Advertisement

PELDOR in Peptide Research

  • Yuri D. TsvetkovEmail author
  • Michael K. Bowman
  • Yuri A. Grishin
Chapter

Abstract

The measurement of distances within and between peptides is an important application of PELDOR or DEER spectroscopy in biology. Individual measurements have been made on many proteins and provide distance information that have been vital for understanding the properties of those proteins. However, the most thoroughly studied peptides belong to the class of peptaibols.

References

  1. 1.
    Toniolo C, Crisma M, Formaggio F, Peggion C, Epand RF, Epand RM (2001) Lipopeptaibols, a novel family of membrane active, antimicrobial peptides. Cell Mol Life Sci 58(9):1179–1188.  https://doi.org/10.1007/Pl00000932CrossRefPubMedGoogle Scholar
  2. 2.
    Peggion C, Formaggio F, Crisma M, Epand RF, Epand RM, Toniolo C (2003) Trichogin: a paradigm for lipopeptaibols. J Pept Sci 9(11–12):679–689.  https://doi.org/10.1002/psc.500CrossRefPubMedGoogle Scholar
  3. 3.
    Toniolo C, Crisma M, Formaggio F, Peggion C, Monaco V, Goulard C, Rebuffat S, Bodo B (1996) Effect of N-alpha-acyl chain length on the membrane-modifying properties of synthetic analogs of the lipopeptaibol trichogin GA IV. J Am Chem Soc 118(21):4952–4958.  https://doi.org/10.1021/ja954081oCrossRefGoogle Scholar
  4. 4.
    Rebuffat S, Goulard C, Bodo B, Roquebert MF (1999) The peptaibol antibiotics from Trichoderma soil fungi; structural diversity and membrane properties. In: Pandalai SG (ed) Recent research developments in organic & bioorganic chemistry, vol 3. Transworld Research Network, Trivandrum, pp 65–91Google Scholar
  5. 5.
    Fox RO, Richards FM (1982) A voltage-gated ion channel model inferred from the crystal-structure of alamethicin at 1.5 Å resolution. Nature 300(5890):325–330.  https://doi.org/10.1038/300325a0CrossRefGoogle Scholar
  6. 6.
    Karle IL, Flippenanderson J, Sukumar M, Balaram P (1987) Conformation of a 16-residue zervamicin-iia analog peptide containing 3 different structural features—3(10)-helix, alpha-helix, and beta-bend ribbon. Proc Natl Acad Sci USA 84(15):5087–5091.  https://doi.org/10.1073/pnas.84.15.5087CrossRefPubMedGoogle Scholar
  7. 7.
    Toniolo C, Peggion C, Crisma M, Formaggio F, Shui XQ, Eggleston DS (1994) Structure determination of racemic trichogin-a-IV using centrosymmetric crystals. Nat Struct Biol 1(12):908–914.  https://doi.org/10.1038/nsb1294-908CrossRefPubMedGoogle Scholar
  8. 8.
    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(4–6):213–218.  https://doi.org/10.1023/A:1008874816982CrossRefGoogle Scholar
  9. 9.
    Toniolo C, Brückner H (2007) Topical issue: peptaibiotics. Chem Biodivers 4(6):1021–1412.  https://doi.org/10.1002/cbdv.200790093CrossRefGoogle Scholar
  10. 10.
    Brückner H, Toniolo C (2013) Special issue: peptaibiotics II. Chem Biodivers 10(5):731–961.  https://doi.org/10.1002/cbdv.201300139CrossRefGoogle Scholar
  11. 11.
    Toniolo C, Brückner H (eds) (2009) Peptaibiotics fungal peptides containing α-dialkyl α-amino acids. Wiley-VCH, WeinheimGoogle Scholar
  12. 12.
    Toniolo C, Crisma M, Formaggio F, Peggion C (2001) Control of peptide conformation by the thorpe-ingold effect (C(alpha)-tetrasubstitution). Biopolymers 60(6):396–419.  https://doi.org/10.1002/bip.10184CrossRefPubMedGoogle Scholar
  13. 13.
    Karle IL, Balaram P (1990) Structural characteristics of alpha-helical peptide molecules containing aib residues. Biochem US 29(29):6747–6756.  https://doi.org/10.1021/bi00481a001CrossRefGoogle Scholar
  14. 14.
    Toniolo C, Crisma M, Formaggio F (1998) TOAC, a nitroxide spin-labeled, achiral C(alpha)-tetrasubstituted alpha-amino acid, is an excellent tool in material science and biochemistry. Biopolymers 47(2):153–158CrossRefGoogle Scholar
  15. 15.
    Hanson P, Millhauser G, Formaggio F, Crisma M, Toniolo C (1996) ESR characterization of hexameric, helical peptides using double TOAC spin labeling. J Am Chem Soc 118(32):7618–7625.  https://doi.org/10.1021/ja961025uCrossRefGoogle Scholar
  16. 16.
    Hanson P, Anderson DJ, Martinez G, Millhauser G, Formaggio F, Crisma M, Toniolo C, Vita C (1998) Electron spin resonance and structural analysis of water soluble, alanine-rich peptides incorporating TOAC. Mol Phys 95(5):957–966.  https://doi.org/10.1080/002689798166576CrossRefGoogle Scholar
  17. 17.
    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(29):6919–6927.  https://doi.org/10.1021/ja984255cCrossRefGoogle Scholar
  18. 18.
    Bobone S, Roversi D, Giordano L, De Zotti M, Formaggio F, Toniolo C, Park Y, Stella L (2012) The lipid dependence of antimicrobial peptide activity is an unreliable experimental test for different pore models. Biochem US 51(51):10124–10126.  https://doi.org/10.1021/bi3015086CrossRefGoogle Scholar
  19. 19.
    Bobone S, Gerelli Y, De Zotti M, Bocchinfuso G, Farrotti A, Orioni B, Sebastiani F, Latter E, Penfold J, Senesi R, Formaggio F, Palleschi A, Toniolo C, Fragneto G, Stella L (2013) Membrane thickness and the mechanism of action of the short peptaibol trichogin GA IV. BBA-Biomem 1828(3):1013–1024.  https://doi.org/10.1016/j.bbamem.2012.11.033CrossRefGoogle Scholar
  20. 20.
    Tsvetkov YD, Milov AD, Maryasov AG (2008) Pulsed electron–electron double resonance (PELDOR) as EPR spectroscopy in nanometre range. Russ Chem Rev 77(6):487–520CrossRefGoogle Scholar
  21. 21.
    Milov AD, Tsvetkov YD, Gorbunova EY, Mustaeva LG, Ovchinnikova TV, Raap J (2002) Self-aggregation properties of spin-labeled zervamicin IIA as studied by PELDOR spectroscopy. Biopolymers 64(6):328–336.  https://doi.org/10.1002/bip.10208CrossRefPubMedGoogle Scholar
  22. 22.
    Milov AD, Tsvetkov YD, Gorbunova EY, Mustaeva LG, Ovchinnikova TV, Handgraaf JW, Raap J (2007) Solvent effects on the secondary structure of the membrane-active zervamicin determined by PELDOR spectroscopy. Chem Biodivers 4(6):1243–1255.  https://doi.org/10.1002/cbdv.200790107CrossRefPubMedGoogle Scholar
  23. 23.
    Toniolo C, Benedetti E (1991) The polypeptide-310-helix. Trends Biochem Sci 16(9):350–353CrossRefGoogle Scholar
  24. 24.
    Yasui SC, Keiderling TA, Bonora GM, Toniolo C (1986) Vibrational circular-dichroism of polypeptides. 5. A study of 310-helical-octapeptides. Biopolymers 25(1):79–89.  https://doi.org/10.1002/bip.360250107CrossRefGoogle Scholar
  25. 25.
    Crisma M, Formaggio F, Moretto A, Toniolo C (2006) Peptide helices based on alpha-amino acids. Biopolymers 84(1):3–12.  https://doi.org/10.1002/bip.20357CrossRefPubMedGoogle Scholar
  26. 26.
    Toniolo C (1980) Intramolecularly hydrogen-bonded peptide conformations. CRC Cr Rev Bioch Mol 9(1):1–44.  https://doi.org/10.3109/10409238009105471CrossRefGoogle Scholar
  27. 27.
    Crisma M, De Zotti M, Moretto A, Peggion C, Drouillat B, Wright K, Couty F, Toniolo C, Formaggio F (2015) Single and multiple peptide gamma-turns: literature survey and recent progress. New J Chem 39(5):3208–3216.  https://doi.org/10.1039/c4nj01564aCrossRefGoogle Scholar
  28. 28.
    Armen R, Alonso DOV, Daggett V (2003) The role of α-, 310-, and π-helix in helix → coil transitions. Protein Sci 12(6):1145–1157.  https://doi.org/10.1110/ps02040103CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Millhauser GL (1995) Views of helical peptides—a proposal for the position of 310-helix along the thermodynamic folding pathway. Biochem US 34(12):3873–3877.  https://doi.org/10.1021/bi00012a001CrossRefGoogle Scholar
  30. 30.
    Milov AD, Maryasov AG, Tsvetkov YD, Raap J (1999) Pulsed ELDOR in spin-labeled polypeptides. Chem Phys Lett 303(1–2):135–143.  https://doi.org/10.1016/S0009-2614(99)00220-1CrossRefGoogle Scholar
  31. 31.
    Milov AD, Maryasov AG, Samoilova RI, Tsvetkov YD, Raap J, Monaco V, Formaggio F, Crisma M, Toniolo C (2000) Pulsed double electron–electron resonance in spin-labeled polypeptides data on the secondary structure. Dokl Akad Nauk 370(2):265–268Google Scholar
  32. 32.
    Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2001) The secondary structure of a membrane-modifying peptide in a supramolecular assembly studied by PELDOR and CW-ESR spectroscopies. J Am Chem Soc 123(16):3784–3789.  https://doi.org/10.1021/ja0033990CrossRefPubMedGoogle Scholar
  33. 33.
    Milov AD, Tsvetkov YD, Raap J, De Zotti M, Formaggio F, Toniolo C (2016) Conformation, self-aggregation, and membrane interaction of peptaibols as studied by pulsed electron double resonance spectroscopy. Biopolymers 106(1):6–24.  https://doi.org/10.1002/bip.22713CrossRefPubMedGoogle Scholar
  34. 34.
    Milov AD, Tsvetkov YD, Maryasov AG, Gobbo M, Prinzivalli C, De Zotti M, Formaggio F, Toniolo C (2012) Conformational properties of the spin-labeled tylopeptin B and heptaibin peptaibiotics based on PELDOR spectroscopy data. Appl Magn Reson 44(4):495–508.  https://doi.org/10.1007/s00723-012-0402-1CrossRefGoogle Scholar
  35. 35.
    Milov AD, Tsvetkov YD, De Zotti M, Prinzivalli C, Biondi B, Formaggio F, Toniolo C, Gobbo M (2013) Aggregation modes of the spin mono-labeled tylopeptin B and heptaibin peptaibiotics in frozen solutions of weak polarity as studied by PELDOR spectroscopy. J Struct Chem 54:S73–S85.  https://doi.org/10.1134/S0022476613070056CrossRefGoogle Scholar
  36. 36.
    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(43):13469–13472.  https://doi.org/10.1021/Jp8046714CrossRefPubMedGoogle Scholar
  37. 37.
    Milov AD, Tsvetkov YD, Formaggio F, Oancea S, Toniolo C, Raap J (2003) Aggregation of spin labeled trichogin GA IV dimers: distance distribution between spin labels in frozen solutions by PELDOR data. J Phys Chem B 107(49):13719–13727.  https://doi.org/10.1021/jp035057xCrossRefGoogle Scholar
  38. 38.
    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(13):3596–3603.  https://doi.org/10.1039/b313701eCrossRefGoogle Scholar
  39. 39.
    Milov AD, Tsvetkov YD, Maryasov AG, Gobbo M, Prinzivalli C, De Zotti M, Formaggio F, Toniolo C (2013) Conformational properties of the spin-labeled tylopeptin B and heptaibin peptaibiotics based on PELDOR spectroscopy data. Appl Magn Reson 44(4):495–508.  https://doi.org/10.1007/s00723-012-0402-1CrossRefGoogle Scholar
  40. 40.
    Milov AD, Tsvetkov YD, Bortolus M, Maniero AL, Gobbo M, Toniolo C, Formaggio F (2014) Synthesis and conformational properties of a TOAC doubly spin-labeled analog of the medium-length, membrane active peptaibiotic ampullosporin A as revealed by CD, fluorescence, and EPR spectroscopies. Biopolymers 102(1):40–48.  https://doi.org/10.1002/bip.22362CrossRefPubMedGoogle Scholar
  41. 41.
    Rabenstein MD, Shin YK (1995) Determination of the distance between 2 spin labels attached to a macromolecule. Proc Natl Acad Sci USA 92(18):8239–8243.  https://doi.org/10.1073/pnas.92.18.8239CrossRefPubMedGoogle Scholar
  42. 42.
    Bortolus M, Tombolato F, Tessari I, Bisaglia M, Mammi S, Bubacco L, Ferrarini A, Maniero AL (2008) Broken helix in vesicle and micelle-bound alpha-synuclein: insights from site-directed spin labeling-EPR experiments and MD simulations. J Am Chem Soc 130(21):6690–6691.  https://doi.org/10.1021/jaB010429CrossRefPubMedGoogle Scholar
  43. 43.
    Karle IL (1994) Diffraction studies of model and natural helical peptides. In: White SH (ed) Membrane protein structure: experimental approaches. Springer, New York, pp 355–380.  https://doi.org/10.1007/978-1-4614-7515-6Google Scholar
  44. 44.
    Balashova TA, Shenkarev ZO, Tagaev AA, Ovchinnikova TV, Raap J, Arseniev AS (2000) NMR structure of the channel-former zervamicin IIB in isotropic solvents. FEBS Lett 466(2–3):333–336.  https://doi.org/10.1016/S0014-5793(99)01707-XCrossRefPubMedGoogle Scholar
  45. 45.
    Peggion C, Coin I, Toniolo C (2004) Total synthesis in solution of alamethicin F50/5 by an easily tunable segment condensation approach. Biopolymers 76(6):485–493.  https://doi.org/10.1002/bip.20161CrossRefPubMedGoogle Scholar
  46. 46.
    Crisma M, Peggion C, Baldini C, MacLean EJ, Vedovato N, Rispoli G, Toniolo C (2007) Crystal structure of a spin-labeled, channel-forming alamethicin analogue. Angew Chem Int Edit 46(12):2047–2050.  https://doi.org/10.1002/anie.200604417CrossRefGoogle Scholar
  47. 47.
    Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2000) Self-assembling properties of membrane-modifying peptides studied by PELDOR and CW-ESR spectroscopies. J Am Chem Soc 122(16):3843–3848.  https://doi.org/10.1021/ja993870tCrossRefGoogle Scholar
  48. 48.
    Milov AD, Tsvetkov YD, Raap J (2000) Aggregation of trichogin analogs in weakly polar solvents: PELDOR and ESR studies. Appl Magn Reson 19(2):215–226.  https://doi.org/10.1007/Bf03162276CrossRefGoogle Scholar
  49. 49.
    Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Raap J (2003) Self-assembling and membrane modifying properties of a lipopeptaibol studied by CW-ESR and PELDOR spectroscopies. J Pept Sci 9(11–12):690–700.  https://doi.org/10.1002/psc.513CrossRefPubMedGoogle Scholar
  50. 50.
    Milov AD, Tsvetkov YD, Formaggio F, Crisma M, Toniolo C, Millhauser GL, Raap J (2001) Self-assembling properties of a membrane-modifying lipopeptaibol in weakly polar solvents, studied by CW ESR. J Phys Chem B 105(45):11206–11213.  https://doi.org/10.1021/Jp011948yCrossRefGoogle Scholar
  51. 51.
    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(6):1275–1298.  https://doi.org/10.1002/cbdv.200790110CrossRefPubMedGoogle Scholar
  52. 52.
    Milov AD, Samoilova RI, Tsvetkov YD, Peggion C, Formaggio F, Toniolo C, Raap J (2006) Aggregation of spin-labeled alamethicin in low-polarity solutions as studied by PELDOR spectroscopy. Dokl Phys Chem 406:21–25.  https://doi.org/10.1134/S0012501606010064CrossRefGoogle Scholar
  53. 53.
    Marsh D (1989) Experimental methods in spin-label spectral analysis. In: Berliner LJ, Reuben J (eds) Spin labeling, theory and applications. Biological magnetic resonance, vol 8. Plenum Press, New York, pp 255–303.  https://doi.org/10.1007/978-1-4613-0743-3Google Scholar
  54. 54.
    Stella L, Mazzuca C, Venanzi M, Palleschi A, Didone M, Formaggio F, Toniolo C, Pispisa B (2004) Aggregation and water-membrane partition as major determinants of the activity of the antibiotic peptide trichogin GA IV. Biophys J 86(2):936–945CrossRefGoogle Scholar
  55. 55.
    Kropacheva TN, Raap J (2002) Ion transport across a phospholipid membrane mediated by the peptide trichogin GA IV. Biochim Biophys Acta (BBA)—Biomemb 1567:193–203.  https://doi.org/10.1016/s0005-2736(02)00616-8CrossRefGoogle Scholar
  56. 56.
    Milov AD, Samoilova RI, Tsvetkov YD, Formaggio F, Toniolo C, Raap J (2005) 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(4):703–716.  https://doi.org/10.1007/Bf03166345CrossRefGoogle Scholar
  57. 57.
    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(4):1532–1540.  https://doi.org/10.1529/biophysj.105.075887CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Milov AD, Erilov DA, Salnikov ES, Tsvetkov YD, Formaggio F, Toniolo C, Raap J (2005) 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(8):1794–1799.  https://doi.org/10.1039/b418414aCrossRefPubMedGoogle Scholar
  59. 59.
    Milov AD, Samoilova RI, Tsvetkov YD, Formaggio F, Toniolo C, Raap J (2007) Self-aggregation of spin-labeled alamethicin in ePC vesicles studied by pulsed electron–electron double resonance. J Am Chem Soc 129(30):9260–9261.  https://doi.org/10.1021/ja072851dCrossRefPubMedGoogle Scholar
  60. 60.
    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(7):2698–2705.  https://doi.org/10.1529/biophysj.107.115287CrossRefPubMedGoogle Scholar
  61. 61.
    Salnikov ES, De Zotti M, Formaggio F, Li X, Toniolo C, O’Neil JDJ, 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(10):3034–3042.  https://doi.org/10.1021/jp8101805CrossRefPubMedGoogle Scholar
  62. 62.
    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(8):3197–3209.  https://doi.org/10.1016/j.bpj.2009.01.026CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    North CL, BarrangerMathys M, Cafiso DS (1995) Membrane orientation of the N-terminal segment of alamethicin determined by solid-state N-15 NMR. Biophys J 69(6):2392–2397CrossRefGoogle Scholar
  64. 64.
    Salnikov ES, Friedrich H, Li X, Bertani P, Reissmann S, Hertweck C, O’Neil JDJ, Raap J, Bechinger B (2009) Structure and alignment of the membrane-associated peptaibols ampullosporin A and alamethicin by oriented N-15 and P-31 solid-state NMR spectroscopy. Biophys J 96(1):86–100.  https://doi.org/10.1529/biophysj.108.136242CrossRefPubMedGoogle Scholar
  65. 65.
    Marsh D, Jost M, Peggion C, Toniolo C (2007) Lipid chain-length dependence for incorporation of alamethicin in membranes: electron paramagnetic resonance studies on TOAC-spin labeled analogs. Biophys J 92(11):4002–4011.  https://doi.org/10.1529/biophysj.107.104026CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Parsegian VA, Fuller N, Rand RP (1979) Measured work of deformation and repulsion of lecithin bilayers. Proc Natl Acad Sci USA 76(6):2750–2754.  https://doi.org/10.1073/pnas.76.6.2750CrossRefPubMedGoogle Scholar
  67. 67.
    Murzyn K, Rog T, Blicharski W, Dutka M, Pyka J, Szytula S, Froncisz W (2006) Influence of the disulfide bond configuration on the dynamics of the spin label attached to cytochrome c. Proteins-Struct Funct Bioinform 62(4):1088–1100.  https://doi.org/10.1002/prot.20838CrossRefGoogle Scholar
  68. 68.
    Spaar A, Munster C, Salditt T (2004) Conformation of peptides in lipid membranes studied by X-ray grazing incidence scattering. Biophys J 87(1):396–407.  https://doi.org/10.1529/biophysj.104.040667CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Reginsson GW, Schiemann O (2011) Studying bimolecular complexes with pulsed electron–electron double resonance spectroscopy. Biochem Soc T 39:128–139.  https://doi.org/10.1042/Bst0390128CrossRefGoogle Scholar
  70. 70.
    Goobes G, Stayton PS, Drobny GP (2007) Solid-state NMR studies of molecular recognition at protein-mineral interfaces. Prog Nucl Mag Res Sp 50(2–3):71–85.  https://doi.org/10.1016/j.pnmrs.2006.11.002CrossRefGoogle Scholar
  71. 71.
    Mirau PA, Naik RR, Gehring P (2011) Structure of peptides on metal oxide surfaces probed by NMR. J Am Chem Soc 133(45):18243–18248.  https://doi.org/10.1021/ja205454tCrossRefPubMedGoogle Scholar
  72. 72.
    Milov AD, Samoilova RI, Tsvetkov YD, Peggion C, Formaggio F, Toniolo C (2014) Peptides on the surface. PELDOR data for spin-labeled alamethicin F50/5 analogues on organic sorbent. J Phys Chem B 118(25):7085–7090.  https://doi.org/10.1021/jp503691nCrossRefGoogle Scholar
  73. 73.
    Syryamina VN, Samoilova RI, Tsvetkov YD, Ischenko AV, De Zotti M, Gobbo M, Toniolo C, Formaggio F, Dzuba SA (2016) Peptides on the surface: spin-label EPR and PELDOR study of adsorption of the antimicrobial peptides trichogin GA IV and ampullosporin A on the silica nanoparticles. Appl Magn Reson 47(3):309–320.  https://doi.org/10.1007/s00723-015-0745-5CrossRefGoogle Scholar
  74. 74.
    Banham JE, Baker CM, Ceola S, Day IJ, Grant GH, Groenen EJJ, Rodgers CT, Jeschke G, Timmel CR (2008) Distance measurements in the borderline region of applicability of CW EPR and DEER: a model study on a homologous series of spin-labelled peptides. J Magn Reson 191(2):202–218.  https://doi.org/10.1016/j.jmr.2007.11.023CrossRefPubMedGoogle Scholar
  75. 75.
    Stoller S, Sicoli G, Baranova TY, Bennati M, Diederichsen U (2011) TOPP: a novel nitroxide-labeled amino acid for EPR distance measurements. Angew Chem Int Edit 50(41):9743–9746CrossRefGoogle Scholar
  76. 76.
    Yang ZY, Kise D, Saxena S (2010) An approach towards the measurement of nanometer range distances based on Cu2+ ions and ESR. J Phys Chem B 114(18):6165–6174.  https://doi.org/10.1021/jp911637sCrossRefPubMedGoogle Scholar
  77. 77.
    Yang ZY, Ji M, Saxena S (2010) Practical aspects of copper ion-based double electron electron resonance distance measurements. Appl Magn Reson 39(4):487–500.  https://doi.org/10.1007/s00723-010-0181-5CrossRefGoogle Scholar
  78. 78.
    Maryasov AG, Tsvetkov YD, Raap J (1998) Weakly coupled radical pairs in solids: ELDOR in ESE structure studies. Appl Magn Reson 14(1):101–113.  https://doi.org/10.1007/Bf03162010CrossRefGoogle Scholar
  79. 79.
    Jun S, Becker JS, Yonkunas M, Coalson R, Saxena S (2006) Unfolding of alanine-based peptides using electron spin resonance distance measurements. Biochem US 45(38):11666–11673.  https://doi.org/10.1021/bi061195bCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Yuri D. Tsvetkov
    • 1
    Email author
  • Michael K. Bowman
    • 2
  • Yuri A. Grishin
    • 3
  1. 1.The Voevodsky Institute of Chemical Kinetics and CombustionNovosibirskRussia
  2. 2.Department of Chemistry and BiochemistryUniversity of AlabamaTuscaloosaUSA
  3. 3.The Voevodsky Institute of Chemical Kinetics and CombustionNovosibirskRussia

Personalised recommendations