|
|
|
Vol. 12, No. 6, pp. 880-893, March 15, 1998
Departments of
1 Biology and
2 Chemistry,
Indiana University, Bloomington, Indiana 47405 USA
In the differentiating bacterium Caulobacter crescentus,
the cell division initiation protein FtsZ is present in only one of the
two cell types. Stalked cells initiate a new round of DNA replication
immediately after cell division and contain FtsZ, whereas the progeny
swarmer cells are unable to initiate DNA replication and do not contain
FtsZ. We show that FtsZ expression is controlled by cell
cycle-dependent transcription and proteolysis. Transcription of
ftsZ is repressed in swarmer cells and is activated
concurrently with the initiation of DNA replication. At the end of the
DNA replication period, transcription of ftsZ decreases
substantially. We show that the global cell cycle regulator CtrA is
involved in the cell cycle control of ftsZ transcription. CtrA
binds to a site that overlaps the ftsZ transcription start
site. Removal of the CtrA-binding site results in transcription of the
ftsZ promoter in swarmer cells. Decreasing the cellular
concentration of CtrA increases ftsZ transcription and
conversely, increasing the concentration of CtrA decreases ftsZ
transcription. Because CtrA is present in swarmer cells, is degraded at
the same time as ftsZ transcription begins, and reappears when
ftsZ transcription decreases at the end of the cell cycle, we
propose that CtrA is a repressor of ftsZ transcription. We show
that proteolysis is an important determinant of cell type-specific
distribution and cell cycle variation of FtsZ. FtsZ is stable when it
is synthesized and assembles into the cytokinetic ring at the beginning
of the cell cycle. After the initiation of cell division, the rate of FtsZ degradation increases as both the constriction site and the FtsZ
ring decrease in diameter. When ftsZ is expressed
constitutively from inducible promoters, the abundance of FtsZ still
varies during the cell cycle. The coupling of transcription and
proteolysis to cell division ensures that FtsZ is inherited only by the
progeny cell that will begin DNA replication immediately after cell division.
[Key Words: Caulobacter; FtsZ; cell division; proteolysis; cell cycle; differentiation]
This article has been cited by other articles:
![]() |
S. J. Reisinger, S. Huntwork, P. H. Viollier, and K. R. Ryan DivL Performs Critical Cell Cycle Functions in Caulobacter crescentus Independent of Kinase Activity J. Bacteriol., November 15, 2007; 189(22): 8308 - 8320. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Collier, H. H. McAdams, and L. Shapiro A DNA methylation ratchet governs progression through a bacterial cell cycle PNAS, October 23, 2007; 104(43): 17111 - 17116. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. D. Goley, A. A. Iniesta, and L. Shapiro Cell cycle regulation in Caulobacter: location, location, location J. Cell Sci., October 15, 2007; 120(20): 3501 - 3507. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. F. Susin, R. L. Baldini, F. Gueiros-Filho, and S. L. Gomes GroES/GroEL and DnaK/DnaJ Have Distinct Roles in Stress Responses and during Cell Cycle Progression in Caulobacter crescentus J. Bacteriol., December 1, 2006; 188(23): 8044 - 8053. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y.-L. Shih and L. Rothfield The Bacterial Cytoskeleton Microbiol. Mol. Biol. Rev., September 1, 2006; 70(3): 729 - 754. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Sakr, M. Thyssen, M. Denis, and C.-C. Zhang Relationship among Several Key Cell Cycle Events in the Developmental Cyanobacterium Anabaena sp. Strain PCC 7120. J. Bacteriol., August 1, 2006; 188(16): 5958 - 5965. [Abstract] [Full Text] [PDF] |
||||
![]() |
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 PNAS, July 18, 2006; 103(29): 10935 - 10940. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. L. Pierce, D. S. O'Donnol, R. C. Allen, J. W. Javens, E. M. Quardokus, and Y. V. Brun Mutations in DivL and CckA Rescue a divJ Null Mutant of Caulobacter crescentus by Reducing the Activity of CtrA. J. Bacteriol., April 1, 2006; 188(7): 2473 - 2482. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Del Sol, J. G. L. Mullins, N. Grantcharova, K. Flardh, and P. Dyson Influence of CrgA on Assembly of the Cell Division Protein FtsZ during Development of Streptomyces coelicolor J. Bacteriol., February 15, 2006; 188(4): 1540 - 1550. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. E. Muir, J. Easter, and J. W. Gober The trans-acting flagellar regulatory proteins, FliX and FlbD, play a central role in linking flagellar biogenesis and cytokinesis in Caulobacter crescentus Microbiology, November 1, 2005; 151(11): 3699 - 3711. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. Roy and P. Ajitkumar Transcriptional Analysis of the Principal Cell Division Gene, ftsZ, of Mycobacterium tuberculosis J. Bacteriol., April 1, 2005; 187(7): 2540 - 2550. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Dziadek, S. A. Rutherford, M. V. Madiraju, M. A. L. Atkinson, and M. Rajagopalan Conditional expression of Mycobacterium smegmatis ftsZ, an essential cell division gene Microbiology, June 1, 2003; 149(6): 1593 - 1603. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. B. Weart and P. A. Levin Growth Rate-Dependent Regulation of Medial FtsZ Ring Formation J. Bacteriol., May 1, 2003; 185(9): 2826 - 2834. [Abstract] [Full Text] [PDF] |
||||
![]() |
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 PNAS, April 2, 2002; 99(7): 4632 - 4637. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-W. Tsai and M. R. K. Alley Proteolysis of the Caulobacter McpA Chemoreceptor Is Cell Cycle Regulated by a ClpX-Dependent Pathway J. Bacteriol., September 1, 2001; 183(17): 5001 - 5007. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Kwak, A. J. Dharmatilake, H. Jiang, and K. E. Kendrick Differential Regulation of ftsZ Transcription during Septation of Streptomyces griseus J. Bacteriol., September 1, 2001; 183(17): 5092 - 5101. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Nanninga Cytokinesis in Prokaryotes and Eukaryotes: Common Principles and Different Solutions Microbiol. Mol. Biol. Rev., June 1, 2001; 65(2): 319 - 333. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. S. Kahng and L. Shapiro The CcrM DNA Methyltransferase of Agrobacterium tumefaciens Is Essential, and Its Activity Is Cell Cycle Regulated J. Bacteriol., May 15, 2001; 183(10): 3065 - 3075. [Abstract] [Full Text] |
||||
![]() |
M. J. Barnett, D. Y. Hung, A. Reisenauer, L. Shapiro, and S. R. Long A Homolog of the CtrA Cell Cycle Regulator Is Present and Essential in Sinorhizobium meliloti J. Bacteriol., May 15, 2001; 183(10): 3204 - 3210. [Abstract] [Full Text] |
||||
![]() |
B. Grünenfelder, G. Rummel, J. Vohradsky, D. Röder, H. Langen, and U. Jenal Proteomic analysis of the bacterial cell cycle PNAS, March 29, 2001; (2001) 71538098. [Abstract] [Full Text] |
||||
![]() |
C. Jacobs, D. Hung, and L. Shapiro Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle PNAS, March 7, 2001; (2001) 51609998. [Abstract] [Full Text] |
||||
![]() |
C. H. Boyd and J. W. Gober Temporal Regulation of Genes Encoding the Flagellar Proximal Rod in Caulobacter crescentus J. Bacteriol., January 15, 2001; 183(2): 725 - 735. [Abstract] [Full Text] |
||||
![]() |
I. Kuhn, L. Peng, S. Bedu, and C.-C. Zhang Developmental Regulation of the Cell Division Protein FtsZ in Anabaena sp. Strain PCC 7120, a Cyanobacterium Capable of Terminal Differentiation J. Bacteriol., August 15, 2000; 182(16): 4640 - 4643. [Abstract] [Full Text] |
||||
![]() |
G. T. Robertson, A. Reisenauer, R. Wright, R. B. Jensen, A. Jensen, L. Shapiro, and R. M. Roop II The Brucella abortus CcrM DNA Methyltransferase Is Essential for Viability, and Its Overexpression Attenuates Intracellular Replication in Murine Macrophages J. Bacteriol., June 15, 2000; 182(12): 3482 - 3489. [Abstract] [Full Text] |
||||
![]() |
A. S. Lang and J. T. Beatty Genetic analysis of a bacterial genetic exchange element: The gene transfer agent of Rhodobacter capsulatus PNAS, January 18, 2000; 97(2): 859 - 864. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Wu, N. Ohta, J.-L. Zhao, and A. Newton A novel bacterial tyrosine kinase essential for cell division and differentiation PNAS, November 9, 1999; 96(23): 13068 - 13073. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Reisenauer, L. S. Kahng, S. McCollum, and L. Shapiro Bacterial DNA Methylation: a Cell Cycle Regulator? J. Bacteriol., September 1, 1999; 181(17): 5135 - 5139. [Full Text] |
||||
![]() |
I. J. Domian, A. Reisenauer, and L. Shapiro Feedback control of a master bacterial cell-cycle regulator PNAS, June 8, 1999; 96(12): 6648 - 6653. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Østerås, A. Stotz, S. Schmid Nuoffer, and U. Jenal Identification and Transcriptional Control of the Genes Encoding the Caulobacter crescentus ClpXP Protease J. Bacteriol., May 15, 1999; 181(10): 3039 - 3050. [Abstract] [Full Text] |
||||
![]() |
A. Reisenauer, K. Quon, and L. Shapiro The CtrA Response Regulator Mediates Temporal Control of Gene Expression during the Caulobacter Cell Cycle J. Bacteriol., April 15, 1999; 181(8): 2430 - 2439. [Abstract] [Full Text] |
||||
![]() |
D. Joseleau-Petit, D. Vinella, and R. D'Ari Metabolic Alarms and Cell Division in Escherichia coli J. Bacteriol., January 1, 1999; 181(1): 9 - 14. [Full Text] |
||||
![]() |
C. Jacobs, D. Hung, and L. Shapiro Dynamic localization of a cytoplasmic signal transduction response regulator controls morphogenesis during the Caulobacter cell cycle PNAS, March 27, 2001; 98(7): 4095 - 4100. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Grunenfelder, G. Rummel, J. Vohradsky, D. Roder, H. Langen, and U. Jenal Proteomic analysis of the bacterial cell cycle PNAS, April 10, 2001; 98(8): 4681 - 4686. [Abstract] [Full Text] [PDF] |
||||