The β-sliding clamp directs the localization of HdaA to the replisome in Caulobacter crescentus

Microbiology (United Kingdom)

Volumn 159, Issue PART11, 2013, Pages 2237-2248

  Fernandez Fernandez, Carmen ^a   Grosse, Karin ^b   Sourjik, Victor ^b   Collier, Justine ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HDAA PROTEIN; MUTANT PROTEIN; REPLICATION INITIATOR PROTEIN DNAA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SLIDING CLAMP; CAULOBACTER CRESCENTUS; CELLULAR DISTRIBUTION; CHROMOSOME REPLICATION; CLAMP; CONTROLLED STUDY; DNA REPLICATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOBLOTTING; IN VIVO STUDY; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REGULATORY INACTIVATION OF DNAA; REPLISOME;

BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; DNA HELICASES; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; PROTEIN INTERACTION MAPPING; PROTEIN MULTIMERIZATION; TRANS-ACTIVATORS;

EID: 84886644512     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.068577-0     Document Type: Article

References (59)

1. Bastedo, D. P. & Marczynski, G. T. (2009). CtrA response regulator binding to the Caulobacter chromosome replication origin is required during nutrient and antibiotic stress as well as during cell cycle progression. Mol Microbiol 72, 139-154.
2. Baxter, J. C. & Sutton, M. D. (2012). Evidence for roles of the Escherichia coli Hda protein beyond regulatory inactivation of DnaA. Mol Microbiol 85, 648-668.
3. Brendler, T., Abeles, A. & Austin, S. (1995). A protein that binds to the P1 origin core and the oriC 13mer region in a methylation-specific fashion is the product of the host seqA gene. EMBO J 14, 4083-4089.
4. Camara, J. E., Breier, A. M., Brendler, T., Austin, S., Cozzarelli, N. R. & Crooke, E. (2005). Hda inactivation of DnaA is the predominant mechanism preventing hyperinitiation of Escherichia coli DNA replication. EMBO Rep 6, 736-741.
5. Collier, J. (2012). Regulation of chromosomal replication in Caulobacter crescentus. Plasmid 67, 76-87.
6. Collier, J. & Shapiro, L. (2009). Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J Bacteriol 191, 5706-5716.
7. Curtis, P. D. & Brun, Y. V. (2010). Getting in the loop: regulation of development in Caulobacter crescentus. MicrobiolMol Biol Rev 74, 13-41.
8. Dalrymple, B. P., Kongsuwan, K., Wijffels, G., Dixon, N. E. & Jennings, P. A. (2001). A universal protein-protein interaction motif in the eubacterial DNA replication and repair systems. Proc Natl Acad Sci U S A 98, 11627-11632.
9. Davey, M. J., Jeruzalmi, D., Kuriyan, J. & O'Donnell, M. (2002). Motors and switches: AAA+ machines within the replisome. Nat Rev Mol Cell Biol 3, 826-835.
10. Ditta, G., Stanfield, S., Corbin, D. & Helinski, D. R. (1980). Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc Natl Acad Sci U S A 77, 7347-7351.
11. Domian, I. J., Quon, K. C. & Shapiro, L. (1997). Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 415-424.
12. Duderstadt, K. E. & Berger, J. M. (2008). AAA+ ATPases in the initiation of DNA replication. Crit Rev Biochem Mol Biol 43, 163-187.
13. Ely, B. (1991). Genetics of Caulobacter crescentus. Methods Enzymol 204, 372-384.
14. Evinger, M. & Agabian, N. (1977). Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol 132, 294-301.
15. Fernandez-Fernandez, C., Gonzalez, D. & Collier, J. (2011). Regulation of the activity of the dual-function DnaA protein in Caulobacter crescentus. PLoS ONE 6, e26028.
16. Fujimitsu, K., Su'etsugu, M., Yamaguchi, Y., Mazda, K., Fu, N., Kawakami, H. & Katayama, T. (2008). Modes of overinitiation, dnaA gene expression, and inhibition of cell division in a novel coldsensitive hda mutant of Escherichia coli. J Bacteriol 190, 5368-5381.
17. Gon, S., Camara, J. E., Klungsøyr, H. K., Crooke, E., Skarstad, K. & Beckwith, J. (2006). A novel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in Escherichia coli. EMBO J 25, 1137-1147.
18. Gorbatyuk, B. & Marczynski, G. T. (2001). Physiological consequences of blocked Caulobacter crescentus dnaA expression, an essential DNA replication gene. Mol Microbiol 40, 485-497.
19. Jensen, R. B., Wang, S. C. & Shapiro, L. (2001). A moving DNA replication factory in Caulobacter crescentus. EMBO J 20, 4952-4963.
20. Jonas, K., Chen, Y. E. & Laub, M. T. (2011). Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication. Curr Biol 21, 1092-1101.
21. Kasho, K. & Katayama, T. (2013). DnaA binding locus datA promotes DnaA-ATP hydrolysis to enable cell cycle-coordinated replication initiation. Proc Natl Acad Sci U S A 110, 936-941.
22. Katayama, T. & 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.
23. 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, 61-71.
24. Katayama, T., Ozaki, S., Keyamura, K. & Fujimitsu, K. (2010). Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat Rev Microbiol 8, 163-170.
25. Kato, J. & Katayama, T. (2001). Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J 20, 4253-4262.
26. Kentner, D. & Sourjik, V. (2009). Dynamic map of protein interactions in the Escherichia coli chemotaxis pathway. Mol Syst Biol 5, 238.
27. Kim, Y. & Kipreos, E. T. (2007). The Caenorhabditis elegans replication licensing factor CDT-1 is targeted for degradation by the CUL-4/ DDB-1 complex. Mol Cell Biol 27, 1394-1406.
28. Kim, P. D., Banack, T., Lerman, D. M., Tracy, J. C., Camara, J. E., Crooke, E., Oliver, D. & Firshein, W. (2003). Identification of a novel membrane-associated gene product that suppresses toxicity of a TrfA peptide from plasmid RK2 and its relationship to the DnaA host initiation protein. J Bacteriol 185, 1817-1824.
29. Kitagawa, R., Ozaki, T., Moriya, S. & 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.
30. Kurokawa, K., Nishida, S., Emoto, A., Sekimizu, K. & Katayama, T. (1999). Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J 18, 6642-6652.
31. Kurz, M., Dalrymple, B., Wijffels, G. & Kongsuwan, K. (2004). Interaction of the sliding clamp β-subunit and Hda, a DnaA-related protein. J Bacteriol 186, 3508-3515.
32. Leonard, A. C. & Grimwade, J. E. (2011). Regulation of DnaA assembly and activity: taking directions from the genome. Annu Rev Microbiol 65, 19-35.
33. López de Saro, F. J. & O'Donnell, M. (2001). Interaction of the βsliding clamp with MutS, ligase, and DNA polymerase I. Proc Natl Acad Sci U S A 98, 8376-8380.
34. Lu, M., Campbell, J. L., Boye, E. & Kleckner, N. (1994). SeqA: a negative modulator of replication initiation in E. coli. Cell 77, 413-426.
35. Marczynski, G. T. (1999). Chromosome methylation and measurement of faithful, once and only once per cell cycle chromosome replication in Caulobacter crescentus. J Bacteriol 181, 1984-1993.
36. Meisenzahl, A. C., Shapiro, L. & Jenal, U. (1997). Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus. J Bacteriol 179, 592-600.
37. Messer, W. (2002). The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol Rev 26, 355-374.
38. Miyawaki, A. & Tsien, R. Y. (2000). Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein. Methods Enzymol 327, 472-500.
39. Mott, M. L. & Berger, J. M. (2007). DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5, 343-354.
40. Nakamura, K. & 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.
41. Neuwald, A. F., Aravind, L., Spouge, J. L. & Koonin, E. V. (1999). AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9, 27-43.
42. Nievera, C., Torgue, J. J., Grimwade, J. E. & Leonard, A. C. (2006). SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E. coli pre-RC. Mol Cell 24, 581-592.
43. Nishitani, H., Sugimoto, N., Roukos, V., Nakanishi, Y., Saijo, M., Obuse, C., Tsurimoto, T., Nakayama, K. I., Nakayama, K. & other authors (2006). Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J 25, 1126-1136.
44. O'Donnell, M. (2006). Replisome architecture and dynamics in Escherichia coli. J Biol Chem 281, 10653-10656.
45. Ogura, T., Whiteheart, S. W. & Wilkinson, A. J. (2004). Conserved arginine residues implicated in ATP hydrolysis, nucleotide-sensing, and inter-subunit interactions in AAA and AAA+ ATPases. J Struct Biol 146, 106-112.
46. Olliver, A., Saggioro, C., Herrick, J. & Sclavi, B. (2010). DnaA-ATP acts as a molecular switch to control levels of ribonucleotide reductase expression in Escherichia coli. Mol Microbiol 76, 1555-1571.
47. Quon, K. C., Yang, B., Domian, I. J., Shapiro, L. & Marczynski, G. T. (1998). Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci U S A 95, 120-125.
48. Riber, L., Olsson, J. A., Jensen, R. B., Skovgaard, O., Dasgupta, S., Marinus, M. G. & Løbner-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.
49. Scholefield, G., Veening, J. W. & Murray, H. (2011). DnaA and ORC: more than DNA replication initiators. Trends Cell Biol 21, 188-194.
50. Slater, S., Wold, S., Lu, M., Boye, E., Skarstad, K. & Kleckner, N. (1995). E. coli SeqA protein binds oriC in two different methylmodulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82, 927-936.
51. Sourjik, V. & Berg, H. C. (2002). Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci U S A 99, 123-127.
52. Speck, C., Weigel, C. & Messer, W. (1999). ATP-and ADP-dnaA protein, a molecular switch in gene regulation. EMBO J 18, 6169-6176.
53. Su'etsugu, M., Takata, M., Kubota, T., Matsuda, Y. & 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.
54. Su'etsugu, M., Shimuta, T. R., Ishida, T., Kawakami, H. & Katayama, T. (2005). Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex. J Biol Chem 280, 6528-6536.
55. Su'etsugu, M., Nakamura, K., Keyamura, K., Kudo, Y. & Katayama, T. (2008). Hda monomerization by ADP binding promotes replicase clamp-mediated DnaA-ATP hydrolysis. J Biol Chem 283, 36118-36131.
56. Taylor, J. A., Ouimet, M. C., Wargachuk, R. & Marczynski, G. T. (2011). The Caulobacter crescentus chromosome replication origin evolved two classes of weak DnaA binding sites. Mol Microbiol 82, 312-326.
57. Thanbichler, M., Iniesta, A. A. & Shapiro, L. (2007). A comprehensive set of plasmids for vanillate-and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res 35, e137.
58. West, L., Yang, D. & Stephens, C. (2002). Use of the Caulobacter crescentus genome sequence to develop a method for systematic genetic mapping. J Bacteriol 184, 2155-2166.
59. Wouters, F. S. & Bastiaens, P. I. (2001). Imaging protein-protein interactions by fluorescence resonance energy transfer (FRET) microscopy. Curr Protoc Protein Sci Chapter 19, Unit 19 15.