Bacterial cell shape

Nature Reviews Microbiology

Volumn 3, Issue 8, 2005, Pages 601-610

  Cabeen, Matthew T ^a   Jacobs Wagner, Christine ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BACTERIAL PROTEIN; CARBOXYPEPTIDASE; CELL MEMBRANE PROTEIN; CRESCENTIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GLYCOSYLTRANSFERASE; HYDROLASE; INTERMEDIATE FILAMENT PROTEIN; MREB PROTEIN; PENICILLIN BINDING PROTEIN; PEPTIDOGLYCAN; PROTEINASE; TUBULIN; UNCLASSIFIED DRUG;

BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIUM IDENTIFICATION; CELL SHAPE; CYTOSKELETON; EUKARYOTE; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; MICROBIAL MORPHOLOGY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; REVIEW; TAXONOMY;

CELL MEMBRANE; CELL WALL; CYTOSKELETON; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; PENICILLIN-BINDING PROTEINS;

EUKARYOTA; NEGIBACTERIA; POSIBACTERIA;

EID: 22944483501     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1205     Document Type: Review

References (121)

1. Weibull, C. The isolation of protoplasts, from Bacillus megaterium by controlled treatment with lysozyme. J. Bacteriol. 66, 688-695 (1953).
2. Lederberg, J. Bacterial protoplasts induced by penicillin. Proc. Natl Acad. Sci. USA 42, 574-577 (1956).
3. Weidel, W. & Pelzer, H. Bagshaped macromolecules - a new outlook on bacterial cell walls. Adv. Enzymol. Relat. Areas. Mol. Biol. 26, 193-232 (1964).
4. Weidel, W., Frank, H. & Martin, H. H. The rigid layer of the cell wall of Escherichia coli strain B. J. Gen. Microbiol. 22, 158-166 (1960).
5. Schwarz, U. & Leutgeb, W. Morphogenetic aspects of murein structure and biosynthesis. J. Bacteriol. 106, 588-595 (1971).
6. Spratt, B. G. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc. Natl Acad. Sci. USA 72, 2999-3003 (1975).
7. Tamaki, S., Matsuzawa, H. & Matsuhashi, M. Cluster of mrdA and mrdB genes responsible for the rod shape and mecillinam sensitivity of Escherichia coli. J. Bacteriol. 141, 52-57 (1980).
8. Nelson, D. E. & Young, K. D. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182, 1714-1721 (2000).
9. Meberg, B. M., Paulson, A. L., Priyadarshini, R. & Young, K. D. Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in determining uniform morphology of Escherichia coli. J. Bacteriol. 186, 8326-8336 (2004).
10. Karamata, D., McConnell, M. & Rogers, H. J. Mapping of rod mutants of Bacillus subtilis. J. Bacteriol. 111, 73-79 (1972).
11. Rogers, H. J., McConnell, M. & Burdett, I. D. The isolation and characterization of mutants of Bacillus subtilis and Bacillus licheniformis with disturbed morphology and cell division. J. Gen. Microbiol. 61, 155-171 (1970).
12. Wagner, P. M. & Stewart, G. C. Role and expression of the Bacillus subtilis rodC operon. J. Bacteriol. 173, 4341-4346 (1991).
13. Levin, P. A., Margolis, P. S., Setlow, P., Losick, R. & Sun, D. Identification of Bacillus subtilis genes for septum placement and shape determination. J. Bacteriol. 174, 6717-6728 (1992).
14. Doi, M. et al. Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells. J. Bacteriol. 170, 4619-4624 (1988).
15. Wachi, M. et al. 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 (1987).
16. Varley, A. W. & Stewart, G. C. 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 (1992).
17. Matsuzawa, H., Hayakawa, K., Sato, T. & Imahori, K. Characterization and genetic analysis of a mutant of Escherichia coli K-12 with rounded morphology. J. Bacteriol. 115, 436-442 (1973).
18. van den Ent, F., Amos, L. A. & Löwe, J. Prokaryotic origin of the actin cytoskeleton. Nature 413, 39-44 (2001).
19. Jones, L. J., Carballido-Lopez, R. & Errington, J. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104, 913-922 (2001).
20. Bork, P., Sander, C. & Valencia, A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl Acad. Sci. USA 89, 7290-7294 (1992).
21. Kruse, T., Møller-Jensen, J., Løbner-Olesen, A. & Gerdes, K. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J. 22, 5283-5292 (2003).
22. Figge, R. M., Divakaruni, A. V. & Gober, J. W. Mre B, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol. Microbiol. 51, 1321-1332 (2004).
23. Shih, Y. L., Le, T. & Rothfield, L. 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 (2003).
24. Ausmees, N., Kuhn, J. R. & Jacobs-Wagner, C. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115, 705-713 (2003).
25. Mobley, H. L., Koch, A. L., Doyle, R. J. & Streips, U. N. Insertion and fate of the cell wall in Bacillus subtilis. J. Bacteriol. 158, 169-179 (1984).
26. Daniel, R. A. & Errington, J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113, 767-776 (2003).
27. De Pedro, M. A., Schwarz, H. & Koch, A. L. Patchiness of murein insertion into the sidewall of Escherichia coli. Microbiology 149, 1753-1761 (2003).
28. Schlaeppi, J. M., Schaefer, O. & Karamata, D. Cell wall and DNA cosegregation in Bacillus subtilis studied by electron microscope autoradiography. J. Bacteriol. 164, 130-135 (1985).
29. Schlaeppi, J. M., Pooley, H. M. & Karamata, D. Identification of cell wall subunits in Bacillus subtilis and analysis of their segregation during growth. J. Bacteriol. 149, 329-337 (1982).
30. Costa, K. et al. The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181, 3710-3715 (1999).
31. Henriques, A. O., Glaser, P., Piggot, P. J. & Moran, C. P. Jr. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol. Microbiol. 28, 235-247 (1998).
32. Labischinski, H., Barnickel, G., Bradaczek, H. & Giesbrecht, P. On the secondary and tertiary structure of murein. Low and medium-angle X-ray evidence against chitin-based conformations of bacterial peptidoglycan. Eur. J. Biochem. 95, 147-155 (1979).
33. Bhavsar, A. P., Erdman, L. K., Schertzer, J. W. & Brown, E. D. Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid. J. Bacteriol. 186, 7865-7873 (2004).
34. Braun, V. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim. Biophys. Acta 415, 335-377 (1975).
35. Braun, V. & Rehn, K. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur. J. Biochem. 10, 426-438 (1969).
36. Belaaouaj, A., Kim, K. S. & Shapiro, S. D. Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science 289, 1185-1188 (2000).
37. Ohara, M., Wu, H. C., Sankaran, K. & Rick, P. D. Identification and characterization of a new lipoprotein, Nlpl, in Escherichia coli K-12. J. Bacteriol. 181, 4319-4325 (1999).
38. Sonntag, I., Schwarz, H., Hirota, Y. & Henning, U. Cell envelope and shape of Escherichia coli: multiple mutants missing the outer membrane lipoprotein and other major outer membrane proteins. J. Bacteriol. 136, 280-285 (1978).
39. Vollmer, W. & Höltje, J. V. The architecture of the murein (peptidoglycan) in Gram-negative bacteria: vertical scaffold or horizontal layer(s)? J. Bacteriol. 186, 5978-5987 (2004).
40. Yao, X., Jericho, M., Pink, D. & Beveridge, T. Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J. Bacteriol. 181, 6865-6875 (1999).
41. Dmitriev, B. A., Toukach, F. V., Holst, O., Rietschel, E. T. & Ehlers, S. Tertiary structure of Staphylococcus aureus cell wall murein. J. Bacteriol. 186, 7141-7148 (2004).
42. Dmitriev, B. A. et al. Tertiary structure of bacterial murein: the scaffold model. J. Bacteriol. 185, 3458-3468 (2003).
43. Koch, A. L. & Doyle, R. J. Inside-to-ourtside growth and turnover of the wall of Gram-positive rods. J. Theor. Biol. 117, 137-157 (1985).
44. Labischinski, H., Goodell, E. W., Goodell, A. & Hochberg, M. L. Direct proof of a "more-than-single-layered" peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J. Bacteriol. 173, 751-756 (1991).
45. Park, J. T. & Burman, L. G. Elongation of the murein sacculus of Escherichia coli. Ann. Inst. Pasteur. Microbiol. 136A, 51-58 (1985).
46. Höltje, J.-V. in Bacterial Growth and Lysis (eds de Pedro, M. A., Höltje, J.-V, Löffelhardt, W.) 419-426 (Plenum Press, New York, 1993).
47. Doyle, R. J. & Marquis, R. E. Elastic, flexible peptidoglycan and bacterial cell wall properties. Trends Microbiol. 2, 57-60 (1994).
48. Marquis, R. E. Salt-induced contraction of bacterial cell walls. J. Bacteriol. 95, 775-781 (1968).
49. Koch, A. L. & Woeste, S. Elasticity of the sacculus of Escherichia coli. J. Bacteriol. 174, 4811-4819 (1992).
50. Boulbitch, A., Quinn, B. & Pink, D. Elasticity of the rodshaped Gram-negative eubacteria. Phys. Rev. Lett. 85, 5246-5249 (2000).
51. de Pedro, M. A., Quintela, J. C., Höltje, J. V. & Schwarz, H. Murein segregation in Escherichia coli. J. Bacteriol. 179, 2823-2834 (1997).
52. Pinho, M. G. & Errington, J. Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol. Microbiol. 50, 871-881 (2003).
53. Morlot, C., Zapun, A., Dideberg, O. & Vernet, T. Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol. Microbiol. 50, 845-855 (2003).
54. Cole, R. M. & Hahn, J. J. Cell wall replication in Streptococcus pyogenes. Science 135, 722-724 (1962).
55. 3H-labeled teichoic acid. J. Cell. Biol. 47, 786-790 (1970).
56. Young, K. D. Bacterial shape. Mol. Microbiol. 49, 571-580 (2003).
57. de Pedro, M. A., Young, K. D., Höltje, J. V. & Schwarz, H. Branching of Escherichia coli cells arises from multiple sites of inert peptidoglycan. J. Bacteriol. 185, 1147-1152 (2003).
58. Graumann, P. L. Cytoskeletal elements in bacteria. Curr. Opin. Microbiol. 7, 565-571 (2004).
59. Møller-Jensen, J. & Löwe, J. Increasing complexity of the bacterial cytoskeleton. Curr. Opin. Cell. Biol. 17, 75-81 (2005).
60. Bi, E. F. & Lutkenhaus, J. FtsZ ring structure associated with division in Escherichia coli. Nature 354, 161-164 (1991).
61. Mukherjee, A., Dai, K. & Lutkenhaus, J. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc. Natl Acad. Sci. USA 90, 1053-1057 (1993).
62. de Boer, P., Crossley, R. & Rothfield, L. The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359, 254-256 (1992).
63. RayChaudhuri, D. & Park, J. T. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359, 251-254 (1992).
64. Bramhill, D. & Thompson, C. M. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc. Natl Acad. Sci. USA 91, 5813-5817 (1994).
65. Mukherjee, A. & Lutkenhaus, J. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176, 2754-2758 (1994).
66. Nogales, E., Wolf, S. G. & Downing, K. H. Structure of the αβ tubulin dimer by electron crystallography. Nature 391, 199-203 (1998).
67. Löwe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203-206 (1998).
68. Errington, J., Daniel, R. A. & Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52-65 (2003).
69. Addinall, S. G. & Lutkenhaus, J. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol. 22, 231-237 (1996).
70. Varma, A. & Young, K. D. FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J. Bacteriol. 186, 6768-6774 (2004).
71. Bi, E. & Lutkenhaus, J. Isolation and characterization of ftsZ alleles that affect septal morphology. J. Bacteriol. 174, 5414-5423 (1992).
72. Anderson, D. E., Gueiros-Filho, F. J. & Erickson, H. P. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186, 5775-5781 (2004).
73. Thanedar, S. & Margolin, W. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol. 14, 1167-1173 (2004).
74. Abhayawardhane, Y. & Stewart G. C. Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene. J. Bacteriol. 177, 765-773 (1995).
75. Defeu Soufo, H. J. & Graumann, P. L. Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep. 5, 789-794 (2004).
76. Defeu Soufo, H. J. & Graumann, P. L. Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr. Biol. 13, 1916-1920 (2003).
77. Carballido-Lopez, R. & Errington, J. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev. Cell. 4, 19-28 (2003).
78. Wortinger, M. A., Quardokus, E. M. & Brun, Y. V. Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol. Microbiol. 29, 963-973 (1998).
79. Vollmer, W., von Rechenberg, M. & Höltje, J. V. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J. Biol. Chem. 274, 6726-6734 (1999).
80. Schiffer, G. & Höltje, J. V. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J. Biol. Chem. 274, 32031-32039 (1999).
81. Romeis, T & Höltje, J. V Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J. Biol. Chem. 269, 21603-21607 (1994).
82. Alaedini, A. & Day, R. A. Identification of two penicillin-binding multienzyme complexes in Haemophilus, influenzae. Biochem. Biophys. Res. Commun. 264, 191-195 (1999).
83. Weiss, D. S. et al. Localization of the Escherichia coli cell division protein Ftsl (PBP3) to the division site and cell pole. Mol. Microbiol. 25, 671-681 (1997).
84. Iwaya, M., Jones, C. W., Khorana, J. & Strominger, J. L. Mapping of the mecillinam-resistant, round morphological mutants of Escherichia coli. J. Bacteriol. 133, 196-202 (1978).
85. Boyle, D. S., Khattar, M. M., Addinall, S. G., Lutkenhaus, J. & Donachie, W. D. ftsW is an essential cell-division gene in Escherichia coli. Mol. Microbiol. 24, 1263-1273 (1997).
86. Ikeda, M. et al. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J. Bacteriol. 171, 6375-6378 (1989).
87. Hara, H., Yasuda, S., Horiuchi, K. & Park, J. T. A promoter for the first nine genes of the Escherichia coli mra cluster of cell division and cell envelope biosynthesis genes, including ftsl and ftsW. J. Bacteriol. 179, 5802-5811 (1997).
88. Matsuzawa, H. et al. Nucleotide sequence of the rodA gene, responsible for the rod shape of Escherichia coli: rodA and the pbpA gene, encoding penicillin-binding protein 2, constitute the rodA operon. J. Bacteriol. 171, 558-560 (1989).
89. Ishino, F. et al. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and rodA protein. J. Biol. Chem. 261, 7024-7031 (1986).
90. Mercer, K. L. & Weiss, D. S. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, Ftsl (PBP3), to the division site. J. Bacteriol. 184, 904-912 (2002).
91. Lee, J. C. & Stewart, G. C. Essential nature of the mreC determinant of Bacillus subtilis. J. Bacteriol. 185, 4490-4498 (2003).
92. Kruse, T., Bork-Jensen, J. & Gerdes, K. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol. Microbiol. 55, 78-89 (2005).
93. Defeu Soufo, H. J. & Graumann, P. L. Bacillus subtilis actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D and other actin-like proteins for proper localization. BMC Cell Biol. 6, 10 (2005).
94. Scheffers, D. J., Jones, L. J. & Errington, J. Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol. Microbiol. 51, 749-764 (2004).
95. Datta, P., Dasgupta, A., Bhakta, S. & Basu, J. Interaction between FtsZ and FtsW of Mycobacterium tuberculosis. J. Biol. Chem. 277, 24983-24987 (2002).
96. Nelson, D. E. & Young, K. D. Contributions of PBP 5 and DD-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J. Bacteriol. 183, 3055-3064 (2001).
97. McPherson, D. C. & Popham, D. L. Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus subtilis. J. Bacteriol. 185, 1423-1431 (2003).
98. Firtel, M., Henderson, G. & Sokolov, I. Nanosurgery: observation of peptidoglycan strands in Lactobacillus helveticus cell walls. Ultramicroscopy 101, 105-109 (2004).
99. Chen, Y. & Erickson, H. P. Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280, 22549-22554 (2005).
100. Esue, O., Cordero, M., Wirtz, D. & Tseng, Y. The assembly of MreB, a prokaryotic homolog of actin. J. Biol. Chem. 280, 2628-2635 (2005).
101. Umeda, A. & Amako, K. Growth of the surface of Corynebacterium diphitheriae. Microbiol. Immunol. 27, 663-671 (1983).
102. Motaleb, M. A. et al. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl Acad. Sci. USA 97, 10899-10904 (2000).
103. Gitai, Z., Dye, N. A., Reisenauer, A., Wachi, M. & Shapiro, L. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120, 329-341 (2005).
104. Trachtenberg, S. Mollicutes-wall-less bacteria with internal cytoskeletons. J. Struct. Blol. 124, 244-256 (1998).
105. Kessel, M., Peleg, I., Muhlrad, A. & Kahane, I. Cytoplasmic helical structure associated with Acholeplasma laidlawii. J. Bacteriol. 147, 653-659 (1981).
106. Hegermann, J., Herrmann, R. & Mayer, F. Cytoskeletal elements in the bacterium Mycoplasma pneumoniae. Naturwissenschaften 89, 453-458 (2002).
107. Williamson, D. L., Renaudin, J. & Bove, J. M. Nucleotide sequence of the Spiroplasma citri fibril protein gene. J. Bacteriol. 173, 4353-4362 (1991).
108. Kürner, J., Frangakis, A. S. & Baumeister, W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307, 436-438 (2005).
109. Trachtenberg, S. & Gilad, R. A bacterial linear motor: cellular and molecular organization of the contractile cytoskeleton of the helical bacterium Spiroplasma melliferum BC3. Mol. Microbiol. 41, 827-848 (2001).
110. Fraser, C. M. et al. The minimal gene complement of Mycoplasma genitalium. Science 270, 397-403 (1995).
111. Wang, X. & Lutkenhaus, J. Characterization of the ftsZ gene from Mycoplasma pulmonis, an organism lacking a cell wall. J. Bacteriol. 178, 2314-2319 (1996).
112. Löwe, J., van den Ent, F. & Amos, L. A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33, 177-198 (2004).
113. Ishino, F., Mitsui, K., Tamaki, S. & Matsuhashi, M. Dual enzyme activities of cell wall peptidoglycan synthesis, peptidoglycan transglycosylase and penicillin-sensitive transpeptidase, in purified preparations of Escherichia coli penicillin-binding protein 1A. Biochem. Biophys. Res. Commun. 97, 287-293 (1980).
114. Nakagawa, J., Tamaki, S., Tomioka, S. & Matsuhashi, M. Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase. J. Biol. Chem. 259, 13937-13946 (1984).
115. Spratt, B. G. & Pardee, A. B. Penicillin-binding proteins and cell shape in E. coli. Nature 254, 516-517 (1975).
116. Adam, M. et al. The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 179, 6005-6009 (1997).
117. Spratt, B. G. Temperature-sensitive cell division mutants of Escherichia coli with thermolabile penicillin-binding proteins. J. Bacteriol. 131, 293-305 (1977).
118. Korat, B., Mottl. H. & Keck, W. Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol. Microbiol. 5, 675-684 (1991).
119. Broome-Smith, J. K., Ioannidis, I., Edelman, A. & Spraft, B. G. Nucleotide sequences of the penicillin-binding protein 5 and 6 genes of Escherichia coli. Nucleic Acids Res. 16, 1617 (1988).
120. Baquero, M. R., Bouzon, M., Quintela, J. C., Ayala, J. A. & Moreno, F. dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with DD-carboxypeptidase activity. J. Bacteriol. 178, 7106-7111 (1996).
121. Romeis, T. & Höltje, J. V. Penicillin-binding protein 7/8 of Escherichia coli is a DD-endopeptidase. Eur. J. Biochem. 224, 597-604 (1994).