Understanding the function of bacterial outer membrane channels by reconstitution into black lipid membranes

Biophysical Chemistry

Volumn 85, Issue 2-3, 2000, Pages 153-167

  Van Gelder, Patrick ^a   Dumas, Fabrice ^a   Winterhalter, Mathias ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Channel; Conductance; Gating; Lipid membrane; Noise; Porin

Indexed keywords

OUTER MEMBRANE PROTEIN;

BACTERIAL MEMBRANE; CHANNEL GATING; ESCHERICHIA COLI; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE CONDUCTANCE; MODEL; PRIORITY JOURNAL; PROTEIN IMMOBILIZATION; REVIEW; TECHNIQUE; THERMODYNAMICS;

BACTERIA (MICROORGANISMS);

EID: 0033933520     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-4622(99)00153-2     Document Type: Article

References (96)

1. Lugtenberg B., vanAlphen L. Molecular architecture and functioning of the outer membrane of Escherichia coli and other Gram-negative bacteria. Biochim. Biophys. Acta. 737:1983;51-115.
2. Schirmer T. General and specific porins from bacterial outer membranes. J. Struct. Biol. 121:1998;101-109.
3. vanAlphen W., Lugtenberg B. Influence on osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J. Bacteriol. 131:1977;623-630.
4. Overbeeke N., Lugtenberg B. Expression of outer membrane protein e of Escherichia coli K-12 by phosphate limitation. FEBS Lett. 112:1980;229-232.
5. Randall-Hazelbauer L., Schwartz M. Isolation of the bacteriophage lambda receptor from Escherichia coli. J. Bacteriol. 116:1973;1436-1446.
6. Szmelcman S., Hofnung M. Maltose transport in Escherichia coli K12. Involvement of the bacteriophage lambda receptor. J. Bacteriol. 124:1975;112-118.
7. Szmelcman S., Schwartz M., Silhavy T.J., Boos W. Maltose transport in Escherichia coli K-12: a comparison of transport kinetics in wild-type and lambda-resistant mutants with the dissociation constant of the maltose-binding protein as measured by fluorescent quenching. Eur. J. Biochem. 65:1976;13-19.
8. Schmid K., Ebner R., Altenbuchner J., Schmitt R., Lengeler J.W. Plasmid-mediated sucrose metabolism in Escherichia coli K12: mapping of the scr genes of pUR400. Mol. Microbiol. 2:1988;1-8.
9. Hardesty C., Ferran C., DiRienzo J.M. Plasmid-mediated sucrose metabolism in Escherichia coli: characterization of scrY, the structural gene for a phosphoenolpyruvate-dependent sucrose phosphotransferase system outer membrane porin. J. Bacteriol. 173:1991;449-456.
10. Maier C., Bremer E., Schmid A., Benz R. Pore-forming activity of the Tsx protein from the outer membrane of Escherichia coli. J. Biol. Chem. 263:1988;2493-2499.
11. Ulmke C., Lengeler J.W., Schmid K. Identification of a new porin, RafY, encoded by the raffinose plasmid pRSD2 of Escherichia coli. J. Bacteriol. 179:1997;5783-5788.
12. Andersen C., Krones D., Ulmke C., Schmid K., Benz R. The porin RafY encoded by the raffinose plasmid pRSD2 of Escherichia coli forms a general diffusion pore and not a carbohydrate-specific porin. Eur. J. Biochem. 254:1998;679-684.
13. Postle K. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:1993;591-601.
14. Hueck C.J. Type III secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433.
15. Filloux A., Michel G., Bally M. GSP-dependent protein secretion in Gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol. Rev. 22:1998;177-198.
16. Freudl R., Schwarz H., Stierhof Y.D., Gamon K., Hindennach I., Henning U. An outer membrane protein (OmpA) of Escherichia coli undergoes a conformational change during export. J. Biol. Chem. 261:1986;11355-11361.
17. Scandella C.J., Kornberg A. A membrane-bound phospholipase A1 purified from Escherichia coli. Biochemistry. 10:1971;4447-4456.
18. Grodberg J., Dunn J.J. ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170:1988;1245-1253.
19. Weiss M.S., Kreusch A., Schiltz E. et al. The structure of porin from Rodobacter capsulatus at 1.8 Å resolution. FEBS Lett. 280:1991;379-382.
20. Kreusch A., Neubuser A., Schiltz E., Weckesser J., Schulz G.E. Structure of the membrane channel porin from Rhodopseudomonas blastica at 2.0 Å resolution. Protein Sci. 3:1994;58-63.
21. Hirsch A., Breed J., Saxena K. et al. The structure of porin from Paracoccus denitrificans at 3.1 Å resolution. FEBS Lett. 404:1996;208-210.
22. Cowan S.W., Schirmer T., Rummel G. et al. Crystal structures explain functional properties of two E coli porins. Nature. 358:1992;727-733.
23. Dutzler R., Rummel G., Alberti S. et al. Crystal structure and functional characterization of OmpK36, the osmoporin of Klebsiella pneumoniae. Structure. 7:1998;425-434.
24. Karshikoff A., Spassov V., Cowan S.W., Ladenstein R., Schirmer T. Electrostatic properties of two porin channels from Escherichia coli. J. Mol. Biol. 240:1994;372-384.
25. Schirmer T., Keller T.A., Wang Y.F., Rosenbusch J.P. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science. 267:1995;512-514.
26. Meyer J.E.W., Hofnung M., Schulz G.E. Structure of maltoporin from Salmonella typhimurium ligated with nitrophenyl-maltotrioside. J. Mol. Biol. 266:1997;761-775.
27. Forst D., Welte W., Wacker T., Diederichs K. Structure of the sucrose-specific porin ScrY from Salmonella typhimurium and its complex with sucrose. Nature Struct. Biol. 5:1998;37-46.
28. Dutzler R., Wang Y.F., Rizkallah P.J., Rosenbusch J.P., Schirmer T. Crystal structures of various maltooligosaccharides bound to maltoporin reveal a specific sugar translocation pathway. Structure. 4:1996;127-134.
29. Hanke W., Schlue W.R. Planar lipid bilayers. 1993;Academic press, N.Y.
30. Mueller P., Rudin D.O., Tien H.T., Wescott W.C. Methods for the formation of single bimolecular lipid membranes in aqueous solution. J. Phys. Chem. 67(3):1996;534-641.
31. Montal M., Mueller P. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl. Acad. Sci. U.S.A. 69:1979;3561-3566.
32. Schindler H. Planar lipid-protein membranes: strategies of formation and of detecting dependencies of ion transport functions on membrane conditions. Methods Enzymol. 171:1989;225-253.
33. Bähr G., Diederich A., Vergeres G., Winterhalter M. Interaction of the effector domain of MARCKS and MARCKS related protein with lipid membranes revealed by electric potential measurements. Biochemistry. 37:1998;16252-16261.
34. Winterhalter M. Sugar transport through channels reconstituted in planar lipid membranes. Coll. Surface. A149:1999;547-551.
35. Wiese A., Reiners J.O., Brandenburg K., Kawahara K., Zahringer U., Seydel U. Planar asymmetric lipid bilayers of glycosphingolipid or lipopolysaccharide on one side and phospholipids on the other: membrane potential, porin function, and complement activation. Biophys. J. 70:1996;321-329.
36. Van Gelder P., Dumas F., Rosenbusch J.P., Winterhalter M. Oriented channels reveal asymmetric energy barriers for sugar translocation through maltoporin of Escherichia coli. Eur. J. Biochem. 267:2000;79-84.
37. Bonhivers M., Ghazi A., Boulanger P., Letellier L. FhuA, a transporter of the Escherichia coli outer membrane is converted into a channel upon binding of bacteriophage T5. EMBO J. 15:1996;1850-1856.
38. VanGelder P., Saint N., vanBoxtel R., Rosenbusch J.P., Tommassen J. Pore functioning of outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng. 10:1997;699-706.
39. Brunen M., Engelhardt H. Asymmetry of orientation and voltage gating of the Acidovorax delafieldii porin Omp34 in lipid bilayers. Eur. J. Biochem. 212:1993;129-135.
40. Zizi M., Thomas L., Blachy-Dyson E., Forte M., Colombini M. Oriented channel insertion reveals the motion of a transmembrane beta strand during voltage gating of VDAC. J. Membr. Biol. 144:1995;121-129.
41. Dargent B., Hofmann W., Pattus F., Rosenbusch J.P. The selectivity filter of voltage-dependent channels formed by phosphoporin PhoE protein from E. coli. EMBO J. 5:1986;773-778.
42. Isshii J., Nakae T. Lipopolysaccharide promoted opening of the porin channel. FEBS Lett. 320:1993;251-255.
43. B. Hille, Ionic channels of excitable membranes, Sinauer, Sunderland, MA 1992.
44. Przybylski M., Glocker M.O., Nestel U. et al. X-ray crystallographic and mass spectrometric structure determination and functional characterization of succinylated porin from Rhodobacter capsulatus: implications for ion selectivity and single-channel conductance. Protein Sci. 5:1996;1477-1489.
45. Saxena K., Drosou V., Maier E., Benz R., Ludwig B. Ion selectivity reversal and induction of voltage-gating by site-directed mutations in the Paracoccus denitrificans porin. Biochemistry. 38:1999;2206-2212.
46. Phale S.P., Schirmer T., Prilipov A., Lou K.L., Hardmeyer A., Rosenbusch J.P. Voltage gating of Escherichia coli porin channels: role of the constriction loop. Proc. Natl. Acad. Sci. U.S.A. 94:1997;6745-6745.
47. Schmid B., Maveyraud L., Krömer M., Schulz G.E. Porin with new channel properties. Protein Science. 7:1998;1603-1611.
48. Nikaido H., Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49:1985;1-32.
49. Nikaido H. Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6:1992;435-442.
50. Ertel A., Marangoni A.G., Marsh J., Hallet F.R., Wood J.M. Mechanical properties of vesicles. Biophys. J. 64:1993;426-434.
51. Krasilnikov O.V., Sabirov R.Z., Ternovsky V.I., Merzliak P.G., Muratkhodjaev J.N. A simple method for the determination of the pore radius of ion channels in planar lipid bilayer membranes. FEMS Microbiol. Immunol. 105:1992;93-100.
52. Bezrukov S.M., Vodyanoy I., Parsegian V.A. Counting polymers moving through a single ion channel. Nature. 370:1994;279-281.
53. Bezrukov S.M., Vodyanoy I., Brutyan R.A., Kasianowicz J.J. Dynamics and free energy of polymer partitioning into a nanoscale pore. Macromolecules. 29:1996;8517-8522.
54. Bezrukov S.M., Kasianowicz J.J. Current noise reveals protonation kinetics and number of ionizable sites in an open protein ion channel. Phys. Rev. Lett. 70:1993;2352-2355.
55. Kasianowicz J.J., Bezrukov S.M. Protonation dynamics of the alpha-toxin ion channel from spectral analysis of pH-dependent current fluctuations. Biophys. J. 69:1995;94-105.
56. Rostovtseva T.K., Aguilella V.M., Vodyanoy I., Bezrukov S.M., Parsegian V.A. Membrane surface-charge titration probed by gramicidin A channel conductance. Biophys. J. 75:1998;1783-1792.
57. Darveau R.P., Hancock R.E.W., Benz R. Chemical modification of the anion selectivity of the PhoE porin from the. Escherichia coli outer membrane. Biochim. Biophys. Acta. 774:1984;67-74.
58. Brunen M., Engelhardt H. Significance of positively charged amino acids for the function of the Acidovorax delafieldii porin Omp34. FEMS Microbiol. Lett. 126:1995;127-132.
59. Van Gelder P., Saint N., Phale P. et al. Voltage gating in OmpF and PhoE porins of Escherichia coli: role of charged residues. J. Mol. Biol. 269:1997;468-472.
60. Bauer K., Struyvé M., Bosch D., Benz R., Tommassen J. One single lysine residue is responsible for the special interaction between polyphosphate and the outer membrane porin PhoE of Escherichia coli. J. Biol. Chem. 264:1989;16393-16398.
61. Dargent B., Hofmann W., Pattus F., Rosenbusch J.P. The selectivity filter of voltage-dependent channels formed by phosphoporin PhoE protein from E. coli. EMBO J. 5:1986;773-778.
62. Tokunaga H., Tokunaga M., Nakae T. Permeability properties of chemically modified porin trimers from Escherichia coli B. J. Biol. Chem. 256:1981;8024-8029.
63. Jeanteur D., Schirmer T., Fourel D. et al. Structural and functional alterations of a colicin-resistant mutant of OmpF porin from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 91:1994;10675-10679.
64. Saint N., Lou K.L., Widmer C., Luckey M., Schirmer T., Rosenbusch J.P. Structural and functional characterization of OmpF porin mutants selected for larger pore size. II. Functional characterization. J. Biol. Chem. 271:1996;20676-20680.
65. Sen K., Hellman J., Nikaido H. Porin channels in intact cells of Escherichia coli are not affected by Donnan potentials across the outer membrane. J. Biol. Chem. 263:1988;1182-1187.
66. Delcour A.H., Adler J., Kung C., Martinac B. Membrane-derived oligosaccharides MDO's promote closing of an E. coli porin channel. FEBS Lett. 304:1992;216-220.
67. delaVega A.L., Delcour A.H. Cadaverine induces closing of E. coli porins. EMBO J. 14:1995;6058-6065.
68. delaVega A.L., Delcour A.H. Polyamines decrease Escherichia coli outer membrane permeability. J. Bacteriol. 178:1996;3715-3721.
69. Le Dain A.C., Häse C.C., Tommassen J., Martinac B. Porins of Escherichia coli unidirectional gating by pressure. EMBO J. 15:1996;3524-3528.
70. Lakey J.H., Lea E.J.H., Pattus F. ompC mutants which allow growth on maltodextrins show increased channel size and greater voltage sensitivity. FEBS Lett. 278:1991;31-34.
71. Samartzidou H., Delcour A.H. E. coli PhoE porin has an opposite voltage-dependence to the homologous OmpF. EMBO J. 17:1998;93-100.
72. Watanabe M., Rosenbusch J., Schirmer T., Karplus M. Computer simulations of the OmpF porin from the outer membrane of Escherichia coli. Biophys. J. 72:1997;2094-2102.
73. Bainbridge G., Mobasheri H., Armstrong G.A., Lea E.J.A., Lakey J.H. Voltage-gating of Escherichia coli porin: A cystine-scanning mutagenesis study of loop 3. J. Mol. Biol. 275:1998;171-176.
74. Eppens E.F., Saint N., VanGelder P., vanBoxtel R., Tommassen J. Role of the constriction-loop in the gating of porin PhoE of Escherichia coli. FEBS Lett. 415:1997;317-320.
75. Soares C.M., Björkstén J., Tapia O. L3 loop-mediated mechanism of pore closing in porin: a molecular dynamics perturbation approach. Protein Eng. 8:1995;5-12.
76. Björkstén J., Soares C.M., Nilsson O., Tapia O. On the stability and plastic properties of the interior L3 loop in R. capsulatus porin. Protein Eng. 7:1994;487-493.
77. L.K. Bühler, Porins of Escherichia coli: Properties of the ion channels of porin B, porin F, porin C and phosphoporin, Ph.D. thesis, Basel, 1989.
78. Bishop N.D., Lea E.J.A., Mobasheri H., Spiro S. Altered voltage sensitivity of mutant OmpC porin channels. FEBS Lett. 379:1996;295-298.
79. Berrier C., Coulombe A., Houssin C., Ghazi A. Fast and slow kinetics of porin channels from Escherichia coli reconstituted into giant liposomes and studied by patch-clamp. FEBS Lett. 306:1992;251-256.
80. Liu N., Delcour A.H. The spontaneous gating activity of OmpC porin is affected by mutations of a putative hydrogen bond network or of a salt bridge between the L3 loop and the barrel. Protein Eng. 11:1998;797-802.
81. Gutman M., Tsfadia Y., Masad A., Nachliel E. Quantitation of physical-chemical properties of the aqueous phase inside the phoE channel. Biochim. Biophys. Acta. 1109:1992;141-148.
82. Benz R., Schmid A., Nakae T., VosScheperkeuter G.H. Pore formation by LamB of Escherichia coli in lipid bilayer membranes. J. Bacteriol. 165:1986;978-986.
83. Benz R., Bauer K. Permeation of hydrophilic molecules through the outer membrane of Gram-negative bacteria. Reviews on bacterial porins. Eur. J. Biochem. 176:1988;1-19.
84. Benz R., Schmid A., VosScheperkeuter G.H. Mechanism of sugar transport through the sugar-specific LamB channel of Escherichia coli outer membrane. J. Membr. Biol. 100:1987;21-29.
85. Nekolla S., Andersen C., Benz R. Noise analysis of ion current through the open and the sugar-induced closed state of the LamB channel of Escherichia coli outer membrane: evaluation of the sugar binding kinetics to the channel interior. Biophys. J. 66:1994;1388-1397.
86. Andersen C., Jordy M., Benz R. Evaluation of the rate constants of sugar transport through maltoporin LamB of Escherichia coli from the sugar-induced current noise. J. Gen. Physiol. 105:1995;385-401.
87. Jordy M., Andersen C., Schülein K., Ferenci T., Benz R. Rate constants of sugar transport through two LamB mutants of Escherichia coli: comparison with wild-type maltoporin and LamB of Salmonella typhimurium. J. Mol. Biol. 259:1996;666-678.
88. Andersen C., Rak B., Benz R. The gene bglH present in the bgl operon of Escherichia coli, responsible for uptake and fermentation of β-glucosides encodes for a carbohydrate-specific outer membrane porin. Mol. Microbiol. 31:1999;499-510.
89. Schwarz G. Bernasconi C.F. In Investigations of Rates and Mechanism of Reactions, vol. 6. 1986;27-139 Wiley, NY.
90. P. Van Gelder, C. Hilti, I. Bartoldus, J. Rosenbusch, M. Winterhalter, Sugar transport through Maltoporin of Escherichia coli, Submitted.
91. Kasianowicz J.J., Brandin E., Branton D., Deamer D.W. Characterization of individual polynucleotide molecules using a membrane channel. Proc. Acad. Sci. U.S.A. 93:1996;13770-13773.
92. Rostovtseva T.K., Bezrukov S.M. ATP transport through a single mitochondrial channel, VDAC, studied by current fluctuation analysis. Biophys. J. 74:1998;2365-2373.
93. Diederich A., Bähr G., Winterhalter M. Influence of surface charges on the rupture of black lipid membranes. Phys. Rev. 58E:1998;4883-4889.
94. Braun V. Energy-coupled transport and signal transduction through the Gram-negative outer membrane via TonB-ExbB-ExbD-dependent receptor proteins. FEMS Microbiol. Rev. 16:1995;295-307.
95. Klebba P.E., Rutz J.M., Liu J., Murphy C.K. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope. J. Bioenerg. Biomembr. 25:1993;603-611.
96. Locher K.P., Rees B., Koebnik R. et al. Transmembrane signalling across the ligand-gated FhuA-receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell. 95:1998;771-778.