Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening

Nature Chemical Biology

Volumn 2, Issue 11, 2006, Pages 627-635

  Hong, Heedeok ^a   Szabo, Gabor ^a   Tamm, Lukas K ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; OUTER MEMBRANE PROTEIN A;

ARTICLE; CELL MEMBRANE PERMEABILITY; CHANNEL GATING; CONTROLLED STUDY; CORRELATION ANALYSIS; DISULFIDE BOND; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; POINT MUTATION; POROSITY; PRIORITY JOURNAL; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 33750255413     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio827     Document Type: Article

References (49)

1. Perutz, M.F. Electrostatic effects in proteins. Science 201, 1187-1191 (1978).
2. Lee, L.P. & Tidor, B. Barstar is electrostatically optimized for tight binding to barnase. Nat. Struct. Biol. 8, 73-76 (2001).
3. Waldburger, C.D., Schildbach, J.F. & Sauer, R.T. Are buried salt bridges important for protein stability and conformational specificity? Nat. Struct. Biol. 2, 122-128 (1995).
4. Yang, A.-S. & Honig, B. Electrostatic effects on protein stability. Curr. Opin. Struct. Biol. 2, 40-45 (1992).
5. Engelman, D.M. et al. Membrane protein folding: beyond the two stage model. FEBS Lett. 555, 122-125 (2003).
6. Call, M.E., Pyrdol, J., Wiedmann, M. & Wucherpfennig, K.W. The organizing principle in the formation of the T cell receptor-CD3 complex. Cell 111, 967-979 (2002).
7. Kim, J.M. et al. Structural origins of constitutive activation in rhodopsin: role of the K296/E113 salt bridge. Proc. Natl. Acad. Sci. USA 101, 12508-12513 (2004).
8. Jiang, Y., Ruta, V., Chen, J., Lee, A. & MacKinnon, R. The principle of gating charge movement in a voltage-dependent K+ channel. Nature 423, 42-48 (2003).
9. Lecar, H., Larsson, H.P. & Grabe, M. Electrostatic model of S4 motion in voltage-gated ion channels. Biophys. J. 85, 2854-2864 (2003).
10. Koebnik, R., Locher, K.P. & Van Gelder, P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37, 239-253 (2000).
11. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656 (2003).
12. Vogel, H. & Jähnig, F. Models for the structure of outer-membrane proteins of Escherichia coli derived from Raman spectroscopy and prediction methods. J. Mol. Biol. 190, 191-199 (1986).
13. Sugawara, E. & Nikaido, H. Pore-forming activity of OmpA protein of Escherichia coli. J. Biol. Chem. 267, 2507-2511 (1992).
14. Saint, N., De, E., Julien, S., Orange, N. & Molle, G. Ionophore properties of OmpA of Escherichia coli. Biochim. Biophys. Acta 1145, 119-123 (1993).
15. Zakharian, E. & Reusch, R.N. Outer membrane protein A of Escherichia coli forms temperature-sensitive channels in planar lipid bilayers. FEBS Lett. 555, 229-235 (2003).
16. Arora, A., Rinehart, D., Szabo, G. & Tamm, L.K. Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers. J. Biol. Chem. 275, 1594-1600 (2000).
17. Schweizer, M., Hindennach, I., Garten, W. & Henning, U. Major proteins of the Escherichia coli outer cell envelope membrane. Interaction of protein II with lipopolysaccharide. Eur. J. Biochem. 82, 211-217 (1978).
18. Prasadarao, N.V. et al. Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect. Immun. 64, 146-153 (1996).
19. Pautsch, A. & Schulz, G.E. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5, 1013-1017 (1998).
20. Arora, A., Abildgaard, F., Bushweller, J.H. & Tamm, L.K. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat. Struct. Biol. 8, 334-338 (2001).
21. Bond, P.J., Faraldo-Gomez, J.D. & Sansom, M.S. OmpA: a pore or not a pore? Simulation and modeling studies. Biophys. J. 83, 763-775 (2002).
22. Fersht, A.R., Matouschek, A. & Serrano, L. The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. J. Mol. Biol. 224, 771-782 (1992).
23. Pautsch, A. & Schulz, G.E. High-resolution structure of the OmpA membrane domain. J. Mol. Biol. 298, 273-282 (2000).
24. Hong, H. & Tamm, L.K. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. USA 101, 4065-4070 (2004).
25. Kleinschmidt, J.H. & Tamm, L.K. Folding intermediates of a b-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35, 12993-13000 (1996).
26. Colquhoun, D. & Hawkes, A.G. in Single Channel Recording (eds. Sakmann, B. & Nehrer, E.) 397-482 (Plenum, New York, 1995).
27. Horovitz, A., Serrano, L., Avron, B., Bycroft, M. & Fersht, A.R. Strength and cooperativity of contributions of surface salt bridges to protein stability. J. Mol. Biol. 216, 1031-1044 (1990).
28. Tissot, A.C., Vuilleumier, S. & Fersht, A.R. Importance of two buried salt bridges in the stability and folding pathway of barnase. Biochemistry 35, 6786-6794 (1996).
29. Marqusee, S. & Sauer, R.T. Contributions of a hydrogen bond/salt bridge network to the stability of secondary and tertiary structure in l repressor. Protein Sci. 3, 2217-2225 (1994).
30. Anderson, D.E., Becktel, W.J. & Dahlquist, F.W. pH-induced denaturation of proteins: a single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29, 2403-2408 (1990).
31. Kumar, S. & Nussinov, R. Fluctuations in ion pairs and their stabilities in proteins. Proteins 43, 433-454 (2001).
32. Gallivan, J.P. & Dougherty, D.A. Cation-p interactions in structural biology. Proc. Natl. Acad. Sci. USA 96, 9459-9464 (1999).
33. Thompson, S.E. & Smithrud, D.B. Carboxylates stacked over aromatic rings promote salt bridge formation in water. J. Am. Chem. Soc. 124, 442-449 (2002).
34. Tafer, H., Hiller, S., Hilty, C., Fernandez, C. & Wuthrich, K. Nonrandom structure in the urea-unfolded Escherichia coli outer membrane protein X (OmpX). Biochemistry 43, 860-869 (2004).
35. Myers, J.K., Pace, C.N. & Scholtz, J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148 (1995).
36. Bond, P.J. & Sansom, M.S. Membrane protein dynamics versus environment: simulations of OmpA in a micelle and in a bilayer. J. Mol. Biol. 329, 1035-1053 (2003).
37. Tamm, L.K., Abildgaard, F., Arora, A., Blad, H. & Bushweller, J.H. Structure, dynamics and function of the outer membrane protein A (OmpA) and influenza hemagglutinin fusion domain in detergent micelles by solution NMR. FEBS Lett. 555, 139-143 (2003).
38. Prilipov, A., Phale, P.S., Koebnik, R., Widmer, C. & Rosenbusch, J.P. Identification and characterization of two quiescent porin genes, nmpC and ompN, in Escherichia coli BE. J. Bacteriol. 180, 3388-3392 (1998).
39. Csonka, L.N. & Hanson, A.D. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 45, 569-606 (1991).
40. Wood, J.M. Osmosensing by bacteria: signals and membrane-based sensors. Microbiol. Mol. Biol. Rev. 63, 230-262 (1999).
41. Schindler, H. & Rosenbusch, J.P. Matrix protein from Escherichia coli outer membranes forms voltage-controlled channels in lipid bilayers. Proc. Natl. Acad. Sci. USA 75, 3751-3755 (1978).
42. Khalid, S., Bond, P.J., Deol, S.S. & Sansom, M.S. Modeling and simulations of a bacterial outer membrane protein: OprF from Pseudomonas aeruginosa. Proteins 63, 6-15 (2006).
43. Booth, P.J. Sane in the membrane: designing systems to modulate membrane proteins. Curr. Opin. Struct. Biol. 15, 435-440 (2005).
44. Bowie, J.U. Solving the membrane protein folding problem. Nature 438, 581-589 (2005).
45. Lau, F.W. & Bowie, J.U. A method for assessing the stability of a membrane protein. Biochemistry 36, 5884-5892 (1997).
46. Senes, A., Engel, D.E. & DeGrado, W.F. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479 (2004).
47. Kleinschmidt, J.H., den Blaauwen, T., Driessen, A.J. & Tamm, L.K. Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry 38, 5006-5016 (1999).
48. Prilipov, A., Phale, P.S., Van Gelder, P., Rosenbusch, J.P. & Koebnik, R. Coupling site-directed mutagenesis with high-level expression: large scale production of mutant porins from E coli. FEMS Microbiol. Lett. 163, 65-72 (1998).
49. Neher, E. & Stevens, C.F. Conductance fluctuations and ionic pores in membranes. Annu. Rev. Biophys. Bioeng. 6, 345-381 (1977).