Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET

Molecular Microbiology

Volumn 77, Issue 2, 2010, Pages 384-398

  Alexeeva, Svetlana ^a   Gadella Jr , Theodorus W J ^a   Verheul, Jolanda ^a   Verhoeven, Gertjan S ^b   Den Blaauwen, Tanneke ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b FOM INSTITUTE AMOLF   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI PROTEIN; FTSZ PROTEIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 1B; PENICILLIN BINDING PROTEIN 3; PROTEIN FTSI; PROTEIN FTSN; PROTEIN FTSQ; PROTEIN FTSW; PROTEIN ZAPA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CARBOXYPEPTIDASE TRANSPEPTIDASE; CARRIER PROTEIN; CYTOSKELETON PROTEIN; FTSI PROTEIN, E COLI; FTSN PROTEIN, E COLI; FTSZ PROTEIN, BACTERIA; MEMBRANE PROTEIN; PENICILLIN-BINDING PROTEIN 1B, E COLI; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; ZAPA PROTEIN, E COLI;

ARTICLE; BACTERIAL CELL; CELL DIVISION; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL PROTEINS; CARRIER PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMBRANE PROTEINS; PENICILLIN-BINDING PROTEINS; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE;

EID: 77954376358     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07211.x     Document Type: Article

References (70)

1. Aarsman, M.E.G., Piette, A., Fraipont, C., Vinkenvleugel, T.M., Nguyen-Disteche, M. den Blaauwen, T. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55 : 1631 1645.
2. Addinall, S.G., Cao, C. Lutkenhaus, J. (1997) FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol 25 : 303 309.
3. Anderson, D.E., Gueiros-Filho, F.J. Erickson, H.P. (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 186 : 5775 5781.
4. Bernhard, T. Gottschalk, G. (1978) Cell yields of Escherichia coli during anaerobic growth on fumarate and molecular hydrogen. Arch Microbiol 116 : 235 238.
5. Bertsche, U., Kast, T., Wolf, B., Fraipont, C., Aarsman, M.E., Kannenberg, K., et al. (2006) Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol Microbiol 61 : 675 690.
6. Billinton, N. Knight, A.W. (2001) Seeing the wood through the trees: a review of techniques for distinguishing green fluorescent protein from endogenous autofluorescence. Anal Biochem 291 : 175 197.
7. den Blaauwen, T., de Pedro, M.A., Nguyen-Disteche, M. Ayala, J.A. (2008) Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32 : 321 344.
8. Bramhill, D. Thompson, C.M. (1994) GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci USA 91 : 5813 5817.
9. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A. Tsien, R.Y. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99 : 7877 7882.
10. Chen, J.C., Weiss, D.S., Ghigo, J.M. Beckwith, J. (1999) Septal localization of FtsQ, an essential cell division protein in Escherichia coli. J Bacteriol 181 : 521 530.
11. Chen, Y. Erickson, H.P. (2009) FtsZ filament dynamics at steady state: subunit exchange with and without nucleotide hydrolysis. Biochemistry 48 : 6664 6673.
12. Clegg, R.M. (1992) Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol 211 : 353 388.
13. Clegg, R.M., Murchie, A.I., Zechel, A., Carlberg, C., Diekmann, S. Lilley, D.M. (1992) Fluorescence resonance energy transfer analysis of the structure of the four-way DNA junction. Biochemistry 31 : 4846 4856.
14. Dai, K., Xu, Y. Lutkenhaus, J. (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.
15. Den Blaauwen, T., Buddelmeijer, N., Aarsman, M.E., Hameete, C.M. Nanninga, N. (1999) Timing of FtsZ assembly in Escherichia coli. J Bacteriol 181 : 5167 5175.
16. Den Blaauwen, T., Aarsman, M.E., Vischer, N.O. Nanninga, N. (2003) Penicillin-binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole. Mol Microbiol 47 : 539 547.
17. Di Lallo, G., Fagioli, M., Barionovi, D., Ghelardini, P. Paolozzi, L. (2003) Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149 : 3353 3359.
18. Draper, G.C., McLennan, N., Begg, K., Masters, M. Donachie, W.D. (1998) Only the N-terminal domain of FtsK functions in cell division. J Bacteriol 180 : 4621 4627.
19. Epe, B., Steinhauser, K.G. Woolley, P. (1983) Theory of measurement of Förster-type energy transfer in macromolecules. Proc Natl Acad Sci USA 80 : 2579 2583.
20. Erickson, H.P., Taylor, D.W., Taylor, K.A. Bramhill, D. (1996) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci USA 93 : 519 523.
21. Errington, J., Daniel, R.A. Scheffers, D.J. (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67 : 52 65, table of contents.
22. Fields, S. (2005) High-throughput two-hybrid analysis. The promise and the peril. FEBS J 272 : 5391 5399.
23. Fishov, I., Zaritsky, A. Grover, N.B. (1995) On microbial states of growth. Mol Microbiol 15 : 789 794.
24. Förster, T. (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz (Intermolecular energy migration and fluorescence). Annalen der Physik 2 : 55 75.
25. Gadella, T.W.J. (2009) FRET and FLIM Imaging Techniques.
26. Garrido, T., Sanchez, M., Palacios, P., Aldea, M. Vicente, M. (1993) Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. EMBO J 12 : 3957 3965.
27. Geissler, B. Margolin, W. (2005) Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol Microbiol 58 : 596 612.
28. Gerding, M.A., Liu, B., Bendezu, F.O., Hale, C.A., Bernhardt, T.G. de Boer, P.A. (2009) Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J Bacteriol 191 : 7383 7401.
29. Goehring, N.W. Beckwith, J. (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15 : R514 R526.
30. Goehring, N.W., Gueiros-Filho, F. Beckwith, J. (2005) Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. Genes Dev 19 : 127 137.
31. Goehring, N.W., Robichon, C. Beckwith, J. (2007) Role for the nonessential N terminus of FtsN in divisome assembly. J Bacteriol 189 : 646 649.
32. Gueiros-Filho, F.J. Losick, R. (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16 : 2544 2556.
33. Guerlava, P., Izac, V. Tholozan, J.L. (1998) Comparison of different methods of cell lysis and protein measurements in Clostridium perfringens: application to the cell volume determination. Curr Microbiol 36 : 131 135.
34. Karasawa, S., Araki, T., Nagai, T., Mizuno, H. Miyawaki, A. (2004) Cyan-emitting and orange-emitting fluorescent proteins as a donor/acceptor pair for fluorescence resonance energy transfer. Biochem J 381 : 307 312.
35. Karimova, G., Dautin, N. Ladant, D. (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187 : 2233 2243.
36. Koppelman, C.M., Aarsman, M.E., Postmus, J., Pas, E., Muijsers, A.O., Scheffers, D.J., et al. (2004) R174 of Escherichia coli FtsZ is involved in membrane interaction and protofilament bundling, and is essential for cell division. Mol Microbiol 51 : 645 657.
37. Kremers, G.J. Goedhart, J. (2009) Visible fluorescent proteins for FRET. In FRET and FLIM Imaging Techniques. Gadella, T.W.J. (ed.).
38. Kremers, G.J., Goedhart, J., van Munster, E.B. Gadella, T.W., Jr. (2006) Cyan and yellow super fluorescent proteins with improved brightness, protein folding, and FRET Förster radius. Biochemistry 45 : 6570 6580.
39. Kremers, G.J., Goedhart, J., van den Heuvel, D.J., Gerritsen, H.C. Gadella, T.W., Jr. (2007) Improved green and blue fluorescent proteins for expression in bacteria and mammalian cells. Biochemistry 46 : 3775 3783.
40. Lakowicz, J.R. (2006) Principles of Fluorescence Spectroscopy.
41. Li, I.T., Pham, E. Truong, K. (2006) Protein biosensors based on the principle of fluorescence resonance energy transfer for monitoring cellular dynamics. Biotechnol Lett 28 : 1971 1982.
42. Low, H.H., Moncrieffe, M.C. Lowe, J. (2004) The crystal structure of ZapA and its modulation of FtsZ polymerisation. J Mol Biol 341 : 839 852.
43. 2+-induced FtsZ sheets. EMBO J 18 : 2364 2371.
44. Maggi, S., Massidda, O., Luzi, G., Fadda, D., Paolozzi, L. Ghelardini, P. (2008) Division protein interaction web: identification of a phylogenetically conserved common interactome between Streptococcus pneumoniae and Escherichia coli. Microbiology 154 : 3042 3052.
45. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6 : 862 871.
46. Merzlyak, E.M., Goedhart, J., Shcherbo, D., Bulina, M.E., Shcheglov, A.S., Fradkov, A.F., et al. (2007) Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat Methods 4 : 555 557.
47. Mohammadi, T., Ploeger, G.E., Verheul, J., Comvalius, A.D., Martos, A., Alfonso, C., et al. (2009) The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48 : 11056 11066.
48. Monahan, L.G., Robinson, A. Harry, E.J. (2009) Lateral FtsZ association and the assembly of the cytokinetic Z ring in bacteria. Mol Microbiol 74 : 1004 1017.
49. Mukherjee, A. Lutkenhaus, J. (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176 : 2754 2758.
50. Müller, P., Ewers, C., Bertsche, U., Anstett, M., Kallis, T., Breukink, E., et al. (2007) The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem 282 : 36394 36402.
51. Murchie, A.I., Clegg, R.M., von Kitzing, E., Duckett, D.R., Diekmann, S. Lilley, D.M. (1989) Fluorescence energy transfer shows that the four-way DNA junction is a right-handed cross of antiparallel molecules. Nature 341 : 763 766.
52. Oliva, M.A., Cordell, S.C. Löwe, J. (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11 : 1243 1250.
53. Pastoret, S., Fraipont, C., Blaauwen, T., Wolf, B., Aarsman, M.E., Piette, A., et al. (2004) Functional analysis of the cell division protein FtsW of Escherichia coli. J Bacteriol 186 : 8370 8379.
54. Rico, A.I., Garcia-Ovalle, M., Palacios, P., Casanova, M. Vicente, M. (2010) Role of Escherichia coli FtsN protein in the assembly and stability of the cell division ring. Mol Microbiol 76 : 760 771.
55. Sambrook, J., Maniatis, T. Fritsch, E.F. (1989) Molecular Cloning: A Laboratory Manual.
56. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22 : 1567 1572.
57. Small, E., Marrington, R., Rodger, A., Scott, D.J., Sloan, K., Roper, D., et al. (2007) FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J Mol Biol 369 : 210 221.
58. Sundararaj, S., Guo, A., Habibi-Nazhad, B., Rouani, M., Stothard, P., Ellison, M. Wishart, D.S. (2004) The CyberCell Database (CCDB): a comprehensive, self-updating, relational database to coordinate and facilitate in silico modeling of Escherichia coli. Nucleic Acids Res 32 : D293 D295.
59. Taschner, P.E., Huls, P.G., Pas, E. Woldringh, C.L. (1988) Division behavior and shape changes in isogenic ftsZ, ftsQ, ftsA, pbpB, and ftsE cell division mutants of Escherichia coli during temperature shift experiments. J Bacteriol 170 : 1533 1540.
60. Torriani, A. (1960) Influence of inorganic phosphate in the formation of phosphatases by Escherichia coli. Biochim Biophys Acta 38 : 460 469.
61. Ursinus, A., van den Ent, F., Brechtel, S., de Pedro, M., Holtje, J.V., Lowe, J. Vollmer, W. (2004) Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli. J Bacteriol 186 : 6728 6737.
62. Van Munster, E.B. Gadella, T.W., Jr. (2004) phiFLIM: a new method to avoid aliasing in frequency-domain fluorescence lifetime imaging microscopy. J Microsc 213 : 29 38.
63. Van Munster, E.B. Gadella, T.W.J., Jr. (2005) Fluorescence lifetime imaging microscopy (FLIM). In Microscopic Techniques, Vol. 95. Rietdorf, J. (ed.).
64. Van Munster, E.B., Kremers, G.J., Adjobo-Hermans, M.J. Gadella, T.W., Jr. (2005) Fluorescence resonance energy transfer (FRET) measurement by gradual acceptor photobleaching. J Microsc 218 : 253 262.
65. Vicente, M., Rico, A.I., Martinez-Arteaga, R. Mingorance, J. (2006) Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188 : 19 27.
66. Wang, X., Huang, J., Mukherjee, A., Cao, C. Lutkenhaus, J. (1997) Analysis of the interaction of FtsZ with itself, GTP, and FtsA. J Bacteriol 179 : 5551 5559.
67. Weiss, D.S., Chen, J.C., Ghigo, J.M., Boyd, D. Beckwith, J. (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.
68. Willemse, J. van Wezel, G.P. (2009) Imaging of Streptomyces coelicolor A3(2) with reduced autofluorescence reveals a novel stage of FtsZ localization. PLoS One 4 : e4242.
69. Wissel, M.C. Weiss, D.S. (2004) Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. J Bacteriol 186 : 490 502.
70. Wlodarczyk, J., Woehler, A., Kobe, F., Ponimaskin, E., Zeug, A. Neher, E. (2008) Analysis of FRET signals in the presence of free donors and acceptors. Biophys J 94 : 986 1000.