Paramagnetic metal ions in pulsed ESR distance distribution measurements

Accounts of Chemical Research

Volumn 47, Issue 2, 2014, Pages 688-695

  Ji, Ming ^a   Ruthstein, Sharon ^a,b   Saxena, Sunil ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b BAR ILAN UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84894250067     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400245z     Document Type: Article

References (77)

1. Eaton, S. S.; Eaton, G. R. In Distance Measurements in Biological Systems by EPR; Berliner, L. J., Eaton, S. S., Eaton, G. R., Eds.; Kluwer Academic/Plenum Publisher: New York, 2000; Vol. 19, pp 19-154.
2. Saxena, S.; Freed, J. H. Theory of double quantum two-dimensional electron spin resonance with application to distance measurements J. Chem. Phys. 1997, 107, 1317-1340 (Pubitemid 127572868)
3. Borbat, P. P.; Freed, J. H. Multiple-quantum ESR and distance measurements Chem. Phys. Lett. 1999, 313, 145-154 (Pubitemid 129556635)
4. Milov, A. D.; Ponomarev, A. B.; Tsvetkov, Y. D. Electron-electron double resonance in electron spin echo: Model biradical systems and the sensitized photolysis of decalin Chem. Phys. Lett. 1984, 110, 67-72
5. Larsen, R. G.; Singel, D. J. Double electron-electron resonance spin-echo modulation: Spectroscopic measurement of electron spin pair separations in orientationally disordered solids J. Chem. Phys. 1993, 98, 5134-5146
6. Milov, A. D.; Maryasov, A. G.; Tsvetkov, Y. D. Pulsed electron double resonance (PELDOR) and its applications in free-radical research Appl. Magn. Reson. 1998, 15, 107-143
7. Martin, R. E.; Pannier, M.; Diederich, F.; Gramlich, V.; Hubrich, M.; Spiess, H. W. 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. Engl. 1998, 37, 2833-2837
8. Pannier, M.; Veit, S.; Godt, A.; Jeschke, G.; Spiess, H. W. Dead-time free measurement of dipole-dipole interactions between electron spins J. Magn. Reson. 2000, 142, 331-340
9. Jeschke, G.; Panek, G.; Godt, A.; Bender, A.; Paulsen, H. Data analysis procedures for pulse ELDOR measurements of broad distance distributions Appl. Magn. Reson. 2004, 26, 223-244 (Pubitemid 38860166)
10. Chiang, Y.-W.; Borbat, P. P.; Freed, J. H. The determination of pair distance distributions by pulsed ESR using Tikhonov regularization J. Magn. Reson. 2005, 172, 279-295 (Pubitemid 40072533)
11. Hubbell, W. L.; Altenbach, C. Investigation of structure and dynamics in membrane proteins using site-directed spin labeling Curr. Opin. Struct. Biol. 1994, 4, 566-573 (Pubitemid 24268990)
12. Steinhoff, H.-J. Inter- and intra-molecular distances determined by EPR spectroscopy and site-directed spin labeling reveal protein-protein and protein-oligonucleotide interaction Biol. Chem. 2005, 385, 913-920 (Pubitemid 39481138)
13. Schiemanna, O.; Prisner, T. F. Long-range distance determinations in biomacromolecules by EPR spectroscopy Q. Rev. Biophys. 2007, 40, 1-53 (Pubitemid 47343581)
14. Tsvetkov, Y. D.; Milov, A. D.; Maryasov, A. G. Pulsed electron-electron double resonance (PELDOR) as EPR spectroscopy in nanometer range Russ. Chem. Rev. 2008, 77, 487-520
15. Jeschke, G. DEER distance measurements on proteins Annu. Rev. Phys. Chem. 2012, 63, 419-446
16. Polyhach, Y.; Bordignon, E.; Jeschke, G. Rotamer libraries of spin labelled cysteines for protein studies Phys. Chem. Chem. Phys. 2011, 13, 2356-2366
17. Hatmal, M. M.; Li, Y.; Hegde, B. G.; Hegde, P. B.; Jao, C. C.; Langen, R.; Haworth, I. S. Computer modeling of nitroxide spin labels on proteins Biopolymers 2011, 97, 35-44
18. Klose, D.; Klare, J. P.; Grohmann, D.; Kay, C. W.; Werner, F.; Steinhoff, H. J. Simulation vs. reality: A comparison of in silico distance predictions with DEER and FRET measurements PLoS One 2012, 7 e39492
19. Hagelueken, G.; Ward, R.; Naismith, J. H.; Schiemann, O. MtsslWizard: In silico spin-labeling and generation of distance distributions in PyMOL Appl. Magn. Reson. 2012, 42, 377-391
20. Mamonov, A. B.; Lettieri, S.; Ding, Y.; Sarver, J. L.; Palli, R.; Cunningham, T. F.; Saxena, S.; Zuckerman, D. M. Tunable, mixed-resolution modeling using library-based Monte Carlo and graphics processing units J. Chem. Theory Comput. 2012, 8, 2921-2929
21. Sarver, J. L.; Townsend, J. E.; Rajapakse, G.; Jen-Jacobson, L.; Saxena, S. Simulating the dynamics and orientations of spin labeled side chains in a protein-DNA complex J. Phys. Chem. B 2012, 116, 4024-4033
22. Roux, B.; Islam, S. M. Restrained-ensemble molecular dynamics simulations based on distance histograms from double electron-electron resonance spectroscopy J. Phys. Chem. B 2013, 117, 4733-4739
23. Cai, Q.; Kusnetzow, A. K.; Hideg, K.; Price, E. A.; Haworth, I. S.; Qin, P. Z. Nanometer distance measurements in RNA using site-directed spin labeling Biophys. J. 2007, 93, 2110-2117 (Pubitemid 47437593)
24. Malkin, R.; Bearden, A. J. Primary reactions of photosynthesis: photoreduction of a bound chloroplast ferredoxin at low temperature as detected by EPR spectroscopy Proc. Natl. Acad. Sci. U.S.A. 1971, 68, 16-19
25. Bolton, J. R.; Cammack, R. Primary electron acceptor complex of photosystem I in spinach chloroplasts Nature 1975, 256, 668-670
26. Rouault, T. A.; Stout, C. D.; Kapatin, S.; Harford, J. B.; Klausner, R. D. Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications Cell 1991, 64, 881-883
27. Hentze, M. W.; Argos, P. Homology between IRE-BP, a regulatory RNA-binding protein, aconitase, and isopropylmalate isomerase Nucleic Acids Res. 1991, 19, 1739-1740 (Pubitemid 21913272)
28. Enemark, J. H.; Young, C. G. Bioinorganic chemistry of protein-containing molybdenum and tungsten enzymes Adv. Inorg. Chem. 1993, 40, 1-88
29. Reczkowski, R. S.; Ash, D. E. EPR evidence for binuclear manganese(II) centers in rat liver arginase J. Am. Chem. Soc. 1992, 114, 10992-10994
30. Khangulov, S. V.; Pessiki, P. J.; Barynin, V. V.; Ash, D. E.; Dismukes, G. C. Determination of the metal ion separation and energies of the three lowest electronic states of dimanganese(II,II) complexes and enzymes: Catalase and liver Arginase Biochemistry 1995, 34, 2015-2025
31. Shi, O.; Morris, S. M., Jr.; Zoghbi, H.; Porter, C. W.; O'Brien, W. E. Generation of a mouse model for Arginase II deficiency by targeted disruption of the arginase II gene Mol. Cell. Biol. 2001, 21, 811-813 (Pubitemid 32104729)
32. Lovell, M. A.; Robertson, J. D.; Teesdale, W. J.; Campbell, J. L.; Markesbery, W. R. Copper, iron and zinc in Alzheimer's disease senile plaques J. Neurol. Sci. 1998, 158, 47-52 (Pubitemid 28277534)
33. Huang, X.; Cuajungco, M.; Atwood, C. G.; Hartshorn, M. A.; Tyndall, J. D. A.; Hanson, G. R.; Stokes, K. C.; Leopold, M.; Multhaup, G.; Goldstein, L. E.; Scarpa, R. C.; Saunders, A. J.; Lom, J.; Moir, R. D.; Glabe, C.; Bowden, E. F.; Masters, C. L.; Fairlie, D. P.; Tanzi, R. E.; Bush, A. I. Cu(II) potentiation of Alzhermer Aβ neurotoxicity J. Biol. Chem. 1999, 274, 37111-37116
34. Bush, A. I. Metal complexing agents and therapies for Alzheimer's disease Neurobiol. Aging 2002, 23, 1031-1038 (Pubitemid 35447784)
35. Kirkitadze, M. D.; Bitan, G.; Teplow, D. B. Paradigm shifts in Alzhermer's disease and other neurodegenerative disorders: The emerging role of oligomeric assemblies J. Neurosci. Res. 2002, 69, 567-577 (Pubitemid 34966869)
36. Miller, L. M.; Wang, Q.; Telivala, T. P.; Smith, R. J.; Lanzirotti, A.; Miklossy, J. Synchrotron-based infrared and X-ray imaging shows focalized accumulation of Cu and Zn co-localized with β-amyloid deposits in Alzheimer's disease J. Struct. Biol. 2006, 155, 30-37 (Pubitemid 43867313)
37. Waldron, K. J.; Rutherford, J. C.; Ford, D.; Robinson, N. J. Metalloproteins and metal sensing Nature 2009, 460, 823-830
38. van Amsterdam, I. M. C.; Ubbink, M.; Canters, G. W.; Huber, M. Measurement of a Cu-Cu distance of 26 A by a pulsed EPR method Angew. Chem., Int. Ed. 2003, 42, 62-64 (Pubitemid 36109498)
39. Narr, E.; Godt, A.; Jeschke, G. 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. 2002, 41, 3907-3910 (Pubitemid 35278037)
40. Kay, C. W. M.; Mkami, H. E.; Cammack, R.; Evans, R. W. Pulsed ELDOR determination of the intramolecular distance between the metal binding sites in dicupric human serum transferrin and lactoferrin J. Am. Chem. Soc. 2007, 129, 4868-4869 (Pubitemid 46651347)
41. Bode, B. E.; Plackmeyer, J.; Prisner, T. F.; Schiemann, O. PELDOR measurements on a nitroxide-labeled Cu(II) porphyrin: Orientation selection, spin-density distribution, and conformational flexibility J. Phys. Chem. A 2008, 112, 5064-5073
42. Bode, B. E.; Plackmeyer, J.; Bolte, M.; Prisner, T. F.; Schiemann, O. PELDOR on an exchange coupled nitroxide copper(II) spin pair J. Organomet. Chem. 2009, 694, 1172-1179
43. 2+ ions and ESR J. Phys. Chem. B 2010, 114, 6165-6174
44. 2+ sites in a DNA-modifying enzyme to reveal determinants of catalytic specificity Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E993-E1000
45. Elsaesser, C.; Brecht, M.; Bittl, R. Pulsed electron-electron double resonance on multinuclear metal clusters: Assignment of spin projection factors based on the dipolar interaction J. Am. Chem. Soc. 2002, 124, 12606-12611 (Pubitemid 35204587)
46. Elsaesser, C.; Brecht, M.; Bittl, R. Treatment of spin-coupled metal centres in pulsed electron-electron double-resonance experiments Biochem. Soc. Trans. 2005, 33, 15-19 (Pubitemid 40313750)
47. Roessler, M. M.; King, M. S.; Robinson, A. J.; Armstrong, F. A.; Harmer, J.; Hirst, J. 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. 2010, 107, 1930-1935
48. 3+ complexes as potential spin labels for high field pulsed EPR distance measurements J. Am. Chem. Soc. 2007, 129, 14138-14139 (Pubitemid 350171415)
49. 3+ ions and nitroxide radicals J. Phys. Chem. Lett. 2011, 2, 604-609
50. 3+ spin labels Phys. Chem. Chem. Phys. 2012, 14, 4355-4358
51. 3+ spin labeling J. Am. Chem. Soc. 2010, 132, 9040-9048
52. Song, Y.; Meade, T. J.; Astashkin, A. V.; Klein, E. L.; Enemark, J. H.; Raitsimring, A. Pulsed dipolar spectroscopy distance measurements in biomacromolecules labeled with Gd(III) markers J. Magn. Reson. 2011, 210, 59-68
53. Potapov, A.; Song, Y.; Meade, T. J.; Goldfarb, D.; Astashkin, A. V.; Raitsimring, A. 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. 2010, 205, 38-49
54. Yagi, H.; Banerjee, D.; Graham, B.; Huber, T.; Goldfarb, D.; Otting, G. Gadolinium tagging for high-precision measurements of 6 nm distances in protein assemblies by EPR J. Am. Chem. Soc. 2011, 133, 10418-10421
55. 3+/nitroxide mixed-labeled protein dimer with a dual mode cavity J. Magn. Reson. 2013, 227, 66-71
56. 3+-DTPA chelate complexes Phys. Chem. Chem. Phys. 2012, 14, 10732-10746
57. Matalon, E.; Huber, T.; Hagelueken, G.; Graham, B.; Frydman, V.; Feintuch, A.; Otting, G.; Goldfarb, D. Gadolinium(III) spin labels for high-sensitivity distance measurements in transmembrane helices Angew. Chem., Int. Ed. Engl. 2013, 52, 1-5
58. 2+ tags J. Phys. Chem. Lett. 2012, 3, 157-160
59. Goldfarb, D. Metal-Based Spin Labeling for Distance Determination; Springer: Berlin Heidelberg, 2012.
60. Stone, K.; Townsend, J. E.; Sarver, J.; Sapienza, P. J.; Saxena, S.; Jen-Jacobson, L. Electron spin resonance shows common structural features for different classes of EcoRI-DNA complexes Angew. Chem., Int. Ed. 2008, 47, 10192-10194
61. Maryasov, A. G.; Tsvetkov, Y. D.; Raap, J. Weakly coupled radical pairs in solids: ELDOR in ESE structure studies Appl. Magn. Reson. 1998, 14, 101-113 (Pubitemid 128657420)
62. Milov, A. D.; Tsvetkov, Y. D.; Formaggio, F.; Crisma, M.; Toniolo, C.; Raap, J. The secondary structure of a membrane-modifying peptide in a supramolecular assembly studied by PELDOR and CW-ESR spectroscopies J. Am. Chem. Soc. 2001, 123, 3784-3789 (Pubitemid 32879540)
63. Salikhov, K. M.; Dzuba, S. A.; Raitsimring, A. M. The theory of electron spin-echo signal decay resulting from dipole-dipole interactions between paramagnetic centers in solids J. Magn. Reson. 1981, 42, 255-276
64. Jeschke, G.; Polyhach, Y. Distance measurements on spin-labelled biomacromolecules by pulsed electron paramagnetic resonance Phys. Chem. Chem. Phys. 2007, 9, 1895-1910
65. Yang, Z.; Ji, M.; Saxena, S. Practical aspects of copper-ion based DEER distance measurements Appl. Magn. Reson. 2010, 39, 487-500
66. 2+ distance measurements in a protein-DNA complex by DQC-ESR J. Phys. Chem. B 2013, 117, 6227-6230
67. Yang, Z.; Becker, J.; Saxena, S. On Cu(II)-Cu(II) distance measurements using pulsed electron electron double resonance J. Magn. Reson. 2007, 188, 337-343 (Pubitemid 47562814)
68. Lovett, J. E.; Bowen, A. M.; Timmel, C. R.; Jones, M. W.; Dilworth, J. R.; Caprotti, D.; Bell, S. G.; Wong, L. L.; Harmer, J. Structural information from orientationally selective DEER spectroscopy Phys. Chem. Chem. Phys. 2009, 11, 6840-6848
69. Godt, A.; Schulte, M.; Zimmermann, H.; Jeschke, G. How flexible are poly(paraphenyleneethynylene)s? Angew. Chem., Int. Ed. 2006, 45, 7560-7564 (Pubitemid 44851682)
70. Kaminker, I.; Florent, M.; Epel, B.; Goldfarb, D. Simultaneous acquisition of pulse EPR orientation selective spectra J. Magn. Reson. 2011, 208, 95-102
71. Marko, A.; Margraf, D.; Yu, H.; Mu, Y.; Stock, G.; Prisner, T. F. Molecular orientation studies by pulsed electron-electron double resonance experiments J. Chem. Phys. 2009, 130 064102
72. Woodhead, J. L.; Bhave, N.; Malcolm, A. D. B. Cation dependence of restriction endonuclease EcoRI activity Eur. J. Biochem. 1981, 115, 293-296 (Pubitemid 11103632)
73. Grigorescu, A.; Horvath, M.; Wilkosz, P.; Chandrasekhar, K.; Rosenberg, J. In Restriction Endonucleases; Springer-Verlag: Heidelberg, 2004; pp 137-177.
74. Kurpiewski, M. R.; Engler, L. E.; Wozniak, L. A.; Kobylanska, A.; Koziolkiewicz, M.; Stec, W. J.; Jen-Jacobson, L. Mechanism of coupling between DNA recognition specificity and catalysis in EcoRI endonuclease Structure 2004, 12, 1775-1788 (Pubitemid 39298962)
75. van Wonderen, J.; Kostrz, D. N.; Dennison, C.; MacMillan, F. Refined distances between paramagnetic centers of a multi-copper nitrite reductase determined by pulsed EPR (iDEER) spectroscopy Angew. Chem., Int. Ed. 2013, 52, 1990-1993
76. Jeschke, G.; Chechik, V.; Ionita, P.; Godt, A.; Zimmermann, H.; Banham, J.; Timmel, C. R.; Hilger, D.; Jung, H. DeerAnalysis2006-a comprehensive software package for analyzing pulsed ELDOR data Appl. Magn. Reson. 2006, 30, 473-498
77. Sengupta, I.; Nadaud, P. S.; Jaroniec, C. P. Protein structure determination with paramagnetic solid-state NMR spectroscopy Acc. Chem. Res. 2013, 46, 2117-2126