A multistranded polymer model explains MinDE dynamics in E. coli cell division

Biophysical Journal

Volumn 93, Issue 4, 2007, Pages 1134-1150

  Cytrynbaum, Eric N ^a   Marshall, Brandon D L ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; MIND PROTEIN; PROTEIN MIN E; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CELL DIVISION; CELL MUTANT; CONTROLLED STUDY; ESCHERICHIA COLI; MATHEMATICAL MODEL; MICROTUBULE; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; POLYMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; STRUCTURE ACTIVITY RELATION; THEORETICAL STUDY; WILD TYPE;

ESCHERICHIA COLI;

EID: 34548255900     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.097162     Document Type: Article

References (70)

1. Margolin, W. 2005. FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6:862-871.
2. Yu, X., and W. Margolin. 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.
3. de Boer, P., R. Crossley, and L. Rothfield. 1992. Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J. Bacteriol. 174:63-70.
4. Hu, Z., A. Mukherjee, S. Pichoff, and J. Lutkenhaus. 1999. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. USA. 96:14819-14824.
5. de Boer, P., R. Crossley, and L. Rothfield. 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.
6. Raskin, D., and P. de Boer. 1999. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181:6419-6424.
7. Hu, Z., and J. Lutkenhaus. 2001. Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol. Cell. 7:1337-1343.
8. Raskin, D., and P. de Boer. 1999. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA. 96:4971-4976.
9. Shih, Y., T. Le, and L. Rothfield. 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. USA. 100:7865-7870.
10. Raskin, D., and P. de Boer. 1997. The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli. Cell. 91:685-694.
11. Hu, Z., E. Gogol, and J. Lutkenhaus. 2002. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. USA. 99:6761-6766.
12. Fu, X., Y. Shih, Y. Zhang, and L. Rothfield. 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. USA. 98:980-985.
13. Hale, C., H. Meinhardt, and P. de Boer. 2001. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 20:1563-1572.
14. Meinhardt, H., and P. de Boer. 2001. Pattern formation in Escherichia coli: amodel for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc. Natl. Acad. Sci. USA. 98:14202-14207.
15. Howard, M., A. Rutenberg, and S. de Vet. 2001. Dynamic compartmentalization of bacteria: accurate division in E. coli. Phys. Rev. Lett. 87:278102.
16. Kruse, K. 2002. A dynamic model for determining the middle of Escherichia coli. Biophys. J. 82:618-627.
17. Huang, K., Y. Meir, and N. Wingreen. 2003. Dynamic structures in Escherichia coli: spontaneous formation of MinE rings and MinD polar zones. Proc. Natl. Acad. Sci. USA. 100:12724-12728.
18. Howard, M., and A. Rutenberg. 2003. Pattern formation inside bacteria: fluctuations due to the low copy number of proteins. Phys. Rev. Lett. 90:128102.
19. Huang, K., and N. Wingreen. 2004. Min-protein oscillations in round bacteria. Phys. Biol. 1:229-235.
20. Meacci, G., and K. Kruse. 2005. Min-oscillations in Escherichia coli induced by interactions of membrane-bound proteins. Phys. Biol. 2:89-97.
21. Kerr, R., H. Levine, T. Sejnowski, and W. Rappel. 2006. Division accuracy in a stochastic model of Min oscillations in Escherichia coli. Proc. Natl. Acad. Sci. USA. 103:347-352.
22. Pavin, N., H. Paljetak, and V. Krstic. 2006. Min-protein oscillations in Escherichia coli with spontaneous formation of two-stranded filaments in a three-dimensional stochastic reaction-diffusion model. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73:021904.
23. Tostevin, F., and M. Howard. 2006. A stochastic model of Min oscillations in Escherichia coli and Min protein segregation during cell division. Phys. Biol. 3:1-12.
24. Shih, Y., X. Fu, G. King, T. Le, and L. Rothfield. 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.
25. Suefuji, K., R. Valluzzi, and D. R. Chaudhuri. 2002. Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc. Natl. Acad. Sci. USA. 99:16776-16781.
26. Drew, D., M. Osborn, and L. Rothfield. 2005. A polymerization- depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement. Proc. Natl. Acad. Sci. USA. 102:6114-6118.
27. Norris, V., C. Woldringh, and E. Mileykovskaya. 2004. A hypothesis to explain division site selection in Escherichia coli by combining nucleoid occlusion and Min. FEBS Lett. 561:3-10.
28. Mileykovskaya, E., and W. Dowhan. 2000. Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-n-nonyl acridine orange. J. Bacteriol. 182:1172-1175.
29. Mileykovskaya, E., I. Fishov, X. Fu, B. Corbin, W. Margolin, and W. Dowhan. 2003. Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J. Biol. Chem. 278:22193-22198.
30. Fange, D., and J. Elf. 2006. Noise-induced Min phenotypes in E. coli. PLoS Comput. Biol. 2:e80.
31. Kenworthy, A., B. Nichols, C. Remmert, G. Hendrix, M. Kumar, J. Zimmerberg, and J. Lippincott-Schwartz. 2004. Dynamics of putative raft-associated proteins at the cell surface. J. Cell Biol. 165:735-746.
32. Lackner, L., D. Raskin, and P. de Boer. 2003. ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J. Bacteriol. 185:735-749.
33. Holy, T., and S. Leibler. 1994. Dynamic instability of microtubules as an efficient way to search in space. Proc. Natl. Acad. Sci. USA. 91:5682-5685.
34. Hu, Z., C. Saez, and J. Lutkenhaus. 2003. Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J. Bacteriol. 185:196-203.
35. de Boer, P., R. Crossley, A. Hand, and L. Rothfield. 1991. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10:4371-4380.
36. Zhang, Y., S. Rowland, G. King, E. Braswell, and L. Rothfield. 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.
37. Szeto, T., S. Rowland, L. Rothfield, and G. King. 2002. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc. Natl. Acad. Sci. USA. 99:15693-15698.
38. Hu, Z., and J. Lutkenhaus. 2003. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 47:345-355.
39. Lutkenhaus, J., and M. Sundaramoorthy. 2003. MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol. Microbiol. 48:295-303.
40. Sweitzer, S., and J. Hinshaw. 1998. Dynamin undergoes a GTP-dependent conformational change causing vesiculation. Cell. 93:1021-1029.
41. Fygenson, D., J. Marko, and A. Libchaber. 1997. Mechanics of microtubule-based membrane extension. Phys. Rev. Lett. 79:44974500.
42. Bo, L., and R. Waugh. 1989. Determination of bilayer membrane bending stiffness by tether formation from giant, thin-walled vesicles. Biophys. J. 55:509-517.
43. Huang, K., R. Mukhopadhyay, and N. Wingreen. 2006. A curvature-mediated mechanism for localization of lipids to bacterial poles. PLoS Comput. Biol. 2:e151.
44. Lipowsky, R., and R. Dimova. 2003. Domains in membranes and vesicles. J. Phys. Cond. Matter. 15:S31-S45.
45. Edelstein-Keshet, L., and G. Ermentrout. 1998. Models for the length distributions of actin filaments: I. Simple polymerization and fragmentation. Bull. Math. Biol. 60:449-475.
46. Fygenson, D., H. Flyvbjerg, K. Sneppen, A. Libchaber, and S. Leibler. 1995. Spontaneous nucleation of microtubules. Phys. Rev. E Stat. Nonlin. Soft Matter. Phys. 51:5058-5063.
47. Zhao, C., P. de Boer, and L. Rothfield. 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. USA. 92:4313-4317.
48. Pichoff, S., B. Vollrath, C. Touriol, and J. Bouche. 1995. Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli. Mol. Microbiol. 18:321-329.
49. King, G., Y. Shih, M. Maciejewski, N. Bains, B. Pan, S. Rowland, G. Mullen, and L. Rothfield. 2000. Structural basis for the topological specificity function of MinE. Nat. Struct. Biol. 7:1013-1017.
50. Zhou, H., R. Schulze, S. Cox, C. Saez, Z. Hu, and J. Lutkenhaus. 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.
51. Ma, L., G. King, and L. Rothfield. 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.
52. Szeto, J., N. Eng, S. Acharya, M. Rigden, and J. Dillon. 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.
53. Hayashi, I., T. Oyama, and K. Morikawa. 2001. Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. EMBO J. 20:1819-1828.
54. Howard, J. 2001. Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates, Sunderland, MA.
55. Wollman, R., E. Cytrynbaum, J. Jones, T. Meyer, J. Scholey, and A. Mogilner. 2005. Efficient chromosome capture requires a bias in the "search-and-capture" process during mitotic-spindle assembly. Curr. Biol. 15:828-832.
56. Rowland, S., X. Fu, M. Sayed, Y. Zhang, W. Cook, and L. Rothfield. 2000. Membrane redistribution of the Escherichia coli MinD protein induced by MinE. J. Bacteriol. 182:613-619.
57. VanBuren, V., L. Cassimeris, and D. Odde. 2005. Mechanochemical model of microtubule structure and self-assembly kinetics. Biophys. J. 89:2911-2926.
58. Garner, E., C. Campbell, and R. Mullins. 2004. Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science. 306:1021-1025.
59. Gillespie, D. 1976. General method for numerically simulating stochastic time evolution of coupled chemical-reactions. Phys. Rev. Lett. 22:403-434.
60. Carlier, M., R. Melki, D. Pantaloni, T. Hill, and Y. Chen. 1987. Synchronous oscillations in microtubule polymerization. Proc. Natl. Acad. Sci. USA. 84:5257-5261.
61. Pirollet, F., D. Job, R. Margolis, and J. Garel. 1987. An oscillatory mode for microtubule assembly. EMBO J. 6:3247-3252.
62. Marx, A., and E. Mandelkow. 1994. A model of microtubule oscillations. Eur. Biophys. J. 22:405-421.
63. Sept, D., H. Limbach, H. Bolterauer, and J. Tuszynski. 1999. A chemical kinetics model for microtubule oscillations. J. Theor. Biol. 197:77-88.
64. Gonze, D., J. Halloy, and A. Goldbeter. 2002. Robustness of circadian rhythms with respect to molecular noise. Proc. Natl. Acad. Sci. USA. 99:673-678.
65. Sun, Q., and W. Margolin. 2001. Influence of the nucleoid on placement of FtsZ and MinE rings in Escherichia coli. J. Bacteriol. 183:1413-1422.
66. Evans, E., and W. Rawicz. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64:2094-2097.
67. Fournier, L., and B. Joos. 2003. Lattice model for the kinetics of rupture of fluid bilayer membranes. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 67:051908.
68. Elowitz, M., M. Surette, P. Wolf, J. Stock, and S. Leibler. 1999. Protein mobility in the cytoplasm of Escherichia coli. J. Bacteriol. 181:197-203.
69. Meacci, G., J. Ries, E. Fischer-Friedrich, N. Kahya, P. Schwille, and K. Kruse. 2006. Mobility of Min-proteins in Escherichia coli measured by fluorescence correlation spectroscopy. Phys. Biol. 3:255-263.
70. Stricker, J., P. Maddox, E. Salmon, and H. Erickson. 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA. 99:3171-3175.