Association of neighboring β-strands of outer membrane protein A in lipid bilayers revealed by site-directed fluorescence quenching

Journal of Molecular Biology

Volumn 407, Issue 2, 2011, Pages 316-332

  Kleinschmidt, Jörg H ^a   Bulieris, Paula V ^a   Qu, Jian ^a   Dogterom, Marileen ^b,c   Den Blaauwen, Tanneke ^b  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c FOM INSTITUTE AMOLF   (Netherlands)

Author keywords

BAM complex; fluorescence quenching; kinetics; lipidprotein interactions; membrane protein folding

Indexed keywords

CYSTEINE; MUTANT PROTEIN; OUTER MEMBRANE PROTEIN A; TRYPTOPHAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; FLUORESCENCE; LIPID BILAYER; LIPID MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; SPIN LABELING;

EID: 79952313002     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.01.021     Document Type: Article

References (59)

1. Popot J.L., Gerchman S.E., and Engelman D.M. Refolding of bacteriorhodopsin in lipid bilayers. A thermodynamically controlled two-stage process J. Mol. Biol. 198 1987 655 676 (Pubitemid 18034980)
2. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., and Dupuy A.D. Membrane protein folding: beyond the two stage model FEBS Lett. 555 2003 122 125 (Pubitemid 37431108)
3. Booth P.J. A paradigm of membrane protein folding: principles, kinetics and stability of bacteriorhodopsin folding L.K. Tamm, Protein-Lipid Interactions: From Membrane Domains to Cellular Networks 2005 Wiley-VCH Weinheim, Germany 57 80
4. Mackenzie K.R. Folding and stability of α-helical integral membrane proteins Chem. Rev. 106 2006 1931 1977 (Pubitemid 43792787)
5. Stanley A.M., and Fleming K.G. The process of folding proteins into membranes: challenges and progress Arch. Biochem. Biophys. 469 2008 46 66 (Pubitemid 350212853)
6. MacKenzie K.R., and Engelman D.M. Structure-based prediction of the stability of transmembrane helix-helix interactions: the sequence dependence of glycophorin A dimerization Proc. Natl Acad. Sci. USA 95 1998 3583 3590
7. Lemmon M.A., Flanagan J.M., Treutlein H.R., Zhang J., and Engelman D.M. Sequence specificity in the dimerization of transmembrane α-helices Biochemistry 31 1992 12719 12725 (Pubitemid 23027049)
8. Melnyk R.A., Partridge A.W., and Deber C.M. Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage J. Mol. Biol. 315 2002 63 72 (Pubitemid 34722111)
9. Mingarro I., Elofsson A., and von Heijne G. Helix-helix packing in a membrane-like environment J. Mol. Biol. 272 1997 633 641 (Pubitemid 27429847)
10. Walters R.F., and DeGrado W.F. Helix-packing motifs in membrane proteins Proc. Natl Acad. Sci. USA 103 2006 13658 13663 (Pubitemid 44413963)
11. Schneider D. Rendezvous in a membrane: close packing, hydrogen bonding, and the formation of transmembrane helix oligomers FEBS Lett. 577 2004 5 8 (Pubitemid 39452353)
12. Arora A., Abildgaard F., Bushweller J.H., and Tamm L.K. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy Nat. Struct. Biol. 8 2001 334 338 (Pubitemid 32275019)
13. Pautsch A., and Schulz G.E. High-resolution structure of the OmpA membrane domain J. Mol. Biol. 298 2000 273 282
14. Fernandez C., Adeishvili K., and Wüthrich K. Transverse relaxation-optimized NMR spectroscopy with the outer membrane protein OmpX in dihexanoyl phosphatidylcholine micelles Proc. Natl Acad. Sci. USA 98 2001 2358 2363 (Pubitemid 32209487)
15. Vogt J., and Schulz G.E. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence Structure Folding Des. 7 1999 1301 1309 (Pubitemid 29482991)
16. Remaut H., Tang C., Henderson N.S., Pinkner J.S., Wang T., and Hultgren S.J. Fiber formation across the bacterial outer membrane by the chaperone/usher pathway Cell 133 2008 640 652 (Pubitemid 351636304)
17. Hiller S., Garces R.G., Malia T.J., Orekhov V.Y., Colombini M., and Wagner G. Solution structure of the integral human membrane protein VDAC-1 in detergent micelles Science 321 2008 1206 1210
18. Bayrhuber M., Meins T., Habeck M., Becker S., Giller K., and Villinger S. Structure of the human voltage-dependent anion channel Proc. Natl Acad. Sci. USA 105 2008 15370 15375
19. Huang K.S., Bayley H., Liao M.J., London E., and Khorana H.G. Refolding of an integral membrane protein. Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments J. Biol. Chem. 256 1981 3802 3809
20. Debnath D., Nielsen K.L., and Otzen D.E. In vitro association of fragments of a β-sheet membrane protein Biophys. Chem. 148 2010 112 120
21. Koebnik R. In vivo membrane assembly of split variants of the E. coli outer membrane protein OmpA EMBO J. 15 1996 3529 3537 (Pubitemid 26239765)
22. von Heijne G., and Gavel Y. Topogenic signals in integral membrane proteins Eur. J. Biochem. 174 1988 671 678
23. Ben-Tal N., Sitkoff D., Topol I.A., Yang A.S., Burt S.K., and Honig B. Free energy of amide hydrogen bond formation in vaccuum, in water, and in liquid alkane solution J. Phys. Chem. B 101 1997 450 457 (Pubitemid 127617329)
24. White S.H., and Wimley W.C. Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365 (Pubitemid 29319262)
25. Bulieris P.V., Behrens S., Holst O., and Kleinschmidt J.H. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide J. Biol. Chem. 278 2003 9092 9099 (Pubitemid 36800389)
26. Kleinschmidt J.H. Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers Chem. Phys. Lipids 141 2006 30 47 (Pubitemid 43744430)
27. Kleinschmidt J.H., den Blaauwen T., Driessen A., and Tamm L.K. Outer membrane protein A of E. coli inserts and folds into lipid bilayers by a concerted mechanism Biochemistry 38 1999 5006 5016
28. London E., and Feigenson G.W. Fluorescence quenching in model membranes. 1. Characterization of quenching caused by a spin-labeled phospholipid Biochemistry 20 1981 1932 1938
29. Pautsch A., and Schulz G.E. Structure of the outer membrane protein A transmembrane domain Nat. Struct. Biol. 5 1998 1013 1017 (Pubitemid 28506635)
30. Cierpicki T., Liang B., Tamm L.K., and Bushweller J.H. 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 (Pubitemid 43830581)
31. Delano W.L. The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
32. Surrey T., and Jähnig F. Refolding and oriented insertion of a membrane protein into a lipid bilayer Proc. Natl Acad. Sci. USA 89 1992 7457 7461
33. Chattopadhyay A., and London E. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids Biochemistry 26 1987 39 45
34. Ladokhin A.S., and Holloway P.W. Fluorescence of membrane-bound tryptophan octyl ester: a model for studying intrinsic fluorescence of protein-membrane interactions Biophys. J. 69 1995 506 517
35. Ebie Tan A., Burgess N.K., DeAndrade D.S., Marold J.D., and Fleming K.G. Self-association of unfolded outer membrane proteins Macromol. Biosci. 10 2010 763 767
36. Kleinschmidt J.H., and Tamm L.K. Secondary and tertiary structure formation of the β-barrel membrane protein OmpA is synchronized and depends on membrane thickness J. Mol. Biol. 324 2002 319 330 (Pubitemid 35379031)
37. Kleinschmidt J.H., and Tamm L.K. Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism Biochemistry 35 1996 12993 13000 (Pubitemid 26349447)
38. Kleinschmidt J.H., and Tamm L.K. Time-resolved distance determination by tryptophan fluorescence quenching: probing intermediates in membrane protein folding Biochemistry 38 1999 4996 5005
39. Marsh D., Shanmugavadivu B., and Kleinschmidt J.H. Membrane elastic fluctuations and the insertion and tilt of β-barrel proteins Biophys. J. 91 2006 227 232 (Pubitemid 44015322)
40. King M.D., and Marsh D. Free volume model for lipid lateral diffusion coefficients. Assessment of the temperature dependence in phosphatidylcholine and phosphatidylethanolamine bilayers Biochim. Biophys. Acta 862 1986 231 234
41. Huysmans G.H., Baldwin S.A., Brockwell D.J., and Radford S.E. The transition state for folding of an outer membrane protein Proc. Natl Acad. Sci. USA 107 2010 4099 4104
42. Rodionova N.A., Tatulian S.A., Surrey T., Jähnig F., and Tamm L.K. Characterization of two membrane-bound forms of OmpA Biochemistry 34 1995 1921 1929
43. Qu J., Behrens-Kneip S., Holst O., and Kleinschmidt J.H. Binding regions of outer membrane protein A in complexes with the periplasmic chaperone Skp. A site-directed fluorescence study Biochemistry 48 2009 4926 4936
44. Pocanschi C.L., Patel G.J., Marsh D., and Kleinschmidt J.H. Curvature elasticity and refolding of OmpA in large unilamellar vesicles Biophys. J. 91 2006 L75 L78
45. Pocanschi C.L., Apell H.J., Puntervoll P., Høgh B.T., Jensen H.B., Welte W., and Kleinschmidt J. The major outer membrane protein of Fusobacterium nucleatum (FomA) folds and inserts into lipid bilayers via parallel folding pathways J. Mol. Biol. 355 2006 548 561 (Pubitemid 41785756)
46. Anbazhagan V., Vijay N., Kleinschmidt J.H., and Marsh D. Protein-lipid interactions with Fusobacterium nucleatum major outer membrane protein foma: spin-label EPR and polarized infrared spectroscopy Biochemistry 47 2008 8414 8423
47. Kleivdal H., Benz R., Tommassen J., and Jensen H.B. Identification of positively charged residues of FomA porin of Fusobacterium nucleatum which are important for pore function Eur. J. Biochem. 260 1999 818 824 (Pubitemid 29148649)
48. Puntervoll P., Ruud M., Bruseth L.J., Kleivdal H., Høgh B.T., Benz R., and Jensen H.B. Structural characterization of the fusobacterial non-specific porin FomA suggests a 14-stranded topology, unlike the classical porins Microbiology 148 2002 3395 3403 (Pubitemid 35414451)
49. Buchanan S.K. Overexpression and refolding of an 80-kDa iron transporter from the outer membrane of Escherichia coli Biochem. Soc. Trans. 27 1999 903 908 (Pubitemid 30032150)
50. Burgess N.K., Dao T.P., Stanley A.M., and Fleming K.G. β-barrel proteins that reside in the Escherichia coli outer membrane in vivo demonstrate varied folding behavior in vitro J. Biol. Chem. 283 2008 26748 26758
51. Patel G.J., Behrens-Kneip S., Holst O., and Kleinschmidt J.H. The periplasmic chaperone Skp facilitates targeting, insertion and folding of OmpA into lipid membranes with a negative membrane surface potential Biochemistry 48 2009 10235 10245
52. Prilipov A., Phale P.S., Van Gelder P., Rosenbusch J.P., and Koebnik R. Coupling site-directed mutagenesis with high-level expression: large scale production of mutant porins from E. coli FEMS Microbiol. Lett. 163 1998 65 72 (Pubitemid 28267359)
53. Chung C.T., Niemela S.L., and Miller R.H. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution Proc. Natl Acad. Sci. USA 86 1989 2172 2175 (Pubitemid 19102474)
54. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
55. Owenius R., Osterlund M., Lindgren M., Svensson M., Olsen O.H., and Persson E. Properties of spin and fluorescent labels at a receptor-ligand interface Biophys. J. 77 1999 2237 2250 (Pubitemid 29463184)
56. Riddles P.W., Blakeley R.L., and Zerner B. Reassessment of Ellman's reagent Methods Enzymol. 91 1983 49 60
57. Heinrikson R.L. The selective S-methylation of sulfhydryl groups in proteins and peptides with methyl-p-nitrobenzenesulfonate J. Biol. Chem. 246 1971 4090 4096
58. Hunziker P.E. Cysteine modification of metallothionein Methods Enzymol. 205 1991 399 400
59. Kleinschmidt J.H., Wiener M.C., and Tamm L.K. Outer membrane protein A of E. coli folds into detergent micelles, but not in the presence of monomeric detergent Protein Sci. 8 1999 2065 2071 (Pubitemid 29489934)