Structural and dynamic properties of juxta-membrane segments of caveolin-1 and caveolin-2 at the membrane interface

European Biophysics Journal

Volumn 39, Issue 2, 2010, Pages 307-325

  Le Lan, Charlotte ^a,b   Gallay, Jacques ^c   Vincent, Michel ^c   Neumann, Jean Michel ^a,b   De Foresta, Béatrice ^a,b   Jamin, Nadège ^a,b  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b CNRS   (France)

^c INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

Author keywords

Caveolin; DM; DPC; Fluorescence; Interface; NMR

Indexed keywords

AMINO ACID SEQUENCE; CAVEOLIN 1; CAVEOLIN 2; CIRCULAR DICHROISM; DETERGENTS; FLUORESCENCE; GLUCOSIDES; HYDROPHOBICITY; MEMBRANES, ARTIFICIAL; MICELLES; MODELS, MOLECULAR; NORMAL DISTRIBUTION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLCHOLINE; PROTEIN STRUCTURE, SECONDARY; ROTATION; WATER;

EID: 73649086865     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-009-0548-4     Document Type: Article

References (76)

1. A Arbuzova L Wang J Wang G Hangyas-Mihalyne D Murray B Honig S McLaughlin 2000 Membrane binding of peptides containing both basic and aromatic residues. Experimental studies with peptides corresponding to the scaffolding region of caveolin and the effector region of MARCKS Biochemistry 39 10330 10339 10.1021/bi001039j 1:CAS:528:DC%2BD3cXltVOjtrs%3D 10956022 (Pubitemid 30665202)
2. N Ben-Tal B Honig RM Peitzsch G Denisov S McLaughlin 1996 Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results Biophys J 71 561 575 10.1016/S0006-3495(96)79280-9 1:CAS:528:DyaK28XkslOqtL4%3D 8842196
3. V Beswick R Guerois F Cordier-Ochsenbein YM Coïc HD Tam J Tostain JP Noël A Sanson JM Neumann 1999 Dodecylphosphocholine micelles as a membrane-like environment: new results from NMR relaxation and paramagnetic relaxation enhancement analysis Eur Biophys J 28 48 58 10.1007/s002490050182 1:STN:280:DyaK1M7jt1KrtA%3D%3D 9933923
4. K Bhattacharyya B Bagchi 2000 Slow dynamics of constrained water in complex geometries J Phys Chem A 104 10603 10613 10.1021/jp001878f 1:CAS:528:DC%2BD3cXntlKgurk%3D (Pubitemid 32023490)
5. N Bocquet H Nury M Baaden C Le Poupon JP Changeux M Delarue PJ Corringer 2009 X-ray structure of a pentameric ligand-gated ion channel in an apparently open conformation Nature 457 111 114 10.1038/nature07462 1:CAS:528: DC%2BD1MXhtVGhug%3D%3D 18987633
6. A Bouhss M Vincent H Munier AM Gilles M Takahashi O Bârzu A Danchin J Gallay 1996 Conformational transitions within the calmodulin-binding site of Bordetella pertussis adenylate cyclase studied by time-resolved fluorescence of Trp242 and circular dichroism Eur J Biochem 237 619 628 10.1111/j.1432-1033. 1996.0619p.x 1:CAS:528:DyaK28XivV2jsr8%3D 8647105
7. JC Brochon 1994 Maximum entropy method of data analysis in time-resolved spectroscopy Methods Enzymol 240 262 311 10.1016/S0076-6879(94)40052-0 1:CAS:528:DyaK2MXivFWmtbg%3D 7823835
8. LR Brown C Bosch K Wüthrich 1981 Location and orientation relative to the micelle surface for glucagon in mixed micelles with dodecylphosphocholine: EPR and NMR studies Biochim Biophys Acta 642 296 312 10.1016/0005-2736(81)90447-8 1:CAS:528:DyaL3MXktVaht7c%3D 6269613
9. EA Burstein VI Emelyanenko 1996 Log-normal description of fluorescence spectra of organic fluorophores Photochem Photobiol 64 316 320 10.1111/j.1751-1097.1996.tb02464.x 1:CAS:528:DyaK28XltVKrurw%3D
10. EA Burstein SM Abornev YK Reshetnyak 2001 Decomposition of protein tryptophan fluorescence spectra into log-normal components. I. Decomposition algorithms Biophys J 81 1699 1709 10.1016/S0006-3495(01)75823-7 1:CAS:528:DC%2BD3MXmtlCktb0%3D 11509382
11. Y Chen MD Barkley 1998 Toward understanding tryptophan fluorescence in proteins Biochemistry 37 9976 9982 10.1021/bi980274n 1:CAS:528: DyaK1cXjvFyrtLk%3D 9665702 (Pubitemid 28366351)
12. AW Cohen R Hnasko W Schubert MP Lisanti 2004 Role of caveolae and caveolins in health and disease Physiol Rev 84 1341 1379 10.1152/physrev.00046. 2003 1:CAS:528:DC%2BD2cXovVyltb0%3D 15383654 (Pubitemid 39287953)
13. YM Coïc M Vincent J Gallay F Baleux F Mousson V Beswick JM Neumann B de Foresta 2005 Single-spanning membrane protein insertion in membrane mimetic systems: role and localization of aromatic residues Eur Biophys J 35 27 39 10.1007/s00249-005-0002-1 16025323 (Pubitemid 41667023)
14. B de Foresta N Legros D Plusquellec M Le Maire P Champeil 1996 Brominated detergents as tools to study protein-detergent interactions Eur J Biochem 241 343 354 10.1111/j.1432-1033.1996.00343.x 8917429 (Pubitemid 26356819)
15. B de Foresta J Gallay J Sopkova P Champeil M Vincent 1999 Tryptophan octyl ester in detergent micelles of dodecylmaltoside: fluorescence properties and quenching by brominated detergent analogs Biophys J 77 3071 3084 10.1016/S0006-3495(99)77138-9 10585929
16. B de Foresta L Tortech M Vincent J Gallay 2002 Location and dynamics of tryptophan in transmembrane alpha-helix peptides: a fluorescence and circular dichroism study Eur Biophys J 31 185 197 10.1007/s00249-002-0211-9 12029331
17. CJ Drummond GG Warr F Grieser BW Ninham D Fennell Evans 1985 Surface properties and micellar interfacial microenvironment of n-dodecyl-β-d- maltoside J Phys Chem 89 2103 2109 10.1021/j100256a060 1:CAS:528: DyaL2MXhvVWitr0%3D
18. C Dupuy X Auvray C Petipas I Rico-Lattes A Lattes 1997 Anomeric effects on the structure of micelles of alkyl maltosides in water Langmuir 13 3965 3967 10.1021/la9604285 1:CAS:528:DyaK2sXkt1Gisbs%3D
19. JM East AG Lee 1982 Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid Biochemistry 21 4144 4151 10.1021/bi00260a035 1:CAS:528:DyaL38Xks1ygtbs%3D 6127102
20. MR Eftink 1991 Fluorescence techniques for studying protein structure Methods Biochem Anal 35 127 205 10.1002/9780470110560.ch3 1:CAS:528: DyaK3MXkvVyntrk%3D 2002770
21. D Eisenberg RM Weiss TC Terwilliger 1984 The hydrophobic moment detects periodicity in protein hydrophobicity Proc Natl Acad Sci USA 81 140 144 10.1073/pnas.81.1.140 1:CAS:528:DyaL2cXhtFKlt7g%3D 6582470 (Pubitemid 14180843)
22. RM Epand BG Sayer RF Epand 2003 Peptide-induced formation of cholesterol-rich domains Biochemistry 42 14677 14689 10.1021/bi035587j 1:CAS:528:DC%2BD3sXovV2is78%3D 14661981 (Pubitemid 37532015)
23. RM Epand BG Sayer RF Epand 2005 Caveolin scaffolding region and cholesterol-rich domains in membranes J Mol Biol 345 339 350 10.1016/j.jmb.2004.10.064 1:CAS:528:DC%2BD2cXhtVansbzO 15571726 (Pubitemid 39574855)
24. M Fernandez-Vidal S Jayasinghe AS Ladokhin SH White 2007 Folding amphipathic helices into membranes: amphiphilicity trumps hydrophobicity J Mol Biol 370 459 470 10.1016/j.jmb.2007.05.016 1:CAS:528:DC%2BD2sXmsFCltbw%3D 17532340 (Pubitemid 46898437)
25. J Gallay M Vincent IML de la Sierra H Munier-Lehmann M Renouard H Sakamoto O Barzu AM Gilles 2004 Insight into the activation mechanism of Bordetella pertussis adenylate cyclase by calmodulin using fluorescence spectroscopy Eur J Biochem 271 821 833 10.1111/j.1432-1033.2004.03987.x 1:CAS:528:DC%2BD2cXhslKqtr8%3D 14764099 (Pubitemid 38250926)
26. K Hristova SH White 2005 An experiment-based algorithm for predicting the partitioning of unfolded peptides into phosphatidylcholine bilayer interfaces Biochemistry 44 12614 12619 10.1021/bi051193b 1:CAS:528:DC%2BD2MXpt1Cns7k%3D 16156674 (Pubitemid 41324352)
27. C Krittanai WC Johnson 1997 Correcting the circular dichroism spectra of peptides for contributions of absorbing side chains Anal Biochem 253 57 64 10.1006/abio.1997.2366 1:CAS:528:DyaK2sXnsVegtrw%3D 9356142 (Pubitemid 27490605)
28. Lakowicz JR (1999) Principles of fluorescence spectroscopy. Kluwer, New York
29. J Lauterwein C Bösch LR Brown K Wüthrich 1979 Physicochemical studies of the protein-lipid interactions in melittin-containing micelles Biochim Biophys Acta 556 244 264 10.1016/0005-2736(79)90046-4 1:CAS:528:DyaE1MXlvVygsLg%3D 534626
30. C Le Lan JM Neumann N Jamin 2006 Role of the membrane interface on the conformation of the caveolin scaffolding domain: a CD and NMR study FEBS Lett 580 5301 5305 10.1016/j.febslet.2006.08.075 16979631 (Pubitemid 44415808)
31. M le Maire P Champeil JV Møller 2000 Interaction of membrane proteins and lipids with solubilizing detergents Biochim Biophys Acta 1508 86 111 10.1016/S0304-4157(00)00010-1 1:CAS:528:DC%2BD3cXot1yisLY%3D 11090820 (Pubitemid 30945650)
32. H Li V Papadopoulos 1998 Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern Endocrinology 139 4991 4997 10.1210/en.139.12.4991 1:CAS:528:DyaK1cXns1eht7k%3D 9832438
33. P Liu M Rudick RG Anderson 2002 Multiple functions of caveolin-1 J Biol Chem 277 41295 41298 10.1074/jbc.R200020200 1:CAS:528:DC%2BD38XotF2htL4%3D 12189159 (Pubitemid 35257426)
34. AK Livesey JC Brochon 1987 Analyzing the distribution of decay constants in pulse-fluorimetry using the maximum entropy method Biophys J 52 693 706 10.1016/S0006-3495(87)83264-2 1:CAS:528:DyaL1cXptFajtQ%3D%3D 19431708
35. E London GW Feigenson 1981 Fluorescence quenching in model membranes. 2. Determination of local lipid environment of the calcium adenosinetriphosphatase from sarcoplasmic reticulum Biochemistry 20 1939 1948 10.1021/bi00510a033 1:CAS:528:DyaL3MXhvVOkt7s%3D 6452901
36. 2+-ATPase from sarcoplasmic reticulum J Biol Chem 264 4907 4915 1:CAS:528:DyaL1MXitVygt7o%3D 2522447
37. SL Moors M Hellings M De Maeyer Y Engelborghs A Ceulemans 2006 Tryptophan rotamers as evidenced by X-ray, fluorescence lifetimes, and molecular dynamics modeling Biophys J 91 816 823 10.1529/biophysj.106.085100 1:CAS:528: DC%2BD28XnsFOjsbc%3D 16698786 (Pubitemid 44161913)
38. V Muñoz L Serrano 1995 Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides J Mol Biol 245 275 296 10.1006/jmbi.1994.0023 7844817
39. D Murray L Hermida-Matsumoto CA Buser J Tsang CT Sigal N Ben-Tal B Honig MD Resh S McLaughlin 1998 Electrostatics and the membrane association of Src: theory and experiment Biochemistry 37 2145 2159 10.1021/bi972012b 1:CAS:528:DyaK1cXotFGmug%3D%3D 9485361 (Pubitemid 28119288)
40. RP Nanga JR Brender J Xu G Veglia A Ramamoorthy 2008 Structures of rat and human islet amyloid polypeptide IAPP1-19 in micelles by NMR spectroscopy Biochemistry 47 12689 12697 10.1021/bi8014357 1:CAS:528:DC%2BD1cXhtlCns7bF 18989932
41. A Neumoin B Arshava J Becker O Zerbe F Naider 2007 NMR studies in dodecylphosphocholine of a fragment containing the seventh transmembrane helix of a G-protein-coupled receptor from Saccharomyces cerevisiae Biophys J 93 467 482 10.1529/biophysj.106.103770 1:CAS:528:DC%2BD2sXnvVaktLY%3D 17449670 (Pubitemid 47057813)
42. CN Pace F Vajdos L Fee G Grimsley T Gray 1995 How to measure and predict the molar absorption coefficient of a protein Protein Sci 4 2411 2423 10.1002/pro.5560041120 1:CAS:528:DyaK2MXpsVGqt7k%3D 8563639
43. CP Pan MD Barkley 2004 Conformational effects on tryptophan fluorescence in cyclic hexapeptides Biophys J 86 3828 3835 10.1529/biophysj.103.038901 1:CAS:528:DC%2BD2cXltlGltL8%3D 15189879 (Pubitemid 38780259)
44. RG Parton K Simons 2007 The multiple faces of caveolae Nat Rev Mol Cell Biol 8 185 194 10.1038/nrm2122 1:CAS:528:DC%2BD2sXitVGrsrk%3D 17318224 (Pubitemid 46310548)
45. RG Parton M Hanzal-Bayer JF Hancock 2006 Biogenesis of caveolae: a structural model for caveolin-induced domain formation J Cell Sci 119 787 796 10.1242/jcs.02853 1:CAS:528:DC%2BD28XjtFCntb4%3D 16495479
46. RM Peitzsch S McLaughlin 1993 Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins Biochemistry 32 10436 10443 10.1021/bi00090a020 1:CAS:528:DyaK3sXmt1SjsLg%3D 8399188 (Pubitemid 23320168)
47. F Perrin 1936 Mouvement brownien d'un ellipsoide (II). Rotation libre et dépolarisation des fluorescences. Translation et diffusion de molécules ellipsoidales J Phys et le Radium 7 1 11 10.1051/jphysrad: 01936007010100 1:CAS:528:DyaA28XjtlCiuw%3D%3D
48. DA Phoenix F Harris OA Daman J Wallace 2002 The prediction of amphiphilic alpha-helices Curr Protein Pept Sci 3 201 221 10.2174/1389203024605368 1:CAS:528:DC%2BD38Xjt1ektbc%3D 12188904
49. AM Powl JM East AG Lee 2005 Heterogeneity in the binding of lipid molecules to the surface of a membrane protein: hot spots for anionic lipids on the mechanosensitive channel of large conductance MscL and effects on conformation Biochemistry 44 5873 5883 10.1021/bi047439e 1:CAS:528: DC%2BD2MXisFOns7g%3D 15823046 (Pubitemid 40525124)
50. YK Reshetnyak EA Burstein 2001 Decomposition of protein tryptophan fluorescence spectra into log-normal components. II. The statistical proof of discreteness of tryptophan classes in proteins Biophys J 81 1710 1734 10.1016/S0006-3495(01)75824-9 1:CAS:528:DC%2BD3MXmtlCktbo%3D 11509383
51. S Roche S Bressanelli FA Rey Y Gaudin 2006 Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G Science 313 187 191 10.1126/science.1127683 1:CAS:528:DC%2BD28Xmslansro%3D 16840692 (Pubitemid 44066243)
52. DM Rogers JD Hirst 2004 First-principles calculations of protein circular dichroism in the near ultraviolet Biochemistry 43 11092 11102 10.1021/bi049031n 1:CAS:528:DC%2BD2cXmt12ktr4%3D 15323568 (Pubitemid 39439963)
53. P Rosevear T VanAken J Baxter S Ferguson-Miller 1980 Alkyl glycoside detergents: a simpler synthesis and their effects on kinetic and physical properties of cytochrome c oxidase Biochemistry 19 4108 4115 10.1021/bi00558a032 1:CAS:528:DyaL3cXlsVGhsro%3D 6250583
54. N Rouvière M Vincent CT Craescu J Gallay 1997 Immunosuppressor binding to the immunophilin FKBP59 affects the local structural dynamics of a surface beta-strand: time-resolved fluorescence study Biochemistry 36 7339 7352 10.1021/bi962289w 9200682 (Pubitemid 27262357)
55. NC Santos M Prieto MA Castanho 2003 Quantifying molecular partition into model systems of biomembranes: an emphasis on optical spectroscopic methods Biochim Biophys Acta 1612 123 135 10.1016/S0005-2736(03)00112-3 1:CAS:528:DC%2BD3sXkt1ensr0%3D 12787930 (Pubitemid 36629567)
56. DJ Schibli LT Nguyen SD Kernaghan O Rekdal HJ Vogel 2006 Structure-function analysis of tritrpticin analogs: potential relationships between antimicrobial activities, model membrane interactions, and their micelle-bound NMR structures Biophys J 91 4413 4426 10.1529/biophysj.106.085837 1:CAS:528:DC%2BD28XhtlWgurbO 16997878 (Pubitemid 44904228)
57. A Schlegel RB Schwab PE Scherer MP Lisanti 1999 A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro J Biol Chem 274 22660 22667 10.1074/jbc.274.32.22660 1:CAS:528:DyaK1MXlt1Cntr0%3D 10428847 (Pubitemid 29379312)
58. J Seelig 2004 Thermodynamics of lipid-peptide interactions Biochim Biophys Acta 1666 40 50 1:CAS:528:DC%2BD2cXptFOktL4%3D 15519307
59. A Sillen Y Engelborghs 1998 The correct use of "average" fluorescence parameters Photochem Photobiol 67 475 486 1:CAS:528: DyaK1cXjsFSmu7w%3D
60. H Sjögren CA Ericsson J Evenas S Ulvenlund 2005 Interactions between charged polypeptides and nonionic surfactants Biophys J 89 4219 4233 10.1529/biophysj.105.065342 16199501 (Pubitemid 41725641)
61. BL Sowmya MV Jagannadham R Nagaraj 2006 Interaction of synthetic peptides corresponding to the scaffolding domain of caveolin-3 with model membranes Biopolymers 84 615 624 10.1002/bip.20595 1:CAS:528:DC%2BD28Xht12hurnJ 16948121 (Pubitemid 44935261)
62. LK Tamm 1991 Membrane insertion and lateral mobility of synthetic amphiphilic signal peptides in lipid model membranes Biochim Biophys Acta 1071 123 148 1:CAS:528:DyaK3MXltVyltLY%3D 1854792
63. DP Tieleman D van der Spoel HJC Berendsen 2000 Molecular dynamics simulations of dodecylphosphocholine micelles at three different aggregate sizes: micellar structure and chain relaxation J Phys Chem B 104 6380 6388 10.1021/jp001268f 1:CAS:528:DC%2BD3cXktVaht7c%3D (Pubitemid 30896648)
64. L Tortech C Jaxel M Vincent J Gallay B de Foresta 2001 The polar headgroup of the detergent governs the accessibility to water of tryptophan octyl ester in host micelles Biochim Biophys Acta 1514 76 86 10.1016/S0005-2736(01)00370-4 1:CAS:528:DC%2BD3MXmtFWjtL0%3D 11513806 (Pubitemid 32769930)
65. M Vincent J Gallay 1995 Solvent relaxation around the excited state of indole: analysis of fluorescence lifetime distributions and time-dependence spectral shifts J Phys Chem 99 14931 14941 10.1021/j100041a006 1:CAS:528:DyaK2MXotFWnsL0%3D
66. M Vincent B de Foresta J Gallay 2005 Nanosecond dynamics of a mimicked membrane-water interface observed by time-resolved stokes shift of LAURDAN Biophys J 88 4337 4350 10.1529/biophysj.104.057497 1:CAS:528: DC%2BD2MXksl2jtb0%3D 15778437 (Pubitemid 40991143)
67. M Vincent J Gallay N Jamin M Garrigos B de Foresta 2007 The predicted transmembrane fragment 17 of the human multidrug resistance protein 1 (MRP1) behaves as an interfacial helix in membrane mimics Biochim Biophys Acta 1768 538 552 10.1016/j.bbamem.2006.11.021 1:CAS:528:DC%2BD2sXit1Kjsb0%3D 17257580 (Pubitemid 46275596)
68. JT Vivian PR Callis 2001 Mechanisms of tryptophan fluorescence shifts in proteins Biophys J 80 2093 2109 10.1016/S0006-3495(01)76183-8 1:CAS:528:DC%2BD3MXkvFWjtr4%3D 11325713
69. GG Warr CJ Drummond F Grieser BW Ninham D Fennell Evans 1986 Aqueous solution properties of nonionic n-dodecyl-β-d-maltoside micelles J Phys Chem 90 4581 4586 10.1021/j100410a022 1:CAS:528:DyaL28Xlt1Wgsb4%3D
70. KJ Willis W Neugebauer M Sikorska AG Szabo 1994 Probing alpha-helical secondary structure at a specific site in model peptides via restriction of tryptophan side-chain rotamer conformation Biophys J 66 1623 1630 10.1016/S0006-3495(94)80954-3 1:CAS:528:DyaK2cXkslKmsr0%3D 8061211
71. R Wimmer KK Andersen B Vad M Davidsen S Molgaard LW Nesgaard HH Kristensen DE Otzen 2006 Versatile interactions of the antimicrobial peptide novispirin with detergents and lipids Biochemistry 45 481 497 10.1021/bi051876r 1:CAS:528:DC%2BD2MXhtlSlu7vJ 16401078 (Pubitemid 43100414)
72. 15N chemical shift referencing in biomolecular NMR J Biomol NMR 6 135 140 10.1007/BF00211777 1:CAS:528:DyaK2MXoslWmtLk%3D 8589602
73. SE Woodman A Schlegel AW Cohen MP Lisanti 2002 Mutational analysis identifies a short atypical membrane attachment sequence (KYWFYR) within caveolin-1 Biochemistry 41 3790 3795 10.1021/bi0120751 1:CAS:528: DC%2BD38Xht1ektbs%3D 11888297 (Pubitemid 34224693)
74. Wüthrich K (1986) NMR of proteins and nucleic acids. John Wiley, New York
75. T Wymore XF Gao T Wong 1999 Molecular dynamics simulation of the structure and dynamics of a dodecylphosphocholine micelle in aqueous solution J Mol Struct 485-486 195 210 10.1016/S0022-2860(99)00090-3 (Pubitemid 29406393)
76. Q Zhang R Horst M Geralt X Ma WX Hong MG Finn RC Stevens K Wüthrich 2008 Microscale NMR screening of new detergents for membrane protein structural biology J Am Chem Soc 130 7357 7363 10.1021/ja077863d 1:CAS:528: DC%2BD1cXlvFyrsrw%3D 18479092 (Pubitemid 351813228)