The transmembrane domains of the bacterial cell division proteins FtsB and ftsl form a stable high-order oligomer

Biochemistry

Volumn 52, Issue 43, 2013, Pages 7542-7550

  Khadria, Ambalika S ^a   Senes, Alessandro ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CELL DIVISION; BIOPHYSICAL ANALYSIS; INTEGRAL MEMBRANE PROTEINS; MULTIVALENT BINDING; OLIGOMERIC COMPLEXES; RESONANCE ENERGY TRANSFER; TRANS-MEMBRANE DOMAINS; TRANSMEMBRANE HELICES;

ACTIVATION ANALYSIS; BIOLOGICAL MEMBRANES; CELL PROLIFERATION; ENERGY TRANSFER; PROTEINS;

OLIGOMERS;

DETERGENT; FTSB PROTEIN; FTSL PROTEIN; LIPID; MEMBRANE PROTEIN; OLIGOMER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CELL DIVISION; CHEMICAL PROCEDURES; CONTROLLED STUDY; ENERGY TRANSFER; IN VITRO STUDY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN ISOLATION; PROTEIN STABILITY; PROTEIN STRUCTURE;

CELL CYCLE PROTEINS; CELL DIVISION; CELL MEMBRANE; DETERGENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; KINETICS; LIPID BILAYERS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PEPTIDE FRAGMENTS; PHOSPHATIDYLCHOLINES; PHOSPHORYLCHOLINE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY;

EID: 84887051938     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4009837     Document Type: Article

References (44)

1. Adams, D. W. and Errington, J. (2009) Bacterial cell division: Assembly, maintenance and disassembly of the Z ring Nat. Rev. Microbiol. 7, 642-653
2. 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
3. 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
4. Goehring, N. W. and Beckwith, J. (2005) Diverse Paths to Midcell: Assembly of the Bacterial Cell Division Machinery Curr. Biol. 15, R514-R526
5. Goehring, N. W., Gonzalez, M. D., and Beckwith, J. (2006) Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly Mol. Microbiol. 61, 33-45
6. Gonzalez, M. D. and Beckwith, J. (2009) Divisome under construction: Distinct domains of the small membrane protein FtsB are necessary for interaction with multiple cell division proteins J. Bacteriol. 191, 2815-2825
7. Robichon, C., Karimova, G., Beckwith, J., and Ladant, D. (2011) Role of Leucine Zipper Motifs in Association of the Escherichia coli Cell Division Proteins FtsL and FtsB J. Bacteriol. 193, 4988-4992
8. 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
9. Buddelmeijer, N., Judson, N., Boyd, D., Mekalanos, J. J., and Beckwith, J. (2002) YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site Proc. Natl. Acad. Sci. U.S.A. 99, 6316-6321
10. Daniel, R. A. and Errington, J. (2000) Intrinsic instability of the essential cell division protein FtsL of Bacillus subtilis and a role for DivIB protein in FtsL turnover Mol. Microbiol. 36, 278-289
11. Ghigo, J.-M., Weiss, D. S., Chen, J. C., Yarrow, J. C., and Beckwith, J. (1999) Localization of FtsL to the Escherichia coli septal ring Mol. Microbiol. 31, 725-737
12. Katis, V. L., Wake, R. G., and Harry, E. J. (2000) Septal Localization of the Membrane-Bound Division Proteins of Bacillus subtilis DivIB and DivIC Is Codependent Only at High Temperatures and Requires FtsZ J. Bacteriol. 182, 3607-3611
13. Robichon, C., King, G. F., Goehring, N. W., and Beckwith, J. (2008) Artificial Septal Targeting of Bacillus subtilis Cell Division Proteins in Escherichia coli: An Interspecies Approach to the Study of Protein-Protein Interactions in Multiprotein Complexes J. Bacteriol. 190, 6048-6059
14. Daniel, R. A., Harry, E. J., Katis, V. L., Wake, R. G., and Errington, J. (1998) Characterization of the essential cell division gene ftsL (yllD) of Bacillus subtilis and its role in the assembly of the division apparatus Mol. Microbiol. 29, 593-604
15. Daniel, R. A., Noirot-Gros, M.-F., Noirot, P., and Errington, J. (2006) Multiple Interactions between the Transmembrane Division Proteins of Bacillus subtilis and the Role of FtsL Instability in Divisome Assembly J. Bacteriol. 188, 7396-7404
16. Bramkamp, M., Weston, L., Daniel, R. A., and Errington, J. (2006) Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis Mol. Microbiol. 62, 580-591
17. Rowland, S. L., Wadsworth, K. D., Robson, S. A., Robichon, C., Beckwith, J., and King, G. F. (2010) Evidence from Artificial Septal Targeting and Site-Directed Mutagenesis that Residues in the Extracytoplasmic Domain of DivIB Mediate Its Interaction with the Divisomal Transpeptidase PBP 2B J. Bacteriol. 192, 6116-6125
18. LaPointe, L. M., Taylor, K. C., Subramaniam, S., Khadria, A., Rayment, I., and Senes, A. (2013) Structural organization of FtsB, a transmembrane protein of the bacterial divisome Biochemistry 52, 2574-2585
19. Rath, A. and Deber, C. M. (2013) Design of transmembrane peptides: Coping with sticky situations Methods Mol. Biol. (N.Y., NY, U.S.) 1063, 197-210
20. Liu, L.-P. and Deber, C. M. (1998) Guidelines for membrane protein engineering derived from de novo designed model peptides Pept. Sci. 47, 41-62
21. Melnyk, R. A., Partridge, A. W., and Deber, C. M. (2001) Retention of Native-like Oligomerization States in Transmembrane Segment Peptides: Application to the Escherichia coli Aspartate Receptor Biochemistry 40, 11106-11113
22. Stahl, P. J., Cruz, J. C., Li, Y., Michael, Yu. S., and Hristova, K. (2012) On-the-resin N-terminal modification of long synthetic peptides Anal. Biochem. 424, 137-139
23. Khadria, A. and Senes, A. (2013) Measurement of Transmembrane Peptide Interactions in Liposomes Using Förster Resonance Energy Transfer (FRET) Methods Mol. Biol. (N.Y., NY, U.S.) 1063, 19-36
24. Li, E., You, M., and Hristova, K. (2005) Sodium Dodecyl Sulfate-Polyacrylamide Gel Electrophoresis and Förster Resonance Energy Transfer Suggest Weak Interactions between Fibroblast Growth Factor Receptor 3 (FGFR3) Transmembrane Domains in the Absence of Extracellular Domains and Ligands Biochemistry 44, 352-360
25. You, M., Li, E., Wimley, W. C., and Hristova, K. (2005) Förster resonance energy transfer in liposomes: Measurements of transmembrane helix dimerization in the native bilayer environment Anal. Biochem. 340, 154-164
26. Schick, S., Chen, L., Li, E., Lin, J., Köper, I., and Hristova, K. (2010) Assembly of the M2 Tetramer Is Strongly Modulated by Lipid Chain Length Biophys. J. 99, 1810-1817
27. Fleming, K. G., Ren, C.-C., Doura, A. K., Eisley, M. E., Kobus, F. J., and Stanley, A. M. (2004) Thermodynamics of glycophorin A transmembrane helix dimerization in C14 betaine micelles Biophys. Chem. 108, 43-49
28. Pace, C. J., Huang, Q., Wang, F., Palla, K. S., Fuller, A. A., and Gao, J. (2011) A FlAsH-Tetracysteine Assay for Quantifying the Association and Orientation of Transmembrane α-Helices ChemBioChem 12, 1018-1022
29. Villanelo, F., Ordenes, A., Brunet, J., Lagos, R., and Monasterio, O. (2011) A model for the Escherichia coli FtsB/FtsL/FtsQ cell division complex BMC Struct. Biol. 11, 28
30. MacKenzie, K. R. and Fleming, K. G. (2008) Association energetics of membrane spanning α-helices Curr. Opin. Struct. Biol. 18, 412-419
31. Seddon, A. M., Curnow, P., and Booth, P. J. (2004) Membrane proteins, lipids and detergents: Not just a soap opera Biochim. Biophys. Acta 1666, 105-117
32. Xiao Zhou, F., Cocco, M. J., Russ, W. P., Brunger, A. T., and Engelman, D. M. (2000) Interhelical hydrogen bonding drives strong interactions in membrane proteins Nat. Struct. Mol. Biol. 7, 154-160
33. Choma, C., Gratkowski, H., Lear, J. D., and DeGrado, W. F. (2000) Asparagine-mediated self-association of a model transmembrane helix Nat. Struct. Mol. Biol. 7, 161-166
34. Hendsch, Z. S. and Tidor, B. (1999) Electrostatic interactions in the GCN4 leucine zipper: Substantial contributions arise from intramolecular interactions enhanced on binding Protein Sci. 8, 1381-1392
35. Renthal, R., Brancaleon, L., Pena, I., Silva, F., and Chen, L. Y. (2011) Interaction of a two-transmembrane-helix peptide with lipid bilayers and dodecyl sulfate micelles Biophys. Chem. 159, 321-327
36. Tulumello, D. V. and Deber, C. M. (2011) Positions of Polar Amino Acids Alter Interactions between Transmembrane Segments and Detergents Biochemistry 50, 3928-3935
37. Posokhov, Y. O., Merzlyakov, M., Hristova, K., and Ladokhin, A. S. (2008) A Simple "Proximity" Correction for FRET Efficiency Determination in Membranes Using Lifetime Measurements Anal. Biochem. 380, 134-136
38. Doura, A. K. and Fleming, K. G. (2004) Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer J. Mol. Biol. 343, 1487-1497
39. Burgess, N. K., Stanley, A. M., and Fleming, K. G. (2008) Determination of Membrane Protein Molecular Weights and Association Equilibrium Constants Using Sedimentation Equilibrium and Sedimentation Velocity. In Methods in Cell Biology (Correia, J. J. and Detrich, H. W., Eds.) pp 181-211, Academic Press, New York.
40. Gonzalez, M. D., Akbay, E. A., Boyd, D., and Beckwith, J. (2010) Multiple interaction domains in FtsL, a protein component of the widely conserved bacterial FtsLBQ cell division complex J. Bacteriol. 192, 2757-2768
41. Masson, S., Kern, T., Le Gouëllec, A., Giustini, C., Simorre, J.-P., Callow, P., Vernet, T., Gabel, F., and Zapun, A. (2009) Central domain of DivIB caps the C-terminal regions of the FtsL/DivIC coiled-coil rod J. Biol. Chem. 284, 27687-27700
42. Van den Berg van Saparoea, H. B., Glas, M., Vernooij, I. G. W. H., Bitter, W., den Blaauwen, T., and Luirink, J. (2013) Fine-mapping the Contact Sites of the Escherichia coli Cell Division Proteins FtsB and FtsL on the FtsQ Protein J. Biol. Chem. 288, 24340-24350
43. D'Ulisse, V., Fagioli, M., Ghelardini, P., and Paolozzi, L. (2007) Three functional subdomains of the Escherichia coli FtsQ protein are involved in its interaction with the other division proteins Microbiology (Reading, U.K.) 153, 124-138
44. 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