Archaea-specific D-family DNA polymerase (PolD) forms a dimeric heterodimer consisting of two large polymerase subunits and two small exonuclease subunits. According to the protein-protein interactions identified among the domains of large and small subunits of PolD, a symmetrical model for the domain topology of the PolD holoenzyme is proposed. The experimental evidence supports various aspects of the model. The conserved amphipathic nature of the N-terminal putative α-helix of the large subunit plays a key role in the homodimeric assembly and the self-cyclization of the large subunit and is deeply involved in the archaeal PolD stability and activity. We also discuss the evolutional transformation from archaeal D-family to eukaryotic B-family polymerase on the basis of the structural information.
References
[1]
Leipe, D.D.; Aravind, L.; Koonin, E.V. Did DNA replication evolve twice independently? Nucleic Acids Res.？1999, 27, 3389–3401, doi:10.1093/nar/27.17.3389.
[2]
Bailey, S.; Wing, R.A.; Steitz, T.A. The structure of T. aquaticus DNA polymerase III is distinct from eukaryotic replicative DNA polymerases. Cell？2006, 893–904, doi:10.1016/j.cell.2006.07.027.
[3]
Burgers, P.M.; Koonin, E.V.; Bruford, E.; Blanco, L.; Burtis, K.C.; Christman, M.F.; Copeland, W.C.; Friedberg, E.C.; Hanaoka, F.; Hinkle, D.C.; et al. Eukaryotic DNA polymerases: Proposal for a revised nomenclature. J. Biol. Chem.？2001, 276, 43487–43490, doi:10.1074/jbc.R100056200.
[4]
Grabowski, B.; Kelman, Z. Archaeal DNA replication: Eukaryal proteins in a bacterial context. Annu. Rev. Microbiol.？2003, 57, 487–516, doi:10.1146/annurev.micro.57.030502.090709.
[5]
Pavlov, Y.I.; Shcherbakova, P.V.; Rogozin, I.B. Roles of DNA polymerase in replication, repair, and recombination in eukaryotes. Int. Rev. Cytol.？2006, 255, 41–132, doi:10.1016/S0074-7696(06)55002-8.
[6]
Hubscher, U.; Maga, G.; Spadari, S. Eukaryotic DNA polymerases. Annu. Rev. Biochem.？2002, 71, 133–163, doi:10.1146/annurev.biochem.71.090501.150041.
[7]
Ishino, Y.; Komori, K.; Cann, I.K.; Koga, Y. A novel DNA polymerase family found in Archaea. J. Bacteriol.？1998, 180, 2232–2236. 9555910
[8]
Shen, Y.; Musti, K.; Hiramoto, M.; Kikuchi, H.; Kawarabayasi, Y.; Matsui, I. Invariant Asp-1122 and Asp-1124 are essential residues for polymerization catalysis of family D DNA polymerase from Pyrococcus horikoshii. J. Biol. Chem.？2001, 276, 27376–27383, doi:10.1074/jbc.M011762200. 11319225
[9]
Henneke, G.; Flament, D.; Hübscher, U.; Querellou, J.; Raffin, J.P. The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J. Mol. Biol.？2005, 350, 53–64, doi:10.1016/j.jmb.2005.04.042.
[10]
Kurr, M.; Huber, R.; Konig, H.; Jannasch, H.W.; Fricke, H.; Trincone, A.; Kristjansson, J.K.; Stetter, K.O. Methanopyrus kandleri, gen. and sp. nov. represents a novel group of hyperthermophilic methanogen, growing at 110 °C. Arch. Microbiol.？1991, 156, 239–247, doi:10.1007/BF00262992.
[11]
Waters, E.; Hohn, M.J.; Ahel, I.; Graham, D.E.; Adams, M.D.; Barnstead, M.; Beeson, K.Y.; Bibbs, L.; Bolanos, R.; Keller, M.; et al. The genome of Nanoarchaeum equitans: Insights into early archaeal evolution and derived parasitism. Proc. Natl. Acad. Sci. USA？2003, 100, 12984–12988, doi:10.1073/pnas.1735403100.
[12]
Brochier-Armanet, C.; Boussau, B.; Gribaldo, S.; Forterre, P. Mesophillic Crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol.？2008, 6, 245–252, doi:10.1038/nrmicro1852.
[13]
Elkins, J.G.; Podar, M.; Graham, D.E.; Makarova, K.S.; Wolf, Y.; Randau, L.; Hedlund, B.P.; Brochier-Armanet, C.; Kunin, V.; Anderson, I.; et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl. Acad. Sci. USA？2008, 105, 8102–8107, doi:10.1073/pnas.0801980105.
[14]
Tahirov, T.H.; Makarova, K.S.; Rogozin, I.B.; Pavlov, Y.I.; Koonin, E.V. Evolution of DNA polymerases: An inactivated polymerase-exonuclease module in Pol ε and a chimeric origin of eukaryotic polymerases from two classes of Archaeal ancestors. Biol. Direct？2009, 4, 11–15, doi:10.1186/1745-6150-4-11.
[15]
Berquist, B.R.; DasSarma, P.; DasSarma, S. Essential and non-essential DNA replication genes in the model halophilic archaeon, Halobacterium sp. NRC-1. BMC Genet.？2007, 8, e31, doi:10.1186/1471-2156-8-31.
[16]
Rouillon, C.; Henneke, G.; Flament, D.; Querellou, J.; Raffin, J.P. DNA polymerase switching on homotrimeric PCNA at the replication fork of the Euryarchaea Pyrococcus abyssi. J. Mol. Biol.？2007, 350, 53–64.
[17]
Shen, Y.; Tang, X.-F.; Yokoyama, H.; Matsui, E.; Matsui, I. A 21-amino acid peptide from the cysteine cluster II of the family D DNA polymerase from Pyrococcus horikoshii stimulate its nuclease activity which is Mre-11-like and prefers manganese ion as the cofactor. Nucleic Acids Res.？2004, 32, 158–168, doi:10.1093/nar/gkh153.
[18]
Aravind, L.; Koonin, E.V. Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res.？1998, 26, 3746–3752, doi:10.1093/nar/26.16.3746.
[19]
Gueguen, Y.; Rolland, J.; Lecompte, O.; Azam, P.; Romancer, G.L.; Flament, D.; Raffin, J.P.; Dietrich, J. Characterization of two DNA polymerases from the hyperthermophilic euryarchaeon Pyrococcus abyssi. Eur. J. Biochem.？2001, 268, 5961–5969, doi:10.1046/j.0014-2956.2001.02550.x.
[20]
Hopfner, K.; Karcher, A.; Craig, L.; Woo, T.T.; Carney, J.P.; Tainer, J.A. Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell？2001, 105, 473–485, doi:10.1016/S0092-8674(01)00335-X.
[21]
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, 2, 499–512, doi:10.1046/j.1365-2443.1997.1380336.x.
[22]
Shen, Y.; Tang, X.-F.; Matsui, I. Subunit interaction and regulation of activity through terminal domains of the family D DNA polymerase from Pyrococcus horikoshii. J. Biol. Chem.？2003, 278, 21247–21257, doi:10.1074/jbc.M212286200.
[23]
Tang, X.-F.; Shen, Y.; Matsui, E.; Matsui, I. Domain topology of the DNA polymerase D complex from hyperthermophilic archaeon Pyrococcus horikoshii. Biochemistry？2004, 43, 11818–11827, doi:10.1021/bi0362931.
[24]
Matsui, I.; Urushibata, Y.; Shen, Y.; Matsui, E.; Yokoyama, H. 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 horikoshi. FEBS Lett.？2011, 585, 452–458, doi:10.1016/j.febslet.2010.12.040.
[25]
Yamasaki, K.; Urushibata, Y.; Yamasaki, T.; Arisaka, F.; Matsui, I. Solution structure of the N-terminal domain of the archaeal D-family DNA polymerase small subunit reveals evolutionary relationship to eukaryotic B-family polymerase. FEBS Lett.？2010, 584, 3370–3375, doi:10.1016/j.febslet.2010.06.026.
[26]
Holm, L.; Sander, C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol.？1993, 233, 123–138, doi:10.1006/jmbi.1993.1489.
[27]
Nuutinen, T.; Tossavainen, H.; Fredriksson, K.; Piril？, P.; Permi, P.; Pospiech, H.; Syvaoja, J.E. The solution structure of the amino-terminal domain of human DNA polymerase ε subunit B is homologous to C-domains of AAA+ proteins. Nucleic Acids Res.？2008, 36, 5102–5110, doi:10.1093/nar/gkn497.
[28]
Jeruzalmi, D.; Yurieva, O.; Zhao, Y.; Young, M.; Stewart, J.; Hingorani, M.; O’Donnel, M.; Kuriyan, J. Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E.coli DNA polymerase III. Cell？2001, 106, 417–428, doi:10.1016/S0092-8674(01)00462-7.
[29]
Putnam, C.D.; Clancy, S.B.; Tsuruta, H.; Gonzalez, S.; Wetmur, J.G.; Tainer, J.A. Structure and mechanism of the RuvB Holliday junction branch migration motor. J. Mol. Biol.？2001, 311, 297–310, doi:10.1006/jmbi.2001.4852.
[30]
Neuwald, A.F.; Aravind, L.; Spouge, J.L.; Koonin, E.V. AAA+: A class of chaperonine-like ATPases associated with the assemply, operation, and disassembly of protein complexes. Genome Res.？1999, 9, 27–43. 9927482
[31]
Baranovskiy, A.G.; Babayeva, N.D.; Liston, V.G.; Rogozin, I.B.; Koonin, E.V.; Pavlov, Y.I.; Vassylyev, D.G.; Tahirov, T.H. X-ray structure of the complex of regulatory subunits of human DNA polymerase delta. Cell Cycle？2008, 7, 3026–3036, doi:10.4161/cc.7.19.6720. 18818516
[32]
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. USA？1998, 95, 14250–14255, doi:10.1073/pnas.95.24.14250.
[33]
M？kiniemi, M.; Pospiech, H.; Kilpel？inen, S.; Jokela, M.; Vihinen, M.; Syv？oja, J.E. A novel family of DNA-polymerase-associated B subunits. Trends Biochem. Sci.？1999, 24, 14–16, doi:10.1016/S0968-0004(98)01327-9.
[34]
Bryson, K.; McGuffin, L.J.; Marsden, R.L.; Ward, J.J.; Sodhi, J.S.; Jones, D.T. Protein structure prediction servers at University College London. Nucleic Acids Res.？2005, 33, W36–W38, doi:10.1093/nar/gki410.
[35]
Castrec, B.; Laurent, S.; Henneke, G.; Flament, D.; Raffin, J.P. The glycine-rich motif of Pyrococcus abyssi DNA polymerase is critical for protein stability. J. Mol. Biol.？2010, 396, 840–848, doi:10.1016/j.jmb.2010.01.006.
