The spin label amino acid TOAC and its uses in studies of peptides: Chemical, physicochemical, spectroscopic, and conformational aspects

Biophysical Reviews

Volumn 4, Issue 1, 2012, Pages 45-66

  Schreier, Shirley ^a   Bozelli, José Carlos ^a   Marín, Nélida ^a   Vieira, Renata F F ^b   Nakaie, Clóvis R ^b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Backbone dynamics; EPR; Membrane; Paramagnetic enhanced relaxation; Peptide; Spin label; TOAC

Indexed keywords

EID: 84868362067     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-011-0064-5     Document Type: Review

References (180)

1. Altenbach C, Flitsch SL, Khorana HG, Hubbell WL (1989) Structural studies on transmembrane proteins. 2. Spin labeling of bacteriorhodopsin mutants at unique cysteines. Biochemistry 28: 7806-7812.
2. Anderson DJ, Hanson P, McNulty J, Millhauser G, Monaco V, Formaggio F, Crisma M, Toniolo C (1999) Solution structures of TOAC-labeled trichogin GA IV peptides from allowed (g ≈ 2) and half-field electron spin resonance. J Am Chem Soc 121: 6919-6927.
3. Atherton E, Sheppard RC (1989) Solid phase peptide synthesis: a practical approach. I. L. R. Press, Oxford.
4. Balog M, Kálai T, Jeko J, Berente Z, Steinhoff H-J, Engelhard M, Hideg K (2003) Synthesis of new conformationally rigid paramagnetic α-amino acids. Tetrahedron Lett 44: 9213-9217.
5. Barbosa SR, Cilli EM, Lamy-Freund MT, Castrucci AM, Nakaie CR (1999) First synthesis of a fully active spin-labeled peptide hormone. FEBS Lett 446: 45-48.
6. Bartucci R, Guzzi R, De Zotti M, Toniolo C, Sportelli L, Marsh D (2008) Backbone dynamics of alamethicin bound to lipid membranes: spin-echo electron paramagnetic resonance of TOAC-spin labels. Biophys J 94: 2698-2705.
7. 2O. Biophys J 96: 997-1007.
8. Bettio A, Gutewort V, Pöppl A, Dinger MC, Zschörnig O, Klaus A, Toniolo C, Beck-Sickinger AG (2002) Electron paramagnetic resonance backbone dynamics studies on spin-labelled neuropeptide Y analogues. J Pept Sci 8: 671-682.
9. Bozelli Jr. JC (2011) MSc dissertation, University of São Paulo.
10. Brière R, Lemaire H, Rassat A (1965) Nitroxydes XV: Synthèse et étude de radicaux libres stables piperidiniques et pyrrolidinique. Bull Soc Chim Fr 3273-3283.
11. Brogden KA (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
12. Budil DE, Lee S, Saxena S, Freed JH (1996) Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm. J Magn Res Ser A 120: 155-189.
13. α-tetrasubstituted α-amino acid for peptide conformational analysis by CD spectroscopy in the visible region. Part I. J Chem Soc, Perkin Trans 2: 1043-1046.
14. Cann JR, London RE, Unkefer CJ, Vavrek RJ, Stewart JM (1987) CD-n. m. r. study of the solution conformation of bradykinin analogs containing α-aminoisobutyric acid. Int J Pept Protein Res 29: 486-496.
15. 10-helices through an integrated spin labeling and computational approach. J Am Chem Soc 129: 11248-11258.
16. Cilli EM, Oliveira E, Marchetto R, Nakaie CR (1996) Correlation between solvation of peptide-resins and solvent properties. J Org Chem 61: 8992-9000.
17. Cilli EM, Marchetto R, Schreier S, Nakaie CR (1997) Use of spin label EPR spectra to monitor peptide chain aggregation inside resin beads. Tetrahedron Lett 38: 517-520.
18. Cilli EM, Marchetto R, Schreier S, Nakaie CR (1999) Correlation between the mobility of spin-labeled peptide chains and resin solvation: an approach to optimize the synthesis of aggregating sequences. J Org Chem 64: 9118-9123.
19. Cilli EM, Vicente EF, Crusca E, Nakaie CR (2007) EPR investigation of the influence of side chain protecting groups on peptide-resin solvation of the Asx and Glx model containing peptides. Tetrahedron Lett 48: 5521-5524.
20. Cornish VW, Benson DR, Altenbach CA, Hideg K, Hubbell WL, Schultz PG (1994) Site-specific incorporation of biophysical probes into proteins. Proc Natl Acad Sci USA 91: 2910-2914.
21. Corvaja C, Sartori E, Toffoletti A, Formaggio F, Crisma M, Toniolo C (2000a) Interaction between TOAC free radical and photoexcited triplet chromophores linked to peptide templates. Biopolymers 55: 486-495.
22. Corvaja C, Sartori E, Toffoletti A, Formaggio F, Crisma M, Toniolo C, Mazaleyrat JP, Wakselman M (2000b) CIDEP effects of intramolecular quenching of singlet and triplet excited states by nitroxide radicals in oligopeptides: a potentially useful new method for investigating peptide secondary structures in solution. Chem-Eur J 6: 2775-2782.
23. Crisma M, Monaco V, Formaggio F, Toniolo C, George C, Flippen-Anderson JL (1997) Crystallographic structure of a helical lipopeptaibol antibiotic analogue. Lett Pept Sci 4: 213-218.
24. Crisma M, Formaggio F, Mezzato S, Toniolo C, Savrda J, Mazaleyrat JP, Wakselman M (2000) Afc can adopt either the fully extended or a turn conformation. Lett Pept Sci 7: 123-131.
25. Crisma M, Deschamps JR, George C, Flippen-Anderson JL, Kaptein B, Broxterman QB, Moretto A, Oancea S, Jost M, Formaggio F, Toniolo C (2005) A topographically and conformationally constrained, spin-labeled, alpha-amino acid: crystallographic characterization in peptides. J Pept Res 65: 564-579.
26. Crisma M, Monaco V, Formaggio F, Toniolo C, George C, Flippen-Anderson JL (2007) Crystallographic structure of a helical lipopeptaibol antibiotic analogue. Lett Pept Sci 4: 213-218.
27. Csekö J, Hankovszki HO, Hideg K (1985) Synthesis of novel, highly reactive 1-oxyl-2, 2, 6, 6-tetramethyl-1, 2, 5, 6-tetrahydropyridine derivatives. Can J Chem 63: 940-943.
28. D'Amore M, Improta R, Barone V (2003) Conformational behavior and magnetic properties of a nitroxide amino acid derivative in vacuo and in aqueous solution. J Phys Chem A 107: 6264-6269.
29. Devaux P, McConnell HM (1972) Lateral diffusion in spin-labeled phosphatidylcholine multilayers. J Am Chem Soc 94: 4475-4481.
30. Dratz EA, Furstenau JE, Lambert CG, Thireault DL, Rarick H, Schepers T, Pakhlevaniants S, Hamm HE (1993) NMR structure of a receptor-bound G-protein peptide. Nature 363: 276-281.
31. Duarte DL, Malavolta L, Vieira RFF, Oliveira L, Schreier S, Nakaie CR (2011) An unusual spectroscopic approach for assessing the binding site of the bradykinin B2 receptor. In: Bridges B, Lebl M (eds) Peptides. Prompt Scientific Publishing, San Diego, pp 254-255.
32. Dupeyre RM, Lemaire H, Rassat A (1964) Nitroxydes (VII): radicaux libres stables pyrrolidiniques. Tetrahedron Lett 27: 1781-1785.
33. Dutot L, Wright K, Gaucher A, Wakselman M, Mazaleyrat J-P, De Zotti M, Peggion C, Formaggio F, Toniolo C (2008) The Bip method, based on the induced circular dichroism of a flexible biphenyl probe in terminally protected -Bip-Xaa*- dipeptides, for assignment of the absolute configuration of β-amino acids. J Am Chem Soc 130: 5986-5992.
34. Dyszy FH (2008) PhD thesis, University of São Paulo.
35. Elsässer C, Monien B, Haehnel W, Bittl R (2005) Orientation of spin labels in de novo peptides. Magn Reson Chem 43: S26-S33.
36. Epand R, Epand RM, Monaco V, Stoia S, Formaggio F, Crisma M, Toniolo C (1999) The antimicrobial peptide trichogin and its interaction with phospholipid membranes. Eur J Biochem 266: 1021-1028.
37. Esposito C, Tedeschi A, Scrima M, D'errico G, Ottaviani MF, Rovero P, D'ursi AM (2006) Exploring interaction of β-amyloid segment (25-35) with membrane models through paramagnetic probes. J Pept Sci 12: 766-774.
38. Fernandez RM, Vieira RF, Nakaie CR, Lamy MT, Ito AS (2005a) Acid-base titration of melanocortin peptides: evidence of Trp rotational conformers interconversion. Biopolymers 80: 643-650.
39. Fernandez RM, Vieira RF, Nakaie CR, Ito AS, Lamy MT (2005b) Peptide-lipid interaction monitored by spin-labeled biologically active melanocortin peptides. Peptides 26: 1825-1834.
40. Fields GB, Noble RL (1990) Solid phase peptide synthesis utilizing 9-fluorenylmethoxycarbonyl amino acids. Int J Pept Protein Res 35: 161-214.
41. α,α-disubstituted glycine, in simple derivatives and model peptides. Int J Pept Protein Res 47: 231-238.
42. Formaggio F, Bonchio M, Crisma M, Peggion C, Mezzato S, Polese A, Barazza A, Antonello S, Maran F, Broxterman QB, Kaptein B, Kamphuis J, Vitale RM, Saviano M, Benedetti E, Toniolo C (2002) Nitroxyl peptides as catalysts of enantioselective oxidations. Chem-Eur J 8: 84-93.
43. Fox RO Jr, Richards FM (1982) A voltage-gated ion channel model inferred from the crystal structure of alamethicin at 1. 5-Å resolution. Nature 300: 325-330.
44. Gatto E, Stella L, Formaggio F, Toniolo C, Lorenzelli L, Venanzi M (2008) Electroconductive and photocurrent generation properties of self-assembled monolayers formed by functionalized, conformationally-constrained peptides on gold electrodes. J Pept Sci 14: 184-191.
45. Hamm HE, Deretic D, Arendt A, Hargrave PA, Koenig B, Hofmann KP (1988) Site of G protein binding to rhodopsin mapped with synthetic peptides from the α subunit. Science 241: 832-835.
46. Hanson P, Millhauser G, Formaggio F, Crisma M, Toniolo C (1996a) ESR characterization of hexameric, helical peptides using double TOAC spin labeling. J Am Chem Soc 118: 7618-7625.
47. Hanson P, Martinez G, Millhauser G, Formaggio F, Crisma M, Toniolo C, Vita C (1996b) Distinguishing helix conformations in alanine-rich peptides using the unnatural amino acid TOAC and Electron Spin Resonance. J Am Chem Soc 118: 271-272.
48. Hanson P, Anderson DJ, Martinez G, Millhauser G, Formaggio F, Crisma M, Toniolo T, Vita C (1998) Electron spin resonance and structural analysis of water soluble, alanine-rich peptides incorporating TOAC. Mol Phys 95: 957-966.
49. Herget M, Baldauf C, Schölz C, Parcej D, Wiesmüller KH, Tampé R, Abele R, Bordignon E (2011) Conformation of peptides bound to the transporter associated with antigen processing (TAP). Proc Natl Acad Sci USA 108: 1349-1354.
50. Hoffmann AK, Henderson AT (1961) A new stable free radical: di-t-butylnitroxide. J Am Chem Soc 83: 4671-4672.
51. Hsia J-C, Schneider H, Smith ICP (1970) Spin label studies of oriented phospholipids: egg lecithin. Biochim Biophys Acta 202: 399-402.
52. Hubbell WL, McConnell HM (1968) Spin-label studies of the excitable membranes of nerve and muscle. Proc Natl Acad Sci USA 61: 12-16.
53. Hubbell WL, McConnell HM (1969) Motion of steroid spin labels in membranes. Proc Natl Acad Sci USA 63: 16-22.
54. Hubbell WL, McConnell HM (1971) Molecular motion in spin-labeled phospholipids and membranes. J Am Chem Soc 93: 314-326.
55. Inbaraj JJ, Cardon TB, Laryukhin M, Grosser SM, Lorigan GA (2006) Determining the topology of integral membrane peptides using EPR spectroscopy. J Am Chem Soc 128: 9549-9554.
56. Inbaraj JJ, Laryukhin M, Lorigan GA (2007) Determining the helical tilt angle of a transmembrane helix in mechanically aligned lipid bilayers using EPR spectroscopy. J Am Chem Soc 129: 7710-7711.
57. 7, 18, 19] alamethicin F50/5 from paramagnetic relaxation enhancement measurements with data obtained from an X-ray diffraction-based model. J Pept Sci 17: 377-382.
58. Karim CB, Kirby TL, Zhang Z, Nesmelov Y, Thomas DD (2004) Phospholamban structural dynamics in lipid bilayers probed by a spin label rigidly coupled to the peptide backbone. Proc Natl Acad Sci USA 101: 14437-14442.
59. Karim CB, Zhang Z, Howard EC, Torgersen KD, Thomas DD (2006) Phosphorylation-dependent conformational switch in spin-labeled phospholamban bound to SERCA. J Mol Biol 358: 1032-1040.
60. Karim CB, Zhang Z, Thomas DD (2007) Synthesis of TOAC spin-labeled proteins and reconstitution in lipid membranes. Nat Protoc 2: 42-49.
61. Karp ES, Inbaraj JJ, Laryukhin M, Lorigan GA (2006) Electron paramagnetic resonance studies of an integral membrane peptide inserted into aligned phospholipid bilayer nanotube arrays. J Am Chem Soc 128: 12070-12071.
62. Keizers PHJ, Ubbink M (2011) Paramagnetic tagging for protein structure and dynamics analysis. Prog Nucl Magn Reson Spectrosc 58: 88-96.
63. Kisselev OG, Kao J, Ponder JW, Fann YC, Gautam N, Marshall GR (1998) Light-activated rhodopsin induces structural binding motif in G protein α-subunit. Proc Natl Acad Sci USA 95: 4270-4275.
64. Kornberg RD, McConnell HM (1971) Inside-outside transitions of phospholipids in vesicle membranes. Biochemistry 10: 1111-1120.
65. Lebedev OL, Kazarnovskii SN (1959) Papers on Chemistry and Chemical Technology, Gor'kii, 649 (in Russian).
66. Leigh JS Jr (1970) ESR rigid-lattice line shape in a system of two interacting spins. J Chem Phys 52: 2608-2612.
67. Lex L, Hideg K, Hankovszky HO (1982) Nitroxides. IX. Synthesis of nitroxide free radical α-amino acids. Can J Chem 60: 1448-1451.
68. Lindfors HE, de Koning PE, Drijfhout JW, Venezia B, Ubbink M (2008) Mobility of TOAC spin-labelled peptides binding to the Src SH3 domain studied by paramagnetic NMR. J Biomol NMR 41: 157-167.
69. Livshits VA, Dzikovski BG, Marsh D (2001) Mechanism of relaxation enhancement of spin labels in membranes by paramagnetic ion salts: dependence on 3d and 4f ions and on the anions. J Magn Res 148: 221-237.
70. Lopes DD, Poletti EF, Vieira RFF, Jubilut GN, Oliveira L, Paiva ACM, Schreier S, Nakaie CR (2008) A proposed EPR approach to evaluating agonist binding site of a peptide receptor. Int J Pept Res Ther 14: 121-126.
71. Luckhurst GR (1976) Biradicals as spin probes. In: Berliner LJ (ed) Spin labeling theory and applications. Academic New York, pp 133-181.
72. Malavolta L, Oliveira E, Cilli EM, Nakaie CR (2002) Solvation of polymers as models for solvent effect investigation: proposition of a novel polarity scale. Tetrahedron 58: 4383-4394.
73. Malavolta L, Poletti EF, Silva EH, Schreier S, Nakaie CR (2008) Application of electron paramagnetic resonance spectroscopy for validation of the novel (AN plus DN) solvent polarity scale. Int J Mol Sci 9: 1321-1332.
74. Mangels C, Kellner R, Einsiedel J, Weiglmeier PR, Rosch P, Gmeiner P, Schwarzinger S (2010) The therapeutically anti-prion active antibody-fragment scFv-W226: paramagnetic relaxation-enhanced NMR spectroscopy aided structure elucidation of the paratope-epitope interface. J Biomol Struct Dyn 28: 13-22.
75. Marchetto R, Schreier S, Nakaie CR (1993) A novel spin-labeled amino acid derivative for use in peptide synthesis: (9-fluorenylmethyloxycarbonyl)-2, 2, 6, 6-tetramethyl piperidine-N-oxyl-4-amino-4-carboxylic acid. J Am Chem Soc 115: 11042-11043.
76. Marchetto R, Cilli EM, Jubilut GN, Schreier S, Nakaie CR (2005) Determination of site-site distance and site concentration within polymer beads: a combined swelling-electron paramagnetic resonance study. J Org Chem 70: 4561-4568.
77. Marín N (2007) PhD thesis, University of São Paulo.
78. Marín N, Vieira RFF, Nakaie CR, Schreier S (2011) Spectroscopic studies of conformational properties of bradykinin and its TOAC-labeled derivatives in solution and in the presence of model membranes. In: Lebl M (ed) Peptides. Building Bridges. Prompt Publishing, San Diego, pp 242-243.
79. Marsh D (2006) Orientation of TOAC amino-acid spin labels in α-helices and β-strands. J Magn Reson 180: 305-310.
80. Marsh D, Toniolo C (2008) Polarity dependence of EPR parameters for TOAC and MTSSL spin labels: correlation with DOXYL spin labels for membrane studies. J Magn Reson 190: 211-221.
81. Marsh D, Jost M, Peggion C, Toniolo C (2007a) Solvent dependence of the rotational diffusion of TOAC-spin-labeled alamethicin. Chem Biodivers 4: 1269-1274.
82. Marsh D, Jost M, Peggion C, Toniolo C (2007b) TOAC spin labels in the backbone of alamethicin: EPR studies in lipid membranes. Biophys J 92: 473-481.
83. Marsh D, Jost M, Peggion C, Toniolo C (2007c) Lipid chain-length dependence for incorporation of alamethicin in membranes: electron paramagnetic resonance studies on TOAC-spin-labeled analogs. Biophys J 92: 4002-4011.
84. Martin EL, Rens-Domiano S, Schatz PJ, Hamm HE (1996) Potent peptide analogues of a G protein-receptor-binding region obtained with a combinatorial library. J Biol Chem 271: 361-366.
85. McNulty JM, Millhauser GL (2002) TOAC the rigid nitroxide side chain. In: Berliner LJ, Eaton GR, Eaton SS (eds) Biological magnetic resonance, vol 19. Kluwer, New York, pp 277-307.
86. McNulty JC, Silapie JL, Carnevali M, Farrar CT, Griffin RG, Formaggio F, Crisma M, Toniolo C, Millhauser GL (2000) Electron spin resonance of TOAC labeled peptides: folding transitions and high frequency spectroscopy. Biopolymers 55: 479-485.
87. Melino S, Gallo M, Trotta E, Mondello F, Paci M, Petruzzelli R (2006) Metal-binding and nuclease activity of an antimicrobial peptide analogue of the salivary histatin 5. Biochemistry 45: 15373-15383.
88. Merrifield RB (1963) Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J Am Chem Soc 85: 2149-2154.
89. 10-helices and not α-helices in aqueous solution. Nature 359: 653-655.
90. Milov AD, Tsvetkov YD, Raap J (2000a) Aggregation of trichogin analogs in weakly polar solvents: PELDOR and ESR studies. Appl Magn Reson 19: 215-226.
91. Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2000b) Self-assembling properties of membrane-modifying peptides studied by PELDOR and CW-ESR spectroscopies. J Am Chem Soc 122: 3843-3848.
92. Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2001a) The secondary structure of a membrane-modifying peptide in a supramolecular assembly studied by PELDOR and CW-ESR spectroscopies. J Am Chem Soc 123: 3784-3789.
93. Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo M, Millhauser GL, Raap J (2001b) Self-assembling properties of a membrane-modifying lipopeptaibol in weakly polar solvents studied by CW ESR. J Phys Chem B 105: 11206-11213.
94. Milov AD, Samoilova RI, Tsvetkov YD, Gusev VA, Formaggio F, Crisma M, Toniolo C, Raap J (2002) Spatial distribution of spin-labeled trichogin GA IV in the gram-positive bacterial cell membrane determined from PELDOR data. Appl Magn Reson 23: 81-95.
95. Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2003a) Self-assembling and membrane modifying properties of a lipopeptaibol studied by CW-ESR and PELDOR spectroscopies. J Pept Sci 9: 690-700.
96. Milov AD, Tsvetkov YD, Formaggio F, Oancea S, Toniolo C, Raap J (2003b) Aggregation of spin-labeled trichogin GA IV dimers: distance distribution between spin labels in frozen solutions by PELDOR data. J Phys Chem B 107: 13719-13727.
97. Milov AD, Tsvetkov YD, Formaggio F, Oancea S, Toniolo C, Raap J (2004) Solvent effect on the distance distribution between spin labels in aggregated spin-labeled trichogin GA IV dimer peptides as studied by pulsed electron-electron double resonance. Phys Chem Chem Phys 6: 3596-3603.
98. Milov AD, Erilov DA, Salnikov ES, Tsvetkov YD, Formaggio F, Toniolo C, Raap J (2005a) Structure and spatial distribution of the spin-labelled lipopeptide trichogin GA IV in a phospholipid membrane studied by pulsed electron-electron double resonance (PELDOR). Phys Chem Chem Phys 7: 1794-1799.
99. Milov AD, Samoilova RI, Tsvetkov YD, Formaggio F, Toniolo C, Raap R (2005b) Membrane-peptide interaction studied by PELDOR and CW ESR: Peptide conformations and cholesterol effect on the spatial peptide distribution in the membrane. Appl Magn Reson 29: 703-716.
100. Milov AD, Samoilova MI, Tsvetkov YD, Jost M, Peggion C, Formaggio F, Crisma M, Toniolo C, Handgraaf JW, Raap J (2007) Supramolecular structure of self-assembling alamethicin analog studied by ESR and PELDOR. Chem Biodivers 4: 1275-1298.
101. Milov AD, Samoilova RI, Tsvetkov YD, De Zotti M, Toniolo C, Raap J (2008) PELDOR conformational analysis of bis-labeled alamethicin aggregated in phospholipid vesicles. J Phys Chem B 112: 13469-13472.
102. Milov AD, Samoilova RI, Tsvetkov YD, De Zotti M, Formaggio F, Toniolo C, Handgraaf JW, Raap J (2009) Structure of self-aggregated alamethicin in ePC membranes detected by pulsed electron-electron double resonance and electron spin echo envelope modulation spectroscopies. Biophys J 96: 3197-3209.
103. α-tetrasubstituted α-aminoacid. Bioorg Med Chem 7: 119-131.
104. Monaco V, Formaggio F, Crisma M, Toniolo C, Hanson P, Millhauser GL (1999b) Orientation and immersion depth of a helical lipopeptaibol in membranes using TOAC as an ESR probe. Biopolymers 50: 239-253.
105. Moraes LG, Fázio MA, Vieira RF, Nakaie CR, Miranda MT, Schreier S, Daffre S, Miranda A (2007) Conformational and functional studies of gomesin analogues by CD, EPR and fluorescence spectroscopies. Biochim Biophys Acta 1768: 52-58.
106. Nakaie CR, Goissis G, Schreier S, Paiva ACM (1981) pH dependence of EPR spectra of nitroxides containing ionizable groups. Braz J Med Biol Res 14: 173-180.
107. Nakaie CR, Schreier S, Paiva ACM (1983) Synthesis and conformational properties of spin-labeled angiotensin derivatives. Biochim Biophys Acta 742: 63-71.
108. Nakaie CR, Marchetto R, Schreier S, Paiva ACM (1988) Synthetic and physicochemical studies of benzhydrylamine-resin with different substitution levels: implications for the solid phase peptide synthesis. In: Marshall GR (ed) Peptides. Structure and function. ESCOM, Leiden, pp 249-251.
109. Nakaie CR, Marchetto R, Schreier S, Paiva ACM (1990) High-loading effect in solid phase peptide synthesis: swelling and ESR approaches. In: Rivier JE, Marshall GR (eds) Peptides. Chemistry, structure and biology. ESCOM, Leiden, pp 1022-1023.
110. Nakaie CR, Barbosa SR, Vieira RF, Fernandez RM, Cilli EM, Castrucci AM, Visconti MA, Ito AS, Lamy-Freund MT (2001) Comparative EPR and fluorescence conformational studies of fully active spin-labeled melanotropic peptides. FEBS Lett 497: 103-107.
111. Nakaie CR, Silva EG, Cilli EM, Marchetto R, Schreier S, Paiva TB, Paiva AC (2002) Synthesis and pharmacological properties of TOAC-labeled angiotensin and bradykinin analogs. Peptides 23: 65-70.
112. Nakaie CR, Malavolta L, Schreier S, Trovatti E, Marchetto R (2006) Direct electron paramagnetic resonance monitoring of the peptide synthesis coupling reaction in polymeric support. Polymer 47: 4531-4536.
113. Nesmelov YE, Karim CB, Song L, Fajer PG, Thomas DD (2007) Rotational dynamics of phospholamban determined by multifrequency electron paramagnetic resonance. Biophys J 93: 2805-2812.
114. Newstadt JP, Mayo DJ, Inbaraj JJ, Subbaraman N, Lorigan GA (2009) Determining the helical tilt of membrane peptides using electron paramagnetic resonance spectroscopy. J Magn Reson 198: 1-7.
115. Ohnishi S, McConnell HM (1965) Interaction of the radical ion of chlorpromazine with deoxyribonucleic acid. J Am Chem Soc 87: 2293-2299.
116. Oliveira E, Cilli EM, Miranda A, Jubilut GN, Albericio F, Andreu D, Paiva ACM, Schreier S, Tominaga M, Nakaie CR (2002) Monitoring the chemical assembly of a transmembrane bradykinin receptor fragment: correlation between resin solvation, peptide chain mobility, and rate of coupling. Eur J Org Chem 21: 3686-3694.
117. Peggion C, Jost M, Baldini C, Formaggio F, Toniolo C (2007a) Total syntheses in solution of TOAC-labelled alamethicin F50/5 analogues. Chem Biodivers 4: 1183-1199.
118. Peggion C, Jost M, De Borggraeve WM, Crisma M, Formaggio F, Toniolo C (2007b) Conformational analysis of TOAC-labelled alamethicin F50/5 analogues. Chem Biodivers 4: 1256-1268.
119. Pertinhez TA, Nakaie CR, Carvalho RSH, Paiva ACM, Tabak A, Toma F, Schreier S (1995) Conformational changes upon binding of a receptor loop to lipid structures: possible role in signal transduction. FEBS Lett 375: 239-242.
120. Pertinhez TA, Nakaie CR, Paiva ACM, Schreier S (1997) Spin-labeled extracellular loop from a seven-transmembrane helix receptor: studies in solution and interaction with model membranes. Biopolymers 42: 821-829.
121. Pertinhez-Sini TA, Nakaie CR, Carvalho RSH, Paiva ACM, Tabak M, Toma F, Schreier S (1994) Binding of peptide fragments from a seven helix membrane receptor to lipid bilayers and micelles. Braz J Med Biol Res 27: 535-540.
122. Péter A, Török R, Wright K, Wakselman M, Mazaleyrat JP (2003) Liquid chromatographic enantioseparation of spin-labelled β-amino acids. J Chromatogr A 1021: 1-10.
123. Petrlova J, Hong HS, Bricarello DA, Harishchandra G, Lorigan GA, Jin LW, Voss JC (2011) A differential association of Apolipoprotein E isoforms with the amyloid-β oligomer in solution. Proteins 79: 402-416.
124. Pispisa B, Palleschi A, Stella L, Venanzi M, Toniolo C (1998) A nitroxide derivative as probe for conformational studies of short linear peptides in solution. Spectroscopic and molecular mechanics investigation. J Phys Chem B 102: 7890-7898.
125. Pispisa B, Stella L, Venanzi M, Palleschi A, Marchiori F, Polese A, Toniolo C (2000a) A spectroscopic and molecular mechanics investigation on a series of Aib-based linear peptides and a peptide template, both containing tryptophan and a nitroxide derivative as probes. Biopolymers 53: 169-181.
126. Pispisa B, Mazzuca C, Palleschi A, Stella L, Venanzi M, Formaggio F, Polese A, Toniolo C (2000b) Structural features of linear (αMe)Val-based peptides in solution by photophysical and theoretical conformational studies. Biopolymers 55: 425-435.
127. Pispisa B, Palleschi A, Stella L, Venanzi M, Mazzuca C, Formaggio F, Toniolo C, Broxterman QB (2002) Effects of helical distortions on the optical properties of amide NH infrared absorption in short peptides in solution. J Phys Chem B 106: 5733-5738.
128. Pispisa B, Mazzuca C, Palleschi A, Stella L, Venanzi M, Formaggio F, Toniolo C, Mazaleyrat JP, Wakselman M (2003a) Spectroscopic properties and conformational features of short linear peptides in solution: a fluorescence and molecular mechanics investigation. J Fluoresc 13: 139-147.
129. Pispisa B, Mazzuca C, Palleschi A, Stella L, Venanzi M, Wakselman M, Mazaleyrat JP, Rainaldi M, Formaggio F, Toniolo C (2003b) A combined spectroscopic and theoretical study of a series of conformationally restricted hexapeptides carrying a rigid binaphthyl-nitroxide donor-acceptor pair. Chem-Eur J 9: 4084-4093.
130. Polese A, Anderson DJ, Millhauser G, Formaggio F, Crisma M, Marchiori F, Toniolo C (1999) First interchain peptide interaction detected by ESR in fully synthetic, template-assisted, two-helix bundles. J Am Chem Soc 121: 11071-11078.
131. Rajca A, Kathirvelu V, Roy SK, Pink M, Rajca S, Sarkar S, Eaton SS, Eaton GR (2010) A spirocyclohexyl nitroxide amino acid spin label for pulsed EPR distance measurements. Chem-Eur J 16: 5778-5782.
132. Rassat A, Rey P (1967) Nitroxides. 23. Preparation of amino acid free radicals and their complex salts. Bull Soc Chim Fr 3: 815-818.
133. Ribeiro SCF, Schreier S, Nakaie CR, Cilli EM (2001) Effect of temperature on peptide chain aggregation: an EPR study of model peptidyl-resins. Tetrahedron Lett 42: 3243-3246.
134. Rozantsev EG (1970) Free nitroxyl radicals. Plenum, New York.
135. Sackmann E, Träuble H (1972a) Studies of the crystalline-liquid phase transition of lipid model membranes. I. Use of spin labels and optical probes as indicators of the phase transition. J Am Chem Soc 94: 4482-4491.
136. Sackmann E, Träuble H (1972b) Studies of the crystalline-liquid crystalline phase transition of lipid model membranes. II. Analysis of electron spin resonance spectra of steroid labels incorporated into lipid membranes. J Am Chem Soc 94: 4492-4498.
137. Salnikov ES, Erilov DA, Milov AD, Tsvetkov YD, Peggion C, Formaggio F, Toniolo C, Raap J, Dzuba SA (2006) Location and aggregation of the spin-labeled peptide trichogin GA IV in a phospholipid membrane as revealed by pulsed EPR. Biophys J 91: 1532-1540.
138. Salnikov ES, De Zotti M, Formaggio F, Li X, Toniolo C, O'Neil JD, Raap J, Dzuba SA, Bechinger B (2009) Alamethicin topology in phospholipid membranes by oriented solid-state NMR and EPR spectroscopies: a comparison. J Phys Chem B 113: 3034-3042.
139. Santos EL, de Picoli SK, Sabatini RA, Martin RP, Fernandes L, Nardi DT, Malavolta L, Shimuta SI, Nakaie CR, Pesquero JB (2008) Functional assessment of angiotensin II and bradykinin analogues containing the paramagnetic amino acid TOAC. Int Immunopharmacol 8: 293-299.
140. Sartori E, Corvaja C, Oancea S, Formaggio F, Crisma M, Toniolo C (2005) Linear configuration of the spins of a stable trinitroxide radical based on a ternary helical peptide. Chem Phys Chem 6: 1472-1475.
141. Saviano M, Improta R, Benedetti E, Carrozzini B, Cascarano GL, Didierjean C, Toniolo C, Crisma M (2004) Benzophenone photophore flexibility and proximity: molecular and crystal-state structure of a Bpa containing trichogin dodecapeptide analogue. Chembiochem 5: 541-544.
142. Scheerer P, Park JH, Hildebrand PW, Kim YJ, Krauss N, Choe HW, Hofmann KP, Ernst OP (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455: 497-502.
143. Schreier S, Barbosa SR, Casallanovo F, Vieira RFF, Cilli EM, Paiva ACM, Nakaie CR (2004) Conformational basis for the biological activity of TOAC-labeled angiotensin II and bradykinin. EPR, circular dichroism and fluorescence studies. Biopolymers 74: 389-402.
144. Schreier-Muccillo S, Marsh D, Dugas H, Schneider H, Smith ICP (1973) A spin probe study of the influence of cholesterol on motion and orientation of phospholipids in oriented multibilayers and vesicles. Chem Phys Lipids 10: 11-27.
145. Schwyzer R (1995) 100 years lock-and-key concept: are peptide keys shaped and guided to their receptor by the target cell membrane? Biopolymers 37: 5-16.
146. Seelig J (1970) Spin label studies of oriented smectic liquid crystals (a model system for bilayer membranes). J Am Chem Soc 92: 3881-3887.
147. Shafer AM, Nakaie CR, Deupi X, Bennett VJ, Voss JC (2008) Characterization of a conformationally sensitive TOAC spin-labeled substance P. Peptides 29: 1919-1929.
148. 10-Helical conformation of alanine-based peptides in aqueous solution: an electron spinresonance investigation. J Am Chem Soc 117: 10555-10562.
149. Stewart JM, Young JD (1984) Solid phase peptide synthesis. Pierce Chemical, Rockford.
150. Stone TJ, Buckman T, Nordio PL, McConnell HM (1965) Spin-labeled biomolecules. Proc Natl Acad Sci USA 54: 1010-1017.
151. Su X-C, Otting G (2010) Paramagnetic labeling of proteins and oligonucleotides for NMR. J Biomol NMR 46: 101-112.
152. Syryamina VN, Isaev NP, Peggion C, Formaggio F, Toniolo C, Raap J, Dzuba SA (2010) Small-amplitude backbone motions of the spin-labeled lipopeptide trichogin GA IV in a lipid membrane as revealed by electron spin echo. J Phys Chem B 114: 12277-12283.
153. Teixeira LGD, Bersanetti PA, Schreier S, Carmona AK, Nakaie CR (2007) Analogues containing the paramagnetic amino acid TOAC as substrates for angiotensin I-converting enzyme. FEBS Lett 581: 2411-2415.
154. Thomas L, Scheidt HA, Bettio A, Huster D, Beck-Sickinger AG, Arnold K, Zschörnig O (2005) Membrane interaction of neuropeptide Y detected by EPR and NMR spectroscopy. Biochim Biophys Acta 1714: 103-113.
155. Thomas L, Scheidt HA, Bettio A, Beck-Sickinger AG, Huster D, Zschörnig O (2009) The interaction of neuropeptide Y with negatively charged and zwitterionic phospholipid membranes. Eur Biophys J 38: 663-677.
156. Todd AP, Cong JP, Levinthal F, Levinthal C, Hubbell WL (1989) Site-directed mutagenesis of colicin-E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation. Proteins 6: 294-305.
157. Tominaga M, Barbosa SR, Poletti EF, Zukerman-Schpector J, Marchetto R, Schreier S, Paiva AC, Nakaie CR (2001) Fmoc-POAC: [(9-fluorenylmethyloxycarbonyl)-2, 2, 5, 5-tetramethylpyrrolidine-N-oxyl-3-amino-4-carboxylic acid]: a novel protected spin-labeled β-amino acid for peptide and protein chemistry. Chem Pharm Bull 49: 1027-1029.
158. Toniolo C, Peggion C, Crisma M, Formaggio F, Shui X, Eggleston DS (1994) Structure determination of racemic trichogin A IV using centrosymmetric crystals. Nat Struct Biol 1: 908-914.
159. α,α-disubstituted glycine. J Pept Sci 1: 45-57.
160. α-tetrasubstituted α-amino acid, is an excellent tool in material science and biochemistry. Biopolymers 47: 153-158.
161. Toniolo C, Formaggio F, Crisma M, Mazaleyrat JP, Wakselman M, George C, Deschamps JR, Flippen-Anderson JL, Pispisa B, Venanzi M, Palleschi A (1999) First peptide-based system of rigid donor-rigid interchromophore spacer-rigid acceptor: a structural and photophysical study. Chem-Eur J 5: 2254-2264.
162. Toropov YV, Dzuba SA, Tsvetkov YD, Monaco V, Formaggio F, Crisma M, Toniolo C, Raap J (1998) Molecular dynamics and spatial distribution of TOAC spin-labelled peptaibols studied in glassy liquid by echo-detected EPR spectroscopy. Appl Magn Reson 15: 237-246.
163. Träuble H, Sackmann E (1972) Studies of the crystalline-liquid crystalline phase transition of lipid model membranes. 3. Structure of a steroid-lecithin system below and above the lipid-phase transition. J Am Chem Soc 94: 4499-4510.
164. van Eps N, Anderson LL, Kisselev OG, Baranski TJ, Hubbell WL, Marshall GR (2010) Electron paramagnetic resonance studies of functionally active, nitroxide spin-labeled peptide analogues of the C-terminus of a G-protein alpha subunit. Biochemistry 49: 6877-6886.
165. Venanzi M, Valeri A, Palleschi A, Stella L, Moroder L, Formaggio F, Toniolo C, Pispisa B (2004) Structural properties and photophysical behavior of conformationally constrained hexapeptides functionalized with a new fluorescent analog of tryptophan and a nitroxide radical quencher. Biopolymers 75: 128-139.
166. Venanzi M, Gatto E, Bocchinfuso G, Palleschi A, Stella L, Formaggio F, Toniolo C (2006) Dynamics of formation of a helix-turn-helix structure in a membrane-active peptide: a time resolved spectroscopic study. Chembiochem 7: 43-45.
167. Victor KG, Cafiso DS (2001) Location and dynamics of basic peptides at the membrane interface: electron paramagnetic resonance of tetramethyl-piperidine-N-oxyl-4-amino-4-carboxylic acid-labeled peptides. Biophys J 81: 2241-2250.
168. Vieira RFF, Casallanovo F, Cilli EM, Paiva ACM, Schreier S, Nakaie CR (2002) Conformational studies of TOAC-labeled bradykinin analogues in model membranes. Lett Pept Sci 9: 83-89.
169. Vieira RFF, Casallanovo F, Marín N, Paiva AC, Schreier S, Nakaie CR (2009) Conformational properties of angiotensin II and its active and inactive TOAC-labeled analogs in the presence of micelles. Electron paramagnetic resonance, fluorescence, and circular dichroism studies. Biopolymers 92: 525-537.
170. Wilson EK (2000) A new spin: peptide probes. Chem Eng News 78: 54-59.
171. Wright K, Crisma M, Toniolo C, Török R, Péter A, Wakselman M, Mazaleyrat JP (2003a) 4-Amino-1-oxyl-2, 2, 6, 6-tetramethylpiperidine-3-carboxylic acid (β-TOAC), the first spin-labelled, cyclic, chiral β-amino acid resolved in an enantiomerically pure state. Tetrahedron Lett 44: 3381-3384.
172. Wright K, Formaggio F, Toniolo C, Török R, Péter A, Wakselman A, Mazaleyrat JP (2003b) First access to the spin-labelled β-amino acid POAC in an enantiopure state by resolution through its binaphthyl esters. Tetrahedron Lett 44: 4183-4186.
173. Wright K, de Castries A, Sarciaux M, Formaggio F, Toniolo C, Toffoletti A, Wakselman M, Mazaleyrat JP (2005) Synthesis and spectroscopic characterization of enantiopure protected trans-4-amino-1-oxyl-2, 2, 6, 6-tetramethyl piperidine-3-carboxylic acid (trans β-TOAC). Tetrahedron Lett 46: 5573-5576.
174. Wright K, Sarciaux M, de Castries A, Wakselman M, Mazaleyrat JP, Toffoletti A, Corvaja C, Crisma M, Peggion C, Formaggio F, Toniolo C (2007) Synthesis of enantiomerically pure cis- and trans-4-amino-1-oxyl-2, 2, 6, 6-tetramethylpiperidine-3-carboxylic acid: a spin-labelled, cyclic, chiral β-amino acid, and 3D-structural analysis of a doubly spin-labelled β-hexapeptide. Eur J Org Chem 2007: 3133-3144.
175. Wright K, Dutot L, Wakselman M, Mazaleyrat JP, Crisma M, Formaggio F, Toniolo C (2008) Synthesis, resolution and assignment of absolute configuration of trans 3-amino-1-oxyl-2, 2, 5, 5-tetramethylpyrrolidine-4-carboxylic acid (POAC), a cyclic, spin-labelled beta-amino acid. Tetrahedron 64: 4416-4426.
176. Wright K, Wakselman M, Mazaleyrat JP, Franco L, Toffoletti A, Formaggio F, Toniolo C (2010) Synthesis and conformational characterisation of hexameric β-peptide foldamers by using double POAC spin labelling and cw-EPR. Chem-Eur J 16: 11160-11166.
177. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
178. 2-Aib-OMe in acetonitrile. J Phys Chem B 111: 2668-2674.
179. Zhang Z, Remmer HA, Thomas DD, Karim CB (2007) Backbone dynamics determined by electron paramagnetic resonance to optimize solid-phase peptide synthesis of TOAC-labeled phospholamban. Biopolymers 88: 29-35.
180. Zhang Z, Xi X, Scholes CP, Karim CB (2008) Rotational dynamics of HIV-1 nucleocapsid protein NCp7 as probed by a spin label attached by peptide synthesis. Biopolymers 89: 1125-1135.