Generation and sensing of membrane curvature: Where materials science and biophysics meet

Current Opinion in Solid State and Materials Science

Volumn 17, Issue 4, 2013, Pages 164-174

  Cui, Qiang ^a   Zhang, Leili ^a   Wu, Zhe ^a   Yethiraj, Arun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Annular lipids; Antimicrobial peptides; Biomembrane remodeling; Cell penetration peptides; Curvature sensing; Gemini surfactants; Hydrophobic mismatch; Phase behavior

Indexed keywords

CONTINUUM MECHANICS; PEPTIDES; PHASE BEHAVIOR;

ANTIMICROBIAL PEPTIDE; BIO MEMBRANES; CELL PENETRATION; CURVATURE SENSING; GEMINI SURFACTANT; HYDROPHOBIC MISMATCH;

BIOLOGICAL MATERIALS;

EID: 84886726299     PISSN: 13590286     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cossms.2013.06.002     Document Type: Review

References (128)

1. B. Alberts, D. Bray, J. Lewis, M. Raff, K. Roberts, and J.D. Watson Molecular biology of the cell 1994 Garland Publishing, Inc.
2. D. Boal Mechanics of the cell 2002 Cambridge University Press Cambridge, UK
3. P.A. Janmey, and P.K.J. Kinnunen Biophysical properties of lipids and dynamic membranes Trends Cell Biol 16 2006 538 546
4. 2+-triggered exocytosis Annu Rev Biophys Biomol Struct 35 2006 135 160
5. H.T. McMahon, and J.L. Gallop Membrane curvature and mechanisms of dynamic cell membrane remodeling Nature 438 2005 590 596
6. J. Zimmerberg, and M.M. Kozlov How proteins produce cellular membrane curvature Nat Rev Mol Cell Biol 7 2006 9 19
7. G.J. Doherty, and H.T. McMahon Mediation, modulation, and consequences of membrane-cytoskeleton interactions Annu Rev Biochem 37 2008 65 95
8. Y. Shibata, J. Hu, M.M. Kozlov, and T.A. Rapoport Mechanisms shaping the membranes of cellular organelles Annu Rev Cell Dev Biol 25 2009 329 354
9. T.R. Graham, and M.M. Kozlov Interplay of proteins and lipids in generating membrane curvature Curr Opin Cell Biol 22 2010 430 436
10. A. Frost, V.M. Unger, and P. De Camilli The BAR domain superfamily: membrane molding macromolecules Cell 137 2009 191 196
11. M.G. Ford, I.G. Mills, B.J. Peter, Y. Vallis, G.J. Praefcke, and P.R. Evans Curvature of clathrin-coated pits driven by epsin Nature 419 2002 361 366
12. J. Bigay, P. Gounon, S. Robineau, and B. Antonny Lipid packing sensed by ArfGAP1 couples COPI coat disassembly to membrane bilayer curvature Nature 426 2003 563 566
13. J.G. Donaldson, and C.L. Jackson ARF family G proteins and their regulators: roles in membrane transport, development and disease Nat Rev Mol Cell Biol 12 2011 362 375
14. E.R. Chapman How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77 2008 615 641
15. J. Bigay, and B. Antonny Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity Dev Cell 23 2012 886 895
16. F. Campelo, H.T. McMahon, and M.M. Kozlov The hydrophobic insertion mechanism of membrane curvature generation by proteins Biophys J 95 2008 2325 2339
17. S. McLaughlin, and D. Murray Plasma membrane phosphoinositide organization by protein electrostatics Nature 438 2005 605 611
18. J. Saarikangas, H.X. Zhao, A. Pykalainen, P. Laurinmaki, P.K. Mattila, and P.K.J. Kinnunen Molecular mechanisms of membrane deformation by I-BAR domain proteins Curr Biol 19 2009 95 107
19. V.K. Bhatia, N.S. Hatzakis, and D. Stamou A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins Semin Cell Dev Biol 21 2010 381 390
20. G. Khelashvili, D. Harries, and H. Weinstein Modeling membrane deformations and lipid demixing upon protein-membrane interaction: the BAR dimer adsorption Biophys J 97 2009 1626 1635
21. A.L. Lai, L.K. Tamm, J.F. Ellena, and D.S. Cafiso Synaptotagmin 1 modulates lipid acyl chain order in lipid bilayers by demixing phosphosphatidylserine J Biol Chem 286 2011 25291 25300
22. J. Zimmerberg, and S. McLaughlin Membrane curvature: how bar domains bend bilayers Curr Biol 14 2004 R250 R252
23. M. Masuda, S. Takeda, M. Sone, T. Ohki, H. Mori, and Y. Kamioka Endophilin BAR domain drives membrane curvature by two newly identified structure-based mechanisms EMBO J 25 2006 2889 2897
24. H.S. Cui, E. Lyman, and G.A. Voth Mechanism of membrane curvature sensing by amphipathic helix containing proteins Biophys J 100 2011 1271 1279
25. G. Drin, and B. Antonny Amphipathic helices and membrane curvature FEBS Lett 584 2010 1840 1847
26. J.C. Stachowiak, E.M. Schmid, C.J. Ryan, H.S. Ann, D.Y. Sasaki, and M.B. Sherman Membrane bending by protein-protein crowding Nat Cell Biol 14 2012 944
27. T. Baumgart, B.R. Capraro, C. Zhu, and S.L. Das Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids Annu Rev Phys Chem 62 2011 483 506
28. K.C. Huang, and K.S. Ramanurthi Macromolecules that prefer their membrane curvy Mol Microbiol 76 2010 822 832
29. J.T. Groves, and J. Kuriyan Molecular mechanisms in signal transduction at the membrane Nat Struct Mol Biol 17 2010 659 665
30. B. Antonny Mechanisms of membrane curvature sensing Annu Rev Biochem 80 2011 101 123
31. A.D. Thompson, L.N. Makley, K. McMenimen, and J.E. Gestwicki The three cornerstones of chemical biology: Innovative probes, new discoveries, and enabling tools ACS Chem Biol 7 2012 791 796
32. K.M. Davies, M. Strauss, B. Daum, J.H. Kief, H.D. Osiewacz, and A. Rycovska Macromolecular organization of ATP synthase and complex I in whole mitochondria Proc Natl Acad Sci USA 108 2011 14121 14126
33. L.D. Renner, and D.B. Weibel Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes Proc Natl Acad Sci USA 108 2011 6264 6269
34. L.D. Renner, and D.B. Weibel MinD and MinE interact with anionic phospholipids and regulate division plane formation in Escherichia coli J Biol Chem 287 2012 38835 38844
35. C. Arnarez, J.P. Mazat, J. Elezgaray, S.J. Marrink, and X. Periole Evidence for cardiolipin binding sites on the membrane-exposed surface of the cytochrome bc(1) J Am Chem Soc 135 2013 3112 3120
36. R.O. Dror, R.M. Dirks, J.P. Grossman, H.F. Xu, and D.E. Shaw Biomolecular simulation: a computational microscope for molecular biology Annu Rev Biophys 41 2012 429 452
37. F. Khalili-Araghi, J. Gumbart, P.C. Wen, M. Sotomayor, E. Tajkhorshid, and K. Schulten Molecular dynamics simulations of membrane channels and transporters Curr Opin Struct Biol 19 2009 128 137
38. H.J. Risselada, and H. Grubmüller How snare molecules mediate membrane fusion: recent insights from molecular simulations Curr Opin Struct Biol 22 2012 187 196
39. J.B. Klauda, R.M. Venable, J.A. Freites, J.W. O'Connor, D.J. Tobias, and C. Mondragon-Ramirez Update of the charmm all-atom additive force field for lipids: validation on six lipid types J Phys Chem B 114 2010 7830 7843
40. A.J. Sodt, and R.W. Pastor Bending free energy from simulation: correspondence of planar and inverse hexagonal lipid phases Biophys J 104 2013 2202 2211
41. Y. Luo, and B. Roux Simulation of osmotic pressure in concentrated aqueous salt solutions J Phys Chem Lett 1 2010 183 189
42. C. Neale, W.F.D. Bennett, D.P. Tieleman, and R. Pomes Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers J Chem Theory Comput 7 2011 4175 4188
43. J.T. Kindt Atomistic simulation of mixed-lipid bilayers: mixed methods for mixed membranes Mol Simulat 37 2011 516 524
44. G.S. Ayton, W.G. Noid, and G.A. Voth Multiscale modeling of biomolecular systems: in serial and in parallel Curr Opin Struct Biol 17 2007 192 198
45. M. Deserno Mesoscopic membrane physics: concepts, simulations, and selected applications Macromol Rapid Commun 30 2009 752 771
46. M.G. Saunders, and G.A. Voth Coarse-graining of multiprotein assemblies Curr Opin Struct Biol 22 2012 144 150
47. S. Takada Coarse-grained molecular simulations of large biomolecules Curr Opin Struct Biol 22 2012 130 137
48. W. Shinoda, R. DeVane, and M.L. Klein Computer simulation studies of self-assembling macromolecules Curr Opin Struct Biol 22 2012 175 186
49. S.J. Marrink, H.J. Risselada, S. Yefimov, D.P. Tieleman, and A.H. de Vries The MARTINI force field: coarse grained model for biomolecular simulations J Phys Chem B 111 2007 7812 7824
50. L. Monticelli, S.K. Kandasamy, X. Periole, R.G. Larson, D.P. Tieleman, and S.J. Marrink The MARTINI coarse-grained force field: Extension to proteins J Chem Theory Comput 4 2008 819 834
51. D.H. de Jong, G. Singh, W.F.D. Bennett, C. Arnarez, T.A. Wassenaar, and L.V. Schafer Improved parameters for the MARTINI coarse-grained protein force field J Chem Theory Comput 9 2013 687 697
52. Z. Wu, Q. Cui, and A. Yethiraj A new coarse-grained model for water: the importance of electrostatic interactions J Phys Chem B 114 2010 10524 10529
53. Z. Wu, Q. Cui, and A. Yethiraj A new coarse-grained force field for membrane-peptide simulations J Chem Theory Comput 7 2011 3793 3802
54. C.L. Bergstrom, P.A. Baeles, Y. Lv, T.K. Vanderlick, and J.T. Groves Cytochrome c causes pore formation in cardiolipin-containing membranes Proc Natl Acad Sci USA 110 2013 6269 6274
55. M. Orsi, M.G. Noro, and J.W. Essex Dual-resolution molecular dynamics simulation of antimicrobials in biomembranes J Roy Soc Interface 8 2011 826 841
56. A.J. Rzepiela, M. Louhivuori, C. Peter, and S.J. Marrink Hybrid simulations: combining atomistic and coarse-grained force fields using virtual sites Phys Chem Chem Phys 13 2011 10437 10448
57. S. Riniker, J.R. Allison, and W.F. van Gunsteren On developing coarse-grained models for biomolecular simulation: a review Phys Chem Chem Phys 14 2012 12423 12430
58. T.A. Wassenaar, H.I. Ingolfsson, M. Priebeta, S.J. Marrink, and L.V. Schäfer Mixing MARTINI: electrostatic coupling in hybrid atomistic-coarse-grained biomolecular simulations J Phys Chem B 117 2013 3516 3530
59. S.O. Nielsen, R.E. Bulo, P.B. Moore, and B. Ensing Recent progress in adaptive multiscale molecular dynamics simulations of soft matter Phys Chem Chem Phys 12 2010 12401 12414
60. E. Lyman, F.M. Ytreberg, and D.M. Zuckerman Resolution exchange simulation Phys Rev Lett 96 2006 028105
61. A.J. Rzepiela, L.V. Schäfer, N. Goga, H.J. Risselada, A.H. de Vries, and S.J. Marrink Software news and update reconstruction of atomistic details from coarse-grained structures J Comput Chem 31 2010 1333 1343
62. J. Yoo, M.B. Jackson, and Q. Cui A comparison of coarse-grained and continuum models for membrane bending in lipid bilayer fusion pores Biophys J 104 2013 841 852
63. Mondal S, Khelashvili G, Shan J, Andersen OS, Weinstein H. Quantitative modeling of membrane deformations by multihelical membrane proteins: application to G-protein coupled receptors. Biophys J 2011;101:2902-101.
64. J. Yoo, and Q. Cui Membrane-mediated protein-protein interactions and connection to elastic models: a coarse-grained simulation analysis of gramicidin A association Biophys J 104 2013 128 138
65. F.L.H. Brown Continuum simulations of biomembrane dynamics and the importance of hydrodynamic effects Q Rev Biophys 44 2011 391 432
66. G.S. Ayton, and G.A. Voth Multiscale simulation of protein mediated membrane remodeling Semin Cell Dev Biol 21 2010 357 362
67. W. Im, M. Feig, and C.L. Brooks An implicit membrane generalized born theory for the study of structure, stability, and interactions of membrane proteins Biophys J 85 2003 2900 2918
68. T. Lazaridis Effective energy function for proteins in lipid membranes Proteins: Struct Funct Gene 52 2003 176 192
69. M. Mihajlovic, and T. Lazaridis Antimicrobial peptides bind more strongly to membrane pores Biochim Biophys Acta - Biomem 1798 2010 1494 1502
70. H. Zhan, and T. Lazaridis Inclusion of lateral pressure/curvature stress effects in implicit membrane models Biophys J 104 2013 643 654
71. S. Choe, K.A. Hecht, and M. Grabe A continuum method for determining membrane protein insertion energies and the problem of charged residues J Gen Physiol 131 2008 563 573
72. A. Panahi, and M. Feig Dynamic heterogeneous dielectric generalized born (DHDGB): an implicit membrane model with a dynamically varying bilayer thickness J Chem Theory Comput 9 2013 1709 1719
73. P.D. Blood, and G.A. Voth Direct observation of Bin/Amphiphysin/Rvs (BAR) domain-induced membrane curvature by means of molecular dynamics simulations Proc Natl Acad Sci USA 103 2006 15068 15072
74. A. Mishra, V.D. Gordon, L. Yang, R. Coridan, and G.C.L. Wong HIV TAT forms pores in membrans by inducing saddle-splay curvature: potential role of bidentate hydrogen bonding Angew Chem Int Ed Engl 47 2008 2986 2989
75. N. Schmidt, A. Mishra, G.H. Lai, and G.C.L. Wong Arginine-rich cell-penetrating peptides FEBS Lett 584 2010 1806 1813
76. M. Fuhrmans, and S.J. Marrink Molecular view of the role of fusion peptides in promoting positive membrane curvature J Am Chem Soc 134 2012 1543 1552
77. G.H. Fredrickson The equilibrium theory of inhomogeneous polymers 2006 Oxford Science Publications Oxford, UK
78. J. Mondal, M.K. Mahanthappa, and A. Yethiraj Self-assembly of gemini surfactants: a computer simulation study J Phys Chem B 117 2013 4254 4262
79. D.J. Mitchell, L. Steinman, D.T. Kim, C.G. Fathman, and J.B. Rothbard Polyargnine enters cells more efficiently than other polycationic homopolymers J Pept Res 56 2000 318 325
80. Wu Z, Cui Q, Yethiraj A. Why do Poly-Arg and Poly-Lys organize lipids differently? Insights from coarse-grained and atomistic simulations. J Phys Chem B; 2013, submitted for publication.
81. A. Mishra, G.H. Lai, N.W. Schmidt, V.Z. Sun, A.R. Rodriguez, and R. Tong Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions Proc Natl Acad Sci USA 108 2011 16883 16888
82. N.W. Schmidt, M. Lis, K. Zhao, G.H. Lai, A.N. Alexandrova, and G.N. Tew Molecular basis for nanoscopic membrane curvature generation from quantum mechanical models and synthetic transporter sequences J Am Chem Soc 134 2012 19207 19216
83. P.A. Wender, E. Kreider, E.T. Pelkey, J. Rothbard, and C.L. VanDeusen Dendrimetic molecular transporters: synthesis and evaluation of tunable polyguanidino dendrimers that facilitate cellular uptake Org Lett 7 2005 452 472
84. G.R. Meyer, J. Gullingsrud, K. Schulten, and B. Martinac Molecular dynamics study of MscL interactions with a curved lipid bilayer Biophys J 91 2006 1630 1637
85. O.H.S. Ollila, H.J. Risselada, M. Louhivuori, E. Lindahl, I. Vattulainen, and S.J. Marrink 3D pressure field in lipid membranes and membrane-protein complexes Phys Rev Lett 102 2009 078101
86. V.A. Harmandaris, and M. Deserno A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers J Chem Phys 125 2006 204905
87. H. Wang, J. de Joannis, Y. Jiang, J.C. Gaulding, B. Albrecht, and F. Yin Bilayer edge and curvature effects on partitioning of lipids by tail length: atomistic simulations Biophys J 95 2008 2647 2657
88. L.A. Morton, H. Yang, J.P. Saludes, Z. Fiorini, L. Beninson, and E.R. Chapman MARCKS-ED peptide as a curvature and lipid sensor ACS Chem Biol 8 2013 218 225
89. Y.Z. Ohkubo, T.V. Pogorelov, M.J. Arcario, G.A. Christensen, and E. Tajkhorshid Accelerating membrane insertion of peripheral proteins with a novel membrane mimetic model Biophys J 102 2012 2130 2139
90. A. Arkhipov, Y. Yin, and K. Schulten Four-scale description of membrane sculpting by BAR domains Biophys J 95 2008 2806 2821
91. S.J. Marrink, A.H. de Vries, and D.P. Tieleman Lipids on the move: simulations of membrane pores, domains, stalks and curves Biochim Biophys Acta - Biomem 1788 2009 149 168
92. R.P. Cheng, S.H. Gellman, and W.F. Degrado β-peptides: from structure to function Chem Rev 101 2001 3219 3232
93. S.H. Gellman Foldamers: a manifesto Acc Chem Res 31 1998 173 180
94. T.L. Raguse, E.A. Porter, and S.H. Gellman Structure-activity studies of 14-helical antimicrobial β-peptides: probing the relationship between conformational stability and antimicrobial potency J Am Chem Soc 124 2002 12774 12785
95. E.A. Porter, B. Weisblum, and S.H. Gellman Mimicry of host-defense peptides by unnatural oligomers: antimicrobial β-peptides J Am Chem Soc 124 2002 7324 7330
96. M.A. Schmitt, B. Weisblum, and S.H. Gellman Interplay among folding, sequence, and lipophilicity in the antibacterial and hemolytic activities of α/β-peptides J Am Chem Soc 129 2007 417 428
97. A.J. Karlsson, W.L. Pomerantz, S.H. Gellman, and S.P. Palecek Antifungal activity from 14-helical β-peptides J Am Chem Soc 128 2006 12630 12631
98. A.J. Karlsson, W.L. Pomerantz, K.J. Neilsen, S.H. Gellman, and S.P. Palecek Effect of sequence and structural properties on 14-helical β-peptide activity against candida albicans planktonic cells and biofilms ACS Chem Biol 4 2009 567 579
99. B.P. Mowery, S.E. Lee, D.A. Kissounko, R.F. Epand, B. Weisblum, and S.S. Stahl Mimicry of antimicrobial host-defense peptides by random copolymers J Am Chem Soc 129 2007 15474 15475
100. B.P. Mowery, A.H. Lindner, B. Weisblum, S.S. Stahl, and S.H. Gellman Structure-activity relationships among random nylon-3 copolymers that mimic antibacterial host-defense peptides J Am Chem Soc 131 2009 9735 9745
101. R.F. Epand, B.P. Mowery, S.E. Lee, S.S. Stahl, R.I. Lehrer, and S.H. Gellman Dual mechanism of bacterial lethality for a cationic sequence-random copolymer that mimics host-defense antimicrobial peptides J Mol Biol 379 2008 38 50
102. J. Mondal, X. Zhu, Q. Cui, and A. Yethiraj Sequence-dependent interaction of β-peptides with membranes J Phys Chem B 114 2010 13585 13592
103. X. Zhu, A. Yethiraj, and Q. Cui Establishing effective simulation protocols for β and mixed α/β peptides, I. QM and QM/MM models J Chem Theory Comput 3 2007 1538 1549
104. X. Zhu, P. König, S. Gellman, A. Yethiraj, and Q. Cui Establishing effective simulation protocols for β- and α/β-peptides. II. Molecular Mechanical (MM) model for a cyclic β-residue J Phys Chem B 112 2008 5439 5448
105. X. Zhu, P. König, M. Hoffman, A. Yethiraj, and Q. Cui Establishing effective simulation protocols for β- and α/β-peptides. III. Molecular Mechanical (MM) model for a non-cyclic β-residue J Comput Chem 31 2010 2063 2077
106. H.W. Huang Deformation free-energy of bilayer-membrane and its effect on gramicidin channel lifetime Biophys J 50 1986 1061 1070
107. K.S. Kim, J. Neu, and G. Oster Curvature-mediated interactions between membrane proteins Biophys J 75 1998 2274 2291
108. K.S. Kim, J. Neu, and G. Oster Effect of protein shape on multibody interactions between membrane inclusions Phys Rev E 61 2000 4281 4285
109. T. Chou, K.S. Kim, and G. Oster Statistical thermodynamics of membrane bending-mediated protein-protein attractions Biophys J 80 2001 1075 1087
110. J. Yoo, and Q. Cui Curvature generation and pressure profile modulation in membrane by lysolipids: insights from coarse-grained simulations Biophys J 97 2009 2267 2276
111. E. Perozo Gating prokaryotic mechanosensitive channels Nat Rev Mol Cell Biol 7 2006 109 119
112. C. Kung A possible unifying principle for mechanosensation Nature 436 2005 647 654
113. + channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane Proc Natl Acad Sci USA 105 2008 19276 19281
114. O.S. Andersen, and R.E. Koeppe Bilayer thickness and membrane protein function: an energetic perspective Annu Rev Biophys Biomol Struct 36 2007 107 130
115. R. Phillips, T. Ursell, P. Wiggins, and P. Sens Emerging roles for lipids in shaping membrane-protein function Nature 459 2009 379 385
116. o-ATP synthase dimer and its role in shaping the mitochondrial cristae Proc Natl Acad Sci USA 109 2012 13602 13607
117. B.J. Reynwar, G. Illya, V.A. Harmandaris, M.M. Muller, K. Kremer, and M. Deserno Aggregation and vesiculation of membrane proteins by curvature-mediated interactions Nature 447 2007 461 464
118. J.A. Lundbæk, S.A. Collingwood, H.I. Ingólfsson, R. Kapoor, and O.S. Andersen Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes J R Soc Interface 7 2010 373 395
119. R.L. Goforth, A.K. Chi, D.V. Greathouse, L.L. Providence, R.E. Koeppe, and O.S. Andersen Hydrophobic coupling of lipid bilayer energetics to channel function J Gen Physiol 121 2003 477 493
120. J. Yoo, and Q. Cui Three-dimensional stress field around a membrane protein: atomistic and coarse-grained simulation analysis of gramicidin A Biophys J 104 2013 117 127
121. T. Kim, K. Lee, P. Morris, R.W. Pastor, O.S. Andersen, and W. Im Influence of hydrophobic mismatch on structures and dynamics of gramicidin A and lipid bilayers Biophys J 102 2012 1551 1560
122. M. Yiannourakou, L. Marsella, F. de Meyer, and B. Smit Towards an understanding of membrane-mediated protein-protein interactions Faraday Discuss 144 2010 359 367 discussion 445-81
123. D.L. Parton, J.W. Klingelhoefer, and M.S.P. Sansom Aggregation of model membrane proteins, modulated by hydrophobic mismatch, membrane curvature, and protein class Biophys J 101 2011 691 699
124. H.-J.J. Kaiser, A. Orlowski, T. Róg, T.K.M. Nyholm, W. Chai, and T. Feizi Lateral sorting in model membranes by cholesterol-mediated hydrophobic matching Proc Natl Acad Sci USA 108 2011 16628 16633
125. B. de Kruijff, J.A. Killian, D.N. Ganchev, H.A. Rinia, and E. Sparr Striated domains: self-organizing ordered assemblies of transmembrane alpha-helical peptides and lipids in bilayers Biol Chem 387 2006 235 241
126. J. Mou, D.M. Czajkowsky, and Z. Shao Gramicidin A aggregation in supported gel state phosphatidylcholine bilayers Biochemistry 35 1996 3222 3226
127. S.L. Grage, A.M. Keleshian, T. Turdzeladze, A.R. Battle, W.C. Tay, and R.P. May Bilayer-mediated clustering and functional interaction of MscL channels Biophys J 100 2011 1252 1260
128. D.B. Weibel, W.R. DiLuzio, and G.M. Whitesides Microfabrication meets microbiology Nat Rev Microbiol 5 2007 209 218