Mapping of unfolding states of integral helical membrane proteins by GPS-NMR and scattering techniques: TFE-induced unfolding of KcsA in DDM surfactant

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 9, 2012, Pages 2290-2301

  Calcutta, Antonello ^a   Jessen, Christian M ^b   Behrens, Manja Annette ^b   Oliveira, Cristiano L P ^b,e   Renart, Maria Lourdes ^c   González Ros, José M ^c   Otzen, Daniel E ^a   Pedersen, Jan Skov ^b   Malmendal, Anders ^a,d   Nielsen, Niels Chr ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

DDM micelle; Dynamic light scattering; KcsA surfactant complex; PCA; Small angle X ray scattering; TFE induced unfolding

Indexed keywords

MEMBRANE PROTEIN; N DODECYL BETA DEXTRO MALTOSIDE; POTASSIUM CHANNEL; SURFACTANT; TETRAMER; UNCLASSIFIED DRUG;

ANALYTIC METHOD; ARTICLE; CONTROLLED STUDY; DYNAMIC LIGHT SCATTERING; GLOBAL PROTEIN FOLDING STATE MAPPING BY MULTIVARIATE NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; LIGHT SCATTERING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN UNFOLDING; PROTON NUCLEAR MAGNETIC RESONANCE; SCORING SYSTEM; SMALL ANGLE SCATTERING;

BACTERIAL PROTEINS; ESCHERICHIA COLI; GLUCOSIDES; LIGHT; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; MODELS, CHEMICAL; MODELS, MOLECULAR; MOLECULAR CONFORMATION; POTASSIUM CHANNELS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SCATTERING, RADIATION; SCATTERING, SMALL ANGLE; SURFACE-ACTIVE AGENTS; X-RAYS;

EID: 84861820607     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.04.005     Document Type: Article

References (60)

1. J. Preiner, H. Janovjak, C. Rankl, H. Knaus, D.A. Cisneros, A. Kedrov, F. Kienberger, D.J. Muller, P. Hinterdorfer, Free energy of membrane protein unfolding derived from single-molecule force measurements, Biophys. J. 93 (2007) 930-937. (Pubitemid 47219785)
2. Y. Pan, L. Brown, L. Konermann, Mapping the structure of an integral membrane protein under semi-denaturing conditions by laser-induced oxidative labeling and mass spectrometry, J. Mol. Biol. 394 (2009) 968-981.
3. J.P. Whitelegge, C.B. Gundersen, K.F. Faull, Electrospray-ionization mass spectrometry of intact intrinsic membrane proteins, Protein Sci. 7 (1998) 1423-1430. (Pubitemid 28272911)
4. P.J. Booth, J. Clarke, Membrane protein folding makes the transition, Proc. Natl. Acad. Sci. U. S. A. 107 (2010) 3947-3948.
5. U. Mayor, C.M. Johnson, V. Daggett, A.R. Fersht, Protein folding and unfolding in microseconds to nanoseconds by experiment and simulation, Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 13518-13522.
6. J.U. Bowie, Solving the membrane protein folding problem, Nature 438 (2005) 581-589. (Pubitemid 41740561)
7. N.H. Joh, A. Min, S. Faham, J.P. Whitelegge, D. Yang, V.L. Woods, J.U. Bowie, Modest stabilization by most hydrogen-bonded side-chain interactions in membrane proteins, Nature 453 (2008) 1266-1270. (Pubitemid 351913594)
8. K.R. Mackenzie, Folding and stability of alpha-helical integral membrane proteins, Chem. Rev. 106 (2006) 1931-1977.
9. P.J. Booth, P. Curnow, Membrane proteins shape up: understanding in vitro folding, Curr. Opin. Struct. Biol. 16 (2006) 480-488. (Pubitemid 44149065)
10. D.E. Otzen, P. Sehgal, L.W. Nesgaard, Alternative membrane protein conformations in alcohols, Biochemistry 46 (2007) 4348-4359. (Pubitemid 46559400)
11. D.E. Otzen, Mapping the folding pathway of the transmembrane protein DsbB by protein engineering, Protein Eng. Des. Sel. 24 (2010) 139-149.
12. D.E. Otzen, Folding of DsbB in mixed micelles: a kinetic analysis of the stability of a bacterial membrane protein, J. Mol. Biol. 330 (2003) 641-649.
13. P. Sehgal, D.E. Otzen, Thermodynamics of unfolding of an integral membrane protein in mixed micelles, Protein Sci. 15 (2006) 890-899.
14. P. Curnow, P.J. Booth, Combined kinetic and thermodynamic analysis of alpha-helical membrane protein unfolding, Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 18970-18975.
15. F.W. Lau, J.U. Bowie, A method for assessing the stability of a membrane protein, Biochemistry 36 (1997) 5884-5892. (Pubitemid 27214941)
16. F.N. Barrera, M.L. Renart, J.A. Poveda, B. de Kruijff, J.A. Killian, J.M. Gonzalez-Ros, Protein Self-Assembly and Lipid Binding in the Folding of the Potassium Channel KcsA, Biochemistry 47 (2008) 2123-2133. (Pubitemid 351287138)
17. K.S. Huang, H. Bayley, M.J. Liao, E. London, H.G. Khorana, Refolding of an integral membrane protein. Denaturation, renaturation, and reconstitution of intact bacteriorhodopsin and two proteolytic fragments, J. Biol. Chem. 256 (1981) 3802-3809.
18. P.J. Booth, S.L. Flitsch, L.J. Stern, D.A. Greenhalgh, P.S. Kim, H.G. Khorana, Intermediates in the folding of the membrane protein bacteriorhodopsin, Nat. Struct. Biol. 2 (1995) 139-143. (Pubitemid 26040650)
19. A.R. Curran, R.H. Templer, P.J. Booth, Modulation of folding and assembly of the membrane protein bacteriorhodopsin by intermolecular forces within the lipid bilayer, Biochemistry 38 (1999) 9328-9336.
20. E.L. Compton, N.A. Farmer, M. Lorch, J.M. Mason, K.M. Moreton, P.J. Booth, Kinetics of an individual transmembrane helix during bacteriorhodopsin folding, J. Mol. Biol. 357 (2006) 325-338. (Pubitemid 43339334)
21. D.M. Cortes, E. Perozo, Structural dynamics of the Streptomyces lividans K+ channel (SKC1): secondary structure characterization from FTIR spectroscopy, Biochemistry 36 (1997) 10343-10352. (Pubitemid 27357747)
22. F.N. Barrera, M.L. Renart, M.L. Molina, J.A. Poveda, J.A. Encinar, A.M. Fernandez, J.L. Neira, J.M. Gonzalez-Ros, Unfolding and refolding in vitro of a tetrameric, alpha-helical membrane protein: the prokaryotic potassium channel KcsA, Biochemistry 44 (2005) 14344-14352. (Pubitemid 41533059)
23. E. van den Brink-van der Laan, V. Chupin, J.A. Killian, B. de Kruijff, Stability of KcsA tetramer depends on membrane lateral pressure, Biochemistry 43 (2004) 4240-4250. (Pubitemid 38445645)
24. E. van den Brink-van der Laan, V. Chupin, J.A. Killian, B. de Kruijff, Small alcohols destabilize the KcsA tetramer via their effect on the membrane lateral pressure, Biochemistry 43 (2004) 5937-5942. (Pubitemid 38669461)
25. A. Malmendal, J. Underhaug, D.E. Otzen, N.C. Nielsen, Fast mapping of global protein folding states by multivariate NMR: a GPS for proteins, PLoS One 5 (2010) e10262.
26. J.A.A. Demmers, A. van Dalen, B. de Kruijff, A.J.R. Heck, J.A. Killian, Interaction of the K+channel KcsA with membrane phospholipids as studied by ESI mass spectrometry, FEBS Lett. 541 (2003) 28-32. (Pubitemid 36428912)
27. M. Liu, X.- Mao, C. Ye, H. Huang, J.K. Nicholson, J.C. Lindon, Improved WATERGATE pulse sequences for solvent suppression in NMR spectroscopy, J. Magn. Reson. 132 (1998) 125-129. (Pubitemid 128450594)
28. W.J. Dunn III, D.R. Scott, W.G. Glen, Principal components analysis and partial least squares regression, Tetrahedron Comput. Method. 2 (1989) 349-376.
29. S. Wold, Cross-validatory estimation of the number of components in factor and principal components models, Technometrics 20 (1978) 397-405.
30. G. Gente, C. La Mesa, Water-trifluoroethanol mixtures: some physicochemical properties, J. Solution Chem. 29 (2000) 1159-1172.
31. J. García de la Torre,M.L.Huertas, B. Carrasco, Calculation of hydrodynamic properties of globular proteins fromtheir atomic-level structure, Biophys. J. 78 (2000) 719-730. (Pubitemid 30211830)
32. A. Ortega, D. Amorós, J. García de la Torre, Prediction of hydrodynamic and other solution properties of rigid proteins from atomic- and residue-level models, Biophys. J. 101 (2011) 892-898.
33. J.Y. Kim, S.H. Ahn, S.T. Kang, B.J. Yoon, Electrophoretic mobility equation for protein with molecular shape and charge multipole effects, J. Colloid Interface Sci. 299 (2006) 486-492. (Pubitemid 43765527)
34. J. Pedersen, A flux- and background-optimized version of the NanoSTAR small-angle X-ray scattering camera for solution scattering, J. Appl. Crystallogr. 37 (2004) 369-380.
35. O. Glatter, A new method for the evaluation of small-angle scattering data, J. Appl. Crystallogr. 10 (1977) 415-421.
36. J.S. Pedersen, S. Hansen, R. Bauer, The aggregation behavior of zinc-free insulin studied by small-angle neutron scattering, Eur. Biophys. J. 23 (1994) 227-229.
37. C.L.P. Oliveira, M.A. Behrens, J.S. Pedersen, K. Erlacher, D. Otzen, J.S. Pedersen, A SAXS study of glucagon fibrillation, J. Mol. Biol. 387 (2009) 147-161.
38. P. Baverback, C.L.P. Oliveira, V.M. Garamus, I. Varga, P.M. Claesson, J.S. Pedersen, Structural properties of beta-dodecylmaltoside and C12E6 mixed micelles, Langmuir 25 (2009) 7296-7303.
39. P. Debye, Dispersion of Rontgen rays, Ann. Phys. Leipzig 46 (1915) 809-823.
40. C. Spearman, "General intelligence" objectively determined and measured, Am. J. Psychol. 15 (1904) 201-292.
41. J. Chill, J. Louis, J. Baber, A. Bax, Measurement of 15N relaxation in the detergent-solubilized tetrameric KcsA potassium channel, J. Biomol. NMR 36 (2006) 123-136. (Pubitemid 44473532)
42. M. Hirano, Y. Takeuchi, T. Aoki, T. Yanagida, T. Ide, Rearrangements in the KcsA cytoplasmic domain underlie its gating, J. Biol. Chem. 285 (2010) 3777-3783.
43. J.H. Chill, J.M. Louis, C. Miller, A. Bax, NMR study of the tetrameric KcsA potassium channel in detergent micelles, Protein Sci. 15 (2006) 684-698.
44. D.M. Cortes, L.G. Cuello, E. Perozo, Molecular architecture of full-length KcsA: role of cytoplasmic domains in Ion permeation and activation gating, J. Gen. Physiol. 117 (2001) 165-180. (Pubitemid 32423754)
45. D.K. Wilkins, S.B. Grimshaw, V. Receveur, C.M. Dobson, J.A. Jones, L.J. Smith, Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques, Biochemistry 38 (1999) 16424-16431.
46. J.R. Brender, R.P.R. Nanga, N. Popovych, R. Soong, P.M. Macdonald, A. Ramamoorthy, The amyloidogenic SEVI precursor, PAP248-286, is highly unfolded in solution despite an underlying helical tendency, Biochimica et Biophysica Acta (BBA) - Biomembranes 1808 (2011) 1161-1169.
47. M. Buck, Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins, Q. Rev. Biophys. 31 (1998) 297-355. (Pubitemid 29213772)
48. S. Kuprin, A. Graslund, A. Ehrenberg, M.H. Koch, Nonideality of water-hexafluoropropanol mixtures as studied by X-ray small angle scattering, Biochem. Biophys. Res. Commun. 217 (1995) 1151-1156. (Pubitemid 26019772)
49. K.- Yamaguchi, H. Naiki, Y. Goto, Mechanism by which the amyloid-like fibrils of a [beta]2-microglobulin fragment are induced by fluorine-substituted alcohols, J. Mol. Biol. 363 (2006) 279-288.
50. B. Alonso, D. Massiot, Multi-scale NMR characterisation of mesostructured materials using 1H 13C through-bond polarisation transfer, fast MAS, and 1H spin diffusion, J. Magn. Reson. 163 (2003) 347-352.
51. F. Chiti, P. Webster, N. Taddei, A. Clark, M. Stefani, G. Ramponi, C.M. Dobson, Designing conditions for in vitro formation of amyloid protofilaments and fibrils, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3590-3594. (Pubitemid 29168954)
52. F. Chiti, N. Taddei, M. Bucciantini, P. White, G. Ramponi, C.M. Dobson, Mutational analysis of the propensity for amyloid formation by a globular protein, EMBO J. 19 (2000) 1441-1449. (Pubitemid 30182151)
53. S.N. Timasheff, Protein-solvent interactions and protein conformation, Acc. Chem. Res. 3 (1970) 62-68.
54. E.S.A.M. Al-Sherbini, M.H. Abdel-Kader, R.Y. Hamzah, Effect of binary solvents on the critical micelles concentration by using1-methyl-4-[4 ′-aminostyryl]pyridinium iodide, Colloids Surf., A Physicochem. Eng. Asp. 194 (2001) 133-142. (Pubitemid 32946827)
55. P. Sevilla Sierra, C. Civera Tejuca, F. García-Blanco, C. Díaz Oliva, J. Catalán Sierra, G. Gorostidi, Properties of 2,2,2-trifluoroethanol/water mixtures: acidity, basicity, and dipolarity, Helv. Chim. Acta 88 (2005) 312-324. (Pubitemid 40380477)
56. M.J. Vold, Micellization process with emphasis on premicelles, Langmuir 8 (1992) 1082-1085.
57. C. Dupuy, X. Auvray, C. Petipas, I. Rico-Lattes, A. Lattes, Anomeric effects on the structure of micelles of alkyl maltosides in water, Langmuir 13 (1997) 3965-3967. (Pubitemid 127591808)
58. C. Cecutti, B. Focher, B. Perly, T. Zemb, Glycolipid self-assembly: micellar structure, Langmuir 7 (1991) 2580-2585.
59. M.L. Molina, F.N. Barrera, A.M. Fernandez, J.A. Poveda, M.L. Renart, J.A. Encinar, G. Riquelme, J.M.G.Gonzalez-Rose, Clustering and coupled gatingmodulate the activity in KcsA, a potassium channel model, J. Biol. Chem. 281 (2006) 18837-18848. (Pubitemid 44035543)
60. F.I. Valiyaveetil, Y.F. Zhou, R. Mackinnon, Lipids in the structure, folding, and function of the KcsA K+ channel, Biochemistry 41 (2002) 10771-10777. (Pubitemid 34971053)