Solution NMR studies of cell-penetrating peptides in model membrane systems

Advanced Drug Delivery Reviews

Volumn 65, Issue 8, 2013, Pages 1002-1011

  Mäler, Lena ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Bicelle; CPP; Dynamics; Membrane; NMR; Structure

Indexed keywords

BICELLE; CATIONIC PEPTIDES; CELL-PENETRATING PEPTIDE; CELLULAR MEMBRANES; CPP; MODEL MEMBRANE SYSTEMS; SOLUTION STRUCTURES; THREE-DIMENSIONAL STRUCTURE;

CELL MEMBRANES; DYNAMICS; MEMBRANES; NUCLEAR MAGNETIC RESONANCE; STRUCTURE (COMPOSITION);

PEPTIDES;

AMPHOLYTE; CARBON 13; CELL PENETRATING PEPTIDE; DETERGENT; DIHEXANOYL PHOSPHOCHOLINE; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIMYRISTOYLPHOSPHATIDYLGLYCEROL; DODECYL SULFATE SODIUM; DODECYLPHOSPHORYLCHOLINE; LYSOLYSOMYRISTOYLPHOSPHATIDYLCHOLINE; LYSOMYRISTOYLPHOSPHATIDYLGLYCEROL; MASTOPARAN; MEMBRANE PROTEIN; NANODISC; ORGANIC SOLVENT; PENETRATIN; SYNTHETIC PEPTIDE; TRANSPORTAN; UNCLASSIFIED DRUG;

CRITICAL MICELLE CONCENTRATION; LIPID BILAYER; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PARTICLE SIZE; PHOSPHOLIPID VESICLE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW;

EID: 84881022447     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2012.10.011     Document Type: Review

References (192)

1. Green M., Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell 1988, 55:1179-1188.
2. Derossi D., Joliot A.H., Chassaing G., Prochiantz A. The third helix of the Antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 1994, 269:10444-10450.
3. Derossi D., Calvet S., Trembleau A., Brunissen A., Chassaing G., Prochiantz A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 1996, 271:18188-18193.
4. Jarver P., Langel U. Cell-penetrating peptides-a brief introduction. Biochim. Biophys. Acta 2006, 1758:260-263.
5. Madani F., Lindberg S., Langel U., Futaki S., Gräslund A. Mechanisms of cellular uptake of cell-penetrating peptides. J. Biophys. 2011, 2011:414729.
6. Zorko M., Langel Ü. Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv. Drug Deliv. Rev. 2005, 57:529-545.
7. El-Andaloussi S., Holm T., Langel U. Cell-penetrating peptides: mechanisms and applications. Curr. Pharm. Des. 2005, 11:3597-3611.
8. Thorén P.E.G., Persson D., Isakson P., Goksör M., Önfelt A., Nordén B. Uptake of analogs of penetratin, Tat (48-60) and oligoarginine in live cells. Biochem. Biophys. Res. Commun. 2003, 307:100-107.
9. Deshayes S., Plénat T., Aldrian-Herrada G., Divita G., Le Grimellec C., Heitz F. Primary amphipathic cell-penetrating peptides: structural requirements and interactions with model membranes. Biochemistry 2004, 43:7698-7706.
10. Magzoub M., Gräslund A. Cell-penetrating peptides: from inception to application. Q. Rev. Biophys. 2004, 37:147-195.
11. Derossi D., Chassing G., Prochiantz A. Trojan peptides: the penetratin system for intracellular delivery. Trends Cell Biol. 1998, 8:84-87.
12. Matsuzaki K., Yoneyama S., Murase O., Miyajima K. Transbilayer transport of ions and lipids coupled with mastoparan X translocation. Biochemistry 1996, 35:8450-8456.
13. Matsuzaki K., Yoneyama S., Miyajima K. Pore formation and translocation of melittin. Biophys. J. 1997, 73:831-838.
14. Matsuzaki K. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1998, 1376:391-400.
15. Pouny Y., Rapaport D., Mor A., Nicolas P., Shai Y. Interaction of antimicrobial dermaseptin and its fluorescently labeled analogues with phospholipid membranes. Biochemistry 1992, 31:12416-12423.
16. Lee M.T., Hung W.C., Chen F.Y., Huang H.W. Many-body effect of antimicrobial peptides: on the correlation between lipid's spontaneous curvature and pore formation. Biophys. J. 2005, 89:4006-4016.
17. Magzoub M., Oglecka K., Pramanik A., Goran Eriksson L., Gräslund A. Membrane perturbation effects of peptides derived from the N-termini of unprocessed prion proteins. Biochim. Biophys. Acta 2005, 1716:126-136.
18. Saar K., Lindgren M., Hansen M., Eiríksdóttir E., Jiang Y., Rosenthal-Aizman K., Sassian M., Langel Ü. Cell-penetrating peptides: a comparative membrane toxicity study. Anal. Biochem. 2005, 345:55-65.
19. Hessa T., White S.H., Von Heijne G. Membrane insertion of a potassium-channel voltage sensor. Science 2005, 307:1427.
20. B.M. Backlund, Structural and Dynamical Studies of the Gastrintestinal Petide Hormone Motilin, in: Anonymous Doctoral Dissertion, Umeå, 1995.
21. Sargent D., Schwyzer R. Membrane lipid phase as catalyst for peptide-receptor interactions. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:5774-5778.
22. Zasloff M. Magainins, a class of antimicrobial peptides from Xenopus skin: isolation, characterization of two active forms, partial cDNA sequence of a precursor. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:5449-5453.
23. Matsuzaki K., Murase O., Fujii N., Miyajima K. Translocation of a channel-forming antimicrobial peptide, magainin 2, across lipid bilayers by forming a pore. Biochemistry 1995, 34:6521-6526.
24. Kobayashi S., Takeshima K., Park C.B., Kim S.C., Matsuzaki K. Interactions of the novel antimicrobial peptide buforin 2 with lipid bilayers: proline as a translocation promoting factor. Biochemistry 2000, 39:8648-8654.
25. Takeshima K., Chikushi A., Lee K.K., Yonehara S., Matsuzaki K. Translocation of analogues of the antimicrobial peptides magainin and buforin across human cell membranes. J. Biol. Chem. 2003, 278:1310-1315.
26. Batenburg A.M., van Esch J.H., de Kruijff B. Melittin-induced changes of the macroscopic structure of phosphatidylethanolamines. Biochemistry 1988, 27:2324-2331.
27. Duforc E.J., Smith I.C.P., Dufourcq J. Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR. Biochemistry 1986, 25:6448-6455.
28. Lauterwein J., Bosch C., Brown L.R., Wuthrich K. Physicochemical studies of the protein-lipid interactions in melittin-containing micelles. Biochim. Biophys. Acta 1979, 556:244-264.
29. Dempsey C.E. The actions of melittin on membranes. Biochim. Biophys. Acta 1990, 1031:143-161.
30. Habermann E. Bee and wasp venoms. Science 1972, 177:314-322.
31. Dufourcq J., Faucon J.F., Fourche G., Dasseux J.L., Le Maire M., Gulik-Krzywicki T. Morphological changes of phosphatidylcholine bilayers induced by melittin: vesicularization, fusion, discoidal particles. Biochim. Biophys. Acta 1986, 859:33-48.
32. Wimley W.C., Hristova K. Antimicrobial peptides: successes, challenges and unanswered questions. J. Membr. Biol. 2011, 1-8.
33. Fernández-Reyes M., Díaz D., de la Torre B.G., Cabrales-Rico A., Vallès-Miret M., Jiménez-Barbero J., Andreu D., Rivas L. Lysine Nε-trimethylation, a tool for improving the selectivity of antimicrobial peptides. J. Med. Chem. 2010, 53:5587-5596.
34. Marcotte I., Auger M. Bicelles as model membranes for solid-and solution-state NMR studies of membrane peptides and proteins. Concepts Magn. Reson. 2005, 24:17-37.
35. Gräslund A., Mäler L. Testing membrane interactions of CPPs. Methods Mol. Biol. 2011, 683:33-40.
36. Mäler L., Gräslund A. NMR studies of three-dimensional structure and positioning of CPPs in membrane model systems. Methods Mol. Biol. 2011, 683:57-67.
37. Mäler L., Gräslund A. Artificial membrane models for the study of macromolecular delivery. Methods Mol. Biol. 2009, 480:129-139.
38. Sanders C.R., Sonnichsen F. Solution NMR of membrane proteins: practice and challenges. Magn. Reson. Chem. 2006, 44:S24-S40.
39. Sanders C.R., Prosser R.S. Bicelles: a model membrane system for all seasons?. Structure 1998, 6:1227-1234.
40. Warschawski D.E., Arnold A.A., Beaugrand M., Gravel A., Chartrand É., Marcotte I. Choosing membrane mimetics for NMR structural studies of transmembrane proteins. Biochim. Biophys. Acta 2011, 1808:1957-1974.
41. Prosser R.S., Evanics F., Kitevski J.L., Al-Abdul-Wahid M.S. Current applications of bicelles in NMR studies of membrane-associated amphiphiles and proteins. Biochemistry 2006, 45:8453-8465.
42. Sanders C.R., Oxenoid K. Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins1. Biochim. Biophys. Acta 2000, 1508:129-145.
43. Vinogradova O., Sönnichsen F., Sanders C.R. On choosing a detergent for solution NMR studies of membrane proteins. J. Biomol. NMR 1998, 11:381-386.
44. Popot J.L. Amphipols, nanodiscs, and fluorinated surfactants: three nonconventional approaches to studying membrane proteins in aqueous solutions. Annu. Rev. Biochem. 2010, 79:737-775.
45. Mäler L. Solution NMR studies of peptide-lipid interactions in model membranes. Mol. Membr. Biol. 2012, 1-22.
46. Gabriel N.E., Roberts M.F. Spontaneous formation of stable unilamellar vesicles. Biochemistry 1984, 23:4011-4015.
47. Mayer L., Hope M., Cullis P. Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta 1986, 858:161-168.
48. Hope M., Bally M., Mayer L., Janoff A., Cullis P. Generation of multilamellar and unilamellar phospholipid vesicles. Chem. Phys. Lipids 1986, 40:89-107.
49. Vold R.R., Prosser R.S., Deese A.J. Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides. J. Biomol. NMR 1997, 9:329-335.
50. Damberg P., Jarvet J., Graslund A. Micellar systems as solvents in peptide and protein structure determination. Methods Enzymol. 2001, 339:271-285.
51. Chou J.J., Kaufman J.D., Stahl S.J., Wingfield P.T., Bax A. Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel. J. Am. Chem. Soc. 2002, 124:2450-2451.
52. Andersson A., Maler L. NMR solution structure and dynamics of motilin in isotropic phospholipid bicellar solution. J. Biomol. NMR 2002, 24:103-112.
53. Aniansson E., Wall S., Almgren M., Hoffmann H., Kielmann I., Ulbricht W., Zana R., Lang J., Tondre C. Theory of the kinetics of micellar equilibria and quantitative interpretation of chemical relaxation studies of micellar solutions of ionic surfactants. J. Phys. Chem. 1976, 80:905-922.
54. Itri R., Amaral L. Distance distribution function of sodium dodecyl sulfate micelles by x-ray scattering. J. Phys. Chem. 1991, 95:423-427.
55. le Maire M., Champeil P., Møller J.V. Interaction of membrane proteins and lipids with solubilizing detergents. Biochim. Biophys. Acta 2000, 1508:86-111.
56. Lin T.L., Chen S.H., Gabriel N.E., Roberts M.F. The use of small-angle neutron scattering to determine the structure and interaction of dihexanoylphosphatidylcholine micelles. J. Am. Chem. Soc. 1986, 108:3499-3507.
57. Hauser H. Short-chain phospholipids as detergents. Biochim. Biophys. Acta 2000, 1508:164-181.
58. Chou J.J., Baber J.L., Bax A. Characterization of phospholipid mixed micelles by translational diffusion. J. Biomol. NMR 2004, 29:299-308.
59. Arora A., Abildgaard F., Bushweller J.H., Tamm L.K. Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nat. Struct. Biol. 2001, 8:334-338.
60. Fernández C., Hilty C., Bonjour S., Adeishvili K., Pervushin K., Wüthrich K. Solution NMR studies of the integral membrane proteins OmpX and OmpA from Escherichia coli. FEBS Lett. 2001, 504:173-178.
61. Papavoine C., Konings R., Hilbers C., van der Van F. Location of M13 coat protein in sodium dodecyl micelles as determined by NMR. Biochemistry 1994, 33:12990-12997.
62. Papavoine C.H.M., Christiaans B.E.C., Folmer R.H.A., Konings R.N.H., Hilbers C.W. Solution structure of the M13 major coat protein in detergent micelles: a basis for a model of phage assembly involving specific residues. J. Mol. Biol. 1998, 282:401-419.
63. Jarvet J., Zdunek J., Damberg P., Gräslund A. Three-dimensional structure and position of porcine motilin in sodium dodecyl sulfate micelles determined by 1H NMR. Biochemistry 1997, 36:8153-8163.
64. Lindberg M., Biverståhl H., Gräslund A., Mäler L. Structure and positioning comparison of two variants of penetratin in two different membrane mimicking systems by NMR. Eur. J. Biochem. 2003, 270:3055-3063.
65. Unnerståle S., Lind J., Papadopoulos E., Mäler L. Solution structure of the HsapBK K -channel voltage-sensor paddle sequence. Biochemistry 2009, 48:5813-5821.
66. Lind J., Rämö T., Klement M.L.R., Bárány-Wallje E., Epand R.M., Epand R.F., Mäler L., Wieslander Å. High cationic charge and bilayer interface-binding helices in a regulatory lipid glycosyltransferase. Biochemistry 2007, 46:5664-5677.
67. Lindberg M., Jarvet J., Langel U., Gräslund A. Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 2001, 40:3141-3149.
68. Stafford R.E., Fanni T., Dennis E.A. Interfacial properties and critical micelle concentration of lysophospholipids. Biochemistry 1989, 28:5113-5120.
69. Funasaki N., Hada S., Neya S. Odd-even alternation in the aggregation number dependence of stepwise aggregation constants. J. Phys. Chem. 1991, 95:1846-1850.
70. Chattopadhyay A., Harikumar K. Dependence of critical micelle concentration of a zwitterionic detergent on ionic strength: implications in receptor solubilization. FEBS Lett. 1996, 391:199-202.
71. Ram P., Prestegard J. Magnetic field induced ordering of bile salt/phospholipid micelles: new media for NMR structural investigations. Biochim. Biophys. Acta 1988, 940:289-294.
72. Prestegard J. Magnetically orientable phospholipid bilayers containing small amounts of a bile salt analogue, CHAPSO. Biophys. J. 1990, 58:447-460.
73. Lin T.L., Liu C.C., Roberts M.F., Chen S.H. Structure of mixed short-chain lecithin/long-chain lecithin aggregates studied by small-angle neutron scattering. J. Phys. Chem. 1991, 95:6020-6027.
74. Sanders C.R., Schwonek J.P. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry 1992, 31:8898-8905.
75. Sanders C.R.I.I., Hare B.J., Howard K.P., Prestegard J.H. Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules. Prog. Nucl. Magn. Reson. Spectrosc. 1994, 26:421-444.
76. De Angelis A.A., Howell S.C., Nevzorov A.A., Opella S.J. Structure determination of a membrane protein with two trans-membrane helices in aligned phospholipid bicelles by solid-state NMR spectroscopy. J. Am. Chem. Soc. 2006, 128:12256-12267.
77. Tjandra N., Bax A. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 1997, 278:1111-1114.
78. Struppe J., Vold R.R. Dilute bicellar solutions for structural NMR work. J. Magn. Reson. 1998, 135:541-546.
79. Sanders C.R., Landis G.C. Reconstitution of membrane proteins into lipid-rich bilayered mixed micelles for NMR studies. Biochemistry 1995, 34:4030-4040.
80. Whiles J.A., Brasseur R., Glover K.J., Melacini G., Komives E.A., Vold R.R. Orientation and effects of mastoparan X on phospholipid bicelles. Biophys. J. 2001, 80:280-293.
81. Whiles J.A., Glover K.J., Vold R.R., Komives E.A. Methods for studying transmembrane peptides in bicelles: consequences of hydrophobic mismatch and peptide sequence. J. Magn. Reson. 2002, 158:149-156.
82. Glover K.J., Whiles J.A., Wu G., Yu N., Deems R., Struppe J.O., Stark R.E., Komives E.A., Vold R.R. Structural evaluation of phospholipid bicelles for solution-state studies of membrane-associated biomolecules. Biophys. J. 2001, 81:2163-2171.
83. Struppe J., Whiles J.A., Vold R.R. Acidic phospholipid bicelles: a versatile model membrane system. Biophys. J. 2000, 78:281-289.
84. Andersson A., Mäler L. Size and shape of fast-tumbling bicelles as determined by translational diffusion. Langmuir 2006, 22:2447-2449.
85. van Dam L., Karlsson G., Edwards K. Direct observation and characterization of DMPC/DHPC aggregates under conditions relevant for biological solution NMR. Biochim. Biophys. Acta 2004, 1664:241-256.
86. Luchette P.A., Vetman T.N., Prosser R.S., Hancock R.E.W., Nieh M.P., Glinka C.J., Krueger S., Katsaras J. Morphology of fast-tumbling bicelles: a small angle neutron scattering and NMR study. Biochim. Biophys. Acta 2001, 1513:83-94.
87. Triba M.N., Warschawski D.E., Devaux P.F. Reinvestigation by phosphorus NMR of lipid distribution in bicelles. Biophys. J. 2005, 88:1887-1901.
88. Andersson A., Almqvist J., Hagn F., Mäler L. Diffusion and dynamics of penetratin in different membrane mimicking media. Biochim. Biophys. Acta 2004, 1661:18-25.
89. Triba M.N., Devaux P.F., Warschawski D.E. Effects of lipid chain length and unsaturation on bicelles stability. A phosphorus NMR study. Biophys. J. 2006, 91:1357-1367.
90. Lind J., Nordin J., Mäler L. Lipid dynamics in fast-tumbling bicelles with varying bilayer thickness: effect of model transmembrane peptides. Biochim. Biophys. Acta 2008, 1778:2526-2534.
91. Andersson A., Biverståhl H., Nordin J., Danielsson J., Lindahl E., Mäler L. The membrane-induced structure of melittin is correlated with the fluidity of the lipids. Biochim. Biophys. Acta 2007, 1768:115-121.
92. Andersson A., Mäler L. Magnetic Resonance Investigations of Lipid Motion in Isotropic Bicelles. Langmuir 2005, 21:7702-7709.
93. Bárány-Wallje E., Andersson A., Gräslund A., Mäler L. Dynamics of transportan in bicelles is surface charge dependent. J. Biomol. NMR 2006, 35:137-147.
94. Bayburt T.H., Grinkova Y.V., Sligar S.G. Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2002, 2:853-856.
95. Denisov I., Grinkova Y., Lazarides A., Sligar S. Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size. J. Am. Chem. Soc. 2004, 126:3477-3487.
96. Nath A., Atkins W.M., Sligar S.G. Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 2007, 46:2059-2069.
97. Nakano M., Fukuda M., Kudo T., Miyazaki M., Wada Y., Matsuzaki N., Endo H., Handa T. Static and dynamic properties of phospholipid bilayer nanodiscs. J. Am. Chem. Soc. 2009, 131:8308-8312.
98. Ritchie T., Grinkova Y., Bayburt T., Denisov I., Zolnerciks J., Atkins W., Sligar S. Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 2009, 464:211-231.
99. Lyukmanova E.N., Shenkarev Z.O., Paramonov A.S., Sobol A.G., Ovchinnikova T.V., Chupin V.V., Kirpichnikov M.P., Blommers M.J.J., Arseniev A.S. Lipid-protein nanoscale bilayers: a versatile medium for NMR investigations of membrane proteins and membrane-active peptides. J. Am. Chem. Soc. 2008, 130:2140-2141.
100. Borch J., Hamann T. The nanodisc: a novel tool for membrane protein studies. Biol. Chem. 2009, 390:805-814.
101. Chromy B.A., Arroyo E., Blanchette C.D., Bench G., Benner H., Cappuccio J.A., Coleman M.A., Henderson P.T., Hinz A.K., Kuhn E.A. Different apolipoproteins impact nanolipoprotein particle formation. J. Am. Chem. Soc. 2007, 129:14348-14354.
102. Bayburt T.H., Sligar S.G. Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks. Proc. Natl. Acad. Sci. 2002, 99:6725-6730.
103. Jonas A. [32] Reconstitution of high-density lipoproteins. Methods Enzymol. 1986, 128:553-582.
104. Kowalewski J., Mäler L. Nuclear spin relaxation in liquids: theory, experiments, and applications 2006, Taylor & Francis Group.
105. Cavanagh J., Fairbrother W.J., Palmer A.G., Skelton N.J. Protein NMR Spectroscopy 1996, Academic Press, San Diego.
106. Wüthrich K. NMR of proteins and nucleic acids 1986, Wiley.
107. Jeener J., Meier B.H., Bachmann P., Ernst R.R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 1979, 71:4546-4553.
108. Tolman J., Flanagan J., Kennedy M.A., Prestegard J. Nuclear magnetic dipole interactions in field-oriented proteins: information for structure determination in solution. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9279-9283.
109. Tompa P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002, 27:527-533.
110. Tompa P. Unstructural biology coming of age. Curr. Opin. Struct. Biol. 2011, 21:419-425.
111. Uversky V.N. Intrinsically disordered proteins from A to Z. Int. J. Biochem. Cell Biol. 2011, 43:1090-1103.
112. Dyson H.J., Wright P.E. Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol. 2005, 6:197-208.
113. Camilloni C., De Simone A., Vranken W.F., Vendruscolo M. Determination of secondary structure populations in disordered States of proteins using nuclear magnetic resonance chemical shifts. Biochemistry 2012, 51:2224-2231.
114. Marsh J.A., Singh V.K., Jia Z., Forman-Kay J.D. Sensitivity of secondary structure propensities to sequence differences between α - and γ - synuclein: implications for fibrillation. Protein Sci. 2006, 15:2795-2804.
115. Magzoub M., Eriksson L.E., Gräslund A. Conformational states of the cell-penetrating peptide penetratin when interacting with phospholipid vesicles: effects of surface charge and peptide concentration. Biochim. Biophys. Acta 2002, 1563:53-63.
116. Czajlik A., Meskó E., Penke B., Perczel A. Investigation of penetratin peptides Part 1. The environment dependent conformational properties of penetratin and two of its derivatives. J. Pept. Sci. 2002, 8:151-171.
117. Magzoub M., Eriksson L.E.G., Gräslund A. Comparison of the interaction, positioning, structure induction and membrane perturbation of cell-penetrating peptides and non-translocating variants with phospholipid vesicles. Biophys. Chem. 2003, 103:271-288.
118. Bárány-Wallje E., Andersson A., Gräslund A., Mäler L. NMR solution structure and position of transportan in neutral phospholipid bicelles. FEBS Lett. 2004, 567:265-269.
119. Poget S.F., Cahill S.M., Girvin M.E. Isotropic bicelles stabilize the functional form of a small multidrug-resistance pump for NMR structural studies. J. Am. Chem. Soc. 2007, 129:2432-2433.
120. Poget S.F., Girvin M.E. Solution NMR of membrane proteins in bilayer mimics: small is beautiful, but sometimes bigger is better. Biochim. Biophys. Acta 2007, 1768:3098-3106.
121. Biverståhl H., Andersson A., Gräslund A., Mäler L. NMR solution structure and membrane interaction studies of the N-terminal sequence (1-30) of the bovine prion protein. Biochemistry 2004, 43:14940-14947.
122. Deshayes S., Morris M., Divita G., Heitz F. Cell-penetrating peptides: tools for intracellular delivery of therapeutics. Cell. Mol. Life Sci. 2005, 62:1839-1849.
123. Ruzza P., Calderan A., Guiotto A., Osler A., Borin G. Tat cell-penetrating peptide has the characteristics of a poly (proline) II helix in aqueous solution and in SDS micelles. J. Pept. Sci. 2004, 10:423-426.
124. Herbig M.E., Weller K., Krauss U., Beck-Sickinger A.G., Merkle H.P., Zerbe O. Membrane surface-associated helices promote lipid interactions and cellular uptake of human calcitonin-derived cell penetrating peptides. Biophys. J. 2005, 89:4056-4066.
125. Albrizio S., Giusti L., D'Errico G., Esposito C., Porchia F., Caliendo G., Novellino E., Mazzoni M.R., Rovero P., Anna M. Driving forces in the delivery of penetratin conjugated G protein fragment. J. Med. Chem. 2007, 50:1458-1464.
126. Pooga M., Hällbrink M., Zorko M., Langel Ü. Cell penetration by transportan. FASEB J. 1998, 12:67.
127. Lindgren M., Gallet X., Soomets U., Hällbrink M., Bråkenhielm E., Pooga M., Brasseur R., Langel Ü. Translocation properties of novel cell penetrating transportan and penetratin analogues. Bioconjug. Chem. 2000, 11:619-626.
128. Pooga M., Kut C., Kihlmark M., Hällbrink M., Fernaeus S., Raid R., Land T., Hallberg E., Bartfai T., Langel Ü. Cellular translocation of proteins by transportan. FASEB J. 2001, 15:1451-1453.
129. Higashijima T., Uzu S., Nakajima T., Ross E.M. Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J. Biol. Chem. 1988, 263:6491.
130. Wakamatsu K., Okada A., Miyazawa T., Ohya M., Higashijima T. Membrane-bound conformation of mastoparan-X, a G-protein-activating peptide. Biochemistry 1992, 31:5654-5660.
131. Seigneuret M., Lévy D. A high-resolution 1 H NMR approach for structure determination of membrane peptides and proteins in non-deuterated detergent: application to mastoparan X solubilized in n-octylglucoside. J. Biomol. NMR 1995, 5:345-352.
132. Bodenhausen G., Wagner G., Rance M., Sørensen O., Wüthrich K., Ernst R. Longitudinal two-spin order in 2D exchange spectroscopy (NOESY). J. Magn. Reson. 1984, 59:542-550.
133. Wagner G., Bodenhausen G., Mueller N., Rance M., Soerensen O.W., Ernst R.R., Wuethrich K. Exchange of two-spin order in nuclear magnetic resonance: separation of exchange and cross-relaxation processes. J. Am. Chem. Soc. 1985, 107:6440-6446.
134. Loria J.P., Rance M., Palmer A.G. A relaxation-compensated Carr-Purcell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy. J. Am. Chem. Soc. 1999, 121:2331-2332.
135. Wang C., Grey M.J., Palmer A.G. CPMG sequences with enhanced sensitivity to chemical exchange. J. Biomol. NMR 2001, 21:361-366.
136. Palmer A.G., Kroenke C.D., Loria J.P. [10] Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules. Methods Enzymol. 2001, 339:204-238.
137. Palmer A.G. NMR characterization of the dynamics of biomacromolecules. Chem. Rev. 2004, 104:3623-3640.
138. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity. J. Am. Chem. Soc. 1982, 104:4546-4559.
139. Skelton N.J., Palmer A.G., Akke M., Kördel J., Rance M., Chazin W.J. Practical aspects of two-dimentional proton-detected 15N spin relaxation measurements. J. Magn. Reson. B 1993, 102:253-264.
140. Lipari G., Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 2. Analysis of experimental results. J. Am. Chem. Soc. 1982, 104:4559-4570.
141. Clore G.M., Szabo A., Bax A., Kay L.E., Driscoll P.C., Gronenborn A.M. Deviations from the simple two-parameter model-free approach to the interpretation of nitrogen-15 nuclear magnetic relaxation of proteins. J. Am. Chem. Soc. 1990, 112:4989-4991.
142. Ellena J.F., Lepore L.S., Cafiso D.S. Estimating lipid lateral diffusion in phospholipid vesicles from carbon-13 spin-spin relaxation. J. Phys. Chem. 1993, 97:2952-2957.
143. Guterstam P., Madani F., Hirose H., Takeuchi T., Futaki S., Andaloussi S.E.L., Graslund A., Langel U. Elucidating cell-penetrating peptide mechanisms of action for membrane interaction, cellular uptake, and translocation utilizing the hydrophobic counter-anion pyrenebutyrate. Biochim. Biophys. Acta 2009, 1788:2509-2517.
144. Lindblom G., Orädd G. NMR Studies of translational diffusion in lyotropic liquid crystals and lipid membranes. Prog. Nucl. Magn. Reson. Spectrosc. 1994, 26:483-516.
145. Oraedd G., Lindblom G. Lateral diffusion studied by pulsed field gradient NMR on oriented lipid membranes. Magn. Reson. Chem. 2004, 42:123-131.
146. Orädd G., Lindblom G. Nmr studies of lipid lateral diffusion in the DMPC/gramicidin D/water system: peptide aggregation and obstruction effects. Biophys. J. 2004, 87:980-987.
147. Filippov A., Orädd G., Lindblom G. Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys. J. 2004, 86:891-896.
148. Gaede H.C., Gawrisch K. Lateral diffusion rates of lipid, water, and a hydrophobic drug in a multilamellar liposome. Biophys. J. 2003, 85:1734-1740.
149. Mayer C., Grobner G., Muller K., Weisz K., Kothe G. Orientation-dependent deuteron spin-lattice relaxation times in bilayer membranes: characterization of the overall lipid motion. Chem. Phys. Lett. 1990, 165:155-161.
150. Yeagle P. The structure of biological membranes 2005, CRC Press.
151. Brown M.F., Ribeiro A.A., Williams G.D. New view of lipid bilayer dynamics from 2H and 13C NMR relaxation time measurements. Proc. Natl. Acad. Sci. U. S. A. 1983, 80:4325-4329.
152. Lepore L.S., Ellena J.F., Cafiso D.S. Comparison of the lipid acyl chain dynamics between small and large unilamellar vesicles. Biophys. J. 1992, 61:767-775.
153. Gent M., Prestegard J. Comparison of 13C spin-lattice relaxation times in phospholipid vesicles and multilayers. Biochem. Biophys. Res. Commun. 1974, 58:549-555.
154. Fuson M., Prestegard J. Dynamics of an interfacial methylene in dimyristoylphosphatidylcholine vesicles using carbon-13 spin relaxation. Biochemistry 1983, 22:1311-1316.
155. Wennerström H., Lindblom G., Lindman B. Theoretical aspects on the NMR of quadrupolar ionic nuclei in micellar solutions and amphiphilic liquid crystals. Chem. Scr. 1974, 6:97-103.
156. Halle B., Wennerström H. Interpretation of magnetic resonance data from water nuclei in heterogeneous systems. J. Chem. Phys. 1981, 75:1928-1943.
157. Pastor R.W., Venable R.M., Karplus M., Szabo A. A simulation based model of NMR T relaxation in lipid bilayer vesicles. J. Chem. Phys. 1988, 89:1128-1140.
158. Biverståhl H., Lind J., Bodor A., Mäler L. Biophysical studies of the membrane location of the voltage-gated sensors in the HsapBK and KvAP K channels. Biochim. Biophys. Acta 2009, 1788:1976-1986.
159. Seelig J. Deuterium magnetic resonance: theory and application to lipid membranes. Q. Rev. Biophys. 1977, 10:353-418.
160. Seelig J. 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta 1978, 515:105-140.
161. Seelig J., Seelig A. Lipid conformation in model membranes and biological membranes. Q. Rev. Biophys. 1980, 13:19-61.
162. Pointer-Keenan C.D., Lee D.K., Hallok K., Tan A., Zand R., Ramamoorthy A. Investigation of the interaction of myelin basic protein with phospholipid bilayers using solid-state NMR spectroscopy. Chem. Phys. Lipids 2004, 132:47-54.
163. Ramamoorthy A., Thennarasu S., Tan A., Lee D.K., Clayberger C., Krensky A.M. Cell selectivity correlates with membrane-specific interactions: a case study on the antimicrobial peptide G15 derived from granulysin. Biochim. Biophys. Acta 2006, 1758:154-163.
164. Ramamoorthy A., Thennarasu S., Lee D.K., Tan A., Maloy L. Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 2006, 91:206-216.
165. Brender J.R., Dürr U.H.N., Heyl D., Budarapu M.B., Ramamoorthy A. Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. Biochim. Biophys. Acta 2007, 1768:2026-2029.
166. Dvinskikh S.V., Castro V., Sandström D. Probing segmental order in lipid bilayers at variable hydration levels by amplitude-and phase-modulated cross-polarization NMR. Phys. Chem. Chem. Phys. 2005, 7:3255-3257.
167. Dvinskikh S., Dürr U., Yamamoto K., Ramamoorthy A. A high resolution solid state NMR approach for the structural studies of bicelles. J. Am. Chem. Soc. 2006, 128:6326-6327.
168. Ottiger M., Bax A. Characterization of magnetically oriented phospholipid micelles for measurement of dipolar couplings in macromolecules. J. Biomol. NMR 1998, 12:361-372.
169. Killian J.A. Synthetic peptides as models for intrinsic membrane proteins. FEBS Lett. 2003, 555:134-138.
170. de Planque M.R.R., Killian J.A. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring. Mol. Membr. Biol. 2003, 20:271-284.
171. Killian J.A., Salemink I., de Planque M.R.R., Lindblom G., Koeppe R.E., Greathouse D.V. Induction of nonbilayer structures in diacylphosphatidylcholine model membranes by transmembrane α-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry 1996, 35:1037-1045.
172. Morein S., Strandberg E., Killian J., Persson S., Arvidson G., Koeppe R., Lindblom G. Influence of membrane-spanning alpha-helical peptides on the phase behavior of the dioleoylphosphatidylcholine/water system. Biophys. J. 1997, 73:3078-3088.
173. Killian J.A. Hydrophobic mismatch between proteins and lipids in membranes. Biochim. Biophys. Acta 1998, 1376:401-415.
174. de Planque M.R.R., Greathouse D.V., Koeppe R.E., Schäfer H., Marsh D., Killian J.A. Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. A 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A. Biochemistry 1998, 37:9333-9345.
175. de Planque M.R.R., Kruijtzer J.A.W., Liskamp R.M.J., Marsh D., Greathouse D.V., Koeppe R.E., de Kruijff B., Killian J.A. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides. J. Biol. Chem. 1999, 274:20839-20846.
176. Morein S., Koeppe R.E., Lindblom G., de Kruijff B., Antoinette Killian J. The effect of peptide/lipid hydrophobic mismatch on the phase behavior of model membranes mimicking the lipid composition in Escherichia coli membranes. Biophys. J. 2000, 78:2475-2485.
177. Killian J.A., von Heijne G. How proteins adapt to a membrane-water interface. Trends Biochem. Sci. 2000, 25:429-434.
178. de Planque M.R.R., Goormaghtigh E., Greathouse D.V., Koeppe R.E., Kruijtzer J.A.W., Liskamp R.M.J., de Kruijff B., Killian J.A. Sensitivity of single membrane-spanning α-helical peptides to hydrophobic mismatch with a lipid bilayer: effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry 2001, 40:5000-5010.
179. de Planque M.R.R., Boots J.W.P., Rijkers D.T.S., Liskamp R.M.J., Greathouse D.V., Killian J.A. The effects of hydrophobic mismatch between phosphatidylcholine bilayers and transmembrane α-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 2002, 41:8396-8404.
180. Weiss T.M., van der Wel P.C.A., Killian J.A., Koeppe R.E., Huang H.W. Hydrophobic mismatch between helices and lipid bilayers. Biophys. J. 2003, 84:379-385.
181. de Planque M.R.R., Bonev B.B., Demmers J.A.A., Greathouse D.V., Koeppe R.E., Separovic F., Watts A., Killian J.A. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 2003, 42:5341-5348.
182. Su Y., Mani R., Doherty T., Waring A.J., Hong M. Reversible sheet-turn conformational change of a cell-penetrating peptide in lipid bilayers studied by solid-state NMR. J. Mol. Biol. 2008, 381:1133-1144.
183. Su Y., Doherty T., Waring A.J., Ruchala P., Hong M. Roles of arginine and lysine residues in the translocation of a cell-penetrating peptide from 13C, 31P, and 19F solid-state NMR. Biochemistry 2009, 48:4587-4595.
184. Su Y., Mani R., Hong M. Asymmetric insertion of membrane proteins in lipid bilayers by solid-state NMR paramagnetic relaxation enhancement: a cell-penetrating peptide example. J. Am. Chem. Soc. 2008, 130:8856-8864.
185. Su Y., Waring A.J., Ruchala P., Hong M. Membrane-bound dynamic structure of an arginine-rich cell-penetrating peptide, the protein transduction domain of HIV TAT, from solid-state NMR. Biochemistry 2010, 49:6009-6020.
186. Chattopadhyay A., London E. Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 1987, 26:39-45.
187. Abrams F.S., London E. Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry 1993, 32:10826-10831.
188. Pintacuda G., Otting G. Identification of protein surfaces by NMR measurements with a paramagnetic Gd (III) chelate. J. Am. Chem. Soc. 2002, 124:372-373.
189. Mayer M., Meyer B. Characterization of ligand binding by saturation transfer difference NMR spectroscopy. Angew. Chem. Int. Ed. 1999, 38:1784-1788.
190. Mayer M., Meyer J. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor. J. Am. Chem. Soc. 2001, 123:6108-6117.
191. Lind J., Gräslund A., Mäler L. Membrane interactions of dynorphins. Biochemistry 2006, 45:15931-15940.
192. Zhang W., Smith S.O. Mechanism of penetration of Antp (43-58) into membrane bilayers. Biochemistry 2005, 44:10110-10118.