Studying biomolecular complexes with pulsed electron-electron double resonance spectroscopy

Biochemical Society Transactions

Volumn 39, Issue 1, 2011, Pages 128-139

  Reginsson, Gunnar W ^a   Schiemann, Olav ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

Biomolecular complex; Double electron electron resonance (DEER); Electron paramagnetic resonance (EPR); Pulsed electron electron double resonance (PELDOR); Spin labelling

Indexed keywords

COPPER; DNA; FLAVOPROTEIN; NITROXIDE; RIBONUCLEOTIDE REDUCTASE;

ANALYTIC METHOD; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONFERENCE PAPER; ELECTRON; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ESCHERICHIA COLI; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOURIER TRANSFORMATION; MAGNETIC FIELD; MOLECULE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARACOCCUS DENITRIFICANS; PRIORITY JOURNAL; PULSED ELECTRON ELECTRON DOUBLE RESONANCE SPECTROSCOPY; SPECTROSCOPY; SPIN LABELING; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEINS; SPIN LABELS;

EID: 79551492492     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390128     Document Type: Conference Paper

References (84)

1. Svejstrup, J.Q., Vichi, P. and Egly, J.-M. (1996) The multiple roles of transcription/repair factor TFIIH. Trends Biochem. Sci. 21, 346-350
2. Lehmann, A.R. (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85, 1101-1111
3. Whittle, P.J. and Blundell, T.L. (1994) Protein structure-based drug design. Annu. Rev. Biophys. Biomol. Struct. 23, 349-375
4. Drenth, J. (1999) Principles of Protein X-Ray Crystallography, Springer-Verlag, Berlin
5. Wagner, G., Hyberts, S.G. and Havel, T.F. (1992) NMR Structure Determination In Solution: a critique and comparison with X-ray crystallography. Annu. Rev. Biophys. Biomol. Struct. 21, 167-198
6. Schiemann, O. and Prisner, T.F. (2007) Long-range distance determinations in bimacromolecules by EPR spectroscopy. Q. Rev. Biophys. 40, 1-53
7. Agafonov, R.V., Negrashov, I.V., Tkachev, Y.V., Blakely, S.E., Titus, M.A., Thomas, D.D. and Nesmelov, Y.E. (2009) Structural dynamics of the myosin relay helix by time-resolved EPR and FRET. Proc. Natl. Acad. Sci. U.S.A. 106, 21625-21630
8. Schiemann, O., Fritscher, J., Kisseleva, N., Sigurdsson, S.T. and Prisner, T.F. (2003) Structural investigation of a high-affinity Mn(II) binding site in the hammerhead ribozyme by EPR spectroscopy and DFT calculations: effects of neomycin B on metal-ion binding. ChemBioChem 4, 1057-1065
9. Hunsicker-Wang, L., Vogt, M. and DeRose, V.J. (2009) EPR methods to study specific metal-ion binding sites in RNA. Methods Enzymol. 468, 335-367
10. Elsässer, C., Brecht, M. and 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, 12606-12611
11. Ohnishi, T., Ragan, I. and Hatefi, Y. (1985) EPR studies of iron-sulfur clusters in isolated subunits and subfractions of NADH-ubiquinone oxidoreductase. J. Biol. Chem. 260, 2782-2788
12. Borovykh, I.V., Ceola, S., Gajula, P., Gast, P., Steinhoff, H.-J. and Huber, M. (2006) Distance between a native cofactor and a spin label in the reaction centre of Rhodobacter sphaeroides by a two-frequency pulsed electron paramagnetic resonance method and molecular dynamics simulations. J. Magn. Reson. 180, 178-185
13. Savitsky, A., Dubinskii, A.A., Flores, M., Lubitz, W. and Möbius, K. (2007) Orientation-resolving pulsed electron dipolar high-field EPR spectroscopy on disordered solids. I. Structure of spin-correlated radical pairs in bacterial photosynthetic reaction centers. J. Phys. Chem. B 111, 6245-6262
14. Denysenkov, V.P., Biglino, D., Lubitz, W., Prisner, T. and Bennati, M. (2008) Structure of the tyrosyl biradical in mouse R2 ribonucleotide reductase from high-field PELDOR. Angew. Chem. Int. Ed. 47, 1224-1227
15. Schiemann, O., Piton, N., Mu, Y., Stock, G., Engels, J.W. and Prisner, T.F. (2004) A PELDOR-based nanometer distance ruler for oligonucleotides. J. Am. Chem. Soc. 126, 5722-5729
16. Piton, N., Schiemann, O., Mu, Y., Stock, G., Prisner, T.F. and Engels, J.W. (2005) Synthesis of spin-labeled RNAs for long range distance measurements by PELDOR. Nucleosides, Nucleotides Nucleic Acids 24, 771-775
17. Piton, N., Mu, Y., Stock, G., Prisner, T., Schiemann, O. and Engels, J.W. (2007) Base-specific spin-labeling of RNA for structure determination. Nucleic Acids Res. 35, 3128-3143
18. Rao, J.N., Jao, C.C., Hegde, B.G., Lange, R. and Ulmer, T.S. (2010) A combinatorial NMR and EPR approach for evaluating the structural ensemble of partially folded proteins. J. Am. Chem. Soc. 132, 8657-8668
19. Qin, P.Z. and Dieckmann, T. (2004) Application of NMR and EPR methods to the study of RNA. Curr. Opin. Struct. Biol. 14, 350-359
20. Yang, Y., Ramelot, T.A., McCarrick, R.M., Ni, S., Feldmann, E.A., Cort, J.R., Wang, H., Ciccosanti, C., Jian, M., Janjua, H. et al. (2010) Combining NMR and EPR methods for homodimer protein structure determination. J. Am. Chem. Soc. 132, 11910-11913
21. Hagelueken, G., Ingledew, W.J., Huang, H., Petrovic-Stojanovska, B., Whitfield, C., El Mkami, H., Schiemann, O. and Naismith, J.H. (2009) PELDOR spectroscopy distance fingerprinting of the octameric outer-membrane protein Wza from Escherichia coli. Angew. Chem. Int. Ed. 48, 1-4
22. Griffith, O.H. and Waggoner, A.S. (1969) Nitroxide free radicals: spin labels for probing biomolecular structure. Acc. Chem. Res. 2, 17-24
23. Columbus, L. and Hubbell, W.L. (2002) A new spin on protein dynamics. Trends Biochem. Sci. 27, 288-295
24. Owenius, R., Engström, M. and Lindgren, M. (2001) Influence of solvent polarity and hydrogen bonding on the EPR parameters of a nitroxide spin label studied by 9-GHz and 95-GHz EPR spectroscopy and DFT calculations. J. Phys. Chem. A 105, 10967-10977
25. Hyodo, F., Matsumoto, S., Devasahayam, N., Dharmaraj, C., Subramanian, S., Mitchell, J.B. and Krishna, M.C. (2009) Pulsed EPR imaging of nitroxides in mice. J. Magn. Reson. 197, 181-185
26. Yang, Z., Becker, J. and Saxena, S. (2007) On Cu(II)-Cu(II) distance measurements using pulsed electron electron double resonance. J. Magn. Reson. 188, 337-343
27. Kisseleva, N., Khvorova, A., Westhof, E. and Schiemann, O. (2005) Binding of manganese(II) to a tertiary stabilized hammerhead ribozyme as studied by electron paramagnetic resonance spectroscopy. RNA 11, 1-6
28. 3+ complexes as potential spin labels for high field pulsed EPR distance measurements. J. Am. Chem. Soc. 129, 14138-14139
29. 3+ spin labeling. J. Am. Chem. Soc. 132, 9040-9048
30. Potapov, A., Song, Y., Meade, T.J., Goldfarb, D., Astashkin, A.V. and Raitsimring, A.M. (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, 38-49
31. Hubbell, W.L., Cafiso, D.S. and Altenbach, C. (2000) Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7, 735-739
32. Berliner, L.J. (2010) Spin labeling: a modern perspective. In Stable Radicals: Fundamentals and Applied Aspects of Odd-Electron Compounds (Hicks, R., ed.), John Wiley and Sons, Hoboken
33. Klare, J. and Steinhoff, H.-J. (2009) Spin labeling EPR. Photosynth. Res. 102, 377-390
34. Newstadt, J.P., Mayo, D.J., Inbaraj, J.J., Subbaraman, N. and Lorigan, G.A. (2009) Determining the helical tilt of membrane peptides using electron paramagnetic resonance spectroscopy. J. Magn. Reson. 198, 1-7
35. Wright, K., Wakselman, M., Mazaleyrat, J.-P., Franco, L., Toffoletti, A., Formaggio, F. and Toniolo, C. (2010) Synthesis and conformational characterisation of hexameric β-peptide foldamers by using double POAC spin labelling and cw-EPR. Chemistry 16, 11160-11166
36. Popova, A.M. and Qin, P.Z. (2010) A nucleotide-independent nitroxide probe reports on site-specific stereomeric environment in DNA. Biophys. J. 99, 2180-2189
37. Cai, Q., Kusnetzow, A.K., Hubbell, W.L., Haworth, I.S., Gacho, G.P.C., Eps, N.V., Hideg, K., Chambers, E.J. and Qin, P.Z. (2006) Site-directed spin labeling measurements of nanometer distances in nucleic acids using a sequence-independent nitroxide probe. Nucleic Acids Res. 34, 4722-4730
38. Edwards, T.E., Okonogi, T.M., Robinson, B.H. and Sigurdsson, S.T. (2001) Site-specific incorporation of nitroxide spin-labels into internal sites of the TAR RNA; structure-dependent dynamics of RNA by EPR spectroscopy. J. Am. Chem. Soc. 123, 1527-1528
39. Schiemann, O., Weber, A., Edwards, T.E., Prisner, T.F. and Sigurdsson, S.T. (2003) Nanometer distance measurements on RNA using PELDOR. J. Am. Chem. Soc. 125, 3434-3435
40. Jakobsen, U., Shelke, S., Vogel, S. and Sigurdsson, S.T. (2010) Site-directed spin-labeling of nucleic acids by click chemistry: detection of abasic sites in duplex DNA by EPR spectroscopy. J. Am. Chem. Soc. 132, 10424-10428
41. Giordano, C., Fratini, F., Attanasio, D. and Cellai, L. (2011) Preparation of spin-labeled 2-amino-dA, dA, dC and 5-methyl-dC phosphoramidites for the automatic synthesis of EPR active oligonucleotides. Synthesis 4, 565-572
42. Ding, P., Wunnicke, D., Steinhoff, H.J. and Seela, F. (2010) Site-directed spin-labeling of DNA by the azide-alkyne 'click' reaction: nanometre distance measurements on 7-deaza-2′-deoxyadenosine and 2′-deoxyuridine nitroxide conjugates spatially separated or linked to a 'dA-dT' base pair. Chem. Eur. J. 16, 14385-14396
43. Schiemann, O., Piton, N., Plackmeyer, J., Prisner, T.F. and Engels, J.W. (2007) Spin labeling of oligonucleotides with the nitroxide TPA and use of PELDOR, a pulse EPR method, to measure intramolecular distances. Nat. Protoc. 2, 904-923
44. Zhang, X., Cekan, P., Sigurdsson, S.T. and Qin, P.Z. (2009) Studying RNA using site-directed spin-labeling and continuous-wave electron paramagnetic resonance spectroscopy. Methods Enzymol. 469, 303-328
45. Barhate, N., Cekan, P., Massey, A.P. and Sigurdsson, S.T. (2007) A nucleoside that contains a rigid nitroxide spin label: a fluorophore in disguise. Angew. Chem. Int. Ed. 46, 2655-2658
46. Cekan, P., Jonsson, E. Ö. and Sigurdsson, S.T. (2009) Folding of the cocaine aptamer studied by EPR and fluorescence spectroscopies using the bifunctional spectroscopic probe Ç. Nucleic Acids Res. 37, 3990-3995
47. Shelke, S. and Sigurdsson, S.T. (2010) Noncovalent and site-directed spin labeling of nucleic acids. Angew. Chem. 49, 7984-7986
48. Schweiger, A. and Jeschke, G. (2001) Principles of Pulse Electron Paramagnetic Resonance. Oxford University Press, Oxford
49. Weil, J.A. and Bolton, J.R. (2007) Electron Paramagnetic Resonance: Elementary Theory and Practical Applications. John Wiley and Sons, Hoboken
50. Weber, A., Schiemann, O., Bode, B. and Prisner, T.F. (2002) PELDOR at S- and X-band frequencies and the separation of exchange coupling from dipolar coupling. J. Magn. Reson. 157, 277-285
51. Riplinger, C., Kao, J.P. Y., Rosen, G.M., Kathirvelu, V., Eaton, G.R., Eaton, S.S., Kutateladze, A. and Neese, F. (2009) Interaction of radical pairs through-bond and through-space: scope and limitations of the point-dipole approximation in electron paramagnetic resonance spectroscopy. J. Am. Chem. Soc. 131, 10092-10106
52. Bode, B.E., Plackmeyer, J., Prisner, T.F. and 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, 5064-5073
53. Berliner, L.J. and Krishna, N.R. (2000) Biological Magnetic Resonance 17: Structural Computation and Dynamics in Proteins, Kluwer Academic/Plenum Publishers, New York
54. Hustedt, E.J. and Beth, A.H. (1999) Nitroxide spin-spin interactions: applications to protein structure and dynamics. Ann. Rev. Biophys. Biomol. Struct. 28, 129-153
55. Otteman, K.M., Thorgeirsson, T.E., Kolodziej, A.F., Shin, Y.-K. and Koshland, D.E. (1998) Direct measurement of small ligand-induced conformational changes in the aspartate chemoreceptor using EPR. Biochemistry 37, 7062-7069
56. Milov, A.D., Salikhov, K.M. and Shirov, M.D. (1981) Application of the double resonance method to electron spin echo in a study of the spatial distribution of paramagnetic centers in solids. Sov. Phys. Solid State 23, 565-569
57. Larsen, R.G. and Singel, D.J. (1993) Double electron-electron resonance spin-echo modulation: spectroscopic measurement of electron spin pair separations in orientationally disordered solids. J. Chem. Phys. 98, 5134-5146
58. Milov, A.D., Maryasov, A.G., Tsvetkov, Y.D. and Raap, J. (1999) Pulsed ELDOR in spin-labeled polypeptides. Chem. Phys. Lett. 303, 135-143
59. Martin, R.E., Pannier, M., Diederich, F., Gramlich, V., Hubrich, M. and Spiess, H.W. (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. Ed. 37, 2833-2837
60. Pannier, M., Veit, S., Godt, A., Jeschke, G. and Spiess, H.W. (2000) Dead-time free measurement of dipole-dipole interactions between electron spins. J. Magn. Reson. 142, 331-340
61. Jeschke, G. (2002) Distance measurements in the nanometer range by pulse EPR. ChemPhysChem 3, 927-932
62. Bode, B.E., Margraf, D., Plackmeyer, J., Dürner, G., Prisner, T.F. and Schiemann, O. (2008) Counting the monomers in nanometer-sized oligomers by pulsed electron-electron double resonance. J. Am. Chem. Soc. 129, 6736-6745
63. Jeschke, G. and Polyhach, Y. (2007) Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance. Phys. Chem. Chem. Phys. 9, 1895-1910
64. Tscetkov, Y.D., Milov, A.D. and Maryasov, A.G. (2008) Pulsed electron-electron double resonance (PELDOR) as EPR spectroscopy in nanometer range. Russ. Chem. Rev. 77, 487-520
65. Jeschke, G., Panek, G., Godt, A., Bender, A. and Paulsen, H. (2004) Data analysis procedures for pulse ELDOR measurements of broad distance distributions. Appl. Magn. Reson. 26, 223-244
66. Jeschke, G., Chechik, I.P., Godt, A., Zimmermann, H., Banham, J., Timmel, C.R. and Jung, H. (2006) DeerAnalysis2006: a comprehensive software package for analyzing pulsed ELDOR data. Appl. Magn. Reson. 30, 473-498
67. Sicoli, G., Wachowius, F., Bennati, M. and Höbartner, C. (2010) Probing secondary structures of spin-labeled RNA by pulsed EPR spectroscopy. Angew. Chem. Int. Ed. 49, 6443-6447
68. Krstić, I., Frolow, O., Sezer, D., Endeward, B., Weigand, J.E., Suess, B., Engels, J.W. and Prisner, T. (2010) PELDOR spectroscopy reveals preorganization of the neomycin-responsive riboswitch tertiary structure. J. Am. Chem. Soc. 132, 1454-1455
69. Dockter, C., Volkov, A., Bauer, C., Polyhach, Y., Joly-Lopez, Z. and Jeschke, G. (2009) Refolding of the integral membrane proteins light-harvesting complex II monitored by pulse EPR. Proc. Am. Chem. Soc. 106, 18485-18490
70. Swanson, M.A., Kathirvelu, V., Majtan, T., Frerman, F.E., Eaton, G.R. and Eaton, S.S. (2009) DEER distance measurement between a spin label and a native FAD semiquinone in electron transfer flavoprotein. J. Am. Chem. Soc. 131, 15978-15979
71. Tsvetkov, Y.D., Milov, A.D. and Maryasov, A.G. (1998) Pulsed elecron double resonance (PELDOR) and its applications in free-radicals research. Appl. Magn. Reson. 15, 107-143
72. Schiemann, O., Cekan, P., Margraf, D., Prisner, T.F. and Sigurdsson, S.T. (2009) Relative orientation of rigid nitroxides by PELDOR: beyond distance measurements in nucleic acids. Angew. Chem. Int. Ed. 48, 3292-3295
73. Endeward, B., Butterwick, J.A., MacKinnon, R. and 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, 15246-15250
74. Denysenkov, V.P., Prisner, T.F., Stubbe, J. and 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. U.S.A. 103, 13386-13390
75. Margraf, D., Cekan, P., Prisner, T., Sigurdsson, S.T. and Schiemann, O. (2009) Ferro- and antiferromagnetic exchange coupling constants in PELDOR spectra. Phys. Chem. Chem. Phys. 11, 6708-6714
76. II-salen complexes in DNA. Angew. Chem. Int. Ed. 49, 4927-4929
77. Upadhyay, A.K., Borbat, P.P., Wang, J., Freed, J.H. and Edmondson, D.E. (2008) Determination of the oligomeric states of human and rat monoamine oxidases in the outer mitochondrial membrane and octyl β-D-glucopyranoside micelles using pulsed dipolar electron spin resonance spectroscopy. Biochemistry. 47, 1554-1566
78. + antiporter of E. coli. Biophys. J. 89, 1328-1338
79. Bode, B.E., Plackmeyer, J., Bolte, M., Prisner, T. and Schiemann, O. (2009) PELDOR on an exchange coupled nitroxide copper(II) spin pair. J. Organomet. Chem. 694, 1172-1179
80. Narr, E., Godt, A. and 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. Ed. 41, 3907-3910
81. Amsterdam, I.M. C.v., Ubbink, M., Canters, G.W. and Huber, M. (2003) Measurement of a Cu-Cu distance of 26 Å by a pulsed EPR method. Angew. Chem. Int. Ed. 42, 62-64
82. Kay, C.W. M., El Mkami, H., Cammack, R. and Evans, R.W. (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
83. Dole, F., Medina, M., More, C., Cammack, R., Bertrand, P. and Guigliarelli, B. (1996) Spin-spin interactions between the Ni site and the [4Fe-4S] centers as a probe of light-induced structural changes in active Desulfovibrio gigas hydrogenase. Biochemistry 35, 16399-16406
84. Cruickshank, P.A.S., Bolton, D.R., Robertson, D.A., Hunter, R.I., Wylde, R.J. and Smith, G.M. (2009) A kilowatt pulsed 94 GHz electron paramagnetic resonance spectrometer with high concentration sensitivity, high instantaneous bandwidth, and low dead time. Rev. Sci. Instrum. 80, 103102