Plasmid replication initiator interactions with origin 13-mers and polymerase subunits contribute to strand-specific replisome assembly

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 31, 2015, Pages E4188-E4196

  Wawrzycka, Aleksandra ^a   Gross, Marta ^a   Wasaznik, Anna ^a   Konieczny, Igor ^a  

^a UNIVERSITY OF GDA SK   (Poland)

Author keywords

DNA replication initiation; Plasmid RK2; Polymerase III; Rep; clamp

Indexed keywords

BACTERIAL DNA; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; DNA HELICASE; DNA PRIMASE; REPLICATION INITIATOR PROTEIN DNAA; ADENOSINE TRIPHOSPHATASE; DNA DIRECTED DNA POLYMERASE; DNA SYNTHESOME; DNAB HELICASE; ESCHERICHIA COLI PROTEIN; MULTIENZYME COMPLEX; MUTANT PROTEIN; NUCLEOPROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT; TRFA PROTEIN, E COLI;

ARTICLE; CONTROLLED STUDY; DNA DENATURATION; ESCHERICHIA COLI; IN VITRO STUDY; MUTANT; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN INTERACTION; REPLICON; REPLISOME; WILD TYPE; CIRCULAR DICHROISM; DNA REPLICATION; DNA REPLICATION ORIGIN; DNA TEMPLATE; ENZYMOLOGY; METABOLISM; PROTEIN SUBUNIT;

ADENOSINE TRIPHOSPHATASES; CIRCULAR DICHROISM; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; DNAB HELICASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MULTIENZYME COMPLEXES; MUTANT PROTEINS; NUCLEOPROTEINS; PLASMIDS; PROTEIN BINDING; PROTEIN SUBUNITS; REPLICATION ORIGIN; TEMPLATES, GENETIC;

EID: 84964697028     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504926112     Document Type: Article

References (73)

1. Costa A, Hood IV, Berger JM (2013) Mechanisms for initiating cellular DNA replication. Annu Rev Biochem 82:25-54.
2. Kurth I, O'Donnell M (2013) New insights into replisome fluidity during chromosome replication. Trends Biochem Sci 38(4):195-203.
3. LeBowitz JH, McMacken R (1986) The Escherichia coli dnaB replication protein is a DNA helicase. J Biol Chem 261(10):4738-4748.
4. Fang L, Davey MJ, O'Donnell M (1999) Replisome assembly at oriC, the replication origin of E. coli, reveals an explanation for initiation sites outside an origin. Mol Cell 4(4):541-553.
5. Tougu K, Marians KJ (1996) The interaction between helicase and primase sets the replication fork clock. J Biol Chem 271(35):21398-21405.
6. Fuller RS, Funnell BE, Kornberg A (1984) The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38(3):889-900.
7. Duderstadt KE, Chuang K, Berger JM (2011) DNA stretching by bacterial initiators promotes replication origin opening. Nature 478(7368):209-213.
8. Ozaki S, Katayama T (2012) Highly organized DnaA-oriC complexes recruit the singlestranded DNA for replication initiation. Nucleic Acids Res 40(4):1648-1665.
9. Marszalek J, et al. (1996) Domains of DnaA protein involved in interaction with DnaB protein, and in unwinding the Escherichia coli chromosomal origin. J Biol Chem 271(31):18535-18542.
10. Marszalek J, Kaguni JM (1994) DnaA protein directs the binding of DnaB protein in initiation of DNA replication in Escherichia coli. J Biol Chem 269(7):4883-4890.
11. Funnell BE, Baker TA, Kornberg A (1987) In vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome. J Biol Chem 262(21):10327-10334.
12. Kim S, Dallmann HG, McHenry CS, Marians KJ (1996) Coupling of a replicative polymerase and helicase: A tau-DnaB interaction mediates rapid replication fork movement. Cell 84(4):643-650.
13. Lu YB, Ratnakar PV, Mohanty BK, Bastia D (1996) Direct physical interaction between DnaG primase and DnaB helicase of Escherichia coli is necessary for optimal synthesis of primer RNA. Proc Natl Acad Sci USA 93(23):12902-12907.
14. Yuzhakov A, Kelman Z, O'Donnell M (1999) Trading places on DNA-A three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell 96(1):153-163.
15. Kelch BA, Makino DL, O'Donnell M, Kuriyan J (2011) How a DNA polymerase clamp loader opens a sliding clamp. Science 334(6063):1675-1680.
16. Jeruzalmi D, et al. (2001) Mechanism of processivity clamp opening by the delta subunit wrench of the clamp loader complex of E. coli DNA polymerase III. Cell 106(4): 417-428.
17. Yuzhakov A, Turner J, O'Donnell M (1996) Replisome assembly reveals the basis for asymmetric function in leading and lagging strand replication. Cell 86(6):877-886.
18. Bloom LB (2009) Loading clamps for DNA replication and repair. DNA Repair (Amst) 8(5):570-578.
19. Kolatka K, Kubik S, Rajewska M, Konieczny I (2010) Replication and partitioning of the broad-host-range plasmid RK2. Plasmid 64(3):119-134.
20. Rajewska M, Wegrzyn K, Konieczny I (2012) AT-rich region and repeated sequences-The essential elements of replication origins of bacterial replicons. FEMS Microbiol Rev 36(2):408-434.
21. Konieczny I (2003) Strategies for helicase recruitment and loading in bacteria. EMBO Rep 4(1):37-41.
22. Perri S, Helinski DR, Toukdarian A (1991) Interactions of plasmid-encoded replication initiation proteins with the origin of DNA replication in the broad host range plasmid RK2. J Biol Chem 266(19):12536-12543.
23. Erzberger JP, Pirruccello MM, Berger JM (2002) The structure of bacterial DnaA: Implications for general mechanisms underlying DNA replication initiation. EMBO J 21(18):4763-4773.
24. Giraldo R, Fernández-Tornero C, Evans PR, Díaz-Orejas R, Romero A (2003) A conformational switch between transcriptional repression and replication initiation in the RepA dimerization domain. Nat Struct Biol 10(7):565-571.
25. Giraldo R (2003) Common domains in the initiators of DNA replication in Bacteria, Archaea and Eukarya: Combined structural, functional and phylogenetic perspectives. FEMS Microbiol Rev 26(5):533-554.
26. Konieczny I, Doran KS, Helinski DR, Blasina A (1997) Role of TrfA and DnaA proteins in origin opening during initiation of DNA replication of the broad host range plasmid RK2. J Biol Chem 272(32):20173-20178.
27. Jiang Y, Pacek M, Helinski DR, Konieczny I, Toukdarian A (2003) A multifunctional plasmid-encoded replication initiation protein both recruits and positions an active helicase at the replication origin. Proc Natl Acad Sci USA 100(15):8692-8697.
28. Konieczny I, Helinski DR (1997) Helicase delivery and activation by DnaA and TrfA proteins during the initiation of replication of the broad host range plasmid RK2. J Biol Chem 272(52):33312-33318.
29. Wegrzyn K, et al. (2014) Sequence-specific interactions of Rep proteins with ssDNA in the AT-rich region of the plasmid replication origin. Nucleic Acids Res 42(12): 7807-7818.
30. Kongsuwan K, Josh P, Picault MJ, Wijffels G, Dalrymple B (2006) The plasmid RK2 replication initiator protein (TrfA) binds to the sliding clamp beta subunit of DNA polymerase III: Implication for the toxicity of a peptide derived from the amino-terminal portion of 33-kilodalton TrfA. J Bacteriol 188(15):5501-5509.
31. Kaguni JM, Kornberg A (1984) Replication initiated at the origin (oriC) of the E. coli chromosome reconstituted with purified enzymes. Cell 38(1):183-190.
32. Marszalek J, Kaguni JM (1992) Defective replication activity of a dominant-lethal dnaB gene product from Escherichia coli. J Biol Chem 267(27):19334-19340.
33. Toukdarian AE, Helinski DR, Perri S (1996) The plasmid RK2 initiation protein binds to the origin of replication as a monomer. J Biol Chem 271(12):7072-7078.
34. Konieczny I, Helinski DR (1997) The replication initiation protein of the broad-hostrange plasmid RK2 is activated by the ClpX chaperone. Proc Natl Acad Sci USA 94(26): 14378-14382.
35. Konieczny I, Liberek K (2002) Cooperative action of Escherichia coli ClpB protein and DnaK chaperone in the activation of a replication initiation protein. J Biol Chem 277(21):18483-18488.
36. Kubik S, Wegrzyn K, Pierechod M, Konieczny I (2012) Opposing effects of DNA on proteolysis of a replication initiator. Nucleic Acids Res 40(3):1148-1159.
37. Arai K, Kornberg A (1979) A general priming system employing only dnaB protein and primase for DNA replication. Proc Natl Acad Sci USA 76(9):4308-4312.
38. Kato J, Katayama T (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20(15):4253-4262.
39. Katayama T, Kubota T, Kurokawa K, Crooke E, Sekimizu K (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase. Cell 94(1):61-71.
40. Swart JR, Griep MA (1995) Primer synthesis kinetics by Escherichia coli primase on single-stranded DNA templates. Biochemistry 34(49):16097-16106.
41. Rowen L, Kornberg A (1978) A ribo-deoxyribonucleotide primer synthesized by primase. J Biol Chem 253(3):770-774.
42. Ogawa T, Baker TA, van der Ende A, Kornberg A (1985) Initiation of enzymatic replication at the origin of the Escherichia coli chromosome: Contributions of RNA polymerase and primase. Proc Natl Acad Sci USA 82(11):3562-3566.
43. Pierechod M, et al. (2009) Conformation of a plasmid replication initiator protein affects its proteolysis by ClpXP system. Protein Sci 18(3):637-649.
44. Jergic S, et al. (2013) A direct proofreader-clamp interaction stabilizes the Pol III replicase in the polymerization mode. EMBO J 32(9):1322-1333.
45. Pacek M, Konopa G, Konieczny I (2001) DnaA box sequences as the site for helicase delivery during plasmid RK2 replication initiation in Escherichia coli. J Biol Chem 276(26):23639-23644.
46. Meyer RJ, Helinski DR (1977) Unidirectional replication of the P-group plasmid RK2. Biochim Biophys Acta 478(1):109-113.
47. Caspi R, et al. (2001) A broad host range replicon with different requirements for replication initiation in three bacterial species. EMBO J 20(12):3262-3271.
48. Caspi R, Helinski DR, Pacek M, Konieczny I (2000) Interactions of DnaA proteins from distantly related bacteria with the replication origin of the broad host range plasmid RK2. J Biol Chem 275(24):18454-18461.
49. San Martin MC, Stamford NP, Dammerova N, Dixon NE, Carazo JM (1995) A structural model for the Escherichia coli DnaB helicase based on electron microscopy data. J Struct Biol 114(3):167-176.
50. Kittell BL, Helinski DR (1991) Iteron inhibition of plasmid RK2 replication in vitro: Evidence for intermolecular coupling of replication origins as a mechanism for RK2 replication control. Proc Natl Acad Sci USA 88(4):1389-1393.
51. Stukenberg PT, Turner J, O'Donnell M (1994) An explanation for lagging strand replication: Polymerase hopping among DNA sliding clamps. Cell 78(5):877-887.
52. Wijffels G, et al. (2004) Inhibition of protein interactions with the beta 2 sliding clamp of Escherichia coli DNA polymerase III by peptides from beta 2-binding proteins. Biochemistry 43(19):5661-5671.
53. Scheuermann RH, Echols H (1984) A separate editing exonuclease for DNA replication: The epsilon subunit of Escherichia coli DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 81(24):7747-7751.
54. Studwell-Vaughan PS, O'Donnell M (1993) DNA polymerase III accessory proteins. V. Theta encoded by holE. J Biol Chem 268(16):11785-11791.
55. Tanner NA, et al. (2008) Single-molecule studies of fork dynamics in Escherichia coli DNA replication. Nat Struct Mol Biol 15(2):170-176.
56. Ozawa K, et al. (2005) Cell-free protein synthesis in an autoinduction system for NMR studies of protein-protein interactions. J Biomol NMR 32(3):235-241.
57. Wickner W, Kornberg A (1974) A holoenzyme form of deoxyribonucleic acid polymerase III. Isolation and properties. J Biol Chem 249(19):6244-6249.
58. Xiao H, Crombie R, Dong Z, Onrust R, O'Donnell M (1993) DNA polymerase III accessory proteins. III. holC and holD encoding chi and psi. J Biol Chem 268(16): 11773-11778.
59. Kolatka K, Witosinska M, Pierechod M, Konieczny I (2008) Bacterial partitioning proteins affect the subcellular location of broad-host-range plasmid RK2. Microbiology 154(Pt9):2847-2856.
60. Grimminger V, Richter K, Imhof A, Buchner J, Walter S (2004) The prion curing agent guanidinium chloride specifically inhibits ATP hydrolysis by Hsp104. J Biol Chem 279(9):7378-7383.
61. Studwell PS, O'Donnell M (1990) Processive replication is contingent on the exonuclease subunit of DNA polymerase III holoenzyme. J Biol Chem 265(2):1171-1178.
62. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287(2):252-260.
63. Studier FW, Moffatt BA (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189(1):113-130.
64. Appleyard RK (1954) Segregation of new lysogenic types during growth of a doubly lysogenic strain derived from Escherichia coli K12. Genetics 39(4):440-452.
65. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166(4):557-580.
66. Bullock WO, Fernandez JM, Short JM (1987) XL1-Blue-a high-efficiency plasmid transforming recA Escherichia coli strain with β-galactosidase selection. Biotechniques 5(3):376-379.
67. Kovach ME, et al. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166(1):175-176.
68. Baker TA, Kornberg A (1988) Transcriptional activation of initiation of replication from the E. coli chromosomal origin: An RNA-DNA hybrid near oriC. Cell 55(1): 113-123.
69. Hamdan S, et al. (2002) Hydrolysis of the 5′-p-nitrophenyl ester of TMP by the proofreading exonuclease (epsilon) subunit of Escherichia coli DNA polymerase III. Biochemistry 41(16):5266-5275.
70. Jergic S, et al. (2007) The unstructured C-terminus of the tau subunit of Escherichia coli DNA polymerase III holoenzyme is the site of interaction with the alpha subunit. Nucleic Acids Res 35(9):2813-2824.
71. Doran KS, Konieczny I, Helinski DR (1998) Replication origin of the broad host range plasmid RK2. Positioning of various motifs is critical for initiation of replication. J Biol Chem 273(14):8447-8453.
72. Oakley AJ, et al. (2003) Flexibility revealed by the 1.85 A crystal structure of the beta sliding-clamp subunit of Escherichia coli DNA polymerase III. Acta Crystallogr D Biol Crystallogr 59(Pt 7):1192-1199.
73. Valla S, Haugan K, Durland R, Helinski DR (1991) Isolation and properties of temperature-sensitive mutants of the trfA gene of the broad host range plasmid RK2. Plasmid 25(2):131-136.