Abstract
ABSTRACTFormation of theEscherichia colidivision septum is catalyzed by a number of essential proteins (named Fts) that assemble into a ring-like structure at the future division site. Several of these Fts proteins are intrinsic transmembrane proteins whose functions are largely unknown. Although these proteins appear to be recruited to the division site in a hierarchical order, the molecular interactions underlying the assembly of the cell division machinery remain mostly unspecified. In the present study, we used a bacterial two-hybrid system based on interaction-mediated reconstitution of a cyclic AMP (cAMP) signaling cascade to unravel the molecular basis of septum assembly by analyzing the protein interaction network amongE. colicell division proteins. Our results indicate that the Fts proteins are connected to one another through multiple interactions. A deletion mapping analysis carried out with two of these proteins, FtsQ and FtsI, revealed that different regions of the polypeptides are involved in their associations with their partners. Furthermore, we showed that the association between two Fts hybrid proteins could be modulated by the coexpression of a third Fts partner. Altogether, these data suggest that the cell division machinery assembly is driven by the cooperative association among the different Fts proteins to form a dynamic multiprotein structure at the septum site. In addition, our study shows that the cAMP-based two-hybrid system is particularly appropriate for analyzing molecular interactions between membrane proteins.
References
46
Referenced
413
-
Bernhardt, T. G., and P. A. de Boer. 2003. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol.48:1171-1182.
(
10.1046/j.1365-2958.2003.03511.x
) / Mol. Microbiol. (2003) -
Bernhardt, T. G., and P. A. de Boer. 2004. Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol. Microbiol.52:1255-1269.
(
10.1111/j.1365-2958.2004.04063.x
) / Mol. Microbiol. (2004) -
Bi, E. F., and J. Lutkenhaus. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature354:161-164.
(
10.1038/354161a0
) / Nature (1991) -
Bramhill, D. 1997. Bacterial cell division. Annu. Rev. Cell Dev. Biol.13:395-424.
(
10.1146/annurev.cellbio.13.1.395
) / Annu. Rev. Cell Dev. Biol. (1997) -
Buddelmeijer, N., and J. Beckwith. 2002. Assembly of cell division proteins at the E. coli cell center. Curr. Opin. Microbiol.5:553-557.
(
10.1016/S1369-5274(02)00374-0
) / Curr. Opin. Microbiol. (2002) -
Buddelmeijer, N., and J. Beckwith. 2004. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol. Microbiol.52:1315-1327.
(
10.1111/j.1365-2958.2004.04044.x
) / Mol. Microbiol. (2004) -
Buddelmeijer, N., N. Judson, D. Boyd, J. J. Mekalanos, and J. Beckwith. 2002. YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site. Proc. Natl. Acad. Sci. USA99:6316-6321.
(
10.1073/pnas.092128499
) / Proc. Natl. Acad. Sci. USA (2002) -
Carballido-Lopez, R., and J. Errington. 2003. A dynamic bacterial cytoskeleton. Trends Cell Biol.13:577-583.
(
10.1016/j.tcb.2003.09.005
) / Trends Cell Biol. (2003) -
Carettoni, D., P. Gomez-Puertas, L. Yim, J. Mingorance, O. Massidda, M. Vicente, A. Valencia, E. Domenici, and D. Anderluzzi. 2003. Phage-display and correlated mutations identify an essential region of subdomain 1C involved in homodimerization of Escherichia coli FtsA. Proteins50:192-206.
(
10.1002/prot.10244
) / Proteins (2003) 10.1128/JB.184.3.695-705.2002
10.1128/JB.181.2.521-530.1999
- Choquet, D., and A. Triller. 2003. The role of receptor diffusion in the organization of the postsynaptic membrane. Nat. Rev. Neurosci.4:251-265. / Nat. Rev. Neurosci. (2003)
10.1128/JB.186.22.7736-7744.2004
10.1128/jb.174.19.6145-6151.1992
10.1128/jb.175.12.3790-3797.1993
10.1128/JB.182.24.7060-7066.2000
-
Di Lallo, G., L. Castagnoli, P. Ghelardini, and L. Paolozzi. 2001. A two-hybrid system based on chimeric operator recognition for studying protein homo/heterodimerization in Escherichia coli. Microbiology147:1651-1656.
(
10.1099/00221287-147-6-1651
) / Microbiology (2001) -
Di Lallo, G., M. Fagioli, D. Barionovi, P. Ghelardini, and L. Paolozzi. 2003. Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology149:3353-3359.
(
10.1099/mic.0.26580-0
) / Microbiology (2003) -
Dove, S. L., and A. Hochschild. 1998. Conversion of the omega subunit of Escherichia coli RNA polymerase into a transcriptional activator or an activation target. Genes Dev.12:745-754.
(
10.1101/gad.12.5.745
) / Genes Dev. (1998) -
Ehrmann, M., R. Ehrle, E. Hofmann, W. Boos, and A. Schlosser. 1998. The ABC maltose transporter. Mol. Microbiol.29:685-694.
(
10.1046/j.1365-2958.1998.00915.x
) / Mol. Microbiol. (1998) -
Fields, S., and O. Song. 1989. A novel genetic system to detect protein-protein interactions. Nature340:245-246.
(
10.1038/340245a0
) / Nature (1989) -
Goryshin, I. Y., T. A. Naumann, J. Apodaca, and W. S. Reznikoff. 2003. Chromosomal deletion formation system based on Tn5 double transposition: use for making minimal genomes and essential gene analysis. Genome Res.13:644-653.
(
10.1101/gr.611403
) / Genome Res. (2003) 10.1128/jb.179.16.5094-5103.1997
-
Hale, C. A., and P. A. de Boer. 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell88:175-185.
(
10.1016/S0092-8674(00)81838-3
) / Cell (1997) 10.1128/JB.184.9.2552-2556.2002
-
Haney, S. A., E. Glasfeld, C. Hale, D. Keeney, Z. He, and P. de Boer. 2001. Genetic analysis of the Escherichia coli FtsZ.ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J. Biol. Chem.276:11980-11987.
(
10.1074/jbc.M009810200
) / J. Biol. Chem. (2001) -
Hu, J. C. 1995. Repressor fusions as a tool to study protein-protein interactions. Structure3:431-433.
(
10.1016/S0969-2126(01)00176-9
) / Structure (1995) -
Karimova, G., D. Ladant, and A. Ullmann. 2004. Relief of catabolite repression in a cAMP-independent catabolite gene activator mutant of Escherichia coli. Res. Microbiol.155:76-79.
(
10.1016/j.resmic.2003.11.002
) / Res. Microbiol. (2004) -
Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. USA95:5752-5756.
(
10.1073/pnas.95.10.5752
) / Proc. Natl. Acad. Sci. USA (1998) - Karimova, G., A. Ullmann, and D. Ladant. 2001. Protein-protein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J. Mol. Microbiol. Biotechnol.3:73-82. / J. Mol. Microbiol. Biotechnol. (2001)
-
Kolmar, H., F. Hennecke, K. Gotze, B. Janzer, B. Vogt, F. Mayer, and H. J. Fritz. 1995. Membrane insertion of the bacterial signal transduction protein ToxR and requirements of transcription activation studied by modular replacement of different protein substructures. EMBO J.14:3895-3904.
(
10.1002/j.1460-2075.1995.tb00061.x
) / EMBO J. (1995) -
Liu, Z., A. Mukherjee, and J. Lutkenhaus. 1999. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol.31:1853-1861.
(
10.1046/j.1365-2958.1999.01322.x
) / Mol. Microbiol. (1999) -
Lutkenhaus, J. 2002. Dynamic proteins in bacteria. Curr. Opin. Microbiol.5:548-552.
(
10.1016/S1369-5274(02)00376-4
) / Curr. Opin. Microbiol. (2002) 10.1128/jb.179.21.6788-6797.1997
-
Margolin, W. 2000. Green fluorescent protein as a reporter for macromolecular localization in bacterial cells. Methods20:62-72.
(
10.1006/meth.1999.0906
) / Methods (2000) 10.1128/jb.184.4.904-912.2002
- Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
10.1128/jb.176.9.2754-2758.1994
-
Pardee, A. B., and L. S. Prestidge. 1959. On the nature of the repressor of beta-galactosidase synthesis in Escherichia coli. Biochim. Biophys. Acta36:545-547.
(
10.1016/0006-3002(59)90202-1
) / Biochim. Biophys. Acta (1959) -
Rothfield, L., S. Justice, and J. Garcia-Lara. 1999. Bacterial cell division. Annu. Rev. Genet.33:423-448.
(
10.1146/annurev.genet.33.1.423
) / Annu. Rev. Genet. (1999) - Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
10.1128/JB.186.3.785-793.2004
10.1128/jb.166.3.985-992.1986
10.1128/jb.179.17.5551-5559.1997
-
Weiss, D. S. 2004. Bacterial cell division and the septal ring. Mol. Microbiol.54:588-597.
(
10.1111/j.1365-2958.2004.04283.x
) / Mol. Microbiol. (2004) 10.1128/JB.182.22.6366-6373.2000
Dates
Type | When |
---|---|
Created | 20 years, 5 months ago (March 17, 2005, 4:41 p.m.) |
Deposited | 1 year, 7 months ago (Jan. 23, 2024, 10:14 p.m.) |
Indexed | 1 month, 1 week ago (July 14, 2025, 11:39 p.m.) |
Issued | 20 years, 4 months ago (April 1, 2005) |
Published | 20 years, 4 months ago (April 1, 2005) |
Published Print | 20 years, 4 months ago (April 1, 2005) |
@article{Karimova_2005, title={Interaction Network amongEscherichia coliMembrane Proteins Involved in Cell Division as Revealed by Bacterial Two-Hybrid Analysis}, volume={187}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.187.7.2233-2243.2005}, DOI={10.1128/jb.187.7.2233-2243.2005}, number={7}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Karimova, Gouzel and Dautin, Nathalie and Ladant, Daniel}, year={2005}, month=apr, pages={2233–2243} }