1887

Microbiology Society logo

Volume 163, Issue 5

Non-essential MCM-related proteins mediate a response to DNA damage in the archaeon Free

Abstract

The single minichromosome maintenance (MCM) protein found in most archaea has been widely studied as a simplified model for the MCM complex that forms the catalytic core of the eukaryotic replicative helicase. Organisms of the order are unusual in possessing multiple MCM homologues. The S2 genome encodes four MCM homologues, McmA–McmD. DNA helicase assays reveal that the unwinding activity of the three MCM-like proteins is highly variable despite sequence similarities and suggests additional motifs that influence MCM function are yet to be identified. While the gene encoding McmA could not be deleted, strains harbouring individual deletions of genes encoding each of the other MCMs display phenotypes consistent with these proteins modulating DNA damage responses. S2 is the first archaeon in which MCM proteins have been shown to influence the DNA damage response.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): archaea , DNA damage , methanogen and minichromosome maintenance
© 2017 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000460
2017-05-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/163/5/745.html?itemId=/content/journal/micro/10.1099/mic.0.000460&mimeType=html&fmt=ahah

References

  1. Labib K, Tercero JA, Diffley JF. Uninterrupted MCM2-7 function required for DNA replication fork progression. Science 2000; 288:1643–1647 [View Article][PubMed]
     [Google Scholar]
  2. Ilves I, Petojevic T, Pesavento JJ, Botchan MR. Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol Cell 2010; 37:247–258 [View Article][PubMed]
     [Google Scholar]
  3. Bochman ML, Schwacha A. The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol Mol Biol Rev 2009; 73:652–683 [View Article][PubMed]
     [Google Scholar]
  4. Takei Y, Assenberg M, Tsujimoto G, Laskey R. The MCM3 acetylase MCM3AP inhibits initiation, but not elongation, of DNA replication via interaction with MCM3. J Biol Chem 2002; 277:43121–43125 [View Article][PubMed]
     [Google Scholar]
  5. Sheu YJ, Stillman B. Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol Cell 2006; 24:101–113 [View Article][PubMed]
     [Google Scholar]
  6. Lei M, Kawasaki Y, Young MR, Kihara M, Sugino A et al. Mcm2 is a target of regulation by Cdc7-Dbf4 during the initiation of DNA synthesis. Genes Dev 1997; 11:3365–3374 [View Article][PubMed]
     [Google Scholar]
  7. Ibarra A, Schwob E, Méndez J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci USA 2008; 105:8956–8961 [View Article][PubMed]
     [Google Scholar]
  8. Woodward AM, Göhler T, Luciani MG, Oehlmann M, Ge X et al. Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 2006; 173:673–683 [View Article][PubMed]
     [Google Scholar]
  9. Maki K, Inoue T, Onaka A, Hashizume H, Somete N et al. Abundance of prereplicative complexes (Pre-RCs) facilitates recombinational repair under replication stress in fission yeast. J Biol Chem 2011; 286:41701–41710 [View Article][PubMed]
     [Google Scholar]
  10. Cortez D, Glick G, Elledge SJ. Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc Natl Acad Sci USA 2004; 101:10078–10083 [View Article][PubMed]
     [Google Scholar]
  11. Shi Y, Dodson GE, Mukhopadhyay PS, Shanware NP, Trinh AT et al. Identification of carboxyl-terminal MCM3 phosphorylation sites using polyreactive phosphospecific antibodies. J Biol Chem 2007; 282:9236–9243 [View Article][PubMed]
     [Google Scholar]
  12. Lee JH, Paull TT. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005; 308:551–554 [View Article][PubMed]
     [Google Scholar]
  13. D'Amours D, Jackson SP. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002; 3:317–327 [View Article][PubMed]
     [Google Scholar]
  14. Han X, Pozo FM, Wisotsky JN, Wang B, Jacobberger JW et al. Phosphorylation of mini-chromosome maintenance 3 (MCM3) by Chk1 negatively regulates DNA replication and checkpoint activation. J Biol Chem 2015; 289:24716–24723 [CrossRef]
     [Google Scholar]
  15. Komata M, Bando M, Araki H, Shirahige K. The direct binding of Mrc1, a checkpoint mediator, to Mcm6, a replication helicase, is essential for the replication checkpoint against methyl methanesulfonate-induced stress. Mol Cell Biol 2009; 29:5008–5019 [View Article][PubMed]
     [Google Scholar]
  16. Bailis JM, Luche DD, Hunter T, Forsburg SL. Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote S-phase genome stability. Mol Cell Biol 2008; 28:1724–1738 [View Article][PubMed]
     [Google Scholar]
  17. Trenz K, Smith E, Smith S, Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. Embo J 2006; 25:1764–1774 [View Article][PubMed]
     [Google Scholar]
  18. Han X, Aslanian A, Fu K, Tsuji T, Zhang Y. The interaction between checkpoint kinase 1 (Chk1) and the minichromosome maintenance (MCM) complex is required for DNA damage-induced Chk1 phosphorylation. J Biol Chem 2014; 289:24716–24723 [View Article][PubMed]
     [Google Scholar]
  19. Ilves I, Tamberg N, Botchan MR. Checkpoint kinase 2 (Chk2) inhibits the activity of the Cdc45/MCM2-7/GINS (CMG) replicative helicase complex. Proc Natl Acad Sci USA 2012; 109:13163–13170 [View Article][PubMed]
     [Google Scholar]
  20. McNairn AJ, Rinaldi VD, Schimenti JC. Repair of meiotic DNA breaks and homolog pairing in mouse meiosis requires a minichromosome maintenance (MCM) Paralog. Genetics 2017; 205:529–537 [View Article][PubMed]
     [Google Scholar]
  21. Park J, Long DT, Lee KY, Abbas T, Shibata E et al. The MCM8-MCM9 complex promotes RAD51 recruitment at DNA damage sites to facilitate homologous recombination. Mol Cell Biol 2013; 33:1632–1644 [View Article][PubMed]
     [Google Scholar]
  22. Traver S, Coulombe P, Peiffer I, Hutchins JR, Kitzmann M et al. MCM9 is required for mammalian DNA mismatch repair. Mol Cell 2015; 59:831–839 [View Article][PubMed]
     [Google Scholar]
  23. Bell SD, Botchan MR. The minichromosome maintenance replicative helicase. Cold Spring Harb Perspect Biol 2013; 5:a012807 [View Article][PubMed]
     [Google Scholar]
  24. McGeoch AT, Trakselis MA, Laskey RA, Bell SD. Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat Struct Mol Biol 2005; 12:756–762 [View Article][PubMed]
     [Google Scholar]
  25. Jenkinson ER, Chong JP. Minichromosome maintenance helicase activity is controlled by N- and C-terminal motifs and requires the ATPase domain helix-2 insert. Proc Natl Acad Sci USA 2006; 103:7613–7618 [View Article][PubMed]
     [Google Scholar]
  26. Kasiviswanathan R, Shin JH, Melamud E, Kelman Z. Biochemical characterization of the Methanothermobacter thermautotrophicus minichromosome maintenance (MCM) helicase N-terminal domains. J Biol Chem 2004; 279:28358–28366 [View Article][PubMed]
     [Google Scholar]
  27. Chong JP, Hayashi MK, Simon MN, Xu RM, Stillman B. A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci USA 2000; 97:1530–1535 [View Article][PubMed]
     [Google Scholar]
  28. Walters AD, Chong JP. An archaeal order with multiple minichromosome maintenance genes. Microbiology 2010; 156:1405–1414 [View Article][PubMed]
     [Google Scholar]
  29. Krupovic M, Gribaldo S, Bamford DH, Forterre P. The evolutionary history of archaeal MCM helicases: a case study of vertical evolution combined with hitchhiking of mobile genetic elements. Mol Biol Evol 2010; 27:2716–2732 [View Article][PubMed]
     [Google Scholar]
  30. Hendrickson EL, Kaul R, Zhou Y, Bovee D, Chapman P et al. Complete genome sequence of the genetically tractable hydrogenotrophic methanogen Methanococcus maripaludis. J Bacteriol 2004; 186:6956–6969 [View Article][PubMed]
     [Google Scholar]
  31. McGeoch AT, Bell SD. Extra-chromosomal elements and the evolution of cellular DNA replication machineries. Nat Rev Mol Cell Biol 2008; 9:569–574 [View Article][PubMed]
     [Google Scholar]
  32. Majerník AI, Lundgren M, McDermott P, Bernander R, Chong JP. DNA content and nucleoid distribution in Methanothermobacter thermautotrophicus. J Bacteriol 2005; 187:1856–1858 [View Article][PubMed]
     [Google Scholar]
  33. Pan M, Santangelo TJ, Li Z, Reeve JN, Kelman Z. Thermococcus kodakarensis encodes three MCM homologs but only one is essential. Nucleic Acids Res 2011; 39:9671–9680 [View Article][PubMed]
     [Google Scholar]
  34. Sarmiento F, Leigh JA, Whitman WB. Genetic systems for hydrogenotrophic methanogens. Methods Enzymol 2011; 494:43–73 [View Article][PubMed]
     [Google Scholar]
  35. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997; 25:4876–4882 [View Article][PubMed]
     [Google Scholar]
  36. Shin JH, Jiang Y, Grabowski B, Hurwitz J, Kelman Z. Substrate requirements for duplex DNA translocation by the eukaryal and archaeal minichromosome maintenance helicases. J Biol Chem 2003; 278:49053–49062 [View Article][PubMed]
     [Google Scholar]
  37. Moore BC, Leigh JA. Markerless mutagenesis in Methanococcus maripaludis demonstrates roles for alanine dehydrogenase, alanine racemase, and alanine permease. J Bacteriol 2005; 187:972–979 [View Article][PubMed]
     [Google Scholar]
  38. Haydock AK, Porat I, Whitman WB, Leigh JA. Continuous culture of Methanococcus maripaludis under defined nutrient conditions. FEMS Microbiol Lett 2004; 238:85–91 [View Article][PubMed]
     [Google Scholar]
  39. Sarmiento F, Mrázek J, Whitman WB. Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proc Natl Acad Sci USA 2013; 110:4726–4731 [View Article][PubMed]
     [Google Scholar]
  40. Bernander R, Poplawski A. Cell cycle characteristics of thermophilic archaea. J Bacteriol 1997; 179:4963–4969 [View Article][PubMed]
     [Google Scholar]
  41. Maisnier-Patin S, Malandrin L, Birkeland NK, Bernander R. Chromosome replication patterns in the hyperthermophilic euryarchaea Archaeoglobus fulgidus and Methanocaldococcus (Methanococcus) jannaschii. Mol Microbiol 2002; 45:1443–1450 [View Article][PubMed]
     [Google Scholar]
  42. Hildenbrand C, Stock T, Lange C, Rother M, Soppa J. Genome copy numbers and gene conversion in methanogenic archaea. J Bacteriol 2011; 193:734–743 [View Article][PubMed]
     [Google Scholar]
  43. Cooper S, Helmstetter CE. Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 1968; 31:519–540 [View Article][PubMed]
     [Google Scholar]
  44. Breuert S, Allers T, Spohn G, Soppa J. Regulated polyploidy in halophilic archaea. PLoS One 2006; 1:e92 [View Article][PubMed]
     [Google Scholar]
  45. Kiener A, Gall R, Rechsteiner T, Leisinger T. Photoreactivation in Methanobacterium thermoautotrophicum. Arch Microbiol 1985; 143:147–150 [View Article]
     [Google Scholar]
  46. Ishimi Y. A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J Biol Chem 1997; 272:24508–24513 [View Article][PubMed]
     [Google Scholar]
  47. Xia Q, Hendrickson EL, Zhang Y, Wang T, Taub F et al. Quantitative proteomics of the archaeon Methanococcus maripaludis validated by microarray analysis and real time PCR. Mol Cell Proteomics 2006; 5:868–881 [View Article][PubMed]
     [Google Scholar]
  48. Schwab BL, Leist M, Knippers R, Nicotera P. Selective proteolysis of the nuclear replication factor MCM3 in apoptosis. Exp Cell Res 1998; 238:415–421 [View Article][PubMed]
     [Google Scholar]
  49. Schories B, Engel K, Dörken B, Gossen M, Bommert K. Characterization of apoptosis-induced Mcm3 and Cdc6 cleavage reveals a proapoptotic effect for one Mcm3 fragment. Cell Death Differ 2004; 11:940–942 [View Article][PubMed]
     [Google Scholar]
  50. Delmas S, Shunburne L, Ngo HP, Allers T. Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination. PLoS Genet 2009; 5:e1000552 [View Article][PubMed]
     [Google Scholar]
  51. Li Z, Santangelo TJ, Cuboňová L, Reeve JN, Kelman Z. Affinity purification of an archaeal DNA replication protein network. MBio 2010; 1:e00221–10 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000460
Loading
Non-essential MCM-related proteins mediate a response to DNA damage in the archaeon Methanococcus maripaludis
Microbiology 163, 745 (2017); https://doi.org/10.1099/mic.0.000460
/content/journal/micro/10.1099/mic.0.000460
/content/journal/micro/10.1099/mic.0.000460
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error