Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication

Current Biology

Volumn 21, Issue 13, 2011, Pages 1092-1101

  Jonas, Kristina ^a   Chen, Y Erin ^a,b   Laub, Michael T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CTRA PROTEIN, CAULOBACTER; DNA BINDING PROTEIN; DNAA PROTEIN, BACTERIA; TRANSCRIPTION FACTOR;

ARTICLE; CAULOBACTER CRESCENTUS; CELL CYCLE; CYTOLOGY; DNA REPLICATION; EVOLUTION; GENETICS; METABOLISM; PERIODICITY; PHYSIOLOGY;

BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; CAULOBACTER CRESCENTUS; CELL CYCLE; DNA REPLICATION; DNA-BINDING PROTEINS; PERIODICITY; TRANSCRIPTION FACTORS;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CAULOBACTER; CAULOBACTER VIBRIOIDES;

EID: 79960180892     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2011.05.040     Document Type: Article

References (48)

1. R.P. Bhattacharyya, A. Reményi, B.J. Yeh, and W.A. Lim Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits Annu. Rev. Biochem. 75 2006 655 680 (Pubitemid 44118047)
2. L.H. Hartwell, J.J. Hopfield, S. Leibler, and A.W. Murray From molecular to modular cell biology Nature 402 6761, Suppl 1999 C47 C52
3. G.T. Marczynski Chromosome methylation and measurement of faithful, once and only once per cell cycle chromosome replication in Caulobacter crescentus J. Bacteriol. 181 1999 1984 1993 (Pubitemid 29164949)
4. P.H. Viollier, M. Thanbichler, P.T. McGrath, L. West, M. Meewan, H.H. McAdams, and L. Shapiro Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication Proc. Natl. Acad. Sci. USA 101 2004 9257 9262 (Pubitemid 38812862)
5. B. Gorbatyuk, and G.T. Marczynski Physiological consequences of blocked Caulobacter crescentus dnaA expression, an essential DNA replication gene Mol. Microbiol. 40 2001 485 497 (Pubitemid 32391642)
6. M.L. Mott, and J.M. Berger DNA replication initiation: mechanisms and regulation in bacteria Nat. Rev. Microbiol. 5 2007 343 354 (Pubitemid 46605488)
7. J.M. Kaguni DnaA: controlling the initiation of bacterial DNA replication and more Annu. Rev. Microbiol. 60 2006 351 375
8. T. Katayama, S. Ozaki, K. Keyamura, and K. Fujimitsu Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC Nat. Rev. Microbiol. 8 2010 163 170
9. L. Klasson, and S.G. Andersson Evolution of minimal-gene-sets in host-dependent bacteria Trends Microbiol. 12 2004 37 43 (Pubitemid 38045258)
10. J. Kato, and T. Katayama Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli EMBO J. 20 2001 4253 4262 (Pubitemid 32751841)
11. P.D. Curtis, and Y.V. Brun Getting in the loop: regulation of development in Caulobacter crescentus Microbiol. Mol. Biol. Rev. 74 2010 13 41
12. K.C. Quon, B. Yang, I.J. Domian, L. Shapiro, and G.T. Marczynski Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin Proc. Natl. Acad. Sci. USA 95 1998 120 125 (Pubitemid 28103917)
13. K.C. Quon, G.T. Marczynski, and L. Shapiro Cell cycle control by an essential bacterial two-component signal transduction protein Cell 84 1996 83 93 (Pubitemid 26031463)
14. M.T. Laub, S.L. Chen, L. Shapiro, and H.H. McAdams Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle Proc. Natl. Acad. Sci. USA 99 2002 4632 4637 (Pubitemid 34286036)
15. E.G. Biondi, S.J. Reisinger, J.M. Skerker, M. Arif, B.S. Perchuk, K.R. Ryan, and M.T. Laub Regulation of the bacterial cell cycle by an integrated genetic circuit Nature 444 2006 899 904 (Pubitemid 46024998)
16. I.J. Domian, K.C. Quon, and L. Shapiro Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle Cell 90 1997 415 424 (Pubitemid 27347232)
17. A.A. Iniesta, P.T. McGrath, A. Reisenauer, H.H. McAdams, and L. Shapiro A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression Proc. Natl. Acad. Sci. USA 103 2006 10935 10940 (Pubitemid 44148398)
18. C.G. Tsokos, B.S. Perchuk, and M.T. Laub A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus Dev. Cell 20 2011 329 341
19. D.P. Bastedo, and G.T. Marczynski 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 2009 139 154
20. X. Shen, J. Collier, D. Dill, L. Shapiro, M. Horowitz, and H.H. McAdams Architecture and inherent robustness of a bacterial cell-cycle control system Proc. Natl. Acad. Sci. USA 105 2008 11340 11345
21. J. Collier, H.H. McAdams, and L. Shapiro A DNA methylation ratchet governs progression through a bacterial cell cycle Proc. Natl. Acad. Sci. USA 104 2007 17111 17116 (Pubitemid 350211000)
22. J. Collier, and L. Shapiro Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter J. Bacteriol. 191 2009 5706 5716
23. R.B. Jensen, and L. Shapiro The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation Proc. Natl. Acad. Sci. USA 96 1999 10661 10666 (Pubitemid 29442200)
24. Y.E. Chen, C. Tropini, K. Jonas, C.G. Tsokos, K.C. Huang, and M.T. Laub Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium Proc. Natl. Acad. Sci. USA 108 2011 1052 1057 10.1073/pnas.1015397108 Published online December 29, 2010
25. C. Jacobs, I.J. Domian, J.R. Maddock, and L. Shapiro Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division Cell 97 1999 111 120 (Pubitemid 29165894)
26. J. Wu, N. Ohta, J.L. Zhao, and A. Newton A novel bacterial tyrosine kinase essential for cell division and differentiation Proc. Natl. Acad. Sci. USA 96 1999 13068 13073
27. J.M. Sommer, and A. Newton Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus J. Bacteriol. 171 1989 392 401
28. T. Atlung, A. Løbner-Olesen, and F.G. Hansen Overproduction of DnaA protein stimulates initiation of chromosome and minichromosome replication in Escherichia coli Mol. Gen. Genet. 206 1987 51 59 (Pubitemid 17014165)
29. L. Cheng, and K.C. Keiler Correct timing of dnaA transcription and initiation of DNA replication requires trans translation J. Bacteriol. 191 2009 4268 4275
30. S. Nishida, K. Fujimitsu, K. Sekimizu, T. Ohmura, T. Ueda, and T. Katayama A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: Evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo J. Biol. Chem. 277 2002 14986 14995 (Pubitemid 34952573)
31. T. Katayama, T. Kubota, K. Kurokawa, E. Crooke, and K. Sekimizu The initiator function of DnaA protein is negatively regulated by the sliding clamp of the E. coli chromosomal replicase Cell 94 1998 61 71 (Pubitemid 28347470)
32. K. Nakamura, and T. Katayama 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 2010 302 317
33. M. Su'etsugu, T.R. Shimuta, T. Ishida, H. Kawakami, and T. Katayama Protein associations in DnaA-ATP hydrolysis mediated by the Hda-replicase clamp complex J. Biol. Chem. 280 2005 6528 6536 (Pubitemid 40341202)
34. A.A. Iniesta, N.J. Hillson, and L. Shapiro Polar remodeling and histidine kinase activation, which is essential for Caulobacter cell cycle progression, are dependent on DNA replication initiation J. Bacteriol. 192 2010 3893 3902
35. M.T. Laub, H.H. McAdams, T. Feldblyum, C.M. Fraser, and L. Shapiro Global analysis of the genetic network controlling a bacterial cell cycle Science 290 2000 2144 2148 (Pubitemid 32001594)
36. G. Zweiger, and L. Shapiro Expression of Caulobacter dnaA as a function of the cell cycle J. Bacteriol. 176 1994 401 408 (Pubitemid 24034058)
37. H. Murray, and J. Errington Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA Cell 135 2008 74 84
38. J.K. Wagner, K.A. Marquis, and D.Z. Rudner SirA enforces diploidy by inhibiting the replication initiator DnaA during spore formation in Bacillus subtilis Mol. Microbiol. 73 2009 963 974
39. M.F. Noirot-Gros, E. Dervyn, L.J. Wu, P. Mervelet, J. Errington, S.D. Ehrlich, and P. Noirot An expanded view of bacterial DNA replication Proc. Natl. Acad. Sci. USA 99 2002 8342 8347 (Pubitemid 34651054)
40. L. Rahn-Lee, H. Merrikh, A.D. Grossman, and R. Losick The sporulation protein SirA inhibits the binding of DnaA to the origin of replication by contacting a patch of clustered amino acids J. Bacteriol. 193 2010 1302 1307 10.1128/JB.01390-10 Published online January 14, 2011
41. B. Gorbatyuk, and G.T. Marczynski Regulated degradation of chromosome replication proteins DnaA and CtrA in Caulobacter crescentus Mol. Microbiol. 55 2005 1233 1245 (Pubitemid 40299190)
42. M. Brilli, M. Fondi, R. Fani, A. Mengoni, L. Ferri, M. Bazzicalupo, and E.G. Biondi The diversity and evolution of cell cycle regulation in alpha-proteobacteria: a comparative genomic analysis BMC Syst. Biol. 4 2010 52
43. R. Hallez, A.F. Bellefontaine, J.J. Letesson, and X. De Bolle Morphological and functional asymmetry in alpha-proteobacteria Trends Microbiol. 12 2004 361 365
44. R. Hallez, J. Mignolet, V. Van Mullem, M. Wery, J. Vandenhaute, J.J. Letesson, C. Jacobs-Wagner, and X. De Bolle The asymmetric distribution of the essential histidine kinase PdhS indicates a differentiation event in Brucella abortus EMBO J. 26 2007 1444 1455 (Pubitemid 46398701)
45. H. Lam, J.Y. Matroule, and C. Jacobs-Wagner The asymmetric spatial distribution of bacterial signal transduction proteins coordinates cell cycle events Dev. Cell 5 2003 149 159 (Pubitemid 36827349)
46. S.M. Shaheen, M.C. Ouimet, and G.T. Marczynski Comparative analysis of Caulobacter chromosome replication origins Microbiology 155 2009 1215 1225
47. A.K. Brassinga, R. Siam, W. McSween, H. Winkler, D. Wood, and G.T. Marczynski Conserved response regulator CtrA and IHF binding sites in the alpha-proteobacteria Caulobacter crescentus and Rickettsia prowazekii chromosomal replication origins J. Bacteriol. 184 2002 5789 5799
48. Y. Lu, and F.R. Cross Periodic cyclin-Cdk activity entrains an autonomous Cdc14 release oscillator Cell 141 2010 268 279