Molecular Interactions of Lipopolysaccharide with an Outer Membrane Protein from Pseudomonas aeruginosa Probed by Solution NMR

Biochemistry

Volumn 55, Issue 36, 2016, Pages 5061-5072

  Kucharska, Iga ^a   Liang, Binyong ^a   Ursini, Nicholas ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; BINS; BIOLOGICAL MEMBRANES; CHEMICAL COMPOUNDS; CHEMICAL SHIFT; DIAGNOSIS; DISSOCIATION; ESCHERICHIA COLI; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; STABILITY;

ANTIBIOTIC RESISTANCE; DISSOCIATION CONSTANT; INTEGRAL MEMBRANE PROTEINS; NMR CHEMICAL SHIFT PERTURBATIONS; OUTER MEMBRANE PROTEIN; PSEUDOMONAS AERUGINOSA; SINGLE-SITE MUTATIONS; STRUCTURAL STABILITIES;

PROTEINS;

ARGININE; BACTERIAL PROTEIN; LIPOPOLYSACCHARIDE; LYSINE; OUTER MEMBRANE PROTEIN;

ARTICLE; CARBOHYDRATE ANALYSIS; MEMBRANE PERMEABILITY; MICELLE; MOLECULAR INTERACTION; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PSEUDOMONAS AERUGINOSA; STATIC ELECTRICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROCEDURES; PROTEIN FOLDING; SITE DIRECTED MUTAGENESIS;

BACTERIAL OUTER MEMBRANE PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; LIPOPOLYSACCHARIDES; MUTAGENESIS, SITE-DIRECTED; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN FOLDING; PSEUDOMONAS AERUGINOSA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84987664888     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.6b00630     Document Type: Article

References (40)

1. Govan, J. R., Brown, A. R., and Jones, A. M. (2007) Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection Future Microbiol. 2, 153-164 10.2217/17460913.2.2.153
2. Rajan, S. and Saiman, L. (2002) Pulmonary infections in patients with cystic fibrosis Semin. Respir. Infect. 17, 47-56 10.1053/srin.2002.31690
3. Gellatly, S. L. and Hancock, R. E. (2013) Pseudomonas aeruginosa: new insights into pathogenesis and host defenses Pathog. Dis. 67, 159-173 10.1111/2049-632X.12033
4. Silby, M. W., Winstanley, C., Godfrey, S. A., Levy, S. B., and Jackson, R. W. (2011) Pseudomonas genomes: diverse and adaptable FEMS Microbio.l Rev. 35, 652-680 10.1111/j.1574-6976.2011.00269.x
5. Hancock, R. E. (1998) Resistance mechanisms in Pseudomonas aeruginosa and other nonfermentative gram-negative bacteria Clin. Infect. Dis. 27 (Suppl. 1) S93-S99 10.1086/514909
6. Nicas, T. I. and Hancock, R. E. (1983) Pseudomonas aeruginosa outer membrane permeability: isolation of a porin protein F-deficient mutant J. Bacteriol. 153, 281-285
7. Koebnik, R., Locher, K. P., and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell Mol. Microbiol. 37, 239-253 10.1046/j.1365-2958.2000.01983.x
8. Mayer, H., Tharanathan, R. N., and Weckesser, J. (1985) Analysis of lipopolysaccharides of gram-negative bacteria Methods Microbiol. 18, 157-207 10.1016/S0580-9517(08)70475-6
9. Vaara, M. (1992) Agents that increase the permeability of the outer membrane Microbiol. Rev. 56, 395-411
10. Macfarlane, E. L., Kwasnicka, A., and Hancock, R. E. (2000) Role of Pseudomonas aeruginosa PhoP-phoQ in resistance to antimicrobial cationic peptides and aminoglycosides Microbiology 146, 2543-2554 10.1099/00221287-146-10-2543
11. Gellatly, S. L., Needham, B., Madera, L., Trent, M. S., and Hancock, R. E. (2012) The Pseudomonas aeruginosa PhoP-PhoQ two-component regulatory system is induced upon interaction with epithelial cells and controls cytotoxicity and inflammation Infect. Immun. 80, 3122-3131 10.1128/IAI.00382-12
12. Macfarlane, E. L., Kwasnicka, A., Ochs, M. M., and Hancock, R. E. (1999) PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance Mol. Microbiol. 34, 305-316 10.1046/j.1365-2958.1999.01600.x
13. Miller, A. K., Brannon, M. K., Stevens, L., Johansen, H. K., Selgrade, S. E., Miller, S. I., Hoiby, N., and Moskowitz, S. M. (2011) PhoQ mutations promote lipid A modification and polymyxin resistance of Pseudomonas aeruginosa found in colistin-treated cystic fibrosis patients Antimicrob. Agents Chemother. 55, 5761-5769 10.1128/AAC.05391-11
14. Mueller, P., Rudin, D. O., Tien, H. T., and Wescott, W. C. (1962) Reconstitution of cell membrane structure in vitro and its transformation into an excitable system Nature 194, 979-980 10.1038/194979a0
15. Muller, C., Plesiat, P., and Jeannot, K. (2011) A two-component regulatory system interconnects resistance to polymyxins, aminoglycosides, fluoroquinolones, and beta-lactams in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 55, 1211-1221 10.1128/AAC.01252-10
16. Edrington, T. C., Kintz, E., Goldberg, J. B., and Tamm, L. K. (2011) Structural basis for the interaction of lipopolysaccharide with outer membrane protein H (OprH) from Pseudomonas aeruginosa J. Biol. Chem. 286, 39211-39223 10.1074/jbc.M111.280933
17. Kucharska, I., Edrington, T. C., Liang, B., and Tamm, L. K. (2015) Optimizing nanodiscs and bicelles for solution NMR studies of two beta-barrel membrane proteins J. Biomol. NMR 61, 261-274 10.1007/s10858-015-9905-z
18. Tugarinov, V., Kanelis, V., and Kay, L. E. (2006) Isotope labeling strategies for the study of high-molecular-weight proteins by solution NMR spectroscopy Nat. Protoc. 1, 749-754 10.1038/nprot.2006.101
19. Kucharska, I., Seelheim, P., Edrington, T., Liang, B., and Tamm, L. K. (2015) OprG Harnesses the Dynamics of its Extracellular Loops to Transport Small Amino Acids across the Outer Membrane of Pseudomonas aeruginosa Structure 23, 2234-2245 10.1016/j.str.2015.10.009
20. Sturiale, L., Garozzo, D., Silipo, A., Lanzetta, R., Parrilli, M., and Molinaro, A. (2005) New conditions for matrix-assisted laser desorption/ionization mass spectrometry of native bacterial R-type lipopolysaccharides Rapid Commun. Mass Spectrom. 19, 1829-1834 10.1002/rcm.1994
21. Hardy, E., Pupo, E., Castellanos-Serra, L., Reyes, J., and Fernandez-Patron, C. (1997) Sensitive reverse staining of bacterial lipopolysaccharides on polyacrylamide gels by using zinc and imidazole salts Anal. Biochem. 244, 28-32 10.1006/abio.1996.9719
22. Hyberts, S. G., Arthanari, H., and Wagner, G. (2011) Applications of non-uniform sampling and processing Top. Curr. Chem. 316, 125-148 10.1007/128-2011-187
23. Hyberts, S. G., Milbradt, A. G., Wagner, A. B., Arthanari, H., and Wagner, G. (2012) Application of iterative soft thresholding for fast reconstruction of NMR data non-uniformly sampled with multidimensional Poisson Gap scheduling J. Biomol. NMR 52, 315-327 10.1007/s10858-012-9611-z
24. Hyberts, S. G., Takeuchi, K., and Wagner, G. (2010) Poisson-gap sampling and forward maximum entropy reconstruction for enhancing the resolution and sensitivity of protein NMR data J. Am. Chem. Soc. 132, 2145-2147 10.1021/ja908004w
25. Goddard, T. D. and Kneller, D. G. SPARKY 3, University of California, San Francisco.
26. Tobias, P. S., Soldau, K., and Ulevitch, R. J. (1989) Identification of a lipid A binding site in the acute phase reactant lipopolysaccharide binding protein J. Biol. Chem. 264, 10867-10871
27. Abraham, S. J., Hoheisel, S., and Gaponenko, V. (2008) Detection of protein-ligand interactions by NMR using reductive methylation of lysine residues J. Biomol. NMR 42, 143-148 10.1007/s10858-008-9274-y
28. Means, G. E. and Feeney, R. E. (1968) Reductive alkylation of amino groups in proteins Biochemistry 7, 2192-2201 10.1021/bi00846a023
29. Fielding, L. (2003) NMR methods for the determination of protein-ligand dissociation constants Curr. Top. Med. Chem. 3, 39-53 10.2174/1568026033392705
30. Seelig, J., Seelig, A., and Tamm, L. K. (1982) Nuclear Magnetic Resonance and Lipid-Protein Interactions, Vol. 2, John R. Wiley & Sons, New York.
31. Yeagle, P. L. (2014) Non-covalent binding of membrane lipids to membrane proteins Biochim. Biophys. Acta, Biomembr. 1838, 1548-1559 10.1016/j.bbamem.2013.11.009
32. Laganowsky, A., Reading, E., Allison, T. M., Ulmschneider, M. B., Degiacomi, M. T., Baldwin, A. J., and Robinson, C. V. (2014) Membrane proteins bind lipids selectively to modulate their structure and function Nature 510, 172-175 10.1038/nature13419
33. Barrett, P. J., Song, Y., Van Horn, W. D., Hustedt, E. J., Schafer, J. M., Hadziselimovic, A., Beel, A. J., and Sanders, C. R. (2012) The amyloid precursor protein has a flexible transmembrane domain and binds cholesterol Science 336, 1168-1171 10.1126/science.1219988
34. Ferguson, A. D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J. W., and Diederichs, K. (2000) A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins Structure 8, 585-592 10.1016/S0969-2126(00)00143-X
35. Srimal, S., Surolia, N., Balasubramanian, S., and Surolia, A. (1996) Titration calorimetric studies to elucidate the specificity of the interactions of polymyxin B with lipopolysaccharides and lipid A Biochem. J. 315 (Pt 2) 679-686 10.1042/bj3150679
36. Schindler, M. and Osborn, M. J. (1979) Interaction of divalent cations and polymyxin B with lipopolysaccharide Biochemistry 18, 4425-4430 10.1021/bi00587a024
37. Kabanov, D. S. and Prokhorenko, I. R. (2010) Structural analysis of lipopolysaccharides from Gram-negative bacteria Biochemistry (Moscow) 75, 383-404 10.1134/S0006297910040012
38. Ernst, R. K., Hajjar, A. M., Tsai, J. H., Moskowitz, S. M., Wilson, C. B., and Miller, S. I. (2003) Pseudomonas aeruginosa lipid A diversity and its recognition by Toll-like receptor 4 J. Endotoxin Res. 9, 395-400 10.1177/09680519030090060201
39. Pier, G. B. (2007) Pseudomonas aeruginosa lipopolysaccharide: a major virulence factor, initiator of inflammation and target for effective immunity Int. J. Med. Microbiol. 297, 277-295 10.1016/j.ijmm.2007.03.012
40. Ernst, R. K., Yi, E. C., Guo, L., Lim, K. B., Burns, J. L., Hackett, M., and Miller, S. I. (1999) Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa Science 286, 1561-1565 10.1126/science.286.5444.1561