Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box

Molecular Microbiology

Volumn 51, Issue 3, 2004, Pages 873-885

  Cascales, Eric ^a,b   Lloubès, Roland ^a  

^a CNRS and Aix Marseille University   (France)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOPROTEIN; OUTER MEMBRANE PROTEIN A; PEPTIDOGLYCAN; PROTEIN TOLA; PROTEIN TOLB; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CELL DAMAGE; CONTROLLED STUDY; MEMBRANE STABILIZATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CELL WALL; ESCHERICHIA COLI PROTEINS; LIPOPROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDOGLYCAN; PERIPLASMIC PROTEINS; PROTEIN BINDING; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GOSSWEILERODENDRON BALSAMIFERUM;

EID: 1242342946     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03881.x     Document Type: Article

References (65)

1. Abergel, C., Walburger, A., Chenivesse, S., and Lazdunski, C. (2001) Crystallization and preliminary crystallographic study of the peptidoglycan-associated lipoprotein from E. coli. Acta Crystallogr 57: 317-319.
2. Ansaldi, M., Lepelletier, M., and Méjean, V. (1996) Site-specific mutagenesis by using an accurate recombinant polymerase chain reaction method. Anal Biochem 234: 110-111.
3. Bénédetti, H., Lazdunski, C., and Lloubès, R. (1991) Protein Import Into E. coli: collcins A and E1 Interact with a component of their translocation system. EMBO J 10: 1989-1995.
4. Bernadac, A., Gavioli, M., Lazzaroni, J.C., Raina, S., and Lloubès, R. (1998) Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180: 4872-4878.
5. Blair, D., Kim, D., and Berg, H. (1991) Mutant MotB proteins in Escherichia coli. J Bacteriol 173: 4049-4055.
6. Bouveret, E., Derouiche, R., Rigal, A., Lloubès, R., Lazdunski, C., and Bénédetti, H. (1995) Peptidoglycan associated lipoprotein-TolB interaction. J Biol Chem 270: 11071-11077.
7. Bouveret, E., Bénédetti, 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.
8. Bouveret, E., Journet, L., Walburger, A., Cascales, E., Bénédetti, H., and Lloubès, R. (2002) Analysis of the E. coli Tol-Pal and TonB systems by periplasmic production of Tol, TonB, colicin, or phage capsid soluble domains. Biochimie 84: 413-421.
9. Bowden, M., and Kaplan, H. (1998) The Myxococcus xanthus lipopolysaccharide O-antigen is required for social motility and multicellular development. Mol Microbiol 30: 275-284.
10. Braun, V. (1975) Covalent lipoprotein from the outer membrane of E. coli. Biochim Biophys Acta 415: 335-377.
11. Braun, V., and Rehn, K. (1969) Chemical characterization, spatial distribution and function of a lipoprotein (murein lipoprotein) of the Escherichia coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem 10: 426-438.
12. Cadieux, N., and Kadner, R. (1999) Site-directed disulfide bonding reveals an interaction site between energy-coupling protein TonB and BtuB, the outer membrane cobalamin transporter. Proc Natl Acad Sci USA 96: 10673-10678.
13. Cascales, E., Gavioli, M., Sturgis, J.N., and Lloubès, R. (2000) Proton motive force drives the interaction of the inner membrane TolA and outer membrane Pal proteins in E. coli. Mol Microbiol 38: 904-915.
14. Cascales, E., Lloubès, R., and Sturgis, J.N. (2001) The TolQ-TolR proteins energise TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42: 795-807.
15. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J.C., and Lloubès, R. (2002) Pal lipoprotein of E. coli plays a major role in outer membrane integrity. J Bacteriol 184: 754-759.
16. Cavard, D., Crozel, V., Gorvel, J.P., Pattus, F., Baty, D., and Lazdunski, C. (1986) A molecular, genetic and immunological approach to the functioning of colicin A, a pore-forming protein. J Mol Biol 187: 449-459.
17. Choi, D.S., Yamada, H., Mizuno, T., and Mizushima, S. (1986) Trimeric structure and localization of the major lipoprotein in the cell surface of E. coli. J Biol Chem 261: 8953-8957.
18. Clavel, T., Germon, P., Vianney, A., Portalier, R., and Lazzaroni, J.C. (1998) TolB protein of E. coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. Mol Microbiol 29: 359-367.
19. de Cock, H., Pasveer, M., Tommassen, J., and Bouveret, E. (2001) Identification of phospholipids as new components that assist in the in vitro trimerization of a bacterial pore protein. Eur J Biochem 268: 865-875.
20. De Mot, R., and Vanderleyden, J. (1994) The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both gram-positive and gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol Microbiol 12: 333-334.
21. Deprez, C., Blanchard, L., Guerlesquin, F., Gavioli, M., Simorre, J.P., Lazdunski, C., et al. (2002) Macromolecular import into E. coli: the TolA C-terminal domain changes conformation when interacting with the colicin A toxin. Biochemistry 41: 2589-2598.
22. Derouiche, R., Bénédetti, H., Lazzaroni, J.C., Lazdunski, C., and Lloubès, R. (1995) Protein complex within E. coli inner membrane. J Biol Chem 270: 11078-11084.
23. Derouiche, R., Gavioli, M., Bénédetti, H., Prilipov, A., Lazdunski, C., and Lloubès, R. (1996) TolA central domain interacts with E. coli porins. EMBO J 15: 6408-6415.
24. Derouiche, R., Lloubès, R., Sasso, S., Bouteille, H., Oughideni, R., Lazdunski, C., and Loret, E. (1999) Circular dichroism and molecular modeling of the E. coli TolA periplasmic domains. Biospectroscopy 5: 189-198.
25. Dubuisson, J.F., Vianney, A., and Lazzaroni, J.C. (2002) Mutational analysis of the TolA C-terminal domain of E. coli and genetic evidence for an interaction between TolA and TolB. J Bacteriol 184: 4620-4625.
26. Gaspar, J., Thomas, J., Marolda, C., and Valvano, M. (2000) Surface expression of O-specific lipopolysaccharide in E. coli requires the function of the TolA protein. Mol Microbiol 38: 262-275.
27. Gennity, J.M., and Inouye, M. (1991) The protein sequence responsible for lipoprotein membrane localization in E. coli exhibits remarkable specificity. J Biol Chem 266: 16458-16464.
28. Germon, P., Clavel, T., Vianney, A., Portalier, R., and Lazzaroni, J.-C. (1998) Mutational analyses of the E. coli K-12 TolA N-terminal region and characterization of its TolQ-interacting domain by genetic suppression. J Bacteriol 180: 6433-6439.
29. Germon, P., Ray, M.C., Vianney, A., and Lazzaroni, J.C. (2001) Energy-dependent conformational change in the TolA protein of E. coli involves its N-terminal domain, TolQ and TolR. J Bacteriol 183: 4110-4114.
30. Gokce, I., Raggett, E., Hong, Q., Virden, R., Cooper, A., and Lakey, J. (2000) The TolA-recognition site of colicin N. ITC, SPR and stopped-flow fluorescence define a crucial 27-residue segment. J Mol Biol 304: 621-632.
31. Gudmundsdottir, A., Bell, P., Lundrigan, M., Bradbeer, C., and Kadner, R. (1989) Point mutations in a conserved region (TonB box) of Escherichia coli outer membrane protein BtuB affect vitamin B12 transport. J Bacteriol 171: 6526-6533.
32. Isnard, M., Rigal, A., Lazzaroni, J.C., Lazdunski, C., and Lloubès, R. (1994) Maturation and localization of the TolB protein required for colicin import. J Bacteriol 176: 6392-6396.
33. Journet, L., Rigal, A., Lazdunski, C., and Bénédetti, H. (1999) Role of TolR N-terminal, central and C-terminal domains in its dimerisation and interaction with TolA and TolQ. J Bacteriol 181: 4476-4484.
34. Journet, L., Bouveret, E., Rigal, A., Lloubès, R., Lazdunski, C., and Bénédetti, H. (2001) The translocation domain of colicin A interacts with at least three different proteins of the Tol system by three distinct regions. Mol Microbiol 42: 331-344.
35. Koebnik, R. (1995) Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol Microbiol 16: 1269-1270.
36. Koebnik, R., Locher, K., and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37: 239-253.
37. Lazdunski, C., Bouveret, E., Rigal, A., Journet, L., Lloubès, R., and Bénédetti, H. (1998) Colicin import into Escherichia coli cells. J Bacteriol 180: 4993-5002.
38. Lazzaroni, J.C., and Portalier, R. (1981) Genetic and biochemical characterization of periplasmic-leaky mutants of E. coli K-12. J Bacteriol 145: 1351-1358.
39. Lazzaroni, J.C., and Portalier, R. (1992) The excC gene of E. coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (Pal). Mol Microbiol 6: 735-742.
40. Lazzaroni, J.C., Vianney, A., Popot, J.L., Bénédetti, H., Samatey, F., Lazdunski, C., et al. (1995) Transmembrane α-helix interactions are required for the functional assembly of the E. coli Toi complex. J Mol Biol 246: 1-7.
41. Leduc, M., Ishidate, K., Shakibai, N., and Rothfield, L. (1992) Interactions of E. coli membrane lipoproteins with the murein sacculus. J Bacteriol 174: 7982-7988.
42. Lubkowski, J., Hennecke, F., Plückthun, A., and Wlodawer, A. (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA. Struct Fold Des 7: 711-722.
43. Matsuyama, S., Tajima, T., and Tokuda, H. (1995) A novel periplasmic carrier protein involved In the sorting and transport of Escherichia coli lipoproteins destined for the outer membrane. EMBO J 14: 3365-3372.
44. Matsuyama, S., Yokota, N., and Tokuda, H. (1997) A novel outer membrane lipoprotein, LolB (HemM), involved in the LolA (p20)-dependent localization of lipoproteins to the outer membrane of Escherichia coli. EMBO J 16: 6947-6955.
45. Mizuno, T. (1979) A novel peptidoglycan-associated lipoprotein found in the cell envelope of Pseudomonas aeruginosa and Escherichia coli. J Biochem (Tokyo) 86: 991-1000.
46. Nagel de Zwaig, R., and Luria, S. (1967) Genetics and physiology of colicin-tolerant mutants of E. coli. J Bacteriol 94: 1112-1123.
47. Nomura, M., and Witten, C. (1967) Interaction of colicins with bacterial cells. 3. Colicin-tolerant mutations in Escherichia coli. J Bacteriol 94: 1093-1111.
48. Palva, E. (1979) Protein interactions in the outer membrane of E. coli. Eur J Biochem 93: 495-503.
49. Raetz, C. (1996) Bacterial lipopolysaccharides: a remarkable family of bioactive macroamphiphiles. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C. (ed.). Washington, DC: American Society for Microbiology Press.
50. Raggett, E., Bainbridge, G., Evans, L., Cooper, A., and Lakey, J. (1998) Discovery of critical Tol A-binding residues in the bactericidal toxin colicin N: a biophysical approach. Mol Microbiol 28: 1335-1343.
51. 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.
52. 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.
53. Rigal, A., Bouveret, E., Lloubès, R., Lazdunski, C., and Bénédetti, H. (1997) The TolB protein interacts with the porins of E. coli. J Bacteriol 179: 7274-7279.
54. Shu, W., Liu, J., Ji, H., and Lu, M. (2000) Core structure of the outer membrane lipoprotein from Escherichia coli at 1.9 A resolution. J Mol Biol 299: 1101-1112.
55. Sturgis, J.N. (2001) Organization and evolution of the tol-pal gene cluster. J Mol Microbiol Biotechnol 3: 113-122.
56. Sun, T., and Webster, R. (1987) Nucleotide sequence of a gene cluster involved in entry of E colicins and single-stranded DNA of infecting filamentous bacteriophages into E. coli. J Bacteriol 169: 2667-2674.
57. Suzuki, H., Nishimura, Y., Yasuda, S., Nishimura, A., Yamada, M., and Hirota, Y. (1978) Murein-lipoprotein of E. coli: a protein involved in the stabilization of bacterial cell envelope. Mol Gen Genet 167: 1-9.
58. Tabor, S., and Richardson, C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074-1078.
59. Vianney, A., Muller, M., Clavel, T., Lazzaroni, J.C., Portalier, R., and Webster, R. (1996) Characterization of the tol-pal region of E. coli K-12: translational control of tolR expression by ToIQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein. J Bacteriol 178: 4031-4038.
60. 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.
61. Witty, M., Sanz, C., Shah, A., Grossmann, J., Mizuguchi, K., Perham, R., and Luisi, B. (2002) Structure of the periplasmic domain of Pseudomonas aeruginosa TolA: evidence for an evolutionary relationship with the TonB transporter protein. EMBO J 21: 4207-4218.
62. Yakushi, T., Masuda, K., Narita, S., Matsuyama, S., and Tokuda, H. (2000) A new ABC transporter mediating the detachment of lipid-modified proteins from membranes. Nature Cell Biol 2: 212-218.
63. Yem, D., and Wu, H. (1978) Physiological characterization of an E. coli mutant altered in the structure of murein lipoprotein. J Bacteriol 133: 1418-1426.
64. Yokota, N., Koruda, T., Matsuyama, S., and Tokuda, H. (1999) Characterization of the LolA-LolB system as the general lipoprotein localization mechanism of E. coli. J Biol Chem 274: 30995-30999.
65. Youderian, P., Burke, N., White, D., and Hartzell, P. (2003) Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49: 555-570.