A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN

Molecular Microbiology

Volumn 92, Issue 6, 2014, Pages 1212-1226

  Busiek, Kimberly K ^a   Margolin, William ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDASE; CELL CYCLE PROTEIN; FTSI PROTEIN; PROTEIN FTSA; PROTEIN FTSN; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; FTSA PROTEIN, E COLI; FTSN PROTEIN, E COLI; MEMBRANE PROTEIN; PEPTIDOGLYCAN;

ARTICLE; BACTERIAL GENE; BINDING SITE; CELL DIVISION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; ESCHERICHIA COLI; FTSN GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; CELL WALL; ENZYMOLOGY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

CELL DIVISION; CELL WALL; DNA MUTATIONAL ANALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PEPTIDOGLYCAN; PROTEIN STRUCTURE, TERTIARY;

EID: 84902001403     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12623     Document Type: Article

References (42)

1. Aarsman, M.E., Piette, A., Fraipont, C., Vinkenvleugel, T.M., Nguyen-Disteche, M., and 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., and Lutkenhaus, J. (1997) FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol 25: 303-309.
3. Alexeeva, S., Gadella, T.W., Jr, Verheul, J., Verhoeven, G.S., and den Blaauwen, T. (2010) Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77: 384-398.
4. Arends, S.J., Williams, K., Scott, R.J., Rolong, S., Popham, D.L., and Weiss, D.S. (2010) Discovery and characterization of three new Escherichia coli septal ring proteins that contain a SPOR domain: DamX, DedD, and RlpA. J Bacteriol 192: 242-255.
5. Bernard, C.S., Sadasivam, M., Shiomi, D., and Margolin, W. (2007) An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol 64: 1289-1305.
6. Bi, E., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
7. Busiek, K.K., Eraso, J.M., Wang, Y., and Margolin, W. (2012) The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J Bacteriol 194: 1989-2000.
8. Chung, H.S., Yao, Z., Goehring, N.W., Kishony, R., Beckwith, J., and Kahne, D. (2009) Rapid beta-lactam-induced lysis requires successful assembly of the cell division machinery. Proc Natl Acad Sci USA 106: 21872-21877.
9. Corbin, B.D., Geissler, B., Sadasivam, M., and Margolin, W. (2004) Z-ring-independent interaction between a subdomain of FtsA and late septation proteins as revealed by a polar recruitment assay. J Bacteriol 186: 7736-7744.
10. Dai, K., Xu, Y., and 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.
11. Dai, K., Xu, Y., and Lutkenhaus, J. (1996) Topological characterization of the essential Escherichia coli cell division protein FtsN. J Bacteriol 178: 1328-1334.
12. Ding, Z., Zhao, Z., Jakubowski, S.J., Krishnamohan, A., Margolin, W., and Christie, P.J. (2002) A novel cytology-based, two-hybrid screen for bacteria applied to protein-protein interaction studies of a Type IV secretion system. J Bacteriol 184: 5572-5582.
13. Edwards, D.H., Thomaides, H.B., and Errington, J. (2000) Promiscuous targeting of Bacillus subtilis cell division protein DivIVA to division sites in Escherichia coli and fission yeast. EMBO J 19: 2719-2727.
14. Erickson, H.P. (1997) FtsZ, a tubulin homologue in prokaryote division. Trends Cell Biol 7: 362-367.
15. Garza, I., and Christie, P.J. (2013) A putative transmembrane leucine zipper of Agrobacterium VirB10 is essential for T-pilus biogenesis but not type IV secretion. J Bacteriol 195: 3022-3034.
16. 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.
17. Geissler, B., Elraheb, D., and Margolin, W. (2003) A gain of function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc Natl Acad Sci USA 100: 4197-4202.
18. Gerding, M.A., Liu, B., Bendezu, F.O., Hale, C.A., Bernhardt, T.G., and 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.
19. Goehring, N.W., and Beckwith, J. (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15: 514-526.
20. Goehring, N.W., Gueiros-Filho, F., and 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.
21. Goehring, N.W., Petrovska, I., Boyd, D., and Beckwith, J. (2007) Mutants, suppressors, and wrinkled colonies: Mutant alleles of the cell division gene ftsQ point to functional domains in FtsQ and a role for domain 1C of FtsA in divisome assembly. J Bacteriol 189: 633-645.
22. Guzman, L.M., Belin, D., Carson, M.J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130.
23. Guzman, L.M., Weiss, D.S., and Beckwith, J. (1997) Domain-swapping analysis of FtsI, FtsL, and FtsQ, bitopic membrane proteins essential for cell division in Escherichia coli. J Bacteriol 179: 5094-5103.
24. Karimova, G., Dautin, N., and 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.
25. Lutkenhaus, J. (2009) FtsN - trigger for septation. J Bacteriol 191: 7381-7382.
26. Ma, X., Ehrhardt, D.W., and Margolin, W. (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.
27. Muller, P., Ewers, C., Bertsche, U., Anstett, M., Kallis, T., Breukink, E., etal. (2007) The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem 282: 36394-36402.
28. Peters, N.T., Dinh, T., and Bernhardt, T.G. (2011) A fail-safe mechanism in the septal ring assembly pathway generated by the sequential recruitment of cell separation amidases and their activators. J Bacteriol 193: 4973-4983.
29. Pichoff, S., and Lutkenhaus, J. (2002) Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J 21: 685-693.
30. Pichoff, S., and Lutkenhaus, J. (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55: 1722-1734.
31. Pichoff, S., Shen, B., Sullivan, B., and Lutkenhaus, J. (2012) FtsA mutants impaired for self-interaction bypass ZipA suggesting a model in which FtsA's self-interaction competes with its ability to recruit downstream division proteins. Mol Microbiol 83: 151-167.
32. Raychaudhuri, D. (1999) ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J 18: 2372-2383.
33. Rico, A.I., Garcia-Ovalle, M., Palacios, P., Casanova, M., and Vicente, M. (2010) Role of Escherichia coli FtsN protein in the assembly and stability of the cell division ring. Mol Microbiol 76: 760-771.
34. Rico, A.I., Krupka, M., and Vicente, M. (2013) In the beginning, Escherichia coli assembled the proto-ring: an initial phase of division. J Biol Chem 288: 20830-20836.
35. Shiomi, D., and Margolin, W. (2007) Dimerization or oligomerization of the actin-like FtsA protein enhances the integrity of the cytokinetic Z ring. Mol Microbiol 66: 1396-1415.
36. Shiomi, D., and Margolin, W. (2008) Compensation for the loss of the conserved membrane targeting sequence of FtsA provides new insights into its function. Mol Microbiol 67: 558-569.
37. Söderström, B., Skoog, K., Blom, H., Weiss, D.S., von Heijne, G., and Daley, D.O. (2014) Disassembly of the divisome in Escherichia coli: Evidence that FtsZ dissociates before compartmentalization. Mol Microbiol 92: 1-9.
38. Thomas, J.D., Daniel, R.A., Errington, J., and Robinson, C. (2001) Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol Microbiol 39: 47-53.
39. Ursinus, A., van den Ent, F., Brechtel, S., de Pedro, M., Holtje, J.V., Löwe, J., and Vollmer, W. (2004) Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli. J Bacteriol 186: 6728-6737.
40. Vicente, M., and Rico, A.I. (2006) The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol 61: 5-8.
41. Weiss, D.S., Chen, J.C., Ghigo, J.M., Boyd, D., and 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.
42. Wissel, M.C., Wendt, J.L., Mitchell, C.J., and Weiss, D.S. (2005) The transmembrane helix of the Escherichia coli division protein FtsI localizes to the septal ring. J Bacteriol 187: 320-328.