Localization of FtsI (PBP3) to the septal ring requires its membrane anchor, the Z ring, FtsA, FtsQ, and FtsL

Journal of Bacteriology

Volumn 181, Issue 2, 1999, Pages 508-520

  Weiss, David S ^a,b   Chen, Joseph C ^a   Ghigo, Jean Marc ^a,c   Boyd, Dana ^a   Beckwith, Jon ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; GAMMA GLUTAMYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; PROTEIN FTSI; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CELL DIVISION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE FUSION; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 0032932435     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.2.508-520.1999     Document Type: Article

References (59)

1. Adam, M., C. Fraipont, N. Rhazi, M. Nguyen-Distèche, B. Lakaye, J. M. Frère, B. Devreese, J. Van Beeumen, Y. van Heijenoort, J. van Heijenoort, and J. M. Ghuysen. 1997. The himodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes pcptide 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., E. Bi, and J. Lutkenhaus. 1996. FtsZ ring formation in fts mutants. J. Bacteriol. 178:3877-3884.
3. Addinall, S. G., C. Cao, and J. Lutkenhaus. 1997. FtsN, a late recruit to the septum in Escherichia coli. Mol. Microbiol. 25:303-309.
4. Addinall, S. G., C. Cao, and J. Lutkenhaus. 1997. Temperature shift experiments with an ftsZ84(Ts) strain reveal rapid dynamics of FtsZ localization and indicate that the Z ring is required throughout septation and cannot reoccupy division sites once constriction has initiated. J. Bacteriol. 179:4277-4284.
5. Addinall, S. G., and J. Lutkenhaus. 1996. FtsA is localized to the septum in an FtsZ-dependent manner. J. Bacteriol. 178:7167-7172.
6. Alley, M. R., J. R. Maddock, and L. Shapiro. 1993. Requirement of the carboxyl terminus of a bacterial chemoreceptor for its targeted proteolysis. Science 259:1754-1757.
7. Asoh, S., H. Matsuzawa, F. Ishino, J. L. Strominger, M. Matsuhashi, and T. Ohta. 1986. Nucleotide sequence of the pbpA gene and characteristics of the deduced amino acid sequence of penicillin-binding protein 2 of Escherichia coli K12. Eur. J. Biochem. 160:231-238.
8. Bi, E. F., and J. Lutkenhaus. 1991. FtsZ ring structure associated with division in Escherichia coli. Nature 354:161-164.
9. Botta, G. A., and J. T. Park. 1981. Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation hut not during cell elongation. J. Bacteriol. 145:333-340.
10. Bowler, L. D., and B. G. Spratt. 1989. Membrane topology of penicillin-binding protein 3 of Escherichia coli. Mol. Microbiol. 3:1277-1286.
11. Boyd, D., D. S. Weiss, J. C. Chen, and J. Beckwith. Unpublished data.
12. Bramhill, D. 1997. Bacterial cell division. Annu. Rev. Cell. Dev. Biol. 13: 395-424.
13. Broome-Smith, J. K., P. J. Hedge, and B. G. Spratt. 1985. Production of thiol-penicillin-binding protein 3 of Escherichia coli using a two primer method of site-directed mutagenesis. EMBO J. 4:231-235.
14. Chalfie, M., Y. Tu, G. Euskirchen, W. W. Ward, and D. C. Prasher. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802-805.
15. Chen, J. C., D. S. Weiss, J.-M. Ghigo, and J. Beckwith. 1998. Septal localization of FtsQ, an essential cell division protein in Escherichia coli. J. Bacteriol. 181:521-530.
16. Cormack, B. P., R. H. Valdivia, and S. Falkow. 1996. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173:33-38.
17. Dai, K., Y. Xu, and J. Lutkenhaus. 1993. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J. Bacteriol. 175:3790-3797.
18. Din, N., E. M. Quardokus, M. J. Sackett, and Y. V. Brun. 1998. Dominant C-terminal deletions of FtsZ that affect its ability to localize in Caulobacter and its interaction with FtsA. Mol. Microbiol. 27:1051-1063.
19. Dougherty, T. J., K. Kennedy, R. E. Kessler, and M. J. Pucci. 1996. Direct quantitation of the number of individual penicillin-binding proteins per cell in Escherichia coli. J. Bacteriol. 178:6110-6115.
20. Egile, C., H. d'Hauteville, C. Parsot, and P. J. Sansonetti. 1997. SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol. Microbiol. 23:1063-1073.
21. Ehrmann, M., D. Boyd, and J. Beckwith. 1990. Genetic analysis of membrane protein topology by a sandwich gene fusion approach. Proc. Natl. Acad. Sci. USA 87:7574-7578.
22. Fraipont, C., M. Adam, M. Nguyen-Distèche, W. Keck, J. Van Beeumen, J. A. Ayala, B. Granier, H. Hara, and J. M. Ghuysen. 1994. Engineering and overexpression of periplasmic forms of the penicillin-binding protein 3 of Escherichia coli. Biochem. J. 298:189-195.
23. Ghigo, J.-M., D. S. Weiss, J. Chen, J. C. Yarrow, and J. Beckwith. Mol. Microbiol., in press.
24. Ghuysen, J. M. 1994. Molecular structures of penicillin-binding proteins and beta-lactamases. Trends Microbiol. 2:372-380.
25. Goffin, C., C. Fraipont, J. Ayala, M. Terrak, M. Nguyen-Distèche, 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 septalion activity on the folded structure. J. Bacteriol. 178:5402-5409.
26. Guzman, L. M., J. J. Barondess, and J. Beckwith. 1992. FtsL, an essential cytoplasmic membrane protein involved in cell division in Escherichia coli. J. Bacteriol. 174:7716-7728.
27. BAD promoter. J. Bacteriol. 177:4121-4130.
28. 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.
29. 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. Cell 88:175-185.
30. Harry, E. J., and R. G. Wake. 1997. The membrane-bound cell division protein DivIB is localized to the division site in Bacillus subtilis. Mol. Microbiol. 25:275-283.
31. Heim, R., D. C. Prasher, and R. Y. Tsien. 1994. Wavelength mutations and posttranslational autoxidation of green fluorescent protein. Proc. Natl. Acad. Sci. USA 91:12501-12504.
32. Höltje, J. V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
33. Huisman, O., R. D'Ari, and S. Gottesman. 1984. Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc. Natl. Acad. Sci. USA 81:4490-4494.
34. Katis, V. L., E. J. Harry, and R. G. Wake. 1997. The Bacillus subtilis division protein DivIC is a highly abundant membrane-bound protein that localizes to the division site. Mol. Microbiol. 26:1047-1055.
35. Levin, P. A., and R. Losick. 1996. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes Dev. 10:478-488.
36. Levin, P. A., R. Losick, P. Stragier, and F. Arigoni. 1997. Localization of the sporulation protein SpoIIE in Bacillus subtilis is dependent upon the cell division protein FtsZ. Mol. Microbiol. 25:839-846.
37. Lutkenhaus, J., and S. G. Addinall. 1997. Bacterial cell division and the Z ring. Annu. Rev. Biochem. 66:93-116.
38. Ma, X., D. W. Ehrhardt, and W. Margolin. 1996. Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc. Natl. Acad. Sci. USA 93:12998-13003.
39. Ma, X., Q. Sun, R. Wang, G. Singh, E. L. Jonietz, and W. Margolin. 1997. Interactions between heterologous FtsA and FtsZ proteins at the FtsZ ring. J. Bacteriol. 179:6788-6797.
40. 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, Cold Spring Harbor, N.Y.
41. Munro, S. 1995. Localization of proteins to the Golgi apparatus. Trends Cell Biol. 8:11-15.
42. Nakamura, M., I. N. Maruyama, M. Soma, J. Kato, H. Suzuki, and Y. Horota. 1983. On the process of cellular division in Escherichia coli: nucleotide sequence of the gene for penicillin-binding protein 3. Mol. Gen. Genet. 191:1-9.
43. Nanninga, N. 1998. Morphogenesis of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:110-129.
44. Nguyen-Distèche, 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.
45. 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.
46. 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.
47. Pogliano, K., E. Harry, and R. Losick. 1995. Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol. Microbiol. 18:459-170.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
49. Shere, K. D., S. Sallustio, A. Manessis, T. G. D'Aversa, and M. B. Goldberg. 1997. Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol. Microbiol. 25:451-162.
50. 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.
51. Spratt, B. G., and A. B. Pardee. 1975. Penicillin-binding proteins and cell shape in E. coli. Nature 254:516-517.
52. Strauch, K. L., and J. Beckwith. 1988. An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. Natl. Acad. Sci. USA 85:1576-1580.
53. Wang, L., M. K. Khattar, W. D. Donachie, and J. Lutkenhaus. 1998. FtsI and FtsW are localized to the septum in Escherichia coli. J. Bacteriol. 180:2810-2816.
54. Wang, X., J. Huang, A. Mukherjee, C. Cao, and J. Lutkenhaus. 1997. Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J. Bacteriol. 179: 5551-5559.
55. Wang, X., and J. Lutkenhaus. 1993. The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration. Mol. Microbiol. 9:435-442.
56. Ward, J. J., and J. Lutkenhaus. 1985. Overproduction of FtsZ induces minicell formation in E. coli. Cell 42:941-949.
57. Weiss, D. S., K. Pogliano, M. Carson, L. M. Guzman, C. Fraipont, M. Nguyen-Distèche, 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.
58. Wientjes, F. B., and N. Nanninga. 1989. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171:3412-3419.
59. Yu, X. C., A. H. Tran, Q. Sun, and W. Margolin. 1998. Localization of cell division protein FtsK to the Escherichia coli septum and identification of a potential N-terminal targeting domain. J. Bacteriol. 180:1296-1304.