Membrane proteins shape up: understanding in vitro folding

Current Opinion in Structural Biology

Volumn 16, Issue 4, 2006, Pages 480-488

  Booth, Paula J ^a   Curnow, Paul ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ENVIRONMENT; IN VITRO STUDY; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; THERMODYNAMICS;

ANIMALS; HUMANS; MEMBRANE PROTEINS; PROTEIN FOLDING;

EID: 33746644754     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2006.06.004     Document Type: Review

References (84)

1. Daggett V., and Fersht A.R. Is there a unifying mechanism for protein folding?. Trends Biochem Sci 28 (2003) 18-25
2. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
3. Booth P.J. Unravelling the folding of bacteriorhodopsin. Biochim Biophys Acta 1460 (2000) 4-14
4. Booth P.J., Templer R.H., Meijberg J.W., Allen S.J., Lorch M., and Curran A.R. In vitro studies of membrane protein folding. Crit Rev Biochem Mol Biol 36 (2001) 501-603
5. Tamm L.K., Hong H., and Liang B. Folding and assembly of beta-barrel membrane proteins. Biochim Biophys Acta 1666 (2004) 250-263
6. + channel. Biochemistry 41 (2002) 10771-10777
7. Barrera F.N., Renart M.L., Molina M.L., Poveda J.A., Encinar J.A., Fernandez A.M., Neira J.L., and Gonzalez-Ros J.M. Unfolding and refolding in vitro of a tetrameric, alpha-helical membrane protein: the prokaryotic potassium channel KcsA. Biochemistry 44 (2005) 14344-14352. The authors demonstrate that KcsA reversibly folds directly into DDM detergent micelles at high refolding yields when using low concentrations of TFE.
8. 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
9. Valiyaveetil F.I., MacKinnon R., and Muir T.W. Semisynthesis and folding of the potassium channel KcsA. J Am Chem Soc 124 (2002) 9113-9120
10. + channel. Angew Chem Int Ed Engl 43 (2004) 2504-2507. An important breakthrough in membrane protein work with the successful 'semi-synthesis' of a membrane protein. KcsA was made from one synthetic protein fragment and one overexpressed protein fragment, joined by chemical ligation in SDS. The channel was then formed in lipid vesicles with a yield of about 30%.
11. Clayton D., Shapovalov G., Maurer J.A., Dougherty D.A., Lester H.A., and Kochendoerfer G.G. Total chemical synthesis and electrophysiological characterization of mechanosensitive channels from Escherichia coli and Mycobacterium tuberculosis. Proc Natl Acad Sci USA 101 (2004) 4764-4769. Total chemical synthesis of the mechanosensitive channel of large conductance from E. coli (Ec-MscL) and Mycobacterium tuberculosis (Tb-MscL). Synthetic channel proteins were transferred to TFE before reconstitution in lipid vesicles.
12. Kaushal S., and Khorana H.G. Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33 (1994) 6121-6128
13. Hwa J., Klein-Seetharaman J., and Khorana H.G. Structure and function in rhodopsin: mass spectrometric identification of the abnormal intradiscal disulfide bond in misfolded retinitis pigmentosa mutants. Proc Natl Acad Sci USA 98 (2001) 4872-4876
14. Klein-Seetharaman J. Dual role of interactions between membranous and soluble portions of helical membrane receptors for folding and signaling. Trends Pharmacol Sci 26 (2005) 183-189
15. Rader A.J., Anderson G., Isin B., Khorana H.G., Bahar I., and Klein-Seetharaman J. Identification of core amino acids stabilizing rhodopsin. Proc Natl Acad Sci USA 101 (2004) 7246-7251
16. Baneres J.-L., Mesnier D., Martin A., Joubert L., Dumuis A., and Bockaert J. Molecular characterization of a purified 5-HT4 receptor: a structural basis for drug efficacy. J Biol Chem 280 (2005) 20253-20260. A significant and encouraging study, being the second report of the recovery of functional receptor from inclusion bodies in E. coli using a deceptively simple approach. This receptor, as with earlier work on the leukotriene receptor [17], was solubilised from overexpressed His-tag protein aggregates/inclusion bodies in urea. The protein was then purified on a nickel column, using a decreasing linear urea gradient in renaturing micelles. It is unclear how much refolding occurs, because the protein structure in the aggregate or urea is unknown.
17. 4 binding to recombinant BLT1. J Mol Biol 329 (2003) 801-814
18. Booth P.J., Flitsch S.L., Stern L.J., Greenhalgh D.A., Kim P.S., and Khorana H.G. Intermediates in the folding of the membrane protein bacteriorhodopsin. Nat Struct Biol 2 (1995) 139-143
19. Rim J., and Oprian D.D. Constitutive activation of opsin: interaction of mutants with rhodopsin kinase and arrestin. Biochemistry 34 (1995) 11938-11945
20. Reeves P.J., Hwa J., and Khorana H.G. Structure and function in rhodopsin: kinetic studies of retinal binding to purified opsin mutants in defined phospholipid-detergent mixtures serve as probes of the retinal binding pocket. Proc Natl Acad Sci USA 96 (1999) 1927-1931
21. Lazarova T., Brewin K.A., Stoeber K., and Robinson C.R. Characterization of peptides corresponding to the seven transmembrane domains of human adenosine A2A receptor. Biochemistry 43 (2004) 12945-12954. An investigation into the propensities of individual fragments of the adenosine receptor to form helices in lipid bilayers. Only four of the adenosine receptor transmembrane peptides, corresponding to helices TM3, TM4, TM5 and TM7, formed helices, with TM2 helix formation dependent on the presence of negatively charged phosphatidylglycerol lipids.
22. Thevenin D., Roberts M.F., Lazarova T., and Robinson C.R. Identifying interactions between transmembrane helices from the adenosine A2A receptor. Biochemistry 44 (2005) 16239-16245
23. Thevenin D., Lazarova T., Roberts M.F., and Robinson C.R. Oligomerization of the fifth transmembrane domain from the adenosine A2A receptor. Protein Sci 14 (2005) 2177-2186
24. Popot J.-L., and Engelman D.M. Membrane protein folding and oligomerization: the two stage model. Biochemistry 29 (1990) 4031-4037
25. Engelman D.M., Chen Y., Chin C.N., Curran A.R., Dixon A.M., Dupuy A.D., Lee A.S., Lehnert U., Matthews E.E., Reshetnyak Y.K., et al. Membrane protein folding: beyond the two stage model. FEBS Lett 555 (2003) 122-125
26. Hunt J.F., Earnest T.N., Bousche O., Kalghati K., Reilly K., Horváth C., Rothschild K.J., and Engelman D.M. A biophysical study of integral membrane protein folding. Biochemistry 36 (1997) 15156-15176
27. Otzen D.E. Folding of DsbB in mixed micelles: a kinetic analysis of the stability of a bacterial membrane protein. J Mol Biol 330 (2003) 641-649
28. Sehgal P., and Otzen D.E. Thermodynamics of unfolding of an integral membrane protein in mixed micelles. Protein Sci 15 (2006) 890-899
29. Mogensen J.E., Kleinschmidt J.H., Schmidt M.A., and Otzen D.E. Misfolding of a bacterial autotransporter. Protein Sci 14 (2005) 2814-2827
30. Pocanschi C.L., Apell H.J., Puntervoll P., Hogh B., Jensen H.B., Welte W., and Kleinschmidt J.H. 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
31. Linke D., Frank J., Pope M.S., Soll J., Ilkavets I., Fromme P., Burstein E.A., Reshetnyak Y.K., and Emelyanenko V.I. Folding kinetics and structure of OEP16. Biophys J 86 (2004) 1479-1487
32. Prodohl A., Volkmer T., Finger C., and Schneider D. Defining the structural basis for assembly of a transmembrane cytochrome. J Mol Biol 350 (2005) 744-756
33. Lu H., Marti T., and Booth P.J. Proline residues in transmembrane α helices affect the folding of bacteriorhodopsin. J Mol Biol 308 (2001) 437-446
34. Allen S.J., Kim J.-M., Khorana H.G., Lu H., and Booth P.J. Structure and function in bacteriorhodopsin: the effect of the interhelical loops on the protein folding kinetics. J Mol Biol 308 (2001) 423-435
35. Kim J.-M., Booth P., Allen S.J., and Khorana H.G. Structure and function in bacteriorhodopsin: the role of the interhelical loops in the folding and stability of bacteriorhodopsin. J Mol Biol 308 (2001) 409-422
36. Allen S.J., Curran A.R., Templer R.H., Meijberg W., and Booth P.J. Folding kinetics of an α helical membrane protein in phospholipid bilayer vesicles. J Mol Biol 342 (2004) 1279-1291
37. Allen S.J., Curran A.R., Templer R.H., Meijberg W., and Booth P.J. Controlling the folding efficiency of an integral membrane protein. J Mol Biol 342 (2004) 1293-1304. An illuminating study demonstrating how lipid bilayer properties can be used to control membrane protein folding. Bilayer curvature stress seems to affect, in a predictable manner, the folding rate, yield and stability of bacteriorhodopsin. Importantly, the kinetics of the folding reaction are studied, giving insight into the effect on particular stages of folding. The results led to rules for using curvature stress to guide the development of lipid bilayer folding systems.
38. Compton E.L., Farmer N.A., Lorch M., Mason J.M., Moreton K.M., and Booth P.J. Kinetics of an individual transmembrane helix during bacteriorhodopsin folding. J Mol Biol 357 (2006) 325-338. The insertion kinetics of an individual helix of bacteriorhodopsin were monitored during folding from SDS into lipid vesicles. Individual fluorescence labels were incorporated site specifically, via cysteine residues, at certain sites along helix D. This is the first study to follow a specific structural element during membrane protein folding.
39. Janovjak H., Struckmeier J., Hubain M., Kedrov A., Kessler M., and Muller D.J. Probing the energy landscape of the membrane protein bacteriorhodopsin. Structure 12 (2004) 871-879
40. Janovjak H., Kessler M., Oesterhelt D., Gaub H., and Muller D.J. Unfolding pathways of native bacteriorhodopsin depend on temperature. EMBO J 22 (2003) 5220-5229
41. BT per residue. Evidence of the refolding of helix hairpins and individual helices, together with stable helical intermediates, is found, in line with the two-stage model.
42. -1. Denaturation fit well to a two-state equation, with a transition midpoint at about 3 M urea.
43. Kleinschmidt J.H., and Tamm L.K. Secondary and tertiary structure formation of the beta-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J Mol Biol 324 (2002) 319-330
44. Oxenoid K., Sonnichsen F.D., and Sanders C.R. Conformationally specific misfolding of an integral membrane protein. Biochemistry 40 (2001) 5111-5118
45. Nagy J.K., Lonzer W.L., and Sanders C.R. Kinetic study of folding and misfolding of diacylglycerol kinase in model membranes. Biochemistry 40 (2001) 8971-8980
46. Nagy J.K., and Sanders C.R. A critical residue in the folding pathway of an integral membrane protein. Biochemistry 41 (2002) 9021-9025
47. Nagy J.K., and Sanders C.R. Destabilizing mutations promote membrane protein misfolding. Biochemistry 43 (2004) 19-25
48. Lorch M., and Booth P.J. Insertion kinetics of a denatured alpha helical membrane protein into phospholipid bilayer vesicles. J Mol Biol 344 (2004) 1109-1121. The first report on the insertion kinetics of a denatured α-helical membrane protein during folding into lipid vesicles. DGK is refolded from a urea-denatured state. A particularly detailed study of a complex kinetic scheme is presented, including evaluation over a wide range of protein and lipid concentrations. The work also highlights the issue of competing protein misfolding/aggregation before insertion into the lipid bilayer and presents evidence of some reversible aggregation events.
49. Mick V., Geister S., and Paulsen H. The folding state of the lumenal loop determines the thermal stability of light-harvesting chlorophyll a/b protein. Biochemistry 43 (2004) 14704-14711
50. Mick V., Eggert K., Heinemann B., Geister S., and Paulsen H. Single amino acids in the lumenal loop domain influence the stability of the major light-harvesting chlorophyll a/b complex. Biochemistry 43 (2004) 5467-5473
51. Horn R., and Paulsen H. Early steps in the assembly of light-harvesting chlorophyll a/b complex: time-resolved fluorescence measurements. J Biol Chem 279 (2004) 44400-44406. This continues work on the spontaneous assembly of the light-harvesting chlorophyll a/b complex (LHCII) from its pigment and protein components in detergent micelles. Early steps in chlorophyll binding are monitored by measuring excitation energy transfer from a fluorescent dye, which is covalently bound to the protein, to the chlorophylls.
52. Yang C., Horn R., and Paulsen H. The light-harvesting chlorophyll a/b complex can be reconstituted in vitro from its completely unfolded apoprotein. Biochemistry 42 (2003) 4527-4533
53. Reinsberg D., Ottman K., Booth P.J., and Paulsen H. Effects of chlorophyll a, chlorophyll b and xanthophylls on the in vitro assembly of the major light-harvesting chlorophyll a/b complex, LHCIIb. J Mol Biol 308 (2001) 59-67
54. London E., and Khorana H.G. Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures. J Biol Chem 257 (1982) 7003-7011
55. Lu H., and Booth P.J. The final stages of folding of the membrane protein bacteriorhodopsin occur by kinetically indistinguishable parallel folding paths that are mediated by pH. J Mol Biol 299 (2000) 233-243
56. Booth P.J. Sane in the membrane: designing systems to modulate membrane proteins. Curr Opin Struct Biol 15 (2005) 435-440
57. Gorzelle B.M., Nagy J.K., Oxenoid K., Lonzer W.L., Cafiso D.S., and Sanders C.R. Reconstitutive refolding of diacylglycerol kinase, an integral membrane protein. Biochemistry 38 (1999) 16373-16382
58. Lau F.W., and Bowie J.U. A method for assessing the stability of a membrane protein. Biochemistry 36 (1997) 5884-5892
59. Sehgal P., Mogensen J.E., and Otzen D.E. Using micellar mole fractions to assess membrane protein stability in mixed micelles. Biochim Biophys Acta 1716 (2005) 59-68
60. Klug C.S., Su W., Liu J., Klebba P.E., and Feix J.B. Denaturant unfolding of the ferric enterobactin receptor and ligand-induced stabilization studied by site-directed spin labeling. Biochemistry 34 (1995) 14230-14236
61. Oesterhelt F., Oesterhelt D., Pfeiffer M., Engel A., Gaub H.E., and Muller D.J. Unfolding pathways of individual bacteriorhodopsins. Science 288 (2000) 143-146
62. Kedrov A., Ziegler C., Janovjak H., Kuhlbrandt W., and Muller D.J. Controlled unfolding and refolding of a single sodium-proton antiporter using atomic force microscopy. J Mol Biol 340 (2004) 1143-1152
63. Kedrov A., Janovjak H., Ziegler C., Kuhlbrandt W., and Muller D.J. Observing folding pathways and kinetics of a single sodium-proton antiporter from Escherichia coli. J Mol Biol 355 (2006) 2-8
64. Riley M.L., Wallace B.A., Flitsch S.L., and Booth P.J. Slow α helical formation during folding of a membrane protein. Biochemistry 36 (1997) 192-196
65. Booth P.J., and Curran A.R. Membrane protein folding. Curr Opin Struct Biol 9 (1999) 115-121
66. Marti T. Refolding of bacteriorhodopsin from expressed polypeptide fragments. J Biol Chem 273 (1998) 9312-9322
67. Dill K.A., and Chan H.S. From Levinthal to pathways to funnels. Nat Struct Biol 4 (1997) 10-19
68. Bowie J.U. Solving the membrane protein folding problem. Nature 438 (2005) 581-589
69. Eisele J.-L., and Rosenbusch J.P. In vitro folding and oligomerization of a membrane protein. J Biol Chem 265 (1990) 10217-10220
70. 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
71. Surrey T., and Jähnig F. Kinetics of folding and membrane insertion of a β-barrel membrane protein. J Biol Chem 270 (1995) 28199-28203
72. Surrey T., Schmid A., and Jähnig F. Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry 35 (1996) 2283-2288
73. Booth P.J., and Paulsen H. Assembly of the light harvesting chlorophyll a/b complex in vitro. Time-resolved fluorescence measurements. Biochemistry 35 (1996) 5103-5108
74. Russ W.P., and Engelman D.M. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 296 (2000) 911-919
75. Henderson R., Baldwin J.M., Ceska T.A., Zemlin F., Beckmann E., and Downing K.H. Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213 (1990) 899-929
76. Cowan S.W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R.A., Jansonius J.N., and Rosenbusch J.P. Crystal structures explain functional properties of two E. coli porins. Nature 358 (1992) 727-733
77. Kühlbrandt W., Wang D.N., and Fujioshi Y. Atomic model of plant light-harvesting complex by electron crystallography. Nature 367 (1994) 614-621
78. Pautsch A., and Schulz G.E. Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 5 (1998) 1013-1017
79. + conduction and selectivity. Science 280 (1998) 69-77
80. Buchanan S.K., Smith B.S., Venkatramani L., Xia D., Esser L., Palnitkar M., Chakraborty R., and van der Helm D. J. D: Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6 (1999) 56-63
81. Luecke H., Schobert B., Richter H.-T., Cartailler J.-P., and Lanyi J.K. Structure of bacteriorhodopsin at 1.55 Å resolution. J Mol Biol 291 (1999) 899-911
82. Pautsch A., and Schulz G.E. High-resolution structure of the OmpA membrane domain. J Mol Biol 298 (2000) 273-282
83. + selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J Mol Biol 333 (2003) 965-975
84. Liu Z., Yan H., Wang K., Kuang T., Zhang J., Gui L., An X., and Chang W. Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428 (2004) 287-292