Protein structure in membrane domains

Annual Review of Biophysics

Volumn 41, Issue 1, 2012, Pages 135-155

  Rath, Arianna ^a   Deber, Charles M ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Detergent; Folding; Helix helix interactions; Hydrophobicity; Stability; Transmembrane protein

Indexed keywords

MEMBRANE PROTEIN;

HUMAN; HYDROGEN BOND; HYDROPHOBICITY; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS;

ANIMALS; CELL MEMBRANE; HUMANS; LIPID BILAYERS; MEMBRANE PROTEINS; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84861417683     PISSN: 1936122X     EISSN: 19361238     Source Type: Book Series    
DOI: 10.1146/annurev-biophys-050511-102310     Document Type: Review

References (87)

1. Anbazhagan V, Cymer F, Schneider D. 2010. Unfolding a transmembrane helix dimer: a FRET study in mixed micelles. Arch. Biochem. Biophys. 495:159-64
2. Anbazhagan V, Munz C, Tome L, Schneider D. 2010. Fluidizing the membrane by a local anesthetic: phenylethanol affects membrane protein oligomerization. J. Mol. Biol. 404:773-77
3. Anbazhagan V, Schneider D. 2010. The membrane environment modulates self-association of the human GpA TM domain\implications for membrane protein folding and transmembrane signaling. Biochim. Biophys. Acta 1798:1899-907
4. Bordag N, Keller S. 2010. α-Helical transmembrane peptides: a "divide and conquer" approach to membrane proteins. Chem. Phys. Lipids 163:1-26
5. Bowie JU. 1997. Helix packing in membrane proteins. J. Mol. Biol. 272:780-89
6. Brunger AT. 2007. Version 1.2 of the crystallography and NMR system. Nat. Prot. 2:2728-33
7. Chen L, Novicky L, Merzlyakov M, Hristov T, Hristova K. 2010. Measuring the energetics of membrane protein dimerization in mammalian membranes. J. Am. Chem. Soc. 132:3628-35
8. Cunningham F, Poulsen BE, Ip W, Deber CM. 2010. Beta-branched residues adjacent to GG4 motifs promote the efficient association of glycophorin A transmembrane helices. Biopolymers 96:340-47
9. Cunningham F, Rath A, Johnson RM, Deber CM. 2009. Distinctions between hydrophobic helices in globular proteins and transmembrane segments as factors in protein sorting. J. Biol. Chem. 284:5395-402
10. Deber CM, Wang C, Liu LP, Prior AS, Agrawal S, et al. 2001. TM Finder: a prediction program for transmembrane protein segments using a combination of hydrophobicity and nonpolar phase helicity scales. Protein Sci. 10:212-19
11. Dorairaj S, Allen TW. 2007. On the thermodynamic stability of a charged arginine side chain in a transmembrane helix. Proc. Natl. Acad. Sci. USA 104:4943-48
12. Duong MT, Jaszewski TM, Fleming KG, MacKenzie KR. 2007. Changes in apparent free energy of helix-helix dimerization in a biological membrane due to point mutations. J. Mol. Biol. 371:422-34
13. Eilers M, Patel AB, Liu W, Smith SO. 2002. Comparison of helix interactions in membrane and soluble alpha-bundle proteins. Biophys. J. 82:2720-36
14. Engelman DM, Chen Y, Chin CN, Curran AR, Dixon AM, et al. 2003.Membraneprotein folding: beyond the two stage model. FEBS Lett. 555:122-25
15. Enquist K, Fransson M, Boekel C, Bengtsson I, Geiger K, et al. 2009. Membrane-integration characteristics of two ABC transporters, CFTR and P-glycoprotein. J. Mol. Biol. 387:1153-64
16. Fiedler S, Broecker J, Keller S. 2010. Protein folding in membranes. Cell Mol. Life Sci. 67:1779-98
17. Fisher LE, Engelman DM, Sturgis JN. 1999. Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 293:639-51
18. Fisher LE, Engelman DM, Sturgis JN. 2003. Effect of detergents on the association of the glycophorin A transmembrane helix. Biophys. J. 85:3097-105
19. Fleming KG. 2002. Standardizing the free energy change of transmembrane helix-helix interactions. J. Mol. Biol. 323:563-71
20. Fleming KG, Engelman DM. 2001. Specificity in transmembrane helix-helix interactions can define a hierarchy of stability for sequence variants. Proc. Natl. Acad. Sci. USA 98:14340-44
21. Fleming KG, Ren CC, Doura AK, Eisley ME, Kobus FJ, Stanley AM. 2004. Thermodynamics of gly-cophorin A transmembrane helix dimerization in C14 betaine micelles. Biophys. Chem. 108:43-49
22. Gimpelev M, Forrest LR, Murray D, Honig B. 2004. Helical packing patterns in membrane and soluble proteins. Biophys. J. 87:4075-86
23. Granseth E, von Heijne G, Elofsson A. 2005. A study of the membrane-water interface region of membrane proteins. J. Mol. Biol. 346:377-85
24. Gumbart J, Chipot C, Schulten K. 2011. Free-energy cost for translocon-assisted insertion of membrane proteins. Proc. Natl. Acad. Sci. USA 108:3596-601
25. Hedin LE, Ojemalm K, Bernsel A, Hennerdal A, Illergard K, et al. 2010. Membrane insertionof marginally hydrophobic transmembrane helices depends on sequence context. J. Mol. Biol. 396:221-29
26. Henin J, Pohorille A, Chipot C. 2005. Insights into the recognition and association of transmembrane α-helices. The free energy of alpha-helix dimerization in glycophorin A. J. Am. Chem. Soc. 127:8478-84
27. Hessa T, Kim H, Bihlmaier K, Lundin C, Boekel J, et al. 2005. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-81
28. Hessa T, Meindl-Beinker NM, Bernsel A, Kim H, Sato Y, et al. 2007. Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450:1026-30
29. 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 107:19802-7
30. Hong H, Bowie JU. 2011. Dramatic destabilization of transmembrane helix interactions by features of natural membrane environments. J. Am. Chem. Soc. 133:11389-98
31. Hong H, Joh NH, Bowie JU, Tamm LK. 2009. Methods for measuring the thermodynamic stability of membrane proteins. Methods Enzymol. 455:213-36
32. Jacobs RE, White SH. 1989. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry 28:3421-37
33. Janosi L, Prakash A, Doxastakis M. 2010. Lipid-modulated sequence-specific association of glycophorin A in membranes. Biophys. J. 99:284-92
34. Jaud S, Fernandez-Vidal M, Nilsson I, Meindl-Beinker NM, Hubner NC, et al. 2009. Insertion of short transmembrane helices by the Sec61 translocon. Proc. Natl. Acad. Sci. USA 106:11588-93
35. Johansson AC, Lindahl E. 2009. Protein contents in biological membranes can explain abnormal solvation of charged and polar residues. Proc. Natl. Acad. Sci. USA 106:15684-89
36. Johansson AC, Lindahl E. 2009. The role of lipid composition for insertion and stabilization of amino acids in membranes. J. Chem. Phys. 130:185101
37. Johansson AC, Lindahl E. 2009. Titratable amino acid solvation in lipid membranes as a function of protonation state. J. Phys. Chem. B 113:245-53
38. Johnson RM, Rath A, Melnyk RA, Deber CM. 2006. Lipid solvation effects contribute to the affinity of Gly-xxx-Gly motif-mediated helix-helix interactions. Biochemistry 45:8507-15
39. Kauko A, Illergard K, Elofsson A. 2008. Coils in the membrane core are conserved and functionally important. J. Mol. Biol. 380:170-80
40. Kim S, Cross TA. 2002. Uniformity, ideality, and hydrogen bonds in transmembrane alpha-helices. Biophys. J. 83:2084-95
41. Klein-Seetharaman J. 2005. Dual role of interactions between membranous and soluble portions of helical membrane receptors for folding and signaling. Trends Pharmacol. Sci. 26:183-89
42. Koehler J, Woetzel N, Staritzbichler R, Sanders CR, Meiler J. 2009. A unified hydrophobicity scale for multispan membrane proteins. Proteins 76:13-29
43. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-80
44. Langosch D, Brosig B, Kolmar H, Fritz HJ. 1996. Dimerisation of the glycophorin A transmem-brane segment in membranes probed with the ToxR transcription activator. J. Mol. Biol. 263: 525-30
45. Lemmon MA, Flanagan JM, Hunt JF, Adair BD, Bormann BJ, et al. 1992. Glycophorin A dimer-ization is driven by specific interactions between transmembrane alpha-helices. J. Biol. Chem. 267: 7683-89
46. Lemmon MA, Flanagan JM, Treutlein HR, Zhang J, Engelman DM. 1992. Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry 31:12719-25
47. Liu LP, Deber CM. 1998. Guidelines for membrane protein engineering derived from de novo designed model peptides. Biopolymers 47:41-62
48. Lomize MA, Lomize AL, Pogozheva ID, Mosberg HI. 2006. OPM: orientations of proteins in membranes database. Bioinformatics 22:623-25
49. MacCallum JL, Bennett WF, Tieleman DP. 2008. Distribution of amino acids in a lipid bilayer from computer simulations. Biophys. J. 94:3393-404
50. MacCallum JL, Tieleman DP. 2011. Hydrophobicity scales: a thermodynamic looking glass into lipid-protein interactions. Trends Biochem. Sci. 36:653-62
51. MacKenzie KR, Prestegard JH, Engelman DM. 1997. A transmembrane helix dimer: structure and implications. Science 276:131-33
52. Mant CT, Kovacs JM, Kim HM, Pollock DD, Hodges RS. 2009. Intrinsic amino acid side-chain hy-drophilicity/hydrophobicity coefficients determined by reversed-phase high-performance liquid chro-matography of model peptides: comparison with other hydrophilicity/hydrophobicity scales. Biopolymers 92:573-95
53. Mineev KS, Khabibullina NF, Lyukmanova EN, Dolgikh DA, Kirpichnikov MP, Arseniev AS. 2011. Spatial structure and dimer-monomer equilibrium of the ErbB3 transmembrane domain in DPC micelles. Biochim. Biophys. Acta 1808:2081-88
54. Moon CP, Fleming KG. 2011. Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc. Natl. Acad. Sci. USA 108:10174-77
55. Mulvihill CM, Deber CM. 2010. Evidence that the translocon may function as a hydropathy partitioning filter. Biochim. Biophys. Acta 1798:1995-98
56. Norholm MH, Cunningham F, Deber CM, von Heijne G. 2011. Converting a marginally hydrophobic soluble protein into a membrane protein. J. Mol. Biol. 407:171-79
57. Oberai A, Ihm Y, Kim S, Bowie JU. 2006. A limited universe of membrane protein families and folds. Protein Sci. 15:1723-34
58. Ojemalm K, Higuchi T, Jiang Y, Langel U, Nilsson I, et al. 2011. Apolar surface area determines the efficiency of translocon-mediated membrane-protein integration into the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 108:E359-64
59. Page RC, Kim S, Cross TA. 2008. Transmembrane helix uniformity examined by spectral mapping of torsion angles. Structure 16:787-97
60. Patel H, Raval G, Nazari M, Heerklotz H. 2010. Effects of glycerol and urea on micellization, membrane partitioning and solubilization by a non-ionic surfactant. Biophys. Chem. 150:119-28
61. Popot JL, Engelman DM. 1990. Membrane protein folding and oligomerization: the two-stage model. Biochemistry 29:4031-37
62. Punta M, Maritan A. 2003. A knowledge-based scale for amino acid membrane propensity. Proteins 50:114-21
63. Rath A, Deber CM. 2008. Surface recognition elements of membrane protein oligomerization. Proteins 70:786-93
64. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM. 2009. Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc. Natl. Acad. Sci. USA 106:1760-65
65. Rath A, Tulumello DV, Deber CM. 2009. Peptide models of membrane protein folding. Biochemistry 48:3036-45
66. Renthal R. 2006. An unfolding story of helical transmembrane proteins. Biochemistry 45:14559-66
67. Russ WP, Engelman DM. 1999. TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. USA 96:863-68
68. Schow EV, Freites JA, Cheng P, Bernsel A, von Heijne G, et al. 2011. Arginine in membranes: the connection between molecular dynamics simulations and translocon-mediated insertion experiments. J. Membr. Biol. 239:35-48
69. Senes A, Chadi DC, Law PB, Walters RF, Nanda V, Degrado WF. 2007. E(z), a depth-dependent potential for assessing the energies of insertion of amino acid side-chains into membranes: derivation and applications to determining the orientation of transmembrane and interfacial helices. J. Mol. Biol. 366:436-48
70. Sengupta D, Marrink SJ. 2010. Lipid-mediated interactions tune the association of glycophorin A helix and its disruptive mutants in membranes. Phys. Chem. Chem. Phys. 12:12987-96
71. Sereda TJ, Mant CT, Sonnichsen FD, Hodges RS. 1994. Reversed-phase chromatography of synthetic amphipathic alpha-helical peptides as a model for ligand/receptor interactions. Effect of changing hy-drophobic environment on the relative hydrophilicity/hydrophobicity of amino acid side-chains. J. Chro-matogr. A 676:139-53
72. Singer SJ. 2004. Some early history of membrane molecular biology. Annu. Rev. Physiol. 66:1-27
73. Skach WR. 2009. Cellular mechanisms of membrane protein folding. Nat. Struct. Mol. Biol. 16:606-12
74. Smith SO, Song D, Shekar S, Groesbeek M, Ziliox M, Aimoto S. 2001. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 40:6553-58
75. Stevens TJ, Mizuguchi K, Arkin IT. 2004. Distinct protein interfaces in transmembrane domains suggest an in vivo folding model. Protein Sci. 13:3028-37
76. Tulumello DV, Deber CM. 2009. SDS micelles as a membrane-mimetic environment for transmembrane segments. Biochemistry 48:12096-103
77. Tulumello DV, Deber CM. 2011.Positionsofpolar amino acids alter interactions betweentransmembrane segments and detergents. Biochemistry 50:3928-35
78. Ulmschneider MB, Sansom MS, Di Nola A. 2005. Properties of integral membrane protein structures: derivation of an implicit membrane potential. Proteins 59:252-65
79. Walters RF, DeGrado WF. 2006. Helix-packing motifs in membrane proteins. Proc. Natl. Acad. Sci. USA 103:13658-63
80. White SH, Ladokhin AS, Jayasinghe S, Hristova K. 2001. How membranes shape protein structure. J. Biol. Chem. 276:32395-98
81. White SH, von Heijne G. 2008. How translocons select transmembrane helices. Annu. Rev. Biophys. 37:23-42
82. White SH, Wimley WC. 1999. Membrane protein folding and stability: physical principles. Annu. Rev. Biophys. Biomol. Struct. 28:319-65
83. Wiener MC, White SH. 1992. Structure of a fluid dioleoylphosphatidylcholine bilayer determined by joint refinement of X-ray and neutron diffraction data. III. Complete structure. Biophys. J. 61:434-47
84. Wimley WC, Creamer TP, White SH. 1996. Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 35:5109-24
85. Wimley WC, Gawrisch K, Creamer TP, White SH. 1996. Direct measurement of salt-bridge solva-tion energies using a peptide model system: implications for protein stability. Proc. Natl. Acad. Sci. USA 93:2985-90
86. Wimley WC, White SH. 1996. Experimentally determined hydrophobicity scale for proteinsatmembrane interfaces. Nat. Struct. Biol. 3:842-48
87. Zhao G, London E. 2006. An amino acid "transmembrane tendency" scale that approaches the theoretical limit to accuracy for prediction of transmembrane helices: relationship to biological hydrophobicity. Protein Sci. 15:1987-2001