Correct Folding of the β-Barrel of the Human Membrane Protein VDAC Requires a Lipid Bilayer

Journal of Molecular Biology

Volumn 368, Issue 1, 2007, Pages 66-78

  Shanmugavadivu, Baladhandapani ^a   Apell, Hans Jürgen ^a   Meins, Thomas ^b   Zeth, Kornelius ^b   Kleinschmidt, Jörg H ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

membrane insertion; membrane protein folding; membrane protein stability; outer membrane protein; VDAC

Indexed keywords

ADENOSINE TRIPHOSPHATE; DETERGENT; LIPID; OUTER MEMBRANE PROTEIN A; TRANSLOCON; UREA; VOLTAGE DEPENDENT ANION CHANNEL 1;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; BETA SHEET; CELL MEMBRANE; CONDUCTANCE; CONTROLLED STUDY; DILUTION; ENERGY RESOURCE; LIPID BILAYER; MICELLE; MITOCHONDRIAL MEMBRANE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 33947324465     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.01.066     Document Type: Article

References (42)

1. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., Dupuy A.D., et al. Membrane protein folding: beyond the two stage model. FEBS Letters 555 (2003) 122-125
2. Booth P.J. A paradigm of membrane protein folding: principles, kinetics and stability of bacteriorhodopsin folding. In: Tamm L.K. (Ed). Protein-Lipid Interactions: From Membrane Domains to Cellular Networks (2005), Wiley-VCH, Weinheim 57-80
3. Kleinschmidt J.H. Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers. Chem. Phys. Lipids 141 (2006) 30-47
4. Colombini M. VDAC: the channel at the interface between mitochondria and the cytosol. Mol. Cell. Biochem. 256-257 (2004) 107-115
5. Wiedemann N., Truscott K.N., Pfannschmidt S., Guiard B., Meisinger C., and Pfanner N. Biogenesis of the protein import channel Tom40 of the mitochondrial outer membrane: intermembrane space components are involved in an early stage of the assembly pathway. J. Biol. Chem. 279 (2004) 18188-18194
6. Song J., Midson C., Blachly-Dyson E., Forte M., and Colombini M. The topology of VDAC as probed by biotin modification. J. Biol. Chem. 273 (1998) 24406-24413
7. Guo X.W., Smith P.R., Cognon B., D'Arcangelis D., Dolginova E., and Mannella C.A. Molecular design of the voltage-dependent, anion-selective channel in the mitochondrial outer membrane. J. Struct. Biol. 114 (1995) 41-59
8. Abu-Hamad S., Sivan S., and Shoshan-Barmatz V. The expression level of the voltage-dependent anion channel controls life and death of the cell. Proc. Natl Acad. Sci. USA 103 (2006) 5787-5792
9. Benz R. Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta 1197 (1994) 167-196
10. Abrecht H., Goormaghtigh E., Ruysschaert J.M., and Homble F. Structure and orientation of two voltage-dependent anion-selective channel isoforms. An attenuated total reflection fourier-transform infrared spectroscopy study. J. Biol. Chem. 275 (2000) 40992-40999
11. Casadio R., Jacoboni I., Messina A., and De Pinto V. A 3D model of the voltage-dependent anion channel (VDAC). FEBS Letters 520 (2002) 1-7
12. Koppel D.A., Kinnally K.W., Masters P., Forte M., Blachly-Dyson E., and Mannella C.A. Bacterial expression and characterization of the mitochondrial outer membrane channel. Effects of N-terminal modifications. J. Biol. Chem. 273 (1998) 13794-13800
13. Shao L., Kinnally K.W., and Mannella C.A. Circular dichroism studies of the mitochondrial channel, VDAC, from Neurospora crassa. Biophys. J. 71 (1996) 778-786
14. Cowan S.W., Garavito R.M., Jansonius J.N., Jenkins J.A., Karlsson R., Konig N., et al. The structure of OmpF porin in a tetragonal crystal form. Structure 3 (1995) 1041-1050
15. 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
16. Buchanan S.K. β-Barrel proteins from bacterial outer membranes: structure, function and refolding. Curr. Opin. Struct. Biol. 9 (1999) 455-461
17. 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
18. 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
19. Surrey T., Schmid A., and Jähnig F. Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry 35 (1996) 2283-2288
20. Blachly-Dyson E., Zambronicz E.B., Yu W.H., Adams V., McCabe E.R., Adelman J., et al. Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. J. Biol. Chem. 268 (1993) 1835-1841
21. Benz R. Biophysical properties of porin pores from mitochondrial outer membrane of eukaryotic cells. Experientia 46 (1990) 131-137
22. Colombini M. Voltage gating in the mitochondrial channel, VDAC. J. Membr. Biol. 111 (1989) 103-111
23. Liu M.Y., and Colombini M. Regulation of mitochondrial respiration by controlling the permeability of the outer membrane through the mitochondrial channel, VDAC. Biochim. Biophys. Acta 1098 (1992) 255-260
24. 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
25. Bollag D.M., and Edelstein S.J. Protein Methods (1991), Wiley-Liss, New York
26. 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
27. 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
28. Ishikawa D., Yamamoto H., Tamura Y., Moritoh K., and Endo T. Two novel proteins in the mitochondrial outer membrane mediate β-barrel protein assembly. J. Cell Biol. 166 (2004) 621-627
29. Kozjak V., Wiedemann N., Milenkovic D., Lohaus C., Meyer H.E., Guiard B., et al. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 278 (2003) 48520-48523
30. Paschen S.A., Waizenegger T., Stan T., Preuss M., Cyrklaff M., Hell K., et al. Evolutionary conservation of biogenesis of β-barrel membrane proteins. Nature 426 (2003) 862-866
31. Voulhoux R., Bos M.P., Geurtsen J., Mols M., and Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299 (2003) 262-265
32. Werner J., and Misra R. YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol. Microbiol. 57 (2005) 1450-1459
33. Wu T., Malinverni J., Ruiz N., Kim S., Silhavy T.J., and Kahne D. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121 (2005) 235-245
34. Hwang P.M., Choy W.Y., Lo E.I., Chen L., Forman-Kay J.D., Raetz C.R., et al. Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl Acad. Sci. USA 99 (2002) 13560-13565
35. 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. Letters 163 (1998) 65-72
36. In: Ausubel F.M., Brent R., Kingston R.E., Moore D., Seidman J.G., Smith J.A., and Struhl K. (Eds). Short Protocols in Molecular Biology. 4th edit. (1999), John Wiley and Sons, New York
37. Abrams F.S., and London E. Calibration of the parallax fluorescence quenching method for determination of membrane penetration depth: refinement and comparison of quenching by spin-labeled and brominated lipids. Biochemistry 31 (1992) 5312-5322
38. Whitmore L., and Wallace B.A. DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucl. Acids Res. 32 (2004) W668-W673
39. Provencher S.W., and Glockner J. Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20 (1981) 33-37
40. Sreerama N., Venyaminov S.Y., and Woody R.W. Estimation of the number of α-helical and beta-strand segments in proteins using circular dichroism spectroscopy. Protein Sci. 8 (1999) 370-380
41. Compton L.A., and Johnson Jr. W.C. Analysis of protein circular dichroism spectra for secondary structure using a simple matrix multiplication. Anal. Biochem. 155 (1986) 155-167
42. Rouser G., Fleischer S., and Yamamoto A. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5 (1970) 494-496