A Peptidomimetic Antibiotic Interacts with the Periplasmic Domain of LptD from Pseudomonas aeruginosa

ACS Chemical Biology

Volumn 13, Issue 3, 2018, Pages 666-675

  Andolina, Gloria ^a,e   Bencze, László Csaba ^a,f   Zerbe, Katja ^a   Müller, Maik ^b   Steinmann, Jessica ^a   Kocherla, Harsha ^a   Mondal, Milon ^a   Sobek, Jens ^d   Moehle, Kerstin ^a   Malojčić, Goran ^c,g   Wollscheid, Bernd ^b   Robinson, John A ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b ETH ZURICH   (Switzerland)

^c HARVARD UNIVERSITY   (United States)

^d FUNCTIONAL GENOMICS CENTER ZURICH   (Switzerland)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

^f BABE BOLYAI UNIVERSITY   (Romania)

^g Goldfinch Bio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; GENOMIC DNA; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN A; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN B; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN C; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN D; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN E; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN F; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN G; MUREPAVADIN; PERIPLASMIC PROTEIN; TRYPSIN; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; LIPOPOLYSACCHARIDE; OUTER MEMBRANE PROTEIN; PEPTIDOMIMETIC AGENT;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL DISRUPTION; CELL GROWTH; CELL SURFACE; DRUG PROTEIN BINDING; ENANTIOMER; ESCHERICHIA COLI; GENE EXPRESSION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; IN VITRO STUDY; IN VIVO STUDY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; OMICS; OUTER MEMBRANE; PHOTOAFFINITY LABELING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; PROTON NUCLEAR MAGNETIC RESONANCE; PSEUDOMONAS AERUGINOSA; SURFACE PLASMON RESONANCE; SURFACE PROPERTY; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; BINDING SITE; CHEMISTRY; DRUG EFFECT; GRAM NEGATIVE BACTERIUM; METABOLISM; PERIPLASM; PROTEIN TRANSPORT;

ANTI-BACTERIAL AGENTS; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; GRAM-NEGATIVE BACTERIA; LIPOPOLYSACCHARIDES; PEPTIDOMIMETICS; PERIPLASM; PROTEIN DOMAINS; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA;

EID: 85044087383     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.7b00822     Document Type: Article

References (33)

1. (2017) Global Priority List of Antibiotic-resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics, World Health Organization, Geneva, Switzerland.
2. Willyard, C. (2017) The drug-resistant bacteria that pose the greatest health threats. Nature 543, 15, 10.1038/nature.2017.21550
3. Henderson, J. C., Zimmerman, S. M., Crofts, A. A., Boll, J. M., Kuhns, L. G., Herrera, C. M., and Trent, M. S. (2016) The Power of Asymmetry: Architecture and Assembly of the Gram-Negative Outer Membrane Lipid Bilayer. Annu. Rev. Microbiol. 70, 255-278, 10.1146/annurev-micro-102215-095308
4. Whitfield, C. and Trent, M. S. (2014) Biosynthesis and export of bacterial lipopolysaccharides. Annu. Rev. Biochem. 83, 99-128, 10.1146/annurev-biochem-060713-035600
5. Okuda, S., Sherman, D. J., Silhavy, T. J., Ruiz, N., and Kahne, D. (2016) Lipopolysaccharide transport and assembly at the outer membrane: the PEZ model. Nat. Rev. Microbiol. 14, 337-345, 10.1038/nrmicro.2016.25
6. Okuda, S., Freinkman, E., and Kahne, D. (2012) Cytoplasmic ATP Hydrolysis Powers Transport of Lipopolysaccharide Across the Periplasm in E. coli. Science 338, 1214, 10.1126/science.1228984
7. Simpson, B. W., May, J. M., Sherman, D. J., Kahne, D., and Ruiz, N. (2015) Lipopolysaccharide transport to the cell surface: biosynthesis and extraction from the inner membrane. Philos. Trans. R. Soc., B 370, 8, 10.1098/rstb.2015.0029
8. Freinkman, E., Okuda, S., Ruiz, N., and Kahne, D. (2012) Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51, 4800-4806, 10.1021/bi300592c
9. Li, X. J., Gu, Y. H., Dong, H. H., Wang, W. J., and Dong, C. J. (2015) Trapped lipopolysaccharide and LptD intermediates reveal lipopolysaccharide translocation steps across the Escherichia coli outer membrane. Sci. Rep. 5, 8, 10.1038/srep11883
10. Gu, Y. H., Stansfeld, P. J., Zeng, Y., Dong, H. H., Wang, W. J., and Dong, C. J. (2015) Lipopolysaccharide is Inserted into the Outer Membrane through An Intramembrane Hole, A Lumen Gate, and the Lateral Opening of LptD. Structure 23, 496-504, 10.1016/j.str.2015.01.001
11. Laguri, C., Sperandeo, P., Pounot, K., Ayala, I., Silipo, A., Bougault, C. M., Molinaro, A., Polissi, A., and Simorre, J. P. (2017) Interaction of lipopolysaccharides at intermolecular sites of the periplasmic Lpt transport assembly. Sci. Rep. 7, srep9715, 10.1038/s41598-017-10136-0
12. Dong, H. H., Xiang, Q. J., Gu, Y. H., Wang, Z. S., Paterson, N. G., Stansfeld, P. J., He, C., Zhang, Y. Z., Wang, W. J., and Dong, C. J. (2014) Structural basis for outer membrane lipopolysaccharide insertion. Nature 511, 52-56, 10.1038/nature13464
13. Qiao, S., Luo, Q., Zhao, Y., Zhang, X., and Huang, Y. (2014) Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511, 108-111, 10.1038/nature13484
14. Botos, I., Majdalani, N., Mayclin, S. J., McCarthy, J. G., Lundquist, K., Wojtowicz, D., Barnard, T. J., Gumbart, J. C., and Buchanan, S. K. (2016) Structural and Functional Characterization of the LPS Transporter LptDE from Gram-Negative Pathogens. Structure 24, 965-976, 10.1016/j.str.2016.03.026
15. Malojcic, G., Andres, D., Grabowicz, M., George, A. H., Ruiz, N., Silhavy, T. J., and Kahne, D. (2014) LptE binds to and alters the physical state of LPS to catalyze its assembly at the cell surface. Proc. Natl. Acad. Sci. U. S. A. 111, 9467-9472, 10.1073/pnas.1402746111
16. Sperandeo, P. and Polissi, A. (2016) Lipopolysaccharide Transport to the Cell Surface: New Insights in Assembly into the Outer Membrane. Structure 24, 847-849, 10.1016/j.str.2016.05.005
17. Sang, P., Shi, Y., Teng, P., Cao, A., Xu, H., Li, Q., and Cai, J. (2017) Antimicrobial AApeptides. Curr. Top. Med. Chem. 17, 1266-1279, 10.2174/1568026616666161018145945
18. Shi, Y., Teng, P., Sang, P., She, F., Wei, L., and Cai, J. (2016) γ-AApeptides: Design, Structure, and Applications. Acc. Chem. Res. 49, 428-441, 10.1021/acs.accounts.5b00492
19. Srinivas, N., Jetter, P., Ueberbacher, B. J., Werneburg, M., Zerbe, K., Steinmann, J., Van der Meijden, B., Bernardini, F., Lederer, A., Dias, R. L. A., Misson, P. E., Henze, H., Zumbrunn, J., Gombert, F. O., Obrecht, D., Hunziker, P., Schauer, S., Ziegler, U., Kach, A., Eberl, L., Riedel, K., DeMarco, S. J., and Robinson, J. A. (2010) Peptidomimetic Antibiotics Target Outer-Membrane Biogenesis in Pseudomonas aeruginosa. Science 327, 1010-1013, 10.1126/science.1182749
20. Werneburg, M., Zerbe, K., Juhas, M., Bigler, L., Stalder, U., Kaech, A., Ziegler, U., Obrecht, D., Eberl, L., and Robinson, J. A. (2012) Inhibition of Lipopolysaccharide Transport to the Outer Membrane in Pseudomonas aeruginosa by Peptidomimetic Antibiotics. ChemBioChem 13, 1767-1775, 10.1002/cbic.201200276
21. Schmidt, J., Patora-Komisarska, K., Moehle, K., Obrecht, D., and Robinson, J. A. (2013) Structural studies of β-hairpin peptidomimetic antibiotics that target LptD in Pseudomonas sp. Bioorg. Med. Chem. 21, 5806-5810, 10.1016/j.bmc.2013.07.013
22. Vetterli, S. U., Moehle, K., and Robinson, J. A. (2016) Synthesis and antimicrobial activity against Pseudomonas aeruginosa of macrocyclic β-hairpin peptidomimetic antibiotics containing N-methylated amino acids. Bioorg. Med. Chem. 24, 6332-6339, 10.1016/j.bmc.2016.05.027
23. Zerbe, K., Moehle, K., and Robinson, J. A. (2017) Protein Epitope Mimetics: From New Antibiotics to Supramolecular Synthetic Vaccines. Acc. Chem. Res. 50, 1323-1331, 10.1021/acs.accounts.7b00129
24. Chng, S., Ruiz, N., Chimalakonda, G., Silhavy, T., and Kahne, D. (2010) Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc. Natl. Acad. Sci. U. S. A. 107, 5363-5368, 10.1073/pnas.0912872107
25. Noinaj, N., Mayclin, S., Stanley, A. M., Jao, C. C., and Buchanan, S. K. (2016) From Constructs to Crystals-Towards Structure Determination of beta-barrel Outer Membrane Proteins. J. Visualized Exp. e53245, 10.3791/53245
26. Ruiz, N., Chng, S., Hiniker, A., Kahne, D., and Silhavy, T. (2010) Nonconsecutive disulfide bond formation in an essential integral outer membrane protein. Proc. Natl. Acad. Sci. U. S. A. 107, 12245-12250, 10.1073/pnas.1007319107
27. Chng, S., Xue, M., Garner, R., Kadokura, H., Boyd, D., Beckwith, J., and Kahne, D. (2012) Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export. Science 337, 1665-1668, 10.1126/science.1227215
28. Bodelón, G., Palomino, C., and Fernández, L. Á. (2013) Immunoglobulin domains in Escherichia coli and other enterobacteria: from pathogenesis to applications in antibody technologies. FEMS Microbiol. Rev. 37, 204-250, 10.1111/j.1574-6976.2012.00347.x
29. Frey, L., Lakomek, N. A., Riek, R., and Bibow, S. (2017) Micelles, Bicelles, and Nanodiscs: Comparing the Impact of Membrane Mimetics on Membrane Protein Backbone Dynamics. Angew. Chem., Int. Ed. 56, 380-383, 10.1002/anie.201608246
30. Moehle, K., Kocherla, H., Bacsa, B., Jurt, S., Zerbe, K., Robinson, J. A., and Zerbe, O. (2016) Solution Structure and Dynamics of LptE from Pseudomonas aeruginosa. Biochemistry 55, 2936-2943, 10.1021/acs.biochem.6b00313
31. Konovalova, A. and Silhavy, T. J. (2015) Outer membrane lipoprotein biogenesis: Lol is not the end. Phil. Philos. Trans. R. Soc., B 370, 10, 10.1098/rstb.2015.0030
32. Nouwens, A. S., Cordwell, S. J., Larsen, M. R., Molloy, M. P., Gillings, M., Willcox, M. D. P., and Walsh, B. J. (2000) Complementing genomics with proteomics: The membrane subproteome of Pseudomonas aeruginosa PAO1. Electrophoresis 21, 3797-3809, 10.1002/1522-2683(200011)21:17<3797::AID-ELPS3797>3.0.CO;2-P
33. Omasits, U., Ahrens, C. H., Müller, S., and Wollscheid, B. (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30, 884-886, 10.1093/bioinformatics/btt607