Genetic Analysis of the Cell Division Protein FtsI (PBP3): Amino Acid Substitutions that Impair Septal Localization of FtsI and Recruitment of FtsN

Journal of Bacteriology

Volumn 186, Issue 2, 2004, Pages 490-502

  Wissel, Mark C ^a   Weiss, David S ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; PROTEIN FTSI; PROTEIN FTSN; PROTEIN PBP3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CELL DIVISION; CYTOPLASM; GENE MUTATION; GENETIC ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; WESTERN BLOTTING;

AMINO ACID SUBSTITUTION; ANIMALS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; HEAT; MEMBRANE PROTEINS; MUTATION; PENICILLINS; PEPTIDYL TRANSFERASES; RABBITS;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0347915664     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.2.490-502.2004     Document Type: Article

References (41)

1. Adam, M., C. Fraipont, N. Rhazi, M. Nguyen-Disteche, B. Lakaye, J. M. Frere, B. Devreese, J. Van Beeumen, Y. van Heijenoort, J. van Heijenoort, and J. M. Ghuysen. 1997. The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 179:6005-6009.
2. Addinall, S. G., C. Cao, and J. Lutkenhaus. 1997. FtsN, a late recruit to the septum in Escherichia coli. Mol. Microbiol. 25:303-309.
3. Ausubel, F. A., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1998. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
4. 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.
5. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
6. Botta, G. A., and J. T. Park. 1981, Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation. J. Bacteriol. 145:333-340.
7. Bowler, L. D., and B. G. Spratt. 1989. Membrane topology of penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 3:1277-1286.
8. Boyd, D., C. Manoil, and J. Beckwith. 1987. Determinants of membrane protein topology. Proc. Natl. Acad. Sci. USA 84:8525-8529.
9. Boyd, D., D. S. Weiss, J. C. Chen, and J. Beckwith. 2000. Towards single-copy gene expression systems making gene cloning physiologically relevant: lambda InCh, a simple Escherichia coli plasmid-chromosome shuttle system. J. Bacteriol. 182:842-847.
10. Chen, J. C., M. Minev, and J. Beckwith. 2002. Analysis of ftsQ mutant alleles in Escherichia coli: complementation, septal localization, and recruitment of downstream cell division proteins. J. Bacteriol. 184:695-705.
11. Cormack B. P., R. H. Valdivia, and S. Falkow. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
12. Dai, K., Y. Xu, and J. Lutkenhaus. 1996. Topological characterization of the essential Escherichia coli cell division protein FtsN. J. Bacteriol. 178:1328-1334.
13. Dessen, A., N. Mouz, E. Gordon, J. Hopkins, and O. Dideberg. 2001. Crystal structure of PBP2x from a highly penicillin-resistant Streptococcus pneumoniae clinical isolate: a mosaic framework containing 83 mutations. J. Biol. Chem. 276:45106-45112.
14. Eberhardt, C., L. Kuerschner, and D. S. Weiss. 2003. Probing the catalytic activity of a cell division-specific transpeptidase in vivo with beta-lactams. J. Bacteriol. 185:3726-3734.
15. Errington, J., R. A. Daniel, and D. J. Scheffers. 2003. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67:52-65.
16. Ghuysen, J. M. 1991. Serine beta-lactamases and penicillin-binding proteins. Annu. Rev. Microbiol. 45:37-67.
17. Goffin, C., C. Fraipont, J. Ayala, M. Terrak, M. Nguyen-Disteche, and J. M. Ghuysen. 1996. The non-penicillin-binding module of the tripartite penicillin-binding protein 3 of Escherichia coli is required for folding and/or stability of the penicillin-binding module and the membrane-anchoring module confers cell septation activity on the folded structure. J. Bacteriol. 178:5402-5409.
18. Goffin, C., and J. M. Ghuysen. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
19. BAD promoter. J. Bacteriol. 177:4121-4130.
20. Guzman, L. M., D. S. Weiss, and J. Beckwith. 1997. Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli. J. Bacteriol. 179:5094-5103.
21. Haldimann, A., and B. L. Wanner. 2001. Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J. Bacteriol. 183:6384-6393.
22. Hara, H., Y. Nishimura, J. Kato, H., Suzuki, H. Nagasawa, A. Suzuki, and Y. Hirota. 1989. Genetic analyses of processing involving C-terminal cleavage in penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 171:5882-5889.
23. Hara, H., S. Yasuda, K. Horiuchi, and J. T. Park. 1997. A promoter for the first nine genes of the Escherichia coli mra cluster of cell division and cell envelope biosynthesis genes, including ftsI and ftsW. J. Bacteriol. 179:5802-5811.
24. Hashimoto-Gotoh, T., M. Yamaguchi, K. Yasojima, A. Tsujimura, Y. Wakabayashi, and Y. Watanabe. 2000. A set of temperature sensitive-replication/-segregation and temperature resistant plasmid vectors with different copy numbers and in an isogenic background (chloramphenicol, kanamycin, lacZ, repA, par, polA). Gene 241:185-191.
25. Heidrich, C., M. F. Templin, A. Ursinus, M. Merdanovic, J. Berger, H. Schwarz, M. A. de Pedro, and J. V. Holtje. 2001. Involvement of N-acetyl-muramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178.
26. Höltje, J. V. 1996. A hypothetical holoenzyme involved in the replication of the murein sacculus of Escherichia coli. Microbiology 142:1911-1918.
27. Jones, T. A., J. Y. Zou, S. W. Cowan, and Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47:110-119.
28. r penicillin-binding proteins of Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 82:1999-2003.
29. Marrec-Fairley, M., A. Piette, X. Gallet, R. Brasseur, H. Hara, C. Fraipont, J. M. Ghuysen, and M. Nguyen-Distèche. 2000. Differential functionalities of amphiphilic peptide segments of the cell-septation penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 37:1019-1031.
30. Mercer, K. L., and D. S. Weiss. 2002. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J. Bacteriol. 184:904-912.
31. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
32. Nagasawa, H., Y. Sakagami, A. Suzuki, H. Suzuki, H. Hara, and Y. Hirota. 1989. Determination of the cleavage site involved in C-terminal processing of penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 171:5890-5893.
33. Nguyen-Disteche, M., C. Fraipont, N. Buddelmeijer, and N. Nanninga. 1998. The structure and function of Escherichia coli penicillin-binding protein 3. Cell Mol. Life Sci. 54:309-316.
34. Nicholas, R. A., J. L. Strominger, H. Suzuki, and Y. Hirota. 1985. Identification of the active site in penicillin-binding protein 3 of Escherichia coli. J. Bacteriol. 164:456-460.
35. Pares, S., N. Mouz, Y. Petillot, R. Hakenbeck, and O. Dideberg. 1996. X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme. Nat. Struct. Biol. 3:284-289.
36. Pogliano, J., K. Pogliano, D. S. Weiss, R. Losick, and J. Beckwith. 1997. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. Proc. Natl. Acad. Sci. USA 94:559-564.
37. Spratt, B. G. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. USA 72:2999-3003.
38. Vollmer, W., and J. V. Höltje. 2001. Morphogenesis of Escherichia coli. Curr. Opin. Microbiol. 4:625-633.
39. von Rechenberg, M., A. Ursinus, and J. V. Höltje. 1996. Affinity chromatography as a means to study multienzyme complexes involved in murein synthesis. Microb. Drug Resist. 2:155-157.
40. Weiss, D. S., J. C. Chen, J. M. Ghigo, D. Boyd, and J. Beckwith. 1999. Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL. J. Bacteriol. 181:508-520.
41. Weiss, D. S., K. Pogliano, M. Carson, L. M. Guzman, C. Fraipont, M. Nguyen-Disteche, R. Losick, and J. Beckwith. 1997. Localization of the Escherichia coli cell division protein FtsI (PBP3) to the division site and cell pole. Mol. Microbiol. 25:671-681.