Amphipol-assisted folding of bacteriorhodopsin in the presence or absence of lipids: Functional consequences

European Biophysics Journal

Volumn 42, Issue 2-3, 2013, Pages 85-101

  Dahmane, Tassadite ^a,c   Rappaport, Fabrice ^b   Popot, Jean Luc ^a  

^a PSL Research University   (France)

^b National de la Recherche Scientifique Université Pierre et Marie Curie   (France)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Amphipol A8 35; Anfinsen's principle; Folding; Membrane protein; Photocycle

Indexed keywords

AMPHIPOL A8 35; AMPHIPOL A8-35; BACTERIO OPSIN; BACTERIO-OPSIN; BACTERIORHODOPSIN; DODECYL SULFATE SODIUM; MEMBRANE LIPID; POLYMER; PROPYLAMINE; RETINAL; SOLVENT;

CHEMISTRY; CONFERENCE PAPER; DRUG EFFECT; METABOLISM; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; TEMPERATURE; TIME;

BACTERIORHODOPSINS; MEMBRANE LIPIDS; POLYMERS; PROPYLAMINES; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN REFOLDING; PROTEIN STABILITY; RETINALDEHYDE; SODIUM DODECYL SULFATE; SOLVENTS; TEMPERATURE; TIME FACTORS;

EID: 84879501057     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-012-0839-z     Document Type: Conference Paper

References (58)

1. 1. EMBO J 30:4652-4664
2. Anfinsen CB (1973) Principles that govern the folding of protein chains. Science 181:223-230
3. Anfinsen CB, Harber E, Sela M (1961) The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain. Proc Natl Acad Sci USA 47:1309-1314
4. Banères J-L, Popot J-L, Mouillac B (2011) New advances in production and functional folding of G protein-coupled receptors. Trends Biotechnol 29:314-322
5. Bazzacco P, Billon-Denis E, Sharma KS, Catoire LJ, Mary S, Le Bon C, Point E, Banères J-L, Durand G, Zito F, Pucci B, Popot J-L (2012) Non-ionic homopolymeric amphipols: application to membrane protein folding, cell-free synthesis, and solution NMR. Biochemistry 51:1416-1430
6. Béal D, Rappaport F, Joliot P (1999) A new high-sensitivity 10-ns time-resolution spectrophotometric technique adapted to in vivo analysis of the photosynthetic apparatus. Rev Sci Inst 70:202-207
7. Booth PJ, Templer RH, Meijberg W, Allen SJ, Curran AR, Lorch M (2001) In vitro studies of membrane protein folding. Crit Rev Biochem Mol Biol 36:501-603
8. Buchanan SK (1999) Beta-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr Opin Struct Biol 9:455-461
9. 4 adopts a highly constrained conformation when associated to human BLT2. J Am Chem Soc 132:9049-9057
10. Catoire LJ, Zoonens M, van Heijenoort C, Giusti F, Guittet E, Popot J-L (2010b) Solution NMR mapping of water-accessible residues in the transmembrane β-barrel of OmpX. Eur Biophys J 39:623-630
11. 2+-ATPase. J Biol Chem 275:18623-18637
12. Corcelli A, Lattanzio VMT, Mascolo G, Papadia P, Fanizzi F (2002) Lipid-protein stoichiometries in a crystalline biological membrane: NMR quantitative analysis of the lipid extract of the purple membrane. J Lipid Res 43:132-140
13. Dahmane T, Damian M, Mary S, Popot J-L, Banères J-L (2009) Amphipol-assisted in vitro folding of G protein-coupled receptors. Biochemistry 48:6516-6521
14. Dahmane T, Giusti F, Catoire LJ, Popot J-L (2011) Sulfonated amphipols: synthesis, properties and applications. Biopolymers 95:811-823
15. Duarte AMS, Wolfs CJAM, Koehorsta RBM, Popot J-L, Hemminga MA (2008) Solubilization of V-ATPase transmembrane peptides by amphipol A8-35. J Pept Chem 14:389-393
16. Fitter J, Verclas SAW, Lechner RE, Seelert H, Dencher NA (1998) Function and picosecond dynamics of bacteriorhodopsin in purple membrane at different lipidation and hydration. FEBS Lett 433:321-325
17. Fukuda K, Ikegami A, Nasuda-Kouyama A, Kouyama T (1990) Effect of partial delipidation of purple membrane on the photodynamics of bacteriorhodopsin. Biochemistry 29:1997-2002
18. Gohon Y, Pavlov G, Timmins P, Tribet C, Popot J-L, Ebel C (2004) Partial specific volume and solvent interactions of amphipol A8-35. Anal Biochem 334:318-334
19. Gohon Y, Giusti F, Prata C, Charvolin D, Timmins P, Ebel C, Tribet C, Popot J-L (2006) Well-defined nanoparticles formed by hydrophobic assembly of a short and polydisperse random terpolymer, amphipol A8-35. Langmuir 22:1281-1290
20. Gohon Y, Dahmane T, Ruigrok R, Schuck P, Charvolin D, Rappaport F, Timmins P, Engelman DM, Tribet C, Popot J-L, Ebel C (2008) Bacteriorhodopsin/ amphipol complexes: structural and functional properties. Biophys J 94:3523-3537
21. Hartsel SC, Cassim JY (1988) Structure and photodynamics of bacteriorhodopsin in a delipidated contracted lattice form of purple membrane. Biochemistry 27:3720-3724
22. Haupts U, Tittor J, Oesterhelt D (1999) Closing in on bacteriorhodopsin: progress in understanding the molecule. Annu Rev Biophys Biomol Struct 28:367-399
23. Henderson R, Unwin PNT (1975) Three-dimensional model of purple membrane obtained by electron microscopy. Nature 257:28-32
24. Henderson R, Baldwin JM, Ceska TA, Zemlin F, Beckmann E, Downing KH (1990) Model for the structure of bacteriorhodopsin based on high resolution electron cryo-microscopy. J Mol Biol 213:899-929
25. Hendler RW, Bose S (2003) Interconversions among four M-intermediates in the bacteriorhodopsin photocycle. Eur J Biochem 270:3518-3524
26. Hendler RW, Dracheva S (2001) Importance of lipids for bacteriorhodopsin structure, photocycle, and function. Biochemistry (Mosc.) 66:1311-1314
27. Huang K-S, Bayley H, Liao M-J, London E, Khorana HG (1981) Refolding of an integral membrane protein. Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments. J Biol Chem 256:3802-3809
28. Jackson MB, Sturtevant JM (1978) Phase transitions of the purple membranes of Halobacterium halobium. Biochemistry 17:911-915
29. Jang DJ, el-Sayed MA (1988) Deprotonation of lipid-depleted bacteriorhodopsin. Proc Natl Acad Sci USA 85:5918-5922
30. Joshi M, Dracheva S, Mukhopadhyay AK, Bose S, Hendler RW (1998) Importance of specific native lipids in controlling the photocycle of bacteriorhodopsin. Biochemistry 37:14463-14470
31. Kiefer H (2003) In vitro folding of α-helical membrane proteins. Biochim Biophys Acta 1610:57-62
32. Liao M-J, Huang K-S, Khorana HG (1984) Regeneration of native bacteriorhodopsin structure from fragments. J Biol Chem 259:4200-4204
33. London E, Khorana HG (1982) Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures. J Biol Chem 257:7003-7011
34. Martinez KL, Gohon Y, Corringer P-J, Tribet C, Mérola F, Changeux J-P, Popot J-L (2002) Allosteric transitions of Torpedo acetylcholine receptor in lipids, detergent and amphipols: molecular interactions vs. physical constraints. FEBS Lett 528:251-256
35. Milder SJ, Thorgeirsson TE, Miercke LJ, Stroud RM, Kliger DS (1991) Effects of detergent environments on the photocycle of purified monomeric bacteriorhodopsin. Biochemistry 30:1751-1761
36. Mukerjee P, Mysels KJ (1971) Critical micelle concentrations of aqueous surfactant systems. National Bureau of Standards, Washington, p 227
37. Mukhopadhyay AK, Dracheva S, Bose S, Hendler RW (1996) Control of the integral membrane proton pump, bacteriorhodopsin, by purple membrane lipids of Halobacterium halobium. Biochemistry 35:1751-1761
38. Neutze R, Pebay-Peyroula E, Edman K, Royant A, Navarro J, Landau EM (2002) Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport. Biochim Biophys Acta 1565:144-167
39. Oesterhelt D, Stoeckenius W (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol 31:667-678
40. Park E, Rapoport TA (2012) Mechanisms of Sec61/SecY-mediated protein translocation across membranes. Annu Rev Biophys 41:21-40
41. Perlmutter JD, Drasler WJ, Xie W, Gao J, Popot J-L, Sachs JN (2011) All-atom and coarse-grained molecular dynamics simulations of a membrane protein stabilizing polymer. Langmuir 27:10523-10537
42. 2+-ATPase from sarcoplasmic reticulum: a comparative study. Biochemistry 45:1861-1869
43. Pocanschi CL, Dahmane T, Gohon Y, Rappaport F, Apell H-J, Kleinschmidt JH, Popot J-L (2006) Amphipathic polymers: tools to fold integral membrane proteins to their active form. Biochemistry 45:13954-13961
44. Popot J-L (2010) Amphipols, nanodiscs, and fluorinated surfactants: three non-conventional approaches to studying membrane proteins in aqueous solutions. Annu Rev Biochem 79:737-775
45. Popot J-L, Trewhella J, Engelman DM (1986) Reformation of crystalline purple membrane from purified bacteriorhodopsin fragments. EMBO J 5:3039-3044
46. Popot J-L, Gerchman S-E, Engelman DM (1987) Refolding of bacteriorhodopsin in lipid bilayers: a thermodynamically controlled two-stage process. J Mol Biol 198:655-676
47. Popot J-L, Althoff T, Bagnard D, Banères J-L, Bazzacco P, Billon-Denis E, Catoire LJ, Champeil P, Charvolin D, Cocco MJ, Crémel G, Dahmane T, de la Maza LM, Ebel C, Gabel F, Giusti F, Gohon Y, Goormaghtigh E, Guittet E, Kleinschmidt JH, Kühlbrandt W, Le Bon C, Martinez KL, Picard M, Pucci B, Rappaport F, Sachs JN, Tribet C, van Heijenoort C, Wien F, Zito F, Zoonens M (2011) Amphipols from A to Z. Annu Rev Biophys 40:379-408
48. Rehorek M, Heyn MP (1979) Binding of all-trans-retinal to the purple membrane. Evidence for cooperativity and determination of the extinction coefficient. Biochemistry 18:4977-4983
49. Riley ML, Wallace BA, Flitsch SL, Booth PJ (1997) Slow α-helix formation during folding of a membrane protein. Biochemistry 36:192-196
50. Sharma KS, Durand G, Gabel F, Bazzacco P, Le Bon C, Billon-Denis E, Catoire LJ, Popot J-L, Ebel C, Pucci B (2012) Non-ionic amphiphilic homopolymers: synthesis, solution properties, and biochemical validation. Langmuir 28:4625-4639
51. Sonar S, Patel N, Fischer W, Rothschild KJ (1993) Cell-free synthesis, functional refolding, and spectroscopic characterization of bacteriorhodopsin, an integral membrane protein. Biochemistry 32:13777-13781
52. Swords NA, Wallace BA (1993) Circular-dichroism of membrane proteins: examination of environmental effects on bacteriorhodopsin spectra. Biochem J 289:215-219
53. Tribet C, Audebert R, Popot J-L (1996) Amphipols: polymers that keep membrane proteins soluble in aqueous solutions. Proc Natl Acad Sci USA 93:15047-15050
54. Váró G (2000) Analogies between halorhodopsin and bacteriorhodopsin. Biochim Biophys Acta 1460:220-229
55. Váró G, Lanyi JK (1991) Thermodynamics and energy coupling in the bacteriorhodopsin photocycle. Biochemistry 30:5016-5022
56. White SH, von Heijne G (2008) How translocons select transmembrane helices. Annu Rev Biophys 37:23-42
57. Zoonens M, Catoire LJ, Giusti F, Popot J-L (2005) NMR study of a membrane protein in detergent-free aqueous solution. Proc Natl Acad Sci USA 102:8893-8898
58. Zoonens M, Giusti F, Zito F, Popot J-L (2007) Dynamics of membrane protein/amphipol association studied by Förster resonance energy transfer. Implications for in vitro studies of amphipol-stabilized membrane proteins. Biochemistry 46:10392-10404