The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli

Molecular Microbiology

Volumn 63, Issue 4, 2007, Pages 1008-1025

  Gerding, Matthew A ^a   Ogata, Yasuyuki ^b   Pecora, Nicole D ^a   Niki, Hironori ^b   De Boer, Piet A J ^a  

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

^b NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PEPTIDOGLYCAN ASSOCIATED LIPOPROTEIN; TOL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERIUM MUTANT; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANS ISOMER;

BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; CELL DIVISION; CYTOPLASM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GREEN FLUORESCENT PROTEINS; INTRACELLULAR MEMBRANES; LIPOPROTEINS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUTATION; PEPTIDOGLYCAN; PERIPLASMIC PROTEINS; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 33846650968     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05571.x     Document Type: Article

References (107)

1. Aarsman, M.E., Piette, A., Fraipont, C., Vinkenvleugel, T.M., Nguyen-Disteche, M., and den Blaauwen, T. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55: 1631-1645.
2. Addinall, S.G., and Holland, B. (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318: 219-236.
3. Addinall, S.G., Cao, C., and Lutkenhaus, J. (1997) FtsN, a late recruit to the septum in Escherichia coli. Mol Microbiol 25: 303-309.
4. Benedetti, H., Lazdunski, C., and Lloubes, R. (1991) Protein import into Escherichia coli: colicins A and E1 interact with a component of their translocation system. EMBO J 10: 1989-1995.
5. Bernadac, A., Gavioli, M., Lazzaroni, J.C., Raina, S., and Lloubes, R. (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180: 4872-4878.
6. Bernhardt, T.G., and de Boer, P.A.J. (2003) The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol 48: 1171-1182.
7. Bernhardt, T.G., and de Boer, P.A. (2004) Screening for synthetic lethal mutants in Escherichia coli and identification of EnvC (YibP) as a periplasmic septal ring factor with murein hydrolase activity. Mol Microbiol 52: 1255-1269.
8. Bernstein, A., Rolfe, B., and Onodera, K. (1972) Pleiotropic properties and genetic organization of the tolA,B locus of Escherichia coli K-12. J Bacteriol 112: 74-83.
9. Bi, E., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
10. de Boer, P.A.J., Crossley, R.E., and Rothfield, L.I. (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.
11. Bouveret, E., Derouiche, R., Rigal, A., Lloubes, R., Lazdunski, C., and Benedetti, H. (1995) Peptidoglycan-associated lipoprotein-TolB interaction. A possible key to explaining the formation of contact sites between the inner and outer membranes of Escherichia coli. J Biol Chem 270: 11071-11077.
12. Bouveret, E., Benedetti, H., Rigal, A., Loret, E., and Lazdunski, C. (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J Bacteriol 181: 6306-6311.
13. Bouveret, E., Journet, L., Walburger, A., Cascales, E., Benedetti, H., and Lloubes, R. (2002) Analysis of the Escherichia coli Tol-Pal and TonB systems by periplasmic production of Tol, TonB, colicin, or phage capsid soluble domains. Biochimie 84: 413-421.
14. Braun, V., and Herrmann, C. (1993) Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: cross-complementation between the TonB-ExbB-ExbD and the TolA-TolQ-TolR proteins. Mol Microbiol 8: 261-268.
15. Campbell, R.E., Tour, O., Palmer, A.E., Steinbach, P.A., Baird, G.S., Zacharias, D.A., and Tsien, R.Y. (2002) A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99: 7877-7882.
16. Cao, Z., and Klebba, P.E. (2002) Mechanisms of colicin binding and transport through outer membrane porins. Biochimie 84: 399-412.
17. Cascales, E., and Lloubes, R. (2004) Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51: 873-885.
18. Cascales, E., Gavioli, M., Sturgis, J.N., and Lloubes, R. (2000) Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol 38: 904-915.
19. Cascales, E., Lloubes, R., and Sturgis, J.N. (2001) The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42: 795-807.
20. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J.C., and Lloubes, R. (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184: 754-759.
21. Chen, J.C., and Beckwith, J. (2001) FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol Microbiol 42: 395-413.
22. Chen, J.C., Viollier, P.H., and Shapiro, L. (2005) A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant. Mol Microbiol 55: 1085-1103.
23. Clavel, T., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J.C. (1998) TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29: 359-367.
24. Click, E.M., and Webster, R.E. (1997) Filamentous phage infection: required interactions with the TolA protein. J Bacteriol 179: 6464-6471.
25. Click, E.M., and Webster, R.E. (1998) The TolQRA proteins are required for membrane insertion of the major capsid protein of the filamentous phage f1 during infection. J Bacteriol 180: 1723-1728.
26. Cordell, S.C., Robinson, E.J., and Lowe, J. (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA 100: 7889-7894.
27. Cormack, B.P., Valdivia, R.H., and Falkow, S. (1996) FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173: 33-38.
28. Daniel, R.A., Harry, E.J., and Errington, J. (2000) Role of penicillin-binding protein PBP 2B in assembly and functioning of the division machinery of Bacillus subtilis. Mol Microbiol 35: 299-311.
29. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
30. Davies, J.K., and Reeves, P. (1975) Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A. J Bacteriol 123: 102-117.
31. Deprez, C., Blanchard, L., Guerlesquin, F., Gavioli, M., Simorre, J.P., Lazdunski, C., et al. (2002) Macromolecular import into Escherichia coli: the TolA C-terminal domain changes conformation when interacting with the colicin A toxin. Biochemistry 41: 2589-2598.
32. Derouiche, R., Benedetti, H., Lazzaroni, J.C., Lazdunski, C., and Lloubes, R. (1995) Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins. J Biol Chem 270: 11078-11084.
33. Dubuisson, J.F., Vianney, A., and Lazzaroni, J.C. (2002) Mutational analysis of the TolA C-terminal domain of Escherichia coli and genetic evidence for an interaction between TolA and TolB. J Bacteriol 184: 4620-4625.
34. Dubuisson, J.F., Vianney, A., Hugouvieux-Cotte-Pattat, N., and Lazzaroni, J.C. (2005) Tol-Pal proteins are critical cell envelope components of Erwinia chrysanthemi affecting cell morphology and virulence. Microbiology 151: 3337-3347.
35. Errington, J., Daniel, R.A., and Scheffers, D.J. (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52-65.
36. Feilmeier, B.J., Iseminger, G., Schroeder, D., Webber, H., and Phillips, G.J. (2000) Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J Bacteriol 182: 4068-4076.
37. Fung, J., MacAlister, T.J., and Rothfield, L.I. (1978) Role of murein-lipoprotein in morphogenesis of the bacterial division septum; phenotypic similarity of lkyD and lpo mutants. J Bacteriol 133: 1467-1471.
38. Germon, P., Clavel, T., Vianney, A., Portalier, R., and Lazzaroni, J.C. (1998) Mutational analysis of the Escherichia coli K-12 TolA N-terminal region and characterization of its TolQ-interacting domain by genetic suppression. J Bacteriol 180: 6433-6439.
39. Germon, P., Ray, M.C., Vianney, A., and Lazzaroni, J.C. (2001) Energy-dependent conformational change in the TolA protein of Escherichia coli involves its N-terminal domain, TolQ, and TolR. J Bacteriol 183: 4110-4114.
40. Glasner, J.D., Liss, P., Plunkett III, G., Darling, A., Prasad, T., Rusch, M., et al. (2003) ASAP, a systematic annotation package for community analysis of genomes. Nucleic Acids Res 31: 147-151.
41. Goehring, N.W., and Beckwith, J. (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15: R514-R526.
42. Gueiros-Filho, F.J., and Losick, R. (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16: 2544-2556.
43. Guyer, M.S., Reed, R.R., Steitz, J.A., and Low, K.B. (1981) Identification of a sex-factor-affinity site in E. coli as gamma delta. Cold Spring Harb Symp Quant Biol 45: 135-140.
44. Hale, C.A., and de Boer, P.A.J. (1999) Recruitment of ZipA to the septal ring of Escherichia coli is dependent on FtsZ, and independent of FtsA. J Bacteriol 181: 167-176.
45. Hale, C.A., and de Boer, P.A.J. (2002) ZipA is required for recruitment of FtsK, FtsQ, FtsL, and FtsN to the septal ring in Escherichia coli. J Bacteriol 184: 2552-2556.
46. Heidrich, C., Templin, M.F., Ursinus, A., Merdanovic, M., Berger, J., Schwarz, H., et al. (2001) Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 41: 167-178.
47. 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 Bacteriol 184: 6093-6099.
48. Heilpern, A.J., and Waldor, M.K. (2000) CTXphi infection of Vibrio cholerae requires the tolQRA gene products. J Bacteriol 182: 1739-1747.
49. Henry, T., Pommier, S., Journet, L., Bernadac, A., Gorvel, J.P., and Lloubes, R. (2004) Improved methods for producing outer membrane vesicles in Gram-negative bacteria. Res Microbiol 155: 437-446.
50. Hiemstra, H., de Hoop, M.J., Inouye, M., and Witholt, B. (1986) Induction kinetics and cell surface distribution of Escherichia coli lipoprotein under lac promoter control. J Bacteriol 168: 140-151.
51. Hiemstra, H., Nanninga, N., Woldringh, C.L., Inouye, M., and Witholt, B. (1987) Distribution of newly synthesized lipoprotein over the outer membrane and the peptidoglycan sacculus of an Escherichia coli lac-lpp strain. J Bacteriol 169: 5434-5444.
52. James, R., Penfold, C.N., Moore, G.R., and Kleanthous, C. (2002) Killing of E coli cells by E group nuclease colicins. Biochimie 84: 381-389.
53. DMinC/DicB complexes to septal rings in Escherichia coli suggests a multistep mechanism for MinC-mediated destruction of nascent FtsZ-rings. J Bacteriol 184: 2951-2962.
54. Journet, L., Rigal, A., Lazdunski, C., and Benedetti, H. (1999) Role of TolR N-terminal, central, and C-terminal domains in dimerization and interaction with TolA and TolQ. J Bacteriol 181: 4476-4484.
55. Judd, E.M., Comolli, L.R., Chen, J.C., Downing, K.H., Moerner, W.E., and McAdams, H.H. (2005) Distinct constrictive processes, separated in time and space, divide Caulobacter inner and outer membranes. J Bacteriol 187: 6874-6882.
56. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., and Mori, H. (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. 10.1093/dnares/dsi012. DNA Res 12: 291-299.
57. Lai, E.M., Nair, U., Phadke, N.D., and Maddock, J.R. (2004) Proteomic screening and identification of differentially distributed membrane proteins in Escherichia coli. Mol Microbiol 52: 1029-1044.
58. Lazdunski, C.J. (1995) Colicin import and pore formation: a system for studying protein transport across membranes? Mol Microbiol 16: 1059-1066.
59. Lazdunski, C.J., Bouveret, E., Rigal, A., Journet, L., Lloubes, R., and Benedetti, H. (1998) Colicin import into Escherichia coli cells. J Bacteriol 180: 4993-5002.
60. Lazzaroni, J.C., and Portalier, R. (1992) The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol Microbiol 6: 735-742.
61. Lazzaroni, J.C., Vianney, A., Popot, J.L., Benedetti, H., Samatey, F., Lazdunski, C., et al. (1995) Transmembrane alpha-helix interactions are required for the functional assembly of the Escherichia coli Tol complex. J Mol Biol 246: 1-7.
62. Lazzaroni, J.C., Germon, P., Ray, M.C., and Vianney, A. (1999) The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol Lett 177: 191-197.
63. Lazzaroni, J.C., Dubuisson, J.F., and Vianney, A. (2002) The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins. Biochimie 84: 391-397.
64. Liu, Z., Mukherjee, A., and Lutkenhaus, J. (1999) Recruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31: 1853-1861.
65. Llamas, M.A., Ramos, J.L., and Rodriguez-Herva, J.J. (2000) Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J Bacteriol 182: 4764-4772.
66. Lloubes, R., Cascales, E., Walburger, A., Bouveret, E., Lazdunski, C., Bernadac, A., and Journet, L. (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152: 523-529.
67. Lubkowski, J., Hennecke, F., Pluckthun, A., and Wlodawer, A. (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Structure 7: 711-722.
68. Lutkenhaus, J. (1993) FtsZ ring in bacterial cytokinesis. Mol Microbiol 9: 403-409.
69. MacAlister, T.J., Cook, W.R., Weigand, R., and Rothfield, L.I. (1987) Membrane-murein attachment at the leading edge of the division septum: a second membrane-murein structure associated with morphogenesis of the gram-negative bacterial division septum. J Bacteriol 169: 3945-3951.
70. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6: 862-871.
71. Meury, J., and Devilliers, G. (1999) Impairment of cell division in tolA mutants of Escherichia coli at low and high medium osmolarities. Biol Cell 91: 67-75.
72. Mizuno, T. (1981) A novel peptidoglycan-associated lipoprotein (PAL) found in the outer membrane of Proteus mirabilis and other Gram-negative bacteria. J Biochem (Tokyo) 89: 1039-1049.
73. Mukherjee, A., Cao, C., and Lutkenhaus, J. (1998) Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci USA 95: 2885-2890.
74. Mullineaux, C.W., Nenninger, A., Ray, N., and Robinson, C. (2006) Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J Bacteriol 188: 3442-3448.
75. Nagel de Zwaig, R., and Luria, S.E. (1967) Genetics and physiology of colicin-tolerant mutants of Escherichia coli. J Bacteriol 94: 1112-1123.
76. Ogino, H., Wachi, M., Ishii, A., Iwai, N., Nishida, T., Yamada, S., et al. (2004) FtsZ-dependent localization of GroEL protein at possible division sites. Genes Cells 9: 765-771.
77. Palva, E.T. (1979) Protein interactions in the outer membrane of Escherichia coli. Eur J Biochem 93: 495-503.
78. Parsons, L.M., Lin, F., and Orban, J. (2006) Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45: 2122-2128.
79. Pommier, S., Gavioli, M., Cascales, E., and Lloubes, R. (2005) Tol-dependent macromolecule import through the Escherichia coli cell envelope requires the presence of an exposed TolA binding motif. J Bacteriol 187: 7526-7534.
80. Prouty, A.M., Van Velkinburgh, J.C., and Gunn, J.S. (2002) Salmonella enterica serovar typhimurium resistance to bile: identification and characterization of the tolQRA cluster. J Bacteriol 184: 1270-1276.
81. Ray, M.C., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J.C. (2000) Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction. J Bacteriol 182: 821-824.
82. Riechmann, L., and Holliger, P. (1997) The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell 90: 351-360.
83. Rodolakis, A., Thomas, P., and Starka, J. (1973) Morphological mutants of Escherichia coli. Isolation and ultrastructure of a chain-forming envC mutant. J Gen Microbiol 75: 409-416.
84. Rothfield, L.I., and Justice, S.S. (1997) Bacterial cell division: the cycle of the ring. Cell 88: 581-584.
85. Rothfield, L.I., MacAlister, T.J., and Cook, W.R. (1986) Murein-membrane interactions in cell division. In Bacterial Outer Membranes as Model Systems. Inouye, M. (ed.). New York, NY: John Wiley & Sons, pp. 247-275.
86. Ryan, K.R., and Shapiro, L. (2003) Temporal and spatial regulation in prokaryotic cell cycle progression and development. Annu Rev Biochem 72: 367-394.
87. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
88. Santini, C.L., Bernadac, A., Zhang, M., Chanal, A., Ize, B., Blanco, C., and Wu, L.F. (2001) Translocation of jellyfish green fluorescent protein via the Tat system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J Biol Chem 276: 8159-8164.
89. Schmidt, K.L., Peterson, N.D., Kustusch, R.J., Wissel, M.C., Graham, B., Phillips, G.J., and Weiss, D.S. (2004) A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol 186: 785-793.
90. Shaner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E., and Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567-1572.
91. Siddiqui, R.A., Hoischen, C., Holst, O., Heinze, I., Schlott, B., Gumpert, J., et al. (2006) The analysis of cell division and cell wall synthesis genes reveals mutationally inactivated ftsQ and mraY in a protoplast-type 1-form of Escherichia coli. FEMS Microbiol Lett 258: 305-311.
92. Sturgis, J.N. (2001) Organisation and evolution of the tol-pal gene cluster. J Mol Microbiol Biotechnol 3: 113-122.
93. Sun, T.P., and Webster, R.E. (1986) fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB. J Bacteriol 165: 107-115.
94. Suzuki, H., Nishimura, Y., Yasuda, S., Nishimura, A., Yamada, M., and Hirota, Y. (1978) Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. Mol Gen Genet 167: 1-9.
95. Thomas, J.D., Daniel, R.A., Errington, J., and Robinson, C. (2001) Export of active green fluorescent protein to the periplasm by the twin- arginine translocase (Tat) pathway in Escherichia coli. Mol Microbiol 39: 47-53.
96. Trusca, D., Scott, S., Thompson, C., and Bramhill, D. (1998) Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J Bacteriol 180: 3946-3953.
97. Vianney, A., Muller, M.M., Clavel, T., Lazzaroni, J.C., Portalier, R., and Webster, R.E. (1996) Characterization of the tol-pal region of Escherichia coli K-12: translational control of tolR expression by TolQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein. J Bacteriol 178: 4031-4038.
98. Vicente, M., Rico, A.I., Martinez-Arteaga, R., and Mingorance, J. (2006) Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188: 19-27.
99. Vines, E.D., Marolda, C.L., Balachandran, A., and Valvano, M.A. (2005) Defective O-antigen polymerization in tolA and pal mutants of Escherichia coli in response to extracytoplasmic stress. J Bacteriol 187: 3359-3368.
100. Vischer, N.O.E., Huls, P.G., and Woldringh, C.L. (1994) Object-Image: an interactive image analysis program using structured point collection. Binary 6: 160-166.
101. Walburger, A., Lazdunski, C., and Corda, Y. (2002) The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. Mol Microbiol 44: 695-708.
102. Weigand, R.A., Vinci, K.D., and Rothfield, L.I. (1976) Morphogenesis of the bacterial division septum: a new class of septation-defective mutants. Proc Natl Acad Sci USA 73: 1882-1886.
103. Weiss, D.S. (2004) Bacterial cell division and the septal ring. Mol Microbiol 54: 588-597.
104. Wissel, M.C., and Weiss, D.S. (2004) Genetic analysis of the cell division protein FtsI (PBP3): amino acid substitutions that impair septal localization of FtsI and recruitment of FtsN. J Bacteriol 186: 490-502.
105. Woldringh, C.L. (1976) Morphological analysis of nuclear separation and cell division during the life cycle of Escherichia coli. J Bacteriol 125: 248-257.
106. Yem, D.W., and Wu, H.C. (1978) Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J Bacteriol 133: 1419-1426.
107. Yu, D., Ellis, H.M., Lee, E.C., Jenkins, N.A., Copeland, N.G., and Court, D.L. (2000) An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci USA 97: 5978-5983.