Cu2 + as an ESR Probe of Protein Structure and Function

Methods in Enzymology

Volumn 563, Issue , 2015, Pages 459-481

  Yang, Zhongyu ^a,b   Ji, Ming ^a,c   Cunningham, Timothy F ^a   Saxena, Sunil ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b JULES STEIN EYE INSTITUTE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Copper; Distance measurements; Electron spin resonance spectroscopy; Protein structure

Indexed keywords

CUPRIC OXIDE; NITROXIDE; CYSTEINE; NITROGEN OXIDE; NITROXYL; PROTEIN; SPIN LABELING;

DOUBLE ELECTRON ELECTRON RESONANCE; DOUBLE QUANTUM COHERENCE; ELECTRON SPIN RESONANCE; PROTEIN FUNCTION; PROTEIN STRUCTURE; PULSED DIPOLAR SPECTROSCOPY; QUANTUM MECHANICS; RELAXATION ENHANCEMENT; SITE DIRECTED SPIN LABELING; SPECTROSCOPY; SPIN LABELING; CHEMISTRY; PROCEDURES; STRUCTURE ACTIVITY RELATION;

CYSTEINE; ELECTRON SPIN RESONANCE SPECTROSCOPY; NITROGEN OXIDES; PROTEINS; SPIN LABELS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84944356345     PISSN: 00766879     EISSN: 15577988     Source Type: Book Series    
DOI: 10.1016/bs.mie.2015.05.026     Document Type: Chapter

References (88)

1. D. Abdullin, N. Florin, G. Hagelueken, and O. Schiemann EPR-based approach for the localization of paramagnetic metal ions in biomolecules Angewandte Chemie International Edition 54 2015 1827 1831
2. D. Abdullin, G. Hagelueken, R.I. Hunter, G.M. Smith, and O. Schiemann Geometric model-based fitting algorithm for orientation-selective PELDOR data Molecular Physics 113 2015 544 560
3. J. Abe, S. Ueki, T. Arata, S. Nakazawa, S. Yamauchi, and Y. Ohba Improved sensitivity by isotopic substitution in distance measurements based on double quantum coherence EPR Applied Magnetic Resonance 42 4 2012 473 485
4. D. Akhmetzyanov, J. Plackmeyer, B. Endeward, V. Denysenkov, and T.F. Prisner Pulsed electron-electron double resonance spectroscopy between a high-spin Mn2 + ion and a nitroxide spin label Physical Chemistry Chemical Physics 17 10 2015 6760 6766
5. N. Akyuz, E.R. Georgieva, Z. Zhou, S. Stolzenberg, M.A. Cuendet, G. Khelashvili, and et al. Transport domain unlocking sets the uptake rate of an aspartate transporter Nature 518 7537 2015 68 73
6. E. Aronoff-Spencer, C.S. Burns, N.I. Avdievich, G.J. Gerfen, J. Peisach, W.E. Antholine, and et al. Identification of the Cu2 + binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy Biochemistry 39 45 2000 13760 13771
7. J.S. Becker, and S. Saxena Double quantum coherence electron spin resonance on coupled Cu(II)-Cu(II) electron spins Chemical Physics Letters 414 2005 248 252
8. I. Bertini, C. Luchinat, and G. Parigi Solution NMR of paramagnetic molecules: Applications to metallobiomolecules and models Vol. 2 2001 Elsevier Science New York
9. N. Bloembergen, E.M. Purcell, and R.V. Pound Relaxation effects in nuclear magnetic resonance absorption Physical Review 73 1948 679 712
10. N. Bloembergen, S. Shapiro, P.S. Pershan, and J.O. Artman Cross-relaxation in spin system Physical Review 114 1959 445 459
11. B.E. Bode, J. Plackmeyer, T.F. Prisner, and O. Schiemann PELDOR measurements on a nitroxide-labeled Cu(II) porphyrin: Orientation selection, spin-density distribution, and conformational flexibility The Journal of Physical Chemistry. A 112 23 2008 5064 5073
12. M. Bonora, J. Becker, and S. Saxena Suppression of electron spin-echo envelope modulation peaks in double quantum coherence electron spin resonance Journal of Magnetic Resonance 170 2 2004 278 283
13. M. Bonora, S. Pornsuwan, and S. Saxena Nitroxide spin-relaxation over the entire motional range The Journal of Physical Chemistry B 108 13 2004 4196 4198
14. P. Borbat, and J. Freed Pulse dipolar ESR: Distance measurements J. Harmer, C. Timmel, Structural information from spin-labels and intrinsic paramagnetic centers in the biosciences Structure and bonding Vol. 152 2014 Springer New York, USA 1 82 Heidelberg, Germany
15. P.P. Borbat, J.H. Freed, I. Melvin, B.R.C. Simon, and C. Alexandrine Measuring distances by pulsed dipolar ESR spectroscopy: Spin-labeled histidine kinases Methods in enzymology Vol. 423 2007 Elsevier Inc. New York 52 116
16. M. Bridges, K. Hideg, and W. Hubbell Resolving conformational and rotameric exchange in spin-labeled proteins using saturation recovery EPR Applied Magnetic Resonance 37 1-4 2010 363 390
17. D.S. Cafiso Identifying and quantitating conformational exchange in membrane proteins using site-directed spin labeling Accounts of Chemical Research 47 10 2014 3102 3109
18. Y.-W. Chiang, P.P. Borbat, and J.H. Freed The determination of pair distance distributions by pulsed ESR using Tikhonov regularization Journal of Magnetic Resonance 172 2 2005 279 295
19. 2 +-binding motif: A highly rigid, site-specific spin probe for electron spin resonance distance measurements Angewandte Chemie International Edition 127 2015 6428 6432
20. T.F. Cunningham, M.D. Shannon, M.R. Putterman, R.J. Arachchige, I. Sengupta, M. Gao, and et al. Cysteine-specific Cu2 + chelating tags used as paramagnetic probes in double electron electron resonance The Journal of Physical Chemistry B 119 7 2015 2839 2843
21. O. Duss, E. Michel, M. Yulikov, M. Schubert, G. Jeschke, and F.H.T. Allain Structural basis of the non-coding RNA RsmZ acting as a protein sponge Nature 509 7502 2015 588 592
22. O. Duss, M. Yulikov, G. Jeschke, and F.H.-T. Allain EPR-aided approach for solution structure determination of large RNAs or protein-RNA complexes Nature Communications 5 2014 Article number: 3669
23. G. Eaton, and S. Eaton Relaxation times of organic radicals and transition metal ions L. Berliner, G. Eaton, S. Eaton, Distance measurements in biological systems by EPR Vol. 19 2002 Kluwer Academic/Plenum Publisher New York 29 154
24. G.E. Fanucci, and D.S. Cafiso Recent advances and applications of site-directed spin labeling Current Opinion in Structural Biology 16 5 2006 644 653
25. L. Garbuio, E. Bordignon, E.K. Brooks, W.L. Hubbell, G. Jeschke, and M. Yulikov Orthogonal spin labeling and Gd(III)-nitroxide distance measurements on bacteriophage T4-lysozyme The Journal of Physical Chemistry B 117 11 2013 3145 3153
26. A. Godt, M. Schulte, H. Zimmermann, and G. Jeschke How flexible are poly(para-phenyleneethynylene)s? Angewandte Chemie International Edition 45 45 2006 7560 7564
27. D. Goldfarb Gd3 + spin labeling for distance measurements by pulse EPR spectroscopy Physical Chemistry Chemical Physics 16 21 2014 9685 9699
28. G. Hagelueken, D. Abdullin, R. Ward, and O. Schiemann mtsslSuite: In silico spin labelling, trilateration and distance-constrained rigid body docking in PyMOL Molecular Physics 111 18-19 2013 2757 2766
29. D.J. Hirsh, W.F. Beck, J.B. Innes, and G.W. Brudvig Using saturation-recovery EPR to measure distances in proteins: Applications to photosystem II Biochemistry 31 2 1992 532 541
30. D.J. Hirsh, and G.W. Brudvig Measuring distances in proteins by saturation-recovery EPR Nature Protocols 2 7 2007 1770 1781
31. D.J. Hirsh, J. McCracken, R. Biczo, and K.-A. Gesuelli Saturation-recovery EPR with nitroxyl radical-dy(III) spin pairs: Distances and orientations The Journal of Physical Chemistry B 117 40 2013 11960 11977
32. W.L. Hubbell, D.S. Cafiso, and C. Altenbach Identifying conformational changes with site-directed spin labeling Nature Structural Biology 7 2000 735 739
33. W.L. Hubbell, C.J. López, C. Altenbach, and Z. Yang Technological advances in site-directed spin labeling of proteins Current Opinion in Structural Biology 23 5 2013 725 733
34. H. Jäger, A. Koch, V. Maus, H.W. Spiess, and G. Jeschke Relaxation-based distance measurements between a nitroxide and a lanthanide spin label Journal of Magnetic Resonance 194 2 2008 254 263
35. G. Jeschke DEER distance measurements on proteins Annual Review of Physical Chemistry 63 1 2012 419 446
36. G. Jeschke, V. Chechik, P. Ionita, A. Godt, H. Zimmermann, J. Banham, and et al. DeerAnalysis2006 - Comprehensive software package for analyzing pulsed ELDOR data Applied Magnetic Resonance 30 3-4 2006 473 498
37. M. Ji, S. Ruthstein, and S. Saxena Paramagnetic metal ions in pulsed ESR distance distribution measurements Accounts of Chemical Research 47 2 2014 688 695
38. M. Ji, L. Tan, L. Jen-Jacobson, and S. Saxena Insights into copper coordination in the EcoRI-DNA complex by ESR spectroscopy Molecular Physics 112 24 2014 3173 3182
39. S. Jun, J.S. Becker, M. Yonkunas, R. Coalson, and S. Saxena Unfolding of alanine-based peptides using electron spin resonance distance measurements Biochemistry 45 38 2006 11666 11673
40. I. Kaminker, M. Florent, B. Epel, and D. Goldfarb Simultaneous acquisition of pulse EPR orientation selective spectra Journal of Magnetic Resonance 208 1 2011 95 102
41. I. Kaminker, H. Yagi, T. Huber, A. Feintuch, G. Otting, and D. Goldfarb Spectroscopic selection of distance measurements in a protein dimer with mixed nitroxide and Gd3 + spin labels Physical Chemistry Chemical Physics 14 13 2012 4355 4358
42. A.V. Kulikov, and G.I. Likhtenstein The use of spin relaxation phenomena in the investigation of the structure of model and biological systems by the method of spin labels Advances in Molecular Relaxation and Interaction Processes 10 1 1977 47 79
43. N.C. Kunjir, G.W. Reginsson, O. Schiemann, and S.T. Sigurdsson Measurements of short distances between trityl spin labels with CW EPR, DQC and PELDOR Physical Chemistry Chemical Physics 15 45 2013 19673 19685
44. A. Kusumi, W.K. Subczynski, and J.S. Hyde Oxygen transport parameter in membranes as deduced by saturation recovery measurements of spin-lattice relaxation times of spin labels Proceedings of the National Academy of Sciences 79 6 1982 1854 1858
45. K.V. Lakshmi, and G.W. Brudvig Pulsed electron paramagnetic resonance methods for macromolecular structure determination Current Opinion in Structural Biology 11 5 2001 523 531
46. K.V. Lakshmi, O.G. Poluektov, M.J. Reifler, A.M. Wagner, M.C. Thurnauer, and G.W. Brudvig Pulsed high-frequency EPR study on the location of carotenoid and chlorophyll cation radicals in photosystem II Journal of the American Chemical Society 125 17 2003 5005 5014
47. C.J. López, Z. Yang, C. Altenbach, and W.L. Hubbell Conformational selection and adaptation to ligand binding in T4 lysozyme cavity mutants Proceedings of the National Academy of Sciences 110 46 2013 E4306 E4315
48. J.E. Lovett, A.M. Bowen, C.R. Timmel, M.W. Jones, J.R. Dilworth, D. Caprotti, and et al. Structural information from orientationally selective DEER spectroscopy Physical Chemistry Chemical Physics 11 31 2009 6840 6848
49. 2 Journal of Physical Chemistry Letters 3 10 2012 1336 1340
50. P. Lueders, G. Jeschke, and M. Yulikov Double electron-electron resonance measured between Gd3 + ions and nitroxide radicals Journal of Physical Chemistry Letters 2 6 2011 604 609
51. S. Lyubenova, T. Maly, K. Zwicker, U. Brandt, B. Ludwig, and T. Prisner Multifrequency pulsed electron paramagnetic resonance on metalloproteins Accounts of Chemical Research 43 2 2009 181 189
52. S. Lyubenova, M.K. Siddiqui, M.J.M. Penning de Vries, B. Ludwig, and T.F. Prisner Protein-protein interactions studied by EPR relaxation measurements: Cytochrome c and cytochrome c oxidase The Journal of Physical Chemistry B 111 14 2007 3839 3846
53. A. Marko, D. Margraf, H. Yu, Y. Mu, G. Stock, and T. Prisner Molecular orientation studies by pulsed electron-electron double resonance experiments The Journal of Chemical Physics 130 6 2009 064102
54. A. Marko, and T.F. Prisner An algorithm to analyze PELDOR data of rigid spin label pairs Physical Chemistry Chemical Physics 15 2 2013 619 627
55. A. Martorana, G. Bellapadrona, A. Feintuch, E. Di Gregorio, S. Aime, and D. Goldfarb Probing protein conformation in cells by EPR distance measurements using Gd3 + spin labeling Journal of the American Chemical Society 136 38 2014 13458 13465
56. H.S. McHaourab, P.R. Steed, and K. Kazmier Toward the fourth dimension of membrane protein structure: Insight into dynamics from spin-labeling EPR spectroscopy Structure 19 11 2011 1549 1561
57. G.E. Merz, P.P. Borbat, A.J. Pratt, E.D. Getzoff, J.H. Freed, and B.R. Crane Copper-based pulsed dipolar ESR spectroscopy as a probe of protein conformation linked to disease states Biophysical Journal 107 7 2014 1669 1674
58. V. Meyer, M.A. Swanson, L.J. Clouston, P.J. Boratyński, R.A. Stein, H.S. McHaourab, and et al. Room-temperature distance measurements of immobilized spin-labeled protein by DEER/PELDOR Biophysical Journal 108 5 2015 1213 1219
59. E. Narr, A. Godt, and G. Jeschke 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 Angewandte Chemie International Edition 41 20 2002 3907 3910
60. M. Pannier, S. Veit, A. Godt, G. Jeschke, and H.W. Spiess Dead-time free measurement of dipole-dipole interactions between electron spins Journal of Magnetic Resonance 142 2 2000 331 340
61. S.-Y. Park, P.P. Borbat, G. Gonzalez-Bonet, J. Bhatnagar, A.M. Pollard, J.H. Freed, and et al. Reconstruction of the chemotaxis receptor-kinase assembly Nature Structural & Molecular Biology 13 2006 400 407
62. R. Pietras, M. Sarewicz, and A. Osyczka Molecular organization of cytochrome c2 near the binding domain of cytochrome bc1 studied by electron spin-lattice relaxation enhancement The Journal of Physical Chemistry B 118 24 2014 6634 6643
63. A. Potapov, H. Yagi, T. Huber, S. Jergic, N.E. Dixon, G. Otting, and et al. Nanometer-scale distance measurements in proteins using Gd3 + spin labeling Journal of the American Chemical Society 132 26 2010 9040 9048
64. A.J. Pratt, D.S. Shin, G.E. Merz, R.P. Rambo, W.A. Lancaster, K.N. Dyer, and et al. Aggregation propensities of superoxide dismutase G93 hotspot mutants mirror ALS clinical phenotypes Proceedings of the National Academy of Sciences 111 43 2014 E4568 E4576
65. M. Qi, A. Gross, G. Jeschke, A. Godt, and M. Drescher Gd(III)-PyMTA label is suitable for in-cell EPR Journal of the American Chemical Society 136 43 2014 15366 15378
66. M.H. Rakowsky, K.M. More, A.V. Kulikov, G.R. Eaton, and S.S. Eaton Time-domain electron paramagnetic resonance as a probe of electron-electron spin-spin interaction in spin-labeled low-spin iron porphyrins Journal of the American Chemical Society 117 7 1995 2049 2057
67. S. Razzaghi, E.K. Brooks, E. Bordignon, W.L. Hubbell, M. Yulikov, and G. Jeschke EPR relaxation-enhancement-based distance measurements on orthogonally spin-labeled T4-lysozyme ChemBioChem 14 14 2013 1883 1890
68. S. Ruthstein, M. Ji, P. Mehta, L. Jen-Jacobson, and S. Saxena Sensitive Cu2 + -Cu2 + distance measurements in a protein-DNA complex by double-quantum coherence ESR The Journal of Physical Chemistry B 117 20 2013 6227 6230
69. S. Ruthstein, M. Ji, B. Shin, and S. Saxena A simple double quantum coherence ESR sequence that minimizes nuclear modulations in Cu(II)-ion based distance measurements Journal of Magnetic Resonance 257 2015 45 50
70. I.D. Sahu, R.M. McCarrick, and G.A. Lorigan Use of electron paramagnetic resonance to solve biochemical problems Biochemistry 52 35 2013 5967 5984
71. J. Sarver, K.I. Silva, and S. Saxena Measuring Cu2 + -nitroxide distances using double electron-electron resonance and saturation recovery Applied Magnetic Resonance 44 5 2013 583 594
72. O. Schiemann, and T.F. Prisner Long-range distance determinations in biomacromolecules by EPR spectroscopy Quarterly Reviews of Biophysics 40 01 2007 1 53
73. L.J. Schwartz, G.L. Millhauser, and J.H. Freed Two-dimensional electron spin echoes: Magnetization transfer and molecular dynamics Chemical Physics Letters 127 1 1986 60 66
74. R. Sircar, P.P. Borbat, M.J. Lynch, J. Bhatnagar, M.S. Beyersdorf, C.J. Halkides, and et al. Assembly states of FliM and FliG within the flagellar switch complex Journal of Molecular Biology 427 4 2015 867 886
75. Y. Song, T.J. Meade, A.V. Astashkin, E.L. Klein, J.H. Enemark, and A. Raitsimring Pulsed dipolar spectroscopy distance measurements in biomacromolecules labeled with Gd(III) markers Journal of Magnetic Resonance 210 1 2011 59 68
76. A.P. Todd, J. Cong, F. Levinthal, C. Levinthal, and W.L. Hubbell Site-directed mutagenesis of colicin E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation Proteins: Structure, Function, and Bioinformatics 6 3 1989 294 305
77. D. Ulyanov, B.E. Bowler, G.R. Eaton, and S.S. Eaton Electron-electron distances in spin-labeled low-spin metmyoglobin variants by relaxation enhancement Biophysical Journal 95 11 2008 5306 5316
78. I.M.C. van Amsterdam, M. Ubbink, G.W. Canters, and M. Huber Measurement of a Cu-Cu distance of 26 Å by a pulsed EPR method Angewandte Chemie International Edition 42 1 2003 62 64
79. J.H. van Wonderen, D.N. Kostrz, C. Dennison, and F. MacMillan Refined distances between paramagnetic centers of a multi-copper nitrite reductase determined by pulsed EPR (iDEER) spectroscopy Angewandte Chemie International Edition 52 7 2013 1990 1993
80. J. Voss, L. Salwiński, H.R. Kaback, and W.L. Hubbell A method for distance determination in proteins using a designed metal ion binding site and site-directed spin labeling: Evaluation with T4 lysozyme Proceedings of the National Academy of Sciences 92 26 1995 12295 12299
81. H. Yagi, D. Banerjee, B. Graham, T. Huber, D. Goldfarb, and G. Otting Gadolinium tagging for high-precision measurements of 6 nm distances in protein assemblies by EPR Journal of the American Chemical Society 133 27 2011 10418 10421
82. Z. Yang, J. Becker, and S. Saxena On Cu(II)-Cu(II) distance measurements using pulsed electron electron double resonance Journal of Magnetic Resonance 188 2 2007 337 343
83. Z. Yang, M. Ji, and S. Saxena Practical aspects of copper ion-based double electron electron resonance distance measurements Applied Magnetic Resonance 39 2010 487 500
84. Z. Yang, G. Jiménez-Osés, C.J. López, M.D. Bridges, K.N. Houk, and W.L. Hubbell Long-range distance measurements in proteins at physiological temperatures using saturation recovery EPR spectroscopy Journal of the American Chemical Society 136 43 2014 15356 15365
85. 2 + ions and ESR The Journal of Physical Chemistry B 114 18 2010 6165 6174
86. Z. Yang, M.R. Kurpiewski, M. Ji, J.E. Townsend, P. Mehta, L. Jen-Jacobson, and et al. ESR spectroscopy identifies inhibitory Cu2 + sites in a DNA-modifying enzyme to reveal determinants of catalytic specificity Proceedings of the National Academy of Sciences 109 17 2012 E993 E1000
87. Z. Yang, Y. Liu, P. Borbat, J.L. Zweier, J.H. Freed, and W.L. Hubbell Pulsed ESR dipolar spectroscopy for distance measurements in immobilized spin labeled proteins in liquid solution Journal of the American Chemical Society 134 24 2012 9950 9952
88. M. Yulikov, P. Lueders, M. Farooq Warsi, V. Chechik, and G. Jeschke Distance measurements in Au nanoparticles functionalized with nitroxide radicals and Gd3 + -DTPA chelate complexes Physical Chemistry Chemical Physics 14 30 2012 10732 10746