Specificity of helix packing in transmembrane dimer of the cell death factor BNIP3: A molecular modeling study

Proteins: Structure, Function and Genetics

Volumn 69, Issue 2, 2007, Pages 309-325

  Vereshaga, Yana A ^a   Volynsky, Pavel E ^a   Pustovalova, Julia E ^a,b   Nolde, Dmitry E ^a   Arseniev, Alexander S ^a   Efremov, Roman G ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

Author keywords

Apoptosis; Glycophorin A; Hydrophobicity mapping; Implicit explicit lipid bilayer; Membrane protein; Molecular dynamics; Monte Carlo method; Protein protein interactions

Indexed keywords

DIMER; HISTIDINE; PROTEIN BNIP3; SERINE;

AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; ARTICLE; CARBOXY TERMINAL SEQUENCE; HYDROGEN BOND; LIPID BILAYER; MOLECULAR DYNAMICS; MOLECULAR MODEL; MONTE CARLO METHOD; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF;

AMINO ACID SEQUENCE; APOPTOSIS REGULATORY PROTEINS; CELL DEATH; COMPUTER SIMULATION; GENE DELETION; GENE TARGETING; HISTIDINE; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MITOCHONDRIAL MEMBRANES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

EID: 34548757937     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21555     Document Type: Article

References (63)

1. Ubarretxena-Belandia I, Engelman DM. Helical membrane proteins: diversity of functions in the context of simple architecture. Curr Opin Struct Biol 2001;11:370-376.
2. Kolibaba KS, Druker BJ. Protein tyrosine kinase and cancer. Biochim Biophys Acta 1997;1333:F217-F248.
3. Li E, Hristova K. Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies. Biochemistry 2006;45:6241-6251.
4. Bennasroune A, Gardin A, Auzan C, Clauser E, Dirrig-Grosch S, Meira M, Appert-Collin A, Aunis D, Cremel G, Hubert P. Inhibition by transmembrane peptides of chimeric insulin receptors. Cell Mol Life Sci 2005;628:2124-2131.
5. Bennasroune A, Fickova M, Gardin A, Dirrig-Grosch S, Aunis D, Cremel G, Hubert P. Transmembrane peptides as inhibitors of ErbB receptor signaling. Mol Biol Cell 2004;15:3464-3474.
6. Bowie JU. Solving the membrane protein folding problem. Nature 2005;438:581-589.
7. Gerber D, Sal-Man N, Shai Y. Two motifs within a transmembrane domain, one for homodimerization and the other for heterodimerization. J Biol Chem 2004;279:21177-21182.
8. Tarasova NI, Seth R, Tarasov SG, Kosakowska-Cholody T, Hrycyna CA, Gottesman MM, Michejda CJ. Transmembrane inhibitors of P-glycoprotein, an ABC transporter. J Med Chem 2005;48:3768-3775.
9. Tarasova NI, Rice WG, Michejda CJ. Inhibition of G-protein-coupled receptor function by disruption of transmembrane domain interactions. J Biol Chem 1999;274:34911-34915.
10. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 1998;281:1322-1326.
11. Pinkoski MJ, Waterhouse NJ, Green DR. Mitochondria, apoptosis and autoimmunity. Curr Dir Autoimmun 2006;9:55-73.
12. Chen G, Ray R, Dubik D, Shi L, Cizeau J, Bleackley RC, Saxena S, Gietz RD, Greenberg AH. The E1B 19K/Bcl-2-binding protein Nip3 is a dimeric mitochondrial protein that activates apoptosis. J Exp Med 1997;186:1975-1983.
13. Ray R, Chen G, Vande Velde C, Cizeau J, Park JH, Reed JC, Gietz RD, Greenberg AH. BNIP3 heterodimerizes with Bcl-2/Bcl-XL and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J Biol Chem 2000;275:1439-1448.
14. Vande Velde C, Cizeau J, Dubik D, Alimonti J, Brown T, Israels S, Hakem R, Greenberg AH. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 2000;20:5454-5468.
15. Lee H, Paik SG. Regulation of BNIP3 in normal and cancer cells. Mol Cells 2006;21:1-6.
16. Kubasiak LA, Hernandez OM, Bishopric NH, Webster KA. Hypoxia and acidosis activate cardiac myocyte death through the Bcl-2 family protein BNIP3. Proc Natl Acad Sci USA 2002;99:12825-12830.
17. Graham RM, Frazier DP, Thompson JW, Haliko S, Li H, Wasserlauf BJ, Spiga MG, Bishopric NH, Webster KA. A unique pathway of cardiac myocyte death caused by hypoxia-acidosis. J Exp Biol 2004;207:3189-3200.
18. Hinds MG, Lackmann M, Skea GL, Harrison PJ, Huang DC, Day CL. The structure of Bcl-w reveals a role for the C-terminal residues in modulating biological activity. EMBO J 2003;22:1497-1507.
19. Chen G, Cizeau J, Vande Velde C, Park JH, Bozek G, Bolton J, Shi L, Dubik D, Greenberg A. Nix and Nip3 form a subfamily of pro-apoptotic mitochondrial proteins J Biol Chem 1999;274:7-10.
20. Sulistijo ES, Jaszewski TM, MacKenzie KR. Sequence-specific dimerization of the transmembrane domain of the "BH3-only" protein BNIP3 in membranes and detergent. J Biol Chem 2003;278:51950-51956.
21. Regula KM, Ens K, Kirshenbaum LA. Inducible expression of BNIP3 provokes mitochondrial defects and hypoxia-mediated cell death of ventricular myocytes. Circ Res 2002;91:226-231.
22. Lamy L, Ticchioni M, Rouquette-Jazdanian AK, Samson M, Deckert M, Greenberg AH, Bernard A. CD47 and the 19 kDa interacting protein-3 (BNIP3) in T cell apoptosis. J Biol Chem 2003;278:23915-23921.
23. Sulistijo ES, MacKenzie KR. Sequence dependence of BNIP3 transmembrane domain dimerization implicates side-chain hydrogen bonding and a tandem GxxxG motif in specific helix-helix interactions. J Mol Biol 2006;364:974-990.
24. Kim S, Jeon TJ, Oberai A, Yang D, Schmidt JJ, Bowie JU. Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc Natl Acad Sci USA 2005;102:14278-14283.
25. Russ WP, Engelman DM. The GxxxG motif: a framework for transmembrane helix-helix association. J Mol Biol 2000;296:911-919.
26. Senes A, Engel DE, DeGrado WF. Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol 2004;14:465-479.
27. Torres J, Stevens TJ, Samson M. Membrane proteins: the 'Wild West' of structural biology. Trends Biochem Sci 2003;28:137-144.
28. Treutlein HR, Lemmon MA, Engelman DM, Brünger AT. Helix-helix interactions inside lipid bilayers. Biochemistry 1992;31:12726-12732.
29. Adams PD, Engelman DM, Brünger AT. An improved prediction for the structure of the dimeric transmembrane domain of Glycophorin A obtained through global searching. Proteins 1996;26:257-261.
30. Ducarme P, Thomas A, Brasseur R. The optimization of the helix/helix interaction of a transmembrane dimer is improved by the IMPALA restraint field. Biochim Biophys Acta 2000;1509:148-154.
31. Im W, Feig M, Brooks III CL. An implicit membrane generalized Born theory for the study of structure, stability and interactions of membrane proteins. Biophys J 2003;85:2900-2918.
32. Mottamal M, Zhang J, Lazaridis T. Energetics of the native and non-native states of the glycophorin transmembrane helix dimer. Proteins 2006;62:996-1009.
33. MacKenzie KR, Prestegard JH, Engelman DM. A transmembrane helix dimer: structure and implications. Science 1997;276:131-133.
34. Smith SO, Song D, Shekar S, Groesbeek M, Ziliox M, Aimoto S. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry 2001;40:6553-6558.
35. Lemmon MA, Flangan JM, Treutlein HR, Zhang J, Engelman DM. Sequence specificity in the dimerization of transmembrane α-helices. Biochemistry 1992;31:12719-12725.
36. Finger C, Volkmer T, Prodohl A, Otzen DE, Engelman DM, Schneider D. The stability of transmembrane helix interactions measured in a biological membrane. J Mol Biol 2006;358:1221-1228.
37. Fisher LE, Engelman DM, Sturgis JN. Detergents modulate dimerization, but not helicity, of the glycophorin a transmembrane domain. J Mol Biol 1999;293:639-651.
38. Vereshaga YA, Volynsky PE, Nolde DE, Arseniev AS, Efremov RG. Helix interactions in membranes: lessons from unrestrained Monte Carlo simulations. J Chem Theory Comput 2005;1:1252-1264.
39. Efremov RG, Vereshaga YA, Volynsky PE, Nolde DE, Arseniev AS. Association of transmembrane helices: what determines assembling of a dimer? J Comput-Aided Mol Des 2006;20:27-45.
40. Efremov RG, Nolde DE, Konshina AG, Syrtcev NP, Arseniev AS. Peptides and proteins in membranes: what can we learn via computer simulations? Curr Med Chem 2004;11:2421-2442.
41. Braun R, Engelman DM, Schulten K. Molecular dynamics simulations of micelle formation around dimeric glycophorin A transmembrane helices. Biophys J 2004;87:754-763.
42. Ash WL, Stockner T, MacCallum JL, Tieleman DP. Computer modeling of polyleucine-based coiled coil dimers in a realistic membrane environment: insight into helix-helix interactions in membrane proteins. Biochemistry 2004;43:9050-9060.
43. Samna Soumana O, Aller P, Garnier N, Genest M. Transmembrane peptides from tyrosine kinase receptor. Mutation-related behavior in a lipid bilayer investigated by molecular dynamics simulations. J Biomol Struct Dyn 2005;23:91-100.
44. Orekhov VY, Abdulaeva GV, Musina LY, Arseniev AS. 1H-15N-NMR studies of bacteriorhodopsin Halobacterium halobium. Conformational dynamics of the four-helical bundle. Eur J Biochem 1992;210:223-229.
45. Gratkowski H, Dai QH, Wand AJ, DeGrado WF, Lear JD. Cooperativity and specificity of association of a designed transmembrane peptide. Biophys J 2002;83:1613-1619.
46. Stockner T, Ash WL, MacCallum JL, Tieleman DP. Direct simulation of transmembrane helix association: role of asparagines. Biophys J 2004;87:1650-1656.
47. Efremov RG, Nolde DE, Vergoten G, Arseniev AS. A solvent model for simulations of peptides in bilayers. I. Membrane-promoting α-helix formation. Biophys J 1999;76:2448-2459.
48. Nemethy G, Pottle MS, Scheraga HA. Energy parameters in polypeptides, 9: updating of geometrical parameters, non-bonding interactions and hydrogen bonding interactions for naturally occuring amino acids. J Phys Chem 1983;87:1883-1887.
49. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577-2637.
50. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. GROMACS: fast, flexible, and free. J Comput Chem 2005;26:1701-1718.
51. Berger O, Edholm O, Jahnig F. Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys J 1997;72:2002-2013.
52. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
53. Berendsen HJC, Postma JPM, Gunsteren WF van, Hermans J. Interaction models for water in relation to protein hydration. In: Jerusalem Symposia on Quantum Chemistry and Biochemistry 1981, Reidel, Dordrecht, Holland, pp 331-342.
54. Volynsky PE, Polyansky AA, Simakov NA, Arseniev AS, Efremov RG. Effect of lipid composition on the "membrane response" induced by a fusion peptide. Biochemistry 2005;44:14626-14637.
55. Efremov RG, Vergoten G. The hydrophobic nature of membrane-spanning α-helices as revealed by Monte Carlo simulations and molecular hydrophobicity potential analysis. J Phys Chem 1995;99:10658-10666.
56. Weiss TM, van der Wel PC, Killian JA, Koeppe RE 2nd, Huang HW. Hydrophobic mismatch between helices and lipid bilayers. Biophys J 2003;84:379-385.
57. Granseth G, von Heijne G, Elofsson A. A Study of the membrane-water interface region of membrane proteins. J Mol Biol 2005;346:377-385.
58. Popot JL, Engelman DM. Membrane protein folding and oligomerization: the two-stage model. Biochemistry 1990;29:4031-4037.
59. Wales DJ, Scheraga HA. Global optimization of clusters, crystals, and biomolecules. Science 1999;285:1368-1372.
60. Adamian L, Liang J. Interhelical hydrogen bonds and spatial motifs in membrane proteins: polar clamps and serine zippers. Proteins 2002;47:209-218.
61. Kass I, Arkin IT. How pH opens a H+ channel: the gating mechanism of influenza A M2. Structure 2005;13:1789-1798.
62. Chanchevalap S, Yang Z, Cui N, Qu Z, Zhu G, Liu C, Giwa LR, Abdulkadir L, Jiang C. Involvement of histidine residues in proton sensing of ROMK1 channel. J Biol Chem 2000;275:7811-7817.
63. Padanilam BJ, Lu T, Hoshi T, Padanilam BA, Shibata EF, Lee HC. Molecular determinants of intracellular pH modulation of human Kv1 4 N-type inactivation. Mol Pharmacol 2002;62:127-134.