Pal Lipoprotein of Escherichia Coli Plays a Major Role in Outer Membrane Integrity

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2002 Jan 16

PMID 11790745

Citations 144

Authors

Eric Cascales

Alain Bernadac

Marthe Gavioli

Jean-Claude Lazzaroni

Roland Lloubes

Affiliations

Soon will be listed here.

Abstract

The Tol-Pal system of gram-negative bacteria is composed of five proteins. TolA, TolQ, and TolR are inner membrane proteins, TolB is a periplasmic protein, and Pal, the peptidoglycan-associated lipoprotein, is anchored to the outer membrane. In this study, the roles of Pal and major lipoprotein Lpp were compared in Escherichia coli. lpp and tol-pal mutations have previously been found to perturb the outer membrane permeability barrier and to cause the release of periplasmic proteins and the formation of outer membrane vesicles. In this study, we showed that the overproduction of Pal is able to restore the outer membrane integrity of an lpp strain but that overproduced Lpp has no effect in a pal strain. Together with the previously reported observation that overproduced TolA complements an lpp but not a pal strain, these results indicate that the cell envelope integrity is efficiently stabilized by an epistatic Tol-Pal system linking inner and outer membranes. The density of Pal was measured and found to be lower than that of Lpp. However, Pal was present in larger amounts compared to TolA and TolR proteins. The oligomeric state of Pal was determined and a new interaction between Pal and Lpp was demonstrated.

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References

Ray M, Germon P, Vianney A, Portalier R, Lazzaroni J . Identification by genetic suppression of Escherichia coli TolB residues important for TolB-Pal interaction. J Bacteriol. 2000; 182(3):821-4. PMC: 94349. DOI: 10.1128/JB.182.3.821-824.2000. View

Journet L, Rigal A, Lazdunski C, Benedetti H . Role of TolR N-terminal, central, and C-terminal domains in dimerization and interaction with TolA and tolQ. J Bacteriol. 1999; 181(15):4476-84. PMC: 103575. DOI: 10.1128/JB.181.15.4476-4484.1999. View

Shu W, Liu J, Ji H, Lu M . Core structure of the outer membrane lipoprotein from Escherichia coli at 1.9 A resolution. J Mol Biol. 2000; 299(4):1101-12. DOI: 10.1006/jmbi.2000.3776. View

Bouveret E, Benedetti H, Rigal A, Loret E, Lazdunski C . In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J Bacteriol. 1999; 181(20):6306-11. PMC: 103764. DOI: 10.1128/JB.181.20.6306-6311.1999. View

Yokota N, Kuroda T, Matsuyama S, Tokuda H . Characterization of the LolA-LolB system as the general lipoprotein localization mechanism of Escherichia coli. J Biol Chem. 1999; 274(43):30995-9. DOI: 10.1074/jbc.274.43.30995. View

Koebnik R, Locher K, Van Gelder P . Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol. 2000; 37(2):239-53. DOI: 10.1046/j.1365-2958.2000.01983.x. View

Gaspar J, Thomas J, Marolda C, Valvano M . Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the function of the TolA protein. Mol Microbiol. 2000; 38(2):262-75. DOI: 10.1046/j.1365-2958.2000.02094.x. View

Cascales E, Gavioli M, Sturgis J, Lloubes R . Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol. 2000; 38(4):904-15. DOI: 10.1046/j.1365-2958.2000.02190.x. View

Sturgis J . Organisation and evolution of the tol-pal gene cluster. J Mol Microbiol Biotechnol. 2001; 3(1):113-22. View

10.

Abergel C, Walburger A, Chenivesse S, Lazdunski C . Crystallization and preliminary crystallographic study of the peptidoglycan-associated lipoprotein from Escherichia coli. Acta Crystallogr D Biol Crystallogr. 2001; 57(Pt 2):317-9. DOI: 10.1107/s0907444900019739. View

11.

Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A . The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity?. Res Microbiol. 2001; 152(6):523-9. DOI: 10.1016/s0923-2508(01)01226-8. View

12.

Cascales E, Lloubes R, Sturgis J . The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol. 2001; 42(3):795-807. DOI: 10.1046/j.1365-2958.2001.02673.x. View

13.

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. 1969; 10(3):426-38. DOI: 10.1111/j.1432-1033.1969.tb00707.x. View

14.

Braun V . Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim Biophys Acta. 1975; 415(3):335-77. DOI: 10.1016/0304-4157(75)90013-1. View

15.

Yem D, Wu H . Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. J Bacteriol. 1978; 133(3):1419-26. PMC: 222180. DOI: 10.1128/jb.133.3.1419-1426.1978. View

16.

Suzuki H, Nishimura Y, Yasuda S, Nishimura A, Yamada M, Hirota Y . Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. Mol Gen Genet. 1978; 167(1):1-9. DOI: 10.1007/BF00270315. View

17.

Palva E . Protein interactions in the outer membrane of Escherichia coli. Eur J Biochem. 1979; 93(3):495-503. DOI: 10.1111/j.1432-1033.1979.tb12848.x. View

18.

Mizuno T . A novel peptidoglycan-associated lipoprotein found in the cell envelope of Pseudomonas aeruginosa and Escherichia coli. J Biochem. 1979; 86(4):991-1000. DOI: 10.1093/oxfordjournals.jbchem.a132631. View

19.

Towbin H, Staehelin T, Gordon J . Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979; 76(9):4350-4. PMC: 411572. DOI: 10.1073/pnas.76.9.4350. View

20.

Tabor S, Richardson C . A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985; 82(4):1074-8. PMC: 397196. DOI: 10.1073/pnas.82.4.1074. View