Evidence for roles of the Escherichia coli Hda protein beyond regulatory inactivation of DnaA

Molecular Microbiology

Volumn 85, Issue 4, 2012, Pages 648-668

  Baxter, Jamie C ^a   Sutton, Mark D ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA POLYMERASE; DNA POLYMERASE IV; ESCHERICHIA COLI PROTEIN; PLASMID DNA; PROTEIN HDA; REPLICATION INITIATOR PROTEIN DNAA; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIABILITY; BACTERIUM MUTANT; COLD SENSITIVITY; CONTROLLED STUDY; DNA REPLICATION; ESCHERICHIA COLI; FLOW CYTOMETRY; FRAMESHIFT MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; REGULATORY MECHANISM; WILD TYPE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; DNA POLYMERASE BETA; DNA POLYMERASE II; DNA REPLICATION; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE DOSAGE; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION;

ESCHERICHIA COLI;

EID: 84864809268     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08129.x     Document Type: Article

References (85)

1. Atlung, T., Lobner-Olesen, A., and Hansen, F.G. (1987) Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli. Mol Gen Genet 206 : 51-59.
2. Banack, T., Clauson, N., Ogbaa, N., Villar, J., Oliver, D., and Firshein, W. (2005) Overexpression of the Hda DnaA-related protein in Escherichia coli inhibits multiplication, affects membrane permeability, and induces the SOS response. J Bacteriol 187 : 8507-8510.
3. Boye, E., Blinkova, A., and Walker, J.R. (2001) Defective initiation in an Escherichia coli dnaA(Cs, Sx) mutant. Biochimie 83 : 25-32.
4. Bunting, K.A., Roe, S.M., and Pearl, L.H. (2003) Structural basis for recruitment of translesion DNA polymerase Pol IV/DinB to the beta-clamp. EMBO J 22 : 5883-5892.
5. Burgers, P.M., Kornberg, A., and Sakakibara, Y. (1981) The dnaN gene codes for the beta subunit of DNA polymerase III holoenzyme of Escherichia coli. Proc Natl Acad Sci USA 78 : 5391-5395.
6. Camara, J.E., Skarstad, K., and Crooke, E. (2003) Controlled initiation of chromosomal replication in Escherichia coli requires functional Hda protein. J Bacteriol 185 : 3244-3248.
7. Camara, J.E., Breier, A.M., Brendler, T., Austin, S., Cozzarelli, N.R., and Crooke, E. (2005) Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6 : 736-741.
8. Carr, K.M., and Kaguni, J.M. (2001) Stoichiometry of DnaA and DnaB protein in initiation at the Escherichia coli chromosomal origin. J Biol Chem 276 : 44919-44925.
9. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134 : 1141-1156.
10. Charbon, G., Riber, L., Cohen, M., Skovgaard, O., Fujimitsu, K., Katayama, T., and Lobner-Olesen, A. (2011) Suppressors of DnaA(ATP) imposed overinitiation in Escherichia coli. Mol Microbiol 79 : 914-928.
11. Clarey, M.G., Erzberger, J., Grob, P., Leschziner, A.E., Berger, J.M., Nogales, E., and Botchan, M. (2006) Nucleotide-dependent conformational changes in the DnaA-like core of the origin recognition complex. Nat Struct Mol Biol 13 : 684-690.
12. Collier, J., and Shapiro, L. (2009) Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191 : 5706-5716.
13. Cupples, C.G., Cabrera, M., Cruz, C., and Miller, J.H. (1990) A set of lacZ mutations in Escherichia coli that allow rapid detection of specific frameshift mutations. Genetics 125 : 275-280.
14. Dalrymple, B.P., Kongsuwan, K., Wijffels, G., Dixon, N.E., and Jennings, P.A. (2001) A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc Natl Acad Sci USA 98 : 11627-11632.
15. Elledge, S.J., and Walker, G.C. (1983) Proteins required for ultraviolet light and chemical mutagenesis. Identification of the products of the umuC locus of Escherichia coli. J Mol Biol 164 : 175-192.
16. Feeney, M.A., Ke, N., and Beckwith, J. (2012) Mutations at several loci cause increased expression of ribonucleotide reductase in Escherichia coli. J Bacteriol 194 : 1515-1522.
17. Felczak, M.M., and Kaguni, J.M. (2009) DnaAcos hyperinitiates by circumventing regulatory pathways that control the frequency of initiation in Escherichia coli. Mol Microbiol 72 : 1348-1363.
18. Ferullo, D.J., and Lovett, S.T. (2008) The stringent response and cell cycle arrest in Escherichia coli. PLoS Genet 4 : e1000300.
19. Friedberg, E.C., Walker, G.C., and Siede, W. (1995) DNA Repair and Mutagenesis. Washington, DC: ASM Press.
20. Fujimitsu, K., Su'etsugu, M., Yamaguchi, Y., Mazda, K., Fu, N., Kawakami, H., and Katayama, T. (2008) Modes of overinitiation, dnaA gene expression, and inhibition of cell division in a novel cold-sensitive hda mutant of Escherichia coli. J Bacteriol 190 : 5368-5381.
21. Gines-Candelaria, E., Blinkova, A., and Walker, J.R. (1995) Mutations in Escherichia coli dnaA which suppress a dnaX(Ts) polymerization mutation and are dominant when located in the chromosomal allele and recessive on plasmids. J Bacteriol 177 : 705-715.
22. Gonzalez, M., Frank, E.G., Levine, A.S., and Woodgate, R. (1998) Lon-mediated proteolysis of the Escherichia coli UmuD mutagenesis protein: in vitro degradation and identification of residues required for proteolysis. Genes Dev 12 : 3889-3899.
23. Goranov, A.I., Breier, A.M., Merrikh, H., and Grossman, A.D. (2009) YabA of Bacillus subtilis controls DnaA-mediated replication initiation but not the transcriptional response to replication stress. Mol Microbiol 74 : 454-466.
24. Heltzel, J.M., Maul, R.W., Scouten Ponticelli, S.K., and Sutton, M.D. (2009) A model for DNA polymerase switching involving a single cleft and the rim of the sliding clamp. Proc Natl Acad Sci USA 106 : 12664-12669.
25. Horvath, D.J., Jr, Li, B., Casper, T., Partida-Sanchez, S., Hunstad, D.A., Hultgren, S.J., and Justice, S.S. (2011) Morphological plasticity promotes resistance to phagocyte killing of uropathogenic Escherichia coli. Microbes Infect 13 : 426-437.
26. Jarosz, D.F., Godoy, V.G., Delaney, J.C., Essigmann, J.M., and Walker, G.C. (2006) A single amino acid governs enhanced activity of DinB DNA polymerases on damaged templates. Nature 439 : 225-228.
27. Kaguni, J.M. (2006) DnaA: controlling the initiation of bacterial DNA replication and more. Annu Rev Microbiol 60 : 351-375.
28. Katayama, T. (1994) The mutant DnaAcos protein which overinitiates replication of the Escherichia coli chromosome is inert to negative regulation for initiation. J Biol Chem 269 : 22075-22079.
29. Katayama, T., and Crooke, E. (1995) DnaA protein is sensitive to a soluble factor and is specifically inactivated for initiation of in vitro replication of the Escherichia coli minichromosome. J Biol Chem 270 : 9265-9271.
30. Katayama, T., Kubota, T., Kurokawa, K., Crooke, E., and Sekimizu, K. (1998) The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E.coli chromosomal replicase. Cell 94 : 61-71.
31. Katayama, T., Ozaki, S., Keyamura, K., and Fujimitsu, K. (2010) Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8 : 163-170.
32. Kato, J., and Katayama, T. (2001) Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20 : 4253-4262.
33. Kawakami, H., Su'etsugu, M., and Katayama, T. (2006) An isolated Hda-clamp complex is functional in the regulatory inactivation of DnaA and DNA replication. J Struct Biol 156 : 220-229.
34. Kellenberger-Gujer, G., Podhajska, A.J., and Caro, L. (1978) A cold sensitive dnaA mutant of E.coli which overinitiates chromosome replication at low temperature. Mol Gen Genet 162 : 9-16.
35. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4 : 363-371.
36. + domain interaction involved in regulatory inactivation of DnaA. J Biol Chem 286 : 29336-29346.
37. Keyamura, K., Fujikawa, N., Ishida, T., Ozaki, S., Su'etsugu, M., Fujimitsu, K., etal. (2007) The interaction of DiaA and DnaA regulates the replication cycle in E.coli by directly promoting ATP DnaA-specific initiation complexes. Genes Dev 21 : 2083-2099.
38. Kim, S.R., Maenhaut-Michel, G., Yamada, M., Yamamoto, Y., Matsui, K., Sofuni, T., etal. (1997) Multiple pathways for SOS-induced mutagenesis in Escherichia coli: an overexpression of dinB/dinP results in strongly enhancing mutagenesis in the absence of any exogenous treatment to damage DNA. Proc Natl Acad Sci USA 94 : 13792-13797.
39. Kitagawa, R., Ozaki, T., Moriya, S., and Ogawa, T. (1998) Negative control of replication initiation by a novel chromosomal locus exhibiting exceptional affinity for Escherichia coli DnaA protein. Genes Dev 12 : 3032-3043.
40. Kurz, M., Dalrymple, B., Wijffels, G., and Kongsuwan, K. (2004) Interaction of the sliding clamp beta-subunit and Hda, a DnaA-related protein. J Bacteriol 186 : 3508-3515.
41. Learn, B.A., Um, S.J., Huang, L., and McMacken, R. (1997) Cryptic single-stranded-DNA binding activities of the phage lambda P and Escherichia coli DnaC replication initiation proteins facilitate the transfer of E.coli DnaB helicase onto DNA. Proc Natl Acad Sci USA 94 : 1154-1159.
42. Leonard, A.C., and Grimwade, J.E. (2010) Regulating DnaA complex assembly: it is time to fill the gaps. Curr Opin Microbiol 13 : 766-772.
43. Loh, T., Murphy, K.C., and Marinus, M.G. (2001) Mutational analysis of the MutH protein from Escherichia coli. J Biol Chem 276 : 12113-12119.
44. Lopez de Saro, F.J., and O'Donnell, M. (2001) Interaction of the beta sliding clamp with MutS, ligase, and DNA polymerase I. Proc Natl Acad Sci USA 98 : 8376-8380.
45. Lopez de Saro, F.J., Marinus, M.G., Modrich, P., and O'Donnell, M. (2006) The beta sliding clamp binds to multiple sites within MutL and MutS. J Biol Chem 281 : 14340-14349.
46. Lu, M., Campbell, J.L., Boye, E., and Kleckner, N. (1994) SeqA: a negative modulator of replication initiation in E.coli. Cell 77 : 413-426.
47. McHenry, C.S. (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80 : 403-436.
48. Maul, R.W., and Sutton, M.D. (2005) Roles of the Escherichia coli RecA protein and the global SOS response in effecting DNA polymerase selection in vivo. J Bacteriol 187 : 7607-7618.
49. Maul, R.W., Ponticelli, S.K., Duzen, J.M., and Sutton, M.D. (2007) Differential binding of Escherichia coli DNA polymerases to the beta-sliding clamp. Mol Microbiol 65 : 811-827.
50. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia Coli and Related Bacteria. Plainview, NY: Cold Spring Harbor Laboratory Press.
51. Morigen, Molina, F., and Skarstad, K. (2005) Deletion of the datA site does not affect once-per-cell-cycle timing but induces rifampin-resistant replication. J Bacteriol 187 : 3913-3920.
52. Mott, M.L., and Berger, J.M. (2007) DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5 : 343-354.
53. Nakamura, K., and Katayama, T. (2010) Novel essential residues of Hda for interaction with DnaA in the regulatory inactivation of DnaA: unique roles for Hda AAA box VI and VII motifs. Mol Microbiol 76 : 302-317.
54. O'Donnell, M., and Kuriyan, J. (2006) Clamp loaders and replication initiation. Curr Opin Struct Biol 16 : 35-41.
55. Ohmori, H., Friedberg, E.C., Fuchs, R.P., Goodman, M.F., Hanaoka, F., Hinkle, D., etal. (2001) The Y-family of DNA polymerases. Mol Cell 8 : 7-8.
56. Prakash, S., Johnson, R.E., and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74 : 317-353.
57. Rangarajan, S., Woodgate, R., and Goodman, M.F. (1999) A phenotype for enigmatic DNA polymerase II: a pivotal role for pol II in replication restart in UV-irradiated Escherichia coli. Proc Natl Acad Sci USA 96 : 9224-9229.
58. Riber, L., and Lobner-Olesen, A. (2005) Coordinated replication and sequestration of oriC and dnaA are required for maintaining controlled once-per-cell-cycle initiation in Escherichia coli. J Bacteriol 187 : 5605-5613.
59. Riber, L., Olsson, J.A., Jensen, R.B., Skovgaard, O., Dasgupta, S., Marinus, M.G., and Lobner-Olesen, A. (2006) Hda-mediated inactivation of the DnaA protein and dnaA gene autoregulation act in concert to ensure homeostatic maintenance of the Escherichia coli chromosome. Genes Dev 20 : 2121-2134.
60. Riber, L., Fujimitsu, K., Katayama, T., and Lobner-Olesen, A. (2009) Loss of Hda activity stimulates replication initiation from I-box, but not R4 mutant origins in Escherichia coli. Mol Microbiol 71 : 107-122.
61. Rozgaja, T.A., Grimwade, J.E., Iqbal, M., Czerwonka, C., Vora, M., and Leonard, A.C. (2011) Two oppositely oriented arrays of low-affinity recognition sites in oriC guide progressive binding of DnaA during Escherichia coli pre-RC assembly. Mol Microbiol 82 : 475-488.
62. Sanders, L.H., Rockel, A., Lu, H., Wozniak, D.J., and Sutton, M.D. (2006) Role of Pseudomonas aeruginosa dinB-encoded DNA polymerase IV in mutagenesis. J Bacteriol 188 : 8573-8585.
63. Schrödinger, L. (2010) The PyMOL Molecular Graphics System, Version 1.5.0.2.
64. Schwede, T., Kopp, J., Guex, N., and Peitsch, M.C. (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31 : 3381-3385.
65. Seitz, H., Weigel, C., and Messer, W. (2000) The interaction domains of the DnaA and DnaB replication proteins of Escherichia coli. Mol Microbiol 37 : 1270-1279.
66. Simmons, L.A., Breier, A.M., Cozzarelli, N.R., and Kaguni, J.M. (2004) Hyperinitiation of DNA replication in Escherichia coli leads to replication fork collapse and inviability. Mol Microbiol 51 : 349-358.
67. Strauss, B.S., Roberts, R., Francis, L., and Pouryazdanparast, P. (2000) Role of the dinB gene product in spontaneous mutation in Escherichia coli with an impaired replicative polymerase. J Bacteriol 182 : 6742-6750.
68. + box VIII motif in ATP hydrolysis. Mol Microbiol 40 : 376-386.
69. Su'etsugu, M., Takata, M., Kubota, T., Matsuda, Y., and Katayama, T. (2004) Molecular mechanism of DNA replication-coupled inactivation of the initiator protein in Escherichia coli: interaction of DnaA with the sliding clamp-loaded DNA and the sliding clamp-Hda complex. Genes Cells 9 : 509-522.
70. Su'etsugu, M., Shimuta, T.R., Ishida, T., Kawakami, H., and Katayama, T. (2005) Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J Biol Chem 280 : 6528-6536.
71. Su'etsugu, M., Nakamura, K., Keyamura, K., Kudo, Y., and Katayama, T. (2008) Hda monomerization by ADP binding promotes replicase clamp-mediated DnaA-ATP hydrolysis. J Biol Chem 283 : 36118-36131.
72. Sutton, M.D. (2004) The Escherichia coli dnaN159 mutant displays altered DNA polymerase usage and chronic SOS induction. J Bacteriol 186 : 6738-6748.
73. Sutton, M.D., and Duzen, J.M. (2006) Specific amino acid residues in the beta sliding clamp establish a DNA polymerase usage hierarchy in Escherichia coli. DNA Repair (Amst) 5 : 312-323.
74. Sutton, M.D., Carr, K.M., Vicente, M., and Kaguni, J.M. (1998) Escherichia coli DnaA protein. The N-terminal domain and loading of DnaB helicase at the E.coli chromosomal origin. J Biol Chem 273 : 34255-34262.
75. Sutton, M.D., Opperman, T., and Walker, G.C. (1999) The Escherichia coli SOS mutagenesis proteins UmuD and UmuD' interact physically with the replicative DNA polymerase. Proc Natl Acad Sci USA 96 : 12373-12378.
76. Sutton, M.D., Smith, B.T., Godoy, V.G., and Walker, G.C. (2000) The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu Rev Genet 34 : 479-497.
77. Sutton, M.D., Duzen, J.M., and Maul, R.W. (2005) Mutant forms of the Escherichia coli beta sliding clamp that distinguish between its roles in replication and DNA polymerase V-dependent translesion DNA synthesis. Mol Microbiol 55 : 1751-1766.
78. Sutton, M.D., Duzen, J.M., and Scouten Ponticelli, S.K. (2010) A single hydrophobic cleft in the Escherichia coli processivity clamp is sufficient to support cell viability and DNA damage-induced mutagenesis in vivo. BMC Mol Biol 11 : 102.
79. Wagner, J., and Nohmi, T. (2000) Escherichia coli DNA polymerase IV mutator activity: genetic requirements and mutational specificity. J Bacteriol 182 : 4587-4595.
80. Wagner, J., Gruz, P., Kim, S.R., Yamada, M., Matsui, K., Fuchs, R., and Nohmi, T. (1999) The dinB gene encodes a novel E.coli DNA polymerase, DNA pol IV, involved in mutagenesis. Mol Cell 4 : 281-286.
81. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100 : 195-199.
82. Wickens, H.J., Pinney, R.J., Mason, D.J., and Gant, V.A. (2000) Flow cytometric investigation of filamentation, membrane patency, and membrane potential in Escherichia coli following ciprofloxacin exposure. Antimicrob Agents Chemother 44 : 682-687.
83. Williams, A.B., Hetrick, K.M., and Foster, P.L. (2010) Interplay of DNA repair, homologous recombination, and DNA polymerases in resistance to the DNA damaging agent 4-nitroquinoline-1-oxide in Escherichia coli. DNA Repair (Amst) 9 : 1090-1097.
84. Xu, Q., McMullan, D., Abdubek, P., Astakhova, T., Carlton, D., Chen, C., etal. (2009) A structural basis for the regulatory inactivation of DnaA. J Mol Biol 385 : 368-380.
85. Yuan, B., Cao, H., Jiang, Y., Hong, H., and Wang, Y. (2008) Efficient and accurate bypass of N2-(1-carboxyethyl)-2′-deoxyguanosine by DinB DNA polymerase in vitro and in vivo. Proc Natl Acad Sci USA 105 : 8679-8684.