Role of TolR N-terminal, central, and C-terminal domains in dimerization and interaction with TolA and TolQ

Journal of Bacteriology

Volumn 181, Issue 15, 1999, Pages 4476-4484

  Journet, Laure ^a   Rigal, Alain ^a   Lazdunski, Claude ^a   Bénédetti, Hélène ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; COLICIN A; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL MEMBRANE; CARBOXY TERMINAL SEQUENCE; CROSS LINKING; DIMERIZATION; ESCHERICHIA COLI; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GOSSWEILERODENDRON BALSAMIFERUM; NEGIBACTERIA;

EID: 0032794147     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.15.4476-4484.1999     Document Type: Article

References (55)

1. Bachman, B. J. 1987. Derivatives and genotypes of some mutant derivatives of Escherichia coli K-12, p. 1190-1219. In F. C. Neidhardt, J. L. Ingraham, K. B. Low, B. Magasanik, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, D.C.
2. Bénédetti, H., and V. Géli. 1996. Colicin transport, channel formation and inhibition, p. 665-691. In W. N. Konings, H. R. Kaback, and J. S. Lolkema (ed.), Handbook of biological physics, vol. 2. Elsevier Science, New York, N.Y.
3. Bernadac, A., M. Gavioli, J. C. Lazzaroni, S. Raina, and R. Lloubès. 1998. Escherichia coli tot/pal mutants form outer membrane vesicles. J. Bacteriol. 180:4872-4878.
4. Bourdineaud, J. P., S. P. Howard, and C. Lazdunski. 1989. Localization and assembly onto the Escherichia coli envelope of a protein required for entry of colicin A. J. Bacteriol. 171:2458-2465.
5. Bouveret, E., R. Derouiche, A. Rigal, R. Lloubès, C. Lazdunski, and H. Bénédetti. 1995. Peptidoglycan-associated lipoprotein-TolB interaction. J. Biol. Chem. 270:11071-11077.
6. Bouveret, E., A. Rigal, C. Lazdunski, and H. Bénédetti. 1997. The N-terminal domain of colicin E3 interacts with TolB which is involved in the colicin translocation step. Mol. Microbiol. 23:909-920.
7. Bouveret, E., A. Rigal, C. Lazdunski, and H. Bénédetti. 1998. Distinct regions of the colicin A translocation domain are involved in the interaction with TolA and TolB proteins upon import into Escherichia coli. Mol. Microbiol. 27:143-157.
8. Bradbeer, C. 1993. The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J. Bacteriol. 175:3146-3150.
9. Braun, V. 1989. The structurally related exbB and tolQ genes are interchangeable in conferring tonB-dependent colicin, bacteriophage, and albomycin sensitivity. J. Bacteriol. 171:6387-6390.
10. Braun, V., and C. Hermann. 1993. Evolutionary relation 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.
11. Braun, V., S. Gaisser, C. Herrmann, K. Kampfenkel, H. Killmann, and I. Traub. 1996. Energy-coupled transport across the outer membrane of Escherichia coli: ExbB binds ExbD and TonB in vitro, and leucine 132 in the periplasmic region and aspartate 25 in the transmembrane region are important for ExbD activity. J. Bacteriol. 178:2836-2845.
12. Cavard, D., A. Bernadac, J. M. Pagès, and C. Lazdunski. 1984. Colicins are not transiently accumulated in the periplasmic space before release from colicinogenic cells. Biol. Cell 51:79-86.
13. Cavard, D., V. Crozel, J. P. Gorvel, F. Pattus, D. Baty, and C. Lazdunski. 1986. A molecular, genetic and immunological approach to the functioning of colicin A, a pore-forming protein. J. Mol. Biol. 187:449-459.
14. Clavel, T., P. Germon, A. Vianney, R. Portaller, and J. C. Lazzaroni. 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.
15. 14a. Corda, Y., et al. Unpublished data.
16. Davies, J. K., and P. Reeves. 1975. Genetics of resistance to colicins in Escherichia coli K-12. Cross-resistance among colicins of group B. J. Bacteriol. 123:96-101.
17. Davies, J. K., and P. Reeves. 1975. Genetics of resistance to colicins in Escherichia coli K-12. Cross-resistance among colicins of group A. J. Bacteriol. 123:102-117.
18. Deich, R. A., B. N. J. Metcalf, C. W. Finn, J. E. Farley, and B. A. Green. 1988. Cloning of genes encoding a 15,000-dalton peptidoglycan-associated outer membrane lipoprotein and an antigenically related 15,000-dalton protein from Haemophilus influenzae. J. Bacteriol. 170:489-498.
19. Derouiche, R., H. Bénédetti, J. C. Lazzaroni, C. Lazdunski, and R. Lloubès. 1995. Protein complex within Escherichia coli inner membrane - TolA N-terminal domain interacts with TolQ and TolR proteins. J. Biol. Chem. 270: 11078-11084.
20. Derouiche, R., M. Gavloli, H. Bénédetti, A. Prilipov, C. Lazdunski, and R. Lloubès. 1997. TolA central domain interacts with Escherichia coli porins. EMBO J. 15:6408-6415.
21. Fognini-Lefebvre, N., J. C. Lazzaroni, and R. Portalier. 1987. tolA, tolB and excC, three cistrons involved in the control of pleiotropic release of periplasmic proteins by Escherichia coli K12. Mol. Gen. Genet. 209:391-395.
22. Géli, V., D. Baty, and C. Lazdunski. 1988. Use of a foreign epitope as a tag for the localization of minor proteins: the case of the immunity protein to colicin A. Proc. Natl. Acad. Sci. USA 85:689-693.
23. Germon, P., T. Clavel, A. Vianney, R. Portalier, and J. C. Lazzaroni. 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.
24. Ghrayeb, J., H. Kimura, M. Takahara, H. Hsiung, Y. Masui, and M. Inouye. 1984. Secretion cloning vectors in Escherichia coli. EMBO J. 3:2437-2442.
25. Gorvel, J. P., A. Rigal, J. Sarles, and S. Maroux. 1985. Aminopeptidase N and human blood group A-antigenicity along the digestive tract and associated glands in the rabbit. Cell Tissue Res. 239:241-248.
26. Guihard, G., P. Boulanger, H. Bénédetti, R. Lloubès, M. Besnard, and L. Letellier. 1994. Colicin A and the Tol proteins involved in its translocation are preferentially located in the contact sites between the inner and outer membranes of Escherichia coli cells. J. Biol. Chem. 269:5874-5880.
27. Higgs, P. I., P. S. Myers, and K. Postle. 1998. Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J. Bacteriol. 180:6031-6038.
28. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extinction using the polymerase chain reaction. Gene 77:51-59.
29. Ishidate, K., E. S. Creeger, J. Zike, S. Deb, B. Glauner, T. J. MacAlister, and L. I. Rothfield. 1986. Isolation and differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J. Biol. Chem. 261:428-443.
30. Isnard, M., A. Rigal, J. C. Lazzaroni, C. Lazdunski, and R. Lloubès. 1994. Maturation and localization of the TolB protein required for colicin import. J. Bacteriol. 176:6392-6396.
31. Jaskula, J. C., T. E. Letain, S. K. Roof, J. T. Skare, and K. Postle. 1994. Role of the TonB amino terminus in energy transduction between membranes. J. Bacteriol. 175:2326-2338.
32. Jiang, X., M. A. Payne, Z. Cao, S. B. Foster, J. B. Feix, M. C. Newton, and P. E. Klebba. 1997. Ligand-specific opening of a gated-porin channel in the outer membrane of living bacteria. Science 276:1261-1264.
33. Kadner, R. J., C. V. Franklund, and J. T. Lathrop. 1996. Communication between membranes in TonB-dependent transport across the bacterial outer membrane, p. 637-664. In W. N. Konings, H. R. Kaback, and J. S. Lolkema (ed.), Handbook of biological physics, vol. 2. Elsevier Science, New York, N.Y.
34. Karlsson, M., K. Hannavy, and C. F. Higgins. 1993. A sequence-specific function for the N-terminal signal-like sequence of the TonB protein. Mol. Microbiol. 8:379-388.
35. Koebnik, R. 1993. The molecular interaction between components of the TonB-ExbBD-dependent and the TolQRA-dependent bacterial uptake systems. Mol. Microbiol. 9:219.
36. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
37. Larsen, R. A., M. G. Thomas, G. E. Wood, and K. Postle. 1994. Partial suppression of an Escherichia coli TonB transmembrane domain mutation (D17V) by a missense mutation in ExbB. Mol. Microbiol. 13:627-640.
38. Lazdunski, C. J., E. Bouveret, A. Rigal, L. Journet, R. Lloubes, and H. Bénédetti. 1998. Colicin import into Escherichia coli cells. J. Bacteriol. 180: 4993-5002.
39. Lazzaroni, J. C., and R. Portalier. 1981. Genetic and biochemical characterization of periplasmic-leaky mutants of Escherichia coli K-12. J. Bacteriol. 145:1351-1358.
40. Lazzaroni, J. C., A. Vianney, J. L. Popot, H. Benedetti, F. Samatey, C. Lazdunski, R. Portalier, and V. Geli. 1995. Transmembrane alpha-helix interactions are required for the functional assembly of the Escherichia coli Tol complex. J. Mol. Biol. 246:1-7.
41. Letain, T. E., and K. Postle. 1997. TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol. Microbiol. 24:271-283.
42. Lim, A., Jr., D. De Vos, M. Brauns, D. Mossialos, A. Gaballa, D. Quing, and P. Cornelis. 1997. Molecular and immunological characterization of Opr1, the 18 kDa outer membrane peptidoglycan-associated lipoprotein (PAL) of Pseudomonos aeruginosa. Microbiology 143:1709-1711.
43. Miller, J. H. 1992. A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria, p. 435-447. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
44. Pérez-Pérez, J., and J. Gutierrez. 1995. An arabinose-inducible expression vector, pART3, compatible with ColE1-derived plasmids. Gene 158:141-142.
45. Postle, K., and J. T. Skare. 1988. Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J. Biol. Chem. 263:11000-11007.
46. Rigal, A., E. Bouveret, R. Lloubes, C. Lazdunski, and H. Bénédetti. 1997. The TolB protein interacts with the porins of Escherichia coli. J. Bacteriol. 179:7274-7279.
47. Rodríguez-Herva, J. J., M. I. Ramos-González, and J. L. Ramos. 1996. The Pseudomonas putida peptidoglycan-associated outer membrane lipoprotein is involved in maintenance of the integrity of the cell envelope. J. Bacteriol. 178:1699-1706.
48. Rutz, J. M., J. Liu, J. A. Lyons, J. Gotanson, S. K. Armstrong, M. A. McIntosh, J. B. Feix, and P. E. Klebba. 1992. Formation of a gated channel by a ligand-specific transport protein in the bacterial membrane. Science 258: 471-475.
49. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
50. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
51. Skare, J. T., B. M. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vitro to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
52. Sun, T. P., and R. E. Webster. 1986. fii, a bacterial locus required for filamentous phage infection, and its relation to colicin-tolerant tolA and tolB. J. Bacteriol. 165:107-115.
53. Tibor, A., V. Weynants, P. Denoel, B. Lichtfouse, X. de Bolle, E. Saman, J. N. Limet, and J. J. Letesson. 1994. Molecular cloning, nucleotide sequence, and occurrence of a 16.5-kilodalton outer membrane protein of Brucella abortus with similarity to PAL lipoproteins. Infect. Immun. 62:3633-3639.
54. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
55. Vianney, A., M. M. Muller, T. Clavel, J. C. Lazzaroni, R. Portalier, and R. E. Webster. 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.