Dimeric structure of the cell shape protein MreC and its functional implications

Molecular Microbiology

Volumn 62, Issue 6, 2006, Pages 1631-1642

  Van Den Ent, Fusinita ^a   Leaver, Mark ^b   Bendezu, Felipe ^c   Errington, Jeff ^b   De Boer, Piet ^c   Löwe, Jan ^a  

^a MRCLMB   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CARBOXYPEPTIDASE; CHYMOTRYPSIN; DIPEPTIDE; MEMBRANE PROTEIN; MREB PROTEIN; MUREIN SYNTHASE; PENICILLIN BINDING PROTEIN; PROTEIN MREC; PROTEIN MRED; PROTEINASE; SERINE; SYNTHETASE; THREONINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL WALL; BETA CHAIN; CARBOXY TERMINAL SEQUENCE; CELL SHAPE; CELL VIABILITY; CYTOPLASM; DIMERIZATION; ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BLOTTING, WESTERN; CRYSTALLOGRAPHY; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PENICILLIN-BINDING PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN; TWO-HYBRID SYSTEM TECHNIQUES;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES;

EID: 33751363915     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05485.x     Document Type: Article

References (61)

1. Amos, L.A., van den Ent, F., and Löwe, J. (2004) Structural/functional homology between the bacterial and eukaryotic cytoskeletons. Curr Opin Cell Biol 16: 24-31.
2. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng 6: 37-40.
3. Bhavsar, A.P., and Brown, E.D. (2006) Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol Microbiol 60: 1077-1090.
4. Brünger, A., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
5. Carballido-Lopez, R., and Errington, J. (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4: 19-28.
6. Carballido-López, R., Formstone, A., Li, Y., Ehrlich, S.D., Noirot, P., and Errington, J. (2006) Actin homologue MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11: 399-409.
7. Cianci, M., Antonyuk, S., Bliss, N., Bailey, M.W., Buffey, S.G., Cheung, K.C., et al. (2005) A high-throughput structural biology/proteomics beamline at the SRS on a new multipole wiggler. J Synchrotron Radiat 12: 455-466.
8. Collaborative Computing Project, N. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763.
9. Daniel, R.A., and Errington, J. (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rodshaped cell. Cell 113: 767-776.
10. de la Fortelle, E., and Bricogne, G. (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. In Methods in Enzymology: Macromolecular Crystallography, Part A, Vol. 276. Sweet, R.M., and Carter, C.W., Jr (eds). New York, NY: Academic Press, pp. 472-494.
11. Defeu Soufo, H.J., and Graumann, P.L. (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5: 789-794.
12. DeLano, W.L. (2002) The PYMOL Molecular Graphics System. San Carlos, CA: DeLano Scientific.
13. Divakaruni, A.V., Loo, R.R., Xie, Y., Loo, J.A., and Gober, J.W. (2005) The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc Natl Acad Sci USA 102: 18602-18607.
14. Dye, N.A., Pincus, Z., Theriot, J.A., Shapiro, L., and Gitai, Z. (2005) Two independent spiral structures control cell shape in Caulobacter. Proc Natl Acad Sci USA 102: 18608-18613.
15. Engh, R.A., and Huber, R. (1991) Accurate bond and angle parameters for x-ray protein-structure refinement. Acta Crystallogr A 47: 392-400.
16. van den Ent, F., and Löwe, J. (2000) Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J 19: 5300-5307.
17. van den Ent, F., and Löwe, J. (2006) RF cloning: a restriction-free method for inserting target genes into plasmids. J Biochem Biophys Meth 67: 67-74.
18. van den Ent, F., Amos, L.A., and Löwe, J. (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413: 39-44.
19. Figge, R.M., Divakaruni, A.V., and Gober, J.W. (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51: 1321-1332.
20. Formstone, A., and Errington, J. (2005) A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol Microbiol 55: 1646-1657.
21. Fuhrmann, C.N., Kelch, B.A., Ota, N., and Agard, D.A. (2004) The 0.83 A resolution crystal structure of alpha-lytic protease reveals the detailed structure of the active site and identifies a source of conformational strain. J Mol Biol 338: 999-1013.
22. Gitai, Z., Dye, N., and Shapiro, L. (2004) An actin-like gene can determine cell polarity in bacteria. Proc Natl Acad Sci USA 101: 8643-8648.
23. Gitai, Z., Dye, N.A., Reisenauer, A., Wachi, M., and Shapiro, L. (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120: 329-341.
24. Heidrich, C., Ursinus, A., Berger, J., Schwarz, H., and Höltje, J.V. (2002) Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J Bacteriology 184: 6093-6099.
25. Henriques, A.O., Glaser, P., Piggot, P.J., and Moran, C.P., Jr (1998) Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28: 235-247.
26. Holm, L., and Sander, C. (1993) Protein-structure comparison by alignment of distance matrices. J Mol Biology 233: 123-138.
27. Höltje, J.V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62: 181-203.
28. Jones, L.J.F., Carballido-Lopez, R., and Errington, J. (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104: 913-922.
29. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
30. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946-950.
31. Kruse, T., and Gerdes, K. (2005) Bacterial DNA segregation by the actin-like MreB protein. Trends Cell Biol 15: 343-345.
32. Kruse, T., Moller-Jensen, J., Lobner-Olesen, A., and Gerdes, K. (2003) Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22: 5283-5292.
33. Kruse, T., Bork-Jensen, J., and Gerdes, K. (2005) The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55: 78-89.
34. Kruse, T., Blagoev, B., Lobner-Olesen, A., Wachi, M., Sasaki, K., Iwai, N., et al. (2006) Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev 20: 113-124.
35. Kunst, F., and Rapoport, G. (1995) Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis. J Bacteriol 177: 2403-2407.
36. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993) Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26: 283-291.
37. Leaver, M., and Errington, J. (2005) Roles for MreC and MreD proteins in helical growth of the cylindrical cell wall in Bacillus subtilis. Mol Microbiol 57: 1196-1209.
38. Lee, J.C., and Stewart, G.C. (2003) Essential nature of the mreC determinant of Bacillus subtilis. J Bacteriol 185: 4490-4498.
39. Lee, J.C., Cha, J.H., Zerbv, D.B., and Stewart, G.C. (2003) Heterospecific expression of the Bacillus subtilis cell shape determination genes mreBCD in Escherichia coli. Curr Microbiol 47: 146-152.
40. Leslie, A.G.W. (1991) Recent Changes to the MOSFLM Package for Processing Film and Image Plate Data. Daresbury, Warrington WA44AD, UK: SERC Laboratory.
41. Levin, P.A., Margolis, P.S., Setlow, P., Losick, R., and Sun, D.X. (1992) Identification of Bacillus subtilis genes for septum placement and shape determination. J Bacteriol 174: 6717-6728.
42. Löwe, J., van den Ent, F., and Amos, L.A. (2004) Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct 33: 177-198.
43. Merritt, E.A., and Bacon, D.J. (1997) Raster3D: photorealistic molecular graphics. In Methods in Enzymology: Macromolecular Crystallography, Part B, Vol. 277. Carter, C.W., and Sweet, R.M. (eds). London: Academic Press, pp. 505-524.
44. Nelson, D.E., and Young, K.D. (2000) Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 182: 1714-1721.
45. Nilsen, T., Ghosh, A.S., Goldberg, M.B., and Young, K.D. (2004) Branching sites and morphological abnormalities behave as ectopic poles in shape-defective Escherichia coli. Mol Microbiol 52: 1045-1054.
46. Partridge, S.R., and Errington, J. (1993) The importance of morphological events and intercellular interactions in the regulation of prespore-specific gene expression during sporulation in Bacillus subtilis. Mol Microbiol 8: 945-955.
47. Popham, D.L., and Young, K.D. (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6: 594-599.
48. Rashid, R., Liang, B., Baker, D.L., Youssef, O.A., He, Y., Phipps, K., et al. (2006) Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol Cell 21: 249-260.
49. Slovak, P.M., Porter, S.L., and Armitage, J.P. (2006) Differential localization of Mre proteins with PBP2 in Rhodobacter sphaeroides. J Bacteriol 188: 1691-1700.
50. Soufo, H.J., and Graumann, P.L. (2003) Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr Biol 13: 1916-1920.
51. Spratt, B.G. (1975) Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci USA 72: 2999-3003.
52. Spratt, B.G., and Pardee, A.B. (1975) Penicillin-binding proteins and cell shape in E. coli. Nature 254: 516-517.
53. Tamaki, S., Matsuzawa, H., and Matsuhashi, M. (1980) Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli. J Bacteriol 141: 52-57.
54. Terwilliger, T.C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr D Biol Crystallogr 55: 849-861.
55. Tiyanont, K., Doan, T., Lazarus, M.B., Fang, X., Rudner, D.Z., and Walker, S. (2006) Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc Natl Acad Sci USA 103: 11033-11038.
56. Turk, D. (1992)Weiterentwicklung eines Programms für Molekülgrafik und Elektrondichte-Manipulation und seine Anwendung auf verschiedene Protein-Strukturaufklärungen. PhD Thesis. Technische Universität München.
57. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L., and Clardy, J. (1993) Atomic structures of the human immunophilin Fkbp-12 complexes with Fk506 and rapamycin. J Mol Biol 229: 105-124.
58. Varley, A.W., and Stewart, G.C. (1992) The Divivb region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (Mincd) and cell-shape (Mrebcd) determinants. J Bacteriol 174: 6729-6742.
59. Wachi, M., Doi, M., Tamaki, S., Park, W., Nakajima-Iijima, S., and Matsuhashi, M. (1987) Mutant isolation and molecular cloning of mre genes, which determine cell shape, sensitivity to mecillinam, and amount of penicillin-binding proteins in Escherichia coli. J Bacteriol 169: 4935-4940.
60. Wachi, M., Doi, M., Okada, Y., and Matsuhashi, M. (1989) New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J Bacteriol 171: 6511-6516.
61. Wei, Y., Havasy, T., McPherson, D.C., and Popham, D.L. (2003) Rod shape determination by the Bacillus subtilis class B penicillin-binding proteins encoded by pbpA and pbpH. J Bacteriol 185: 4717-4726.