The C-terminus of MinE from Neisseria gonorrhoeae acts as a topological specificity factor by modulating MinD activity in bacterial cell division

Research in Microbiology

Volumn 157, Issue 4, 2006, Pages 333-344

  Eng, Nelson F ^a   Szeto, Jason ^a   Acharya, Sudeep ^a   Tessier, Daniel ^a   Dillon, Jo Anne R ^a,b  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Cell division; MinD; MinE; Neisseria gonorrhoeae; Polymeric array

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; MIND PROTEIN; MUTANT PROTEIN; PROTEIN MINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL CELL; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ESCHERICHIA COLI; NEISSERIA GONORRHOEAE; NONHUMAN; OSCILLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CELL DIVISION; ENZYME ACTIVATION; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEISSERIA GONORRHOEAE;

EID: 33646026711     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2005.09.005     Document Type: Article

References (38)

1. Chen J.C., and Beckwith J. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42 (2001) 395-413
2. Clontech Laboratories I. Clontech Yeast Protocols Handbook (1999), Clontech Laboratories, Palo Alto, CA
3. Corbin B.D., Yu X.C., and Margolin W. Exploring intracellular space: Function of the Min system in round-shaped Escherichia coli. EMBO J. 21 (2002) 1998-2008
4. de Boer P., Crossley R., and Rothfield L. Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli. J. Bacteriol. 170 (1988) 2106-2112
5. de Boer P., and Crossley R. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in Escherichia coli. Cell 56 (1989) 641-649
6. de Boer P., Crossley R.E., Hand A.R., and Rothfield L. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10 (1991) 4371-4380
7. Fu X., Shih Y.-L., Zhang Y., and Rothfield L.I. The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc. Natl. Acad. Sci. USA 98 (2001) 980-985
8. Gitai Z., and Shapiro L. Bacterial cell division spirals into control. Proc. Natl. Acad. Sci. USA 100 (2003) 7423-7424
9. Harder K.W., Owen P., Wong L.K., Aebersold R., Clark-Lewis I., and Jirik F.R. Characterization and kinetic analysis of the intracellular domain of human protein tyrosine phosphatase beta (HPTP beta) using synthetic phosphopeptides. Biochem. J. 298 (1994) 395-401
10. Hu Z., and Lutkenhaus J. Topological regulation of cell division in E. coli: Spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol. Cell 7 (2001) 1337-1343
11. Hu Z., Gogol E.P., and Lutkenhaus J. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. USA 99 (2002) 6761-6766
12. Hu Z., and Lutkenhaus J. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 47 (2003) 345-355
13. Huang J., Cao C., and Lutkenhaus J. Interaction between FtsZ and inhibitors of cell division. J. Bacteriol. 178 (1996) 5080-5085
14. Huang K.C., Meir Y., and Wingreen N.S. Dynamic structures in Escherichia coli: Spontaneous formation of MinE rings and MinD polar zones. Proc. Natl. Acad. Sci. USA 100 (2003) 12724-12728
15. King G.F., Rowland S.L., Pan B., Mackay J.P., Mullen G.P., and Rothfield L.I. The dimerization and topological specificity functions of MinE reside in a structurally autonomous C-terminal domain. Mol. Microbiol. 31 (1999) 1161-1169
16. King G.F., Shih Y.L., Maciejewski M.W., Bains N.P., Pan B., Rowland S.L., Mullen G.P., and Rothfield L.I. Structural basis for the topological specificity function of MinE. Nat. Struct. Biol. 7 (2000) 1013-1017
17. Krogsgaard M., Prado N., Adams E.J., He X.L., Chow D.C., Wilson D.B., Gar K.C., and Davis M.M. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 12 (2003) 1367-1378
18. Lackner L.L., Raskin D.M., and de Boer P.A. ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J. Bacteriol. 185 (2003) 735-749
19. Ma L.Y., King G., and Rothfield L. Mapping the MinE site involved in interaction with the MinD division site selection protein of Escherichia coli. J. Bacteriol. 185 (2003) 4948-4955
20. Mileykovskaya E., Fishov I., Fu X., Corbin B.D., Margolin W., and Dowhan W. Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J. Biol. Chem. 278 (2003) 22193-22198
21. Miroux B., and Walker J.E. Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260 (1996) 289-298
22. Pichoff S., and Lutkenhaus J. Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J. Bacteriol. 183 (2001) 6630-6635
23. Ramirez-Arcos S., Szeto J., Beveridge T.J., Victor C., Francis F., and Dillon J.R. Deletion of the cell division inhibitor MinC results in lysis of Neisseria gonorrhoeae. Microbiology 147 (2001) 225-237
24. Ramirez-Arcos S., Szeto J., Dillon J.A., and Margolin W. Conservation of dynamic localization among MinD and MinE orthologues: Oscillation of Neisseria gonorrhoeae proteins in Escherichia coli. Mol. Microbiol. 46 (2002) 493-504
25. Ramirez-Arcos S., Greco V., Douglas H., Tessier D., Fan D., Szeto J., Wang J., and Dillon J.R. Conserved glycines in the C terminus of MinC proteins are implicated in their functionality as cell division inhibitors. J. Bacteriol. 186 (2004) 2841-2855
26. Raskin D.M., and de Boer P.A.J. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96 (1999) 4971-4976
27. Raskin D.M., and de Boer P.A.J. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181 (1999) 6419-6424
28. Rowland S.L., Fu X., Sayed M.A., Zhang Y., Cook W.R., and Rothfield L.I. Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J. Bacteriol. 182 (2000) 613-619
29. Shih Y.L., Fu X., King G.F., Le T., and Rothfield L. Division site placement in E. coli: Mutations that prevent formation of the MinE ring lead to loss of the normal midcell arrest of growth of polar MinD membrane domains. EMBO J. 21 (2002) 3347-3357
30. Shih Y.L., Le T., and Rothfield L. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc. Natl. Acad. Sci. USA 100 (2003) 7865-7870
31. Szeto J., Ramirez-Arcos S., Raymond C., Hicks L.D., Kay C.M., and Dillon J.R. Gonococcal MinD affects cell division in Neisseria gonorrhoeae and Escherichia coli and exhibits a novel self-interaction. J. Bacteriol. 183 (2001) 6253-6264
32. Szeto J., Eng N.F., Acharya S., Rigden M.D., and Dillon J.R. A conserved polar region in the cell division site determinant MinD is required for responding to MinE-induced oscillation, but not for localization within coiled arrays. Res. Microbiol. 156 (2005) 17-29
33. Szeto J., Acharya S., Eng N.F., and Dillon J.R. The N terminus of MinD contains determinants which affect its dynamic localization and enzymatic activity. J. Bacteriol. 186 (2004) 7175-7185
34. Szeto T.H., Rowland S.L., Rothfield L.I., and King G.F. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc. Natl. Acad. Sci. USA 99 (2002) 15693-15698
35. Thanedar S., and Margolin W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14 (2004) 1167-1173
36. Woldringh C.L., Mulder E., Valkenburg J.A., Wientjes F.B., Zaritsky A., and Nanninga N. Role of the nucleoid in the toporegulation of division. Res. Microbiol. 141 (1990) 39-49
37. Zhao C.-R., de Boer P.A.J., and Rothfield L.I. Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc. Natl. Acad. Sci. USA 92 (1995) 4313-4317
38. Zhou H., and Lutkenhaus J. The switch I and II regions of MinD are required for binding and activating MinC. J. Bacteriol. 186 (2004) 1546-1555