Structure analysis and conformational transitions of the cell penetrating peptide transportan 10 in the membrane-bound state

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Fanghänel, Susanne ^a   Wadhwani, Parvesh ^a   Strandberg, Erik ^a   Verdurmen, Wouter P R ^b   Bürck, Jochen ^a   Ehni, Sebastian ^a   Mykhailiuk, Pavel K ^c,d   Afonin, Sergii ^a   Gerthsen, Dagmar ^a   Komarov, Igor V ^c   Brock, Roland ^b   Ulrich, Anne S ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c TARAS SHEVCHENKO NATIONAL UNIVERSITY OF KYIV   (Ukraine)

^d ENAMINE LTD   (Ukraine)

Author keywords

[No Author keywords available]

Indexed keywords

3 (TRIFLUOROMETHYL) BICYCLOPENT [1.1.1] 1 YLGLYCINE; AMYLOID; CELL PENETRATING PEPTIDE; GLYCINE; PEPTIDE; TRANSPORTAN 10; UNCLASSIFIED DRUG; HYBRID PROTEIN; PROTEIN BINDING; TRANSPORTAN-10;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENANTIOMER; FLUORINE NUCLEAR MAGNETIC RESONANCE; HUMAN; HUMAN CELL; LIPID BILAYER; MEMBRANE BINDING; PROTEIN AGGREGATION; STRUCTURE ANALYSIS; CHEMISTRY; HELA CELL LINE; HYDROGEN BOND; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE;

AMYLOID; CELL MEMBRANE; CELL-PENETRATING PEPTIDES; HELA CELLS; HUMANS; HYDROGEN BONDING; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS;

EID: 84903545886     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099653     Document Type: Article

References (99)

1. Fischer R, Fotin-Mleczek M, Hufnagel H, Brock R (2005) Break on through to the other side-biophysics and cell biology shed light on cell-penetrating peptides. ChemBioChem 6: 2126-2142.
2. Khafagy el S, Morishita M (2012) Oral biodrug delivery using cell-penetrating peptide. Adv Drug Deliv Rev 64: 531-539.
3. Langel Ü (2002) Cell-penetrating peptides: processes and applications. Boca Raton, FL: CRC Press. 406 p.
4. Langel Ü (2007) Handbook of cell-penetrating peptides. Boca Raton: CRC/ Taylor & Francis. 600 p.
5. Mueller J, Kretzschmar I, Volkmer R, Boisguerin P (2008) Comparison of cellular uptake using 22 CPPs in 4 different cell lines. Bioconjug Chem 19: 2363-2374.
6. Nakase I, Akita H, Kogure K, Gräslund A, Langel Ü, et al. (2012) Efficient intracellular delivery of nucleic Acid pharmaceuticals using cell-penetrating peptides. Acc Chem Res 45: 1132-1139.
7. Afonin S, Frey A, Bayerl S, Fischer D, Wadhwani P, et al. (2006) The cellpenetrating peptide TAT(48-60) induces a non-lamellar phase in DMPC membranes. ChemPhysChem 7: 2134-2142.
8. Koren E, Apte A, Sawant RR, Grunwald J, Torchilin VP (2011) Cellpenetrating TAT peptide in drug delivery systems: proteolytic stability requirements. Drug Deliv 18: 377-384.
9. Alves ID, Bechara C, Walrant A, Zaltsman Y, Jiao CY, et al. (2011) Relationships between membrane binding, affinity and cell internalization efficacy of a cell-penetrating peptide: penetratin as a case study. PLoS One 6: e24096.
10. Dupont E, Prochiantz A, Joliot A (2010) Penetratin story: an overview. Methods Mol Biol 683: 21-29.
11. Saalik P, Niinep A, Pae J, Hansen M, Lubenets D, et al. (2011) Penetration without cells: membrane translocation of cell-penetrating peptides in the model giant plasma membrane vesicles. J Control Release 153: 117-125.
12. Barany-Wallje E, Andersson A, Gräslund A, Maler L (2004) NMR solution structure and position of transportan in neutral phospholipid bicelles. FEBS Lett 567: 265-269. (Pubitemid 38748403)
13. Barany-Wallje E, Gaur J, Lundberg P, Langel Ü, Gräslund A (2007) Differential membrane perturbation caused by the cell penetrating peptide Tp10 depending on attached cargo. FEBS Lett 581: 2389-2393. (Pubitemid 46764694)
14. Padari K, Saalik P, Hansen M, Koppel K, Raid R, et al. (2005) Cell transduction pathways of transportans. Bioconjug Chem 16: 1399-1410. (Pubitemid 41681506)
15. Saalik P, Elmquist A, Hansen M, Padari K, Saar K, et al. (2004) Protein cargo delivery properties of cell-penetrating peptides. A comparative study. Bioconjug Chem 15: 1246-1253. (Pubitemid 39552013)
16. Soomets U, Lindgren M, Gallet X, Hällbrink M, Elmquist A, et al. (2000) Deletion analogues of transportan. Biochim Biophys Acta 1467: 165-176. (Pubitemid 30621595)
17. Jones SW, Christison R, Bundell K, Voyce CJ, Brockbank SM, et al. (2005) Characterisation of cell-penetrating peptide-mediated peptide delivery. Br J Pharmacol 145: 1093-1102. (Pubitemid 43079982)
18. Saar K, Lindgren M, Hansen M, Eiriksdottir E, Jiang Y, et al. (2005) Cellpenetrating peptides: a comparative membrane toxicity study. Anal Biochem 345: 55-65. (Pubitemid 41558194)
19. Clark KS, Svetlovics J, McKeown AN, Huskins L, Almeida PF (2011) What determines the activity of antimicrobial and cytolytic peptides in model membranes. Biochemistry 50: 7919-7932.
20. McKeown AN, Naro JL, Huskins LJ, Almeida PF (2011) A thermodynamic approach to the mechanism of cell-penetrating peptides in model membranes. Biochemistry 50: 654-662.
21. Yandek LE, Pokorny A, Almeida PF (2008) Small changes in the primary structure of transportan 10 alter the thermodynamics and kinetics of its interaction with phospholipid vesicles. Biochemistry 47: 3051-3060. (Pubitemid 351328858)
22. Yandek LE, Pokorny A, Floren A, Knoelke K, Langel Ü, et al. (2007) Mechanism of the cell-penetrating peptide transportan 10 permeation of lipid bilayers. Biophys J 92: 2434-2444. (Pubitemid 46536425)
23. Almeida PF, Pokorny A (2009) Mechanisms of antimicrobial, cytolytic, and cellpenetrating peptides: from kinetics to thermodynamics. Biochemistry 48: 8083-8093.
24. Eggenberger K, Mink C, Wadhwani P, Ulrich AS, Nick P (2011) Using the peptide BP100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells. ChemBioChem 12: 132-137.
25. Henriques ST, Melo MN, Castanho MA (2006) Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem J 399: 1-7. (Pubitemid 44505401)
26. Splith K, Neundorf I (2011) Antimicrobial peptides with cell-penetrating peptide properties and vice versa. Eur Biophys J 40: 387-397.
27. Wadhwani P, Reichert J, Bürck J, Ulrich AS (2011) Antimicrobial and cellpenetrating peptides induce lipid vesicle fusion by folding and aggregation. Eur Biophys J 41: 177-187.
28. Pooga M, Hällbrink M, Zorko M, Langel Ü (1998) Cell penetration by transportan. FASEB J 12: 67-77. (Pubitemid 28060272)
29. Pujals S, Fernandez-Carneado J, Lopez-Iglesias C, Kogan MJ, Giralt E (2006) Mechanistic aspects of CPP-mediated intracellular drug delivery: relevance of CPP self-assembly. Biochim Biophys Acta 1758: 264-279. (Pubitemid 44282975)
30. Ambroggio EE, Kim DH, Separovic F, Barrow CJ, Barnham KJ, et al. (2005) Surface behavior and lipid interaction of Alzheimer beta-amyloid peptide 1-42: a membrane-disrupting peptide. Biophys J 88: 2706-2713. (Pubitemid 40976137)
31. Eisenberg D, Nelson R, Sawaya MR, Balbirnie M, Sambashivan S, et al. (2006) The structural biology of protein aggregation diseases: Fundamental questions and some answers. Acc Chem Res 39: 568-575.
32. Naito A, Kawamura I (2007) Solid-state NMR as a method to reveal structure and membrane-interaction of amyloidogenic proteins and peptides. Biochim Biophys Acta 1768: 1900-1912. (Pubitemid 47125853)
33. Nelson R, Eisenberg D (2006) Structural models of amyloid-like fibrils. Adv Protein Chem 73: 235-282. (Pubitemid 44960406)
34. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, et al. (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435: 773-778. (Pubitemid 40839722)
35. Comellas G, Lemkau LR, Zhou DH, George JM, Rienstra CM (2011) Structural intermediates during alpha-synuclein fibrillogenesis on phospholipid vesicles. J Am Chem Soc 134: 5090-5099.
36. Orcellet ML, Fernandez CO (2011) Structures behind the amyloid aggregation of alpha-synuclein: an NMR based approach. Curr Protein Pept Sci 12: 188- 204.
37. Khemtemourian L, Domenech E, Doux JP, Koorengevel MC, Killian JA (2011) Low pH acts as inhibitor of membrane damage induced by human islet amyloid polypeptide. J Am Chem Soc 133: 15598-15604.
38. Huang R, Vivekanandan S, Brender JR, Abe Y, Naito A, et al. (2011) NMR characterization of monomeric and oligomeric conformations of human calcitonin and its interaction with EGCG. J Mol Biol 416: 108-120.
39. 19F NMR label to monitor and to control peptide aggregation in membranes. J Am Chem Soc 130: 16515-16517.
40. 19F NMR. J Am Chem Soc 134: 6512- 6515.
41. Bond PJ, Khalid S (2010) Antimicrobial and cell-penetrating peptides: structure, assembly and mechanisms of membrane lysis via atomistic and coarse-grained molecular dynamics simulations. Protein Pept Lett 17: 1313-1327.
42. Grasnick D, Sternberg U, Strandberg E, Wadhwani P, Ulrich AS (2011) Irregular structure of the HIV fusion peptide in membranes demonstrated by solid-state NMR and MD simulations. European biophysics journal : EBJ 40: 529-543.
43. Grage SL, Afonin S, Grune M, Ulrich AS (2004) Interaction of the fusogenic peptide B18 in its amyloid-state with lipid membranes studied by solid state NMR. Chem Phys Lipids 132: 65-77. (Pubitemid 39458321)
44. Tatemoto K, Rökaeus A, Jörnvall H, McDonald TJ, Mutt V (1983) Galanin - a novel biologically active peptide from porcine intestine. FEBS Lett 164: 124- 128.
45. Higashijima T, Uzu S, Nakajima T, Ross EM (1988) Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem 263: 6491-6494.
46. Kilk K, El-Andaloussi S, Jarver P, Meikas A, Valkna A, et al. (2005) Evaluation of transportan 10 in PEI mediated plasmid delivery assay. J Control Release 103: 511-523. (Pubitemid 40342545)
47. Lindberg M, Jarvet J, Langel Ü, Gräslund A (2001) Secondary structure and position of the cell-penetrating peptide transportan in SDS micelles as determined by NMR. Biochemistry 40: 3141-3149. (Pubitemid 32205358)
48. Bürck J, Roth S, Wadhwani P, Afonin S, Kanithasen N, et al. (2008) Conformation and membrane orientation of amphiphilic helical peptides by oriented circular dichroism. Biophys J 95: 3872-3881.
49. 19F NMR methods for studying biomembranes. Prog Nucl Magn Reson Spectrosc 46: 1-21.
50. Cornell BA, Separovic F, Baldassi AJ, Smith R (1988) Conformation and orientation of gramicidin a in oriented phospholipid bilayers measured by solid state carbon-13 NMR. Biophys J 53: 67-76. (Pubitemid 18009693)
51. 19F NMR spectroscopy. J Am Chem Soc 130: 16512-16514.
52. 19F-NMR structure analysis of membrane-bound peptides. J Pept Sci 13: 614-623.
53. 19F NMR analysis of the antimicrobial peptide PGLa bound to native cell membranes from bacterial protoplasts and human erythrocytes. J Am Chem Soc 132: 8822-8824.
54. Mikhailiuk PK, Afonin S, Chernega AN, Rusanov EB, Platonov MO, et al. (2006) Conformationally rigid trifluoromethyl-substituted α-amino acid designed for peptide structure analysis by solid-state 19F NMR spectroscopy. Angew Chem Int Ed Engl 45: 5659-5661. (Pubitemid 44366771)
55. Strandberg E, Kanithasen N, Tiltak D, Bürck J, Wadhwani P, et al. (2008) Solidstate NMR analysis comparing the designer-made antibiotic MSI-103 with its parent peptide PGLa in lipid bilayers. Biochemistry 47: 2601-2616. (Pubitemid 351304566)
56. Ulrich AS, Wadhwani P, Dürr UHN, Afonin S, Glaser RW, et al. (2005) Solidstate 19F-nuclear magnetic resonance analysis of membrane-active peptides. In: Ramamoorthy A, editor. NMR Spectroscopy of Biological Solids. Boca Raton, FL: Taylor & Francis. 215-236
57. 2H-NMR data. Biophys J 96: 3223-3232.
58. Glaser RW, Sachse C, Dürr UH, Wadhwani P, Afonin S, et al. (2005) Concentration-dependent realignment of the antimicrobial peptide PGLa in lipid membranes observed by solid-state 19F-NMR. Biophys J 88: 3392-3397. (Pubitemid 40586589)
59. 3phenylglycine labels. J Magn Reson 168: 153-163.
60. Strandberg E, Tremouilhac P, Wadhwani P, Ulrich AS (2009) Synergistic transmembrane insertion of the heterodimeric PGLa/magainin 2 complex studied by solid-state NMR. Biochim Biophys Acta 1788: 1667-1679.
61. 3-Bpg). J Fluorine Chem 131: 217-220.
62. 3-Bpg side chain with the hydrophobic coiled-coil interface. Amino Acids 39: 1589-1593.
63. Kubyshkin VS, Komarov IV, Afonin S, Mykhailiuk PK, Grage SL, et al. (2011) Trifluoromethyl-substituted α-amino acids as solid state 19F-NMR labels for structural studies of membrane-bound peptides. In: Gouverneur V and Müller K, editors. Fluorine in pharmaceutical and medinal chemistry: from biological aspects to clinical applications. Imperial Collage Press. 91-138
64. Wadhwani P, Strandberg E, van den Berg J, Mink C, Burck J, et al. (2014) Dynamical structure of the short multifunctional peptide BP100 in membranes. Biochim Biophys Acta 1838: 940-949.
65. Meier M, Seelig J (2007) Thermodynamics of the coil < = = > beta-sheet transition in a membrane environment. J Mol Biol 369: 277-289. (Pubitemid 46635428)
66. Meier M, Seelig J (2008) Length dependence of the coil <-> beta-sheet transition in a membrane environment. J Am Chem Soc 130: 1017-1024.
67. Fields GB, Noble RL (1990) Solid phase peptide synthesis utilizing 9- fluorenylmethoxycarbonyl amino acids. Int J Pept Protein Res 35: 161-214. (Pubitemid 20126875)
68. Johnson WC (1999) Analyzing protein circular dichroism spectra for accurate secondary structures. Proteins 35: 307-312.
69. Sreerama N, Woody RW (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal Biochem 287: 252-260. (Pubitemid 32006234)
70. Provencher SW, Glockner J (1981) Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20: 33-37.
71. van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal Biochem 191: 110-118.
72. Sreerama N, Woody RW (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209: 32-44. (Pubitemid 23084702)
73. Sreerama N, Woody RW (1999) Molecular dynamics simulations of polypeptide conformations in water: A comparison of α, β, and poly(Pro)II conformations. Proteins 36: 400-406. (Pubitemid 29387738)
74. Lobley A, Whitmore L, Wallace BA (2002) DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra. Bioinformatics 18: 211-212. (Pubitemid 34145057)
75. Whitmore L, Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32: W668-673. (Pubitemid 38997420)
76. Rance M, Byrd RA (1983) Obtaining high-fidelity spin-1/2 powder spectra in anisotropic media - phase-cycled Hahn echo spectroscopy. J Magn Reson 52: 221-240.
77. Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. J Magn Reson 142: 97-101.
78. Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103: 6951-6958.
79. Zhang S, Wu XL, Mehring M (1990) Elimination of ringing effects in multiplepulse sequences. Chem Phys Lett 173: 481-484.
80. Glaser RW, Ulrich AS (2003) Susceptibility corrections in solid-state NMR experiments with oriented membrane samples. Part I: applications. J Magn Reson 164: 104-114.
81. 19F-NMR. Biophys J 90: 1676-1686.
82. Tremouilhac P, Strandberg E, Wadhwani P, Ulrich AS (2006) Synergistic transmembrane alignment of the antimicrobial heterodimer PGLa/magainin. J Biol Chem 281: 32089-32094. (Pubitemid 46036763)
83. Ohman A, Lycksell PO, Andell S, Langel Ü, Bartfai T, et al. (1995) Solvent stabilized solution structures of galanin and galanin analogs, studied by circular dichroism spectroscopy. Biochim Biophys Acta 1236: 259-265.
84. Bartels T, Ahlstrom LS, Leftin A, Kamp F, Haass C, et al. (2010) The Nterminus of the intrinsically disordered protein alpha-synuclein triggers membrane binding and helix folding. Biophys J 99: 2116-2124.
85. 2+-sensing and SK channel activation. Proc Natl Acad Sci U S A 110: 4828-4833.
86. Aisenbrey C, Borowik T, Byström R, Bokvist M, Lindström F, et al. (2008) How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur Biophys J 37: 247-255.
87. Hebda JA, Miranker AD (2009) The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes. Ann Rev Biophys 38: 125-152.
88. Gorbenko GP, Kinnunen PK (2006) The role of lipid-protein interactions in amyloid-type protein fibril formation. Chem Phys Lipids 141: 72-82. (Pubitemid 43728804)
89. 3 in membranes. Phys Chem Chem Phys 15: 8962-8971.
90. Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16: 260-265.
91. Khurana R, Coleman C, Ionescu-Zanetti C, Carter SA, Krishna V, et al. (2005) Mechanism of thioflavin T binding to amyloid fibrils. J Str Biol 151: 229-238. (Pubitemid 41338730)
92. Ulrich AS, Tichelaar W, Förster G, Zschörnig O, Weinkauf S, et al. (1999) Ultrastructural characterization of peptide-induced membrane fusion and peptide self-assembly in the lipid bilayer. Biophys J 77: 829-841. (Pubitemid 29362455)
93. Dunkin CM, Pokorny A, Almeida PF, Lee HS (2011) Molecular dynamics studies of transportan 10 (Tp10) interacting with a POPC lipid bilayer. J Phys Chem B 115: 1188-1198.
94. Janek K, Rothemund S, Gast K, Beyermann M, Zipper J, et al. (2001) Study of the conformational transition of Aβ(1-42) using D-amino acid replacement analogues. Biochemistry 40: 5457-5463. (Pubitemid 32458247)
95. Doran TM, Anderson EA, Latchney SE, Opanashuk LA, Nilsson BL (2012) Turn nucleation perturbs amyloid beta self-assembly and cytotoxicity. J Mol Biol 421: 315-328.
96. Sciarretta KL, Gordon DJ, Meredith SC (2006) Peptide-based inhibitors of amyloid assembly. Methods Enzymol 413: 273-312. (Pubitemid 44528696)
97. Kerth A, Erbe A, Dathe M, Blume A (2004) Infrared reflection absorption spectroscopy of amphipathic model peptides at the air/water interface. Biophys J 86: 3750-3758. (Pubitemid 38780253)
98. Lindberg M, Gräslund A (2001) The position of the cell penetrating peptide penetratin in SDS micelles determined by NMR. FEBS Lett 497: 39-44. (Pubitemid 32480177)
99. Magzoub M, Kilk K, Eriksson LE, Langel Ü, Gräslund A (2001) Interaction and structure induction of cell-penetrating peptides in the presence of phospholipid vesicles. Biochim Biophys Acta 1512: 77-89. (Pubitemid 32378784)