Transmembrane helix-helix interactions are modulated by the sequence context and by lipid bilayer properties

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 963-973

  Cymer, Florian ^a   Veerappan, Anbazhagan ^a   Schneider, Dirk ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

GxxxG; Helix dimer; Hydrogen bond; Hydrophobic thickness; Lateral pressure; Membrane protein

Indexed keywords

DETERGENT; EPHRIN A1; EPHRIN A2; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; MEMBRANE PROTEIN; PROTEIN BNIP3; SYNAPTOBREVIN 2; SYNTAXIN 1A;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DIMERIZATION; HYDROGEN BOND; HYDROPHOBICITY; LIPID BILAYER; LIPID COMPOSITION; MICELLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; THERMODYNAMICS;

AMINO ACID SEQUENCE; LIPID BILAYERS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84857529575     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.07.035     Document Type: Article

References (98)

1. J.L. Popot, and D.M. Engelman Membrane protein folding and oligomerization: the two-stage model Biochemistry 29 1990 4031 4037
2. D.M. Engelman, Y. Chen, C.N. Chin, A.R. Curran, A.M. Dixon, A.D. Dupuy, A.S. Lee, U. Lehnert, E.E. Matthews, Y.K. Reshetnyak, A. Senes, and J.L. Popot Membrane protein folding: beyond the two stage model FEBS Lett. 555 2003 122 125
3. D. Schneider Rendezvous in a membrane: close packing, hydrogen bonding, and the formation of transmembrane helix oligomers FEBS Lett. 577 2004 5 8
4. S.E. Harrington, and N. Ben-Tal Structural determinants of transmembrane helical proteins Structure 17 2009 1092 1103
5. J.U. Bowie Solving the membrane protein folding problem Nature 438 2005 581 589
6. W.F. DeGrado, H. Gratkowski, and J.D. Lear How do helix-helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo-oligomeric helical bundles Protein Sci. 12 2003 647 665
7. B.J. Bormann, and D.M. Engelman Intramembrane helix-helix association in oligomerization and transmembrane signaling Annu. Rev. Biophys. Biomol. Struct. 21 1992 223 242
8. D.T. Moore, B.W. Berger, and W.F. DeGrado Protein-protein interactions in the membrane: sequence, structural, and biological motifs Structure 16 2008 991 1001
9. S.H. White, and W.C. Wimley Membrane protein folding and stability: physical principles Annu. Rev. Biophys. Biomol. Struct. 28 1999 319 365
10. N. Ben-Tal, A. Ben-Shaul, A. Nicholls, and B. Honig Free-energy determinants of alpha-helix insertion into lipid bilayers Biophys. J. 70 1996 1803 1812
11. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133
12. B.J. Bormann, W.J. Knowles, and V.T. Marchesi Synthetic peptides mimic the assembly of transmembrane glycoproteins J. Biol. Chem. 264 1989 4033 4037
13. M.A. Lemmon, J.M. Flanagan, H.R. Treutlein, J. Zhang, and D.M. Engelman Sequence specificity in the dimerization of transmembrane alpha-helices Biochemistry 31 1992 12719 12725
14. H.R. Treutlein, M.A. Lemmon, D.M. Engelman, and A.T. Brunger The glycophorin A transmembrane domain dimer: sequence-specific propensity for a right-handed supercoil of helices Biochemistry 31 1992 12726 12732
15. D. Langosch, and J. Heringa Interaction of transmembrane helices by a knobs-into-holes packing characteristic of soluble coiled coils Proteins 31 1998 150 159
16. A. Senes, I. Ubarretxena-Belandia, and D.M. Engelman The Calpha - H.O hydrogen bond: a determinant of stability and specificity in transmembrane helix interactions Proc. Natl. Acad. Sci. U.S.A. 98 2001 9056 9061
17. E. Arbely, and I.T. Arkin Experimental measurement of the strength of a C alpha-H.O bond in a lipid bilayer J. Am. Chem. Soc. 126 2004 5362 5363
18. A.R. Curran, and D.M. Engelman Sequence motifs, polar interactions and conformational changes in helical membrane proteins Curr. Opin. Struct. Biol. 13 2003 412 417
19. A. Senes, D.E. Engel, and W.F. DeGrado Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs Curr. Opin. Struct. Biol. 14 2004 465 479
20. A. Senes, M. Gerstein, and D.M. Engelman Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with beta-branched residues at neighboring positions J. Mol. Biol. 296 2000 921 936
21. W.P. Russ, and D.M. Engelman The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296 2000 911 919
22. D. Schneider, and D.M. Engelman Motifs of two small residues can assist but are not sufficient to mediate transmembrane helix interactions J. Mol. Biol. 343 2004 799 804
23. A.K. Doura, F.J. Kobus, L. Dubrovsky, E. Hibbard, and K.G. Fleming Sequence context modulates the stability of a GxxxG-mediated transmembrane helix-helix dimer J. Mol. Biol. 341 2004 991 998
24. R.A. Melnyk, S. Kim, A.R. Curran, D.M. Engelman, J.U. Bowie, and C.M. Deber The affinity of GXXXG motifs in transmembrane helix-helix interactions is modulated by long-range communication J. Biol. Chem. 279 2004 16591 16597
25. S.O. Smith, D. Song, S. Shekar, M. Groesbeek, M. Ziliox, and S. Aimoto Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers Biochemistry 40 2001 6553 6558
26. S.O. Smith, R. Jonas, M. Braiman, and B.J. Bormann Structure and orientation of the transmembrane domain of glycophorin A in lipid bilayers Biochemistry 33 1994 6334 6341
27. S.O. Smith, M. Eilers, D. Song, E. Crocker, W. Ying, M. Groesbeek, G. Metz, M. Ziliox, and S. Aimoto Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer Biophys. J. 82 2002 2476 2486
28. C. Finger, T. Volkmer, A. Prodöhl, D.E. Otzen, D.M. Engelman, and D. Schneider The stability of transmembrane helix interactions measured in a biological membrane J. Mol. Biol. 358 2006 1221 1228
29. D. Langosch, B. Brosig, H. Kolmar, and H.J. Fritz Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator J. Mol. Biol. 263 1996 525 530
30. A.K. Doura, and K.G. Fleming Complex interactions at the helix-helix interface stabilize the glycophorin a transmembrane dimer J. Mol. Biol. 343 2004 1487 1497
31. B.A. Lewis, and D.M. Engelman Lipid bilayer thickness varies linearly with acyl chain length in fluid phosphatidylcholine vesicles J. Mol. Biol. 166 1983 211 217
32. H.I. Petrache, A. Grossfield, K.R. MacKenzie, D.M. Engelman, and T.B. Woolf Modulation of glycophorin A transmembrane helix interactions by lipid bilayers: molecular dynamics calculations J. Mol. Biol. 302 2000 727 746
33. J. Henin, A. Pohorille, and C. Chipot Insights into the recognition and association of transmembrane alpha-helices. The free energy of alpha-helix dimerization in glycophorin A J. Am. Chem. Soc. 127 2005 8478 8484
34. F. Cymer, and D. Schneider Transmembrane helix-helix interactions involved in ErbB receptor signaling Cell Adh. Migr. 4 2010 299 312
35. B.-H. Luo, and T.A. Springer Integrin structures and conformational signaling Curr. Opin. Cell Biol. 18 2006 579 586 (Cell-to-cell contact and extracellular matrix)
36. D. Schneider, and D.M. Engelman Involvement of transmembrane domain interactions in signal transduction by a/b integrins J. Biol. Chem. 279 2004 9840 9846
37. C. Escher, F. Cymer, and D. Schneider Two GxxxG-like motifs facilitate promiscuous interactions of the human ErbB transmembrane domains J. Mol. Biol. 389 2009 10 16
38. J.M. Mendrola, M.B. Berger, M.C. King, and M.A. Lemmon The single transmembrane domains of ErbB receptors self-associate in cell membranes J. Biol. Chem. 277 2002 4704 4712
39. S.J. Fleishman, J. Schlessinger, and N. Ben-Tal A putative molecular-activation switch in the transmembrane domain of erbB2 Proc. Natl. Acad. Sci. U.S.A. 99 2002 15937 15940
40. E.V. Bocharov, K.S. Mineev, P.E. Volynsky, Y.S. Ermolyuk, E.N. Tkach, A.G. Sobol, V.V. Chupin, M.P. Kirpichnikov, R.G. Efremov, and A.S. Arseniev Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state J. Biol. Chem. 283 2008 6950 6956
41. K.S. Mineev, E.V. Bocharov, Y.E. Pustovalova, O.V. Bocharova, V.V. Chupin, and A.S. Arseniev Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases J. Mol. Biol. 400 2010 231 243
42. R. Li, R. Gorelik, V. Nanda, P.B. Law, J.D. Lear, W.F. DeGrado, and J.S. Bennett Dimerization of the transmembrane domain of integrin alphaIIb subunit in cell membranes J. Biol. Chem. 279 2004 26666 26673
43. T.L. Lau, C. Kim, M.H. Ginsberg, and T.S. Ulmer The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling EMBO J. 28 2009 1351 1361
44. J. Yang, Y.-Q. Ma, R.C. Page, S. Misra, E.F. Plow, and J. Qin Structure of an integrin alpha IIb beta3 transmembrane-cytoplasmic heterocomplex provides insight into integrin activation Proc. Natl. Acad. Sci. 106 2009 17729 17734
45. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, A.A. Schulga, E.O. Artemenko, R.G. Efremov, and A.S. Arseniev Spatial structure and pH-dependent conformational diversity of dimeric transmembrane domain of the receptor tyrosine kinase EphA1 J. Biol. Chem. 283 2008 29385 29395
46. E.V. Bocharov, Y.E. Pustovalova, K.V. Pavlov, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, D.V. Karpunin, A.A. Schulga, M.P. Kirpichnikov, R.G. Efremov, I.V. Maslennikov, and A.S. Arseniev Unique dimeric structure of BNip3 transmembrane domain suggests membrane permeabilization as a cell death trigger J. Biol. Chem. 282 2007 16256 16266
47. E.S. Sulistijo, and K.R. Mackenzie Structural basis for dimerization of the BNIP3 transmembrane domain Biochemistry 48 2009 5106 5120
48. K.S. Mineev, N.F. Khabibullina, E.N. Lyukmanova, D.A. Dolgikh, M.P. Kirpichnikov, and A.S. Arseniev Spatial structure and dimer-monomer equilibrium of the ErbB3 transmembrane domain in DPC micelles Biochim. Biophys. Acta 1808 2011 2081 2088
49. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, K.S. Mineev, E.N. Tkach, Y.S. Ermolyuk, A.A. Schulga, R.G. Efremov, and A.S. Arseniev Left-handed dimer of EphA2 transmembrane domain: helix packing diversity among receptor tyrosine kinases Biophys. J. 98 2010 881 889
50. M.E. Call, J.R. Schnell, C. Xu, R.A. Lutz, J.J. Chou, and K.W. Wucherpfennig The structure of the zetazeta transmembrane dimer reveals features essential for its assembly with the T cell receptor Cell 127 2006 355 368
51. M.E. Call, K.W. Wucherpfennig, and J.J. Chou The structural basis for intramembrane assembly of an activating immunoreceptor complex Nat. Immunol. 11 2010 1023 1029
52. A. Stein, G. Weber, M.C. Wahl, and R. Jahn Helical extension of the neuronal SNARE complex into the membrane Nature 460 2009 525 528
53. M.J. Sternberg, and W.J. Gullick A sequence motif in the transmembrane region of growth factor receptors with tyrosine kinase activity mediates dimerization Protein Eng. 3 1990 245 248
54. M. Weber, A. Prodohl, C. Dreher, C. Becker, J. Underhaug, A.S. Svane, A. Malmendal, N.C. Nielsen, D. Otzen, and D. Schneider SDS-facilitated in vitro formation of a transmembrane B-type cytochrome is mediated by changes in local pH J. Mol. Biol. 407 2011 594 606
55. V. Anbazhagan, F. Cymer, and D. Schneider Unfolding a transmembrane helix dimer: a FRET study in mixed micelles Arch. Biochem. Biophys. 495 2010 159 164
56. M. Orzaez, E. Perez-Paya, and I. Mingarro Influence of the C-terminus of the glycophorin A transmembrane fragment on the dimerization process Protein Sci. 9 2000 1246 1253
57. M. Orzaez, D. Lukovic, C. Abad, E. Perez-Paya, and I. Mingarro Influence of hydrophobic matching on association of model transmembrane fragments containing a minimised glycophorin A dimerisation motif FEBS Lett. 579 2005 1633 1638
58. A.G. Therien, and C.M. Deber Interhelical packing in detergent micelles. Folding of a cystic fibrosis transmembrane conductance regulator construct J. Biol. Chem. 277 2002 6067 6072
59. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain J. Mol. Biol. 293 1999 639 651
60. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Effect of detergents on the association of the glycophorin a transmembrane helix Biophys. J. 85 2003 3097 3105
61. L. Chen, L. Novicky, M. Merzlyakov, T. Hristov, and K. Hristova Measuring the energetics of membrane protein dimerization in mammalian membranes J. Am. Chem. Soc. 132 2010 3628 3635
62. V. Anbazhagan, and D. Schneider The membrane environment modulates self-association of the human GpA TM domain-implications for membrane protein folding and transmembrane signaling Biochim. Biophys. Acta 1798 2010 1899 1907
63. A. Holt, and J. Killian Orientation and dynamics of transmembrane peptides: the power of simple models Eur. Biophys. J. 39 2010 609 621
64. J. Ren, S. Lew, J. Wang, and E. London Control of the transmembrane orientation and interhelical interactions within membranes by hydrophobic helix length Biochemistry 38 1999 5905 5912
65. E. Sparr, W.L. Ash, P.V. Nazarov, D.T. Rijkers, M.A. Hemminga, D.P. Tieleman, and J.A. Killian Self-association of transmembrane alpha-helices in model membranes: importance of helix orientation and role of hydrophobic mismatch J. Biol. Chem. 280 2005 39324 39331
66. L. Cristian, J.D. Lear, and W.F. DeGrado Use of thiol-disulfide equilibria to measure the energetics of assembly of transmembrane helices in phospholipid bilayers Proc. Natl. Acad. Sci. U.S.A. 100 2003 14772 14777
67. K.C. Duong-Ly, V. Nanda, W.F. Degrado, and K.P. Howard The conformation of the pore region of the M2 proton channel depends on lipid bilayer environment Protein Sci. 14 2005 856 861
68. T.K. Nyholm, S. Ozdirekcan, and J.A. Killian How protein transmembrane segments sense the lipid environment Biochemistry 46 2007 1457 1465
69. O.G. Mouritsen, and M.J. Zuckermann What's so special about cholesterol? Lipids 39 2004 1101 1113
70. S. Mall, R. Broadbridge, R.P. Sharma, J.M. East, and A.G. Lee Self-association of model transmembrane alpha-helices is modulated by lipid structure Biochemistry 40 2001 12379 12386
71. V. Anbazhagan, C. Munz, L. Tome, and D. Schneider Fluidizing the membrane by a local anesthetic: phenylethanol affects membrane protein oligomerization J. Mol. Biol. 404 2010 773 777
72. A.G. Lee How lipids affect the activities of integral membrane proteins Biochim. Biophys. Acta 1666 2004 62 87
73. T.W. Keenan, and D.J. Morre Phospholipid class and fatty acid composition of golgi apparatus isolated from rat liver and comparison with other cell fractions Biochemistry 9 1970 19 25
74. L. Orci, R. Montesano, P. Meda, F. Malaisse-Lagae, D. Brown, A. Perrelet, and P. Vassalli Heterogeneous distribution of filipin-cholesterol complexes across the cisternae of the Golgi apparatus Proc. Natl. Acad. Sci. U.S.A. 78 1981 293 297
75. A. Bergstrand, and G. Dallner Isolation of rough and smooth microsomes from rat liver by means of a commercially available centrifuge Anal. Biochem. 29 1969 351 356
76. G. van Meer, D.R. Voelker, and G.W. Feigenson Membrane lipids: where they are and how they behave Nat. Rev. Mol. Cell Biol. 9 2008 112 124
77. M. Fassler, M. Zocher, S. Klare, A.G. de la Fuente, J. Scheuermann, A. Capell, C. Haass, C. Valkova, A. Veerappan, D. Schneider, and C. Kaether Masking of transmembrane-based retention signals controls ER export of gamma-secretase Traffic 11 2010 250 258
78. C. Valkova, M. Albrizio, I.V. Roder, M. Schwake, R. Betto, R. Rudolf, and C. Kaether Sorting receptor Rer1 controls surface expression of muscle acetylcholine receptors by ER retention of unassembled alpha-subunits Proc. Natl. Acad. Sci. U.S.A. 108 2011 621 625
79. J. Fantini, N. Garmy, R. Mahfoud, and N. Yahi Lipid rafts: structure, function and role in HIV, Alzheimer's and prion diseases Expert Rev. Mol. Med. 4 2002 1 22
80. R.M. Johnson, A. Rath, and C.M. Deber The position of the Gly-xxx-Gly motif in transmembrane segments modulates dimer affinity Biochem. Cell Biol. 84 2006 1006 1012
81. R.S. Cantor Lipid composition and the lateral pressure profile in bilayers Biophys. J. 76 1999 2625 2639
82. D. Marsh Lateral pressure profile, spontaneous curvature frustration, and the incorporation and conformation of proteins in membranes Biophys. J. 93 2007 3884 3899
83. E. van den Brink-van der Laan, V. Chupin, J.A. de Killian, and B. Kruijff Stability of KcsA tetramer depends on membrane lateral pressure Biochemistry 43 2004 4240 4250
84. R.S. Cantor The lateral pressure profile in membranes: a physical mechanism of general anesthesia Biochemistry 36 1997 2339 2344
85. M. Langner, and S.W. Hui Merocyanine 540 as a fluorescence indicator for molecular packing stress at the onset of lamellar-hexagonal transition of phosphatidylethanolamine bilayers Biochim. Biophys. Acta 1415 1999 323 330
86. R.H. Templer, S.J. Castle, A.R. Curran, G. Rumbles, and D.R. Klug Sensing isothermal changes in the lateral pressure in model membranes using di-pyrenyl phosphatidylcholine Faraday Discuss. 1998 41 53 (discussion 69-78)
87. I.A. Boldyrev, X. Zhai, M.M. Momsen, H.L. Brockman, R.E. Brown, and J.G. Molotkovsky New BODIPY lipid probes for fluorescence studies of membranes J. Lipid Res. 48 2007 1518 1532
88. A.R. Curran, R.H. Templer, and P.J. Booth Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer Biochemistry 38 1999 9328 9336
89. J.C. Malinverni, and T.J. Silhavy An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane Proc. Natl. Acad. Sci. U.S.A. 106 2009 8009 8014
90. A.A. Gurtovenko, and I. Vattulainen Lipid transmembrane asymmetry and intrinsic membrane potential: two sides of the same coin J. Am. Chem. Soc. 129 2007 5358 5359
91. H. Palsdottir, and C. Hunte Lipids in membrane protein structures Biochim. Biophys. Acta 1666 2004 2 18
92. C.R. Sanders, and J.K. Myers Disease-related misassembly of membrane proteins Annu. Rev. Biophys. Biomol. Struct. 33 2004 25 51
93. E. Li, and K. Hristova Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies Biochemistry 45 2006 6241 6251
94. R. Campanella Membrane lipids modifications in human gliomas of different degree of malignancy J. Neurosurg. Sci. 36 1992 11 25
95. G.V. Sherbet Membrane fluidity and cancer metastasis Exp. Cell Biol. 57 1989 198 205
96. M.H. Mostafa, S.A. Sheweita, and N.M. Abdel-Moneam Influence of some anti-inflammatory drugs on the activity of aryl hydrocarbon hydroxylase and the cytochrome P450 content Environ. Res. 52 1990 77 82
97. K.L. Horan, B.S. Lutzke, A.R. Cazers, J.M. McCall, and D.E. Epps Kinetic evaluation of lipophilic inhibitors of lipid peroxidation in DLPC liposomes Free Radic. Biol. Med. 17 1994 587 596
98. V. Jendrossek, and R. Handrick Membrane targeted anticancer drugs: potent inducers of apoptosis and putative radiosensitisers Curr. Med. Chem. Anticancer Agents 3 2003 343 353