Nitroxide sensing of a DNA microenvironment: Mechanistic insights from EPR spectroscopy and molecular dynamics simulations

Journal of Physical Chemistry B

Volumn 116, Issue 22, 2012, Pages 6387-6396

  Popova, Anna M ^a,b   Hatmal, Ma'Mon M ^a   Frushicheva, Maria P ^a   Price, Eric A ^a,c   Qin, Peter Z ^a   Haworth, Ian S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MOLECULAR DYNAMICS; PARAMAGNETIC RESONANCE; PARAMAGNETISM;

CONTINUOUS WAVES; DIASTEREOMERS; DNA DUPLEXES; DNA MOLECULES; ELECTRON PARAMAGNETIC RESONANCE SPECTROSCOPY; EPR SPECTRA; EPR SPECTROSCOPY; LOCAL BACKBONE DYNAMICS; MD SIMULATION; MICROENVIRONMENTS; MOLECULAR DYNAMICS SIMULATIONS; NITROXIDES; PHOSPHOROTHIOATES; QUANTITATIVE DESCRIPTION; ROTATIONAL DIFFUSION; ROTATIONAL MOTION; SEQUENCE-DEPENDENT; SPECTRAL VARIATION; SPIN LABEL; STEREOSPECIFIC MANNER;

ELECTRON SPIN RESONANCE SPECTROSCOPY;

EID: 84861875178     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp303303v     Document Type: Article

References (67)

1. Lawson, C. L.; Berman, H. M. Indirect Readout of DNA Sequence by Proteins. In Protein-Nucleic Acid Interactions; Correll, C. C., Rice, P. A., Eds.; Royal Society of Chemistry: Cambridge, 2008; p 66.
2. Rohs, R.; West, S. M.; Liu, P.; Honig, B. Curr. Opin. Struct. Biol. 2009, 19, 171
3. Rohs, R.; Jin, X.; West, S. M.; Joshi, R.; Honig, B.; Mann, R. S. Annu. Rev. Biochem. 2010, 79, 233
4. Egli, M.; Pallan, P. S. Curr. Opin. Struct. Biol. 2010, 20, 262
5. Segal, E.; Fondufe-Mittendorf, Y.; Chen, L.; Thastrom, A.; Field, Y.; Moore, I. K.; Wang, J. P.; Widom, J. Nature 2006, 442, 772
6. Peckham, H. E.; Thurman, R. E.; Fu, Y.; Stamatoyannopoulos, J. A.; Noble, W. S.; Struhl, K.; Weng, Z. Genome Res. 2007, 17, 1170
7. Rohs, R.; West, S. M.; Sosinsky, A.; Liu, P.; Mann, R. S.; Honig, B. Nature 2009, 461, 1248
8. Hubbell, W. L.; Cafiso, D. S.; Altenbach, C. Nat. Struct. Biol. 2000, 7, 735
9. Fajer, P. G. Electron spin resonance spectroscopy labeling in proteins and peptides analysis. In Encyclopedia of Analytical Chemistry; Meyers, R., Ed.; John Wiley & Sons: Chichester, 2000; p 5725.
10. Klug, C. S.; Feix, J. B. Methods Cell Biol. 2008, 84, 617
11. Sowa, G. Z.; Qin, P. Z. Site-directed spin labeling studies on nucleic acid structure and dynamics. Progress in Nucleic Acids Research and Molecular Biology; Academic Press: New York, NY, 2008; Vol. 82, p 147.
12. Robinson, B. H.; Mailer, C.; Drobny, G. Annu. Rev. Biophys. Biomol. Struct. 1997, 26, 629
13. Keyes, R. S.; Bobst, A. M. Spin-labeled nucleic acids. In Biological Magnetic Resonance; Berliner, L. J., Ed.; Plenum Press: New York, 1998; Vol. 14; p 283.
14. Krstić, I.; Endeward, B.; Margraf, D.; Marko, A.; Prisner, T. Structure and Dynamics of Nucleic Acids. In EPR Spectroscopy, Applications in Chemistry and Biology; Drescher, M.; Jeschke, G., Eds.; Springer: Berlin/Heidelberg, 2011; Vol. 321; p 159.
15. Reginsson, G. W.; Schiemann, O. Biochem. Soc. Trans. 2011, 39, 128
16. Sigurdsson, S. T. Pure Appl. Chem. 2011, 83, 677
17. Nguyen, P.; Qin, P. Z. WIREs: RNA 2012, 3, 62
18. Qin, P. Z.; Butcher, S. E.; Feigon, J.; Hubbell, W. L. Biochemistry 2001, 40, 6929
19. Qin, P. Z.; Haworth, I. S.; Cai, Q.; Kusnetzow, A. K.; Grant, G. P. G.; Price, E. A.; Sowa, G. Z.; Popova, A.; Herreros, B.; He, H. Nat. Protoc. 2007, 2, 2354
20. Cai, Q.; Kusnetzow, A. K.; Hubbell, W. L.; Haworth, I. S.; Gacho, G. P. C.; Van Eps, N.; Hideg, K.; Chambers, E. J.; Qin, P. Z. Nucleic Acids Res. 2006, 34, 4722
21. Popova, A. M.; Kálai, T.; Hideg, K.; Qin, P. Z. Biochemistry 2009, 48, 8540
22. Popova, A. M.; Qin, P. Z. Biophys. J. 2010, 99, 2180
23. Cai, Q.; Kusnetzow, A. K.; Hideg, K.; Price, E. A.; Haworth, I. S.; Qin, P. Z. Biophys. J. 2007, 93, 2110
24. Grant, G. P. G.; Boyd, N.; Herschlag, D.; Qin, P. Z. J. Am. Chem. Soc. 2009, 131, 3136
25. Zhang, X.; Tung, C.-S.; Sowa, G. Z.; Hatmal, M. M.; Haworth, I. S.; Qin, P. Z. J. Am. Chem. Soc. 2012, 134, 2644
26. Grant, G. P. G.; Popova, A.; Qin, P. Z. Biochem. Biophys. Res. Commun. 2008, 371, 451
27. Earle, K. A.; Budil, D. E. Calculating Slow-motion ESR Spectra of Spin-Labeled Polymers. In Advanced ESR Methods in Polymer Reaserch; Schlick, S., Ed.; John Wiley and Sons: New York, 2006; p 53.
28. Meirovitch, E.; Nayeem, A.; Freed, J. H. J. Phys. Chem. B 1984, 88, 3454
29. Leporc, S.; Mauffret, O.; Tevanian, G.; Lescot, E.; Monnot, M.; Fermandjian, S. Nucleic Acids Res. 1999, 27, 4759
30. Price, E. A.; Sutch, B. T.; Cai, Q.; Qin, P. Z.; Haworth, I. S. Biopolymers 2007, 87, 40
31. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. J. Comput. Chem. 2004, 25, 1157
32. Darden, T.; York, D.; Pedersen, L. J. Chem. Phys. 1993, 98, 10089
33. Lavery, R.; Sklenar, H. J. Biomol. Struct. Dyn. 1988, 6, 63
34. Hartmann, B.; Piazzola, D.; Lavery, R. Nucleic Acids Res. 1993, 21, 561
35. Perez, A.; Luque, F. J.; Orozco, M. J. Am. Chem. Soc. 2007, 129, 14739
36. Lavery, R.; Zakrzewska, K.; Beveridge, D.; Bishop, T. C.; Case, D. A.; Cheatham, T., 3rd; Dixit, S.; Jayaram, B.; Lankas, F.; Laughton, C.; Maddocks, J. H.; Michon, A.; Osman, R.; Orozco, M.; Perez, A.; Singh, T.; Spackova, N.; Sponer, J. Nucleic Acids Res. 2010, 38, 299
37. Heddi, B.; Oguey, C.; Lavelle, C.; Foloppe, N.; Hartmann, B. Nucleic Acids Res. 2010, 38, 1034
38. Okonogi, T. M.; Alley, S. C.; Reese, A. W.; Hopkins, P. B.; Robinson, B. H. Biophys. J. 2000, 78, 2560
39. Edwards, T. E.; Okonogi, T. M.; Robinson, B. H.; Sigurdsson, S. T. J. Am. Chem. Soc. 2001, 123, 1527
40. Gannett, P. M.; Darian, E.; Powell, J.; Johnson, E. M.; Mundoma, C.; Greenbaum, N. L.; Ramsey, C. M.; Dalal, N. S.; Budil, D. E. Nucleic Acids Res. 2002, 30, 5328
41. Cekan, P.; Jonsson, E. O.; Sigurdsson, S. T. Nucleic Acids Res. 2009, 37, 3990
42. Cekan, P.; Sigurdsson, S. T. J. Am. Chem. Soc. 2009, 131, 18054
43. Smith, A. L.; Cekan, P.; Brewood, G. P.; Okonogi, T. M.; Alemayehu, S.; Hustedt, E. J.; Benight, A. S.; Sigurdsson, S. T.; Robinson, B. H. J. Phys. Chem. B 2009, 113, 2664
44. Krstic, I.; Frolow, O.; Sezer, D.; Endeward, B.; Weigand, J. E.; Suess, B.; Engels, J. W.; Prisner, T. F. J. Am. Chem. Soc. 2010, 132, 1454
45. Shelke, S. A.; Sigurdsson, S. T. Nucleic Acids Res. 2012, 40, 3732
46. Robinson, B. H.; Slusky, L. J.; Auteri, F. P. J. Chem. Phys. 1992, 96, 2609
47. Stoica, I. J. Phys. Chem. B 2003, 108, 1771
48. Beier, C.; Steinhoff, H.-J. Biophys. J. 2006, 91, 2647
49. Budil, D. E.; Sale, K. L.; Khairy, K. A.; Fajer, P. G. J. Phys. Chem. A 2006, 110, 3703
50. DeSensi, S. C.; Rangel, D. P.; Beth, A. H.; Lybrand, T. P.; Hustedt, E. J. Biophys. J. 2008, 94, 3798
51. Sezer, D.; Freed, J. H.; Roux, B. J. Am. Chem. Soc. 2009, 131, 2597
52. Sale, K.; Song, L.; Liu, Y. S.; Perozo, E.; Fajer, P. J. Am. Chem. Soc. 2005, 127, 9334
53. Fajer, M. I.; Li, H.; Yang, W.; Fajer, P. G. J. Am. Chem. Soc. 2007, 129, 13840
54. Piton, N.; Mu, Y.; Stock, G.; Prisner, T. F.; Schiemann, O.; Engels, J. W. Nucleic Acids Res. 2007, 35, 3128
55. Ding, F.; Layten, M.; Simmerling, C. J. Am. Chem. Soc. 2008, 130, 7184
56. Galiano, L.; Ding, F.; Veloro, A. M.; Blackburn, M. E.; Simmerling, C.; Fanucci, G. E. J. Am. Chem. Soc. 2009, 131, 430
57. Houriez, C. l.; FerreÌ, N.; Siri, D.; Masella, M. J. Phys. Chem. B 2009, 113, 15047
58. Stendardo, E.; Pedone, A.; Cimino, P.; Cristina Menziani, M.; Crescenzi, O.; Barone, V. Phys. Chem. Chem. Phys. 2010, 12, 11697
59. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E., 3rd; Laughton, C. A.; Orozco, M. Biophys. J. 2007, 92, 3817
60. Wecker, K.; Bonnet, M. C.; Meurs, E. F.; Delepierre, M. Nucleic Acids Res. 2002, 30, 4452
61. Heddi, B.; Foloppe, N.; Bouchemal, N.; Hantz, E.; Hartmann, B. J.Am. Chem. Soc. 2006, 128, 9170
62. Rene, B.; Masliah, G.; Antri, S. E.; Fermandjian, S.; Mauffret, O. J. Phys. Chem. B 2007, 111, 4235
63. Tian, Y.; Kayatta, M.; Shultis, K.; Gonzalez, A.; Mueller, L. J.; Hatcher, M. E. J. Phys. Chem. B 2009, 113, 2596
64. Olson, W. K.; Gorin, A. A.; Lu, X. J.; Hock, L. M.; Zhurkin, V. B. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 11163
65. Lankas, F.; Sponer, J.; Langowski, J.; Cheatham, T. E., 3rd. Biophys. J. 2003, 85, 2872
66. Fujii, S.; Kono, H.; Takenaka, S.; Go, N.; Sarai, A. Nucleic Acids Res. 2007, 35, 6063
67. Goni, J. R.; Perez, A.; Torrents, D.; Orozco, M. Genome Biol. 2007, 8, R263