Skip to main content

Structural Studies of Nucleic Acids

  • Chapter
  • First Online:
Pulsed Electron–Electron Double Resonance

Abstract

Nucleic acids have a very rich range of structures that are important in many biological contexts. PELDOR or DEER spectroscopy has provided a unique glimpse at the structures that form in solution and guide the response of the cellular machinery.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 109.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 139.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Schiemann O, Prisner TF (2007) Long-range distance determinations in biomacromolecules by EPR spectroscopy. Q Rev Biophys 40(1):1–53. https://doi.org/10.1017/S003358350700460x

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. Tsvetkov YD, Milov AD, Maryasov AG (2008) Pulse electron-electron double resonance (PELDOR) as nanometre range EPR spectroscopy. Usp Khim 77(6):515–550

    Article  Google Scholar 

  4. Sowa GZ, Qin PZ (2008) Site-directed spin labeling studies on nucleic acid structure and dynamics. Prog Nucleic Acid Re 82:147–197. https://doi.org/10.1016/S0079-6603(08)00005-6

    Article  CAS  Google Scholar 

  5. Schiemann O (2009) Mapping global folds of oligonucleotides by pulsed electron-electron double resonance. Meth Enzymol 469: Biophysical, chemical, and functional probes of RNA structure, interactions and folding, Pt B 469:329–351. https://doi.org/10.1016/s0076-6879(09)69016-9

    Chapter  Google Scholar 

  6. 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/Bst0390128

    Article  CAS  Google Scholar 

  7. Reginsson GW, Schiemann O (2011) Pulsed electron-electron double resonance: beyond nanometre distance measurements on biomacromolecules. Biochem J 434:353–363. https://doi.org/10.1042/Bj20101871

    Article  CAS  PubMed  Google Scholar 

  8. Schiemann O, Weber A, Edwards TE, Prisner TF, Sigurdsson ST (2003) Nanometer distance measurements on RNA using PELDOR. J Am Chem Soc 125(12):3434–3435

    Article  CAS  Google Scholar 

  9. Kolhe P, Amend E, Singh SK (2010) Impact of freezing on pH of buffered solutions and consequences for monoclonal antibody aggregation. Biotechnol Prog 26(3):727–733. https://doi.org/10.1002/btpr.377

    Article  CAS  PubMed  Google Scholar 

  10. Ward R, Keeble DJ, El-Mkami H, Norman DG (2007) Distance determination in heterogeneous DNA model systems by pulsed EPR. ChemBioChem 8(16):1957–1964. https://doi.org/10.1002/cbic.200700245

    Article  CAS  PubMed  Google Scholar 

  11. Schiemann O, Piton N, Mu YG, Stock G, Engels JW, Prisner TF (2004) A PELDOR-based nanometer distance ruler for oligonucleotides. J Am Chem Soc 126(18):5722–5729. https://doi.org/10.1021/ja0393877

    Article  CAS  PubMed  Google Scholar 

  12. Piton N, Mu YG, Stock G, Prisner TF, Schiemann O, Engels JW (2007) Base-specific spin-labeling of RNA for structure determination. Nucleic Acids Res 35(9):3128–3143

    Article  CAS  Google Scholar 

  13. Cai Q, Kusnetzow AK, Hubbell WL, Haworth IS, Gacho GPC, Van Eps N, Hideg K, Chambers EJ, Qin PZ (2006) Site-directed spin labeling measurements of nanometer distances in nucleic acids using a sequence-independent nitroxide probe. Nucleic Acids Res 34(17):4722–4730. https://doi.org/10.1093/nar/gkl546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Cai Q, Kusnetzow AK, Hideg K, Price EA, Haworth IS, Qin PZ (2007) Nanometer distance measurements in RNA using site-directed spin Labeling. Biophys J 93(6):2110–2117. https://doi.org/10.1529/biophysj.107.109439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Shevelev GY, Krumkacheva OA, Lomzov AA, Kuzhelev AA, Trukhin DV, Rogozhnikova OY, Tormyshev VM, Pyshnyi DV, Fedin MV, Bagryanskaya EG (2015) Triarylmethyl labels: toward improving the accuracy of EPR nanoscale distance measurements in DNAs. J Phys Chem B 119(43):13641–13648

    Article  CAS  Google Scholar 

  16. Shevelev GY, Krumkacheva OA, Lomzov AA, Kuzhelev AA, Rogozhnikova OY, Trukhin DV, Troitskaya TI, Tormyshev VM, Fedin MV, Pyshnyi DV, Bagryanskaya EG (2014) Physiological-temperature distance measurement in nucleic acid using triarylmethyl-based spin labels and pulsed dipolar EPR spectroscopy. J Am Chem Soc 136(28):9874–9877. https://doi.org/10.1021/ja505122n

    Article  CAS  PubMed  Google Scholar 

  17. Raitsimring AM, 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(46):14138–14139. https://doi.org/10.1021/ja075544g

    Article  CAS  PubMed  Google Scholar 

  18. 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

    Article  CAS  Google Scholar 

  19. 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. https://doi.org/10.1016/j.jmr.2011.02.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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/jp911637s

    Article  CAS  PubMed  Google Scholar 

  21. Sicoli G, Mathis G, Delalande O, Boulard Y, Gasparutto D, Gambarelli S (2008) Double electron-electron resonance (DEER): a convenient method to probe DNA conformational changes. Angew Chem Int Edit 47(4):735–737. https://doi.org/10.1002/anie.200704133

    Article  CAS  Google Scholar 

  22. Yu H, Mu YG, Nordenskiold L, Stock G (2008) Influence of nitroxide spin labels on RNA structure: a molecular dynamics simulation study. J Chem Theory Comput 4(10):1781–1787. https://doi.org/10.1021/ct800266e

    Article  CAS  PubMed  Google Scholar 

  23. Romainczyk O, Endeward B, Prisner TF, Engels JW (2011) The RNA-DNA hybrid structure determined by EPR, CD and RNase H1. Mol BioSyst 7(4):1050–1052. https://doi.org/10.1039/c0mb00258e

    Article  CAS  PubMed  Google Scholar 

  24. Savitsky A, Dubinskii AA, Flores M, Lubitz W, Mobius 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 (22):6245–6262. https://doi.org/10.1021/jp070016c

    Article  CAS  Google Scholar 

  25. 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):064102. https://doi.org/10.1063/1.3073040

    Article  CAS  PubMed  Google Scholar 

  26. 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):021911. https://doi.org/10.1103/PhysRevE.81.021911

    Article  CAS  Google Scholar 

  27. 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

    Article  CAS  Google Scholar 

  28. 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(15):2655–2658

    Article  CAS  Google Scholar 

  29. Gophane DB, Endeward B, Prisner TF, Sigurdsson ST (2014) Conformationally restricted isoindoline-derived spin labels in duplex DNA: distances and rotational flexibility by pulsed electron-electron double resonance spectroscopy. Chem-Eur J 20(48):15913–15919. https://doi.org/10.1002/chem.201403726

    Article  CAS  PubMed  Google Scholar 

  30. Tkach I, Halbmair K, Hobartner C, Bennati M (2014) High-frequency 263 GHz PELDOR. Appl Magn Reson 45(10):969–979. https://doi.org/10.1007/s00723-014-0581-z

    Article  Google Scholar 

  31. Hagerman PJ (1988) Flexibility of DNA. Annu Rev Biophys Bio 17:265–286

    Article  CAS  Google Scholar 

  32. Gore J, Bryant Z, Nollmann M, Le MU, Cozzarelli NR, Bustamante C (2006) DNA overwinds when stretched. Nature 442(7104):836–839. https://doi.org/10.1038/nature04974

    Article  CAS  PubMed  Google Scholar 

  33. Marko JF (1997) Stretching must twist DNA. Europhys Lett 38(3):183–188. https://doi.org/10.1209/epl/i1997-00223-5

    Article  CAS  Google Scholar 

  34. Mathew-Fenn RS, Das R, Harbury PAB (2008) Remeasuring the double helix. Science 322(5900):446–449. https://doi.org/10.1126/science.1158881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Marko A, Denysenkov V, Margraft D, Cekan P, Schiemann O, Sigurdsson ST, Prisner TF (2011) Conformational flexibility of DNA. J Am Chem Soc 133(34):13375–13379

    Article  CAS  Google Scholar 

  36. 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(36):6443–6447. https://doi.org/10.1002/anie.201000713

    Article  CAS  Google Scholar 

  37. Krstic I, Frolow O, Sezer D, Endeward B, Weigand JE, Suess B, Engels JW, Prisner TF (2010) PELDOR spectroscopy reveals preorganization of the neomycin-responsive riboswitch tertiary structure. J Am Chem Soc 132(5):1454–1455. https://doi.org/10.1021/ja9077914

    Article  CAS  PubMed  Google Scholar 

  38. Grytz CM, Marko A, Cekan P, Sigurdsson ST, Prisner TF (2016) Flexibility and conformation of the cocaine aptamer studied by PELDOR. Phys Chem Chem Phys 18(4):2993–3002. https://doi.org/10.1039/c5cp06158j

    Article  CAS  PubMed  Google Scholar 

  39. Kim NK, Bowman MK, DeRose VJ (2010) Precise mapping of RNA tertiary structure via nanometer distance measurements with double electron-electron resonance spectroscopy. J Am Chem Soc 132(26):8882–8884. https://doi.org/10.1021/ja101317g

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang XJ, Tung CS, Sowa GZ, Hatmal MM, Haworth IS, Qin PZ (2012) Global structure of a three-way junction in a Phi29 packaging RNA dimer determined using site-directed spin labeling. J Am Chem Soc 134(5):2644–2652. https://doi.org/10.1021/ja2093647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Freeman ADJ, Ward R, El Mkami H, Lilley DMJ, Norman DG (2011) Analysis of conformational changes in the DNA junction-resolving enzyme T7 endonuclease I on binding a four-way junction using EPR. Biochemistry-Us 50(46):9963–9972. https://doi.org/10.1021/bi2011898

    Article  CAS  Google Scholar 

  42. Danielsson J, Inomata K, Murayama S, Tochio H, Lang LS, Shirakawa M, Oliveberg M (2013) Pruning the ALS-associated protein SOD1 for in-cell NMR. J Am Chem Soc 135(28):10266–10269. https://doi.org/10.1021/ja404425r

    Article  CAS  PubMed  Google Scholar 

  43. Banci L, Barbieri L, Bertini I, Luchinat E, Secci E, Zhao YG, Aricescu AR (2013) Atomic-resolution monitoring of protein maturation in live human cells by NMR. Nat Chem Biol 9(5):297–300. https://doi.org/10.1038/Nchembio.1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Sakai T, Tochio H, Tenno T, Ito Y, Kokubo T, Hiroaki H, Shirakawa M (2006) In-cell NMR spectroscopy of proteins inside Xenopus laevis oocytes. J Biomol NMR 36(3):179–188. https://doi.org/10.1007/s10858-006-9079-9

    Article  CAS  PubMed  Google Scholar 

  45. Ogino S, Kubo S, Umemoto R, Huang SX, Nishida N, Shimada I (2009) Observation of NMR signals from proteins introduced into living mammalian cells by reversible membrane permeabilization using a pore-forming toxin, streptolysin O. J Am Chem Soc 131(31):10834–10835. https://doi.org/10.1021/ja904407w

    Article  CAS  PubMed  Google Scholar 

  46. Azarkh M, Singh V, Okle O, Seemann IT, Dietrich DR, Hartig JS, Drescher M (2013) Site-directed spin-labeling of nucleotides and the use of in-cell EPR to determine long-range distances in a biologically relevant environment. Nat Protoc 8(1):131–147. https://doi.org/10.1038/nprot.2012.136

    Article  CAS  PubMed  Google Scholar 

  47. Azarkh M, Okle O, Eyring P, Dietrich DR, Drescher M (2011) Evaluation of spin labels for in-cell EPR by analysis of nitroxide reduction in cell extract of Xenopus laevis oocytes. J Magn Reson 212(2):450–454. https://doi.org/10.1016/j.jmr.2011.07.014

    Article  CAS  PubMed  Google Scholar 

  48. Krstic I, Hansel R, Romainczyk O, Engels JW, Dotsch V, Prisner TF (2011) Long-range distance measurements on nucleic acids in cells by pulsed EPR spectroscopy. Angew Chem Int Edit 50(22):5070–5074. https://doi.org/10.1002/anie.201100886

    Article  CAS  Google Scholar 

  49. Igarashi R, Sakai T, Hara H, Tenno T, Tanaka T, Tochio H, Shirakawa M (2010) Distance determination in proteins inside Xenopus laevis oocytes by double electron-electron resonance experiments. J Am Chem Soc 132(24):8228–8229. https://doi.org/10.1021/ja906104e

    Article  CAS  PubMed  Google Scholar 

  50. Bowman MK, Maryasov AG, Kim N, DeRose VJ (2004) Visualization of distance distribution from pulsed double electron-electron resonance data. Appl Magn Reson 26(1–2):23–39. https://doi.org/10.1007/Bf03166560

    Article  CAS  Google Scholar 

  51. Nakata M, Zanchetta G, Chapman BD, Jones CD, Cross JO, Pindak R, Bellini T, Clark NA (2007) End-to-end stacking and liquid crystal condensation of 6-to 20-base pair DNA duplexes. Science 318(5854):1276–1279. https://doi.org/10.1126/science.1143826

    Article  CAS  PubMed  Google Scholar 

  52. Duchardt-Ferner E, Weigand JE, Ohlenschlager O, Schtnidtke SR, Suess B, Wohnert J (2010) Highly modular structure and ligand binding by conformational capture in a minimalistic riboswitch. Angew Chem Int Edit 49(35):6216–6219. https://doi.org/10.1002/anie.201001339

    Article  CAS  Google Scholar 

  53. Nozinovic S, Furtig B, Jonker HRA, Richter C, Schwalbe H (2010) High-resolution NMR structure of an RNA model system: the 14-mer cUUCGg tetraloop hairpin RNA. Nucleic Acids Res 38(2):683–694. https://doi.org/10.1093/nar/gkp956

    Article  CAS  PubMed  Google Scholar 

  54. Bochman ML, Paeschke K, Zakian VA (2012) DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet 13(11):770–780. https://doi.org/10.1038/nrg3296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Singh V, Azarkh M, Exner TE, Hartig JS, Drescher M (2009) Human telomeric quadruplex conformations studied by pulsed EPR. Angew Chem Int Edit 48(51):9728–9730. https://doi.org/10.1002/anie.200902146

    Article  CAS  Google Scholar 

  56. Wang Y, Patel DJ (1993) Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure 1(4):263–282. https://doi.org/10.1016/0969-2126(93)90015-9

    Article  CAS  PubMed  Google Scholar 

  57. Phan AT, Kuryavyi V, Luu KN, Patel DJ (2007) Structure of two intramolecular G-quadruplexes formed by natural human telomere sequences in K+ solution. Nucleic Acids Res 35(19):6517–6525. https://doi.org/10.1093/nar/gkm706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Parkinson GN, Lee MPH, Neidle S (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417(6891):876–880. https://doi.org/10.1038/nature755

    Article  CAS  PubMed  Google Scholar 

  59. Azarkh M, Singh V, Okle O, Dietrich DR, Hartig JS, Drescher M (2012) Intracellular conformations of human telomeric quadruplexes studied by electron paramagnetic resonance spectroscopy. ChemPhysChem 13(6):1444–1447. https://doi.org/10.1002/cphc.201100980

    Article  CAS  PubMed  Google Scholar 

  60. Shiokawa K, Tashiro K, Yamana K, Sameshima M (1987) Electron-microscopic studies of giant nucleus-like structure formed by lambda DNA introduced into the cytoplasm of Xenopus laevis fertilized-eggs and embryos. Cell Differ Dev 20(4):253–261. https://doi.org/10.1016/0045-6039(87)90470-2

    Article  CAS  Google Scholar 

  61. Singh V, Azarkh M, Drescher M, Hartig JS (2012) Conformations of individual quadruplex units studied in the context of extended human telomeric DNA. Chem Commun 48(66):8258–8260. https://doi.org/10.1039/c2cc32012f

    Article  CAS  Google Scholar 

  62. Martorana A, Bellapadrona G, Feintuch A, Di Gregorio E, Aime S, Goldfarb D (2014) Probing protein conformation in cells by EPR distance measurements using Gd3+ spin labeling. J Am Chem Soc 136(38):13458–13465. https://doi.org/10.1021/ja5079392

    Article  CAS  PubMed  Google Scholar 

  63. Goldfarb D (2014) Gd3+ spin labeling for distance measurements by pulse EPR spectroscopy. Phys Chem Chem Phys 16(21):9685–9699. https://doi.org/10.1039/c3cp53822b

    Article  CAS  PubMed  Google Scholar 

  64. Thonon D, Jacques V, Desreux JF (2007) A gadolinium triacetic monoamide DOTA derivative with a methanethiosulfonate anchor group. Relaxivity properties and conjug. Contrast Media Mol I 2(1):24–34. https://doi.org/10.1002/cmmi.121

    Article  CAS  Google Scholar 

  65. Rossi L, Serafini S, Pierige F, Antonelli A, Cerasi A, Fraternale A, Chiarantini L, Magnani M (2005) Erythrocyte-based drug delivery. Expert Opin Drug Deliv 2(2):311–322. https://doi.org/10.1517/17425247.2.2.311

    Article  CAS  PubMed  Google Scholar 

  66. Markov DE, Boeve H, Gleich B, Borgert J, Antonelli A, Sfara C, Magnani M (2010) Human erythrocytes as nanoparticle carriers for magnetic particle imaging. Phys Med Biol 55(21):6461–6473. https://doi.org/10.1088/0031-9155/55/21/008

    Article  CAS  PubMed  Google Scholar 

  67. Hara H, Tenno T, Shirakawa M (2007) Distance determination in human ubiquitin by pulsed double electron-electron resonance and double quantum coherence ESR methods. J Magn Reson 184(1):78–84. https://doi.org/10.1016/j.jmr.2006.09.017

    Article  CAS  PubMed  Google Scholar 

  68. Sicoli G, Mathis G, Aci-Seche S, Saint-Pierre C, Boulard Y, Gasparutto D, Gambarelli S (2009) Lesion-induced DNA weak structural changes detected by pulsed EPR spectroscopy combined with site-directed spin labelling. Nucleic Acids Res 37(10):3165–3176. https://doi.org/10.1093/nar/gkp165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kuznetsov NA, Milov AD, Koval VV, Samoilova RI, Grishin YA, Knorre DG, Tsvetkov YD, Fedorova OS, Dzuba SA (2009) PELDOR study of conformations of double-spin-labeled single- and double-stranded DNA with non-nucleotide inserts. Phys Chem Chem Phys 11(31):6826–6832. https://doi.org/10.1039/b904873a

    Article  CAS  PubMed  Google Scholar 

  70. 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(9):2670–2680. https://doi.org/10.1039/c1mb05189j

    Article  CAS  PubMed  Google Scholar 

  71. 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. https://doi.org/10.1021/jp212421c

    Article  CAS  PubMed  Google Scholar 

  72. Flaender M, Sicoli G, Aci-Seche S, Reignier T, Maurel V, Saint-Pierre C, Boulard Y, Gambarelli S, Gasparutto D (2011) A triple spin-labeling strategy coupled with DEER analysis to detect DNA modifications and enzymatic repair. ChemBioChem 12(17):2560–2563. https://doi.org/10.1002/cbic.201100550

    Article  CAS  PubMed  Google Scholar 

  73. 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

    Article  CAS  Google Scholar 

  74. Jeschke G, Sajid M, Schulte M, Godt A (2009) Three-spin correlations in double electron-electron resonance. Phys Chem Chem Phys 11(31):6580–6591

    Article  CAS  Google Scholar 

  75. Takeuchi M, Lillis R, Demple B, Takeshita M (1994) Interactions of Escherichia coli endonuclease-IV and exonuclease-III with abasic sites in DNA. J Biol Chem 269(34):21907–21914

    CAS  PubMed  Google Scholar 

  76. Banerjee A, Santos WL, Verdine GL (2006) Structure of a DNA glycosylase searching for lesions. Science 311(5764):1153–1157. https://doi.org/10.1126/science.1120288

    Article  CAS  PubMed  Google Scholar 

  77. Qi Y, Spong MC, Nam K, Karplus M, Verdine GL (2010) Entrapment and structure of an extrahelical guanine attempting to enter the active site of a bacterial DNA glycosylase, MutM. J Biol Chem 285(2):1468–1478. https://doi.org/10.1074/jbc.M109.069799

    Article  CAS  PubMed  Google Scholar 

  78. Gilboa R, Zharkov DO, Golan G, Fernandes AS, Gerchman SE, Matz E, Kycia JH, Grollman AP, Shoham G (2002) Structure of formamidopyrimidine-DNA glycosylase covalently complexed to DNA. J Biol Chem 277(22):19811–19816. https://doi.org/10.1074/jbc.M202058200

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuri D. Tsvetkov .

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Tsvetkov, Y.D., Bowman, M.K., Grishin, Y.A. (2019). Structural Studies of Nucleic Acids. In: Pulsed Electron–Electron Double Resonance. Springer, Cham. https://doi.org/10.1007/978-3-030-05372-7_7

Download citation

Publish with us

Policies and ethics