Orientation-Selective DEER Using Rigid Spin Labels, Cofactors, Metals, and Clusters

Part of the Structure and Bonding book series (STRUCTURE, volume 152)


The dipolar interaction between two paramagnetic centres depends upon their spin–spin distance and relative orientation. Generally most experiments are carried out under conditions where the DEER signal only reports on the spin–spin distances and, for this type of data, sophisticated analysis methods for obtaining distance distributions have been developed. Recently there have been an increasing number of studies on systems where the DEER signals depend upon both distance and spin pair orientation. These investigations have relied on the use of rigid spin labels (those with a well-defined spatial position) and/or spectrometers operating at Q-band frequencies and above capable of performing DEER experiments with high resolution and sensitivity. In this article we discuss in detail orientation-selective DEER experiments for which the modulation depth and the dipolar frequencies depend on the relative orientation of the two paramagnetic centres and the distance. Analysis of the data in the presence of distance and orientation distributions is discussed, and representative examples from the literature are given for systems containing spin labels, organic cofactors, metals, and metal clusters.


Distance measurement DEER EPR ESR Metal Metal cluster Orientation selection PELDOR Spin label Structural information 



Double electron—electron resonance


Double–quantum coherence


Pulsed electron—nuclear double resonance


Electron paramagnetic resonance


Full width half maximum




Hyperfine sublevel correlation






Observer-selective DEER


Pulsed electron—electron double resonance


Relaxation-induced dipole modulation enhancement


Travelling wave tube amplifier


Zero-field splitting


  1. 1.
    Ward R, Bowman A, Sozudogru E, El-Mkami H, Owen-Hughes T, Norman DG (2010) EPR distance measurements in deuterated proteins. J Magn Reson (San Diego, Calif: 1997) 207(1):164–167. doi: 10.1016/j.jmr.2010.08.002 Google Scholar
  2. 2.
    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. doi: 10.1016/j.jmr.2007.11.023 CrossRefGoogle Scholar
  3. 3.
    Schweiger A, Jeschke G (2001) Principles of pulse electron paramagnetic resonance. Oxford University Press, Inc., New YorkGoogle Scholar
  4. 4.
    Milov AD, Ponomarev AB, Tsvetkov YD (1984) Electron electron double resonance in electron-spin-echo – model biradical systems and the sensitized Photolysis of Decalin. Chem Phys Lett 110(1):67–72CrossRefGoogle Scholar
  5. 5.
    Milov AD, Salikhov KM, Schirov MD (1981) Application of ENDOR in Electron-Spin Echo for Paramagnetic Center Space Distributions in Solids. Fiz Tverd Tela 23(4):975–982Google Scholar
  6. 6.
    Martin RE, Pannier M, Diederich F, Gramlich V, Hubrich M, Spiess HW (1998) Determination of end-to-end distances in a series of TEMPO diradicals of up to 2.8 nm length with a new four–pulse double electron electron resonance experiment. Angew Chem Int Edit 37:2834–2837CrossRefGoogle Scholar
  7. 7.
    Pannier M, Veit S, Godt A, Jeschke G, Spiess HW (2000) Dead-time free measurement of dipole–dipole interactions between electron spins. J Magn Reson 142(2):331–340CrossRefGoogle Scholar
  8. 8.
    Astashkin AV, Hara H, Kawamori A (1998) The pulsed electron—electron double resonance and “2+1” electron spin echo study of the oriented oxygen-evolving and Mn-depleted preparations of photosystem II. J Chem Phys 108(9):3805–3812CrossRefGoogle Scholar
  9. 9.
    Saxena S, Freed JH (1997) Theory of double quantum two-dimensional electron spin resonance with application to distance measurements. J Chem Phys 107(5):1317–1340CrossRefGoogle Scholar
  10. 10.
    Kulik LV, Paschenko SV, Dzuba SA (2002) 130 GHz ESEEM induced by electron–electron interaction in biradical. J Magn Reson 159(2):237–241. doi: 10.1016/s1090-7807(02)00038-1 CrossRefGoogle Scholar
  11. 11.
    Milikisyants S, Scarpelli F, Finiguerra MG, Ubbink M, Huber M (2009) A pulsed EPR method to determine distances between paramagnetic centers with strong spectral anisotropy and radicals: the dead-time free RIDME sequence. J Magn Reson 201:48–56CrossRefGoogle Scholar
  12. 12.
    Astashkin AV, Elmore BO, Fan W, Guillemette JG, Feng C (2010) Pulsed EPR determination of the distance between heme iron and FMN centers in a human inducible nitric oxide synthase. J Am Chem Soc 132:12059–12067CrossRefGoogle Scholar
  13. 13.
    Savitsky A, Dubinskii AA, Zimmermann H, Lubitz W, Mobius K (2011) High-field dipolar electron paramagnetic resonance (EPR) spectroscopy of nitroxide biradicals for determining three-dimensional structures of biomacromolecules in disordered solids. J Phys Chem B 115(41):11950–11963. doi: 10.1021/jp206841v CrossRefGoogle Scholar
  14. 14.
    Jeschke G, Koch A, Jonas U, Godt A (2002) Direct conversion of EPR dipolar time evolution data to distance distributions. J Magn Reson 155:72–82CrossRefGoogle Scholar
  15. 15.
    Chiang Y-W, Borbat PP, Freed JH (2005) The determination of pair distance distributions by pulsed ESR using Tikhonov regularization. J Magn Reson 172:279–295CrossRefGoogle Scholar
  16. 16.
    Jeschke G, Chechik V, Ionita P, Godt A, Zimmermann H, Banham J, Timmel CR, Hilger D, Jung H (2006) DeerAnalysis2006 – a comprehensive software package for analyzing pulsed ELDOR data. Appl Magn Reson 30(3–4):473–498CrossRefGoogle Scholar
  17. 17.
    Marko A, Denysenkov VP, Margraf D, Cekan P, Schiemann O, Sigurdsson ST, Prisner T (2011) Conformational flexibility of DNA. J Am Chem Soc 133:13375–13379CrossRefGoogle Scholar
  18. 18.
    Fleissner MR, Bridges MD, Brooks EK, Cascio D, Kálai T, Hideg K, Hubbell WL (2011) Structure and dynamics of a conformationally constrained nitroxide side chain and applications in EPR spectroscopy. Proc Natl Acad Sci U S A 108:16241–16246CrossRefGoogle Scholar
  19. 19.
    Milikisyants S, Groenen EJJ, Huber M (2008) Observer-selective double electron–electron-spin resonance, a pulse sequence to improve orientation selection. J Magn Reson 192:275–279CrossRefGoogle Scholar
  20. 20.
    Borbat PP, Freed JH (2012) Pulse dipolar ESR: distance measurements. In: Timmel CR, Harmer JR (eds) Spin-labels and intrinsic paramagnetic centres in the biosciences: structural information from distance measurements. Struct Bond. Springer-Verlag, Berlin Heidelberg. doi: 10.1007/430_2012_82 Google Scholar
  21. 21.
    Borbat PP, Georgieva ER, Freed JH (2013) Improved sensitivity for long-distance measurements in biomolecules: five-pulse double electron electron resonance. J Phys Chem Lett 4:170–175. doi: 10.1021/jz301788n CrossRefGoogle Scholar
  22. 22.
    Tkach I, Sicoli G, Hobartner C, Bennati M (2011) A dual-mode microwave resonator for double electron–electron spin resonance spectroscopy at W-band microwave frequencies. J Magn Reson 209(2):341–346. doi: 10.1016/j.jmr.2011.01.012 CrossRefGoogle Scholar
  23. 23.
    Tkach I, Pornsuwan S, Höbartner C, Wachowius F, Sigurdsson ST, Baranova TY, Diederichsen U, Sicoli G, Bennati M (2013) Orientation selection in distance measurements between nitroxide spin labels at 94 GHz EPR with variable dual frequency irradiation. Phys Chem Chem Phys 15:3433–3437CrossRefGoogle Scholar
  24. 24.
    Kaminker I, Tkach I, Manukovsky N, Huber T, Yagi H, Otting G, Bennati M, Goldfarb D (2013) W-band orientation selective DEER measurements on a Gd3+/nitroxide mixed-labeled protein dimer with a dual mode cavity. J Magn Reson 227:66–71CrossRefGoogle Scholar
  25. 25.
    Dubinskii AA, Grishin YA, Savitsky AN, Möbius K (2002) Submicrosecond field-jump device for pulsed high-field ELDOR. Appl Magn Reson 22:369–386CrossRefGoogle Scholar
  26. 26.
    Tsvetkov YD, Grishin YA (2009) Techniques for EPR spectroscopy of pulsed electron double resonance (PELDOR): a review. Instrum Exp Tech 52:615–636CrossRefGoogle Scholar
  27. 27.
    Kaminker I, Florent M, Epel B, Goldfarb D (2011) Simultaneous acquisition of pulse EPR orientation selective spectra. J Magn Reson 208(1):95–102. doi: 10.1016/j.jmr.2010.10.010 CrossRefGoogle Scholar
  28. 28.
    Weber A, Schiemann O, Bode B, Prisner TF (2002) PELDOR at S- and X-band frequencies and the separation of exchange coupling from dipolar coupling. J Magn Reson 157(2):277–285. doi: 10.1006/jmre.2002.2596 CrossRefGoogle Scholar
  29. 29.
    Bode B, Plackmeyer J, Bolte M, Prisner T, Schiemann O (2009) PELDOR on an exchange coupled nitroxide copper(II) spin pair. J Organomet Chem 694:1172–1179CrossRefGoogle Scholar
  30. 30.
    Margraf D, Cekan P, Prisner TF, Sigurdsson ST, Schiemann O (2009) Ferro- and antiferromagnetic exchange coupling constants in PELDOR spectra. Phys Chem Chem Phys 11(31):6708–6714. doi: 10.1039/b905524j CrossRefGoogle Scholar
  31. 31.
    Larsen RG, Singel DJ (1993) Double electron—electron resonance spin-echo modulation – spectroscopic measurement of electron-spin pair separations in orientationally disordered solids. J Chem Phys 98(7):5134–5146. doi: 10.1063/1.464916 CrossRefGoogle Scholar
  32. 32.
    Polyhach Y, Godt A, Bauer C, Jeschke G (2007) Spin pair geometry revealed by high-field DEER in the presence of conformational distributions. J Magn Reson 185(1):118–129. doi: 10.1016/j.jmr.2006.11.012 CrossRefGoogle Scholar
  33. 33.
    Margraf D, Bode BE, Marko A, Schiemann O, Prisner TF (2007) Conformational flexibility of nitroxide biradicals determined by X-band PELDOR experiments. Mol Phys 105(15–16):2153–2160. doi: 10.1080/00268970701724982 CrossRefGoogle Scholar
  34. 34.
    Lovett JE, Bowen AM, Timmel CR, Jones MW, Dilworth JR, Caprotti D, Bell SG, Wong LL, Harmer J (2009) Structural information from orientationally selective DEER spectroscopy. Phys Chem Chem Phys 11(31):6840–6848. doi: 10.1039/b907010a CrossRefGoogle Scholar
  35. 35.
    Marko A, Margraf D, Yu H, Mu Y, Stock G, Prisner T (2009) Molecular orientation studies by pulsed electron—electron double resonance experiments. J Chem Phys 130(6). doi:06410210.1063/1.3073040Google Scholar
  36. 36.
    Marko A, Margraf D, Cekan P, Sigurdsson ST, Schiemann O, Prisner TF (2010) Analytical method to determine the orientation of rigid spin labels in DNA. Phys Rev E 81(2):9. doi:02191110.1103/PhysRevE.81.021911Google Scholar
  37. 37.
    Jeschke G (2011) Interpretation of Dipolar EPR Data in Terms of Protein Structure. In: Timmel CR, Harmer JR (eds) Spin-labels and intrinsic paramagnetic centres in the Biosciences: Structural information from distance measurements. Struct Bond. Springer-Verlag, Berlin Heidelberg. doi: 10.1007/430_2011_61 Google Scholar
  38. 38.
    Mims WB (1972) In: Geschwind S (ed) Electron paramagnetic resonance. Plenum, New York, pp 263–351Google Scholar
  39. 39.
    Abe C, Klose D, Dietrich F, Ziegler WH, Polyhach Y, Jeschke G, Steinhoff H-J (2012) Orientation selective DEER measurements on vinculin tail at X-band frequencies reveal spin label orientations. J Magn Reson 216:53–61. doi: 10.1016/j.jmr.2011.12.024 CrossRefGoogle Scholar
  40. 40.
    Marko A, Prisner T (2013) An algorithm to analyze PELDOR data of rigid spin label pairs. Phys Chem Chem Phys 15:619–627CrossRefGoogle Scholar
  41. 41.
    Song L, Larion M, Chamoun J, Bonora M, Fajer P (2010) Distance and dynamics determination by W-band DEER and W-band ST-EPR. Eur Biophys J 39:711–719CrossRefGoogle Scholar
  42. 42.
    Godt A, Schulte M, Zimmermann H, Jeschke G (2006) How flexible are poly(para-phenyleneethynylene)s? Angew Chem Int Edit 45(45):7560–7564CrossRefGoogle Scholar
  43. 43.
    Raitsimring A, Astashkin A, Enemark JH, Blank A, Twig Y, Song Y, Meade TJ (2011) Dielectric Resonator for Ka-band pulsed EPR measurements at cryogenic temperatures: probe head construction and applications. Appl Magn Reson 42(4):441–452. doi: 10.1007/s00723-012-0313-1 CrossRefGoogle Scholar
  44. 44.
    Song Y, Meade TJ, Astashkin AV, Klein EL, Enemark JH, Raitsimring A (2011) Pulsed dipolar spectroscopy distance measurements in biomacromolecules labeled with Gd(III) markers. J Magn Reson 210(1):59–68. doi: 10.1016/j.jmr.2011.02.010 CrossRefGoogle Scholar
  45. 45.
    Polyhach Y, Bordignon E, Tschaggelar R, Gandra S, Godt A, Jeschke G (2012) High sensitivity and versatility of the DEER experiment on nitroxide radical pairs at Q-band frequencies. Phys Chem Chem Phys 14:10762–10773CrossRefGoogle Scholar
  46. 46.
    Endeward B, Butterwick JA, MacKinnon R, Prisner T (2009) Pulsed electron—electron double-resonance determination of spin-label distances and orientations on the tetrameric potassium ion channel KcsA. J Am Chem Soc 131:15246–15250CrossRefGoogle Scholar
  47. 47.
    Sicoli G, Argirevic T, Stubbe J, Tkach I, Bennati M (2010) Effects in 94 GHz orientation-selected PELDOR on a rigid pair of radicals with non-collinear axes. Appl Magn Reson 37(1–4):539–548. doi: 10.1007/s00723-009-0094-3 CrossRefGoogle Scholar
  48. 48.
    Goldfarb D, Lipkin Y, Potapov A, Gorodetsky Y, Epel B, Raitsimring AM, Radoul M, Kaminker I (2008) HYSCORE and DEER with an upgraded 95 GHz pulse EPR spectrometer. J Magn Reson 194(1):8–15. doi: 10.1016/j.jmr.2008.05.019 CrossRefGoogle Scholar
  49. 49.
    Cruickshank PAS, Bolton DR, Robertson DA, Hunter RI, Wylde RJ, Smith GM (2009) A kilowatt pulsed 94 GHz electron paramagnetic resonance spectrometer with high concentration sensitivity, high instantaneous bandwidth, and low dead time. Rev Sci Inst 80:103101–103115Google Scholar
  50. 50.
    Denysenkov VP, Prisner TF, Stubbe J, Bennati M (2006) High-field pulsed electron—electron double resonance spectroscopy to determine the orientation of the tyrosyl radicals in ribonucleotide reductase. Proc Natl Acad Sci USA 103(36):13386–13390. doi: 10.1073/pnas.0605851103 CrossRefGoogle Scholar
  51. 51.
    Denysenkov VP, Biglino D, Lubitz W, Prisner TF, Bennati M (2008) Structure of the tyrosyl biradical in mouse R2 ribonucleotide reductase from high-field PELDOR. Angew Chem Int Edit 47(7):1224–1227. doi: 10.1002/anie.200703753 CrossRefGoogle Scholar
  52. 52.
    Gajula P, Milikisyants S, Steinhoff HJ, Huber M (2007) A short note on orientation selection in the DEER experiments on a native cofactor and a spin label in the reaction center of Rhodobacter sphaeroides. Appl Magn Reson 31(1–2):99–104CrossRefGoogle Scholar
  53. 53.
    Flores M, Savitsky A, Paddock ML, Abresch EC, Dubinskii AA, Okamura MY, Lubitz W, Mobius K (2010) Electron–nuclear and electron–electron double resonance spectroscopies show that the primary quinone acceptor Q(A) in reaction centers from photosynthetic bacteria Rhodobacter sphaeroides remains in the same orientation upon light-induced reduction. J Phys Chem B 114(50):16894–16901. doi: 10.1021/jp107051r CrossRefGoogle Scholar
  54. 54.
    Sicoli G, Wachowius F, Bennati M, Hobartner C (2010) Probing secondary structures of spin-labeled RNA by pulsed EPR spectroscopy. Angew Chem Int Edit 49:6443–6447CrossRefGoogle Scholar
  55. 55.
    Kuznetsov NA, Milov AD, Isaev NP, Vorobjev YN, Koval VV, Dzuba SA, Fedorova OS, Tsvetkov YD (2011) PELDOR analysis of enzyme-induced structural changes in damaged DNA duplexes. Mol Biosyst 7:2670–2680CrossRefGoogle Scholar
  56. 56.
    Reginsson GW, Shelke SA, Rouillon C, White MF, Sigurdsson ST, Schiemann O (2012) Protein-induced changes in DNA structure and dynamics observed with noncovalent site-directed spin labeling and PELDOR. Nucl Acids Res 41(1):e11. doi: 10.1093/nar/gks817
  57. 57.
    Wunnicke D, Ding P, Seela F, Steinhoff HJ (2012) Site-directed spin labeling of DNA reveals mismatch-induced nanometer distance changes between flanking nucleotides. J Phys Chem B 116(14):4118–4123. doi: 10.1021/jp212421c CrossRefGoogle Scholar
  58. 58.
    Barhate N, Cekan P, Massey AP, Sigurdsson ST (2007) A nucleoside that contains a rigid nitroxide spin label: a fluorophore in disguise. Angew Chem Int Edit 46:2655–2658CrossRefGoogle Scholar
  59. 59.
    Schiemann O, Cekan P, Margraf D, Prisner TF, Sigurdsson ST (2009) Relative orientation of rigid nitroxides by PELDOR: beyond distance measurements in nucleic acids. Angew Chem Int Edit 48(18):3292–3295. doi: 10.1002/anie.200805152 CrossRefGoogle Scholar
  60. 60.
    Shelke SA, Sigurdsson ST (2012) Site-directed nitroxide spin labeling of biopolymers. In: Timmel CR, Harmer J (eds) Spin-labels and intrinsic paramagnetic centres in the biosciences: structural information from distance measurements. Structure and Bonding. Springer, Berlin Heidelberg. doi: 10.1007/430_2011_62 Google Scholar
  61. 61.
    Ward R, Schiemann O (2012) Structural information from oligonucleotides. In: Timmel CR, Harmer J (eds) Spin-labels and intrinsic paramagnetic centres in the biosciences: structural information from distance measurements. Structure and bonding. Springer, Berlin Heidelberg. doi: 10.1007/430_2012_76 Google Scholar
  62. 62.
    Stoll S, Schweiger A (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J Magn Reson 178:42–55CrossRefGoogle Scholar
  63. 63.
    Narr E, Godt A, Jeschke G (2002) Selective measurements of a nitroxide–nitroxide separation of 5 nm and a nitroxide–copper separation of 2.5 nm in a terpyridine-based copper(II) complex by pulse EPR spectroscopy. Angew Chem Int Edit 41(20):3907–3910. doi: 10.1002/1521-3773(20021018)41:20<3907::aid-anie3907>;2-t CrossRefGoogle Scholar
  64. 64.
    van Amsterdam IMC, Ubbink M, Canters GW, Huber M (2003) Measurement of a Cu–Cu distance of 26 Angstrom by a pulsed EPR method. Angew Chem Int Ed 42(1):62–64CrossRefGoogle Scholar
  65. 65.
    Kay CWM, El Mkami H, Cammack R, Evans RW (2007) Pulsed ELDOR determination of the intramolecular distance between the metal binding sites in dicupric human serum transferrin and lactoferrin. J Am Chem Soc 129:4868–4869. doi: 10.1021/ja068966j CrossRefGoogle Scholar
  66. 66.
    Becker J, Saxena S (2005) Double quantum coherence electron spin resonance on coupled Cu(II)–Cu(II) electron spins. Chem Phys Lett 414:248–252CrossRefGoogle Scholar
  67. 67.
    Yang Z, Becker J, Saxena S (2007) On Cu(II)–Cu(II) distance measurements using pulsed electron electron double resonance. J Magn Reson 188(2):337–343. doi: 10.1016/j.jmr.2007.08.006 CrossRefGoogle Scholar
  68. 68.
    Yang Z, Kise D, Saxena S (2010) An approach towards the measurement of nanometer range distances based on Cu2+ Ions and ESR. J Phys Chem B 114:6165–6174CrossRefGoogle Scholar
  69. 69.
    Bode BE, Plackmeyer J, Prisner TF, Schiemann O (2008) PELDOR measurements on a nitroxide-labeled Cu(II) porphyrin: orientation selection, spin-density distribution, and conformational flexibility. J Phys Chem A 112(23):5064–5073. doi: 10.1021/jp710504k CrossRefGoogle Scholar
  70. 70.
    Yang Z, Ji M, Saxena S (2010) Practical aspects of copper ion-based double electron electron resonance distance measurements. Appl Magn Res 39:487–500CrossRefGoogle Scholar
  71. 71.
    Maryasov AG, Tsvetkov YD, Raap J (1998) Weakly coupled radical pairs in solids: ELDOR in ESE structure studies. Appl Magn Reson 14:101–113CrossRefGoogle Scholar
  72. 72.
    Yang Z, Kurpiewski MR, Ji M, Townsend JE, Mehta P, Jen-Jacobson L, Saxena S (2012) ESR spectroscopy identifies inhibitory Cu2+ sites in a DNA-modifying enzyme to reveal determinants of catalytic specificity. Proc Natl Acad Sci U S A 109:6366Google Scholar
  73. 73.
    Bowen AM (2012) Magnetic Resonance Studies of Proteins and Model Systems. University of Oxford, Oxford, (DPhil thesis)Google Scholar
  74. 74.
    Bencini A, Gatteschi D (1990) EPR of exchange coupled systems. Springer-Verlag, BerlinGoogle Scholar
  75. 75.
    Mouesca JM, Noodleman L, Case DA, Lamotte B (1995) Spin-densities and spin coupling in iron–sulfur clusters – a new analysis of hyperfine coupling-constants. Inorg Chem 34(17):4347–4359CrossRefGoogle Scholar
  76. 76.
    Kappl R, Ebelshauser M, Hannemann F, Bernhardt R, Huttermann J (2006) Probing electronic and structural properties of the reduced [2Fe–2S] cluster by orientation-selective H-1 ENDOR spectroscopy: Adrenodoxin versus Rieske iron-sulfur protein. Appl Magn Reson 30(3–4):427–459CrossRefGoogle Scholar
  77. 77.
    Abdalla JAB, Bowen AM, Bell SG, Wong LL, Timmel CR, Harmer J (2012) Characterisation of the paramagnetic [2Fe–2S]+ centre in palustrisredoxin-B (PuxB) from Rhodopseudomonas palustris CGA009: g-matrix determination and spin coupling analysis. Phys Chem Chem Phys 14:6526–6537CrossRefGoogle Scholar
  78. 78.
    Elsässer C, Brecht M, Bittl R (2002) Pulsed electron—electron double resonance on multinuclear metal clusters: assignment of spin projection factors based on the dipolar interaction. J Am Chem Soc 124(42):12606–12611. doi: 10.1021/ja027348+ CrossRefGoogle Scholar
  79. 79.
    Elsässer C, Brecht M, Bittl R (2005) Treatment of spin-coupled metal-centres in pulsed electron—electron double-resonance experiments. Biochem Soc Trans 33:15–19CrossRefGoogle Scholar
  80. 80.
    Roessler MM, King MS, Robinson AJ, Armstrong FA, Harmer J, Hirst J (2010) Direct assignment of EPR spectra to structurally defined iron–sulfur clusters in complex I by double electron—electron resonance. Proc Natl Acad Sci U S A 107(5):1930–1935. doi: 10.1073/pnas.0908050107 CrossRefGoogle Scholar
  81. 81.
    Raitsimring A, Gunanathan C, Potapov A, Efremenko I, Martin JML, Milstein D, Goldfarb D (2007) Gd3+ complexes as potential spin labels for high field pulsed EPR distance measurements. J Am Chem Soc 129:14138–14139CrossRefGoogle Scholar
  82. 82.
    Potapov A, Song Y, Meade TJ, Goldfarb D, Astashkin AV, Raitsimring A (2010) Distance measurements in model bis-Gd(III) complexes with flexible “bridge”. Emulation of biological molecules having flexible structure with Gd(III) labels attached. J Magn Reson 205(1):38–49. doi: 10.1016/j.jmr.2010.03.019 CrossRefGoogle Scholar
  83. 83.
    Potapov A, Yagi H, Huber T, Jergic S, Dixon NE, Otting G, Goldfarb D (2010) Nanometer-scale distance measurements in proteins using Gd3+ spin labeling. J Am Chem Soc 132(26):9040–9048. doi: 10.1021/ja1015662 CrossRefGoogle Scholar
  84. 84.
    Gordon-Grossman M, Kaminker I, Gofman Y, Shai Y, Goldfarb D (2011) W-Band pulse EPR distance measurements in peptides using Gd3+-dipicolinic acid derivatives as spin labels. Phys Chem Chem Phys 13(22):10771–10780. doi: 10.1039/c1cp00011j CrossRefGoogle Scholar
  85. 85.
    Yagi H, Banerjee D, Graham B, Huber T, Goldfarb D, Otting G (2011) Gadolinium tagging for high-precision measurements of 6 nm distances in protein assemblies by EPR. J Am Chem Soc 133:10418–10421CrossRefGoogle Scholar
  86. 86.
    Lueders P, Jeschke G, Yulikov M (2011) Double electron—electron resonance measured between Gd3+ ions and nitroxide radicals. J Phys Chem Lett 2:604–609CrossRefGoogle Scholar
  87. 87.
    Kaminker I, Yagi H, Huber T, Feintuch A, Otting G, Goldfarb D (2012) Spectroscopic selection of distance measurements in a protein dimer with mixed nitroxide and Gd3+ spin labels. Phys Chem Chem Phys 14(13):4355–4358. doi: 10.1039/c2cp40219j CrossRefGoogle Scholar
  88. 88.
    Yulikov M, Lueders P, Warsi MF, Chechik V, Jeschke G (2012) Distance measurements in Au nanoparticles functionalized with nitroxide radicals and Gd3+-DTPA chelate complexes. Phys Chem Chem Phys 14:10732–10746CrossRefGoogle Scholar
  89. 89.
    Goldfarb D (2012) Metal-based spin labeling for distance determination. In: Timmel CR, Harmer J (eds) Spin-labels and intrinsic paramagnetic centres in the biosciences: structural information from distance measurements. Structure and bonding. Springer-Verlag, Berlin Heidelberg. doi: 10.1007/430_2011_63 Google Scholar
  90. 90.
    Hara H, Kawamori A, Astashkin AV, Ono T (1996) The distances from tyrosine D to redox-active components on the donor side of Photosystem II determined by pulsed electron—electron double resonance. Biochim Biophys Acta Bioenerg 1276(2):140–146CrossRefGoogle Scholar
  91. 91.
    Banerjee D, Yagi H, Huber T, Otting G, Goldfarb D (2012) Nanometer-range distance measurement in a protein using Mn2+ tags. J Physl Chem Lett 3(2):157–160. doi: 10.1021/jz201521d CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of Chemistry, Centre for Advanced Electron Spin ResonanceUniversity of OxfordOxfordUK
  2. 2.Centre for Advanced ImagingUniversity of QueenslandSt LuciaAustralia

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