MinC protein shortens FtsZ protofilaments by preferentially interacting with GDP-bound subunits

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24625-24635

  Hernández Rocamora, Víctor M ^a   García Montañés, Concepción ^a   Reija, Belén ^b   Monterroso, Begoña ^a   Margolin, William ^c   Alfonso, Carlos ^a   Zorrilla, Silvia ^a,b   Rivas, Germán ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; BIOPHYSICAL ANALYSIS; BIOPHYSICAL METHODS; CONCENTRATION-DEPENDENT; FLUORESCENCE ANISOTROPY MEASUREMENTS; FLUORESCENCE CORRELATION SPECTROSCOPY; NARROW DISTRIBUTION; PHYSIOLOGICAL CONDITION;

BINDING ENERGY; CENTRIFUGATION; FLUORESCENCE SPECTROSCOPY; IONIC STRENGTH; MACHINERY; POLYMERIZATION; SITE SELECTION;

PROTEINS;

FTSZ PROTEIN; GUANOSINE DIPHOSPHATE; MINC PROTEIN; POTASSIUM CHLORIDE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; IONIC STRENGTH; MOLECULAR SIZE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PROTOFILAMENT;

BIOPHYSICS; CELL DIVISION; ESCHERICHIA COLI; FTSZ ASSEMBLY; MIN SYSTEM; PROTEIN COMPLEXES; PROTEIN-PROTEIN INTERACTIONS;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GUANOSINE TRIPHOSPHATE; MEMBRANE PROTEINS; MULTIPROTEIN COMPLEXES; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

EID: 84883156185     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.483222     Document Type: Article

References (42)

1. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76, 539-562
2. Hu, Z., Mukherjee, A., Pichoff, S., and Lutkenhaus, J. (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. U.S.A. 96, 14819-14824
3. Harry, E., Monahan, L., and Thompson, L. (2006) Bacterial cell division: the mechanism and its precision. Int. Rev. Cytol. 253, 27-94
4. Raskin, D. M., and de Boer, P. A. (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
5. Loose, M., Fischer-Friedrich, E., Ries, J., Kruse, K., and Schwille, P. (2008) Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320, 789-792
6. Dajkovic, A., Lan, G., Sun, S. X., Wirtz, D., and Lutkenhaus, J. (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr. Biol. 18, 235-244
7. Raskin, D. M., and de Boer, P. A. (1999) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181, 6419-6424
8. Bramkamp, M., and van Baarle, S. (2009) Division site selection in rodshaped bacteria. Curr. Opin. Microbiol. 12, 683-688
9. Mingorance, J., Rivas, G., Vélez, M., Gómez-Puertas, P., and Vicente, M. (2010) Strong FtsZ is with the force: mechanisms to constrict bacteria. Trends Microbiol. 18, 348-356
10. 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
11. Monterroso, B., Alfonso, C., Zorrilla, S., and Rivas, G. (2013) Combined analytical ultracentrifugation, light scattering and fluorescence spectroscopy studies on the functional associations of the bacterial division FtsZ protein. Methods 59, 349-362
12. González, J. M., Jiménez, M., Vélez, M., Mingorance, J., Andreu, J. M., Vicente, M., and Rivas, G. (2003) Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J. Biol. Chem. 278, 37664-37671
13. Rivas, G., Alfonso, C., Jiménez, M., Monterroso, B., and Zorrilla, S. (2013) Macromolecular interactions of the bacterial division FtsZ protein: from quantitative biochemistry and crowding to reconstructing minimal divisomes in the test tube. Biophys. Rev. 5, 63-77
14. Small, E., and Addinall, S. G. (2003) Dynamic FtsZ polymerization is sensitive to the GTP to GDP ratio and can be maintained at steady state using a GTP-regeneration system. Microbiology 149, 2235-2242
15. González, J. M., Vélez, M., Jiménez, M., Alfonso, C., Schuck, P., Mingorance, J., Vicente, M., Minton, A. P., and Rivas, G. (2005) Cooperative behavior of Escherichia coli cell-division protein FtsZ assembly involves the preferential cyclization of long single-stranded fibrils. Proc. Natl. Acad. Sci. U.S.A. 102, 1895-1900
16. 2+-linked self-assembly of FtsZ in the presence of GTP or a GTP analogue involves the concerted formation of a narrow size distribution of oligomeric species. Biochemistry 51, 4541-4550
17. Fu, G., Huang, T., Buss, J., Coltharp, C., Hensel, Z., and Xiao, J. (2010) In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS One 5, e12682
18. Li, Z., Trimble, M. J., Brun, Y. V., and Jensen, G. J. (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J. 26, 4694-4708
19. Popp, D., Iwasa, M., Narita, A., Erickson, H. P., and Maéda, Y. (2009) FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91, 340-350
20. Yu, X. C., and Margolin, W. (1998) Inhibition of assembly of bacterial cell division protein FtsZ by the hydrophobic dye 5,5′-bis-(8-anilino-1- naphthalenesulfonate). J. Biol. Chem. 273, 10216-10222
21. Chen, Y., and Erickson, H. P. (2009) FtsZ filament dynamics at steady state: subunit exchange with and without nucleotide hydrolysis. Biochemistry 48, 6664-6673
22. Cordell, S. C., Anderson, R. E., and Löwe, J. (2001) Crystal structure of the bacterial cell division inhibitor MinC. EMBO J. 20, 2454-2461
23. Shiomi, D., and Margolin, W. (2007) The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J. Bacteriol. 189, 236-243
24. Wu, W., Park, K. T., Holyoak, T., and Lutkenhaus, J. (2011) Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol. Microbiol. 79, 1515-1528
25. Shen, B., and Lutkenhaus, J. (2009) The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinC(C)/MinD. Mol. Microbiol. 72, 410-424
26. Shen, B., and Lutkenhaus, J. (2010) Examination of the interaction between FtsZ and MinCN in E. coli suggests how MinC disrupts Z rings. Mol. Microbiol. 75, 1285-1298
27. Blasios, V., Bisson-Filho, A. W., Castellen, P., Nogueira, M. L., Bettini, J., Portugal, R. V., Zeri, A. C., and Gueiros-Filho, F. J. (2013) Genetic and biochemical characterization of the MinC-FtsZ interaction in Bacillus subtilis. PLoS One 8, e60690
28. Rivas, G., López, A., Mingorance, J., Ferrándiz, M. J., Zorrilla, S., Minton, A. P., Vicente, M., and Andreu, J. M. (2000) Magnesium-induced linear self-association of the FtsZ bacterial cell division protein monomer. The primary steps for FtsZ assembly. J. Biol. Chem. 275, 11740-11749
29. Okuno, T., Ogoh, M., Tanina, H., Funasaki, N., and Kogure, K. (2009) Direct monitoring of interaction between Escherichia coli proteins, MinC and monomeric FtsZ, in solution. Biol. Pharm. Bull. 32, 1473-1475
30. Reija, B., Monterroso, B., Jiménez, M., Vicente, M., Rivas, G., and Zorrilla, S. (2011) Development of a homogeneous fluorescence anisotropy assay to monitor and measure FtsZ assembly in solution. Anal. Biochem. 418, 89-96
31. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78, 1606-1619
32. Cole, J. L. (2004) Analysis of heterogeneous interactions. Methods Enzymol. 384, 212-232
33. Laue, T., Shah, B., and Ridgeway, T., and Pelletier, S. L. (1992) in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., eds) pp. 90-125, The Royal Society of Chemistry, Cambridge, UK
34. Rosales, T., and Royer, C. A. (2008)Agraphical user interface for BIOEQS: a program for simulating and analyzing complex biomolecular interactions. Anal. Biochem. 381, 270-272
35. Hernández-Rocamora, V. M., Reija, B., García, C., Natale, P., Alfonso, C., Minton, A. P., Zorrilla, S., Rivas, G., and Vicente, M. (2012) Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J. Biol. Chem. 287, 30097-30104
36. Hoenig, M., Lee, R. J., and Ferguson, D. C. (1989) A microtiter plate assay for inorganic phosphate. J. Biochem. Biophys. Methods 19, 249-251
37. Lanzetta, P. A., Alvarez, L. J., Reinach, P. S., and Candia, O. A. (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100, 95-97
38. Hu, Z., and Lutkenhaus, J. (2000) Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J. Bacteriol. 182, 3965-3971
39. Cho, H., McManus, H. R., Dove, S. L., and Bernhardt, T. G. (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc. Natl. Acad. Sci. U.S.A. 108, 3773-3778
40. Dajkovic, A., Mukherjee, A., and Lutkenhaus, J. (2008) Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J. Bacteriol. 190, 2513-2526
41. Chen, Y., Milam, S. L., and Erickson, H. P. (2012) SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51, 3100-3109
42. 2+-linked self-assembly of FtsZ in the presence of GTP or a GTP analogue. Biochemistry 51, 6108-6113