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Volume 156, Issue 5

An archaeal order with multiple minichromosome maintenance genes Free

Abstract

In eukaryotes, a complex of six highly related minichromosome maintenance (MCM) proteins is believed to function as the replicative helicase. Until recently, systems for exploring the molecular mechanisms underlying eukaryotic MCM function have been biochemically intractable. To overcome this, molecular studies of MCM function have been carried out using MCM homologues from the archaea. Archaeal MCM systems studied to date possess a single functional MCM, which forms a homohexameric complex that displays DNA binding, ATPase and helicase activities. We have identified an archaeal order that possesses multiple MCM homologues. searches of available Methanococcales genomes reveal that members of this order possess between two and eight MCM homologues. Phylogenetic analysis suggests that an ancient duplication in the Methanococcales gave rise to two major groups of MCMs. One group contains S2 McmD and possesses a conserved C-terminal insert similar to one observed in eukaryotic MCM3, while the other group contains McmA, -B and -C. Analysis of the genome context of MCMs in the latter group indicates that these genes could have arisen from phage-mediated events. When co-expressed in , the four MCMs from co-purify, indicating the formation of heteromeric complexes . The presence of homologues from both groups in all Methanococcales indicates that there could be functionally important differences between these proteins and that Methanococcales MCMs may therefore provide an interesting additional model for eukaryotic MCM function.

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Keyword(s): GST, glutathione S-transferase , MCM, minichromosome maintenance , ML, maximum-likelihood and NJ, neighbour-joining
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2010-05-01
2024-04-18
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References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
     [Google Scholar]
  2. Bae B., Chen Y. H., Costa A., Onesti S., Brunzelle J. S., Lin Y., Cann I. K., Nair S. K. 2009; Insights into the architecture of the replicative helicase from the structure of an archaeal MCM homolog. Structure 17:211–222
     [Google Scholar]
  3. Bailey T. L., Elkan C. 1994; Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36
     [Google Scholar]
  4. Barry E. R., McGeoch A. T., Kelman Z., Bell S. D. 2007; Archaeal MCM has separable processivity, substrate choice and helicase domains. Nucleic Acids Res 35:988–998
     [Google Scholar]
  5. 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. other authors 1996; Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii. Science 273:1058–1073
     [Google Scholar]
  6. Burland T. G. 2000; dnastar's Lasergene sequence analysis software. Methods Mol Biol 132:71–91
     [Google Scholar]
  7. Campbell A. 1992; Chromosomal insertion sites for phages and plasmids. J Bacteriol 174:7495–7499
     [Google Scholar]
  8. Carpentieri F., De Felice M., De Falco M., Rossi M., Pisani F. M. 2002; Physical and functional interaction between the mini-chromosome maintenance-like DNA helicase and the single-stranded DNA binding protein from the crenarchaeon Sulfolobus solfataricus. J Biol Chem 277:12118–12127
     [Google Scholar]
  9. Castresana J. 2000; Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
     [Google Scholar]
  10. Chong J. P., Hayashi M. K., Simon M. N., Xu R. M., Stillman B. 2000; A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci U S A 97:1530–1535
     [Google Scholar]
  11. Cortez D., Glick G., Elledge S. J. 2004; Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci U S A 101:10078–10083
     [Google Scholar]
  12. Edgell D. R., Doolittle W. F. 1997; Archaea and the origin(s) of DNA replication proteins. Cell 89:995–998
     [Google Scholar]
  13. Galagan J. E., Nusbaum C., Roy A. other authors 2002; The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res 12:532–542
     [Google Scholar]
  14. Grainge I., Scaife S., Wigley D. B. 2003; Biochemical analysis of components of the pre-replication complex of Archaeoglobus fulgidus. Nucleic Acids Res 31:4888–4898
     [Google Scholar]
  15. Groth A. C., Calos M. P. 2004; Phage integrases: biology and applications. J Mol Biol 335:667–678
     [Google Scholar]
  16. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
     [Google Scholar]
  17. Hendrickson E. L., Kaul R., Zhou Y. other authors 2004; Complete genome sequence of the genetically tractable hydrogenotrophic methanogen Methanococcus maripaludis. J Bacteriol 186:6956–6969
     [Google Scholar]
  18. Jenkinson E. R., Chong J. P. 2006; Minichromosome maintenance helicase activity is controlled by N- and C-terminal motifs and requires the ATPase domain helix-2 insert. Proc Natl Acad Sci U S A 103:7613–7618
     [Google Scholar]
  19. Jones D. T., Taylor W. R., Thornton J. M. 1992; The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282
     [Google Scholar]
  20. Kasiviswanathan R., Shin J. H., Melamud E., Kelman Z. 2004; Biochemical characterization of the Methanothermobacter thermautotrophicus minichromosome maintenance (MCM) helicase N-terminal domains. J Biol Chem 279:28358–28366
     [Google Scholar]
  21. Kelman Z., Lee J. K., Hurwitz J. 1999; The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum ΔH contains DNA helicase activity. Proc Natl Acad Sci U S A 96:14783–14788
     [Google Scholar]
  22. Labib K., Tercero J. A., Diffley J. F. 2000; Uninterrupted MCM2–7 function required for DNA replication fork progression. Science 288:1643–1647
     [Google Scholar]
  23. Labib K., Kearsey S. E., Diffley J. F. 2001; MCM2–7 proteins are essential components of prereplicative complexes that accumulate cooperatively in the nucleus during G1-phase and are required to establish, but not maintain, the S-phase checkpoint. Mol Biol Cell 12:3658–3667
     [Google Scholar]
  24. Lin D. I., Aggarwal P., Diehl J. A. 2008; Phosphorylation of MCM3 on Ser-112 regulates its incorporation into the MCM2–7 complex. Proc Natl Acad Sci U S A 105:8079–8084
     [Google Scholar]
  25. McGeoch A. T., Bell S. D. 2005; Eukaryotic/archaeal primase and MCM proteins encoded in a bacteriophage genome. Cell 120:167–168
     [Google Scholar]
  26. McGeoch A. T., Bell S. D. 2008; Extra-chromosomal elements and the evolution of cellular DNA replication machineries. Nat Rev Mol Cell Biol 9:569–574
     [Google Scholar]
  27. Overbeek R., Begley T., Butler R. M. other authors 2005; The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702
     [Google Scholar]
  28. Poplawski A., Grabowski B., Long S. E., Kelman Z. 2001; The zinc finger domain of the archaeal minichromosome maintenance protein is required for helicase activity. J Biol Chem 276:49371–49377
     [Google Scholar]
  29. Prokhorova T. A., Blow J. J. 2000; Sequential MCM/P1 subcomplex assembly is required to form a heterohexamer with replication licensing activity. J Biol Chem 275:2491–2498
     [Google Scholar]
  30. Pruitt K. D., Tatusova T., Maglott D. R. 2007; NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35:D61–D65
     [Google Scholar]
  31. Reiter W. D., Palm P., Yeats S. 1989; Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements. Nucleic Acids Res 17:1907–1914
     [Google Scholar]
  32. Shechter D. F., Ying C. Y., Gautier J. 2000; The intrinsic DNA helicase activity of Methanobacterium thermoautotrophicum ΔH minichromosome maintenance protein. J Biol Chem 275:15049–15059
     [Google Scholar]
  33. Sheu Y. J., Stillman B. 2006; Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol Cell 24:101–113
     [Google Scholar]
  34. Shi Y., Dodson G. E., Mukhopadhyay P. S., Shanware N. P., Trinh A. T., Tibbetts R. S. 2007; Identification of carboxyl-terminal MCM3 phosphorylation sites using polyreactive phosphospecific antibodies. J Biol Chem 282:9236–9243
     [Google Scholar]
  35. Slesarev A. I., Mezhevaya K. V., Makarova K. S. other authors 2002; The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc Natl Acad Sci U S A 99:4644–4649
     [Google Scholar]
  36. Takei Y., Assenberg M., Tsujimoto G., Laskey R. 2002; The MCM3 acetylase MCM3AP inhibits initiation, but not elongation, of DNA replication via interaction with MCM3. J Biol Chem 277:43121–43125
     [Google Scholar]
  37. Thauer R. K. 1998; Biochemistry of methanogenesis: a tribute to Marjory Stephenson; 1998; Marjory Stephenson Prize Lecture. Microbiology 144:2377–2406
     [Google Scholar]
  38. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
     [Google Scholar]
  39. Tsao C. C., Geisen C., Abraham R. T. 2004; Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling. EMBO J 23:4660–4669
     [Google Scholar]
  40. Tsuji T., Ficarro S. B., Jiang W. 2006; Essential role of phosphorylation of MCM2 by Cdc7/Dbf4 in the initiation of DNA replication in mammalian cells. Mol Biol Cell 17:4459–4472
     [Google Scholar]
  41. Tumbula D. L., Bowen T. L., Whitman W. B. 1997; Characterization of pURB500 from the archaeon Methanococcus maripaludis and construction of a shuttle vector. J Bacteriol 179:2976–2986
     [Google Scholar]
  42. Tye B. K. 2000; Insights into DNA replication from the third domain of life. Proc Natl Acad Sci U S A 97:2399–2401
     [Google Scholar]
  43. Walters A. D., Chong J. P. 2009; Methanococcus maripaludis: an archaeon with multiple functional MCM proteins?. Biochem Soc Trans 37:1–6
     [Google Scholar]
  44. Woese C. R., Fox G. E. 1977; Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci U S A 74:5088–5090
     [Google Scholar]
  45. Xia Q., Hendrickson E. L., Zhang Y. other authors 2006; Quantitative proteomics of the archaeon Methanococcus maripaludis validated by microarray analysis and real time PCR. Mol Cell Proteomics 5:868–881
     [Google Scholar]
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An archaeal order with multiple minichromosome maintenance genes
Microbiology 156, 1405 (2010); https://doi.org/10.1099/mic.0.036707-0
/content/journal/micro/10.1099/mic.0.036707-0
/content/journal/micro/10.1099/mic.0.036707-0
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