Binding mechanism of metalṡNTP substrates and stringent-response alarmones to bacterial DnaG-type primases

Structure

Volumn 20, Issue 9, 2012, Pages 1478-1489

  Rymer, Richard U ^a   Solorio, Francisco A ^b   Tehranchi, Ashley K ^c   Chu, Clement ^d   Corn, Jacob E ^e   Keck, James L ^f   Wang, Jue D ^c   Berger, James M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Baylor College of Medicine ^*  (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e GENENTECH INC   (United States)

^f UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA PRIMASE; METAL ION; NUCLEOSIDE TRIPHOSPHATE; BACTERIAL PROTEIN; COORDINATION COMPOUND; DEOXYRIBONUCLEOTIDE; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; MANGANESE;

ARTICLE; CHEMICAL ANALYSIS; COMPARATIVE STUDY; CRYSTAL STRUCTURE; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; SYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; COENZYME; ENZYME ACTIVE SITE; ENZYMOLOGY; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; COENZYMES; CONSERVED SEQUENCE; COORDINATION COMPLEXES; CRYSTALLOGRAPHY, X-RAY; DEOXYRIBONUCLEOTIDES; DNA PRIMASE; GUANOSINE PENTAPHOSPHATE; GUANOSINE TETRAPHOSPHATE; MANGANESE; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL;

EID: 84865723619     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.05.017     Document Type: Article

References (67)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, N. Echols, J.J. Headd, L.W. Hung, S. Jain, G.J. Kapral, and R.W. Grosse Kunstleve The Phenix software for automated determination of macromolecular structures Methods 55 2011 94 106
2. S.F. Altschul, W. Gish, W. Miller, E.W. Myers, and D.J. Lipman Basic local alignment search tool J. Mol. Biol. 215 1990 403 410
3. L. Aravind, D.D. Leipe, and E.V. Koonin Toprim - a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins Nucleic Acids Res. 26 1998 4205 4213
4. S. Bhattacharyya, and M.A. Griep DnaB helicase affects the initiation specificity of Escherichia coli primase on single-stranded DNA templates Biochemistry 39 2000 745 752
5. P.L. Carl Escherichia coli mutants with temperature-sensitive synthesis of DNA Mol. Gen. Genet. 109 1970 107 122
6. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
7. K. Chintakayala, C. Machón, A. Haroniti, M.A. Larson, S.H. Hinrichs, M.A. Griep, and P. Soultanas Allosteric regulation of the primase (DnaG) activity by the clamp-loader (tau) in vitro Mol. Microbiol. 72 2009 537 549
8. R.A. Copeland Evaluation of enzyme inhibitors in drug discovery. A guide for medicinal chemists and pharmacologists Methods Biochem. Anal. 46 2005 1 265
9. J.E. Corn, and J.M. Berger FASTDXL: a generalized screen to trap disulfide-stabilized complexes for use in structural studies Structure 15 2007 773 780
10. J.E. Corn, P.J. Pease, G.L. Hura, and J.M. Berger Crosstalk between primase subunits can act to regulate primer synthesis in trans Mol. Cell 20 2005 391 401
11. J.E. Corn, J.G. Pelton, and J.M. Berger Identification of a DNA primase template tracking site redefines the geometry of primer synthesis Nat. Struct. Mol. Biol. 15 2008 163 169
12. S. Doublié, and T. Ellenberger The mechanism of action of T7 DNA polymerase Curr. Opin. Struct. Biol. 8 1998 704 712
13. S. Doublié, S. Tabor, A.M. Long, C.C. Richardson, and T. Ellenberger Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution Nature 391 1998 251 258
14. G.S. Eadie The inhibition of cholinesterase by physostigmine and prostigmine J. Biol. Chem. 146 1942 85 93
15. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
16. D.N. Frick, and C.C. Richardson DNA primases Annu. Rev. Biochem. 70 2001 39 80
17. G.N. Godson, J. Schoenich, W. Sun, and A.A. Mustaev Identification of the magnesium ion binding site in the catalytic center of Escherichia coli primase by iron cleavage Biochemistry 39 2000 332 339
18. M.A. Griep, and E.R. Lokey The role of zinc and the reactivity of cysteines in Escherichia coli primase Biochemistry 35 1996 8260 8267
19. S.M. Hamdan, and A.M. van Oijen Timing, coordination, and rhythm: acrobatics at the DNA replication fork J. Biol. Chem. 285 2010 18979 18983
20. R.C. Heller, and K.J. Marians Replication fork reactivation downstream of a blocked nascent leading strand Nature 439 2006 557 562
21. B.H. Hofstee On the evaluation of the constants Vm and KM in enzyme reactions Science 116 1952 329 331
22. V. Jain, M. Kumar, and D. Chatterji ppGpp: stringent response and survival J. Microbiol. 44 2006 1 10
23. W. Kabsch Xds Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
24. M. Kato, T. Ito, G. Wagner, C.C. Richardson, and T. Ellenberger Modular architecture of the bacteriophage T7 primase couples RNA primer synthesis to DNA synthesis Mol. Cell 11 2003 1349 1360
25. K. Katoh, K. Misawa, K. Kuma, and T. Miyata MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform Nucleic Acids Res. 30 2002 3059 3066
26. J.L. Keck, D.D. Roche, A.S. Lynch, and J.M. Berger Structure of the RNA polymerase domain of E. coli primase Science 287 2000 2482 2486
27. S. Khopde, E.E. Biswas, and S.B. Biswas Affinity and sequence specificity of DNA binding and site selection for primer synthesis by Escherichia coli primase Biochemistry 41 2002 14820 14830
28. J.R. Kiefer, C. Mao, J.C. Braman, and L.S. Beese Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal Nature 391 1998 304 307
29. T. Kitani, K.Y. Yoda, T. Ogawa, and T. Okazaki Evidence that discontinuous DNA replication in Escherichia coli is primed by approximately 10 to 12 residues of RNA starting with a purine J. Mol. Biol. 184 1985 45 52
30. S.A. Koepsell, S. Hanson, S.H. Hinrichs, and M.A. Griep Fluorometric assay for bacterial primases Anal. Biochem. 339 2005 353 355
31. A.B. Kornberg, and A. Tania DNA Replication Second Edition 1992 W. H. Freeman and Company New York
32. R.D. Kuchta, and G. Stengel Mechanism and evolution of DNA primases Biochim. Biophys. Acta 1804 2010 1180 1189
33. J.B. Lee, R.K. Hite, S.M. Hamdan, X.S. Xie, C.C. Richardson, and A.M. van Oijen DNA primase acts as a molecular brake in DNA replication Nature 439 2006 621 624
34. S.J. Lee, and C.C. Richardson Essential lysine residues in the RNA polymerase domain of the gene 4 primase-helicase of bacteriophage T7 J. Biol. Chem. 276 2001 49419 49426
35. S.J. Lee, and C.C. Richardson Acidic residues in the nucleotide-binding site of the bacteriophage T7 DNA primase J. Biol. Chem. 280 2005 26984 26991
36. A.A. MacDowell, R.S. Celestre, M. Howells, W. McKinney, J. Krupnick, D. Cambie, E.E. Domning, R.M. Duarte, N. Kelez, and D.W. Plate Suite of three protein crystallography beamlines with single superconducting bend magnet as the source J. Synchrotron Radiat. 11 2004 447 455
37. M. Maciag, M. Kochanowska, R. Lyzeń, G. Wegrzyn, and A. Szalewska-Pałasz ppGpp inhibits the activity of Escherichia coli DnaG primase Plasmid 63 2010 61 67
38. M. Makowska-Grzyska, and J.M. Kaguni Primase directs the release of DnaC from DnaB Mol. Cell 37 2010 90 101
39. K.J. Marians Prokaryotic DNA replication Annu. Rev. Biochem. 61 1992 673 719
40. U. Mechold, H. Murphy, L. Brown, and M. Cashel Intramolecular regulation of the opposing (p)ppGpp catalytic activities of Rel(Seq), the Rel/Spo enzyme from Streptococcus equisimilis J. Bacteriol. 184 2002 2878 2888
41. L.V. Mendelman, B.B. Beauchamp, and C.C. Richardson Requirement for a zinc motif for template recognition by the bacteriophage T7 primase EMBO J. 13 1994 3909 3916
42. A.V. Mitkova, S.M. Khopde, and S.B. Biswas Mechanism and stoichiometry of interaction of DnaG primase with DnaB helicase of Escherichia coli in RNA primer synthesis J. Biol. Chem. 278 2003 52253 52261
43. M. Podobnik, P. McInerney, M. O'Donnell, and J. Kuriyan A TOPRIM domain in the crystal structure of the catalytic core of Escherichia coli primase confirms a structural link to DNA topoisomerases J. Mol. Biol. 300 2000 353 362
44. K. Potrykus, and M. Cashel (p)ppGpp: still magical? Annu. Rev. Microbiol. 62 2008 35 51
45. A. Rodina, and G.N. Godson Role of conserved amino acids in the catalytic activity of Escherichia coli primase J. Bacteriol. 188 2006 3614 3621
46. L. Rowen, and A. Kornberg Primase, the dnaG protein of Escherichia coli. An enzyme which starts DNA chains J. Biol. Chem. 253 1978 758 764
47. S.L. Salzberg, A.J. Salzberg, A.R. Kerlavage, and J.F. Tomb Skewed oligomers and origins of replication Gene 217 1998 57 67
48. B.H. Schmidt, A.B. Burgin, J.E. Deweese, N. Osheroff, and J.M. Berger A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases Nature 465 2010 641 644
49. Schrödinger, L. (2010). The PyMOL Molecular Graphics System, Version 1.3 Schrödinger, LLC.
50. A. Srivatsan, and J.D. Wang Control of bacterial transcription, translation and replication by (p)ppGpp Curr. Opin. Microbiol. 11 2008 100 105
51. T.A. Steitz, S.J. Smerdon, J. Jäger, and C.M. Joyce A unified polymerase mechanism for nonhomologous DNA and RNA polymerases Science 266 1994 2022 2025
52. W. Sun, and G.N. Godson Interaction of Escherichia coli primase with a phage G4ori(c)-E. coli SSB complex J. Bacteriol. 178 1996 6701 6705
53. W. Sun, J. Tormo, T.A. Steitz, and G.N. Godson Domains of Escherichia coli primase: functional activity of a 47-kDa N-terminal proteolytic fragment Proc. Natl. Acad. Sci. USA 91 1994 11462 11466
54. W. Sun, J. Schoneich, and G.N. Godson A mutant Escherichia coli primase defective in elongation of primer RNA chains J. Bacteriol. 181 1999 3761 3767
55. J.R. Swart, and M.A. Griep Primer synthesis kinetics by Escherichia coli primase on single-stranded DNA templates Biochemistry 34 1995 16097 16106
56. N.A. Tanner, S.M. Hamdan, S. Jergic, K.V. Loscha, P.M. Schaeffer, N.E. Dixon, and A.M. van Oijen Single-molecule studies of fork dynamics in Escherichia coli DNA replication Nat. Struct. Mol. Biol. 15 2008 170 176
57. K. Tougu, and K.J. Marians The extreme C terminus of primase is required for interaction with DnaB at the replication fork J. Biol. Chem. 271 1996 21391 21397
58. K. Tougu, and K.J. Marians The interaction between helicase and primase sets the replication fork clock J. Biol. Chem. 271 1996 21398 21405
59. K. Tougu, H. Peng, and K.J. Marians Identification of a domain of Escherichia coli primase required for functional interaction with the DnaB helicase at the replication fork J. Biol. Chem. 269 1994 4675 4682
60. T.M. Urlacher, and M.A. Griep Magnesium acetate induces a conformational change in Escherichia coli primase Biochemistry 34 1995 16708 16714
61. A.M. van Oijen, and J.J. Loparo Single-molecule studies of the replisome Annu. Rev. Biophys. 39 2010 429 448
62. J.D. Wang, G.M. Sanders, and A.D. Grossman Nutritional control of elongation of DNA replication by (p)ppGpp Cell 128 2007 865 875
63. A.M. Waterhouse, J.B. Procter, D.M. Martin, M. Clamp, and G.J. Barton Jalview Version 2 - a multiple sequence alignment editor and analysis workbench Bioinformatics 25 2009 1189 1191
64. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, and A. McCoy Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
65. C.A. Wu, E.L. Zechner, and K.J. Marians Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. I. Multiple effectors act to modulate Okazaki fragment size J. Biol. Chem. 267 1992 4030 4044
66. C.A. Wu, E.L. Zechner, J.A. Reems, C.S. McHenry, and K.J. Marians Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. V. Primase action regulates the cycle of Okazaki fragment synthesis J. Biol. Chem. 267 1992 4074 4083
67. E.L. Zechner, C.A. Wu, and K.J. Marians Coordinated leading- and lagging-strand synthesis at the Escherichia coli DNA replication fork. II. Frequency of primer synthesis and efficiency of primer utilization control Okazaki fragment size J. Biol. Chem. 267 1992 4045 4053