Monte Carlo simulations of tBid association with the mitochondrial outer membrane

European Biophysics Journal

Volumn 37, Issue 1, 2007, Pages 19-33

  Veresov, Valery G ^a   Davidovskii, Alexander I ^a  

^a INSTITUTE OF PHOTOBIOLOGY   (Belarus)

Author keywords

Apoptosis; Bid; Cardiolipin; Mitochondria; Protein insertion

Indexed keywords

PROTEIN BID;

ARTICLE; ENERGY TRANSFER; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE; PROTEIN CONFORMATION;

BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BINDING SITES; COMPUTER SIMULATION; MEMBRANE FLUIDITY; MITOCHONDRIAL MEMBRANES; MODELS, CHEMICAL; MODELS, MOLECULAR; MONTE CARLO METHOD; PROTEIN BINDING; PROTEIN CONFORMATION;

BACTERIA (MICROORGANISMS);

EID: 36348946916     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-007-0149-z     Document Type: Article

References (108)

1. Adams JM (2003) Ways of dying: multiple pathways of apoptosis. Genes Dev 172:2481-2495
2. Allen MP, Tildesley DJ (1987) Computer simulations of liquids. Oxford, Clarendon
3. Annis MG, Soucie EL, Dlugosz PJ, Cruz-Aguado JC, Penn LZ, Leber B, Andrews DW (2005) Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis. EMBO J 24:2096-2103
4. Antonsson B, Montessuit S, Lauper S, Eskes R, Martinou JC (2000) Bax oligomerization is required for channel-forming activity in liposomes and to trigger cytochrome c release from mitochondria. Biochem J 345:271-278
5. Ardail D, Privat J-P, Egret-Charlier M, Levrat C, Lerme F, Louisot P (1990) Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem 265:18797-18802
6. Ash WL, Zlomislic MR, Oloo EQ, Tieleman DP (2004) Computer simulations of membrane proteins. Biochim Biophys Acta 1666:158-189
7. Basanez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM, Zimmerberg J (2002) Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 277:49360-49365
8. Baumgartner A (1996) Insertion and hairpin formation of membrane proteins: a Monte Carlo study. Biophys J 71:1248-1255
9. Belzacq AS, Vieira HL, Verrier F, Vandescasteele G, Cohen I, Prevost MC, Larquet E, Pariselli F, Petit PX, Kahn A, Rizzutto R, Brenner C, Kroemer C (2003) Bcl-2 and Bax modulate adenine nucleotides translocase activity. Cancer Res 63:541-546
10. Benz R, Kottke M, Brdiczka D (1990) The cationically selective state of the mitochondrial outer membrane pore: a study with intact mitochondria and reconstituted mitochondrial porin. Biochim Biophys Acta 1022:311-318
11. Bond PJ, Sansom MS (2004) The simulation approach to bacterial outer membrane proteins. Mol Membr Biol 21:151-161
12. Bond PJ, Sansom MS (2006) Insertion and assembly of membrane protein via simulation. J Am Chem Soc 128:2697-2704
13. Bychkova VE, Dujsekina AE, Klenin SI, Tiktopulo EI, Uversky VN, Ptitsyn OB (1996) Molten globule like state of cytochrome c under conditions simulating those near the membrane surface. Biochemistry 35:6058-6063
14. Chenal A, Savarin P, Nizard P, Guillain F, Gillet D, Forge V (2002) Membrane protein insertion regulated by bringing electrostatic and hydrophobic interactions into play. A case study with the translocation domain of diphtheria toxin. J Biol Chem 277:43425-43432
15. Choe S, Bennett MJ, Fujii G, Curmi PM, Kantardjieff KA, Collier RJ, Eisenberg D (1992) The crystal structure of diphtheria toxin. Nature 357:216-222
16. Chou J, Li H, Salvesen G, Yuan J, Wagner G (1999) Solution structure of Bid, an intracellular amplifier of apoptopic signaling. Cell 96:615-624
17. Chang G, Guida WC, Still WC (1989) An internal coordinate Monte-Carlo method for searching conformational space. J Am Chem Soc 111:4379-4386
18. Cory S, Huang DC, Adams JM (2003) The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22:8590-8607
19. Cramer WA, Heimann JB, Shendel SL, Deriy BN, Cohen FS, Etkins PA, Stauffacher CV (1995) Structure-function of the channel-forming colicins. Annu Rev Biophys Biomol Struct 24:611-641
20. Daniel NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116:205-219
21. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B, Martinou JC (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 144:891-901
22. Ducarme P, Rahman M, Brasseur R (1998) IMPALA: a simple restraint field to simulate the biological membranes in molecular structure studies. Proteins 30:357-371
23. Dunfield LG, Burgess AW, Scheraga HA (1978) Energy parameters in polypeptides. 8. Empirical potential energy algorithm for the conformational analysis of large molecules. J Phys Chem 82:2609-2616
24. Efremov RG, Nolde DE, Vergoten G, Arseniev AS (1999a) A solvent model for simulations of peptides in bilayers. I. Membrane-promoting α-helix formation. Biophys J 76:2448-2459
25. Efremov RG, Nolde DE, Vergoten G, Arseniev AS (1999b) A solvent model for simulations of peptides in bilayers. II. Membrane-spanning α-helices. Biophys J 76:2460-2471
26. Efremov RG, Volynsky PE, Nolde DE, Dubovskii PV, Arseniev AS (2002) Interaction of cardiotoxins with membranes: a molecular modeling study. Biophys J 83:144-153
27. Epand RM, Vogel HJ (1999) Diversity of antimicrobial peptides and their mechanisms of ac tion. Biochim Biophys Acta 1462:11-28
28. Epand RF, Martinou J-C, Fornallaz-Mulhauser M, Hughes DW, Epand RM (2002a) The apoptotic protein tBid promotes leakage by altering membrane curvature. J Biol Chem 277:32632-32639
29. Epand RF, Martinou J-C, Montessuit S, Epand RM, Yip CM (2002b) Direct evidence for membrane pore formation by the apoptotic protein Bax. Biochem Biophys Res Commun 298:744-749
30. Eskes R, Desagher S, Antonsson B, Martinou J-C (2000) Bid induces the oligomerization and insertion of BAX into the outer mitochondrial membrane. Mol Cell Biol 20:929-935
31. Forsten KE, Kosack RE, Lauffenburger DA, Subramanian (1994) Numerical solution of nonlinear Poisson-Boltzmann equation for a membrane electrolyte system. J Phys Chem 98:5580-5586
32. Fraczkiewicz R, Braun W (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J Comp Chem 19:319-333
33. Franzin CM, Choi J, Zhai J, Reed D, Marassi FM (2004) Structural studies of apoptosis and ion transport regulatory proteins in membranes. Magn Reson Chem 42:172-179
34. L, Bax, and Bid. Biochemistry 43:10930-10943
35. Garcia-Saez A, Coraiola M, Dalla Serra M, Mingarro I, Muller P, Salgado J (2006) Peptides corresponding to helices 5 and 6 of BAX can independently form lipid pores. FEBS J 273:971-981
36. Gong X-M, Choi J, Franzin CM, Zhai D, Reed JC, Marassi FM (2004) Conformation of membrane-associated proapoptopic tBid. J Biol Chem 279:28954-28960
37. Grinberg M, Sarig R, Zaltsman Y, Frumkin D, Grammatikakis N, Reuveny E, Gross A (2002) tBID homooligomerizes in the mitochondrial membrane to induce apoptosis. J Biol Chem 277:12237-12245
38. Gross A, McDonnel JM, Korsemeyer SJ (1999a) BCL-2 family members and the mitochondria in apoptosis. Genes Dev 13:1899-1911
39. L prevents this release but not tumor necrosis factor R1/FAS death. J Biol Chem 274:1156-1163
40. Gumbart J, Wang Y, Aksimentiev A, Tajkhotshid E, Schulten K (2005) Molecular dynamics simulations of proteins in lipid bilayers. Curr Opin Struct Biol 15:423-431
41. Holm L, Park J (2000) DaliLite workbench for protein structure comparison. Bioinformatics 16:566-567
42. Huang HW, Chen FY, Lee MT (2004) Molecular mechanism of peptide-induced pores in membranes. Phys Rev Lett 92:198304
43. Huang HW (2006) Molecular mechanism of antimicrobial peptides. The origin of cooperativity. Biochim Biophys Acta 1758:1292-1302
44. Kessel A, Shental-Bechor D, Haliloglu T, Ben-Tal N (2003) Interaction of hydrophobic peptides with lipid bilayers: Monte Carlo simulations with M2δ. Biophys J 85:3431-3444
45. Kim TH, Zhao Y, Ding WX, Shin JN, He X, Seo YW, Chen J, Rabinowich H, Amoscato AA, Yin XM (2004) Bid-cardiolipin interaction at Mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome c release. Mol Biol Cell 15:3061-3072
46. Kirkpatrick S, Gelati CD, Vecchi MP (1983) Optimization by simulated annealing. Science 220:671-680
47. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH (2000) Pro-apoptopic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 7:1166-1173
48. Kudla G, Montessuit S, Eskes R, Berrier C, Martinou JC, Gazi A, Antonsson B (2000) The destabilization of lipid membranes induced by the C-terminal fragment of caspase 8-cleaved bid is inhibited by the N-terminal fragment. J Biol Chem 275:22713-22718
49. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR, Newmeyer DD (2002) Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111:331-342
50. Lazaridis T (2005) Implicit solvent simulations of peptide interactions with anionic lipid membranes. Proteins 58:518-527
51. Lesieur C, Vecsey-Semjen B, Abrami L, Fivaz M, van der Goot FG (1997) Membrane insertion: the strategies of toxins. Mol Membr Biol 14:45-64
52. Lee J, Scheraga HA, Rackovsky S (1997) New optimization method for conformational energy calculations on polypeptides: conformational space annealing. J Comput Chem 18:1222-1232
53. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ (2002) Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell 2:183-192
54. Li Z, Scheraga HA (1987) Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc Natl Acad Sci USA 84:6611-6615
55. Li H, Zhu H, Xu CJ, Yuan J (1998) Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94:491-501
56. London E (1992) Diphtheria toxins: membrane interaction and membrane translocation. Biochim Biophys Acta 1113:25-51
57. Lu JX, Damodaran K, Blazyk J, Lorigan GA (2005) Solid-state nuclear magnetic resonance relaxation studies of the interaction mechanism of antimicrobial peptides with phospholipid bilayer membranes. Biochemistry 44:10208-10217
58. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X (1998) Bid, a Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94:481-490
59. Lutter M, Fang M, Lun X, Nishijima M, Xie M, Wang X (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol 2:754-761
60. Maddox MW, Longo ML (2002) A Monte Carlo study of peptide insertion into lipid bilayers: equilibrium conformations and insertion mechanisms. Biophys J 82:244-263
61. Matsuzaki K (1999) Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tacheplysins as archetypes. Biochim Biophys Acta 1452:1-10
62. Mau NV, Kajava AV, Bonfils C, Martinou J-C, Harricane M-C (2006) Interactions of Bax and tBid with lipid monolayers. J Membr Biol 207:1-9
63. McDonnel J, Fushman D, Milliman C, Korsmeyer S, Cowburn D (1999) Solution structure of the proapoptopic molecule BID: a structural basis for apoptopic agonists and antagonists. Cell 96:625-634
64. McLaughlin S (1989) The electrostatic properties of membranes. Annu Rev Biophys Biophys Chem 18:113-136
65. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller EJ (1953) Equation of state calculations by fast computing machines. J Chem Phys 21:1087-1092
66. Milik M, Skolnick J (1993) Insertion of peptide chains into lipid membranes: an off-lattice Monte Carlo dynamics model. Proteins 15:10-25
67. Milik M, Skolnick J (1995) Monte Carlo model of FD and PF1 coat proteins in lipid membranes. Biophys J 69:1382-1386
68. Muchmore SW, Sattler M, Liang H, Meadows RP, Harian JE, Yoon JE, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL, Fesic SW (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381:335-341
69. Mungikar AA, Forciniti D (2004) Conformational changes of peptides at solid/liquid interfaces: a Monte Carlo study. Biomacromolecules 5:2147-2159
70. Nam GH, Choi KY (2002) Association of human tumor necrosis factor-related apoptosis inducing ligand with membrane upon acidification. Eur J Biochem 269:5280-5287
71. Nelson AP, Colonomos P, McQuarrie DA (1975) Electrostatic coupling across a membrane with titratable surface groups. J Theor Biol 50:317-325
72. Némethy G, Pottle MS, Scheraga HA (1983) Energy parameters in polypeptides. 9. Updating of geometrical parameters, nonbonded interactions, and hydrogen bond interactions for the naturally occurring amino acids. J Phys Chem 87:1883-1887
73. Némethy G, Gibson KD, Palmer KA, Yoon CN, Paterlini G, Zagari A, Rumsey S, Scheraga HA (1992) Energy parameters in polypeptides. 10. Improved geometrical parameters and nonbonded interactions for use in ECEPP/3 algorithm with application to proline-containing peptides J Phys Chem 96:6472-6484
74. Oh KJ, Barbuto S, Meyer N, Kim R-S, Collier RJ, Korsmeyer SJ (2005) Conformational changes in BID, a pro-apoptopic BCL-2 family member, upon membrane binding. J Biol Chem 280:753-767
75. Opferman JT, Korsmeyer SJ (2003) Apoptosis in the development and maintenance of the immune system. Nat Immunol 4:410-415
76. Oshima H, Kondo T (1988) Membrane potential and Donnan potential. Biophys Chem 29:277-281
77. Ozkan SB, Meirovitch H (2004) Conformational search of peptides and proteins: Monte Carlo minimization with an adaptive bias method applied to the heptapeptide deltorphin. J Comput Chem 25:565-572
78. Peitzsch RM, Eisenberg M, Sharp KA, McLaughlin S (1995) Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys J 68:729-738
79. Petros AM, Oleiniczak ET, Fesik SW (2004) Structural biology of the Bcl-2 family of proteins. Biochim Biophys Acta 1644:83-94
80. Pillardy J, Czaplewski C, Wedemeyer WJ, Scheraga HA (2000) Conformation-family Monte Carlo (CFMC): an efficient computational method for identifying the low-energy states of a macromolecule. Helv Chim Acta 83:2214-2230
81. Pillardy J, Arnautova YA, Czaplewski C, Gibson KD, Scheraga HA (2001) Conformation-family Monte Carlo: a new method for crystal structure prediction. Proc Natl Acad Sci USA 98:12351-12356
82. Rosconi MP, Zhao G, London E (2004) Analyzing topography of membrane-inserted diphtheria toxin T domain using BODIPY-streptavidin: at low pH, helices 8 and 9 form a transmembrane hairpin but helices 5-7 form stable nonclassical inserted segments on the cis side of the bilayer. Biochemistry 43:9127-9139
83. Roseman MA (1988) Hydrophobicity of polar amino acid side chains is markedly reduced by flanking peptide bonds. J Mol Biol 200:513-522
84. Schendel SL, Azimov R, Pawlowski K, Godzik A, Kagan BL, Reed JC (1999) Ion channel activity of the BH3 only BCL-2 family member. BID J Biol Chem 274:21932-21936
85. Schlame M, Rua D, Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39:257-288
86. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannela CA, Korsmeyer SJ (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell 2:55-67
87. Sintes T, Baumgartner A (1998) Membrane-mediated protein attraction. A Monte Carlo study. Physica A 249:571-575
88. Sperotto MM, May S, Baumgaertner A (2006) Modelling of proteins in membranes. Chem Phys Lipids 141:2-29
89. Stroud RM, Reiling K, Wiener M, Freymann D (1998) Ion-channel forming colicins. Curr Opin Struct Biol 8:525-533
90. Sung S-S (1994) Helix folding simulations with various initial conformations. Biophys J 66:1796-1803
91. Sung S-S (1995) Folding simulations of alanine-based peptides with lysine residues. Biophys J 68:1796-1803
92. Terrones O, Antonsson B, Yamaguchi H, Wang HG, Liu J, Lee RM, Herrmann A, Basanez G (2004) Lipidic pore formation by the concerted action of proapoptopic BAX and tBid. J Biol Chem 279:30081-30091
93. Tzlil S, Ben-Schaul A (2005) Flexible charged molecules on mixed fluid lipid membranes: theory and Monte Carlo simulations. Biophys J 88:2391-2402
94. van der Goot FG, Gonzalez-Manas JM, Lakey JH, Pattus F (1991) A "molten-globule" membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354:408-410
95. Varfolomeev EE, Ashkenazi A (2004) Tumor necrosis factor: an apoptosis JuNKie? Cell 116:491-497
96. Vogt B, Ducarme P, Schinzel S, Brasseur R, Bechinger B (2000) The topology of lysine-containing amphipathic peptides in bilayers by circular dichroism, solid-state NMR, and molecular modeling. Biophys J 79:2644-2656
97. Wang X (2001) The expanding role of mitochondria in apoptosis. Genes Dev 15:2922-2933
98. Wang K, Yin XM, Chao DT, Milliman CL, Korsmeyer SJ (1996) Bid: a novel BH3 domain-only death agonist. Genes Dev 10:2859-2869
99. Wei MC, Lindsen T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsemeyer SJ (2000) tBid, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14:2060-2071
100. Wei MC, Zong WX, Cheng EH, Lindsten T, Panautsakoupolo V, Ross AJ, Roth KA, McGregor GR, Thompson CB, Korsmayer SJ (2001) Proapoptotic Bax and Bak: a requisite gateway to mitochondrial dysfunction and death. Science 292:727-730
101. Willis SN, Adams JM (2005) Life in the balance: how BH3-only proteins induce apoptosis. Curr Opin Cell Biol 17:617-625
102. Winterhalter M, Helfrich W (1992) Bending elacticity of electrically charged bilayers: coupled monolayers, neutral surfaces, and balancing stresses. J Phys Chem 96:327-330
103. Yamaguchi S, Huster D, Waring A, Lehrer RI, Kearney W, Tack BF, Hong M (2001) Orientation and dynamics of an antimicrobial peptide in the lipid bilayer by solid-state NMR spectroscopy. Biophys J 81:2203-2214
104. Yin X-M (2006) Bid, a BH3-only multi-functional molecule, is at the cross road of life and death. Gene 369:7-19
105. Zakharov SD, Cramer WA (2002) Colicin crystal structures: pathways and mechanisms for colicin insertion into membranes. Biochim Biophys Acta 1565:333-346
106. Zemel A, Ben-Shaul A, May S (2004) Membrane perturbation induced by interfacially adsorbed peptides. Biophys J 86:3607-3619
107. Zha J, Weiler S, Oh KJ, Wei MC, Korsemeyer SJ (2000) Posttranslational N-Myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290:1761-1765
108. Zhan L, Chen JZY, Liu W-K (2006) Monte Carlo basin paving: an improved global optimization method. Phys Rev E 73:015701 (1-4)