Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 15 December 2000:
Vol. 290. no. 5499, pp. 2144 - 2148
DOI: 10.1126/science.290.5499.2144
Prev | Table of Contents | Next

Reports

Global Analysis of the Genetic Network Controlling a Bacterial Cell Cycle

Michael T. Laub,1 Harley H. McAdams,1 Tamara Feldblyum,2 Claire M. Fraser,2 Lucy Shapiro1*

This report presents full-genome evidence that bacterial cells use discrete transcription patterns to control cell cycle progression. Global transcription analysis of synchronized Caulobacter crescentus cells was used to identify 553 genes (19% of the genome) whose messenger RNA levels varied as a function of the cell cycle. We conclude that in bacteria, as in yeast, (i) genes involved in a given cell function are activated at the time of execution of that function, (ii) genes encoding proteins that function in complexes are coexpressed, and (iii) temporal cascades of gene expression control multiprotein structure biogenesis. A single regulatory factor, the CtrA member of the two-component signal transduction family, is directly or indirectly involved in the control of 26% of the cell cycle-regulated genes.

1 Department of Developmental Biology, Beckman Center, Stanford University School of Medicine, Stanford, CA 94305, USA.
2 The Institute for Genomic Research, 9712 Medical Center Drive, Rockville, MD 20850, USA.
*   To whom correspondence should be addressed. E-mail: shapiro{at}cmgm.stanford.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Feedback Control of DnaA-Mediated Replication Initiation by Replisome-Associated HdaA Protein in Caulobacter.
J. Collier and L. Shapiro (2009)
J. Bacteriol. 191, 5706-5716
   Abstract »    Full Text »    PDF »
CtrA, a Global Response Regulator, Uses a Distinct Second Category of Weak DNA Binding Sites for Cell Cycle Transcription Control in Caulobacter crescentus.
W. Spencer, R. Siam, M.-C. Ouimet, D. P. Bastedo, and G. T. Marczynski (2009)
J. Bacteriol. 191, 5458-5470
   Abstract »    Full Text »    PDF »
Dynamic Chromosome Organization and Protein Localization Coordinate the Regulatory Circuitry that Drives the Bacterial Cell Cycle.
E.D. Goley, E. Toro, H.H. McAdams, and L. Shapiro (2009)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Cross species analysis of microarray expression data.
Y. Lu, P. Huggins, and Z. Bar-Joseph (2009)
Bioinformatics 25, 1476-1483
   Abstract »    Full Text »    PDF »
Quantitative genome-scale analysis of protein localization in an asymmetric bacterium.
J. N. Werner, E. Y. Chen, J. M. Guberman, A. R. Zippilli, J. J. Irgon, and Z. Gitai (2009)
PNAS 106, 7858-7863
   Abstract »    Full Text »    PDF »
Organization and PprB-Dependent Control of the Pseudomonas aeruginosa tad Locus, Involved in Flp Pilus Biology.
C. S. Bernard, C. Bordi, E. Termine, A. Filloux, and S. de Bentzmann (2009)
J. Bacteriol. 191, 1961-1973
   Abstract »    Full Text »    PDF »
A Systematic Screen for Transcriptional Regulators of the Yeast Cell Cycle.
M. A. White, L. Riles, and B. A. Cohen (2009)
Genetics 181, 435-446
   Abstract »    Full Text »    PDF »
A genetic timer through noise-induced stabilization of an unstable state.
M. Turcotte, J. Garcia-Ojalvo, and G. M. Suel (2008)
PNAS 105, 15732-15737
   Abstract »    Full Text »    PDF »
PflI, a Protein Involved in Flagellar Positioning in Caulobacter crescentus.
P. L. Obuchowski and C. Jacobs-Wagner (2008)
J. Bacteriol. 190, 1718-1729
   Abstract »    Full Text »    PDF »
The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus.
S. K. Radhakrishnan, M. Thanbichler, and P. H. Viollier (2008)
Genes & Dev. 22, 212-225
   Abstract »    Full Text »    PDF »
High-resolution timing of cell cycle-regulated gene expression.
M. Rowicka, A. Kudlicki, B. P. Tu, and Z. Otwinowski (2007)
PNAS 104, 16892-16897
   Abstract »    Full Text »    PDF »
Cell cycle regulation in Caulobacter: location, location, location.
E. D. Goley, A. A. Iniesta, and L. Shapiro (2007)
J. Cell Sci. 120, 3501-3507
   Abstract »    Full Text »    PDF »
Current progress in network research: toward reference networks for key model organisms.
B. S. Srinivasan, N. H. Shah, J. A. Flannick, E. Abeliuk, A. F. Novak, and S. Batzoglou (2007)
Brief Bioinform 8, 318-332
   Abstract »    Full Text »    PDF »
Global Gene Expression Patterns of Nostoc punctiforme in Steady-State Dinitrogen-Grown Heterocyst-Containing Cultures and at Single Time Points during the Differentiation of Akinetes and Hormogonia.
E. L. Campbell, M. L. Summers, H. Christman, M. E. Martin, and J. C. Meeks (2007)
J. Bacteriol. 189, 5247-5256
   Abstract »    Full Text »    PDF »
Genome-wide transcription map of an archaeal cell cycle.
M. Lundgren and R. Bernander (2007)
PNAS 104, 2939-2944
   Abstract »    Full Text »    PDF »
A Sinorhizobium meliloti minE mutant has an altered morphology and exhibits defects in legume symbiosis.
J. Cheng, C. D. Sibley, R. Zaheer, and T. M. Finan (2007)
Microbiology 153, 375-387
   Abstract »    Full Text »    PDF »
Proteolytic Adaptor for Transfer-Messenger RNA-Tagged Proteins from {alpha}-Proteobacteria.
F. H. Lessner, B. J. Venters, and K. C. Keiler (2007)
J. Bacteriol. 189, 272-275
   Abstract »    Full Text »    PDF »
GroES/GroEL and DnaK/DnaJ Have Distinct Roles in Stress Responses and during Cell Cycle Progression in Caulobacter crescentus.
M. F. Susin, R. L. Baldini, F. Gueiros-Filho, and S. L. Gomes (2006)
J. Bacteriol. 188, 8044-8053
   Abstract »    Full Text »    PDF »
Global Map of Growth-Regulated Gene Expression in Burkholderia pseudomallei, the Causative Agent of Melioidosis.
F. Rodrigues, M. Sarkar-Tyson, S. V. Harding, S. H. Sim, H. H. Chua, C. H. Lin, X. Han, R. K. M. Karuturi, K. Sung, K. Yu, et al. (2006)
J. Bacteriol. 188, 8178-8188
   Abstract »    Full Text »    PDF »
Comparative Genomic Evidence for a Close Relationship between the Dimorphic Prosthecate Bacteria Hyphomonas neptunium and Caulobacter crescentus..
J. H. Badger, T. R. Hoover, Y. V. Brun, R. M. Weiner, M. T. Laub, G. Alexandre, J. Mrazek, Q. Ren, I. T. Paulsen, K. E. Nelson, et al. (2006)
J. Bacteriol. 188, 6841-6850
   Abstract »    Full Text »    PDF »
Identification of cell cycle regulators in Mycobacterium tuberculosis by inhibition of septum formation and global transcriptional analysis.
R. A. Slayden, D. L. Knudson, and J. T. Belisle (2006)
Microbiology 152, 1789-1797
   Abstract »    Full Text »    PDF »
The Bifunctional FtsK Protein Mediates Chromosome Partitioning and Cell Division in Caulobacter.
S. C. E. Wang, L. West, and L. Shapiro (2006)
J. Bacteriol. 188, 1497-1508
   Abstract »    Full Text »    PDF »
Classification using functional data analysis for temporal gene expression data.
X. Leng and H.-G. Muller (2006)
Bioinformatics 22, 68-76
   Abstract »    Full Text »    PDF »
Whole-Genome Transcriptional Analysis of Heavy Metal Stresses in Caulobacter crescentus.
P. Hu, E. L. Brodie, Y. Suzuki, H. H. McAdams, and G. L. Andersen (2005)
J. Bacteriol. 187, 8437-8449
   Abstract »    Full Text »    PDF »
Role of Integration Host Factor in the Transcriptional Activation of Flagellar Gene Expression in Caulobacter crescentus.
R. E. Muir and J. W. Gober (2005)
J. Bacteriol. 187, 949-960
   Abstract »    Full Text »    PDF »
Patterns of large-scale genomic variation in virulent and avirulent Burkholderia species.
C. Ong, C. H. Ooi, D. Wang, H. Chong, K. C. Ng, F. Rodrigues, M. A. Lee, and P. Tan (2004)
Genome Res. 14, 2295-2307
   Abstract »    Full Text »    PDF »
Oscillating Global Regulators Control the Genetic Circuit Driving a Bacterial Cell Cycle.
J. Holtzendorff, D. Hung, P. Brende, A. Reisenauer, P. H. Viollier, H. H. McAdams, and L. Shapiro (2004)
Science 304, 983-987
   Abstract »    Full Text »    PDF »
Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis.
K. R. Ryan, S. Huntwork, and L. Shapiro (2004)
PNAS 101, 7415-7420
   Abstract »    Full Text »    PDF »
Network motifs in integrated cellular networks of transcription-regulation and protein-protein interaction.
E. Yeger-Lotem, S. Sattath, N. Kashtan, S. Itzkovitz, R. Milo, R. Y. Pinter, U. Alon, and H. Margalit (2004)
PNAS 101, 5934-5939
   Abstract »    Full Text »    PDF »
Transcriptional Profiling of Caulobacter crescentus during Growth on Complex and Minimal Media.
A. K. Hottes, M. Meewan, D. Yang, N. Arana, P. Romero, H. H. McAdams, and C. Stephens (2004)
J. Bacteriol. 186, 1448-1461
   Abstract »    Full Text »    PDF »
Formation and Composition of the Bacillus anthracis Endospore.
H. Liu, N. H. Bergman, B. Thomason, S. Shallom, A. Hazen, J. Crossno, D. A. Rasko, J. Ravel, T. D. Read, S. N. Peterson, et al. (2004)
J. Bacteriol. 186, 164-178
   Abstract »    Full Text »    PDF »
Systems Biology Is Taking Off.
M. Ehrenberg, J. Elf, E. Aurell, R. Sandberg, and J. Tegner (2003)
Genome Res. 13, 2377-2380
   Full Text »    PDF »
A Bacterial Cell-Cycle Regulatory Network Operating in Time and Space.
H. H. McAdams and L. Shapiro (2003)
Science 301, 1874-1877
   Abstract »    Full Text »    PDF »
A Dual Binding Site for Integration Host Factor and the Response Regulator CtrA inside the Caulobacter crescentus Replication Origin.
R. Siam, A. K. C. Brassinga, and G. T. Marczynski (2003)
J. Bacteriol. 185, 5563-5572
   Abstract »    Full Text »    PDF »
Cell-Cycle-Regulated Expression and Subcellular Localization of the Caulobacter crescentus SMC Chromosome Structural Protein.
R. B. Jensen and L. Shapiro (2003)
J. Bacteriol. 185, 3068-3075
   Abstract »    Full Text »    PDF »
Global Stage-Specific Gene Regulation during the Developmental Cycle of Chlamydia trachomatis.
T. L. Nicholson, L. Olinger, K. Chong, G. Schoolnik, and R. S. Stephens (2003)
J. Bacteriol. 185, 3179-3189
   Abstract »    Full Text »    PDF »
Gene Expression Profiling of Helicobacter pylori Reveals a Growth-Phase-Dependent Switch in Virulence Gene Expression.
L. J. Thompson, D. S. Merrell, B. A. Neilan, H. Mitchell, A. Lee, and S. Falkow (2003)
Infect. Immun. 71, 2643-2655
   Abstract »    Full Text »    PDF »
tmRNA in Caulobacter crescentus Is Cell Cycle Regulated by Temporally Controlled Transcription and RNA Degradation.
K. C. Keiler and L. Shapiro (2003)
J. Bacteriol. 185, 1825-1830
   Abstract »    Full Text »    PDF »
Glutamate at the phosphorylation site of response regulator CtrA provides essential activities without increasing DNA binding.
R. Siam and G. T. Marczynski (2003)
Nucleic Acids Res. 31, 1775-1779
   Abstract »    Full Text »    PDF »
Prokaryotic Development: Emerging Insights.
L. Kroos and J. R. Maddock (2003)
J. Bacteriol. 185, 1128-1146
   Full Text »    PDF »
Generating and Exploiting Polarity in Bacteria.
L. Shapiro, H. H. McAdams, and R. Losick (2002)
Science 298, 1942-1946
   Abstract »    Full Text »    PDF »
Degradation of a Caulobacter Soluble Cytoplasmic Chemoreceptor Is ClpX Dependent.
I. Potocka, M. Thein, M. Osteras, U. Jenal, and M. R. K. Alley (2002)
J. Bacteriol. 184, 6635-6641
   Abstract »    Full Text »    PDF »
Growth phase-dependent and differential transcriptional control of flagellar genes in Helicobacter pylori.
E. Niehus, F. Ye, S. Suerbaum, and C. Josenhans (2002)
Microbiology 148, 3827-3837
   Abstract »    Full Text »    PDF »
Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins.
P. H. Viollier, N. Sternheim, and L. Shapiro (2002)
PNAS 99, 13831-13836
   Abstract »    Full Text »    PDF »
A signal transduction protein cues proteolytic events critical to Caulobacter cell cycle progression.
D. Y. Hung and L. Shapiro (2002)
PNAS 99, 13160-13165
   Abstract »    Full Text »    PDF »
Assigning numbers to the arrows: Parameterizing a gene regulation network by using accurate expression kinetics.
M. Ronen, R. Rosenberg, B. I. Shraiman, and U. Alon (2002)
PNAS 99, 10555-10560
   Abstract »    Full Text »    PDF »
Genome-Wide Dynamic Transcriptional Profiling of the Light-to-Dark Transition in Synechocystis sp. Strain PCC 6803.
R. T. Gill, E. Katsoulakis, W. Schmitt, G. Taroncher-Oldenburg, J. Misra, and G. Stephanopoulos (2002)
J. Bacteriol. 184, 3671-3681
   Abstract »    Full Text »    PDF »
Identification of Genes Periodically Expressed in the Human Cell Cycle and Their Expression in Tumors.
M. L. Whitfield, G. Sherlock, A. J. Saldanha, J. I. Murray, C. A. Ball, K. E. Alexander, J. C. Matese, C. M. Perou, M. M. Hurt, P. O. Brown, et al. (2002)
Mol. Biol. Cell 13, 1977-2000
   Abstract »    Full Text »    PDF »
Use of the Caulobacter crescentus Genome Sequence To Develop a Method for Systematic Genetic Mapping.
L. West, D. Yang, and C. Stephens (2002)
J. Bacteriol. 184, 2155-2166
   Abstract »    Full Text »
Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle.
M. T. Laub, S. L. Chen, L. Shapiro, and H. H. McAdams (2002)
PNAS 99, 4632-4637
   Abstract »    Full Text »    PDF »
A transcriptional profile of multicellular development in Dictyostelium discoideum.
N. Van Driessche, C. Shaw, M. Katoh, T. Morio, R. Sucgang, M. Ibarra, H. Kuwayama, T. Saito, H. Urushihara, M. Maeda, et al. (2002)
Development 129, 1543-1552
   Abstract »    Full Text »    PDF »
Conserved Promoter Motif Is Required for Cell Cycle Timing of dnaX Transcription in Caulobacter.
K. C. Keiler and L. Shapiro (2001)
J. Bacteriol. 183, 4860-4865
   Abstract »    Full Text »    PDF »
Genome-Wide Transcriptional Profiling of the Escherichia coli Responses to Superoxide Stress and Sodium Salicylate.
P. J. Pomposiello, M. H. J. Bennik, and B. Demple (2001)
J. Bacteriol. 183, 3890-3902
   Abstract »    Full Text »    PDF »
Microarrays for microbiologists.
S. Lucchini, A. Thompson, and J. C. D. Hinton (2001)
Microbiology 147, 1403-1414
   Full Text »    PDF »
A Homolog of the CtrA Cell Cycle Regulator Is Present and Essential in Sinorhizobium meliloti.
M. J. Barnett, D. Y. Hung, A. Reisenauer, L. Shapiro, and S. R. Long (2001)
J. Bacteriol. 183, 3204-3210
   Abstract »    Full Text »
New members of the ctrA regulon: the major chemotaxis operon in Caulobacter is CtrA dependent.
S. E. Jones, N. L. Ferguson, and M. R. K. Alley (2001)
Microbiology 147, 949-958
   Abstract »    Full Text »
Proteomic analysis of the bacterial cell cycle.
B. Grünenfelder, G. Rummel, J. Vohradsky, D. Röder, H. Langen, and U. Jenal (2001)
PNAS
   Abstract »    Full Text »
Complete genome sequence of Caulobacter crescentus.
W. C. Nierman, T. V. Feldblyum, M. T. Laub, I. T. Paulsen, K. E. Nelson, J. Eisen, J. F. Heidelberg, M. R. K. Alley, N. Ohta, J. R. Maddock, et al. (2001)
PNAS
   Abstract »    Full Text »
Complete genome sequence of Caulobacter crescentus.
W. C. Nierman, T. V. Feldblyum, M. T. Laub, I. T. Paulsen, K. E. Nelson, J. Eisen, J. F. Heidelberg, M. R. K. Alley, N. Ohta, J. R. Maddock, et al. (2001)
PNAS 98, 4136-4141
   Abstract »    Full Text »    PDF »
Proteomic analysis of the bacterial cell cycle.
B. Grunenfelder, G. Rummel, J. Vohradsky, D. Roder, H. Langen, and U. Jenal (2001)
PNAS 98, 4681-4686
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)