An extended network of genomic maintenance in the archaeon Pyrococcus abyssi highlights unexpected associations between eucaryotic homologs

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Pluchon, Pierre François ^a   Fouqueau, Thomas ^b   Crezé, Christophe ^a   Laurent, Sébastien ^a   Briffotaux, Julien ^a,d   Hogrel, Gaëlle ^a   Palud, Adeline ^a   Henneke, Ghislaine ^a   Godfroy, Anne ^a   Hausner, Winfried ^b   Thomm, Michael ^b   Nicolas, Jacques ^c   Flament, Didier ^a  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c CAMPUS DE BEAULIEU   (France)

^d LABORATOIRE D OPTIQUE ET BIOSCIENCES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; DNA PRIMASE; DNA2 LIKE HELICASE; HELICASE; MRE11 PROTEIN; NUCLEASE; PAB0431 PROTEIN; PAB0961 PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RAD50 PROTEIN; REPLICATION FACTOR A; RNA POLYMERASE; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP D PROTEIN; CARRIER PROTEIN; PROTEIN BINDING; PROTEOME;

ARCHAEAL GENOME; ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; EUKARYOTE; GENOMIC INSTABILITY; GENOMIC MAINTENANCE; HIGH TEMPERATURE; HYPERTHERMOPHILIC ARCHAEON; MASS SPECTROMETRY; NONHUMAN; PROTEIN INTERACTION; PROTEIN PURIFICATION; PYROCOCCUS ABYSSI; REPLISOME; TRANSCRIPTION INITIATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; METABOLISM; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEOMICS;

CARRIER PROTEINS; DNA REPLICATION; GENOMICS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; PYROCOCCUS ABYSSI; RECOMBINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84892409335     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079707     Document Type: Article

References (75)

1. Lindahl T (1993) Instability and decay of the primary structure of DNA. Nature 362: 709-715. doi:10.1038/362709a0. PubMed: 8469282.
2. Palud A, Villani G, L'Haridon S, Querellou J, Raffin JP et al. (2008) Intrinsic properties of the two replicative DNA polymerases of Pyrococcus abyssi in replicating abasic sites: possible role in DNA damage tolerance? Mol Microbiol 70: 746-761. doi:10.1111/j.1365-2958.2008.06446.x. PubMed: 18826407.
3. Grogan DW, Carver GT, Drake JW (2001) Genetic fidelity under harsh conditions: analysis of spontaneous mutation in the thermoacidophilic archaeon Sulfolobus acidocaldarius. Proc Natl Acad Sci U S A 98: 7928-7933. doi:10.1073/pnas.141113098. PubMed: 11427720.
4. Grogan DW (2004) Stability and repair of DNA in hyperthermophilic Archaea. Curr Issues Mol Biol 6: 137-144. PubMed: 15119824.
5. Yutin N, Makarova KS, Mekhedov SL, Wolf YI, Koonin EV (2008) The deep archaeal roots of eukaryotes. Mol Biol Evol 25: 1619-1630. doi: 10.1093/molbev/msn108. PubMed: 18463089.
6. Kelman Z, White MF (2005) Archaeal DNA replication and repair. Curr Opin Microbiol 8: 669-676. doi:10.1016/j.mib.2005.10.001. PubMed: 16242991.
7. Boudsocq F, Iwai S, Hanaoka F, Woodgate R (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta. Nucleic Acids Res 29: 4607-4616.
8. Lucas-Lledó JI, Lynch M (2009) Evolution of mutation rates: phylogenomic analysis of the photolyase/cryptochrome family. Mol Biol Evol 26: 1143-1153. doi:10.1093/molbev/msp029. PubMed: 19228922.
9. Perugino G, Vettone A, Illiano G, Valenti A, Ferrara MC et al. (2012) Activity and regulation of archaeal DNA alkyltransferase: conserved protein involved in repair of DNA alkylation damage. J Biol Chem 287: 4222-4231. doi:10.1074/jbc.M111.308320. PubMed: 22167184.
10. Sartori AA, Jiricny J (2003) Enzymology of base excision repair in the hyperthermophilic archaeon Pyrobaculum aerophilum. J Biol Chem 278: 24563-24576. doi:10.1074/jbc.M302397200. PubMed: 12730226.
11. Busch CR, DiRuggiero J (2010) MutS and MutL are dispensable for maintenance of the genomic mutation rate in the halophilic archaeon Halobacterium salinarum NRC-1. PLOS ONE 5: e9045. doi:10.1371/journal.pone. 0009045. PubMed: 20140215.
12. Atomi H, Imanaka T, Fukui T (2012) Overview of the genetic tools in the Archaea. Front Microbiol 3: 337. PubMed: 23060865.
13. Fujikane R, Ishino S, Ishino Y, Forterre P (2010) Genetic analysis of DNA repair in the hyperthermophilic archaeon, Thermococcus kodakaraensis. Genes Genet Syst 85: 243-257. doi:10.1266/ggs.85.243. PubMed: 21178304.
14. Li Z, Santangelo TJ, Cuboňová L, Reeve JN, Kelman Z (2010) Affinity purification of an archaeal DNA replication protein network. MBio 1. PubMed: 20978540
15. Motz M, Kober I, Girardot C, Loeser E, Bauer U et al. (2002) Elucidation of an archaeal replication protein network to generate enhanced PCR enzymes. J Biol Chem 277: 16179-16188. doi:10.1074/jbc.M107793200. PubMed: 11805086.
16. Li Z, Pan M, Santangelo TJ, Chemnitz W, Yuan W et al. (2011) A novel DNA nuclease is stimulated by association with the GINS complex. Nucleic Acids Res 39: 6114-6123. doi:10.1093/nar/gkr181. PubMed: 21459845.
17. Makarova KS, Koonin EV, Kelman Z (2012) The CMG (CDC45/RecJ, MCM, GINS) complex is a conserved component of the DNA replication system in all archaea and eukaryotes. Biol Direct 7: 7. doi: 10.1186/1745-6150-7-7. PubMed: 22329974.
18. Groisillier A, Hervé C, Jeudy A, Rebuffet E, Pluchon PF et al. (2010) MARINE-EXPRESS: taking advantage of high throughput cloning and expression strategies for the post-genomic analysis of marine organisms. Microb Cell Factories 9: 45. doi:10.1186/1475-2859-9-45. PubMed: 20546566.
19. Godfroy A, Postec A, Raven N (2006) 4 Growth of Hyperthermophilic Microorganisms for Physiological and Nutritional Studies. In: Fred A Rainey DoBSLSUBRLAUSA, Aharon Oren Institute of Life Sciences the Hebrew University of Jerusalem Jerusalem I, editors. Methods in Microbiology: Academic Press. pp. 93-108
20. Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL et al. (2012) A travel guide to Cytoscape plugins. Nat Methods 9: 1069-1076. doi: 10.1038/nmeth.2212. PubMed: 23132118.
21. Yellaboina S, Tasneem A, Zaykin DV, Raghavachari B, Jothi R (2011) DOMINE: a comprehensive collection of known and predicted domain-domain interactions. Nucleic Acids Res 39: D730-D735. doi: 10.1093/nar/gkq1229. PubMed: 21113022.
22. Friedel CC, Zimmer R (2009) Identifying the topology of protein complexes from affinity purification assays. Bioinformatics 25: 2140-2146. doi:10.1093/bioinformatics/btp353. PubMed: 19505940.
23. Milenković T, Memišević V, Bonato A, Pržulj N (2011) Dominating biological networks. PLOS ONE 6: e23016. doi:10.1371/journal. pone.0023016. PubMed: 21887225.
24. Meslet-Cladiére L, Norais C, Kuhn J, Briffotaux J, Sloostra JW et al. (2007) A novel proteomic approach identifies new interaction partners for proliferating cell nuclear antigen. J Mol Biol 372: 1137-1148. doi: 10.1016/j.jmb.2007.06.056. PubMed: 17720188.
25. Ren B, Kühn J, Meslet-Cladiere L, Briffotaux J, Norais C et al. (2009) Structure and function of a novel endonuclease acting on branched DNA substrates. EMBO J 28: 2479-2489. doi:10.1038/emboj.2009.192. PubMed: 19609302.
26. Spitalny P, Thomm M (2003) Analysis of the open region and of DNA-protein contacts of archaeal RNA polymerase transcription complexes during transition from initiation to elongation. J Biol Chem 278: 30497-30505. doi:10.1074/jbc.M303633200. PubMed: 12783891.
27. Bader GD, Hogue CW (2002) Analyzing yeast protein-protein interaction data obtained from different sources. Nat Biotechnol 20: 991-997. doi:10.1038/nbt1002-991. PubMed: 12355115.
28. von Mering C, Krause R, Snel B, Cornell M, Oliver SG et al. (2002) Comparative assessment of large-scale data sets of protein-protein interactions. Nature 417: 399-403. PubMed: 12000970.
29. 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: 10.1186/1471-2156-8-31. PubMed: 17559652.
30. Skowyra A, MacNeill SA (2012) Identification of essential and non-essential single-stranded DNA-binding proteins in a model archaeal organism. Nucleic Acids Res 40: 1077-1090. doi:10.1093/nar/gkr913. PubMed: 21976728.
31. MacNeill SA (2011) Protein-protein interactions in the archaeal core replisome. Biochem Soc Trans 39: 163-168. doi:10.1042/BST0390163. PubMed: 21265766.
32. Warbrick E (2000) The puzzle of PCNA's many partners. Bioessays 22: 997-1006. doi:10.1002/1521-1878(200011)22:11. PubMed: 11056476.
33. Pan M, Kelman LM, Kelman Z (2011) The archaeal PCNA proteins. Biochem Soc Trans 39: 20-24. doi:10.1042/BST0390020. PubMed: 21265741.
34. Rouillon C, Henneke G, Flament D, Querellou J, Raffin JP (2007) DNA polymerase switching on homotrimeric PCNA at the replication fork of the euryarchaea Pyrococcus abyssi. J Mol Biol 369: 343-355. doi: 10.1016/j.jmb.2007.03.054. PubMed: 17442344.
35. Creze C, Ligabue A, Laurent S, Lestini R, Laptenok SP et al. (2012) Modulation of the Pyrococcus abyssi NucS endonuclease activity by the replication clamp PCNA at functional and structural levels. J Biol Chem.
36. Komori K, Ishino Y (2001) Replication protein A in Pyrococcus furiosus is involved in homologous DNA recombination. J Biol Chem 276: 25654-25660. doi:10.1074/jbc.M102423200. PubMed: 11342551.
37. Henneke G, Flament D, Hübscher U, Querellou J, Raffin JP (2005) The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J Mol Biol 350: 53-64. doi:10.1016/j.jmb.2005.04.042. PubMed: 15922358.
38. Stracker TH, Petrini JH (2011) The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 12: 90-103. doi:10.1038/nrm3047. PubMed: 21252998.
39. Constantinesco F, Forterre P, Elie C (2002) NurA, a novel 5′-3′ nuclease gene linked to rad50 and mre11 homologs of thermophilic Archaea. EMBO Rep 3: 537-542. doi:10.1093/embo-reports/kvf112. PubMed: 12052775.
40. Constantinesco F, Forterre P, Koonin EV, Aravind L, Elie C (2004) A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res 32: 1439-1447. doi: 10.1093/nar/gkh283. PubMed: 14990749.
41. Hopkins BB, Paull TT (2008) The P. furiosus mre11/rad50 complex promotes 5′ strand resection at a DNA double-strand break. Cell 135: 250-260. doi:10.1016/j.cell.2008.09.054. PubMed: 18957200.
42. Quaiser A, Constantinesco F, White MF, Forterre P, Elie C (2008) The Mre11 protein interacts with both Rad50 and the HerA bipolar helicase and is recruited to DNA following gamma irradiation in the archaeon Sulfolobus acidocaldarius. BMC Mol Biol 9: 25. doi: 10.1186/1471-2199-9-25. PubMed: 18294364.
43. Delmas S, Shunburne L, Ngo HP, Allers T (2009) Mre11-Rad50 promotes rapid repair of DNA damage in the polyploid archaeon Haloferax volcanii by restraining homologous recombination. PLOS Genet 5: e1000552. PubMed: 19593371.
44. Huertas P (2010) DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol 17: 11-16. doi:10.1038/nsmb.1710. PubMed: 20051983.
45. Beattie TR, Bell SD (2011) Molecular machines in archaeal DNA replication. Curr Opin Chem Biol 15: 614-619. doi:10.1016/j.cbpa.2011.07.017. PubMed: 21852183.
46. Aravind L, Koonin EV (1998) Phosphoesterase domains associated with DNA polymerases of diverse origins. Nucleic Acids Res 26: 3746-3752. doi:10.1093/nar/26.16.3746. PubMed: 9685491.
47. Stano NM, Chen J, McHenry CS (2006) A coproofreading Zn(2+)-dependent exonuclease within a bacterial replicase. Nat Struct Mol Biol 13: 458-459. doi:10.1038/nsmb1078. PubMed: 16604084.
48. Teplyakov A, Obmolova G, Khil PP, Howard AJ, Camerini-Otero RD et al. (2003) Crystal structure of the Escherichia coli YcdX protein reveals a trinuclear zinc active site. Proteins 51: 315-318. doi:10.1002/prot.10352. PubMed: 12661000.
49. Khil PP, Camerini-Otero RD (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microbiol 44: 89-105. doi:10.1046/j.1365-2958.2002.02878.x. PubMed: 11967071.
50. Kusser AG, Bertero MG, Naji S, Becker T, Thomm M et al. (2008) Structure of an archaeal RNA polymerase. J Mol Biol 376: 303-307. doi:10.1016/j.jmb.2007. 08.066. PubMed: 18164030.
51. Lin Y, Lin LJ, Sriratana P, Coleman K, Ha T et al. (2008) Engineering of functional replication protein a homologs based on insights into the evolution of oligonucleotide/oligosaccharide-binding folds. J Bacteriol 190: 5766-5780. doi:10.1128/JB.01930-07. PubMed: 18586938.
52. Richard DJ, Bell SD, White MF (2004) Physical and functional interaction of the archaeal single-stranded DNA-binding protein SSB with RNA polymerase. Nucleic Acids Res 32: 1065-1074. doi: 10.1093/nar/gkh259. PubMed: 14872062.
53. Sikorski TW, Ficarro SB, Holik J, Kim T, Rando OJ et al. (2011) Sub1 and RPA associate with RNA polymerase II at different stages of transcription. Mol Cell 44: 397-409. doi:10.1016/j.molcel.2011.09.013. PubMed: 22055186.
54. Ayyagari R, Gomes XV, Gordenin DA, Burgers PM (2003) Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J Biol Chem 278: 1618-1625. doi:10.1074/jbc.M209801200. PubMed: 12424238.
55. Duxin JP, Moore HR, Sidorova J, Karanja K, Honaker Y et al. (2012) Okazaki fragment processing-independent role for human Dna2 enzyme during DNA replication. J Biol Chem 287: 21980-21991. doi: 10.1074/jbc.M112.359018. PubMed: 22570476.
56. Matsunaga F, Norais C, Forterre P, Myllykallio H (2003) Identification of short 'eukaryotic' Okazaki fragments synthesized from a prokaryotic replication origin. EMBO Rep 4: 154-158. doi:10.1038/sj.embor.embor732. PubMed: 12612604.
57. Henneke G (2012) In vitro reconstitution of RNA primer removal in Archaea reveals the existence of two pathways. Biochem J 447: 271-280. doi:10.1042/BJ20120959. PubMed: 22849643.
58. Lao-Sirieix SH, Pellegrini L, Bell SD (2005) The promiscuous primase. Trends Genet 21: 568-572. doi:10.1016/j.tig.2005.07.010. PubMed: 16095750.
59. Hu J, Guo L, Wu K, Liu B, Lang S et al. (2012) Template-dependent polymerization across discontinuous templates by the heterodimeric primase from the hyperthermophilic archaeon Sulfolobus solfataricus. Nucleic Acids Res 40: 3470-3483. doi:10.1093/nar/gkr1256. PubMed: 22189102.
60. Rudolf J, Makrantoni V, Ingledew WJ, Stark MJ, White MF (2006) The DNA repair helicases XPD and FancJ have essential iron-sulfur domains. Mol Cell 23: 801-808. doi:10.1016/j.molcel.2006.07.019. PubMed: 16973432.
61. Coin F, Oksenych V, Egly JM (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell 26: 245-256. doi:10.1016/j.molcel.2007.03.009. PubMed: 17466626.
62. Rudolf J, Rouillon C, Schwarz-Linek U, White MF (2010) The helicase XPD unwinds bubble structures and is not stalled by DNA lesions removed by the nucleotide excision repair pathway. Nucleic Acids Res 38: 931-941. doi:10.1093/nar/gkp1058. PubMed: 19933257.
63. Boubakri H, de Septenville AL, Viguera E, Michel B (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29: 145-157. doi:10.1038/emboj.2009.308. PubMed: 19851282.
64. White MF (2009) Structure, function and evolution of the XPD family of iron-sulfur-containing 5′ - >3′ DNA helicases. Biochem Soc Trans 37: 547-551. doi:10.1042/BST0370547. PubMed: 19442249.
65. Voloshin ON, Vanevski F, Khil PP, Camerini-Otero RD (2003) Characterization of the DNA damage-inducible helicase DinG from Escherichia coli. J Biol Chem 278: 28284-28293. doi:10.1074/jbc.M301188200. PubMed: 12748189.
66. Shin JH, Santangelo TJ, Xie Y, Reeve JN, Kelman Z (2007) Archaeal minichromosome maintenance (MCM) helicase can unwind DNA bound by archaeal histones and transcription factors. J Biol Chem 282: 4908-4915. PubMed: 17158792.
67. Ishitani R, Sugita Y, Dohmae N, Furuya N, Hattori M et al. (2008) Mg2+-sensing mechanism of Mg2+ transporter MgtE probed by molecular dynamics study. Proc Natl Acad Sci U S A 105: 15393-15398. doi:10.1073/pnas.0802991105. PubMed: 18832160.
68. Scott JW, Hawley SA, Green KA, Anis M, Stewart G et al. (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113: 274-284. doi:10.1172/ JCI19874. PubMed: 14722619.
69. Chan PP, Holmes AD, Smith AM, Tran D, Lowe TM (2012) The UCSC Archaeal Genome Browser: 2012 update. Nucleic Acids Res 40: D646-D652. doi:10.1093/nar/gkr990. PubMed: 22080555.
70. King NP, Lee TM, Sawaya MR, Cascio D, Yeates TO (2008) Structures and functional implications of an AMP-binding cystathionine beta-synthase domain protein from a hyperthermophilic archaeon. J Mol Biol 380: 181-192. doi:10.1016/j.jmb.2008.04.073. PubMed: 18513746.
71. Haldenby S, White MF, Allers T (2009) RecA family proteins in archaea: RadA and its cousins. Biochem Soc Trans 37: 102-107. doi: 10.1042/BST0370102. PubMed: 19143611.
72. Gouge J, Ralec C, Henneke G, Delarue M (2012) Molecular recognition of canonical and deaminated bases by P. abyssi family B DNA polymerase. J Mol Biol 423: 315-336. doi:10.1016/j.jmb.2012.07.025. PubMed: 22902479.
73. Le Breton M, Henneke G, Norais C, Flament D, Myllykallio H et al. (2007) The heterodimeric primase from the euryarchaeon Pyrococcus abyssi: a multifunctional enzyme for initiation and repair? J Mol Biol 374: 1172-1185. doi:10.1016/j.jmb.2007.10.015. PubMed: 17991487.
74. Le Laz S, Le Goaziou A, Henneke G (2010) Structure-specific nuclease activities of Pyrococcus abyssi RNase HII. J Bacteriol 192: 3689-3698. doi:10.1128/JB.00268-10. PubMed: 20472790.
75. Ren B, Kuhn J, Meslet-Cladiere L, Myllykallio H, Ladenstein R (2007) Crystallization and preliminary X-ray analysis of a RecB-family nuclease from the archaeon Pyrococcus abyssi. Acta Crystallogr Sect Struct Biol Cryst Commun 63: 406-408. doi:10.1107/S1744309107015278. PubMed: 17565182.