Conformation of the cell division regulator MinE: Evidence for interactions between the topological specificity and anti-MinCD domains

Biochemistry

Volumn 45, Issue 14, 2006, Pages 4593-4601

  Ramos, Dennis ^a   Ducat, Thierry ^a   Cheng, Jenny ^a   Eng, Nelson F ^a   Dillon, Jo Anne R ^a,b   Goto, Natalie K ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BACTERIOLOGY; BIOLOGICAL MEMBRANES; CYTOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CELL DIVISION; MUTATIONS; STRUCTURAL ASSOCIATION; STRUCTURAL PERTURBATIONS; TOPOLOGICAL SPECIFICITY;

CELL CULTURE;

MINC PROTEIN; MIND PROTEIN; PROTEIN INHIBITOR; PROTEIN MINE; REGULATOR PROTEIN; SOLVENT; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; COMPLEX FORMATION; GENE MUTATION; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL CYCLE PROTEINS; CIRCULAR DICHROISM; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

NEGIBACTERIA; NEISSERIA GONORRHOEAE;

EID: 33645678291     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060022j     Document Type: Article

References (48)

1. Nanninga, N. (1998) Morphogenesis of Escherichia coli, Microbiol. Mol. Biol. Rev. 62, 110-129.
2. Westling-Haggstrom, B., Elmros, T., Normark, S., and Winblad, B. (1977) Growth pattern and cell division in Neisseria gonorrhoeae, J. Bacteriol. 129, 333-342.
3. Fitz-James, P. (1964) Thin sections of dividing Neisseria gonorrhoeae, J. Bacteriol. 87, 1477-1482.
4. Yu, X. C., and Margolin, W. (1999) FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization, Mol. Microbiol. 32, 315-326.
5. Mulder, E., and Woldringh, C. L. (1989) Actively replicating nucleoids influence positioning of division sites in Escherichia coli filaments forming cells lacking DNA, J. Bacteriol. 171, 4303-4314.
6. Ramirez-Arcos, S., Szeto, J., Beveridge, T. J., Victor, C., Francis, F., and Dillon, J. A. R. (2001) Deletion of the cell-division inhibitor MinC results in lysis of Neisseria gonorrhoeae, Microbiology 147, 225-237.
7. Adler, H. I., Fisher, W. D., Cohen, A., and Hardigree, A. A. (1967) Miniature Escherichia coli cells deficient in DNA, Proc. Natl. Acad. Sci. U.S.A. 57, 321-326.
8. Raskin, D. M., and de Boer, P. A. J. (1997) The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli, Cell 91, 685-694.
9. Yu, X. C., Sun, Q., and Margolin, W. (2001) FtsZ rings in mukB mutants with or without the Min system, Biochimie 83, 125-129.
10. De Boer, P. A. J., Crossley, R. E., and Rothfield, L. I. (1988) Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli, J. Bacteriol. 170, 2106-2112.
11. De Boer, P. A. J., Crossley, R. E., and Rothfield, L. I. (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli, Cell 56, 641-649.
12. Ramirez-Arcos, S., Szeto, J., Dillon, J. A. R., and Margolin, W. (2002) Conservation of dynamic localization among MinD and MinE orthologues: oscillation of Neisseria gonorrhoeae proteins in Escherichia coli, Mol. Microbiol. 46, 493-504.
13. Szeto, J., Acharya, S., Eng, N. F., and Dillon, J. A. R. (2004) The N terminus of MinD contains determinants which affect its dynamic localization and enzymatic activity, J. Bacteriol. 186, 7175-7185.
14. Shih, Y. L., Le, T., and Rothfield, L. (2003) 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. U.S.A. 100, 7865-7870.
15. Szeto, J., Eng, N. F., Acharya, S., Rigden, M. D., and Dillon, J. A. R. (2005) 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, 17-29.
16. Raskin, D. M., and de Boer, P. A. J. (1999) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli, J. Bacteriol. 181, 6419-6424.
17. Raskin, D. M., and de Boer, P. A. J. (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 96, 4971-4976.
18. Corbin, B. D., Yu, X. C., and Margolin, W. (2002) Exploring intracellular space: function of the Min system in round-shaped Escherichia coli, EMBO J. 21, 1998-2008.
19. Margolin, W. (2001) Bacterial cell division: a moving MinE sweeper boggles the MinD, Curr. Biol. 11, R395-R398.
20. Hale, C. A., Meinhardt, H., and de Boer, P. A. J. (2001) Dynamic localization cycle of the cell division regulator MinE in Escherichia coli, EMBO J. 20, 1563-1572.
21. Fu, X. L., Shih, Y. L., Zhang, Y., and Rothfield, L. I. (2001) 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. U.S.A. 98, 980-985.
22. Shih, Y. L., Fu, X. L., King, G. F., Le, T., and Rothfield, L. (2002) 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, 3347-3357.
23. Bi, E., and Lutkenhaus, J. (1993) Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring, J. Bacteriol. 175, 1118-1125.
24. Hu, Z. L., and Lutkenhaus, J. (1999) Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE, Mol. Microbiol. 34, 82-90.
25. Justice, S. S., Garcia-Lara, J., and Rothfield, L. I. (2000) Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery, Mol. Microbiol. 37, 410-423.
26. Lackner, L. L., Raskin, D. M., and de Boer, P. A. J. (2003) ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro, J. Bacteriol. 185, 735-749.
27. Hu, Z. L., Gogol, E. P., and Lutkenhaus, J. (2002) Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE, Proc. Natl. Acad. Sci. U.S.A. 99, 6761-6766.
28. Mileykovskaya, E., Fishov, I., Fu, X. Y., Corbin, B. D., Margolin, W., and Dowhan, W. (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo, J. Biol. Chem. 278, 22193-22198.
29. Suefuji, K., Valluzzi, R., and RayChaudhuri, D. (2002) Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE, Proc. Natl. Acad. Sci. U.S.A. 99, 16776-16781.
30. Ma, L. Y., King, G. F., and Rothfield, L. (2004) Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection, Mol. Microbiol. 54, 99-108.
31. Zhou, H. J., Schulze, R., Cox, S., Saez, C., Hu, Z. L., and Lutkenhaus, J. (2005) Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction, J. Bacteriol. 187, 629-638.
32. De Boer, P. A. J., Crossley, R. E., Hand, A. R., and Rothfield, L. I. (1991) The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site, EMBO J. 10, 4371-4380.
33. Lutkenhaus, J., and Sundaramoorthy, M: (2003) MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation, Mol. Microbiol. 48, 295-303.
34. Zhao, C. R., de Boer, P. A. J., and Rothfield, L. I. (1995) 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. U.S.A. 92, 4313-4317.
35. Pichoff, S., Vollrath, B., Touriol, C., and Bouche, J. P. (1995) Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli, Mol. Microbiol. 18, 321-329.
36. King, G. F., Rowland, S. L., Pan, B., Mackay, J. P., Mullen, G. P., and Rothfield, L. I. (1999) The dimerization and topological specificity functions of MinE reside in a structurally autonomous C-terminal domain, Mol. Microbiol. 31, 1161-1169.
37. King, G. F., Shih, Y. L., Maciejewski, M. W., Bains, N. P. S., Pan, B. L., Rowland, S. L., Mullen, G. P., and Rothfield, L. I. (2000) Structural basis for the topological specificity function of MinE, Nat. Struct, Biol. 7, 1013-1017.
38. Eng, N. F., Szeto, J., Acharya, S., Tessier D., and Dillon J. A. R. (2005) The C-terminus of MinE from Neisseria gonorrhoeae acts as a topological specificity factor by modulating MinD activity in bacterial cell division, Res. Microbiol. (in press).
39. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
40. Johnson, B. A., and Blevins, R. A. (1994) NMR View: A computer program for the visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
41. Kanelis, V., Forman-Kay, J. D., and Kay, L. E. (2001) Multidimensional NMR methods for protein structure determination, IUBMB Life 52, 291-302.
42. Sattler, M., Schleucher, J., and Griesinger, C. (1999) Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients, Prog. Nucl. Magn. Res. Spectrosc. 34, 93-158.
43. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
44. Szeto, J., Ramirez-Arcos, S., Raymond, C., Hicks, L. D., Kay, C. M., and Dillon, J. A. R. (2001) Gonococcal MinD affects cell division in Neisseria gonorrhoeae and Escherichia coli and exhibits a novel self-interaction, J. Bacteriol. 183, 6253-6264.
45. Wishart, D. S., Sykes, B. D., and Richards, F. M. (1992) The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy, Biochemistry 31, 1647-1651.
46. Ma, L. Y., King, G., and Rothfield, L. (2003) Mapping the MinE site involved in interaction with the MinD division site selection protein of Escherichia coli, J. Bacteriol. 185, 4948-4955.
47. Zhang, Y., Rowland, S., King, G., Braswell, E., and Rothfield, L. (1998) The relationship between hetero-oligomer formation and function of the topological specificity domain of the Escherichia coli MinE protein, Mol. Microbiol. 30, 265-273.
48. Hu, Z. L., and Lutkenhaus, J. (2001) Topological regulation of cell division in E. coli. Spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipids, Mol. Cell 7, 1337-1343.