Biomembranes in atomistic and coarse-grained simulations

Journal of Physics Condensed Matter

Volumn 27, Issue 32, 2015, Pages

  Pluhackova, Kristyna ^a   Böckmann, Rainer A ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

biomembranes; coarse grained simulation; membranes; molecular dynamics simulation; multiscale modeling; resolution transformation

Indexed keywords

BIOLOGICAL MEMBRANES; CLOSED LOOP CONTROL SYSTEMS; CYTOLOGY; LIPIDS; MEMBRANES; PROTEINS;

BIOMEMBRANES; BIOMOLECULAR STRUCTURES; COARSE-GRAINED; COARSE-GRAINED MOLECULAR DYNAMICS; MEMBRANE MICRODOMAINS; MOLECULAR DYNAMICS SIMULATIONS; MULTI-SCALE MODELING; SPECIFIC DISTRIBUTION;

MOLECULAR DYNAMICS;

LIPID BILAYER;

ANIMAL; CELL MEMBRANE; CHEMISTRY; HUMAN; LIPID BILAYER; MOLECULAR DYNAMICS; THERMODYNAMICS;

ANIMALS; CELL MEMBRANE; HUMANS; LIPID BILAYERS; MEMBRANE MICRODOMAINS; MOLECULAR DYNAMICS SIMULATION; THERMODYNAMICS;

EID: 84938152514     PISSN: 09538984     EISSN: 1361648X     Source Type: Journal    
DOI: 10.1088/0953-8984/27/32/323103     Document Type: Review

References (244)

1. McGuffee S R and Elcock A H 2010 PLoS Comput. Biol. 6 e1000694
2. Dupuy A D and Engelman D M 2008 Proc. Natl Acad. Sci. USA 105 2848-52
3. Takamori S et al 2006 Cell 127 831-46
4. Javanainen M, Hammaren H, Monticelli L, Jeon J H, Miettinen M S, Martinez-Seara H, Metzler R and Vattulainen I 2013 Faraday Discuss. 161 397-417
5. Honigmann A, Sadeghi S, Keller J, Hell S W, Eggeling C and Vink R 2014 eLife 3 e01671
6. van Meer G, Voelker D R and Feigenson G W 2008 Nat. Rev. Mol. Cell. Biol. 9 112-24
7. Klose C, Surma M A, Gerl M J, Meyenhofer F, Shevchenko A and Simons K 2012 PLoS ONE 7 e35063
8. Yang Y, Khoo W J, Zheng Q, Chung H J and Yuk H G 2014 Int. J. Food Microbiol. 172 102-9
9. Atilla-Gokcumen G E, Muro E, Relat-Goberna J, Sasse S, Bedigian A, Coughlin M L, Garcia-Manyes S and Eggert U S 2014 Cell 156 428-39
10. Behnia R and Munro S 2005 Nature 438 597-604
11. Shin J J H and Loewen C J R 2011 BMC Biol. 9 85
12. Leventis P A and Grinstein S 2010 Ann. Rev. Biophys. 39 407-27
13. Menon I, Huber T, Sanyal S, Banerjee S, Barré P, Canis S, Warren J D, Hwa J, Sakmar T P and Menon A K 2011 Curr. Biol. 21 149-53
14. Johnston D and Wu S M 1995 Foundations of Cellular Neurophysiology (Cambridge, MA: MIT Press)
15. Phillips R, Ursell T, Wiggins P and Sens P 2009 Nature 459 379-85
16. Niemelä P S, Miettinen M S, Monticelli L, Hammaren H, Bjelkmar P, Murtola T, Lindahl E and Vattulainen I 2010 J. Am. Chem. Soc. 132 7574-5
17. de Planque M R R, Greathouse D V, Koeppe R E, Schäfer H, Marsh D and Killian J A 1998 Biochemistry 37 9333-45
18. Ramakrishnan N, Sunil Kumar P B and Radhakrishnan R 2014 Phys. Rep. 543 1-60
19. Aimon S, Callan-Jones A, Berthaud A, Pinot M, Toombes G E S and Bassereau P 2014 Dev. Cell 28 212-8
20. Quemeneur F, Sigurdsson J K, Renner M, Atzberger P J, Bassereau P and Lacoste D 2014 Proc. Natl Acad. Sci. USA 111 5083-7
21. Böckmann R A, Hac A, Heimburg T and Grubmüller H 2003 Biophys. J. 85 1647-55
22. Busch S, Pardo L C, Smuda C and Unruh T 2012 Soft Matter 8 3576-85
23. Morhenn H, Busch S and Unruh T 2012 J. Phys.: Condens. Matter 24 375108
24. Bulacu M, Périole X and Marrink S J 2012 Biomacromolecules 13 196-205
25. Kirschner K N, Lins R D, Maass A and Soares T A 2012 J. Chem. Theory Comput. 8 4719-31
26. Piggot T J, Holdbrook D A and Khalid S 2011 J. Phys. Chem. B 115 13381-8
27. Lopéz C A, de Vries A H and Marrink S J 2013 Sci. Rep. 3 2071
28. Dahlberg M 2007 J. Phys. Chem. B 111 7194-200
29. Róg T, Martinez-Seara H, Munck N, Orešič M, Karttunen M and Vattulainen I 2009 J. Phys. Chem. B 113 3413-22
30. Chugunov A, Pyrkova D, Nolde D, Polyansky A, Pentkovsky V and Efremov R 2013 Sci. Rep. 3 1678
31. Borisovska M et al 2012 J. Neurosci. 32 15983-97
32. Ingólfsson H I, Melo M N, van Eerden F J, Arnarez C, Lopez C A, Wassenaar T A, Periole X, de Vries A H, Tieleman D P and Marrink S J 2014 J. Am. Chem. Soc. 136 14554-9
33. Marrink S J, de Vries A H and Tieleman D P 2009 Biochim. Biophys. Acta: Biomembr. 1788 149-68
34. Arkhipov A, Yin Y and Schulten K 2008 Biophys. J. 95 2806-21
35. Yesylevskyy S O, Demchenko A P, Kraszewski S and Ramseyer C 2013 Sci. World J. 2013 1-10
36. Markvoort A J and Marrink S J 2011 Current Topics in Membranes (Current Topics in Membranes vol 68) ed L V Chernomordik and M M Kozlov (London: Academic) pp 259-94
37. Yang K, Shao X and Ma Y 2009 Phys. Rev. E 79 051924
38. Böckmann R A, de Groot B L, Kakorin S, Neumann E and Grubmüller H 2008 Biophys. J. 95 1837-50
39. Bennett W F D and Tieleman D P 2011 J. Chem. Theory Comput. 7 2981-8
40. Pannuzzo M and Böckmann R A 2014 Biophys. J. 106 1-2
41. Bennett W F D and Tieleman D P 2013 Biochim. Biophys. Acta: Biomembr. 1828 1765-76
42. Baoukina S, Mendez-Villuendas E, Bennett W F D and Tieleman D P 2013 Faraday Discuss. 161 63-75
43. Noguchi H 2012 Soft Matter 8 3146-153
44. Nishizawa M and Nishizawa K 2011 J. Biophys. Chem. 2 268-84
45. Phillips J C, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel R D, Kale L and Schulten K 2005 J. Comput. Chem. 26 1781-802
46. Pronk S et al 2013 Bioinformatics 29 845-54
47. Plimpton S 1995 J. Comput. Phys. 117 1-19
48. Scott W R P, Hunenberger P H, Tironi I G, Mark A E, Billeter S R, Fennen J, Torda A E, Huber T, Kruger P and van Gunsteren W F 1999 J. Phys. Chem. A 103 3596-607
49. Brooks B R et al 2009 J. Comput. Chem. 30 1545-614
50. Case D et al 2014 AMBER 14 (San Francisco: University of California)
51. Dror R O, Dirks R M, Grossman J P, Xu H and Shaw D E 2012 Ann. Rev. Biophys. 41 429-52
52. Shaw D E et al 2009 Proc. of the Conf. on High Performance Computing Networking, Storage and Analysis (New York: ACM) pp 39:1-39:11
53. Sodt A J, Sandar M L, Gawrisch K, Pastor R W and Lyman E 2014 J. Am. Chem. Soc. 136 725-32
54. Zuckerman D M 2011 Ann. Rev. Biophys. 40 41-62
55. Berendsen H J C 2007 Simulating the Physical World (Cambridge: Cambridge University Press)
56. Ingólfsson H I, Lopez C A, Uusitalo J J, de Jong D H, Gopal S M, Periole X and Marrink S J 2014 WIREs Comput. Mol. Sci. 4 225-48
57. Limbach H, Arnold A, Mann B and Holm C 2006 Comput. Phys. Commun. 174 704-27
58. Nielsen S O, Bulo R E, Moore P B and Ensing B 2010 Phys. Chem. Chem. Phys. 12 12401-14
59. Lomize M A, Lomize A L, Pogozheva I D and Mosberg H I 2006 Bioinformatics 22 623-5
60. Tieleman D 2012 Comprehensive Biophysics ed E H Egelman (Amsterdam: Elsevier) pp 312-36 in
61. Pluhackova K, Wassenaar T A and Böckmann R A 2013 Membrane Biogenesis (Methods in Molecular Biology vol 1033) ed D Rapaport and J M Herrmann (New York: Humana Press) pp 85-101
62. Wassenaar T A, Pluhackova K, Böckmann R A, Marrink S J and Tieleman D P 2014 J. Chem. Theory Comput. 10 676-90
63. Ash W L, Zlomislic M R, Oloo E O and Tieleman D P 2004 Biochim. Biophys. Acta: Biomembr. 1666 158-89
64. Lyubartsev A P and Rabinovich A L 2011 Soft Matter 7 25-39
65. Nielsen S O, Lopez C F, Srinivas G and Klein M L 2004 J. Phys.: Condens. Matter 16 R481
66. Venturoli M, Sperotto M M, Kranenburg M and Smit B 2006 Phys. Rep. 437 1-54
67. Domański J, Stansfeld P J, Sansom M S P and Beckstein O 2010 J. Membr. Biol. 236 255-8
68. Berger O, Edholm O and Jähnig F 1997 Biophys. J. 72 2002-13
69. Essex J W, Hann M M and Richards W G 1994 Phil. Trans. R. Soc. Lond. 344 239-60
70. Jorgensen W L, Maxwell D S and Tirado-Rives J 1996 J. Am. Chem. Soc. 118 11225-36
71. Duan Y et al 2003 J. Comput. Chem. 24 1999-2012
72. Best R B, Zhu X, Shim J, Lopes P E M, Mittal J, Feig M and MacKerell A D 2012 J. Chem. Theory Comput. 8 3257-73
73. Kaminski G, Friesner R A, Tirado-Rives J and Jorgensen W L 2001 J. Phys. Chem. B 105 6474-87
74. Schmid N, Eichenberger A P, Choutko A, Riniker S, Winger M, Mark A E and Gunsteren W F 2011 Europ. Biophys. J. 40 843-56
75. Provasi D, Bortolato A and Filizola M 2009 Biochemistry 48 10020-9
76. Berka K, Hendrychová T, Anzenbacher P and Otyepka M 2011 J. Phys. Chem. A 115 11248-55
77. Cordomí A, Caltabiano G and Pardo L 2012 J. Chem. Theory Comput. 8 948-58
78. Klauda J B, Venable R M, Freites J A, O'Connor J W, Tobias D J, Mondragon-Ramirez C, Vorobyov I, MacKerell A D and Pastor R W 2010 J. Phys. Chem. B 114 7830-43
79. Guo S, Moore T C, Iacovella C R, Strickland L A and McCabe C 2013 J. Chem. Theory Comput. 9 5116-26
80. Vanommeslaeghe K et al 2010 J. Comput. Chem. 31 671-90
81. Yu W, He X, Vanommeslaeghe K and MacKerell A D 2012 J. Comput. Chem. 33 2451-68
82. Skjevik Å A, Madej B D, Walker R C and Teigen K 2012 J. Phys. Chem. B 116 11124-36
83. Jämbeck J P M and Lyubartsev A P 2012 J. Phys. Chem. B 116 3164-79
84. Jämbeck J P M and Lyubartsev A P 2012 J. Chem. Theory Comput. 8 2938-48
85. Jämbeck J P M and Lyubartsev A P 2013 J. Chem. Theory Comput. 9 774-84
86. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A and Simmerling C 2006 PROTEINS: Struct. Funct. Bioinf. 65 712-25
87. Dickson C J, Madej B D, Skjevik A A, Betz R M, Teigen K, Gould I R and Walker R C 2014 J. Chem. Theory Comput. 10 865-79
88. Huang L and Roux B 2013 J. Chem. Theory Comput. 9 3543-56
89. Kirschner K N, Yongye A B, Tschampel S M, González-Outeirino J, Daniels C R, Foley B L and Woods R J 2008 J. Comput. Chem. 29 622-55
90. Tessier M B, DeMarco M L, Yongye A B and Woods R J 2008 Mol. Simul. 34 349-63
91. Ravi H K, Stach M, Soares T A, Darbre T, Reymond J L and Cascella M 2013 Chem. Commun. 49 8821-3
92. Siu S W I, Pluhackova K and Böckmann R A 2012 J. Chem. Theory Comput. 8 1459-70
93. Maciejewski A, Pasenkiewicz-Gierula M, Cramariuc O, Vattulainen I and Rog T 2014 J. Phys. Chem. B 118 4571-81
94. Marrink S J, de Vries A H and Mark A E 2004 J. Phys. Chem. B 108 750-60
95. Cooke I R, Kremer K and Deserno M 2005 Phys. Rev. E 72 011506
96. Berendsen H J C, Postma J P M, van Gunsteren W F and Hermans J 1981 Intermolecular Forces pp 331-42
97. van Gunsteren W F, Billeter S R, Eising A A, Hünenberger P H, Krüger P, Mark A E, Scott W R P and Tironi I G 1996 Biomolecular Simulation: The GROMOS96 manual and user guide (Zürich, Switzerland: Hochschuleverlag AG an der ETH Zürich)
98. Schuler L D, Daura X and van Gunsteren W F 2001 J. Comput. Chem. 22 1205-18
99. Oostenbrink C, Villa A, Mark A E and Van Gunsteren W F 2004 J. Comput. Chem. 25 1656-76
100. Poger D, Van Gunsteren W F and Mark A E 2010 J. Comput. Chem. 31 1117-25
101. Chiu S W, Pandit S A, Scott H L and Jakobsson E 2009 J. Phys. Chem. B 113 2748-63
102. Bennett W F D and Tieleman D P 2012 J. Lipid Res. 53 421-9
103. Schüttelkopf A W and van Aalten D M F 2004 Acta Cryst. D 60 1355-63
104. Lemkul J A, Allen W J and Bevan D R 2010 J. Chem. Inf. Model. 50 2221-35
105. Siu S W I, Vacha R, Jungwirth P and Böckmann R A 2008 J. Chem. Phys. 128 125103
106. Piggot T J, Pineiro A and Khalid S 2012 J. Chem. Theory Comput. 8 4593-609
107. Ollila O H S 2015 arXiv:1309.2131
108. MacCallum J L, Bennett W F D and Tieleman D P 2008 Biophys. J. 94 3393-404
109. Bereau T and Deserno M 2015 J. Mol. Biol. 248 395-405
110. Levitt M and Warshel A 1975 Nature 253 694-8
111. Dill K A 1985 Biochemistry 24 1501-9
112. Smit B, Hilbers P A J, Esselink K, Rupert L A M, van Os N M and Schlijper A G 1990 Nature 348 624-5
113. Noid W G 2013 J. Chem. Phys. 139 090901
114. Riniker S, Allison J R and van Gunsteren W F 2012 Phys. Chem. Chem. Phys. 14 12423-30
115. Kar P, Gopal S M, Cheng Y M, Panahi A and Feig M 2014 J. Chem. Theory Comput. 10 3459-72
116. Glattli A, Daura X and van Gunsteren W 2002 J. Chem. Phys. 116 9811-28
117. Darré L, Machado M R and Pantano S 2012 WIREs Comput. Mol. Sci. 2 921-30
118. Hadley K R and McCabe C 2012 Molec. Sim. 38 671-81
119. Yesylevskyy S O, Schäfer L V, Sengupta D and Marrink S J 2010 PLoS Comput. Biol. 6 e1000810
120. Riniker S and van Gunsteren W F 2011 J. Chem. Phys. 134 084110
121. Wu Z, Cui Q and Yethiraj A 2010 J. Phys. Chem. B 114 10524-9
122. Orsi M and Essex J W 2011 PLoS ONE 6 e28637
123. Darré L, Machado M R, Dans P D, Herrera F E and Pantano S 2010 J. Chem. Theory Comput. 6 3793-807
124. Marrink S J, Risselada H J, Yefimov S, Tieleman D P and de Vries A H 2007 J. Phys. Chem. B 111 7812-24
125. Monticelli L, Kandasamy S K, Periole X, Larson R G, Tieleman D P and Marrink S J 2008 J. Chem. Theory Comput. 4 819-34
126. López C A, Rzepiela A J, de Vries A H, Dijkhuizen L, Hü nenberger P H and Marrink S J 2009 J. Chem. Theory Comput. 5 3195-210
127. López C A, Sovova Z, van Eerden F J, de Vries A H and Marrink S J 2013 J. Chem. Theory Comput. 9 1694-708
128. Marrink S J, de Vries A H, Harroun T A, Katsaras J and Wassall S R 2008 J. Am. Chem. Soc. 130 10-11
129. de Jong D H, Singh G, Bennett W F D, Arnarez C, Wassenaar T A, Schäfer L V, Periole X, Tieleman D P and Marrink S J 2013 J. Chem. Theory Comput. 9 687-97
130. Pluhackova K, Wassenaar T A, Kirsch S and Böckmann R A 2015 J. Phys. Chem. B 119 4396-408
131. Marrink S J and Tieleman D P 2013 Chem. Soc. Rev. 42 6801-22
132. Shelley J C, Shelley M Y, Reeder R C, Bandyopadhyay S, Moore P B and Klein M L 2001 J. Phys. Chem. B 105 9785-92
133. Pickholz M, Saiz L and Klein M L 2005 Biophys. J. 88 1524-34
134. Nielsen S O, Lopez C F, Ivanov I, Moore P B, Shelley J C and Klein M L 2004 Biophys. J. 87 2107-15
135. Nguyen T H T, Rao N Z, Schroeder W M and Moore P B 2010 Chem. Phys. Lipids 163 530-7
136. Shinoda W, DeVane R and Klein M L 2010 J. Phys. Chem. B 114 6836-49
137. Shinoda W, DeVane R and Klein M L 2012 Curr. Opin. Struct. Biol. 22 175-86
138. DeVane R, Shinoda W, Moore P B and Klein M L 2009 J. Chem. Theory Comput. 5 2115
139. Orsi M, Haubertin D Y, Sanderson W E and Essex J W 2008 J. Phys. Chem. B 112 802-15
140. Michel J, Orsi M and Essex J W 2008 J. Phys. Chem. B 112 657-60
141. Izvekov S and Voth G A 2005 J. Phys. Chem. B 109 2469-73
142. Izvekov S and Voth G A 2006 J. Chem. Theory Comput. 2 637-48
143. Liu P, Izvekov S and Voth G A 2007 J. Phys. Chem. B 111 11566-75
144. Zhou J, Thorpe I F, Izvekov S and Voth G A 2007 Biophys. J. 92 4289-303
145. Thorpe I F, Zhou J and Voth G A 2008 J. Phys. Chem. B 112 13079-90
146. Wang Z J and Deserno M 2010 J. Phys. Chem. B 114 11207-20
147. Bereau T and Deserno M 2009 J. Chem. Phys. 130 235106
148. Bereau T, Globisch C, Deserno M and Peter C 2012 J. Chem. Theory Comput. 8 3750-8
149. Bereau T, Wang Z J and Deserno M 2014 J. Chem. Phys. 140 115101
150. Arnarez C, Uusitalo J J, Masman M F, Ingólfsson H I, de Jong D H, Melo M N, Periole X, de Vries A H and Marrink S J 2015 J. Chem. Theory Comput. 11 260-75
151. Izvekov S and Voth G A 2009 J. Phys. Chem. B 113 4443-55
152. Brannigan G, Lin L C L and Brown F L H 2006 Europ. Biophys. J. 35 104-24
153. Drouffe J M, Maggs A C and Leibler S 1991 Science 254 1353-6
154. Brannigan G and Brown F L H 2004 J. Chem. Phys. 120 1059-71
155. Noguchi H and Takasu M 2001 Phys. Rev. E 64 041913
156. Farago O and Pincus P 2003 APS March Meeting Abstracts K9013
157. Brannigan G, Philips P F and Brown F L H 2005 Phys. Rev. E 72 011915
158. Srivastava A and Voth G A 2013 J. Chem. Theory Comput. 9 750-65
159. Reynwar B J and Deserno M 2008 Biointerphases 3 FA117-24
160. Illya G and Deserno M 2008 Biophys. J. 95 4163-73
161. Reynwar B J, Illya G, Harmandaris V A, Muller M M, Kremer K and Deserno M 2007 Nature 447 461-4
162. Yin Y, Arkhipov A and Schulten K 2009 Structure 17 882-92
163. Murtola T, Falck E, Patra M, Karttunen M and Vattulainen I 2004 J. Chem. Phys. 121 9156-65
164. Noguchi H 2011 J. Chem. Phys. 134 055101
165. Rzepiela A J, Louhivuori M, Peter C and Marrink S J 2011 Phys. Chem. Chem. Phys. 13 10437-48
166. Wassenaar T A, Ingólfsson H I, Prieß M, Marrink S J and Schäfer L V 2013 J. Phys. Chem. B 117 3516-30
167. Orsi M, Noro M G and Essex J W 2011 J. R. Soc. Interface 8 826-41
168. Wang J, Wolf R M, Caldwell J W, Kollman P A and Case D A 2004 J. Comput. Chem. 25 1157-74
169. Orsi M, Michel J and Essex J W 2010 J. Phys.: Condens. Matter 22 155106
170. Liu Y and Ichiye T 1996 J. Phys. Chem. 100 2723-30
171. Orsi M, Ding W and Palaiokostas M 2014 J. Chem. Theory Comput. 10 4684-93
172. Shi Q, Izvekov S and Voth G A 2006 J. Phys. Chem. B 110 15045-8
173. Izvekov S and Voth G A 2009 J. Chem. Theory Comput. 5 3232-44
174. Riniker S and van Gunsteren W F 2012 J. Chem. Phys. 137 044129
175. Praprotnik M, Site L D and Kremer K 2008 Ann. Rev. Phys. Chem. 59 545-71
176. Zavadlav J, Melo M N, Marrink S J and Praprotnik M 2014 J. Chem. Phys. 140 054114
177. Feig M, Rotkiewicz P, Kolinski A, Skolnick J and Brooks I I 2000 Proteins 41 86-97
178. Rotkiewicz P and Skolnick J 2008 J. Comput. Chem. 29 1460-5
179. Brocos P, Mendoza-Espinosa P, Castillo R, Mas-Oliva J and Pineiro A 2012 Soft Matter 8 9005-14
180. Shih A Y, Freddolino P L, Sligar S G and Schulten K 2007 Nano Lett. 7 1692-6
181. Hess B, Leon S, van der Vegt N and Kremer K 2006 Soft Matter 2 409-14
182. Sun Y, McKeever S, Balali-Mood K and Sansom M S P 2007 IEEE Int. Conf. Bioinformatics and Biomedicine pp 294-301
183. Stansfeld P J and Sansom M S 2011 J. Chem. Theory Comput. 7 1157-66
184. Thøgersen L, Schiøtt B, Vosegaard T, Nielsen N C and Tajkhorshid E 2008 Biophys. J. 95 4337-47
185. Rzepiela A J, Schäfer L V, Goga N, Risselada H J, De Vries A H and Marrink S J 2010 J. Comput. Chem. 31 1333-43
186. Shrivastava I H and Sansom M S P 2000 Biophys. J. 78 557-70
187. Espinoza-Fonseca L M, Autry J M and Thomas D D 2014 PLoS One 9 e95979
188. de Groot B L and Grubmüller H 2001 Science 294 2353-87
189. de Groot B L, Frigato T, Helms V and Grubmüller H 2003 J. Molec. Biol. 333 279-93
190. McNulty R, Ulmschneider J P, Luecke H and Ulmschneider M B 2013 Nat. Commun. 4 2900
191. Torrie G M and Valleau J P 1977 J. Comput. Phys. 23 187-99
192. Chattopadhyay A 2014 Adv. Biol. 2014 143023
193. Noguchi N, Saito Y and Urano Y 2014 Biochem. Biophys. Res. Commun. 446 692-6
194. Cyster J G, Dang E V, Reboldi A and Yi T 2014 Nat. Rev. Immunol. 14 731-43
195. Liu J, Xian G, Li M, Zhang Y, Yang M, Yu Y, Lv H, Xuan S, Lin Y and Gao L 2014 Cell Death Dis. 5 e1372
196. Neuvonen M, Manna M, Mokkila S, Javanainen M, Rog T, Liu Z, Bittman R, Vattulainen I and Ikonen E 2014 PLoS One 9 e103743
197. Olsen B N, Schlesinger P H and Baker N A 2009 J. Am. Chem. Soc. 131 4854-65
198. Chandler D E, Strümpfer J, Sener M, Scheuring S and Schulten K 2014 Biophys. J. 106 2503-10
199. Carpenter T, Bond P J, Khalid S and Sansom M S P 2008 Biophys. J. 95 3790-801
200. Sansom M S P, Scott K A and Bond P J 2008 Biochem. Soc. Trans. 36 27-32
201. Esteban-Martín S, Risselada H J, Salgado J and Marrink S J 2009 J. Chem. Theory Comput. 131 15194-202
202. Risselada H J and Marrink S J 2008 Proc. Natl Acad. Sci. USA 105 17367-72
203. Domański J, Marrink S J and Schäfer L V 2012 Biochim. Biophys. Acta: Biomembr. 1818 984-94
204. Johnston J M, Wang H, Provasi D and Filizola M 2012 PLoS Comput. Biol. 8 e1002649
205. Santo K P, Irudayam S J and Berkowitz M L 2013 J. Phys. Chem. B 117 5031-42
206. Leung A K K, Hafez I M, Baoukina S, Belliveau N M, Zhigaltsev I V, Afshinmanesh E, Tieleman D P, Hansen C L, Hope M J and Cullis P R 2012 J. Phys. Chem. C 116 18440-50
207. Risselada H J, Kutzner C and Grubmüller H 2011 ChemBioChem 12 1049-55
208. Murtola T, Vuorela T A, Hyvonen M T, Marrink S J, Karttunen M and Vattulainen I 2011 Soft Matter 7 8135-41
209. Santo K P and Berkowitz M L 2014 J. Chem. Phys. 140 054906
210. Wizert A, Iskander D R and Cwiklik L 2014 PLoS One 9 e92461
211. Srinivas G, Mohan R V and Kelkar A D 2013 J. Phys. Chem. B 117 12095-104
212. de Jong D H, Lopez C A and Marrink S J 2013 Faraday Discuss. 161 347-63
213. Pannuzzo M, Raudino A, Milardi D, La Rosa C and Karttunen M 2013 Sci. Rep. 3 2781
214. Gottwein E, Bodem J, Müller B, Schmechel A, Zentgraf H and Kräusslich H G 2003 J. Virol. 77 9474-85
215. Ayton G S, Noid W G and Voth G A 2007 Curr. Opin. Struct. Biol. 17 192-8
216. Midtgaard S R, Pedersen M C, Kirkensgaard J J K, Sorensen K K, Mortensen K, Jensen K J and Arleth L 2014 Soft Matter 10 738-52
217. Vácha R and Frenkel D 2014 Langmuir 30 4229-35
218. Kalli A C, Devaney I and Sansom M S P 2014 Biochemistry 53 1724-32
219. Pannuzzo M, De Jong D H, Raudino A and Marrink S J 2014 J. Chem. Phys. 140 124905
220. Rzepiela A J, Sengupta D, Goga N and Marrink S J 2010 Faraday Discuss. 144 431-43
221. Maurel D et al 2008 Nat. Methods 5 561-7
222. Kasai R S and Kusumi A 2014 Curr. Opin. Cell Biol. 27 78-86
223. Ghosh A, Sonavane U and Joshi R 2014 Comput. Biol. Chem. 48 29-39
224. Periole X, Knepp A M, Sakmar T P, Marrink S J and Huber T 2012 J. Am. Chem. Soc. 134 10959-65
225. Prasanna X, Chattopadhyay A and Sengupta D 2014 Biophys. J. 106 1290-300
226. Wassenaar T A, Ingólfsson H I, Böckmann R A, Tieleman D P and Marrink S J 2015 J. Chem. Theory Comput. 11 2144-55
227. Bassereau P et al 2014 Biophys. J. 102 234a
228. Chandler D E, Hsin J, Harrison C B, Gumbart J and Schulten K 2008 Biophys. J. 95 2822-36
229. Chandler D E, Gumbart J, Stack J D, Chipot C and Schulten K 2009 Biophys. J. 97 2978-84
230. Pannuzzo M, Raudino A and Böckmann R A 2014 J. Chem. Phys. 141 024901
231. Pande V S et al 2003 Biopolymers 68 91-109
232. Hall B A, Halim K B A, Buyan A, Emmanouil B and Sansom M S P 2014 J. Chem. Theory Comput. 10 2165-75
233. Wassenaar T A, Pluhackova K, Moussatova A, Sengupta D, Marrink S J, Tieleman D P and Böckmann R A 2015 J. Chem. Theory Comput. 11 2278-91
234. Dunton T A, Goose J E, Gavaghan D J, Sansom M S P and Osborne J M 2014 PLoS Comput. Biol. 10 e1003417
235. Pawar A B, Deshpande S A, Gopal S M, Wassenaar T A, Athale C A and Sengupta D 2015 Phys. Chem. Chem. Phys. 17 1390-8
236. Nikolaus J and Herrmann A 2012 Biol. Chem. 393 1231-45
237. Min D, Kim K, Hyeon C, Hoon Cho Y, Shin Y K and Yoon T Y 2013 Nat. Commun. 4 1705
238. Kasson P M and Pande V S 2007 PLoS Comput. Biol. 3 e220
239. Risselada H J, Bubnis G and Grubmüller H 2014 Proc. Natl Acad. Sci. USA 111 11043-8
240. Kawamoto S and Shinoda W 2014 Soft Matter 10 3048-54
241. Larsson P and Kasson P M 2013 PLoS Comput. Biol. 9 e1002950
242. Risselada H J, Marelli G, Fuhrmans M, Smirnova Y G, Grubmüller H, Marrink S J and Müller M 2012 PLoS One 7 e38302
243. Milovanovic D et al 2015 Nat. Commun. 6 5984
244. Hinsen K, Vaitinadapoule A, Ostuni M A, Etchebest C and Lacapere J J 2015 Biochim. Biophys. Acta: Biomembr. 1848 568-80