Energetics of membrane protein folding

Annual Review of Biophysics

Volumn 43, Issue 1, 2014, Pages 233-255

  Fleming, Karen G ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Protein lipid interactions; Thermodynamics

Indexed keywords

BACTERIORHODOPSIN; DETERGENT; DIACYLGLYCEROL KINASE; GLYCOPHORIN A; LIPID; MEMBRANE PROTEIN; OMPLA PROTEIN; OMPW PROTEIN; PAGP PROTEIN; PERIPHERAL MYELIN PROTEIN 22; PROTEIN; UNCLASSIFIED DRUG; WATER;

ARTICLE; BETA SHEET; BILAYER MEMBRANE; CIRCULAR DICHROISM; DIMERIZATION; ENERGY TRANSFER; HUMAN; HYSTERESIS; MICELLE; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STABILITY; SOLUBILITY; THEORETICAL STUDY; TITRIMETRY;

PROTEIN-LIPID INTERACTIONS; THERMODYNAMICS;

BACTERIA; BACTERIAL PROTEINS; LIPID BILAYERS; MEMBRANE PROTEINS; PROTEIN FOLDING; THERMODYNAMICS;

EID: 84901986762     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-051013-022926     Document Type: Article

References (96)

1. Adamian L, Liang J. 2002. Interhelical hydrogen bonds and spatial motifs in membrane proteins: polar clamps and serine zippers. Proteins 47:209-188
2. Adamian L, Nanda V, DeGrado WF, Liang J. 2005. Empirical lipid propensities of amino acid residues in multispan alpha helical membrane proteins. Proteins 59:496-5099
3. Allen SJ, Kim JM, Khorana HG, Lu H, Booth PJ. 2001. Structure and function in bacteriorhodopsin: the effect of the interhelical loops on the protein folding kinetics. J. Mol. Biol. 308:423-355
4. Amici SA, Dunn WA Jr, Notterpek L. 2007. Developmental abnormalities in the nerves of peripheral myelin protein 22-deficient mice. J. Neurosci. Res. 85:238-499
5. Anfinsen CB. 1973. Principles that govern the folding of protein chains. Science 181:223-300
6. Bibi E. 1998. The role of the ribosome-translocon complex in translation and assembly of polytopic membrane proteins. Trends Biochem. Sci. 23:51-555
7. Booth PJ, Farooq A. 1997. Intermediates in the assembly of bacteriorhodopsin investigated by timeresolved absorption spectroscopy. Eur. J. Biochem. 246:674-800
8. Booth PJ, Farooq A, Flitsch SL. 1996. Retinal binding during folding and assembly of the membrane protein bacteriorhodopsin. Biochemistry 35:5902-99
9. Booth PJ, Flitsch SL, Stern LJ, Greenhalgh DA, Kim PS, KhoranaHG. 1995. Intermediates in the folding of the membrane protein bacteriorhodopsin. Nat. Struct. Biol. 2:139-433
10. Cao Z, Schlebach JP, Park C, Bowie JU. 2012. Thermodynamic stability of bacteriorhodopsin mutants measured relative to the bacterioopsin unfolded state. Biochim. Biophys. Acta 1818:1049-544
11. Chen GQ, Gouaux E. 1999. Probing the folding and unfolding of wild-type and mutant forms of bacteriorhodopsin in micellar solutions: evaluation of reversible unfolding conditions. Biochemistry 38:15380-877
12. Chothia C. 1974. Hydrophobic bonding and accessible surface area in proteins. Nature 248:338-399
13. Compton EL, Farmer NA, Lorch M, Mason JM, Moreton KM, Booth PJ. 2006. Kinetics of an individual transmembrane helix during bacteriorhodopsin folding. J. Mol. Biol. 357:325-388
14. Curnow P, Booth PJ. 2007. Combined kinetic and thermodynamic analysis of alpha-helical membrane protein unfolding. Proc. Natl. Acad. Sci. USA 104:18970-755
15. Curnow P, Di Bartolo ND, Moreton KM, Ajoje OO, Saggese NP, Booth PJ. 2011. Stable folding core in the folding transition state of an β-helical integral membrane protein. Proc. Natl. Acad. Sci. USA 108:14133-388
16. Curran AR, Templer RH, Booth PJ. 1999. Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer. Biochemistry 38:9328-366
17. Danoff EJ, Fleming KG. 2011. The soluble, periplasmic domain of OmpA folds as an independent unit and displays chaperone activity by reducing the self-association propensity of the unfolded OmpA transmembrane β-barrel. Biophys. Chem. 159:194-2044
18. Dorairaj S, Allen TW. 2007. On the thermodynamic stability of a charged arginine side chain in a transmembrane helix. Proc. Natl. Acad. Sci. USA 104:4943-488
19. Doura AK, Fleming KG. 2004. Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer. J. Mol. Biol. 343:1487-977
20. Doura AK, Kobus FJ, Dubrovsky L, Hibbard E, Fleming KG. 2004. Sequence context modulates the stability of a GxxxG-mediated transmembrane helix-helix dimer. J. Mol. Biol. 341:991-988
21. Ebie AZ, Fleming KG. 2007. Dimerization of the erythropoietin receptor transmembrane domain in micelles. J. Mol. Biol. 366:517-244
22. Ebie Tan A, Burgess NK, DeAndrade DS, Marold JD, Fleming KG. 2010. Self-association of unfolded outer membrane proteins. Macromol. Biosci. 10:763-677
23. Faham S, Yang D, Bare E, Yohannan S, Whitelegge JP, Bowie JU. 2004. Side-chain contributions to membrane protein structure and stability. J. Mol. Biol. 335:297-3055
24. Fisher LE, Engelman D, Sturgis J. 1999. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293:639-511
25. Fleming KG. 2002. Standardizing the free energy change of transmembrane helix-helix interactions. J. Mol. Biol. 323:563-711
26. Fleming KG, Ackerman AL, Engelman DM. 1997. The effect of point mutations on the free energy of transmembrane β-helix dimerization. J. Mol. Biol. 272:266-755
27. Fleming KG, Engelman DM. 2001. Specificity in transmembrane helix-helix interactions defines a hierarchy of stability for sequence variants. Proc. Natl. Acad. Sci. USA 98:14340-444
28. Fleming PJ, Freites JA, Moon CP, Tobias DJ, Fleming KG. 2012. Outer membrane phospholipase A in phospholipid bilayers: a model system for concerted computational and experimental investigations of amino acid side chain partitioning into lipid bilayers. Biochim. Biophys. Acta 1818:126-344
29. Gratkowski H, Lear JD, DeGradoWF. 2001. Polar side chains drive the association of model transmembrane peptides. Proc. Natl. Acad. Sci. USA 98:880-855
30. Gumbart J, Roux B. 2012. Determination of membrane-insertion free energies by molecular dynamics simulations. Biophys. J. 102:795-8011
31. Gumbart JC, Teo I, Roux B, Schulten K. 2013. Reconciling the roles of kinetic and thermodynamic factors in membrane-protein insertion. J. Am. Chem. Soc. 135:2291-977
32. Haltia T, Freire E. 1995. Forces and factors that contribute to the structural stability of membrane proteins. Biochim. Biophys. Acta 1241:295-3222
33. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, et al. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-811
34. Hessa T, Meindl-Beinker NM, Bernsel A, KimH, Sato Y, et al. 2007. Molecular code for transmembranehelix recognition by the Sec61 translocon. Nature 450:1026-300
35. Hong H, Blois TM, Cao Z, Bowie JU. 2010. Method to measure strong protein-protein interactions in lipid bilayers using a steric trap. Proc. Natl. Acad. Sci. USA 107:19802-77
36. Hong H, Bowie JU. 2011. Dramatic destabilization of transmembrane helix interactions by features of natural membrane environments. J. Am. Chem. Soc. 133:11389-988
37. Hong H, Park S, Jimnez RH, Rinehart D, Tamm LK. 2007. Role of aromatic side chains in the folding and thermodynamic stability of integral membrane proteins. J. Am. Chem. Soc. 129:8320-277
38. Hong H, Rinehart D, Tamm LK. 2013. Membrane depth-dependent energetic contribution of the tryptophan side chain to the stability of integral membrane proteins. Biochemistry 52:4413-211
39. Hong H, Szabo G, Tamm LK. 2006. Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening. Nat. Chem. Biol. 2:627-355
40. Hong H, Tamm LK. 2004. Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc. Natl. Acad. Sci. USA 101:4065-700
41. Howard KP, Lear JD, DeGrado WF. 2002. Sequence determinants of the energetics of folding of a transmembrane four-helix-bundle protein. Proc. Natl. Acad. Sci. USA 99:8568-722
42. 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. 256:3802-99
43. Hunt JF, Earnest TN, Bousch O, Kalghatgi K, Reilly K, et al. 1997. A biophysical study of integral membrane protein folding. Biochemistry 36:15156-766
44. Huysmans GHM, Baldwin SA, Brockwell DJ, Radford SE. 2010. The transition state for folding of an outer membrane protein. Proc. Natl. Acad. Sci. USA 107:4099-1044
45. Joh NH, Min A, Faham S, Whitelegge JP, Yang D, et al. 2008. Modest stabilization by most hydrogenbonded side-chain interactions in membrane proteins. Nature 453:1266-700
46. Joh NH, Oberai A, Yang D, Whitelegge JP, Bowie JU. 2009. Similar energetic contributions of packing in the core of membrane and water-soluble proteins. J. Am. Chem. Soc. 131:10846-477
47. Johnson AE, van Waes MA. 1999. The translocon: a dynamic gateway at the ER membrane. Annu. Rev. Cell Dev. Biol. 15:799-8422
48. Kahn TW, Engelman DM. 1992. Bacteriorhodopsin can be refolded from two independently stable transmembrane helices and the complementary five-helix fragment. Biochemistry 31:6144-511
49. Kim JM, Booth PJ, Allen SJ, Khorana HG. 2001. Structure and function in bacteriorhodopsin: the role of the interhelical loops in the folding and stability of bacteriorhodopsin. J. Mol. Biol. 308:409-222
50. Kobus FJ, Fleming KG. 2005. The GxxxG-containing transmembrane domain of the CCK4 oncogene does not encode preferential self-interactions. Biochemistry 44:1464-700
51. Kochendoerfer GG, Salom D, Lear JD, Wilk-Orescan R, Kent SB, DeGrado WF. 1999. Total chemical synthesis of the integral membrane protein influenza A virusM2: role of itsC-terminal domain in tetramer assembly. Biochemistry 38:11905-133
52. Lau FW, Bowie JU. 1997. A method for assessing the stability of a membrane protein. Biochemistry 36:5884-922
53. Li D, Lyons JA, Pye VE, Vogeley L, Arag?ao D, et al. 2013. Crystal structure of the integral membrane diacylglycerol kinase. Nature 497:521-244
54. Li E, YouM, HristovaK. 2006.FGFR3dimer stabilization due to a single amino acid pathogenicmutation. J. Mol. Biol. 356:600-122
55. Li R, Gorelik R, Nanda V, Law PB, Lear JD, et al. 2004. Dimerization of the transmembrane domain of integrin αIIb subunit in cell membranes. J. Biol. Chem. 279:26666-733
56. Lomize AL, Pogozheva ID, Lomize MA, Mosberg HI. 2006. Positioning of proteins in membranes: a computational approach. Protein Sci. 15:1318-333 (Pubitemid 43800004)
57. Lomize MA, Lomize AL, Pogozheva ID, Mosberg HI. 2006. OPM: Orientations of Proteins in Membranes database. Bioinformatics 22:623-255
58. London E, Khorana HG. 1982. Denaturation and renaturation of bacteriorhodopsin in detergents and lipid-detergent mixtures. J. Biol. Chem. 257:7003-111
59. Lu H, Marti T, Booth PJ. 2001. Proline residues in transmembrane helices affect the folding of bacteriorhodopsin. J. Mol. Biol. 308:437-466
60. Lüneberg J, Widmann M, Dathe M, Marti T. 1998. Secondary structure of bacteriorhodopsin fragments: External sequence constraints specify the conformation of transmembrane helices. J. Biol. Chem. 273:28822-300
61. MacCallum JL, Bennett WF, Tieleman DP. 2008. Distribution of amino acids in a lipid bilayer from computer simulations. Biophys. J. 94:3393-4044
62. MacRaild CA, Hatters DM, Howlett GJ, Gooley PR. 2001. NMR structure of human apolipoprotein C-II in the presence of sodium dodecyl sulfate. Biochemistry 40:5414-211
63. Mobley CK, Myers JK, Hadziselimovic A, Ellis CD, Sanders CR. 2007. Purification and initiation of structural characterization of human peripheral myelin protein 22, an integral membrane protein linked to peripheral neuropathies. Biochemistry 46:11185-955
64. Montserret R, McLeish MJ, Bockmann A, Geourjon C, Penin F. 2000. Involvement of electrostatic interactions in the mechanism of peptide folding induced by sodium dodecyl sulfate binding. Biochemistry 39:8362-733
65. Moon CP, Fleming KG. 2011. Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc. Natl. Acad. Sci. USA 108:10174-777
66. Moon CP, Kwon S, Fleming KG. 2011. Overcoming hysteresis to attain reversible equilibrium folding for outer membrane phospholipase A in phospholipid bilayers. J. Mol. Biol. 413:484-944
67. Moon CP, Zaccai NR, Fleming PJ, Gessman D, Fleming KG. 2013. Membrane protein stability may be the energy sink for sorting in the periplasm. Proc. Natl. Acad. Sci. USA 12:4285-900
68. Myers JK, Mobley CK, Sanders CR. 2008. The peripheral neuropathy-linked Trembler and Trembler-J mutant forms of peripheral myelin protein 22 are folding-destabilized. Biochemistry 47:10620-299
69. Myers JK, Pace CN, Scholtz JM. 1995. Denaturantmvalues and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4:2138-488
70. Pace CN. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131:266-800
71. Pareek S, Suter U, Snipes GJ, Welcher AA, Shooter EM, Murphy RA. 1993. Detection and processing of peripheral myelin protein PMP22 in cultured Schwann cells. J. Biol. Chem. 268:10372-799
72. Pocanschi CL, Patel GJ, Marsh D, Kleinschmidt JH. 2006. Curvature elasticity and refolding of OmpA in large unilamellar vesicles. Biophys. J. 91:L75-777
73. Pogozheva ID, Tristram-Nagle S, Mosberg HI, Lomize AL. 2013. Structural adaptations of proteins to different biological membranes. Biochim. Biophys. Acta 1828:2592-6088
74. Popot JL, Engelman DM. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031-377
75. Renthal R. 2006. An unfolding story of helical transmembrane proteins. Biochemistry 45:14559-666
76. Renthal R,Haas P. 1996. Effect of transmembrane helix packing on tryptophan and tyrosine environments in detergent-solubilized bacterio-opsin. J. Protein Chem. 15:281-899
77. Rozek A, Buchko GW, Cushley RJ. 1995. Conformation of two peptides corresponding to human apolipoprotein C-I residues 7-24 and 35-53 in the presence of sodium dodecyl sulfate by CD and NMR spectroscopy. Biochemistry 34:7401-88
78. Sakakura M, Hadziselimovic A, Wang Z, ScheyKL, SandersCR. 2011. Structural basis for theTrembler-J phenotype of Charcot-Marie-Tooth disease. Structure 19:1160-699
79. Sanchez KM, Gable JE, Schlamadinger DE, Kim JE. 2008. Effects of tryptophan microenvironment, soluble domain, and vesicle size on the thermodynamics of membrane protein folding: lessons from the transmembrane protein OmpA. Biochemistry 47:12844-522
80. Sanders CR, Myers JK. 2004. Disease-related misassembly of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 33:25-511
81. Santoro MM, Bolen DW. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 27:8063-688
82. Santoro MM, Bolen DW. 1992. A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range. Biochemistry 31:4901-77
83. Schlebach JP,Cao Z, Bowie JU, Park C. 2012. Revisiting the folding kinetics of bacteriorhodopsin. Protein Sci. 21:97-1066
84. Stanley AM, Fleming KG. 2005. The transmembrane domains of the ErbB receptors do not dimerize strongly in micelles. J. Mol. Biol. 347:759-722
85. Stanley AM, Fleming KG. 2007. The role of a hydrogen bonding network in the transmembrane β-barrel OMPLA. J. Mol. Biol. 370:912-244
86. Stanley AM, FlemingKG. 2008. The process of folding proteins intomembranes: progress and challenges. Arch. Biochem. Biophys. 469:46-666
87. Storjohann R, Rozek A, Sparrow JT, Cushley RJ. 2000. Structure of a biologically active fragment of human serum apolipoprotein C-II in the presence of sodium dodecyl sulfate and dodecylphosphocholine. Biochim. Biophys. Acta 1486:253-644
88. Ulmschneider MB, SansomMS. 2001. Amino acid distributions in integral membrane protein structures. Biochim. Biophys. Acta 1512:1-144
89. Van Horn WD, Kim H-J, Ellis CD,Hadziselimovic A, Sulistijo ES, et al. 2009. Solution nuclear magnetic resonance structure of membrane-integral diacylglycerol kinase. Science 324:1726-299
90. Wang G, Treleaven WD, Cushley RJ. 1996. Conformation of human serum apolipoprotein A-I(166-185) in the presence of sodium dodecyl sulfate or dodecylphosphocholine by 1H-NMR and CD. Evidence for specific peptide-SDS interactions. Biochim. Biophys. Acta 1301:174-844
91. White SH, von Heijne G. 2004. The machinery of membrane protein assembly. Curr. Opin. Struct. Biol. 14:397-4044
92. White SH, von Heijne G. 2008. How translocons select transmembrane helices. Annu. Rev. Biophys. 37:23-422
93. White SH, Wimley WC. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-655
94. Wimley WC, Creamer TP, White SH. 1996. Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 35:5109-244
95. WimleyWC,White SH. 1996. Experimentally determined hydrophobicity scale for proteins atmembrane interfaces. Nat. Struct. Biol. 3:842-488
96. Yohannan S, Faham S, Yang D, Whitelegge JP, Bowie JU. 2004. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 101:959-633