Energetics of colicin import revealed by genetic cross-complementation between the Tol and Ton systems

Biochemical Society Transactions

Volumn 40, Issue 6, 2012, Pages 1480-1485

  Lloubès, Roland ^a   Goemaere, Emilie ^a   Zhang, Xiang ^a   Cascales, Eric ^a   Duché, Denis ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Colicin; Cross complementation; Tol system; Ton system; Transmembrane helix

Indexed keywords

COLICIN; COLICIN 5; COLICIN A; COLICIN B; COLICIN D; COLICIN E9; COLICIN LA; COLICIN M; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; BACTERIAL GENETICS; BACTERIAL MEMBRANE; CONFERENCE PAPER; ENERGY TRANSFER; IMMUNITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TOL SYSTEM; TON SYSTEM;

AMINO ACID SUBSTITUTION; COLICINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; MEMBRANE POTENTIALS; MEMBRANE PROTEINS; PERIPLASMIC PROTEINS; PHENOTYPE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SUBUNITS; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS); GOSSWEILERODENDRON BALSAMIFERUM;

EID: 84870207309     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120181     Document Type: Conference Paper

References (55)

1. Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H. and de Boer, P.A. (2007) 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. Mol. Microbiol. 63, 1008-1025 (Pubitemid 46188263)
2. Lloubès, 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 (Pubitemid 32635246)
3. 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 Escherichia coli. Mol. Microbiol. 38, 904-915
4. Cascales, E., Lloubès, 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 (Pubitemid 33064487)
5. 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 (Pubitemid 32568060)
6. Bonsor, D.A., Hecht, O., Vankemmelbeke, M., Sharma, A., Krachler, A.M., Housden, N.G., Lilly, K.J., James, R., Moore, G.R. and Kleanthous, C. (2009) Allosteric β-propeller signalling in TolB and its manipulation by translocating colicins. EMBO J. 28, 2846-2857
7. Schauer, K., Rodionov, D.A. and de Reuse, H. (2008) New substrates for TonB-dependent transport: do we only see the 'tip of the iceberg'? Trends Biochem. Sci. 33, 330-338
8. Postle, K. and Kadner, R.J. (2003) Touch and go: tying TonB to transport. Mol. Microbiol. 49, 869-882 (Pubitemid 36981335)
9. Cadieux, N., Barekzi, N. and Bradbeer, C. (2007) Observations on the calcium dependence and reversibility of cobalamin transport across the outer membrane of Escherichia coli. J. Biol. Chem. 282, 34921-34928 (Pubitemid 350232451)
10. Larsen, R.A., Thomas, M.G. and Postle, K. (1999) Proton motive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol. Microbiol. 31, 1809-1824 (Pubitemid 29151279)
11. 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
12. 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 (Pubitemid 23124543)
13. Koebnik, R. (1993) The molecular interaction between components of the TonB-ExbBD-dependent and of the TolQRA-dependent bacterial uptake systems. Mol. Microbiol. 9, 219
14. Guihard, G., Boulanger, P., Benedetti, H., Lloubes, R., Besnard, M. and Letellier, L. (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 (Pubitemid 24242964)
15. 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 (Pubitemid 29006053)
16. Higgs, P.I., Larsen, R.A. and Postle, K. (2002) Quantification of known components of the Escherichia coli TonB energy transduction system: TonB, ExbB, ExbD and FepA. Mol. Microbiol. 44, 271-281 (Pubitemid 34429781)
17. Held, K.G. and Postle, K. (2002) ExbB and ExbD do not function independently in TonB-dependent energy transduction. J. Bacteriol. 184, 5170-5173 (Pubitemid 34971043)
18. Pramanik, A., Hauf, W., Hoffmann, J., Cernescu, M., Brutschy, B. and Braun, V. (2011) Oligomeric structure of ExbB and ExbB-ExbD isolated from Escherichia coli as revealed by LILBID mass spectrometry. Biochemistry 50, 8950-8956
19. 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
20. Kohler, S.D., Weber, A., Howard, S.P., Welte, W. and Drescher, M. (2010) The proline-rich domain of TonB possesses an extended polyproline II-like conformation of sufficient length to span the periplasm of Gram-negative bacteria. Protein Sci. 19, 625-630
21. Chang, C., Mooser, A., Pluckthun, A. and Wlodawer, A. (2001) Crystal structure of the dimeric C-terminal domain of TonB reveals a novel fold. J. Biol. Chem. 276, 27535-27540
22. Deprez, C., Lloubès, R., Gavioli, M., Marion, D., Guerlesquin, F. and Blanchard, L. (2005) Solution structure of the E. coli TolA C-terminal domain reveals conformational changes upon binding to the phage g3p N-terminal domain. J. Mol. Biol. 346, 1047-1057 (Pubitemid 40215529)
23. Kodding, J., Killig, F., Polzer, P., Howard, S.P., Diederichs, K. and Welte, W. (2005) Crystal structure of a 92-residue C-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J. Biol. Chem. 280, 3022-3028 (Pubitemid 40189412)
24. Braun, V., Patzer, S.I. and Hantke, K. (2002) Ton-dependent colicins and microcins: modular design and evolution. Biochimie 84, 365-380 (Pubitemid 35350867)
25. Vankemmelbeke, M., Zhang, Y., Moore, G.R., Kleanthous, C., Penfold, C.N. and James, R. (2009) Energy-dependent immunity protein release during Tol-dependent nuclease colicin translocation. J. Biol. Chem. 284, 18932-18941
26. Bourdineaud, J.P., Boulanger, P., Lazdunski, C. and Letellier, L. (1990) In vivo properties of colicin A: channel activity is voltage dependent but translocation may be voltage independent. Proc. Natl. Acad. Sci. U.S.A. 87, 1037-1041
27. Jakes, K.S. and Finkelstein, A. (2010) The colicin Ia receptor, Cir, is also the translocator for colicin Ia. Mol. Microbiol. 75, 567-578
28. Zakharov, S.D. and Cramer, W.A. (2004) On the mechanism and pathway of colicin import across the E. coli outer membrane. Front. Biosci. 9, 1311-1317 (Pubitemid 39060844)
29. Duché, D. (2007) Colicin E2 is still in contact with its receptor and import machinery when its nuclease domain enters the cytoplasm. J. Bacteriol. 189, 4217-4222
30. Mende, J. and Braun, V. (1990) Import-defective colicin B derivatives mutated in the TonB box. Mol. Microbiol. 4, 1523-1533
31. Benedetti, H., Lazdunski, C. and Lloubès, R. (1991) Protein import into Escherichia coli: colicins A and E1 interact with a component of their translocation system. EMBO J. 10, 1989-1995 (Pubitemid 21905668)
32. Bouveret, E., Journet, L., Walburger, A., Cascales, E., Benedetti, H. and Lloubès, 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 (Pubitemid 35350871)
33. Pommier, S., Gavioli, M., Cascales, E. and Lloubès, 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 (Pubitemid 41507808)
34. Barneoud-Arnoulet, A., Gavioli, M., Lloubès, R. and Cascales, E. (2010) Interaction of the colicin K bactericidal toxin with components of its import machinery in the periplasm of Escherichia coli. J. Bacteriol. 192, 5934-5942
35. Cascales, E., Buchanan, S.K., Duché, D., Kleanthous, C., Lloubès, R., Postle, K., Riley, M., Slatin, S. and Cavard, D. (2007) Colicin biology. Microbiol. Mol. Biol. Rev. 71, 158-229 (Pubitemid 46456687)
36. Kleanthous, C. (2010) Swimming against the tide: progress and challenges in our understanding of colicin translocation. Nat. Rev. Microbiol. 8, 843-848
37. Loftus, S.R., Walker, D., Maté, M.J., Bonsor, D.A., James, R., Moore, G.R. and Kleanthous, C. (2006) Competitive recruitment of the periplasmic translocation portal TolB by a natively disordered domain of colicin E9. Proc. Natl. Acad. Sci. U.S.A. 103, 12353-12358 (Pubitemid 44267263)
38. Bonsor, D.A., Grishkovskaya, I., Dodson, E.J. and Kleanthous, C. (2007) Molecular mimicry enables competitive recruitment by a natively disordered protein. J. Am. Chem. Soc. 129, 4800-4807 (Pubitemid 46648779)
39. Deprez, C., Blanchard, L., Guerlesquin, F., Gavioli, M., Simorre, J.P., Lazdunski, C., Marion, D. and Lloubès, R. (2002) Macromolecular import into Escherichia coli: the TolA C-terminal domain changes conformation when interacting with the colicin A toxin. Biochemistry 41, 2589-2598 (Pubitemid 34168928)
40. Hecht, O., Zhang, Y., Li, C., Penfold, C.N., James, R. and Moore, G.R. (2010) Characterisation of the interaction of colicin A with its co-receptor TolA. FEBS Lett. 584, 2249-2252
41. Howard, S.P., Herrmann, C., Stratilo, C.W. and Braun, V. (2001) In vivo synthesis of the periplasmic domain of TonB inhibits transport through the FecA and FhuA iron siderophore transporters of Escherichia coli. J. Bacteriol. 183, 5885-5895 (Pubitemid 32917407)
42. Henry, T., Pommier, S., Journet, L., Bernadac, A., Gorvel, J.P. and Lloubès, R. (2004) Improved methods for producing outer membrane vesicles in Gram-negative bacteria. Res. Microbiol. 155, 437-446 (Pubitemid 38900823)
43. Brinkman, K.K. and Larsen, R.A. (2008) Interactions of the energy transducer TonB with noncognate energy-harvesting complexes. J. Bacteriol. 190, 421-427
44. Bradbeer, C. (1993) The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J. Bacteriol. 175, 3146-3150
45. Karlsson, M., Hannavy, K. and Higgins, C.F. (1993) A sequence-specific function for the N-terminal signal-like sequence of the TonB protein. Mol. Microbiol. 8, 379-388 (Pubitemid 23124554)
46. Goemaere, E.L., Cascales, E. and Lloubès, R. (2007) Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. J. Mol. Biol. 366, 1424-1436 (Pubitemid 46215605)
47. Zhai, Y.F., Heijne, W. and Saier, Jr, M.H. (2003) Molecular modeling of the bacterial outer membrane receptor energizer, ExbBD/TonB, based on homology with the flagellar motor, MotAB. Biochim. Biophys. Acta 1614, 201-210 (Pubitemid 36929984)
48. Terashima, H., Kojima, S. and Homma, M. (2010) Functional transfer of an essential aspartate for the ion-binding site in the stator proteins of the bacterial flagellar motor. J. Mol. Biol. 397, 689-696
49. Braun, V. and Herrmann, C. (2004) Point mutations in transmembrane helices 2 and 3 of ExbB and TolQ affect their activities in Escherichia coli K-12. J. Bacteriol. 186, 4402-4406 (Pubitemid 38802592)
50. Goemaere, E.L., Devert, A., Lloubès, R. and Cascales, E. (2007) Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex. J. Biol. Chem. 282, 17749-17757 (Pubitemid 47100307)
51. Zhang, X.Y., Goemaere, E.L., Thome, R., Gavioli, M., Cascales, E. and Lloubès, R. (2009) Mapping the interactions between Escherichia coli Tol subunits: rotation of the TolR transmembrane helix. J. Biol. Chem. 284, 4275-4282
52. Devanathan, S. and Postle, K. (2007) Studies on colicin B translocation: FepA is gated by TonB. Mol. Microbiol. 65, 441-453 (Pubitemid 47052733)
53. Duche, D., Frenkian, A., Prima, V. and Lloubès, R. (2006) Release of immunity protein requires functional endonuclease colicin import machinery. J. Bacteriol. 188, 8593-8600 (Pubitemid 44894060)
54. Zakharov, S.D., Sharma, O., Zhalnina, M.V. and Cramer, W.A. (2008) Primary events in the colicin translocon: FRET analysis of colicin unfolding initiated by binding to BtuB and OmpF. Biochemistry 47, 12802-12809
55. Matlack, K.E., Misselwitz, B., Plath, K. and Rapoport, T.A. (1999) BiP acts as a molecular ratchet during post-translational transport of prepro-α factor across the ER membrane. Cell 97, 553-564 (Pubitemid 29256959)