Replication origins experimentally identified in archaeal chromosomes
1. Introduction
One fundamental challenge of cells is to accurately copy their genetic material for cell proliferation. This task is performed by core machineries considered conserved in all three domains of life: bacteria, archaea and eukaryotes [1].
For the vast majority of bacteria, the genome consists of one circular DNA molecule. Replication is initiated at a single replication origin from which two replication forks progress in the opposite direction. Replication termination takes place in the terminus region opposite the origin so that each replication fork has copied approximately one half of the genome. Studies of
Unlike bacterial genomes, eukaryotic chromosomes contain numerous replication origins that can be used as backup origins to rescue arrested forks. Consequently, the importance of replication restart pathways in eukaryotes has long been ignored. However, recent studies have demonstrated that fork restart pathways operate also in eukaryotic cells and are important for cell viability under replication stress conditions. Eukaryotic replication restart pathways described also involve recombination proteins, as in bacteria. Thus it appears that general rules regarding replication restart and the key role of recombination proteins in these processes are conserved in bacteria, yeast and higher eukaryotes, but little is known in archaea, the third domain of life. This is of interest as archaea appear to be evolutionary hybrids between bacteria and eukaryotes.
Three main archaeal phyla are currently recognized: Crenarchaeota, Euryarchaeota [2] and Thaumarchaeota [3]. Similarly to most bacteria, archaeal genomes are also formed by a circular DNA molecule. However, unlike bacteria, some archaeal species have a single origin, whereas others have multiple origins per chromosome. Moreover, the ploidy of the genome in archaea varies considerably, with some species having one copy per cell whereas others have up to 25 copies of their genome in proliferating cells. As archaeal DNA replication consists both of evolutionary conserved as well as original features, understanding replication restart in these microorganisms will shed light on these fundamental but very complex pathways crucial to fulfill DNA replication. In this chapter we present recent advances on replication in archaea, followed by focused description of the Hef/XPF protein and its implication in replication restart in archaeal cells.
2. DNA replication origins in archaea
2.1. Multiple replication origins
Bacteria replicate their circular chromosome from a defined site called a replication origin. Two replication forks assemble at the replication origin and move in opposite directions. Each replication fork progresses at the same rate, and termination occurs at specific sites opposite the origin. Archaeal chromosomes are also circular, but whereas some archaea initiate replication from a single origin others replicate their chromosome from multiple replication origins, as observed for eukaryotic linear chromosomes (Table 1).
Euryarchaeota | 1 | [4] | |
3 | [5-7] | ||
2 | [7] | ||
1 | [8] | ||
|
4 | [9, 10] | |
2 | [11] | ||
1 | [12] | ||
Crenarchaeota | 3 | [13] | |
3 | [13] | ||
3 | [14] | ||
4 | [15] | ||
|
At least 2 | [16] | |
Thaumarchaeota | 1 | [7] |
Replication from a single replication origin was reported experimentally in the euryarchaea
2.2. Archaeal replication initiator Orc1/Cdc6 proteins and origins recognition
How replication is regulated to allow a single circular DNA molecule to be replicated from uneven multiple origins is an ongoing question in archaea (Figure 1).
From each replication origin two replication forks are assembled and progress at the same rate so that termination of the replication is asynchronous. The origin region usually has a high content of adenine and thymine residues flanked by several conserved repeated motifs known as Origin Recognition Boxes (ORBs). In manycases archaeal replication origins are linked to replication genes [15, 18] and are located near genes coding initiator proteins. Despite the conservation of the replication origin-initiator structure, archaeal replication origins exhibit considerable diversity in terms of both ORB elements and their initiator genes [7, 11, 12]. Because replication origins can be dramatically diverse, it may facilitate differential usages by these microorganisms to adapt to various harsh environments.
All sequenced archaeal genomes encode proteins homologous to the eukaryotic initiator proteins Orc1 and Cdc6. Because the archaeal proteins are related both to the eukaryotic Orc1 subunit, involved in the replication origin recognition, and Cdc6, involved in the replicative helicase recruitment, they may combine both activities in a single polypeptide. Indeed, several studies have shown that the archaeal replicative helicase MCM is recruited by Cdc6/Orc1 proteins at replication origins [14, 19, 20]. Archaeal Cdc6/Orc1 proteins also share mechanistic similarities with the bacterial initiator protein DnaA.
How multiple replication origins are regulated by Cdc6/Orc1 proteins in archaeal cells is a complex question. The number of Orc1/Cdc6 proteins varies between species, and recent genetic studies attempting to delete
For instance, four
Moreover, additional role of initiator proteins independent of replication origins has recently been suggested by serial deletions of
2.3. Are replication origins essential for viability in archaea?
The specific initiation sites, replication origins, on the chromosome of
How replication initiates in absence of replication origins? Because no evidence for activation of dormant origins has been found, authors favoured the hypothesis that replication initiation occurs randomly on the chromosome at recombination intermediates. Recombination-Dependent Replication (RDR) has first been observed in
Indeed Hawkins
But the deletion of
An alternative explanation for RDR is activation of dormant origins randomly in cells so that no preferential origin emerged at the level of a cell population [29, 30]. In this scenario the essentiality of RadA could imply that randomly-initiated replication forks more often collapse and have to be restarted. This notion would be consistent with an organization of archaeal genes on the genome preventing collision of replication machinery with transcription machinery [18] and physical connections recently suggested between replication and transcription machineries [31].
In conclusion, this study by Hawkins
3. Archaeal Hef/XPF proteins from the XPF/MUS81/FANCM family
Proteins belonging to the XPF/MUS81/FANCM endonuclease family act on 3’-flap DNA structures that are formed during DNA repair or replication restart. They are found throughout eukarya and archaea but to date have not been identified in bacteria. Eukaryotes have several XPF/MUS81/FANCM family members that all share a conserved nuclease domain [34] whereas MUS81 proteins possess only an active nuclease domain. In XPF, an active nuclease domain is fused to a SF2-helicase domain that is degenerated and appears to be inactive [35]. By contrast, FANCM consists of a helicase:nuclease fusion in which the nuclease domain is degenerated [36, 37]. Other members can be found that have a degenerated nuclease and/or helicase domain. They assemble into heterodimeric complexes with MUS81, XPF or FANCM proteins to form distinct active complexes involved in DNA repair, meiotic recombination and replication restart [38] (Figure 3).
All archaea encode a protein of the XPF/MUS81/FANCM family of endonucleases. It exists in two forms. The long form, referred as Hef, consists of an N-terminal helicase fused to a C-terminal nuclease and is specific to the euryarchaea. The short form, referred as XPF, lacks the helicase domain and is specific to the crenarchaea and the thaumarchaea (Figure 3).
The long-formed Hef protein was first identified in
3.1. In vitro studies of crenarchaeal XPF proteins
The crystallographic structure of XPF from the crenarchaea
The nuclease activity of XPF from
3.2. In vitro characterization of euryarchaeal Hef proteins
As mentioned previously Hef was identified in
More recently,
These biochemical studies have indicated that both creanarchaeal XPF and euryarchaeal Hef proteins interact with PCNA and display biochemical activities consistent for being proteins involved in DNA repair and/or replication restart. Is this hypothesis supported by
3.3. What have we learned deleting hef gene in euryarchaea
The
In contrast, the deletion of
UV irradiation | Up to 150 J/m2 | on plate | - | 2 or 5 J/m2 | on plate | + |
MMS | 0,04% | 1 hour in suspension | - | 0,05% | 4 hours in suspension | ++ |
γ-rays | Up to 1000 Gy | on plate | - | 1700 Gy | in suspension | ++ |
Phleomycin | 1 or 2 mg/ml | 1 hour in suspension | - | |||
Mitomycin C | 0,02 µg/ml | On plate | slow-growing | 100 µg/ml | 4 hours in suspension | +++ |
A possible explanation for these phenotypic differences is that NER proteins in
To further investigate the role of Hef in
4. Dynamic localization of Hef proteins fused to the Green Fluorescent Protein (GFP) in living H. volcanii cells
The Green Fluorescent Protein (GFP) was originally isolated from the jellyfish
4.1. Fusion of the green fluorescent protein to the C-terminal end of Hef protein in H. volcanii
GFP has been used to investigate proteasome-dependant proteolysis and protein levels in
Whether GFP-fused Hef proteins remained functional was then tested by comparing cells deleted for
4.2. Localising the fluorescence signal in H. volcanii living cells
We then observed the localisation of Hef::GFP proteins by fluorescence microscopy, comparing cells exposed to APD to non-treated control samples. Towards this goal, a drop of cells was spotted on an agarose slice placed on a glass slide. After allowing this drop to dry, the agarose pad was covered with a cover-slip for cell imaging studies using a wield-field microscope to visualize a large number of individual cells. Differential Interference Contrast (DIC) [also known as Nomarski Interference Contrast (NIC)], was first used to visualized the cells as it enhances the contrast in unstained, transparent samples. Then fluorescence imaging was performed (exciting at 474 nm and collecting at 527-554 nm). Note however that due to the small cell size (around 1 to 2 µm) and the use of the soft agarose, not all cells were in the same focal plane. In order not to lose any information, fluorescence images were acquired at different focal planes on the z-axis. Consecutive slices of cells in focus were then selected and used to perform a maximum intensity z-projection. At each pixel, the highest fluorescence signal was kept when comparing the selected images. This maximum intensity z-projection resulted into a two-dimensional picture where the maximal fluorescence signals from different focal planes were recorded (Figure 4).
Resulting images contained hundreds of cells that were analysed by quantitative image analyses using IMARIS software. Different imaging parameters were optimized to detect cells and fluorescence foci within cells using automatic thresholds to avoid user-bias. This approch allowed thousands of cells to be analysed in each condition tested, providing extremely high statistical power.
4.3. Hef::GFP molecules are recruited at arrested replication forks
Using such approach, we have shown that Hef::GFP proteins formed fluorescence foci even under normal growth condition, in the absence of any DNA damaging agents. The number of these foci was significantly increased from two to four foci
We have also observed that cell size was increased from 28 to 45 µm² in response to replication arrest (i.e. APD exposure). We have shown using other DNA damaging agents that increased cell size and number of foci were specific to APD treatment, suggesting that indeed
4.4. Diffusing pattern of Hef::GFP molecule upon replication arrests
To investigate the diffusion of Hef::GFP molecules inside and outside fluorescence foci, we performed Fluorescence Recovery After Photobleaching (FRAP) and Number and Brightness (N&B) experiments. These experiments were performed using a confocal microscope on cells immobilized on a poly-D-lysine coated cover-slip.
In FRAP experiments a region of interest was photobleached in a cell. The speed of fluorescence recovery in that region was then measured, reflecting the diffusion of Hef::GFP fluorescent molecules arriving from the non-photobleached region of the cell. In control cells (no aphidicolin), one major population of Hef::GFP diffusing molecules was observed. From the fit of the recovery curve we obtained the recovery constant, allowing then the apparent two-dimensional diffusion rate of Hef::GFP to be estimated at 0.8 to 2.3 µm² per second. This appeared markedly lower than expected for Hef dimer, as revealed by analytical ultracentrifugation experiments on purified
Such changes in the diffusion pattern of Hef::GFP molecules upon replication arrests were also observed using N&B technique that measures fluctuation of fluorescence intensity in each analysed pixel [81]. These analyses were performed on one hundred images taken every 2 seconds, and cell regions including and excluding fluorescence foci were compared. Fluctuation of fluorescence intensity per pixel was then used to determine the number of diffusing molecules and their brightness. This information can then be used to deduce changes in the oligomeric state of the fluorescent molecules. When N&B technique was applied to diffusing Hef::GFP molecules, changes in the oligomeric state (i.e. higher brightness) were observed upon APD treatment. This observation revealed oligomerization and/or co-localisation of several Hef::GFP molecules induced by APD exposure (Figure 7), and provided a feasible explanation for the slow diffusion in APD treated cells revealed by FRAP experiments.
Overall, the results obtained from FRAP and N&B experiments were consistent with the notion that Hef::GFP molecules are actively recruited at arrested replication forks. Whether the slow-diffusion pattern of Hef::GFP molecules reflects their recruitment directly on DNA and/or as part of protein complexes at arrested replication forks are questions that remain to be addressed. Interestingly,
Moreover, our work has also shown that replication forks arrest spontaneously occured in
5. Concluding remarks
In conclusion, as archaea possess hallmarks of both bacterial and eukaryotic replication systems we believe that continuation of studies underlined will shed light on the evolutionary history of replication restart mechanisms and its complex machinery that we are just starting to unravel in eukaryotes and now archaea.
Acknowledgments
We thank A. Lestini for figures 1, 2, 3 and 4. Figures 5, 6, 7 and 8 were reproduced with permission from Lestini
References
- 1.
O'Donnell M, Langston L, Stillman B. Principles and concepts of DNA replication in bacteria, archaea, and eukarya. Cold Spring Harb Perspect Biol2013 Jul;5(7). - 2.
Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A1990 Jun;87(12):4576-9. - 3.
Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol2008 Mar;6(3):245-52. - 4.
Myllykallio H, Lopez P, Lopez-Garcia P, Heilig R, Saurin W, Zivanovic Y, et al. Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science2000 Jun 23;288(5474):2212-5. - 5.
Hawkins M, Malla S, Blythe MJ, Nieduszynski CA, Allers T. Accelerated growth in the absence of DNA replication origins. Nature2013 Nov 28;503(7477):544-7. - 6.
Norais C, Hawkins M, Hartman AL, Eisen JA, Myllykallio H, Allers T. Genetic and physical mapping of DNA replication origins in Haloferax volcanii. PLoS Genet2007 May 18;3(5):e77. - 7.
Pelve EA, Martens-Habbena W, Stahl DA, Bernander R. Mapping of active replication origins in vivo in thaum- and euryarchaeal replicons. Mol Microbiol2013 Nov;90(3):538-50. - 8.
Maisnier-Patin S, Malandrin L, Birkeland NK, Bernander R. Chromosome replication patterns in the hyperthermophilic euryarchaea Archaeoglobus fulgidus and Methanocaldococcus (Methanococcus) jannaschii. Mol Microbiol2002 Sep;45(5):1443-50. - 9.
Berquist BR, DasSarma S. An archaeal chromosomal autonomously replicating sequence element from an extreme halophile, Halobacterium sp. strain NRC-1. J Bacteriol2003 Oct;185(20):5959-66. - 10.
Coker JA, DasSarma P, Capes M, Wallace T, McGarrity K, Gessler R, et al. Multiple replication origins of Halobacterium sp. strain NRC-1: properties of the conserved orc7-dependent oriC1. J Bacteriol2009 Aug;191(16):5253-61. - 11.
Wu Z, Liu H, Liu J, Liu X, Xiang H. Diversity and evolution of multiple orc/cdc6-adjacent replication origins in haloarchaea. BMC Genomics2012;13:478. - 12.
Majernik AI, Chong JP. A conserved mechanism for replication origin recognition and binding in archaea. Biochem J2008 Jan 15;409(2):511-8. - 13.
Lundgren M, Andersson A, Chen L, Nilsson P, Bernander R. Three replication origins in Sulfolobus species: synchronous initiation of chromosome replication and asynchronous termination. Proc Natl Acad Sci U S A2004 May 4;101(18):7046-51. - 14.
Samson RY, Xu Y, Gadelha C, Stone TA, Faqiri JN, Li D, et al. Specificity and function of archaeal DNA replication initiator proteins. Cell Rep2013 Feb 21;3(2):485-96. - 15.
Pelve EA, Lindas AC, Knoppel A, Mira A, Bernander R. Four chromosome replication origins in the archaeon Pyrobaculum calidifontis. Mol Microbiol2012 Sep;85(5):986-95. - 16.
Robinson NP, Bell SD. Extrachromosomal element capture and the evolution of multiple replication origins in archaeal chromosomes. Proc Natl Acad Sci U S A2007 Apr 3;104(14):5806-11. - 17.
Luo H, Zhang C-T, Gao F. Ori-Finder 2, an integrated tool to predict replication origins in the archaeal genomes. Frontiers in Microbiology. (Methods). 2014-September-15;5. - 18.
Andersson AF, Pelve EA, Lindeberg S, Lundgren M, Nilsson P, Bernander R. Replication-biased genome organisation in the crenarchaeon Sulfolobus. BMC Genomics2010;11:454. - 19.
Matsunaga F, Forterre P, Ishino Y, Myllykallio H. In vivo interactions of archaeal Cdc6/Orc1 and minichromosome maintenance proteins with the replication origin. Proc Natl Acad Sci U S A2001 Sep 25;98(20):11152-7. - 20.
Miller JM, Arachea BT, Epling LB, Enemark EJ. Analysis of the crystal structure of an active MCM hexamer. elife2014;3. - 21.
Capaldi SA, Berger JM. Biochemical characterization of Cdc6/Orc1 binding to the replication origin of the euryarchaeon Methanothermobacter thermoautotrophicus. Nucleic Acids Res2004;32(16):4821-32. - 22.
Robinson NP, Dionne I, Lundgren M, Marsh VL, Bernander R, Bell SD. Identification of two origins of replication in the single chromosome of the archaeon Sulfolobus solfataricus. Cell2004 Jan 9;116(1):25-38. - 23.
Wu Z, Liu J, Yang H, Liu H, Xiang H. Multiple replication origins with diverse control mechanisms in Haloarcula hispanica. Nucleic Acids Res2014 Feb;42(4):2282-94. - 24.
Woods WG, Dyall-Smith ML. Construction and analysis of a recombination-deficient (radA) mutant of Haloferax volcanii. Mol Microbiol1997 Feb;23(4):791-7. - 25.
Kolodner RD, Putnam CD, Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science2002 Jul 26;297(5581):552-7. - 26.
Abbas T, Keaton MA, Dutta A. Genomic instability in cancer. Cold Spring Harb Perspect Biol2013 Mar;5(3):a012914. - 27.
Jackson AP, Laskey RA, Coleman N. Replication proteins and human disease. Cold Spring Harb Perspect Biol2014 Jan;6(1). - 28.
Breuert S, Allers T, Spohn G, Soppa J. Regulated polyploidy in halophilic archaea. PLoS One2006;1:e92. - 29.
Cvetic C, Walter JC. Eukaryotic origins of DNA replication: could you please be more specific? Semin Cell Dev Biol2005 Jun;16(3):343-53. - 30.
Michel B, Bernander R. Chromosome replication origins: do we really need them? Bioessays2014 Jun;36(6):585-90. - 31.
Pluchon PF, Fouqueau T, Creze C, Laurent S, Briffotaux J, Hogrel G, et al. An Extended Network of Genomic Maintenance in the Archaeon Pyrococcus abyssi Highlights Unexpected Associations between Eucaryotic Homologs. PLoS One2013;8(11):e79707. - 32.
Lestini R, Duan Z, Allers T. The archaeal Xpf/Mus81/FANCM homolog Hef and the Holliday junction resolvase Hjc define alternative pathways that are essential for cell viability in Haloferax volcanii. DNA Repair (Amst)2010 Sep 4;9(9):994-1002. - 33.
Lestini R, Laptenok SP, Kuhn J, Hink MA, Schanne-Klein MC, Liebl U, et al. Intracellular dynamics of archaeal FANCM homologue Hef in response to halted DNA replication. Nucleic Acids Res2013 Dec 1;41(22):10358-70. - 34.
Enzlin JH, Scharer OD. The active site of the DNA repair endonuclease XPF-ERCC1 forms a highly conserved nuclease motif. EMBO J2002 Apr 15;21(8):2045-53. - 35.
Sgouros J, Gaillard PH, Wood RD. A relationship betweena DNA-repair/recombination nuclease family and archaeal helicases. Trends Biochem Sci1999 Mar;24(3):95-7. - 36.
Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell2007 Feb 9;25(3):331-43. - 37.
Meetei AR, Medhurst AL, Ling C, Xue Y, Singh TR, Bier P, et al. A human ortholog of archaeal DNA repair protein Hef is defective in Fanconi anemia complementation group M. Nat Genet2005 Sep;37(9):958-63. - 38.
Ciccia A, McDonald N, West SC. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem2008;77:259-87. - 39.
Komori K, Fujikane R, Shinagawa H, Ishino Y. Novel endonuclease in Archaea cleaving DNA with various branched structure. Genes Genet Syst2002 Aug;77(4):227-41. - 40.
Mosedale G, Niedzwiedz W, Alpi A, Perrina F, Pereira-Leal JB, Johnson M, et al. The vertebrate Hef ortholog is a component of the Fanconi anemia tumor-suppressor pathway. Nat Struct Mol Biol2005 Sep;12(9):763-71. - 41.
Lally J, Newman M, Murray-Rust J, Fadden A, Kawarabayasi Y, McDonald N. Crystallization of the xeroderma pigmentosum group F endonuclease from Aeropyrum pernix. Acta Crystallogr D Biol Crystallogr2004 Sep;60(Pt 9):1658-61. - 42.
Newman M, Murray-Rust J, Lally J, Rudolf J, Fadden A, Knowles PP, et al. Structure of an XPF endonuclease with and without DNA suggests a model for substrate recognition. EMBO J2005 Mar 9;24(5):895-905. - 43.
Roberts JA, Bell SD, White MF. An archaeal XPF repair endonuclease dependent on a heterotrimeric PCNA. Mol Microbiol2003 Apr;48(2):361-71. - 44.
Meslet-Cladiere L, Norais C, Kuhn J, Briffotaux J, Sloostra JW, Ferrari E, et al. A novel proteomic approach identifies new interaction partners for proliferating cell nuclear antigen. J Mol Biol2007 Oct 5;372(5):1137-48. - 45.
Hutton RD, Craggs TD, White MF, Penedo JC. PCNA and XPF cooperate to distort DNA substrates. Nucleic Acids Res2010 Mar;38(5):1664-75. - 46.
Hutton RD, Roberts JA, Penedo JC, White MF. PCNA stimulates catalysis by structure-specific nucleases using two distinct mechanisms: substrate targeting and catalytic step. Nucleic Acids Res2008 Dec;36(21):6720-7. - 47.
Roberts JA, White MF. DNA end-directed and processive nuclease activities of the archaeal XPF enzyme. Nucleic Acids Res2005;33(20):6662-70. - 48.
Roberts JA, White MF. An archaeal endonuclease displays key properties of both eukaryal XPF-ERCC1 and Mus81. J Biol Chem2005 Feb 18;280(7):5924-8. - 49.
Nishino T, Komori K, Ishino Y, Morikawa K. X-ray and biochemical anatomy of an archaeal XPF/Rad1/Mus81 family nuclease: similarity between its endonuclease domain and restriction enzymes. Structure2003 Apr;11(4):445-57. - 50.
Nishino T, Komori K, Ishino Y, Morikawa K. Structural and functional analyses of an archaeal XPF/Rad1/Mus81 nuclease: asymmetric DNA binding and cleavage mechanisms. Structure2005 Aug;13(8):1183-92. - 51.
Nishino T, Komori K, Tsuchiya D, Ishino Y, Morikawa K. Crystal structure and functional implications of Pyrococcus furiosus hef helicase domain involved in branched DNA processing. Structure2005 Jan;13(1):143-53. - 52.
Komori K, Hidaka M, Horiuchi T, Fujikane R, Shinagawa H, Ishino Y. Cooperation of the N-terminal Helicase and C-terminal endonuclease activities of Archaeal Hef protein in processing stalled replication forks. J Biol Chem2004 Dec 17;279(51):53175-85. - 53.
Doe CL, Osman F, Dixon J, Whitby MC. DNA repair by a Rad22-Mus81-dependent pathway that is independent of Rhp51. Nucleic Acids Res2004;32(18):5570-81. - 54.
Froget B, Blaisonneau J, Lambert S, Baldacci G. Cleavage of stalled forks by fission yeast Mus81/Eme1 in absence of DNA replication checkpoint. Mol Biol Cell2008 Feb;19(2):445-56. - 55.
Kai M, Boddy MN, Russell P, Wang TS. Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stress. Genes Dev2005 Apr 15;19(8):919-32. - 56.
Matulova P, Marini V, Burgess RC, Sisakova A, Kwon Y, Rothstein R, et al. Cooperativity of Mus81.Mms4 with Rad54 in the resolution of recombination and replication intermediates. J Biol Chem2009 Mar 20;284(12):7733-45. - 57.
Roseaulin L, Yamada Y, Tsutsui Y, Russell P, Iwasaki H, Arcangioli B. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J2008 May 7;27(9):1378-87. - 58.
Kaliraman V, Mullen JR, Fricke WM, Bastin-Shanower SA, Brill SJ. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev2001 Oct 15;15(20):2730-40. - 59.
Chen XB, Melchionna R, Denis CM, Gaillard PH, Blasina A, Van de Weyer I, et al. Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol Cell2001 Nov;8(5):1117-27. - 60.
Ciccia A, Constantinou A, West SC. Identification and characterization of the human mus81-eme1 endonuclease. J Biol Chem2003 Jul 4;278(27):25172-8. - 61.
Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, Pichierri P. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. J Cell Biol2008 Oct 20;183(2):241-52. - 62.
Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol2007 Nov;14(11):1096-104. - 63.
Shimura T, Torres MJ, Martin MM, Rao VA, Pommier Y, Katsura M, et al. Bloom's syndrome helicase and Mus81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J Mol Biol2008 Jan 25;375(4):1152-64. - 64.
Ishino S, Yamagami T, Kitamura M, Kodera N, Mori T, Sugiyama S, et al. Multiple interactions of the intrinsically disordered region between the helicase and nuclease domains of the archaeal Hef protein. J Biol Chem2014 Aug 1;289(31):21627-39. - 65.
Fujikane R, Ishino S, Ishino Y, Forterre P. Genetic analysis of DNA repair in the hyperthermophilic archaeon, Thermococcus kodakaraensis. Genes Genet Syst2010;85(4):243-57. - 66.
Rouillon C, White MF. The evolution and mechanisms of nucleotide excision repair proteins. Res Microbiol2011 Jan;162(1):19-26. - 67.
Bardwell AJ, Bardwell L, Tomkinson AE, Friedberg EC. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science1994 Sep 30;265(5181):2082-5. - 68.
Sijbers AM, de Laat WL, Ariza RR, Biggerstaff M, Wei YF, Moggs JG, et al. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell1996 Sep 6;86(5):811-22. - 69.
Duan Z. Genetic Analysis of Two Structure-specific Endonucleases Hef and Fen1 in Archaeon Haloferax volcanii (PhD thesis): University of Nottingham; 2008. - 70.
Shimomura O, Johnson FH, Saiga Y. Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol1962 Jun;59:223-39. - 71.
Ormo M, Cubitt AB, Kallio K, Gross LA, Tsien RY, Remington SJ. Crystal structure of the Aequorea victoria green fluorescent protein. Science1996 Sep 6;273(5280):1392-5. - 72.
Tsien RY. The green fluorescent protein. Annu Rev Biochem1998;67:509-44. - 73.
Chudakov DM, Matz MV, Lukyanov S, Lukyanov KA. Fluorescent proteins and their applications in imaging living cells and tissues. Physiol Rev2010 Jul;90(3):1103-63. - 74.
Vermeulen W. Dynamics of mammalian NER proteins. DNA Repair (Amst)2011 Jul 15;10(7):760-71. - 75.
Reuter CJ, Maupin-Furlow JA. Analysis of proteasome-dependent proteolysis in Haloferax volcanii cells, using short-lived green fluorescent proteins. Appl Environ Microbiol2004 Dec;70(12):7530-8. - 76.
Reuter CJ, Uthandi S, Puentes JA, Maupin-Furlow JA. Hydrophobic carboxy-terminal residues dramatically reduce protein levels in the haloarchaeon Haloferax volcanii. Microbiology2010 Jan;156(Pt 1):248-55. - 77.
Henche AL, Koerdt A, Ghosh A, Albers SV. Influence of cell surface structures on crenarchaeal biofilm formation using a thermostable green fluorescent protein. Environ Microbiol2012 Mar;14(3):779-93. - 78.
Cubitt AB, Woollenweber LA, Heim R. Understanding structure-function relationships in the Aequorea victoria green fluorescent protein. Methods Cell Biol1999;58:19-30. - 79.
Patterson GH, Knobel SM, Sharif WD, Kain SR, Piston DW. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy. Biophys J1997 Nov;73(5):2782-90. - 80.
Forterre P, Elie C, Kohiyama M. Aphidicolin inhibits growth and DNA synthesis in halophilic arachaebacteria. J Bacteriol1984 Aug;159(2):800-2. - 81.
Digman MA, Dalal R, Horwitz AF, Gratton E. Mapping the number of molecules and brightness in the laser scanning microscope. Biophys J2008 Mar 15;94(6):2320-32. - 82.
Bakker ST, van de Vrugt HJ, Rooimans MA, Oostra AB, Steltenpool J, Delzenne-Goette E, et al. Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M. Hum Mol Genet2009 Sep 15;18(18):3484-95. - 83.
Crismani W, Girard C, Froger N, Pradillo M, Santos JL, Chelysheva L, et al. FANCM limits meiotic crossovers. Science2012 Jun 22;336(6088):1588-90. - 84.
Knoll A, Higgins JD, Seeliger K, Reha SJ, Dangel NJ, Bauknecht M, et al. The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell2012 Apr;24(4):1448-64. - 85.
Lorenz A, Osman F, Sun W, Nandi S, Steinacher R, Whitby MC. The fission yeast FANCM ortholog directs non-crossover recombination during meiosis. Science2012 Jun 22;336(6088):1585-8. - 86.
Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer BH, Reimann J, et al. Versatile Genetic Tool Box for the Crenarchaeote Sulfolobus acidocaldarius. Front Microbiol2012;3:214. - 87.
Zhang C, Tian B, Li S, Ao X, Dalgaard K, Gokce S, et al. Genetic manipulation in Sulfolobus islandicus and functional analysis of DNA repair genes. Biochem Soc Trans2013 Feb 1;41(1):405-10.