Site-directed fluorescence labeling reveals a revised N-terminal membrane topology and functional periplasmic residues in the Escherichia coli cell division protein FtsK

Journal of Biological Chemistry

Volumn 289, Issue 34, 2014, Pages 23287-23301

  Berezuk, Alison M ^a   Goodyear, Mara ^a   Khursigara, Cezar M ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; CELL PROLIFERATION; CELLS; CYTOLOGY; ESCHERICHIA COLI; FLUORESCENCE; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; MEMBRANES; PROTEINS;

CHROMOSOME SEGREGATION; ESCHERICHIA COLI CELLS; FLUORESCENCE LABELING; INTEGRAL MEMBRANE PROTEINS; N-TERMINAL DOMAINS; PROTEIN INTERACTION; THIRD AND FOURTH TRANSMEMBRANE DOMAINS; TRANSMEMBRANE SEGMENTS;

TOPOLOGY;

BACTERIAL PROTEIN; PROTEIN FTSK; UNCLASSIFIED DRUG; CYSTEINE; ESCHERICHIA COLI PROTEIN; FLUORESCENT DYE; FTSK PROTEIN, E COLI; MEMBRANE PROTEIN; PRIMER DNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CELL DIVISION; CELL GROWTH; CELL SIZE; CELL WALL; CHEMICAL LABELING; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; FLUORESCENCE ANALYSIS; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSMISSION ELECTRON MICROSCOPY; CELL MEMBRANE; CHEMISTRY; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING;

BASE SEQUENCE; BLOTTING, WESTERN; CELL MEMBRANE; CYSTEINE; DNA PRIMERS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENT DYES; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, SITE-DIRECTED; PERIPLASM; POLYMERASE CHAIN REACTION;

EID: 84906569009     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.569624     Document Type: Article

References (69)

1. Nordström, K., Bernander, R., and Dasgupta, S. (1991) The Escherichia coli cell cycle: one cycle or multiple independent processes that are coordinated? Mol. Microbiol. 5, 769-774
2. Errington, J., Daniel, R. A., and Scheffers, D.-J. (2003) Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52-65
3. Typas, A., Banzhaf, M., Gross, C. A., and Vollmer, W. (2012) From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10, 123-136
4. Goehring, N. W., and Beckwith, J. (2005) Diverse paths to midcell: assem-bly of the bacterial cell division machinery. Curr. Biol. 15, R514-R526
5. Lutkenhaus, J., Pichoff, S., and Du, S. (2012) Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton 69, 778-790
6. Thanbichler, M. (2010) Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harb. Perspect. Biol. 2, a000331
7. Begg, K. J., Dewar, S. J., and Donachie, W. D. (1995) A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177, 6211-6222
8. Liu, G., Draper, G. C., and Donachie, W. D. (1998) FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol. Microbiol. 29, 893-903
9. Demarre, G., Galli, E., and Barre, F. X. (2013) in DNA Helicases and DNA Motor Proteins (Spies, M., ed) pp. 245-262, Springer, New York
10. Bigot, S., Sivanathan, V., Possoz, C., Barre, F.-X., and Cornet, F. (2007) FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64, 1434-1441
11. Barre, F.-X. (2007) FtsK and SpoIIIE: the tale of the conserved tails. Mol. Microbiol. 66, 1051-1055
12. Burton, B., and Dubnau, D. (2010) Membrane-Associated DNA transport machines. Cold Spring Harb. Perspect. Biol. 2, a000406
13. Wu, L. J., and Errington, J. (1994) Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264, 572-575
14. Draper, G. C., McLennan, N., Begg, K., Masters, M., and Donachie, W. D. (1998) Only the N-terminal domain of FtsK functions in cell division. J. Bacteriol. 180, 4621-4627
15. Yu, X.-C., Tran, A. H., Sun, Q., and Margolin, W. (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
16. Wang, L., and Lutkenhaus, J. (1998) FtsK is an essential cell division protein that is localized to the septum and induced as part of the SOS response. Mol. Microbiol. 29, 731-740
17. Dubarry, N., Possoz, C., and Barre, F.-X. (2010) Multiple regions along the Escherichia coli FtsK protein are implicated in cell division. Mol. Microbiol. 78, 1088-1100
18. Yu, X.-C., Weihe, E. K., and Margolin, W. (1998) Role of the C terminus of FtsK in Escherichia coli chromosome segregation. J. Bacteriol. 180, 6424-6428
19. Steiner, W., Liu, G., Donachie, W. D., and Kuempel, P. (1999) The cytoplasmic domain of FtsK protein is required for resolution of chromosome dimers. Mol. Microbiol. 31, 579-583
20. Massey, T. H., Mercogliano, C. P., Yates, J., Sherratt, D. J., and Löwe, J. (2006) Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol. Cell 23, 457-469
21. Aussel, L., Barre, F.-X., Aroyo, M., Stasiak, A., Stasiak, A. Z., and Sherratt, D. (2002) FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108, 195-205
22. Bigot, S., Saleh, O. A., Lesterlin, C., Pages, C., El Karoui, M., Dennis, C., Grigoriev, M., Allemand, J.-F., Barre, F.-X., and Cornet, F. (2005) KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 24, 3770-3780
23. Dubarry, N., and Barre, F.-X. (2010) Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK. EMBO J. 29, 597-605
24. Grainge, I. (2010) FtsK-A bacterial cell division checkpoint? Mol. Microbiol. 78, 1055-1057
25. Grenga, L., Luzi, G., Paolozzi, L., and Ghelardini, P. (2008) The Escherichia coli FtsK functional domains involved in its interaction with its divisome protein partners. FEMS Microbiol. Lett. 287, 163-167
26. Di Lallo, G., Fagioli, M., Barionovi, D., Ghelardini, P., and 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
27. Bi, E., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164
28. Mukherjee, A., Dai, K., and Lutkenhaus, J. (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl. Acad. Sci. U.S.A. 90, 1053-1057
29. Erickson, H. P. (1995) FtsZ, a prokaryotic homolog of tubulin? Cell 80, 367-370
30. Erickson, H. P., Anderson, D. E., and Osawa, M. (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74, 504-528
31. Begg, K. J., Hatfull, G. F., and Donachie, W. D. (1980) Identification of new genes in a cell envelope-cell division gene cluster of Escherichia coli: cell division gene ftsQ. J. Bacteriol. 144, 435-437
32. D'Ulisse, V., Fagioli, M., Ghelardini, P., and Paolozzi, L. (2007) Three functional subdomains of the Escherichia coli FtsQ protein are involved in its interaction with the other division proteins. Microbiology 153, 124-138
33. van den Ent, F., Vinkenvleugel, T. M. F., Ind, A., West, P., Veprintsev, D., Nanninga, N., den Blaauwen, T., and Löwe, J. (2008) Structural and mutational analysis of the cell division protein FtsQ. Mol. Microbiol. 68, 110-123
34. Buddelmeijer, N., and Beckwith, J. (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
35. Guzman, L.-M., Barondess, J. J., and Beckwith, J. (1992) FtsL, an essential cytoplasmic membrane protein involved in cell division in Escherichia coli. J. Bacteriol. 174, 7716-7728
36. Spratt, B. G. (1975) Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl. Acad. Sci. U.S.A. 72, 2999-3003
37. Botta, G. A., and Park, J. T. (1981) Evidence for involvement of penicillinbinding protein 3 in murein synthesis during septation but not during cell elongation. J. Bacteriol. 145, 333-340
38. Dorazi, R., and Dewar, S. J. (2000) Membrane topology of the N terminus of the Escherichia coli FtsK division protein. FEBS Lett. 478, 13-18
39. Bogdanov, M., Zhang, W., Xie, J., and Dowhan, W. (2005) Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAM): application to lipid-specific membrane protein topogenesis. Methods 36, 148-171
40. Geissler, B., and Margolin, W. (2005) Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol. Microbiol. 58, 596-612
41. Potluri, L.-P., Kannan, S., and Young, K. D. (2012) ZipA is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J. Bacteriol. 194, 5334-5342
42. Culham, D. E., Hillar, A., Henderson, J., Ly, A., Vernikovska, Y. I., Racher, K. I., Boggs, J. M., and Wood, J. M. (2003) Creation of a fully functional cysteine-less variant of osmosensor and proton-osmoprotectant symporter ProP from Escherichia coli and its application to assess the transporter's membrane orientation. Biochemistry 42, 11815-11823
43. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
44. Tusnády, G. E., and Simon, I. (1998) Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489-506
45. Tusnády, G. E., and Simon, I. (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849-850
46. Hiraga, S., Ichinose, C., Niki, H., and Yamazoe, M. (1998) Cell cycle-dependent duplication and bidirectional migration of SeqA-Associated DNA-protein complexes in E. coli. Mol. Cell 1, 381-387
47. Beveridge, T. J., Moyles, D., and Harris, B. (2007) in Methods for General and Molecular Microbiology (Reddy, C. A., Beveridge, T. J., Breznak, J. A., Marzluf, G., Schmidt, T. M., and Snyder, L. R., eds) 3rd Ed., pp. 54-81, American Society for Microbiology Press, Washington, D. C.
48. Kuru, E., Hughes, H. V., Brown, P. J., Hall, E., Tekkam, S., Cava, F., de Pedro, M. A., Brun, Y. V., and VanNieuwenhze, M. S. (2012) In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-Amino acids. Angew. Chem. Int. Ed. Engl. 51, 12519-12523
49. Ye, L., Jia, Z., Jung, T., and Maloney, P. C. (2001) Topology of OxlT, the oxalate transporter of Oxalobacter formigenes, determined by site-directed fluorescence labeling. J. Bacteriol. 183, 2490-2496
50. Wood, J. M., Culham, D. E., Hillar, A., Vernikovska, Y. I., Liu, F., Boggs, J. M., and Keates, R. A. B. (2005) A structural model for the osmosensor, transporter, and osmoregulator ProP of Escherichia coli. Biochemistry 44, 5634-5646
51. Larue, K., Ford, R. C., Willis, L. M., and Whitfield, C. (2011) Functional and structural characterization of polysaccharide co-polymerase proteins required for polymer export in ATP-binding cassette transporter-dependent capsule biosynthesis pathways. J. Biol. Chem. 286, 16658-16668
52. Bisicchia, P., Steel, B., Mariam Debela, M. H., Löwe, J., and Sherratt, D. (2013) The N-terminal membrane-spanning domain of the Escherichia coli DNA translocase FtsK hexamerizes at midcell. MBio 4, e00800-e00813
53. Chou, P. Y., and Fasman, G. D. (1974) Conformational parameters for amino acids in helical, β-sheet, and random coil regions calculated from proteins. Biochemistry 13, 211-222
54. Chou, P. Y., and Fasman, G. D. (1974) Prediction of protein conformation. Biochemistry 13, 222-245
55. Wang, X., Possoz, C., and Sherratt, D. J. (2005) Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev. 19, 2367-2377
56. Chen, J. C., and Beckwith, J. (2001) FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42, 395-413
57. Rothfield, L. (2003) New insights into the developmental history of the bacterial cell division site. J. Bacteriol. 185, 1125-1127
58. Strauss, M. P., Liew, A. T. F., Turnbull, L., Whitchurch, C. B., Monahan, L. G., and Harry, E. J. (2012) 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol. 10, e1001389
59. Allard, J. F., and Cytrynbaum, E. N. (2009) Force generation by a dynamic Z-ring in Escherichia coli cell division. Proc. Natl. Acad. Sci. U.S.A. 106, 145-150
60. Lan, G., Daniels, B. R., Dobrowsky, T. M., Wirtz, D., and Sun, S. X. (2009) Condensation of FtsZ filaments can drive bacterial cell division. Proc. Natl. Acad. Sci. U.S.A. 106, 121-126
61. Osawa, M., Anderson, D. E., and Erickson, H. P. (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320, 792-794
62. Addinall, S. G., Bi, E., and Lutkenhaus, J. (1996) FtsZ ring formation in fts mutants. J. Bacteriol. 178, 3877-3884
63. Sun, Q., and Margolin, W. (1998) FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180, 2050-2056
64. Heidrich, C., Ursinus, A., Berger, J., Schwarz, H., and Höltje, J.-V. (2002) Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184, 6093-6099
65. Wientjes, F. B., and Nanninga, N. (1989) Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171, 3412-3419
66. Pogliano, J., Pogliano, K., Weiss, D. S., Losick, R., and Beckwith, J. (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. U.S.A. 94, 559-564
67. Nanninga, N. (1991) Cell division and peptidoglycan assembly in Escherichia coli. Mol. Microbiol. 5, 791-795
68. Lesterlin, C., Pages, C., Dubarry, N., Dasgupta, S., and Cornet, F. (2008) Asymmetry of chromosome replichores renders the DNA translocase activity of FtsK essential for cell division and cell shape maintenance in Escherichia coli. PLoS Genet. 4, e1000288
69. Diez, A. A., Farewell, A., Nannmark, U., and Nyström, T. (1997) A mutation in the ftsK gene of Escherichia coli affects cell-cell separation, stationary-phase survival, stress adaptation, and expression of the gene encoding the stress protein UspA. J. Bacteriol. 179, 5878-5883