Transmembrane domains interactions within the membrane milieu: Principles, advances and challenges

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 4, 2012, Pages 974-983

  Fink, Avner ^a   Sal Man, Neta ^a   Gerber, Doron ^a   Shai, Yechiel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

GALEX; Helix helix interaction; Recognition within the membrane; TOXCAT; ToxR; Transmembrane domain

Indexed keywords

BETA3 INTEGRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCINE; GLYCOPHORIN A; HYDROGEN POTASSIUM ADENOSINE TRIPHOSPHATASE; INTEGRIN; MEMBRANE PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; VALINE;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BIOINFORMATICS; CHEMOTAXIS; CHIRALITY; DIMERIZATION; FLUORESCENCE ANALYSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REPORTER GENE; REVIEW; STIMULUS RESPONSE;

AMINO ACID SEQUENCE; CELL MEMBRANE; MEMBRANE PROTEINS; MODELS, MOLECULAR; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84857652632     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2011.11.029     Document Type: Review

References (107)

1. S. Jayasinghe, K. Hristova, and S.H. White MPtopo: a database of membrane protein topology Protein Sci. 10 2001 455 458
2. S.H. White The progress of membrane protein structure determination Protein Sci. 13 2004 1948 1949
3. S.H. White, and G. von Heijne The machinery of membrane protein assembly Curr. Opin. Struct. Biol. 14 2004 397 404
4. R.R. Hantgan, D.S. Lyles, T.C. Mallett, M. Rocco, C. Nagaswami, and J.W. Weisel Ligand binding promotes the entropy-driven oligomerization of integrin AIIbB3 J. Biol. Chem. 278 2002 3417 3426
5. S.P. Lee, Z. Xie, G. Varghese, T. Nguyen, B.F. O'Dowd, and S.R. George Oligomerization of dopamine and serotonin receptors Neuropsychopharmacology 23 2000 S32 S40
6. S. Park, M. Meyer, A.D. Jones, H.P. Yennawar, N.H. Yennawar, and B.T. Nixon Two-component signaling in the AAA + ATPase DctD: binding Mg2 + and BeF3 - selects between alternative dimeric states of the receiver domain FASEB J. 16 2002 1964 1966
7. C.D. Rios, B.A. Jordan, I. Gomes, and L.A. Devi G-protein-coupled receptor dimerization: modulation of receptor function Pharmacol. Ther. 92 2001 71 87
8. T. Yagyu, H. Kobayashi, K. Wakahara, H. Matsuzaki, T. Kondo, N. Kurita, H. Sekino, K. Inagaki, M. Suzuki, N. Kanayama, and T. Terao A kunitz-type protease inhibitor bikunin disrupts ligand-induced oligomerization of receptors for transforming growth factor (TGF)-beta and subsequently suppresses TGF-beta signalings FEBS Lett. 576 2004 408 416
9. J. Yu, L. Bakhos, L. Chang, M.J. Holterman, W.L. Klein, and D.L. Venton Per-6-substituted beta-cyclodextrin libraries inhibit formation of beta-amyloid-peptide (A beta)-derived, soluble oligomers J. Mol. Neurosci. 19 2002 51 55
10. W.J. Wang, S.J. Russo, S. Mulugeta, and M.F. Beers Biosynthesis of surfactant protein C (SP-C). Sorting of SP-C proprotein involves homomeric association via a signal anchor domain J. Biol. Chem. 277 2002 19929 19937
11. A.G. Therien, and C.M. Deber Oligomerization of a peptide derived from the transmembrane region of the sodium pump gamma subunit: effect of the pathological mutation G41R J. Mol. Biol. 322 2002 583 590
12. Y. He, J.A. Wertheim, L. Xu, J.P. Miller, F.G. Karnell, J.K. Choi, R. Ren, and W.S. Pear The coiled-coil domain and Tyr177 of bcr are required to induce a murine chronic myelogenous leukemia-like disease by bcr/abl Blood 99 2002 2957 2968
13. M.A. Lemmon, J.M. Flanagan, J.F. Hunt, B.D. Adair, B.J. Bormann, C.E. Dempsey, and D.M. Engelman Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices J. Biol. Chem. 267 1992 7683 7689
14. M.A. Lemmon, H.R. Treutlein, P.D. Adams, A.T. Brunger, and D.M. Engelman A dimerization motif for transmembrane alpha-helices Nat. Struct. Biol. 1 1994 157 163
15. W.P. Russ, and D.M. Engelman The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296 2000 911 919
16. R. Gurezka, R. Laage, B. Brosig, and D. Langosch A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments J. Biol. Chem. 274 1999 9265 9270
17. C. Choma, H. Gratkowski, J.D. Lear, and W.F. DeGrado Asparagine-mediated self-association of a model transmembrane helix Nat. Struct. Biol. 7 2000 161 166
18. F.X. Zhou, H.J. Merianos, A.T. Brunger, and D.M. Engelman Polar residues drive association of polyleucine transmembrane helices Proc. Natl. Acad. Sci. U. S. A. 98 2001 2250 2255
19. H. Gratkowski, J.D. Lear, and W.F. DeGrado Polar side chains drive the association of model transmembrane peptides Proc. Natl. Acad. Sci. U. S. A. 98 2001 880 885
20. J.P. Dawson, J.S. Weinger, and D.M. Engelman Motifs of serine and threonine can drive association of transmembrane helices J. Mol. Biol. 316 2002 799 805
21. N. Sal-Man, D. Gerber, and Y. Shai The identification of a minimal dimerization motif QXXS that enables homo- and hetero-association of transmembrane helices in vivo J. Biol. Chem. 280 2005 27449 27457
22. N. Sal-Man, D. Gerber, and Y. Shai The composition rather than position of polar residues (QxxS) drives aspartate receptor transmembrane domain dimerization in vivo Biochemistry 43 2004 2309 2313
23. M.L. Plotkowski, S. Kim, M.L. Phillips, A.W. Partridge, C.M. Deber, and J.U. Bowie Transmembrane domain of myelin protein zero can form dimers: possible implications for myelin construction Biochemistry 46 2007 12164 12173
24. J. Oates, G. King, and A.M. Dixon Strong oligomerization behavior of PDGFbeta receptor transmembrane domain and its regulation by the juxtamembrane regions Biochim. Biophys. Acta 1798 2010 605 615
25. N.A. Noordeen, F. Carafoli, E. Hohenester, M.A. Horton, and B. Leitinger A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1 J. Biol. Chem. 281 2006 22744 22751
26. R.A. Melnyk, A.W. Partridge, and C.M. Deber Transmembrane domain mediated self-assembly of major coat protein subunits from Ff bacteriophage J. Mol. Biol. 315 2002 63 72
27. 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
28. C.L. Perrin, and J.B. Nielson "Strong" hydrogen bonds in chemistry and biology Annu. Rev. Phys. Chem. 48 1997 511 544
29. J.P. Dawson, R.A. Melnyk, C.M. Deber, and D.M. Engelman Sequence context strongly modulates association of polar residues in transmembrane helices J. Mol. Biol. 331 2003 255 262
30. N.M. Meindl-Beinker, C. Lundin, I. Nilsson, S.H. White, and G. von Heijne Asn- and Asp-mediated interactions between transmembrane helices during translocon-mediated membrane protein assembly EMBO Rep. 7 2006 1111 1116
31. A.W. Partridge, R.A. Melnyk, and C.M. Deber Polar residues in membrane domains of proteins: molecular basis for helix-helix association in a mutant CFTR transmembrane segment Biochemistry 41 2002 3647 3653
32. 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
33. D.B. Weiner, J. Liu, J.A. Cohen, W.V. Williams, and M.I. Greene A point mutation in the neu oncogene mimics ligand induction of receptor aggregation Nature 339 1989 230 231
34. C.I. Bargmann, M.C. Hung, and R.A. Weinberg Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of p185 Cell 45 1986 649 657
35. N. Sal-Man, D. Gerber, I. Bloch, and Y. Shai Specificity in transmembrane helix-helix interactions mediated by aromatic residues J. Biol. Chem. 282 2007 19753 19761
36. N. Sal-Man, D. Gerber, and Y. Shai Hetero-assembly between all-L- and all-D-amino acid transmembrane domains: forces involved and implication for inactivation of membrane proteins J. Mol. Biol. 344 2004 855 864
37. P.Z. Ding, and T.H. Wilson The effect of modifications of the charged residues in the transmembrane helices on the transport activity of the melibiose carrier of Escherichia coli Biochem. Biophys. Res. Commun. 285 2001 348 354
38. M. Burnay, G. Crambert, S. Kharoubi-Hess, K. Geering, and J.D. Horisberger Electrogenicity of Na, K- and H, K-ATPase activity and presence of a positively charged amino acid in the fifth transmembrane segment J. Biol. Chem. 278 2003 19237 19244
39. Y. Xu, D.A. Kakhniashvili, D.A. Gremse, D.O. Wood, J.A. Mayor, D.E. Walters, and R.S. Kaplan The yeast mitochondrial citrate transport protein. Probing the roles of cysteines, Arg(181), and Arg(189) in transporter function J. Biol. Chem. 275 2000 7117 7124
40. A.W. Partridge, A.G. Therien, and C.M. Deber Missense mutations in transmembrane domains of proteins: phenotypic propensity of polar residues for human disease Proteins 54 2004 648 656
41. I.C. Meij, J.B. Koenderink, H. van Bokhoven, K.F. Assink, W.T. Groenestege, J.J. de Pont, R.J. Bindels, L.A. Monnens, L.P. van den Heuvel, and N.V. Knoers Dominant isolated renal magnesium loss is caused by misrouting of the Na(+), K(+)-ATPase gamma-subunit Nat. Genet. 26 2000 265 266
42. J.R. Herrmann, A. Fuchs, J.C. Panitz, T. Eckert, S. Unterreitmeier, D. Frishman, and D. Langosch Ionic interactions promote transmembrane helix-helix association depending on sequence context J. Mol. Biol. 396 2010 452 461
43. K. Oosawa, and M. Simon Analysis of mutations in the transmembrane region of the aspartate chemoreceptor in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 83 1986 6930 6934
44. K. Hristova, and W.C. Wimley A look at arginine in membranes J. Membr. Biol. 239 2011 49 56
45. S. Belbeoc'h, C. Falasca, J. Leroy, A. Ayon, J. Massoulie, and S. Bon Elements of the C-terminal t peptide of acetylcholinesterase that determine amphiphilicity, homomeric and heteromeric associations, secretion and degradation Eur. J. Biochem. 271 2004 1476 1487
46. R. Ramachandran, R.K. Tweten, and A.E. Johnson Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit beta-strand alignment Nat. Struct. Mol. Biol. 11 2004 697 705
47. C. Soto, E.M. Sigurdsson, L. Morelli, R.A. Kumar, E.M. Castano, and B. Frangione Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy Nat. Med. 4 1998 822 826
48. M.M. Pallitto, J. Ghanta, P. Heinzelman, L.L. Kiessling, and R.M. Murphy Recognition sequence design for peptidyl modulators of beta-amyloid aggregation and toxicity Biochemistry 38 1999 3570 3578
49. M.A. Findeis, G.M. Musso, C.C. Arico-Muendel, H.W. Benjamin, A.M. Hundal, J.J. Lee, J. Chin, M. Kelley, J. Wakefield, N.J. Hayward, and S.M. Molineaux Modified-peptide inhibitors of amyloid beta-peptide polymerization Biochemistry 38 1999 6791 6800
50. E.R. Bernstein, and S. Sun Aromatic van der Waals clusters: structure and nonrigidity J. Phys. Chem. 100 1996 13348 13366
51. E. Gazit A possible role for pi-stacking in the self-assembly of amyloid fibrils FASEB J. 16 2002 77 83
52. G.B. McGaughey, M. Gagne, and A.K. Rappe Pi-stacking interactions. Alive and well in proteins J. Biol. Chem. 273 1998 15458 15463
53. R. Azriel, and E. Gazit Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation J. Biol. Chem. 276 2001 34156 34161
54. K.S. Campbell, B.T. Backstrom, G. Tiefenthaler, and E. Palmer CART: a conserved antigen receptor transmembrane motif Semin. Immunol. 6 1994 393 410
55. A. Ridder, P. Skupjen, S. Unterreitmeier, and D. Langosch Tryptophan supports interaction of transmembrane helices J. Mol. Biol. 354 2005 894 902
56. R.M. Johnson, K. Hecht, and C.M. Deber Aromatic and cation-pi interactions enhance helix-helix association in a membrane environment Biochemistry 46 2007 9208 9214
57. A. Rath, R.M. Johnson, and C.M. Deber Peptides as transmembrane segments: decrypting the determinants for helix-helix interactions in membrane proteins Biopolymers 88 2007 217 232
58. J.K. Lee, and R.M. Stroud Unlocking the eukaryotic membrane protein structural proteome Curr. Opin. Struct. Biol. 20 2011 464 470
59. E. Dobrovetsky, J. Menendez, A.M. Edwards, and C.M. Koth A robust purification strategy to accelerate membrane proteomics Methods 41 2007 381 387
60. S. Leviatan, K. Sawada, Y. Moriyama, and N. Nelson Combinatorial method for overexpression of membrane proteins in Escherichia coli J. Biol. Chem. 285 2010 23548 23556
61. E.E. Matthews, M. Zoonens, and D.M. Engelman Dynamic helix interactions in transmembrane signaling Cell 127 2006 447 450
62. 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
63. D. Gerber, and Y. Shai In vivo detection of hetero-association of glycophorin-A and its mutants within the membrane J. Biol. Chem. 276 2001 31229 31232
64. R.A. Melnyk, A.W. Partridge, and C.M. Deber Retention of native-like oligomerization states in transmembrane segment peptides: application to the Escherichia coli aspartate receptor Biochemistry 40 2001 11106 11113
65. X. Han, and L.K. Tamm A host-guest system to study structure-function relationships of membrane fusion peptides Proc. Natl. Acad. Sci. U. S. A. 97 2000 13097 13102
66. F. Liu, R.N. Lewis, R.S. Hodges, and R.N. McElhaney Effect of variations in the structure of a polyleucine-based alpha-helical transmembrane peptide on its interaction with phosphatidylethanolamine bilayers Biophys. J. 87 2004 2470 2482
67. W.P. Russ, and D.M. Engelman TOXCAT: a measure of transmembrane helix association in a biological membrane Proc. Natl. Acad. Sci. U. S. A. 96 1999 863 868
68. D. Schneider, and D.M. Engelman GALLEX, a measurement of heterologous association of transmembrane helices in a biological membrane J. Biol. Chem. 278 2003 3105 3111
69. 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
70. J. Tang, H. Yin, J. Qiu, M.J. Tucker, W.F. DeGrado, and F. Gai Using two fluorescent probes to dissect the binding, insertion, and dimerization kinetics of a model membrane peptide J. Am. Chem. Soc. 131 2009 3816 3817
71. L. He, A.R. Hoffmann, C. Serrano, K. Hristova, and W.C. Wimley High-throughput selection of transmembrane sequences that enhance receptor tyrosine kinase activation J. Mol. Biol. 412 2011 43 54
72. E. Psachoulia, D.P. Marshall, and M.S. Sansom Molecular dynamics simulations of the dimerization of transmembrane alpha-helices Acc. Chem. Res. 43 2010 388 396
73. J. Zhang, and T. Lazaridis Transmembrane helix association affinity can be modulated by flanking and noninterfacial residues Biophys. J. 96 2009 4418 4427
74. C.P. Chng, and S.M. Tan Leukocyte integrin alphaLbeta2 transmembrane association dynamics revealed by coarse-grained molecular dynamics simulations Proteins 79 2011 2203 2213
75. D.W. Sammond, D.E. Bosch, G.L. Butterfoss, C. Purbeck, M. Machius, D.P. Siderovski, and B. Kuhlman Computational design of the sequence and structure of a protein-binding peptide J. Am. Chem. Soc. 133 2011 4190 4192
76. O. Samna Soumana, N. Garnier, and M. Genest Molecular dynamics simulation approach for the prediction of transmembrane helix-helix heterodimers assembly Eur. Biophys. J. 36 2007 1071 1082
77. O. Samna Soumana, N. Garnier, and M. Genest Insight into the recognition patterns of the ErbB receptor family transmembrane domains: heterodimerization models through molecular dynamics search Eur. Biophys. J. 37 2008 851 864
78. 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
79. I.T. Arkin, and A.T. Brunger Statistical analysis of predicted transmembrane alpha-helices Biochim. Biophys. Acta 1429 1998 113 128
80. J.T. Jones, R.W. Akita, and M.X. Sliwkowski Binding specificities and affinities of egf domains for ErbB receptors FEBS Lett. 447 1999 227 231
81. Y. Yarden, and M.X. Sliwkowski Untangling the ErbB signalling network Nat. Rev. Mol. Cell Biol. 2 2001 127 137
82. D. Gerber, N. Sal-Man, and Y. Shai Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization J. Biol. Chem. 279 2004 21177 21182
83. A.J. Beevers, A. Damianoglou, J. Oates, A. Rodger, and A.M. Dixon Sequence-dependent oligomerization of the Neu transmembrane domain suggests inhibition of "conformational switching" by an oncogenic mutant Biochemistry 49 2010 2811 2820
84. L. He, N. Shobnam, and K. Hristova Specific inhibition of a pathogenic receptor tyrosine kinase by its transmembrane domain Biochim. Biophys. Acta 1808 2011 253 259
85. L. Chen, M. Merzlyakov, T. Cohen, Y. Shai, and K. Hristova Energetics of ErbB1 transmembrane domain dimerization in lipid bilayers Biophys. J. 96 2009 4622 4630
86. M.T. Duong, T.M. Jaszewski, K.G. Fleming, and K.R. MacKenzie Changes in apparent free energy of helix-helix dimerization in a biological membrane due to point mutations J. Mol. Biol. 371 2007 422 434
87. 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
88. W. Li, D.G. Metcalf, R. Gorelik, R. Li, N. Mitra, V. Nanda, P.B. Law, J.D. Lear, W.F. Degrado, and J.S. Bennett A push-pull mechanism for regulating integrin function Proc. Natl. Acad. Sci. U. S. A. 102 2005 1424 1429
89. H. Yin, R.I. Litvinov, G. Vilaire, H. Zhu, W. Li, G.A. Caputo, D.T. Moore, J.D. Lear, J.W. Weisel, W.F. Degrado, and J.S. Bennett Activation of platelet alphaIIbbeta3 by an exogenous peptide corresponding to the transmembrane domain of alphaIIb J. Biol. Chem. 281 2006 36732 36741
90. H. Zhu, D.G. Metcalf, C.N. Streu, P.C. Billings, W.F. Degrado, and J.S. Bennett Specificity for homooligomer versus heterooligomer formation in integrin transmembrane helices J. Mol. Biol. 401 2010 882 891
91. R. Mesibov, and J. Adler Chemotaxis toward amino acids in Escherichia coli J. Bacteriol. 112 1972 315 326
92. M.L. Hedblom, and J. Adler Chemotactic response of Escherichia coli to chemically synthesized amino acids J. Bacteriol. 155 1983 1463 1466
93. J. Adler, G.L. Hazelbauer, and M.M. Dahl Chemotaxis toward sugars in Escherichia coli J. Bacteriol. 115 1973 824 847
94. D.L. Milligan, and D.E. Koshland Jr. Site-directed cross-linking. Establishing the dimeric structure of the aspartate receptor of bacterial chemotaxis J. Biol. Chem. 263 1988 6268 6275
95. J.J. Falke, and S.H. Kim Structure of a conserved receptor domain that regulates kinase activity: the cytoplasmic domain of bacterial taxis receptors Curr. Opin. Struct. Biol. 10 2000 462 469
96. N. Sal-Man, and Y. Shai Arginine mutations within a transmembrane domain of Tar, an Escherichia coli aspartate receptor, can drive homodimer dissociation and heterodimer association in vivo Biochem. J. 385 2005 29 36
97. D. Gerber, and Y. Shai Chirality-independent protein-protein recognition between transmembrane domains in vivo J. Mol. Biol. 322 2002 491 495
98. D. Gerber, N. Sal-Man, and Y. Shai Structural adaptation of the glycophorin A transmembrane homodimer to D-amino acid modifications J. Mol. Biol. 339 2004 243 250
99. N. Manolios, S. Collier, J. Taylor, J. Pollard, L.C. Harrison, and V. Bender T-cell antigen receptor transmembrane peptides modulate T-cell function and T cell-mediated disease Nat. Med. 3 1997 84 88
100. D. Gerber, F.J. Quintana, I. Bloch, I.R. Cohen, and Y. Shai D-enantiomer peptide of the TCRalpha transmembrane domain inhibits T-cell activation in vitro and in vivo FASEB J. 19 2005 1190 1192
101. F.J. Quintana, D. Gerber, I. Bloch, I.R. Cohen, and Y. Shai A structurally altered D,L-amino acid TCRalpha transmembrane peptide interacts with the TCRalpha and inhibits T-cell activation in vitro and in an animal model Biochemistry 46 2007 2317 2325
102. N.I. Tarasova, R. Seth, S.G. Tarasov, T. Kosakowska-Cholody, C.A. Hrycyna, M.M. Gottesman, and C.J. Michejda Transmembrane inhibitors of P-glycoprotein, an ABC transporter J. Med. Chem. 48 2005 3768 3775
103. J.L. Popot, and D.M. Engelman Membrane protein folding and oligomerization: the two-stage model Biochemistry 29 1990 4031 4037
104. 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
105. A. Bennasroune, M. Fickova, A. Gardin, S. Dirrig-Grosch, D. Aunis, G. Cremel, and P. Hubert Transmembrane peptides as inhibitors of ErbB receptor signaling Mol. Biol. Cell 15 2004 3464 3474
106. M.R. Afara, C.A. Trieber, J.P. Glaves, and H.S. Young Rational design of peptide inhibitors of the sarcoplasmic reticulum calcium pump Biochemistry 45 2006 8617 8627
107. S.J. Shandler, I.V. Korendovych, D.T. Moore, K.B. Smith-Dupont, C.N. Streu, R.I. Litvinov, P.C. Billings, F. Gai, J.S. Bennett, and W.F. Degrado Computational design of a beta-peptide that targets transmembrane helices J. Am. Chem. Soc. 133 2011 12378 12381