Adaptable Lipid Matrix Promotes Protein-Protein Association in Membranes

Journal of Chemical Theory and Computation

Volumn 11, Issue 9, 2015, Pages 4415-4426

  Kuznetsov, Andrey S ^a   Polyansky, Anton A ^a,b   Fleck, Markus ^b   Volynsky, Pavel E ^a   Efremov, Roman G ^a,c  

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

^b MAX F PERUTZ LABORATORIES   (Austria)

^c NATIONAL RESEARCH UNIVERSITY HIGHER SCHOOL OF ECONOMICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPHORIN; LIPID; LIPID BILAYER; PEPTIDE; POLYALANINE; POLYLEUCINE; PROTEIN BINDING;

CHEMISTRY; LIPID BILAYER; MOLECULAR DYNAMICS; THERMODYNAMICS;

GLYCOPHORIN; LIPID BILAYERS; LIPIDS; MOLECULAR DYNAMICS SIMULATION; PEPTIDES; PROTEIN BINDING; THERMODYNAMICS;

EID: 84941088938     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/acs.jctc.5b00206     Document Type: Article

References (63)

1. Bergsagel, P. L.; Chesi, M. V. Molecular Classification and Risk Stratification of Myeloma Hematol. Oncol. 2013, 31, 38-41 10.1002/hon.2065
2. Al Hussain, T. O.; Akhtar, M. Molecular Basis of Urinary Bladder Cancer Adv. Anat. Pathol. 2013, 20, 53-60 10.1097/PAP.0b013e31827bd0ec
3. Nikonov, A. V.; Kreibich, G. Organization of Translocon Complexes in ER Membranes Biochem. Soc. Trans. 2003, 31, 1253-1256 10.1042/BST0311253
4. Fleming, K. G. Energetics of Membrane Protein Folding Annu. Rev. Biophys. 2014, 43, 233-255 10.1146/annurev-biophys-051013-022926
5. Nyathi, Y.; Wilkinson, B. M.; Pool, M. R. Co-Translational Targeting and Translocation of Proteins to the Endoplasmic Reticulum Biochim. Biophys. Acta, Mol. Cell Res. 2013, 1833, 2392-2402 10.1016/j.bbamcr.2013.02.021
6. Schlebach, J. P.; Sanders, C. R. The Safety Dance: Biophysics of Membrane Protein Folding and Misfolding in a Cellular Context Q. Rev. Biophys. 2015, 48, 1-34 10.1017/S0033583514000110
7. Jura, N.; Endres, N. F.; Engel, K.; Deindl, S.; Das, R.; Lamers, M. H.; Wemmer, D. E.; Zhang, X.; Kuriyan, J. Mechanism for Activation of the EGF Receptor Catalytic Domain by the Juxtamembrane Segment Cell 2009, 137, 1293-1307 10.1016/j.cell.2009.04.025
8. Bae, J. H.; Schlessinger, J. Asymmetric Tyrosine Kinase Arrangements in Activation or Autophosphorylation of Receptor Tyrosine Kinases Mol. Cells 2010, 29, 443-448 10.1007/s10059-010-0080-5
9. MacKenzie, K. R.; Prestegard, J. H.; Engelman, D. M. A Transmembrane Helix Dimer: Structure and Implications Science 1997, 276, 131-133 10.1126/science.276.5309.131
10. Bocharov, E. V.; Lesovoy, D. M.; Goncharuk, S. A.; Goncharuk, M. V.; Hristova, K.; Arseniev, A. S. Structure of FGFR3 Transmembrane Domain Dimer: Implications for Signaling and Human Pathologies Structure 2013, 21, 2087-2093 10.1016/j.str.2013.08.026
11. Mineev, K. S.; Lesovoy, D. M.; Usmanova, D. R.; Goncharuk, S. A.; Shulepko, M. A.; Lyukmanova, E. N.; Kirpichnikov, M. P.; Bocharov, E. V.; Arseniev, A. S. NMR-Based Approach to Measure the Free Energy of Transmembrane Helix-helix Interactions Biochim. Biophys. Acta, Biomembr. 2014, 1838, 164-172 10.1016/j.bbamem.2013.08.021
12. Bocharov, E. V.; Mayzel, M. L.; Volynsky, P. E.; Mineev, K. S.; Tkach, E. N.; Ermolyuk, Y. S.; Schulga, A. A.; Efremov, R. G.; Arseniev, A. S. Left-Handed Dimer of EphA2 Transmembrane Domain: Helix Packing Diversity among Receptor Tyrosine Kinases Biophys. J. 2010, 98, 881-889 10.1016/j.bpj.2009.11.008
13. Bocharov, E. V.; Mineev, K. S.; Goncharuk, M. V.; Arseniev, A. S. Structural and Thermodynamic Insight into the Process of "weak" Dimerization of the ErbB4 Transmembrane Domain by Solution NMR Biochim. Biophys. Acta, Biomembr. 2012, 1818, 2158-2170 10.1016/j.bbamem.2012.05.001
14. Endres, N. F.; Das, R.; Smith, A. W.; Arkhipov, A.; Kovacs, E.; Huang, Y.; Pelton, J. G.; Shan, Y.; Shaw, D. E.; Wemmer, D. E.; Groves, J. T.; Kuriyan, J. Conformational Coupling across the Plasma Membrane in Activation of the EGF Receptor Cell 2013, 152, 543-556 10.1016/j.cell.2012.12.032
15. Engelman, D. M.; Adair, B. D.; Brünger, A.; Flanagan, J. M.; Hunt, J. F.; Lemmon, M. A.; Treutlein, H.; Zhang, J. Dimerization of Glycophorin A Transmembrane Helices: Mutagenesis and Modeling Soc. Gen. Physiol. Ser. 1993, 48, 11-21
16. Fleming, K. G.; Engelman, D. M. Specificity in Transmembrane Helix-Helix Interactions Can Define a Hierarchy of Stability for Sequence Variants Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 14340-14344 10.1073/pnas.251367498
17. Vereshaga, Y. A.; Volynsky, P. E.; Nolde, D. E.; Arseniev, A. S.; Efremov, R. G. Helix Interactions in Membranes: Lessons from Unrestrained Monte Carlo Simulations J. Chem. Theory Comput. 2005, 1, 1252-1264 10.1021/ct0501250
18. Polyansky, A. A.; Volynsky, P. E.; Efremov, R. G. Multistate Organization of Transmembrane Helical Protein Dimers Governed by the Host Membrane J. Am. Chem. Soc. 2012, 134, 14390-14400 10.1021/ja303483k
19. Volynsky, P. E.; Polyansky, A. A.; Fakhrutdinova, G. N.; Bocharov, E. V.; Efremov, R. G. Role of Dimerization Efficiency of Transmembrane Domains in Activation of Fibroblast Growth Factor Receptor 3 J. Am. Chem. Soc. 2013, 135, 8105-8108 10.1021/ja4011942
20. Polyansky, A. A.; Chugunov, A. O.; Volynsky, P. E.; Krylov, N. A.; Nolde, D. E.; Efremov, R. G. PREDDIMER: A Web Server for Prediction of Transmembrane Helical Dimers Bioinformatics 2014, 30, 889-890 10.1093/bioinformatics/btt645
21. Hénin, J.; Pohorille, A.; Chipot, C. Insights into the Recognition and Association of Transmembrane Alpha-Helices. The Free Energy of Alpha-Helix Dimerization in Glycophorin A J. Am. Chem. Soc. 2005, 127, 8478-8484 10.1021/ja050581y
22. MacKenzie, K. R.; Engelman, D. M. Structure-Based Prediction of the Stability of Transmembrane Helix-Helix Interactions: The Sequence Dependence of Glycophorin A Dimerization Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 3583-3590 10.1073/pnas.95.7.3583
23. Park, S.; Im, W. Two Dimensional Window Exchange Umbrella Sampling for Transmembrane Helix Assembly J. Chem. Theory Comput. 2013, 9, 13-17 10.1021/ct3008556
24. Melnyk, R. A.; Kim, S.; Curran, A. R.; Engelman, D. M.; Bowie, J. U.; Deber, C. M. The Affinity of GXXXG Motifs in Transmembrane Helix-Helix Interactions Is Modulated by Long-Range Communication J. Biol. Chem. 2004, 279, 16591-16597 10.1074/jbc.M313936200
25. Doura, A. K.; Kobus, F. J.; Dubrovsky, L.; Hibbard, E.; Fleming, K. G. Sequence Context Modulates the Stability of a GxxxG-Mediated Transmembrane Helix-Helix Dimer J. Mol. Biol. 2004, 341, 991-998 10.1016/j.jmb.2004.06.042
26. Cymer, F.; Veerappan, A.; Schneider, D. Transmembrane Helix-Helix Interactions Are Modulated by the Sequence Context and by Lipid Bilayer Properties Biochim. Biophys. Acta, Biomembr. 2012, 1818, 963-973 10.1016/j.bbamem.2011.07.035
27. Mineev, K. S.; Khabibullina, N. F.; Lyukmanova, E. N.; Dolgikh, D. A.; Kirpichnikov, M. P.; Arseniev, A. S. Spatial Structure and Dimer-monomer Equilibrium of the ErbB3 Transmembrane Domain in DPC Micelles Biochim. Biophys. Acta, Biomembr. 2011, 1808, 2081-2088 10.1016/j.bbamem.2011.04.017
28. Duneau, J.-P.; Vegh, A. P.; Sturgis, J. N. A Dimerization Hierarchy in the Transmembrane Domains of the HER Receptor Family Biochemistry 2007, 46, 2010-2019 10.1021/bi061436f
29. Russ, W. P.; Engelman, D. M. TOXCAT: A Measure of Transmembrane Helix Association in a Biological Membrane Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 863-868 10.1073/pnas.96.3.863
30. Chipot, C. Free Energy Calculations Applied to Membrane Proteins Methods Mol. Biol. 2008, 443, 121-144 10.1007/978-1-59745-177-2-7
31. Pohorille, A.; Jarzynski, C.; Chipot, C. Good Practices in Free-Energy Calculations J. Phys. Chem. B 2010, 114, 10235-10253 10.1021/jp102971x
32. Polyansky, A. A.; Volynsky, P. E.; Efremov, R. G. Structural, Dynamic, and Functional Aspects of Helix Association in Membranes: A Computational View Adv. Protein Chem. Struct. Biol. 2011, 83, 129-161 10.1016/B978-0-12-381262-9.00004-5
33. Smith, S. O.; Eilers, M.; Song, D.; Crocker, E.; Ying, W.; Groesbeek, M.; Metz, G.; Ziliox, M.; Aimoto, S. Implications of Threonine Hydrogen Bonding in the Glycophorin A Transmembrane Helix Dimer Biophys. J. 2002, 82, 2476-2486 10.1016/S0006-3495(02)75590-2
34. Lee, J.; Im, W. Role of Hydrogen Bonding and Helix-Lipid Interactions in Transmembrane Helix Association J. Am. Chem. Soc. 2008, 130, 6456-6462 10.1021/ja711239h
35. Anbazhagan, V.; Schneider, D. The Membrane Environment Modulates Self-Association of the Human GpA TM domain-Implications for Membrane Protein Folding and Transmembrane Signaling Biochim. Biophys. Acta, Biomembr. 2010, 1798, 1899-1907 10.1016/j.bbamem.2010.06.027
36. Hong, H.; Blois, T. M.; Cao, Z.; Bowie, J. U. Method to Measure Strong Protein-Protein Interactions in Lipid Bilayers Using a Steric Trap Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 19802-19807 10.1073/pnas.1010348107
37. Hong, H.; Bowie, J. U. Dramatic Destabilization of Transmembrane Helix Interactions by Features of Natural Membrane Environments J. Am. Chem. Soc. 2011, 133, 11389-11398 10.1021/ja204524c
38. Janosi, L.; Prakash, A.; Doxastakis, M. Lipid-Modulated Sequence-Specific Association of Glycophorin A in Membranes Biophys. J. 2010, 99, 284-292 10.1016/j.bpj.2010.04.005
39. Caputo, G. A. Analyzing the Effects of Hydrophobic Mismatch on Transmembrane A-Helices Using Tryptophan Fluorescence Spectroscopy Methods Mol. Biol. 2013, 1063, 95-116 10.1007/978-1-62703-583-5-5
40. Prakash, A.; Janosi, L.; Doxastakis, M. GxxxG Motifs, Phenylalanine, and Cholesterol Guide the Self-Association of Transmembrane Domains of ErbB2 Receptors Biophys. J. 2011, 101, 1949-1958 10.1016/j.bpj.2011.09.017
41. Lensink, M. F.; Govaerts, C.; Ruysschaert, J.-M. Identification of Specific Lipid-Binding Sites in Integral Membrane Proteins J. Biol. Chem. 2010, 285, 10519-10526 10.1074/jbc.M109.068890
42. Poveda, J. A.; Giudici, A. M.; Renart, M. L.; Molina, M. L.; Montoya, E.; Fernández-Carvajal, A.; Fernández-Ballester, G.; Encinar, J. A.; González-Ros, J. M. Lipid Modulation of Ion Channels through Specific Binding Sites Biochim. Biophys. Acta, Biomembr. 2014, 1838, 1560-1567 10.1016/j.bbamem.2013.10.023
43. Sharma, S.; Lensink, M. F.; Juffer, A. H. The Structure of the CD3ζζ Transmembrane Dimer in Lipid Bilayers Biochim. Biophys. Acta, Biomembr. 2014, 1838, 739-746 10.1016/j.bbamem.2013.12.001
44. Prasanna, X.; Chattopadhyay, A.; Sengupta, D. Cholesterol Modulates the Dimer Interface of the β2-Adrenergic Receptor via Cholesterol Occupancy Sites Biophys. J. 2014, 106, 1290-1300 10.1016/j.bpj.2014.02.002
45. Pyrkova, D. V.; Tarasova, N. K.; Krylov, N. A.; Nolde, D. E.; Pentkovsky, V. M.; Efremov, R. G. Dynamic Clustering of Lipids in Hydrated Two-Component Membranes: Results of Computer Modeling and Putative Biological Impact J. Biomol. Struct. Dyn. 2013, 31, 87-95 10.1080/07391102.2012.691365
46. Parton, D. L.; Tek, A.; Baaden, M.; Sansom, M. S. P. Formation of Raft-like Assemblies within Clusters of Influenza Hemagglutinin Observed by MD Simulations PLoS Comput. Biol. 2013, 9, e1003034 10.1371/journal.pcbi.1003034
47. Mineev, K. S.; Bocharov, E. V.; Volynsky, P. E.; Goncharuk, M. V.; Tkach, E. N.; Ermolyuk, Y. S.; Schulga, A. A.; Chupin, V. V.; Maslennikov, I. V.; Efremov, R. G.; Arseniev, A. S. Dimeric Structure of the Transmembrane Domain of Glycophorin a in Lipidic and Detergent Environments Acta Naturae 2011, 3, 90-98
48. Van Der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, Flexible, and Free J. Comput. Chem. 2005, 26, 1701-1718 10.1002/jcc.20291
49. Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling J. Chem. Phys. 2007, 126, 014101 10.1063/1.2408420
50. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular Dynamics with Coupling to an External Bath J. Chem. Phys. 1984, 81, 3684 10.1063/1.448118
51. Andricioaei, I.; Karplus, M. On the Calculation of Entropy from Covariance Matrices of the Atomic Fluctuations J. Chem. Phys. 2001, 115, 6289-6292 10.1063/1.1401821
52. Numata, J.; Knapp, E.-W. Balanced and Bias-Corrected Computation of Conformational Entropy Differences for Molecular Trajectories J. Chem. Theory Comput. 2012, 8, 1235-1245 10.1021/ct200910z
53. Baron, R.; McCammon, J. A. (Thermo)dynamic Role of Receptor Flexibility, Entropy, and Motional Correlation in Protein-Ligand Binding ChemPhysChem 2008, 9, 983-988 10.1002/cphc.200700857
54. Mehrbod, M.; Mofrad, M. R. K. Localized Lipid Packing of Transmembrane Domains Impedes Integrin Clustering PLoS Comput. Biol. 2013, 9, e1002948 10.1371/journal.pcbi.1002948
55. Kik, R. A.; Leermakers, F. A. M.; Kleijn, J. M. Molecular Modeling of Proteinlike Inclusions in Lipid Bilayers: Lipid-Mediated Interactions Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2010, 81, 021915 10.1103/PhysRevE.81.021915
56. Baron, R.; de Vries, A. H.; Hünenberger, P. H.; van Gunsteren, W. F. Configurational Entropies of Lipids in Pure and Mixed Bilayers from Atomic-Level and Coarse-Grained Molecular Dynamics Simulations J. Phys. Chem. B 2006, 110, 15602-15614 10.1021/jp061627s
57. Krylov, N. A.; Pentkovsky, V. M.; Efremov, R. G. Nontrivial Behavior of Water in the Vicinity and inside Lipid Bilayers as Probed by Molecular Dynamics Simulations ACS Nano 2013, 7, 9428-9442 10.1021/nn4042392
58. Yin, H.; Slusky, J. S.; Berger, B. W.; Walters, R. S.; Vilaire, G.; Litvinov, R. I.; Lear, J. D.; Caputo, G. A.; Bennett, J. S.; DeGrado, W. F. Computational Design of Peptides That Target Transmembrane Helices Science 2007, 315, 1817-1822 10.1126/science.1136782
59. Najumudeen, A. K.; Kajanajmudeen, A. Receptor Tyrosine Kinase Transmembrane Domain Interactions: Potential Target for "Interceptor" Therapy Sci. Signaling 2010, 3, jc6 10.1126/scisignal.3138jc6
60. Arpel, A.; Sawma, P.; Spenlé, C.; Fritz, J.; Meyer, L.; Garnier, N.; Velázquez-Quesada, I.; Hussenet, T.; Aci-Sèche, S.; Baumlin, N.; Genest, M.; Brasse, D.; Hubert, P.; Crémel, G.; Orend, G.; Laquerrière, P.; Bagnard, D. Transmembrane Domain Targeting Peptide Antagonizing ErbB2/Neu Inhibits Breast Tumor Growth and Metastasis Cell Rep. 2014, 8, 1714-1721 10.1016/j.celrep.2014.07.044
61. Bennasroune, A.; Fickova, M.; Gardin, A.; Dirrig-Grosch, S.; Aunis, D.; Crémel, G.; Hubert, P. Transmembrane Peptides as Inhibitors of ErbB Receptor Signaling Mol. Biol. Cell 2004, 15, 3464-3474 10.1091/mbc.E03-10-0753
62. He, L.; Shobnam, N.; Hristova, K. Specific Inhibition of Pathogenic Receptor Tyrosine Kinase Activation by Its Transmembrane Domain Biochim. Biophys. Acta, Biomembr. 2011, 1808, 253-259 10.1016/j.bbamem.2010.08.007
63. Zhang, J.; Lazaridis, T. Transmembrane Helix Association Affinity Can Be Modulated by Flanking and Noninterfacial Residues Biophys. J. 2009, 96, 4418-4427 10.1016/j.bpj.2009.03.008