OprG Harnesses the Dynamics of its Extracellular Loops to Transport Small Amino Acids across the Outer Membrane of Pseudomonas aeruginosa

Structure

Volumn 23, Issue 12, 2015, Pages 2234-2245

  Kucharska, Iga ^a   Seelheim, Patrick ^a   Edrington, Thomas ^a,b   Liang, Binyong ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b MONSANTO COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALKANOL; AMINO ACID; CARBOHYDRATE DERIVATIVE; DESONIDE; FATTY ACID DERIVATIVE; GLYCINE; LIPOSOME; OPRG PROTEIN; OUTER MEMBRANE PROTEIN; POLYHISTIDINE TAG; PORIN; PROLINE DERIVATIVE; SERINE; SIGNAL PEPTIDE; THREONINE; UNCLASSIFIED DRUG; VALINE; OPRG PROTEIN, PSEUDOMONAS AERUGINOSA; PROTEIN BINDING;

AMINO ACID TRANSPORT; ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; BACTERIAL STRUCTURES; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL INCLUSION; CELL STRUCTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE MUTATION; GENE OVEREXPRESSION; GROWTH CURVE; HYDROGEN BOND; HYDROPHILICITY; HYDROPHOBICITY; LIPID BILAYER; MEMBRANE PERMEABILITY; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN REFOLDING; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; SUBSTRATE CONCENTRATION; AMINO ACID SEQUENCE; CHEMISTRY; CONSERVED SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; AMINO ACIDS; BACTERIAL OUTER MEMBRANE PROTEINS; CONSERVED SEQUENCE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84949320221     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.10.009     Document Type: Article

References (45)

1. A.D. Bangham, J. De Gier, and G.D. Greville Osmotic properties and water permeability of phospholipid liquid crystals Chem. Phys. Lipids 1 1967 225 246
2. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, N.S. Pannu, and et al. Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
3. S. Chamberland, A.S. Bayer, T. Schollaardt, S.A. Wong, and L.E. Bryan Characterization of mechanisms of quinolone resistance in Pseudomonas aeruginosa strains isolated in vitro and in vivo during experimental endocarditis Antimicrob. Agents Chemother. 33 1989 624 634
4. T. Cierpicki, B. Liang, L.K. Tamm, and J.H. Bushweller Increasing the accuracy of solution NMR structures of membrane proteins by application of residual dipolar couplings. High-resolution structure of outer membrane protein A J. Am. Chem. Soc. 128 2006 6947 6951
5. G. Cornilescu, F. Delaglio, and A. Bax Protein backbone angle restraints from searching a database for chemical shift and sequence homology J. Biomol. NMR 13 1999 289 302
6. A.H. Delcour Outer membrane permeability and antibiotic resistance Biochim. Biophys. Acta 1794 2009 808 816
7. S.A. Denome, D.C. Stanley, E.S. Olson, and K.D. Young Metabolism of dibenzothiophene and naphthalene in Pseudomonas strains: complete DNA sequence of an upper naphthalene catabolic pathway J. Bacteriol. 175 1993 6890 6901
8. T.C. Edrington, E. Kintz, J.B. Goldberg, and L.K. Tamm Structural basis for the interaction of lipopolysaccharide with outer membrane protein H (OprH) from Pseudomonas aeruginosa J. Biol. Chem. 286 2011 39211 39223
9. C. Fernandez, C. Hilty, G. Wider, P. Guntert, and K. Wuthrich NMR structure of the integral membrane protein OmpX J. Mol. Biol. 336 2004 1211 1221
10. D.A. Fox, P. Larsson, R.H. Lo, B.M. Kroncke, P.M. Kasson, and L. Columbus Structure of the neisserial outer membrane protein Opa(6)(0): loop flexibility essential to receptor recognition and bacterial engulfment J. Am. Chem. Soc. 136 2014 9938 9946
11. J.R. Govan, A.R. Brown, and A.M. Jones Evolving epidemiology of Pseudomonas aeruginosa and the Burkholderia cepacia complex in cystic fibrosis lung infection Future Microbiol. 2 2007 153 164
12. F. Hagn, M. Etzkorn, T. Raschle, and G. Wagner Optimized phospholipid bilayer nanodiscs facilitate high-resolution structure determination of membrane proteins J. Am. Chem. Soc. 135 2013 1919 1925
13. R.E. Hancock, and F.S. Brinkman Function of Pseudomonas porins in uptake and efflux Annu. Rev. Microbiol. 56 2002 17 38
14. E.M. Hearn, D.R. Patel, B.W. Lepore, M. Indic, and B. van den Berg Transmembrane passage of hydrophobic compounds through a protein channel wall Nature 458 2009 367 370
15. H. Hong, D.R. Patel, L.K. Tamm, and B. van den Berg The outer membrane protein OmpW forms an eight-stranded beta-barrel with a hydrophobic channel J. Biol. Chem. 281 2006 7568 7577
16. H. Hong, S. Park, R.H. Jimenez, D. Rinehart, and L.K. Tamm Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins J. Am. Chem. Soc. 129 2007 8320 8327
17. R. Horst, P. Stanczak, and K. Wuthrich NMR polypeptide backbone conformation of the E. coli outer membrane protein W Structure 22 2014 1204 1209
18. D.A. Johnson, S.G. Tetu, K. Phillippy, J. Chen, Q. Ren, and I.T. Paulsen High-throughput phenotypic characterization of Pseudomonas aeruginosa membrane transport genes PLoS Genet. 4 2008 e1000211
19. I. Kucharska, T.C. Edrington, B. Liang, and L.K. Tamm Optimizing nanodiscs and bicelles for solution NMR studies of two beta-barrel membrane proteins J. Biomol. NMR 61 2015 261 274
20. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486
21. W.C. Lathe 3rd, B. Snel, and P. Bork Gene context conservation of a higher order than operons Trends Biochem. Sci. 25 2000 474 479
22. D. Lee, C. Hilty, G. Wider, and K. Wuthrich Effective rotational correlation times of proteins from NMR relaxation interference J. Magn. Reson. 178 2006 72 76
23. B. Liang, and L.K. Tamm Structure of outer membrane protein G by solution NMR spectroscopy Proc. Natl. Acad. Sci. USA 104 2007 16140 16145
24. A.L. Lomize, I.D. Pogozheva, M.A. Lomize, and H.I. Mosberg Positioning of proteins in membranes: a computational approach Protein Sci. 15 2006 1318 1333
25. J.B. McPhee, S. Tamber, M. Bains, E. Maier, S. Gellatly, A. Lo, R. Benz, and R.E. Hancock The major outer membrane protein OprG of Pseudomonas aeruginosa contributes to cytotoxicity and forms an anaerobically regulated, cation-selective channel FEMS Microbiol. Lett. 296 2009 241 247
26. N. Mesaros, P. Nordmann, P. Plesiat, M. Roussel-Delvallez, J. Van Eldere, Y. Glupczynski, Y. Van Laethem, F. Jacobs, P. Lebecque, A. Malfroot, and et al. Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium Clin. Microbiol. Infect. 13 2007 560 578
27. 15N NMR assignments and global folding pattern Biochemistry 32 1993 13818 13829
28. B. Nandi, R.K. Nandy, A. Sarkar, and A.C. Ghose Structural features, properties and regulation of the outer-membrane protein W (OmpW) of Vibrio cholerae Microbiology 151 2005 2975 2986
29. T.M. Neher, and D.R. Lueking Pseudomonas fluorescens ompW: plasmid localization and requirement for naphthalene uptake Can. J. Microbiol. 55 2009 553 563
30. H. Nikaido, and E.Y. Rosenberg Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins J. Bacteriol. 153 1983 241 252
31. A. Pautsch, and G.E. Schulz High-resolution structure of the OmpA membrane domain J. Mol. Biol. 298 2000 273 282
32. X. Peng, C. Xu, H. Ren, X. Lin, L. Wu, and S. Wang Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Pseudomonas aeruginosa responding to ampicillin, kanamycin, and tetracycline resistance J. Proteome Res. 4 2005 2257 2265
33. S. Rajan, and L. Saiman Pulmonary infections in patients with cystic fibrosis Semin. Respir. Infect. 17 2002 47 56
34. G.E. Schulz The structure of bacterial outer membrane proteins Biochim. Biophys. Acta 1565 2002 308 317
35. Y. Shen, F. Delaglio, G. Cornilescu, and A. Bax TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts J. Biomol. NMR 44 2009 213 223
36. S. Tamber, M.M. Ochs, and R.E. Hancock Role of the novel OprD family of porins in nutrient uptake in Pseudomonas aeruginosa J. Bacteriol. 188 2006 45 54
37. D.S. Touw, D.R. Patel, and B. van den Berg The crystal structure of OprG from Pseudomonas aeruginosa, a potential channel for transport of hydrophobic molecules across the outer membrane PLoS One 5 2010 e15016
38. B. van den Berg The FadL family: unusual transporters for unusual substrates Curr. Opin. Struct. Biol. 15 2005 401 407
39. J. Vogt, and G.E. Schulz The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence Structure 7 1999 1301 1309
40. G. Walzer, E. Rosenberg, and E.Z. Ron Identification of outer membrane proteins with emulsifying activity by prediction of beta-barrel regions J. Microbiol. Methods 76 2009 52 57
41. L. Wu, X. Lin, F. Wang, D. Ye, X. Xiao, S. Wang, and X. Peng OmpW and OmpV are required for NaCl regulation in Photobacterium damsela J. Proteome Res. 5 2006 2250 2257
42. E.L. Wu, P.J. Fleming, M.S. Yeom, G. Widmalm, J.B. Klauda, K.G. Fleming, and W. Im E. coli outer membrane and interactions with OmpLA Biophys. J. 106 2014 2493 2502
43. J.M. Yates, G. Morris, and M.R. Brown Effect of iron concentration and growth rate on the expression of protein G in Pseudomonas aeruginosa FEMS Microbiol. Lett. 49 1989 259 262
44. O. Yildiz, K.R. Vinothkumar, P. Goswami, and W. Kuhlbrandt Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation EMBO J. 25 2006 3702 3713
45. T. Zhuang, C. Chisholm, M. Chen, and L.K. Tamm NMR-based conformational ensembles explain pH-gated opening and closing of OmpG channel J. Am. Chem. Soc. 135 2013 15101 15113