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Biochemistry & Molecular Biology

Replication protein A complex in Thermococcus kodakarensis interacts with DNA polymerases and helps their effective strand synthesis

, ORCID Icon, & ORCID Icon
Pages 695-704 | Received 21 Oct 2018, Accepted 07 Dec 2018, Published online: 22 Dec 2018

References

  • Ashton NW, Bolderson E, Cubeddu L, et al. Human single-stranded DNA binding proteins are essential for maintaining genomic stability. BMC Mol Biol. 2013;14:9.
  • Dickey TH, Altschuler SE, Wuttke DS. Single-stranded DNA-binding proteins: multiple domains for multiple functions. Structure. 2013;21:1074–1084.
  • Raghunathan S, Ricard CS, Lohman TM, et al. Crystal structure of the homo-tetrameric DNA binding domain of Escherichia coli single-stranded DNA-binding protein determined by multiwavelength x-ray diffraction on the selenomethionyl protein at 2.9Å resolution. Proc Natl Acad Sci USA. 1997;94:6652–6657.
  • Bochkarev A, Pfuetzner RA, Edwards AM, et al. Structure of the single-stranded-DNA-binding domain of replication protein A bound to DNA. Nature. 1997;385:176–181.
  • Bochkarev A, Bochkareva E, Frappier L, et al. The crystal structure of the complex of replication protein A subunits RPA32 and RPA14 reveals a mechanism for single-stranded DNA binding. Embo J. 1999;18:4498–4504.
  • Murzin AG. OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. Embo J. 1993;12:861–867.
  • Sancar A, Williams KR, Chase JW, et al. Sequences of the ssb gene and protein. Proc Natl Acad Sci USA. 1981;78:4274–4278.
  • Dabrowski S, Olszewski M, Piatek R, et al. Identification and characterization of single-stranded-DNA-binding proteins from Thermus thermophilus and Thermus aquaticus - new arrangement of binding domains. Microbiology. 2002;148:3307–3315.
  • Bochkareva E, Korolev S, Lees-Miller SP, et al. Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. Embo J. 2002;21:1855–1863.
  • Braun KA, Lao Y, He Z, et al. Role of protein-protein interactions in the function of replication protein A (RPA): RPA modulates the activity of DNA polymerase alpha by multiple mechanisms. Biochemistry. 1997;36:8443–8454.
  • Lin YL, Chen C, Keshav KF, et al. Dissection of functional domains of the human DNA replication protein complex replication protein A. J Biol Chem. 1996;271:17190–17198.
  • Bochkareva E, Frappier L, Edwards AM, et al. The RPA32 subunit of human replication protein A contains a single-stranded DNA-binding domain. J Biol Chem. 1998;273:3932–3936.
  • Philipova D, Mullen JR, Maniar HS, et al. A hierarchy of SSB protomers in replication protein A. Genes Dev. 1996;10:2222–2233.
  • Gomes XV, Wold MS. Structural analysis of human replication protein A. Mapping functional domains of the 70-kDa subunit. J Biol Chem. 1995;270:4534–4543.
  • Mer G, Bochkarev A, Gupta R, et al. Structural basis for the recognition of DNA repair proteins UNG2, XPA, and RAD52 by replication factor RPA. Cell. 2000;103:449–456.
  • Chedin F, Seitz EM, Kowalczykowski SC. Novel homologs of replication protein A in archaea: implications for the evolution of ssDNA-binding proteins. Trends Biochem Sci. 1998;23:273–277.
  • Kelly TJ, Simancek P, Brush GS. Identification and characterization of a single-stranded DNA-binding protein from the archaeon Methanococcus jannaschii. Proc Natl Acad Sci USA. 1998;95:14634–14639.
  • Kelman Z, Pietrokovski S, Hurwitz J. Isolation and characterization of a split B-type DNA polymerase from the archaeon Methanobacterium thermoautotrophicum DeltaH. J Biol Chem. 1999;274:28751–28761.
  • Kerr ID, Wadsworth RI, Cubeddu L, et al. Insights into ssDNA recognition by the OB fold from a structural and thermodynamic study of Sulfolobus SSB protein. Embo J. 2003;22:2561–2570.
  • Komori K, Ishino Y. Replication protein A in Pyrococcus furiosus is involved in homologous DNA recombination. J Biol Chem. 2001;276:25654–25660.
  • Robbins JB, Murphy MC, White BA, et al. Functional analysis of multiple single-stranded DNA-binding proteins from Methanosarcina acetivorans and their effects on DNA synthesis by DNA polymerase BI. J Biol Chem. 2004;279:6315–6326.
  • Raymann K, Forterre P, Brochier-Armanet C, et al. Global phylogenomic analysis disentangles the complex evolutionary history of DNA replication in archaea. Genome Biol Evol. 2014;6:192–212.
  • Ishino Y, Ishino S. Rapid progress of DNA replication studies in Archaea, the third domain of life. Sci China Life Sci. 2012;55:386–403.
  • Lujan SA, Williams JS, Kunkel TA. DNA polymerases divide the labor of genome replication. Trends Cell Biol. 2016;26:640–654.
  • Ishino S, Ishino Y. DNA polymerases as useful reagents for biotechnology - the history of developmental research in the field. Front Microbiol. 2014;5:465.
  • Uemori T, Sato Y, Kato I, et al. A novel DNA polymerase in the hyperthermophilic archaeon, Pyrococcus furiosus: gene cloning, expression, and characterization. Genes Cells. 1997;2:499–512.
  • Cann IKO, Komori K, Toh H, et al. A heterodimeric DNA polymerase: evidence that members of Euryarchaeota possess a distinct DNA polymerase. Proc Natl Acad Sci U S A. 1998;95:14250–14255.
  • Makarova KS, Krupovic M, Koonin EV. Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery. Front Microbiol. 2014;5:354.
  • Matsunaga F, Norais C, Forterre P, et al. Identification of short ‘eukaryotic’ Okazaki fragments synthesized from a prokaryotic replication origin. EMBO Rep. 2003;4:154–158.
  • Greenough L, Kelman Z, Gardner AF. The roles of family B and D DNA polymerases in Thermococcus species 9°N Okazaki fragment maturation. J Biol Chem. 2015;290:12514–12522.
  • Li Z, Santangelo TJ, Cubonova L, et al. Affinity purification of an archaeal DNA replication protein network. MBio. 2010;1.
  • Henneke G, Flament D, Hubscher U, et al. The hyperthermophilic euryarchaeota Pyrococcus abyssi likely requires the two DNA polymerases D and B for DNA replication. J Mol Biol. 2005;350:53–64.
  • Berquist BR, DasSarma P, DasSarma S. Essential and non-essential DNA replication genes in the model halophilic Archaeon, Halobacterium sp. NRC-1. BMC Genet. 2007;8:31.
  • Cubonova L, Richardson T, Burkhart BW, et al. Archaeal DNA polymerase D but not DNA polymerase B is required for genome replication in Thermococcus kodakarensis. J Bacteriol. 2013;195:2322–2328.
  • Ishino S, Ishino Y. Comprehensive search for DNA polymerase in the hyperthermophilic archaeon, Pyrococcus furiosus. Nucleosides Nucleotides Nucleic Acids. 2006;25:681–691.
  • Rouillon C, Henneke G, Flament D, et al. DNA polymerase switching on homotrimeric PCNA at the replication fork of the euryarchaea Pyrococcus abyssi. J Mol Biol. 2007;369:343–355.
  • Henneke G. In vitro reconstitution of RNA primer removal in Archaea reveals the existence of two pathways. Biochem J. 2012;447:271–280.
  • Kuba Y, Ishino S, Yamagami T, et al. Comparative analyses of the two proliferating cell nuclear antigens from the hyperthermophilic archaeon, Thermococcus kodakarensis. Genes Cells. 2012;17:923–937.
  • Nagata M, Ishino S, Yamagami T, et al. The Cdc45/RecJ-like protein forms a complex with GINS and MCM, and is important for DNA replication in Thermococcus kodakarensis. Nucleic Acids Res. 2017;45:10693–10705.
  • Oyama T, Ishino S, Shirai T, et al. Atomic structure of an archaeal GAN suggests its dual roles as an exonuclease in DNA repair and a CMG component in DNA replication. Nucleic Acids Res. 2016;44:9505–9517.
  • Komori K, Miyata T, DiRuggiero J, et al. Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J Biol Chem. 2000;275:33782–33790.
  • Wilkins MR, Gasteiger E, Bairoch A, et al. Protein identification and analysis tools in the ExPASy server. Methods Mol Biol. 1999;112:531–552.
  • Nagata M, Ishino S, Yamagami T, et al. Possible function of the second RecJ-like protein in stalled replication fork repair by interacting with Hef. Sci Rep. 2017;7:16949.
  • Larkin MA, Blackshields G, Brown NP, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–2948.
  • Radivojac P, Iakoucheva LM, Oldfield CJ, et al. Intrinsic disorder and functional proteomics. Biophys J. 2007;92:1439–1456.
  • Linding R, Jensen LJ, Diella F, et al. Protein disorder prediction: implications for structural proteomics. Structure. 2003;11:1453–1459.
  • Brosey CA, Yan C, Tsutakawa SE, et al. A new structural framework for integrating replication protein A into DNA processing machinery. Nucleic Acids Res. 2013;41:2313–2327.
  • Bochkareva E, Belegu V, Korolev S, et al. Structure of the major single-stranded DNA-binding domain of replication protein A suggests a dynamic mechanism for DNA binding. Embo J. 2001;20:612–618.
  • Morin JA, Cerron F, Jarillo J, et al. DNA synthesis determines the binding mode of the human mitochondrial single-stranded DNA-binding protein. Nucleic Acids Res. 2017;45:7237–7248.
  • Wadsworth RI, White MF. Identification and properties of the crenarchaeal single-stranded DNA binding protein from Sulfolobus solfataricus. Nucleic Acids Res. 2001;29:914–920.
  • Dornreiter I, Erdile LF, Gilbert IU, et al. Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. Embo J. 1992;11:769–776.
  • Molineux IJ, Gefter ML. Properties of the Escherichia coli in DNA binding (unwinding) protein: interaction with DNA polymerase and DNA. Proc Natl Acad Sci USA. 1974;71:3858–3862.
  • Alberts BM, Barry J, Bedinger P, et al. Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):655–668.
  • Kelman Z, Lee JK, Hurwitz J. The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc Natl Acad Sci USA. 1999;96:14783–14788.
  • Pluchon PF, Fouqueau T, Creze C, et al. An extended network of genomic maintenance in the archaeon Pyrococcus abyssi highlights unexpected associations between eucaryotic homologs. PLoS One. 2013;8:e79707.
  • Szambowska A, Tessmer I, Prus P, et al. Cdc45-induced loading of human RPA onto single-stranded DNA. Nucleic Acids Res. 2017;45:3217–3230.
  • Han ES, Cooper DL, Persky NS, et al. RecJ exonuclease: substrates, products and interaction with SSB. Nucleic Acids Res. 2006;34:1084–1091.
  • Jiao J, Wang L, Xia W, et al. Function and biochemical characterization of RecJ in Deinococcus radiodurans. DNA Repair (Amst). 2012;11:349–356.
  • Sharma R, Rao DN. Orchestration of Haemophilus influenzae RecJ exonuclease by interaction with single-stranded DNA-binding protein. J Mol Biol. 2009;385:1375–1396.
  • Sanchez-Pulido L, Ponting CP. Cdc45: the missing RecJ ortholog in eukaryotes? Bioinformatics. 2011;27:1885–1888.
  • Makarova KS, Koonin EV, Kelman Z. The CMG (CDC45/RecJ, MCM, GINS) complex is a conserved component of the DNA replication system in all archaea and eukaryotes. Biol Direct. 2012;7:7.
  • Persky NS, Lovett ST. Mechanisms of recombination: lessons from E. coli. Crit Rev Biochem Mol Biol. 2008;43:347–370.
  • Dianov G, Lindahl T. Reconstitution of the DNA base excision-repair pathway. Curr Biol. 1994;4:1069–1076.
  • Burdett V, Baitinger C, Viswanathan M, et al. In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair. Proc Natl Acad Sci USA. 2001;98:6765–6770.
  • Lin YL, Shivji MK, Chen C, et al. The evolutionarily conserved zinc finger motif in the largest subunit of human replication protein a is required for DNA replication and mismatch repair but not for nucleotide excision repair. J Biol Chem. 1998;273:1453–1461.
  • Fujisawa R, Ohashi E, Hirota K, et al. Human CTF18-RFC clamp-loader complexed with non-synthesising DNA polymerase epsilon efficiently loads the PCNA sliding clamp. Nucleic Acids Res. 2017;45:4550–4563.
  • Salas TR, Petruseva I, Lavrik O, et al. Human replication protein A unfolds telomeric G-quadruplexes. Nucleic Acids Res. 2006;34:4857–4865.
  • Safa L, Gueddouda NM, Thiebaut F, et al. 5ʹ to 3ʹ unfolding directionality of DNA secondary structures by replication protein A: G-quadruplexes and duplexes. J Biol Chem. 2016;291:21246–21256.
  • Lancrey A, Safa L, Chatain J, et al. The binding efficiency of RPA to telomeric G-strands folded into contiguous G-quadruplexes is independent of the number of G4 units. Biochimie. 2017;146:68–72.
  • Safa L, Delagoutte E, Petruseva I, et al. Binding polarity of RPA to telomeric sequences and influence of G-quadruplex stability. Biochimie. 2014;103:80–88.
  • Audry J, Maestroni L, Delagoutte E, et al. RPA prevents G-rich structure formation at lagging-strand telomeres to allow maintenance of chromosome ends. Embo J. 2015;34:1942–1958.
  • Lavrik OI, Kolpashchikov DM, Weisshart K, et al. RPA subunit arrangement near the 3ʹ-end of the primer is modulated by the length of the template strand and cooperative protein interactions. Nucleic Acids Res. 1999;27:4235–4240.
  • Taylor MRG, Yeeles JTP. The initial response of a eukaryotic replisome to DNA damage. Mol Cell. 2018;70:1067–1080 e12.
  • Guilliam TA, Brissett NC, Ehlinger A, et al. Molecular basis for PrimPol recruitment to replication forks by RPA. Nat Commun. 2017;8:15222.
  • Martinez-Jimenez MI, Lahera A, Blanco L. Human PrimPol activity is enhanced by RPA. Sci Rep. 2017;7:783.
  • Garcia-Gomez S, Reyes A, Martinez-Jimenez MI, et al. PrimPol, an archaic primase/polymerase operating in human cells. Mol Cell. 2013;52:541–553.
  • Motz M, Kober I, Girardot C, et al. Elucidation of an archaeal replication protein network to generate enhanced PCR enzymes. J Biol Chem. 2002;277:16179–16188.
  • Heider MR, Burkhart BW, Santangelo TJ, et al. Defining the RNaseH2 enzyme-initiated ribonucleotide excision repair pathway in Archaea. J Biol Chem. 2017;292:8835–8845.
  • Bianco PR, Pottinger S, Tan HY, et al. The IDL of E. coli SSB links ssDNA and protein binding by mediating protein-protein interactions. Protein Sci. 2017;26:227–241.
  • Shereda RD, Kozlov AG, Lohman TM, et al. SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol. 2008;43:289–318.
  • Lohman TM, Ferrari ME. Escherichia coli single-stranded DNA-binding protein: multiple DNA-binding modes and cooperativities. Annu Rev Biochem. 1994;63:527–570.
  • Morten MJ, Gamsjaeger R, Cubeddu L, et al. High-affinity RNA binding by a hyperthermophilic single-stranded DNA-binding protein. Extremophiles. 2017;21:369–379.
  • Kozlov AG, Weiland E, Mittal A, et al. Intrinsically disordered C-terminal tails of E. coli single-stranded DNA binding protein regulate cooperative binding to single-stranded DNA. J Mol Biol. 2015;427:763–774.
  • Tan HY, Wilczek LA, Pottinger S, et al. The intrinsically disordered linker of E. coli SSB is critical for the release from single-stranded DNA. Protein Sci. 2017;26:700–717.
  • Qian Y, Johnson KA. The human mitochondrial single-stranded DNA-binding protein displays distinct kinetics and thermodynamics of DNA binding and exchange. J Biol Chem. 2017;292:13068–13084.

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