NMR-based approach to measure the free energy of transmembrane helix-helix interactions

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 1 PARTB, 2014, Pages 164-172

  Mineev, Konstantin S ^a   Lesovoy, Dmitry M ^a   Usmanova, Dinara R ^a,b   Goncharuk, Sergey A ^a,c   Shulepko, Mikhail A ^a,c   Lyukmanova, Ekaterina N ^a   Kirpichnikov, Mikhail P ^a,c   Bocharov, Eduard V ^a   Arseniev, Alexander S ^a  

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

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

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Detergent micelle; Dimerization; Free energy; NMR spectroscopy; Transmembrane helix

Indexed keywords

DETERGENT; DIMER; FIBROBLAST GROWTH FACTOR RECEPTOR 3; MONOMER; OLIGOMER; VASCULOTROPIN RECEPTOR 2;

ALPHA HELIX; ARTICLE; BIOENERGY; DIMERIZATION; DISSOCIATION; MEMBRANE BIOLOGY; MEMBRANE STRUCTURE; MICELLE; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

EID: 84887844378     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.08.021     Document Type: Article

References (40)

1. E. Li, and K. Hristova Role of receptor tyrosine kinase transmembrane domains in cell signaling and human pathologies Biochemistry 45 2006 6241 6251 (Pubitemid 43787791)
2. E.V. Bocharov, K.S. Mineev, P.E. Volynsky, Y.S. Ermolyuk, E.N. Tkach, A.G. Sobol, V.V. Chupin, M.P. Kirpichnikov, R.G. Efremov, and A.S. Arseniev Spatial structure of the dimeric transmembrane domain of the growth factor receptor ErbB2 presumably corresponding to the receptor active state J. Biol. Chem. 283 2008 6950 6956
3. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133 (Pubitemid 27161261)
4. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, K.S. Mineev, E.N. Tkach, Y.S. Ermolyuk, A.A. Schulga, R.G. Efremov, and A.S. Arseniev Left-handed dimer of EphA2 transmembrane domain: helix packing diversity among receptor tyrosine kinases Biophys. J. 98 2010 881 889
5. T.-L. Lau, C. Kim, M.H. Ginsberg, and T.S. Ulmer The structure of the integrin alphaIIbbeta3 transmembrane complex explains integrin transmembrane signalling EMBO J. 28 2009 1351 1361
6. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, A.A. Schulga, E.O. Artemenko, R.G. Efremov, and A.S. Arseniev Spatial structure and pH-dependent conformational diversity of dimeric transmembrane domain of the receptor tyrosine kinase EphA1 J. Biol. Chem. 283 2008 29385 29395
7. K.S. Mineev, E.V. Bocharov, Y.E. Pustovalova, O.V. Bocharova, V.V. Chupin, and A.S. Arseniev Spatial structure of the transmembrane domain heterodimer of ErbB1 and ErbB2 receptor tyrosine kinases J. Mol. Biol. 400 2010 231 243
8. M.A. Lemmon, J.M. Flanagan, J.F. Hunt, B.D. Adair, B.J. Bormann, C.E. Dempsey, and D.M. Engelman Glycophorin A dimerization is driven by specific interactions between transmembrane alpha-helices J. Biol. Chem. 267 1992 7683 7689
9. K.G. Fleming, A.L. Ackerman, and D.M. Engelman The effect of point mutations on the free energy of transmembrane alpha-helix dimerization J. Mol. Biol. 272 1997 266 275 (Pubitemid 27397350)
10. A.J. Beevers, A. Nash, M. Salazar-Cancino, D.J. Scott, R. Notman, and A.M. Dixon Effects of the oncogenic V 664 E mutation on membrane insertion, structure, and sequence-dependent interactions of the neu transmembrane domain in micelles and model membranes: an integrated biophysical and simulation study Biochemistry 51 2012 2558 2568
11. D. Langosch, B. Brosig, H. Kolmar, and H.J. Fritz Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator J. Mol. Biol. 263 1996 525 530 (Pubitemid 26382072)
12. W.P. Russ, and D.M. Engelman TOXCAT: a measure of transmembrane helix association in a biological membrane Proc. Natl. Acad. Sci. U. S. A. 96 1999 863 868 (Pubitemid 29072149)
13. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain J. Mol. Biol. 293 1999 639 651 (Pubitemid 29512062)
14. T. Zhuang, B.K. Jap, and C.R. Sanders Solution NMR approaches for establishing specificity of weak heterodimerization of membrane proteins J. Am. Chem. Soc. 133 2011 20571 20580
15. K.S. Mineev, N.F. Khabibullina, E.N. Lyukmanova, D.A. Dolgikh, M.P. Kirpichnikov, and A.S. Arseniev Spatial structure and dimer-monomer equilibrium of the ErbB3 transmembrane domain in DPC micelles Biochim. Biophys. Acta 1808 2011 2081 2088
16. E.V. Bocharov, K.S. Mineev, M.V. Goncharuk, and A.S. Arseniev Structural and thermodynamic insight into the process of "weak" dimerization of the ErbB4 transmembrane domain by solution NMR Biochim. Biophys. Acta 1818 2012 2158 2170
17. N.F. Khabibullina, E.N. Lyukmanova, G.S. Kopeina, Z.O. Shenkarev, A.S. Arseniev, D.A. Dolgikh, and M.P. Kirpichnikov Development and optimization of a coupled cell-free system for the synthesis of the transmembrane domain of the receptor tyrosine kinase ErbB3 Russ. J. Bioorg. Chem. 36 2010 603 609
18. D. Nietlispach Suppression of anti-TROSY lines in a sensitivity enhanced gradient selection TROSY scheme J. Biomol. NMR 31 2005 161 166 (Pubitemid 40425224)
19. S.A. Goncharuk, M.V. Goncharuk, M.L. Mayzel, D.M. Lesovoy, V.V. Chupin, E.V. Bocharov, A.S. Arseniev, and M.P. Kirpichnikov Bacterial synthesis and purification of normal and mutant forms of human FGFR3 transmembrane segment Acta Nat. 3 2011 77 84
20. E. Li, M. You, and K. Hristova Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and forster resonance energy transfer suggest weak interactions between fibroblast growth factor receptor 3 (FGFR3) transmembrane domains in the absence of extracellular domains and ligands Biochemistry 44 2005 352 360 (Pubitemid 40095737)
21. J.H. Chill, J.M. Louis, J.L. Baber, and A. Bax Measurement of 15N relaxation in the detergent-solubilized tetrameric KcsA potassium channel J. Biomol. NMR 36 2006 123 136 (Pubitemid 44473532)
22. D. Josse, C. Ebel, D. Stroebel, A. Fontaine, F. Borges, A. Echalier, D. Baud, F. Renault, M. Le Maire, E. Chabrieres, and P. Masson Oligomeric states of the detergent-solubilized human serum paraoxonase (PON1) J. Biol. Chem. 277 2002 33386 33397 (Pubitemid 34984862)
23. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Effect of detergents on the association of the glycophorin a transmembrane helix Biophys. J. 85 2003 3097 3105 (Pubitemid 37345797)
24. K.G. Fleming Standardizing the free energy change of transmembrane helix-helix interactions J. Mol. Biol. 323 2002 563 571 (Pubitemid 35283680)
25. R.A. Deems, B.R. Eaton, and E.A. Dennis Kinetic analysis of phospholipase A2 activity toward mixed micelles and its implications for the study of lipolytic enzymes J. Biol. Chem. 250 1975 9013 9020
26. E.A. Dennis Phospholipase A2 activity towards phosphatidylcholine in mixed micelles: surface dilution kinetics and the effect of thermotropic phase transitions Arch. Biochem. Biophys. 158 1973 485 493
27. L. Chen, M. Merzlyakov, T. Cohen, Y. Shai, and K. Hristova Energetics of ErbB1 transmembrane domain dimerization in lipid bilayers Biophys. J. 96 2009 4622 4630
28. J. WYMAN Jr. Linked functions and reciprocal effects in hemoglobin: a second look Adv. Protein Chem. 19 1964 223 286
29. K.D. Nadezhdin, O.V. Bocharova, E.V. Bocharov, and A.S. Arseniev Dimeric structure of transmembrane domain of amyloid precursor protein in micellar environment FEBS Lett. 586 2012 1687 1692
30. J. Zhang, and T. Lazaridis Calculating the free energy of association of transmembrane helices Biophys. J. 91 2006 1710 1723 (Pubitemid 44352436)
31. L. Chen, L. Novicky, M. Merzlyakov, T. Hristov, and K. Hristova Measuring the energetics of membrane protein dimerization in mammalian membranes J. Am. Chem. Soc. 132 2010 3628 3635
32. J. Placone, and K. Hristova Direct assessment of the effect of the Gly380Arg achondroplasia mutation on FGFR3 dimerization using quantitative imaging FRET PLoS One 7 2012 e46678
33. S. Sarabipour, and K. Hristova Glycophorin A transmembrane domain dimerization in plasma membrane vesicles derived from CHO, HEK 293T, and A431 cells Biochim. Biophys. Acta 1828 2013 1829 1833
34. J.-P. Duneau, A.P. Vegh, and J.N. Sturgis A dimerization hierarchy in the transmembrane domains of the HER receptor family Biochemistry 46 2007 2010 2019 (Pubitemid 46290552)
35. R. Soong, M. Merzlyakov, and K. Hristova Hill coefficient analysis of transmembrane helix dimerization J. Membr. Biol. 230 2009 49 55
36. V. Anbazhagan, and D. Schneider The membrane environment modulates self-association of the human GpA TM domain - implications for membrane protein folding and transmembrane signaling Biochim. Biophys. Acta, Biomembr. 1798 2010 1899 1907
37. F.J. Kobus, and K.G. Fleming The GxxxG-containing transmembrane domain of the CCK4 oncogene does not encode preferential self-interactions Biochemistry 44 2005 1464 1470 (Pubitemid 40204390)
38. P. Stanczak, R. Horst, P. Serrano, and K. Wüthrich NMR characterization of membrane protein-detergent micelle solutions by use of microcoil equipment J. Am. Chem. Soc. 131 2009 18450 18456
39. I.G. Denisov, Y.V. Grinkova, A.A. Lazarides, and S.G. Sligar Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size J. Am. Chem. Soc. 126 2004 3477 3487 (Pubitemid 38366738)
40. T.H. Bayburt, and S.G. Sligar Membrane protein assembly into nanodiscs FEBS Lett. 584 2010 1721 1727