24.14250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chédin F., Seitz E. M., Kowalczykowski S. C. Novel homologs of replication protein A in archaea: implications for the evolution of ssDNA-binding proteins. Trends Biochem Sci. 1998 Aug;23(8):273–277. doi: 10.1016/s0968-0004(98)01243-2. [DOI] [PubMed] [Google Scholar]
  14. Cooper A. A., Stevens T. H. Protein splicing: excision of intervening sequences at the protein level. Bioessays. 1993 Oct;15(10):667–674. doi: 10.1002/bies.950151006. [DOI] [PubMed] [Google Scholar]
  15. Cullmann G., Fien K., Kobayashi R., Stillman B. Characterization of the five replication factor C genes of Saccharomyces cerevisiae. Mol Cell Biol. 1995 Sep;15(9):4661–4671. doi: 10.1128/mcb.15.9.4661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Delarue M., Poch O., Tordo N., Moras D., Argos P. An attempt to unify the structure of polymerases. Protein Eng. 1990 May;3(6):461–467. doi: 10.1093/protein/3.6.461. [DOI] [PubMed] [Google Scholar]
  17. Edgell D. R., Doolittle W. F. Archaea and the origin(s) of DNA replication proteins. Cell. 1997 Jun 27;89(7):995–998. doi: 10.1016/s0092-8674(00)80285-8. [DOI] [PubMed] [Google Scholar]
  18. Edgell D. R., Klenk H. P., Doolittle W. F. Gene duplications in evolution of archaeal family B DNA polymerases. J Bacteriol. 1997 Apr;179(8):2632–2640. doi: 10.1128/jb.179.8.2632-2640.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fitz-Gibbon S., Choi A. J., Miller J. H., Stetter K. O., Simon M. I., Swanson R., Kim U. J. A fosmid-based genomic map and identification of 474 genes of the hyperthermophilic archaeon Pyrobaculum aerophilum. Extremophiles. 1997 Feb;1(1):36–51. doi: 10.1007/s007920050013. [DOI] [PubMed] [Google Scholar]
  20. Foiani M., Marini F., Gamba D., Lucchini G., Plevani P. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol Cell Biol. 1994 Feb;14(2):923–933. doi: 10.1128/mcb.14.2.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Forterre P., Elie C., Kohiyama M. Aphidicolin inhibits growth and DNA synthesis in halophilic arachaebacteria. J Bacteriol. 1984 Aug;159(2):800–802. doi: 10.1128/jb.159.2.800-802.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Gary R., Ludwig D. L., Cornelius H. L., MacInnes M. A., Park M. S. The DNA repair endonuclease XPG binds to proliferating cell nuclear antigen (PCNA) and shares sequence elements with the PCNA-binding regions of FEN-1 and cyclin-dependent kinase inhibitor p21. J Biol Chem. 1997 Sep 26;272(39):24522–24529. doi: 10.1074/jbc.272.39.24522. [DOI] [PubMed] [Google Scholar]
  23. Gogarten J. P., Kibak H., Dittrich P., Taiz L., Bowman E. J., Bowman B. J., Manolson M. F., Poole R. J., Date T., Oshima T. Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6661–6665. doi: 10.1073/pnas.86.17.6661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Goldberg J., Huang H. B., Kwon Y. G., Greengard P., Nairn A. C., Kuriyan J. Three-dimensional structure of the catalytic subunit of protein serine/threonine phosphatase-1. Nature. 1995 Aug 31;376(6543):745–753. doi: 10.1038/376745a0. [DOI] [PubMed] [Google Scholar]
  25. Gulbis J. M., Kelman Z., Hurwitz J., O'Donnell M., Kuriyan J. Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell. 1996 Oct 18;87(2):297–306. doi: 10.1016/s0092-8674(00)81347-1. [DOI] [PubMed] [Google Scholar]
  26. Hansen J. L., Long A. M., Schultz S. C. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure. 1997 Aug 15;5(8):1109–1122. doi: 10.1016/s0969-2126(97)00261-x. [DOI] [PubMed] [Google Scholar]
  27. Hopfner K. P., Eichinger A., Engh R. A., Laue F., Ankenbauer W., Huber R., Angerer B. Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius. Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3600–3605. doi: 10.1073/pnas.96.7.3600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Hosfield D. J., Frank G., Weng Y., Tainer J. A., Shen B. Newly discovered archaebacterial flap endonucleases show a structure-specific mechanism for DNA substrate binding and catalysis resembling human flap endonuclease-1. J Biol Chem. 1998 Oct 16;273(42):27154–27161. doi: 10.1074/jbc.273.42.27154. [DOI] [PubMed] [Google Scholar]
  29. Hosfield D. J., Mol C. D., Shen B., Tainer J. A. Structure of the DNA repair and replication endonuclease and exonuclease FEN-1: coupling DNA and PCNA binding to FEN-1 activity. Cell. 1998 Oct 2;95(1):135–146. doi: 10.1016/s0092-8674(00)81789-4. [DOI] [PubMed] [Google Scholar]
  30. Huberman J. A. New views of the biochemistry of eucaryotic DNA replication revealed by aphidicolin, an unusual inhibitor of DNA polymerase alpha. Cell. 1981 Mar;23(3):647–648. doi: 10.1016/0092-8674(81)90426-8. [DOI] [PubMed] [Google Scholar]
  31. Imamura M., Uemori T., Kato I., Ishino Y. A non-alpha-like DNA polymerase from the hyperthermophilic archaeon Pyrococcus furiosus. Biol Pharm Bull. 1995 Dec;18(12):1647–1652. doi: 10.1248/bpb.18.1647. [DOI] [PubMed] [Google Scholar]
  32. Ishino Y., Komori K., Cann I. K., Koga Y. A novel DNA polymerase family found in Archaea. J Bacteriol. 1998 Apr;180(8):2232–2236. doi: 10.1128/jb.180.8.2232-2236.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ito J., Braithwaite D. K. Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res. 1991 Aug 11;19(15):4045–4057. doi: 10.1093/nar/19.15.4045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Iwabe N., Kuma K., Hasegawa M., Osawa S., Miyata T. Evolutionary relationship of archaebacteria, eubacteria, and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9355–9359. doi: 10.1073/pnas.86.23.9355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Johnson R. E., Prakash S., Prakash L. Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta. Science. 1999 Feb 12;283(5404):1001–1004. doi: 10.1126/science.283.5404.1001. [DOI] [PubMed] [Google Scholar]
  36. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., Miyajima N., Hirosawa M., Sugiura M., Sasamoto S. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 1996 Jun 30;3(3):109–136. doi: 10.1093/dnares/3.3.109. [DOI] [PubMed] [Google Scholar]
  37. Kawarabayasi Y., Sawada M., Horikawa H., Haikawa Y., Hino Y., Yamamoto S., Sekine M., Baba S., Kosugi H., Hosoyama A. Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3. DNA Res. 1998 Apr 30;5(2):55–76. doi: 10.1093/dnares/5.2.55. [DOI] [PubMed] [Google Scholar]
  38. Kearsey S. E., Labib K. MCM proteins: evolution, properties, and role in DNA replication. Biochim Biophys Acta. 1998 Jun 16;1398(2):113–136. doi: 10.1016/s0167-4781(98)00033-5. [DOI] [PubMed] [Google Scholar]
  39. Kelman Z. PCNA: structure, functions and interactions. Oncogene. 1997 Feb 13;14(6):629–640. doi: 10.1038/sj.onc.1200886. [DOI] [PubMed] [Google Scholar]
  40. Klenk H. P., Clayton R. A., Tomb J. F., White O., Nelson K. E., Ketchum K. A., Dodson R. J., Gwinn M., Hickey E. K., Peterson J. D. The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature. 1997 Nov 27;390(6658):364–370. doi: 10.1038/37052. [DOI] [PubMed] [Google Scholar]
  41. Klimczak L. J., Grummt F., Burger K. J. Purification and characterization of DNA polymerase from the archaebacterium Sulfolobus acidocaldarius. Nucleic Acids Res. 1985 Jul 25;13(14):5269–5282. doi: 10.1093/nar/13.14.5269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Knopf C. W. Evolution of viral DNA-dependent DNA polymerases. Virus Genes. 1998;16(1):47–58. doi: 10.1023/a:1007997609122. [DOI] [PubMed] [Google Scholar]
  43. Kohlstaedt L. A., Wang J., Friedman J. M., Rice P. A., Steitz T. A. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science. 1992 Jun 26;256(5065):1783–1790. doi: 10.1126/science.1377403. [DOI] [PubMed] [Google Scholar]
  44. Konisky J., Paule S. M., Carinato M. E., Kansy J. W. The DNA polymerase gene from the methanogenic archaeon Methanococcus voltae. J Bacteriol. 1994 Oct;176(20):6402–6403. doi: 10.1128/jb.176.20.6402-6403.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Krishna T. S., Kong X. P., Gary S., Burgers P. M., Kuriyan J. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell. 1994 Dec 30;79(7):1233–1243. doi: 10.1016/0092-8674(94)90014-0. [DOI] [PubMed] [Google Scholar]
  46. Lee S. H., Pan Z. Q., Kwong A. D., Burgers P. M., Hurwitz J. Synthesis of DNA by DNA polymerase epsilon in vitro. J Biol Chem. 1991 Nov 25;266(33):22707–22717. [PubMed] [Google Scholar]
  47. Li Y., Korolev S., Waksman G. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J. 1998 Dec 15;17(24):7514–7525. doi: 10.1093/emboj/17.24.7514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Lopez P., Philippe H., Myllykallio H., Forterre P. Identification of putative chromosomal origins of replication in Archaea. Mol Microbiol. 1999 May;32(4):883–886. doi: 10.1046/j.1365-2958.1999.01370.x. [DOI] [PubMed] [Google Scholar]
  49. Mattila P., Korpela J., Tenkanen T., Pitkänen K. Fidelity of DNA synthesis by the Thermococcus litoralis DNA polymerase--an extremely heat stable enzyme with proofreading activity. Nucleic Acids Res. 1991 Sep 25;19(18):4967–4973. doi: 10.1093/nar/19.18.4967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Meindl A., Berger W., Meitinger T., van de Pol D., Achatz H., Dörner C., Haasemann M., Hellebrand H., Gal A., Cremers F. Norrie disease is caused by mutations in an extracellular protein resembling C-terminal globular domain of mucins. Nat Genet. 1992 Oct;2(2):139–143. doi: 10.1038/ng1092-139. [DOI] [PubMed] [Google Scholar]
  51. Morell V. Life's last domain. Science. 1996 Aug 23;273(5278):1043–1045. doi: 10.1126/science.273.5278.1043. [DOI] [PubMed] [Google Scholar]
  52. Mäkiniemi M., Pospiech H., Kilpeläinen S., Jokela M., Vihinen M., Syväoja J. E. A novel family of DNA-polymerase-associated B subunits. Trends Biochem Sci. 1999 Jan;24(1):14–16. doi: 10.1016/s0968-0004(98)01327-9. [DOI] [PubMed] [Google Scholar]
  53. Nakayama M., Kohiyama M. An alpha-like DNA polymerase from Halobacterium halobium. Eur J Biochem. 1985 Oct 15;152(2):293–297. doi: 10.1111/j.1432-1033.1985.tb09197.x. [DOI] [PubMed] [Google Scholar]
  54. Nastopoulos V., Pisani F. M., Savino C., Federici L., Rossi M., Tsernoglou D. Crystallization and preliminary X-ray diffraction studies of DNA polymerase from the thermophilic archaeon Sulfolobus solfataricus. Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):1002–1004. doi: 10.1107/s0907444998002443. [DOI] [PubMed] [Google Scholar]
  55. Nelson J. R., Lawrence C. W., Hinkle D. C. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science. 1996 Jun 14;272(5268):1646–1649. doi: 10.1126/science.272.5268.1646. [DOI] [PubMed] [Google Scholar]
  56. Nethanel T., Reisfeld S., Dinter-Gottlieb G., Kaufmann G. An Okazaki piece of simian virus 40 may be synthesized by ligation of shorter precursor chains. J Virol. 1988 Aug;62(8):2867–2873. doi: 10.1128/jvi.62.8.2867-2873.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ollis D. L., Brick P., Hamlin R., Xuong N. G., Steitz T. A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. 1985 Feb 28-Mar 6Nature. 313(6005):762–766. doi: 10.1038/313762a0. [DOI] [PubMed] [Google Scholar]
  58. Onrust R., Finkelstein J., Naktinis V., Turner J., Fang L., O'Donnell M. Assembly of a chromosomal replication machine: two DNA polymerases, a clamp loader, and sliding clamps in one holoenzyme particle. I. Organization of the clamp loader. J Biol Chem. 1995 Jun 2;270(22):13348–13357. doi: 10.1074/jbc.270.22.13348. [DOI] [PubMed] [Google Scholar]
  59. Onrust R., Stukenberg P. T., O'Donnell M. Analysis of the ATPase subassembly which initiates processive DNA synthesis by DNA polymerase III holoenzyme. J Biol Chem. 1991 Nov 15;266(32):21681–21686. [PubMed] [Google Scholar]
  60. Pause A., Sonenberg N. Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor eIF-4A. EMBO J. 1992 Jul;11(7):2643–2654. doi: 10.1002/j.1460-2075.1992.tb05330.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Perler F. B., Comb D. G., Jack W. E., Moran L. S., Qiang B., Kucera R. B., Benner J., Slatko B. E., Nwankwo D. O., Hempstead S. K. Intervening sequences in an Archaea DNA polymerase gene. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5577–5581. doi: 10.1073/pnas.89.12.5577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Perler F. B., Davis E. O., Dean G. E., Gimble F. S., Jack W. E., Neff N., Noren C. J., Thorner J., Belfort M. Protein splicing elements: inteins and exteins--a definition of terms and recommended nomenclature. Nucleic Acids Res. 1994 Apr 11;22(7):1125–1127. doi: 10.1093/nar/22.7.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Perler F. B., Kumar S., Kong H. Thermostable DNA polymerases. Adv Protein Chem. 1996;48:377–435. doi: 10.1016/s0065-3233(08)60367-8. [DOI] [PubMed] [Google Scholar]
  64. Pisani F. M., De Martino C., Rossi M. A DNA polymerase from the archaeon Sulfolobus solfataricus shows sequence similarity to family B DNA polymerases. Nucleic Acids Res. 1992 Jun 11;20(11):2711–2716. doi: 10.1093/nar/20.11.2711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Rao H. G., Rosenfeld A., Wetmur J. G. Methanococcus jannaschii flap endonuclease: expression, purification, and substrate requirements. J Bacteriol. 1998 Oct;180(20):5406–5412. doi: 10.1128/jb.180.20.5406-5412.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Russell R. J., Ferguson J. M., Hough D. W., Danson M. J., Taylor G. L. The crystal structure of citrate synthase from the hyperthermophilic archaeon pyrococcus furiosus at 1.9 A resolution,. Biochemistry. 1997 Aug 19;36(33):9983–9994. doi: 10.1021/bi9705321. [DOI] [PubMed] [Google Scholar]
  67. Sako Y., Nomura N., Uchida A., Ishida Y., Morii H., Koga Y., Hoaki T., Maruyama T. Aeropyrum pernix gen. nov., sp. nov., a novel aerobic hyperthermophilic archaeon growing at temperatures up to 100 degrees C. Int J Syst Bacteriol. 1996 Oct;46(4):1070–1077. doi: 10.1099/00207713-46-4-1070. [DOI] [PubMed] [Google Scholar]
  68. Schleper C., Swanson R. V., Mathur E. J., DeLong E. F. Characterization of a DNA polymerase from the uncultivated psychrophilic archaeon Cenarchaeum symbiosum. J Bacteriol. 1997 Dec;179(24):7803–7811. doi: 10.1128/jb.179.24.7803-7811.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Smith D. R., Doucette-Stamm L. A., Deloughery C., Lee H., Dubois J., Aldredge T., Bashirzadeh R., Blakely D., Cook R., Gilbert K. Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol. 1997 Nov;179(22):7135–7155. doi: 10.1128/jb.179.22.7135-7155.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Stillman B. Smart machines at the DNA replication fork. Cell. 1994 Sep 9;78(5):725–728. doi: 10.1016/s0092-8674(94)90362-x. [DOI] [PubMed] [Google Scholar]
  71. Sun Y., Jiang Y., Zhang P., Zhang S. J., Zhou Y., Li B. Q., Toomey N. L., Lee M. Y. Expression and characterization of the small subunit of human DNA polymerase delta. J Biol Chem. 1997 May 16;272(20):13013–13018. doi: 10.1074/jbc.272.20.13013. [DOI] [PubMed] [Google Scholar]
  72. Takagi M., Nishioka M., Kakihara H., Kitabayashi M., Inoue H., Kawakami B., Oka M., Imanaka T. Characterization of DNA polymerase from Pyrococcus sp. strain KOD1 and its application to PCR. Appl Environ Microbiol. 1997 Nov;63(11):4504–4510. doi: 10.1128/aem.63.11.4504-4510.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tomb J. F., White O., Kerlavage A. R., Clayton R. A., Sutton G. G., Fleischmann R. D., Ketchum K. A., Klenk H. P., Gill S., Dougherty B. A. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 1997 Aug 7;388(6642):539–547. doi: 10.1038/41483. [DOI] [PubMed] [Google Scholar]
  74. Tsurimoto T., Melendy T., Stillman B. Sequential initiation of lagging and leading strand synthesis by two different polymerase complexes at the SV40 DNA replication origin. Nature. 1990 Aug 9;346(6284):534–539. doi: 10.1038/346534a0. [DOI] [PubMed] [Google Scholar]
  75. Turner J., Hingorani M. M., Kelman Z., O'Donnell M. The internal workings of a DNA polymerase clamp-loading machine. EMBO J. 1999 Feb 1;18(3):771–783. doi: 10.1093/emboj/18.3.771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Uemori T., Ishino Y., Doi H., Kato I. The hyperthermophilic archaeon Pyrodictium occultum has two alpha-like DNA polymerases. J Bacteriol. 1995 Apr;177(8):2164–2177. doi: 10.1128/jb.177.8.2164-2177.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Uemori T., Ishino Y., Toh H., Asada K., Kato I. Organization and nucleotide sequence of the DNA polymerase gene from the archaeon Pyrococcus furiosus. Nucleic Acids Res. 1993 Jan 25;21(2):259–265. doi: 10.1093/nar/21.2.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Uemori T., Sato Y., Kato I., Doi H., Ishino Y. A novel DNA polymerase in the hyperthermophilic archaeon, Pyrococcus furiosus: gene cloning, expression, and characterization. Genes Cells. 1997 Aug;2(8):499–512. doi: 10.1046/j.1365-2443.1997.1380336.x. [DOI] [PubMed] [Google Scholar]
  79. Uhlmann F., Cai J., Gibbs E., O'Donnell M., Hurwitz J. Deletion analysis of the large subunit p140 in human replication factor C reveals regions required for complex formation and replication activities. J Biol Chem. 1997 Apr 11;272(15):10058–10064. doi: 10.1074/jbc.272.15.10058. [DOI] [PubMed] [Google Scholar]
  80. Umar A., Buermeyer A. B., Simon J. A., Thomas D. C., Clark A. B., Liskay R. M., Kunkel T. A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 1996 Oct 4;87(1):65–73. doi: 10.1016/s0092-8674(00)81323-9. [DOI] [PubMed] [Google Scholar]
  81. Waga S., Stillman B. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature. 1994 May 19;369(6477):207–212. doi: 10.1038/369207a0. [DOI] [PubMed] [Google Scholar]
  82. Waga S., Stillman B. The DNA replication fork in eukaryotic cells. Annu Rev Biochem. 1998;67:721–751. doi: 10.1146/annurev.biochem.67.1.721. [DOI] [PubMed] [Google Scholar]
  83. Wang J., Sattar A. K., Wang C. C., Karam J. D., Konigsberg W. H., Steitz T. A. Crystal structure of a pol alpha family replication DNA polymerase from bacteriophage RB69. Cell. 1997 Jun 27;89(7):1087–1099. doi: 10.1016/s0092-8674(00)80296-2. [DOI] [PubMed] [Google Scholar]
  84. Wernette C. M., Kaguni L. S. A mitochondrial DNA polymerase from embryos of Drosophila melanogaster. Purification, subunit structure, and partial characterization. J Biol Chem. 1986 Nov 5;261(31):14764–14770. [PubMed] [Google Scholar]
  85. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Wong S. W., Wahl A. F., Yuan P. M., Arai N., Pearson B. E., Arai K., Korn D., Hunkapiller M. W., Wang T. S. Human DNA polymerase alpha gene expression is cell proliferation dependent and its primary structure is similar to both prokaryotic and eukaryotic replicative DNA polymerases. EMBO J. 1988 Jan;7(1):37–47. doi: 10.1002/j.1460-2075.1988.tb02781.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Xu M. Q., Southworth M. W., Mersha F. B., Hornstra L. J., Perler F. B. In vitro protein splicing of purified precursor and the identification of a branched intermediate. Cell. 1993 Dec 31;75(7):1371–1377. doi: 10.1016/0092-8674(93)90623-x. [DOI] [PubMed] [Google Scholar]
  88. Yuzhakov A., Kelman Z., O'Donnell M. Trading places on DNA--a three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell. 1999 Jan 8;96(1):153–163. doi: 10.1016/s0092-8674(00)80968-x. [DOI] [PubMed] [Google Scholar]
  89. Zhang P., Zhang S. J., Zhang Z., Woessner J. F., Jr, Lee M. Y. Expression and physicochemical characterization of human proliferating cell nuclear antigen. Biochemistry. 1995 Aug 29;34(34):10703–10712. doi: 10.1021/bi00034a002. [DOI] [PubMed] [Google Scholar]
  90. Zhou J. Q., He H., Tan C. K., Downey K. M., So A. G. The small subunit is required for functional interaction of DNA polymerase delta with the proliferating cell nuclear antigen. Nucleic Acids Res. 1997 Mar 15;25(6):1094–1099. doi: 10.1093/nar/25.6.1094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Zhou M., Mao C., Rodriguez A. C., Kiefer J. R., Kucera R. B., Beese L. S. Crystallization and preliminary diffraction analysis of a hyperthermostable DNA polymerase from a Thermococcus archaeon. Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):994–995. doi: 10.1107/s0907444998001553. [DOI] [PubMed] [Google Scholar]
  92. Zlotkin T., Kaufmann G., Jiang Y., Lee M. Y., Uitto L., Syväoja J., Dornreiter I., Fanning E., Nethanel T. DNA polymerase epsilon may be dispensable for SV40- but not cellular-DNA replication. EMBO J. 1996 May 1;15(9):2298–2305. [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES