Abstract
Electron Paramagnetic Resonance (EPR) has a long history with the first spectrum being reported in 1945 (Zavoisky 1945) and is adopted widely, in its original continuous wave (CW) form, as a tool for the analysis of both biological systems and materials bearing unpaired electrons. The related technique of “Nuclear Magnetic Resonance” (NMR) developed rapidly thanks to the technological advances that enabled the use of pulsed radiofrequency and Fourier Transformation (FT). In EPR, the challenges posed by needing to generate short and very powerful microwave pulses and the fast relaxation times, of the electron spin, led to a much slower adaptation of pulsed excitation schemes. Nevertheless, early experiments using an NMR spectrometer with a greatly reduced magnetic field had shown the feasibility of pulse EPR (Blume 1958). It was not until the availability of commercial systems in the 1980s that this technique began to be applied more widely outside laboratories focused on the development of instrumentation. Over the last decades the application of pulse EPR has seen a very wide variety of systems studied from biological systems to those of materials science. This development was paralleled by a constant innovation in EPR instrumentation and methodology. Recent success in using arbitrary waveform generators (AWGs) and the commercial implementation and user uptake indicates that EPR is just entering a new era with tremendous opportunities offered by bespoke excitation schemes.
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References
Abdullin D, Duthie F, Meyer A, Muller ES, Hagelueken G, Schiemann O (2015) Comparison of PELDOR and RIDME for distance measurements between nitroxides and low-spin Fe(III) ions. J Phys Chem B 119(43):13534–13542. https://doi.org/10.1021/acs.jpcb.5b02118
Ackermann K, Bode BE (2018) Pulse EPR distance measurements to study multimers and multimerisation. Mol Phys 116(12):1513–1521. https://doi.org/10.1080/00268976.2017.1421324
Ackermann K, Giannoulis A, Cordes DB, Slawin AMZ, Bode BE (2015) Assessing dimerisation degree and cooperativity in a biomimetic small-molecule model by pulsed EPR. Chem Commun 51(84):15472. https://doi.org/10.1039/c5cc90439k
Ackermann K, Pliotas C, Valera S, Naismith JH, Bode BE (2017) Sparse labeling PELDOR spectroscopy on multimeric mechanosensitive membrane channels. Biophys J 113(9):1968–1978. https://doi.org/10.1016/j.bpj.2017.09.005
Akhmetzyanov D, Ching HYV, Denysenkov V, Demay-Drouhard P, Bertrand HC, Tabares LC, Policar C, Prisner TF, Un S (2016) RIDME spectroscopy on high-spin Mn2+ centers. Phys Chem Chem Phys 18(44):30857–30866. https://doi.org/10.1039/c6cp05239h
Blume RJ (1958) Electron spin relaxation times in sodium-ammonia solutions. Phys Rev 109(6):1867–1873. https://doi.org/10.1103/PhysRev.109.1867
Bode BE, Margraf D, Plackmeyer J, Durner G, Prisner TF, Schiemann O (2007) Counting the monomers in nanometer-sized oligomers by pulsed electron—electron double resonance. J Am Chem Soc 129(21):6736–6745. https://doi.org/10.1021/ja065787t
Borbat PP, Freed JH (1999) Multiple-quantum ESR and distance measurements. Chem Phys Lett 313(1–2):145–154. https://doi.org/10.1016/S0009-2614(99)00972-0
Bowen AM, Erlenbach N, van Os P, Stelzl LS, Sigurdsson ST, Prisner TF (2018) Orientation selective 2D-SIFTER experiments at X-Band frequencies. Appl Magn Reson 49(12):1355–1368. https://doi.org/10.1007/s00723-018-1057-3
Bowman A, Hammond CM, Stirling A, Ward R, Shang WF, El-Mkami H, Robinson DA, Svergun DI, Norman DG, Owen-Hughes T (2014) The histone chaperones Vps75 and Nap1 form ring-like, tetrameric structures in solution. Nucleic Acids Res 42(9):6038–6051. https://doi.org/10.1093/nar/gku232
Cieslak JA, Focia PJ, Gross A (2010) Electron spin-echo envelope modulation (ESEEM) reveals water and phosphate interactions with the KcsA potassium channel. Biochem-US 49(7):1486–1494. https://doi.org/10.1021/bi9016523
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 Instrum 80(10):103102. https://doi.org/10.1063/1.3239402
Deligiannakis Y, Louloudi M, Hadjiliadis N (2000) Electron spin echo envelope modulation (ESEEM) spectroscopy as a tool to investigate the coordination environment of metal centers. Coord Chem Rev 204:1–112. https://doi.org/10.1016/S0010-8545(99)00218-0
Dockter C, Volkov A, Bauer C, Polyhach Y, Joly-Lopez Z, Jeschke G, Paulsen H (2009) Refolding of the integral membrane protein light-harvesting complex II monitored by pulse EPR. Proc Natl Acad Sci USA 106(44):18485–18490. https://doi.org/10.1073/pnas.0906462106
Doll A, Jeschke G (2014) Fourier-transform electron spin resonance with bandwidth-compensated chirp pulses. J Magn Reson 246:18–26. https://doi.org/10.1016/j.jmr.2014.06.016
Doll A, Jeschke G (2016) EPR-correlated dipolar spectroscopy by Q-band chirp SIFTER. Phys Chem Chem Phys 18(33):23111–23120. https://doi.org/10.1039/c6cp03067j
El Mkami H, Norman DG (2015) EPR distance measurements in deuterated proteins. Method Enzym 564:125–152. https://doi.org/10.1016/bs.mie.2015.05.027
Georgieva ER, Borbat PP, Norman HD, Freed JH (2015) Mechanism of influenza A M2 transmembrane domain assembly in lipid membranes. Sci Rep-UK 5:11757. https://doi.org/10.1038/srep11757
Giannoulis A, Ward R, Branigan E, Naismith JH, Bode BE (2013) PELDOR in rotationally symmetric homo-oligomers. Mol Phys 111(18–19):2845–2854. https://doi.org/10.1080/00268976.2013.798697
Giannoulis A, Oranges M, Bode BE (2017) Monitoring complex formation by relaxation-induced pulse electron paramagnetic resonance distance measurements. ChemPhysChem 18(17):2318–2321. https://doi.org/10.1002/cphc.201700666
Giannoulis A, Motion CL, Oranges M, Buhl M, Smith GM, Bode BE (2018) Orientation selection in high-field RIDME and PELDOR experiments involving low-spin Co-II ions. Phys Chem Chem Phys 20(4):2151–2154. https://doi.org/10.1039/c7cp07248a
Jeschke G, Polyhach Y (2007) Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance. Phys Chem Chem Phys 9(16):1895–1910. https://doi.org/10.1039/b614920k
Jeschke G, Pannier M, Godt A, Spiess HW (2000) Dipolar spectroscopy and spin alignment in electron paramagnetic resonance. Chem Phys Lett 331(2–4):243–252. https://doi.org/10.1016/S0009-2614(00)01171-4
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):473–498. https://doi.org/10.1007/Bf03166213
Kaur H, Abreu B, Akhmetzyanov D, Lakatos-Karoly A, Soares CM, Prisner T, Glaubitz C (2018) Unexplored nucleotide binding modes for the ABC exporter MsbA. J Am Chem Soc 140(43):14112–14125. https://doi.org/10.1021/jacs.8b06739
Keller K, Doll A, Qi MA, Godt A, Jeschke G, Yulikov M (2016) Averaging of nuclear modulation artefacts in RIDME experiments. J Magn Reson 272:108–113. https://doi.org/10.1016/j.jmr.2016.09.016
Kerry PS, Turkington HL, Ackermann K, Jameison SA, Bode BE (2014) Analysis of influenza A virus NS1 dimer interfaces in solution by pulse EPR distance measurements. J Phys Chem B 118(37):10882–10888. https://doi.org/10.1021/jp508386r
Kotler SA, Tugarinov V, Schmidt T, Ceccon A, Libich DS, Ghirlando R, Schwieters CD, Clore GM (2019) Probing initial transient oligomerization events facilitating Huntingtin fibril nucleation at atomic resolution by relaxation-based NMR. Proc Natl Acad Sci USA 116(9):3562–3571. https://doi.org/10.1073/pnas.1821216116
Kulik LV, Dzuba SA, Grigoryev IA, Tsvetkov YD (2001) Electron dipole-dipole interaction in ESEEM of nitroxide biradicals. Chem Phys Lett 343(3–4):315–324. https://doi.org/10.1016/S0009-2614(01)00721-7
McCracken J (2011) Electron spin echo envelope modulation (ESEEM) spectroscopy. In: Encyclopedia of inorganic and bioinorganic chemistry. Wiley. https://doi.org/10.1002/9781119951438.eibc0311
Meyer A, Schiemann O (2016) PELDOR and RIDME measurements on a high-spin manganese(II) bisnitroxide model complex. J Phys Chem A 120(20):3463–3472. https://doi.org/10.1021/acs.jpca.6b00716
Meyer A, Abdullin D, Schnakenburg G, Schiemann O (2016) Single and double nitroxide labeled bis(terpyridine)-copper(II): influence of orientation selectivity and multispin effects on PELDOR and RIDME. Phys Chem Chem Phys 18(13):9262–9271. https://doi.org/10.1039/c5cp07621h
Meyer A, Jassoy JJ, Spicher S, Berndhauser A, Schiemann O (2018) Performance of PELDOR, RIDME, SIFTER, and DQC in measuring distances in trityl based bi- and triradicals: exchange coupling, pseudosecular coupling and multi-spin effects. Phys Chem Chem Phys 20(20):13858–13869. https://doi.org/10.1039/c8cp01276h
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(1):48–56. https://doi.org/10.1016/j.jmr.2009.08.008
Pliotas C, Ward R, Branigan E, Rasmussen A, Hagelueken G, Huang HX, Black SS, Booth IR, Schiemann O, Naismith JH (2012) Conformational state of the MscS mechanosensitive channel in solution revealed by pulsed electron-electron double resonance (PELDOR) spectroscopy. Proc Natl Acad Sci USA 109(40):E2675–E2682. https://doi.org/10.1073/pnas.1202286109
Pliotas C, Dahl ACE, Rasmussen T, Mahendran KR, Smith TK, Marius P, Gault J, Banda T, Rasmussen A, Miller S, Robinson CV, Bayley H, Sansom MSP, Booth IR, Naismith JH (2015) The role of lipids in mechanosensation. Nat Struct Mol Biol 22(12):991–998. https://doi.org/10.1038/nsmb.3120
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(30):10762–10773. https://doi.org/10.1039/c2cp41520h
Prisner T, Rohrer M, MacMillan F (2001) Pulsed EPR spectroscopy: biological applications. Annu Rev Phys Chem 52:279–313. https://doi.org/10.1146/annurev.physchem.52.1.279
Schmidt T, Ghirlando R, Baber J, Clore GM (2016a) Quantitative resolution of monomer-dimer populations by inversion modulated deer epr spectroscopy. ChemPhysChem 17(19):2987–2991. https://doi.org/10.1002/cphc.201600726
Schmidt T, Walti MA, Baber JL, Hustedt EJ, Clore GM (2016b) Long distance measurements up to 160 angstrom in the GroEL tetradecamer using Q-Band DEER EPR spectroscopy. Angew Chem Int Edit 55(51):15905–15909. https://doi.org/10.1002/anie.201609617
Spindler PE, Glaser SJ, Skinner TE, Prisner TF (2013) Broadband inversion PELDOR spectroscopy with partially adiabatic shaped pulses. Angew Chem Int Edit 52(12):3425–3429. https://doi.org/10.1002/anie.201207777
Valera S, Ackermann K, Pliotas C, Huang HX, Naismith JH, Bode BE (2016) Accurate extraction of nanometer distances in multimers by pulse EPR. Chem-Eur J 22(14):4700–4703. https://doi.org/10.1002/chem.201505143
Van Doorslaer S (2017) Hyperfine spectroscopy: ESEEM. Emagres 6(1):51–69. https://doi.org/10.1002/9780470034590.emrstm1517
Volkov A, Dockter C, Bund T, Paulsen H, Jeschke G (2009) Pulsed EPR determination of water accessibility to spin-labeled amino acid residues in LHCIIb. Biophys J 96(3):1124–1141. https://doi.org/10.1016/j.bpj.2008.09.047
von Hagens T, Polyhach Y, Sajid M, Godt A, Jeschke G (2013) Suppression of ghost distances in multiple-spin double electron-electron resonance. Phys Chem Chem Phys 15(16):5854–5866. https://doi.org/10.1039/c3cp44462g
Ward R, Bowman A, Sozudogru E, El-Mkami H, Owen-Hughes T, Norman DG (2010) EPR distance measurements in deuterated proteins. J Magn Reson 207(1):164–167. https://doi.org/10.1016/j.jmr.2010.08.002
Ward R, Pliotas C, Branigan E, Hacker C, Rasmussen A, Hagelueken G, Booth IR, Miller S, Lucocq J, Naismith JH, Schiemann O (2014) Probing the structure of the mechanosensitive channel of small conductance in lipid bilayers with pulsed electron-electron double resonance. Biophys J 106(4):834–842. https://doi.org/10.1016/j.bpj.2014.01.008
Yang ZY, Liu YP, Borbat P, Zweier JL, Freed JH, Hubbell WL (2012) Pulsed ESR dipolar spectroscopy for distance measurements in immobilized spin labeled proteins in liquid solution. J Am Chem Soc 134(24):9950–9952. https://doi.org/10.1021/ja303791p
Zavoisky E (1945) Spin-magnetic resonance in paramagnetics. J Phys USSR 9:211–245
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Bode, B.E., Norman, D.G. (2019). Pulsed Electron-Electron Double Resonance (PELDOR) and Electron Spin Echo Envelope Modulation (ESEEM) Spectroscopy in Bioanalysis. In: Pereira, A., Tavares, P., Limão-Vieira, P. (eds) Radiation in Bioanalysis. Bioanalysis, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-28247-9_7
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