Dual orientation of the outer membrane lipoprotein pal in Escherichia coli

Microbiology (United Kingdom)

Volumn 161, Issue 6, 2015, Pages 1251-1259

  Michel, Lea Vacca ^a   Shaw, Juliana ^a   Macpherson, Victoria ^a   Barnard, David ^a   Bettinger, John ^a   D’arcy, Brooke ^a   Surendran, Naveen ^b   Hellman, Judith ^c   Pichichero, Michael E ^b  

^a ROCHESTER INSTITUTE OF TECHNOLOGY   (United States)

^b ROCHESTER GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; ESCHERICHIA COLI PROTEIN; LIPOPROTEIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PEPTIDOGLYCAN; PEPTIDOGLYCAN ASSOCIATED LIPOPROTEIN; PEPTIDOGLYCAN ASSOCIATED LIPOPROTEIN ANTIBODY; PROTEIN ANTIBODY; TOL PROTEIN; TRANSMEMBRANE PROTEIN OMPA; UNCLASSIFIED DRUG; EXCC PROTEIN, E COLI;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL SURFACE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI; FLOW CYTOMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; CHEMISTRY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL OUTER MEMBRANE PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLOW CYTOMETRY; LIPOPROTEINS; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; PEPTIDOGLYCAN;

EID: 84936105789     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.000084     Document Type: Article

References (32)

1. Abergel, C., Bouveret, E., Claverie, J. M., Brown, K., Rigal, A., Lazdunski, C. & Bénédetti, H. (1999). Structure of the Escherichia coli TolB protein determined by MAD methods at 1.95 A resolution. Structure 7, 1291-1300.
2. Bernadac, A., Gavioli, M., Lazzaroni, J. C., Raina, S. & Lloubè s, R. (1998). Escherichia coli tol-pal mutants form outer membrane vesicles. J Bacteriol 180, 4872-4878.
3. Bouveret, E., Derouiche, R., Rigal, A., Lloubè s, R., Lazdunski, C. & Bénédetti, 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.
4. Bouveret, E., Bénédetti, H., Rigal, A., Loret, E. & Lazdunski, C. (1999). In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J Bacteriol 181, 6306-6311.
5. Braun, V. & Bosch, V. (1972). Sequence of the murein-lipoprotein and the attachment site of the lipid. Eur J Biochem 28, 51-69.
6. Braun, V. & Rehn, K. (1969). 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 10, 426-438.
7. Cascales, E. & Lloubè s, R. (2004). Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51, 873-885.
8. Cascales, E., Gavioli, M., Sturgis, J. N. & Lloubè s, 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.
9. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J. -C. & Lloubè s, R. (2002). Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184, 754-759.
10. Clavel, T., Germon, P., Vianney, A., Portalier, R. & 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.
11. Cowles, C. E., Li, Y., Semmelhack, M. F., Cristea, I. M. & Silhavy, T. J. (2011). The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli. Mol Microbiol 79, 1168-1181.
12. Deprez, C., Lloubè s, R., Gavioli, M., Marion, D., Guerlesquin, F. & Blanchard, L. (2005). Solution structure of the E. coli TolA Cterminal domain reveals conformational changes upon binding to the phage g3p N-terminal domain. J Mol Biol 346, 1047-1057.
13. Gerding, M. A., Ogata, Y., Pecora, N. D., Niki, H. & 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.
14. Godlewska, R., Wiśniewska, K., Pietras, Z. & Jagusztyn-Krynicka, E. K. (2009). Peptidoglycan-associated lipoprotein (Pal) of Gramnegative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis. FEMS Microbiol Lett 298, 1-11.
15. Hellman, J., Zanzot, E. M., Loiselle, P. M., Amato, S. F., Black, K. M., Ge, Y., Kurnick, J. T. & Warren, H. S. (1997). Antiserum against Escherichia coli J5 contains antibodies reactive with outer membrane proteins of heterologous gram-negative bacteria. J Infect Dis 176, 1260-1268.
16. Hellman, J., Loiselle, P. M., Tehan, M. M., Allaire, J. E., Boyle, L. A., Kurnick, J. T. & Andrews, D. M. (2000). Outer membrane protein A, peptidoglycan-associated lipoprotein, and murein lipoprotein are released by Escherichia coli bacteria into serum. Infect Immun 68, 2566-2572.
17. Hellman, J., Roberts, J. D. Jr, Tehan, M. M., Allaire, J. E. & Warren, H. S. (2002). Bacterial peptidoglycan-associated lipoprotein is released into the bloodstream in gram-negative sepsis and causes inflammation and death in mice. J Biol Chem 277, 14274-14280.
18. Lazzaroni, J. C. & Portalier, R. (1992). The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycanassociated lipoprotein (PAL). Mol Microbiol 6, 735-742.
19. Leduc, M., Ishidate, K., Shakibai, N. & Rothfield, L. (1992). Interactions of Escherichia coli membrane lipoproteins with the murein sacculus. J Bacteriol 174, 7982-7988.
20. Lei, H., Velez, G. & Kazlauskas, A. (2011). Pathological signaling via platelet-derived growth factor receptor alpha involves chronic activation of Akt and suppression of p53. Mol Cell Biol 31, 1788-1799.
21. Liang, M. D., Bagchi, A., Warren, H. S., Tehan, M. M., Trigilio, J. A., Beasley-Topliffe, L. K., Tesini, B. L., Lazzaroni, J. C., Fenton, M. J. & Hellman, J. (2005). Bacterial peptidoglycan-associated lipoprotein: a naturally occurring toll-like receptor 2 agonist that is shed into serum and has synergy with lipopolysaccharide. J Infect Dis 191, 939-948.
22. Michel, L. V., Snyder, J., Schmidt, R., Milillo, J., Grimaldi, K., Kalmeta, B., Khan, M. N., Sharma, S., Wright, L. K. & Pichichero, M. E. (2013). Dual orientation of the outer membrane lipoprotein P6 of nontypeable Haemophilus influenzae. J Bacteriol 195, 3252-3259.
23. Mizuno, T. (1981). A novel peptidoglycan-associated lipoprotein (PAL) found in the outer membrane of Proteus mirabilis and other Gram-negative bacteria. J Biochem 89, 1039-1049.
24. Narita, S. & Tokuda, H. (2010). Protein secretion. In Methods in Molecular Biology. vol. 619, Chapter 7. Edited by A. Economou. New York, NY: Springer Science+Business Media, LLC.
25. Narita, S., Matsuyama, S. & Tokuda, H. (2004). Lipoprotein trafficking in Escherichia coli. Arch Microbiol 182, 1-6.
26. Park, J. S., Lee, W. C., Yeo, K. J., Ryu, K.-S., Kumarasiri, M., Hesek, D., Lee, M., Mobashery, S., Song, J. H. & other authors (2012). Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane. FASEB J 26, 219-228.
27. Parsons, L. M., Lin, F. & Orban, J. (2006). Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45, 2122-2128.
28. Valentine, C. H., Hellman, J., Beasley-Topliffe, L. K., Bagchi, A. & Warren, H. S. (2006). Passive immunization to outer membrane proteins MLP and PAL does not protect mice from sepsis. Mol Med 12, 252-258.
29. Vollmer, W. & Bertsche, U. (2008). Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778, 1714-1734.
30. Wang, Y. & Kim, K. S. (2002). Role of OmpA and IbeB in Escherichia coli K1 invasion of brain microvascular endothelial cells in vitro and in vivo. Pediatr Res 51, 559-563.
31. Yeh, Y.-C., Comolli, L. R., Downing, K. H., Shapiro, L. & McAdams, H. H. (2010). The caulobacter Tol-Pal complex is essential for outer membrane integrity and the positioning of a polar localization factor. J Bacteriol 192, 4847-4858.
32. Zakharian, E. & Reusch, R. N. (2005). Kinetics of folding of Escherichia coli OmpA from narrow to large pore conformation in a planar bilayer. Biochemistry 44, 6701-6707.