Electron-electron distances in spin-labeled low-spin metmyoglobin variants by relaxation enhancement

Biophysical Journal

Volumn 95, Issue 11, 2008, Pages 5306-5316

  Ulyanov, Dmitriy ^a   Bowler, Bruce E ^a   Eaton, Gareth R ^a   Eaton, Sandra S ^a  

^a UNIVERSITY OF DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METMYOGLOBIN; MUTANT PROTEIN;

ANIMAL; ARTICLE; CHEMISTRY; ELECTRON; ELECTRON SPIN RESONANCE; GENETICS; MUTATION; SPIN LABELING; TEMPERATURE; TIME;

ANIMALS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRONS; METMYOGLOBIN; MUTANT PROTEINS; MUTATION; SPIN LABELS; TEMPERATURE; TIME FACTORS;

EID: 58149332178     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.108.141887     Document Type: Article

References (64)

1. Berliner, L. J., G. R. Eaton, and S. S. Eaton, editors. 2000. Biological Magnetic Resonance, Volume 19: Distance Measurements in Biological Systems by EPR. Kluwer Academic: New York.
2. Rabenstein, M. D., and Y.-K. Shin. 1995. Determination of the distance between two spin labels attached to a macromolecule. Proc. Natl. Acad. Sci. USA. 92:8239-8243.
3. Hustedt, E. J., A. I. Smirnov, C. F. Laub, C. E. Cobb, and A. H. Beth. 1997. Molecular distances from dipolar coupled spin-labels: the global analysis of multifrequency continuous wave electron paramagnetic resonance data. Biophys. J. 72:1861-1877.
4. Jeschke, G. 2002. Distance measurements in the nanometer range by pulse EPR. Chem. Phys. Chem. 3:927-932.
5. Jeschke, G., M. Pannier, and H. W. Spiess. 2000. Double electronelectron resonance. Biol. Magn. Reson. 19:493-512.
6. Tsvetkov, Y. D., and A. D. Milov. 2002. Pulsed ESR double resonance (PELDOR) spectroscopy: applications to spin-labeled peptides. In EPR in the 21st Century: Basics and Applications to Material, Life, and Earth Sciences. A. Kawamori, J. Yamauchi, and H. Ohta, editors. Elsevier, Amsterdam. 647-658.
7. Borbat, P. P., and J. H. Freed. 2000. Double-quantum ESR and distance measurements. Biol. Magn. Reson. 19:383-459.
8. Chiang, Y.-W., P. P. Borbat, and J. H. Freed. 2005. The determination of pair distance distributions by pulsed ESR using Tikhonov regularization. J. Magn. Reson. 172:279-295.
9. Bloembergen, N., E. M. Purcell, and R. V. Pound. 1948. Relaxation effects in nuclear resonance absorption. Phys. Rev. 73:679-712.
10. Lakshmi, K. V., and G. W. Brudvig. 2001. Pulsed electron paramagnetic resonance methods for macromolecular structure determination. Curr. Opin. Struct. Biol. 11:523-531.
11. Likhtenshtein, G. I. 2000. Depth of immersion of paramagnetic centers in biological systems. Biol. Magn. Reson. 19:309-346.
12. Rakowsky, M. H., K. M. More, A. V. Kulikov, G. R. Eaton, and S. S. Eaton. 1995. Time-domain electron paramagnetic resonance as a probe of electron-electron spin-spin interaction in spin-labeled low-spin iron porphyrins. J. Am. Chem. Soc. 117:2049-2057.
13. Zhou, Y., B. E. Bowler, G. R. Eaton, and S. S. Eaton. 2000. Electron spin-lattice relaxation rates for high-spin Fe(III) complexes in glassy solvents at temperatures between 6 and 298 K. J. Magn. Reson. 144:115-122.
14. Zhou, Y., B. E. Bowler, K. Lynch, S. S. Eaton, and G. R. Eaton. 2000. Interspin distances in spin-labeled metmyoglobin variants determined by saturation recovery EPR. Biophys. J. 79:1039-1052.
15. Budker, V., J.-L. Du, M. Seiter, G. R. Eaton, and S. S. Eaton. 1995. Electron-electron spin-spin interaction in spin-labeled low-spin methemoglobin. Biophys. J. 68:2531-2542.
16. Seiter, M., V. Budker, J.-L. Du, G. R. Eaton, and S. S. Eaton. 1998. Interspin distances determined by time domain EPR of spin-labeled high-spin methemoglobin. Inorg. Chim. Acta. 273:354-366.
17. + cluster and a flavin mononucleotide radical in the enzyme trimethylamine dehydrogenase: a high-field electron paramagnetic resonance study. J. Chem. Phys. 109:10905-10913.
18. Guigliarelli, B., C. More, A. Fournel, M. Asso, E. C. Hatchikian, R. Williams, R. Cammack, and P. Bertrand. 1995. Structural organization of the Ni and (4Fe-4S) centers in the active form of Desulfovibrio gigas hydrogenase. Analysis of the magnetic interactions by electron paramagnetic resonance spectroscopy. Biochemistry. 34:4781-4790.
19. Stevenson, R. C., W. R. Dunham, R. H. Sands, T. P. Singer, and H. Beinert. 1986. Studies on the spin-spin interaction between flavin and iron-sulfur cluster in an iron-sulfur flavoprotein. Biochim. Biophys. Acta. 869:81-88.
20. Vinogradov, A. D., V. D. Sled, D. S. Burbaev, V. G. Grivennikova, I. A. Moroz, and T. Ohnishi. 1995. Energy-dependent complex I-associated ubisemiquinones in submitochondrial particles. FEBS Lett. 370:83-87.
21. Fielding, A. J., R. J. Usselman, N. Watmough, M. Simkovic, F. E. Frerman, G. R. Eaton, and S. S. Eaton. 2008. Electron paramagnetic resonance characterization and interspin distance measurement of electron transfer flavoprotein ubiquinone oxidoreductase (ETF-QO). J. Magn. Reson. 190:222-232.
22. + cluster and on the catalytic activity in electron transfer flavoprotein-ubiquinone oxidoreductase (ETF-QO). Biochemistry. 47:92-100.
23. Lyubenova, S., M. K. Siddiqui, M. J. M. Penning DeVries, B. Ludwig, and T. F. Prisner. 2007. Protein-protein interactions studied by EPR relaxation measurements: cytochrome c and cytochrome c oxidase. J. Phys. Chem. B. 111:3839-3846.
24. m effects. Biol. Magn. Reson. 19:347-381.
25. Suzuki, T., and K. Imai. 1998. Evolution of myoglobin. Cell. Mol. Life Sci. 54:979-1004.
26. Takano, T. 1977. Structure of myoglobin refined at 2.0 Å resolution. II. Structure of deoxymyoglobin from sperm whale. J. Mol. Biol. 110: 569-584.
27. Takano, T. 1977. Structure of myoglobin refined to 2.0 Å resolution. I. Crystallographic refinement of metmyoglobin from sperm whale. J. Mol. Biol. 110:537-568.
28. Maurus, R., R. Bogumil, N. T. Nguyen, A. G. Mauk, and G. Brayer. 1998. Structural and spectroscopic studies of azide complexes of horse heart myoglobin and the His-64 to Thr variant. Biochem. J. 332:67-74.
29. Lee, B., and F. M. Richards. 1971. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:379-400.
30. Bowler, B. E., K. May, T. Zaragoza, P. York, A. Dong, and W. S. Caughey. 1993. Destabilizing effects of replacing a surface lysine of cytochrome c with aromatic amino acids: implications for the denatured state. Biochemistry. 32:183-187.
31. Alber, T. S., S. Dao-pin, J. A. Nye, D. C. Muchmore, and B. W. Matthews. 1987. Temperature-sensitive mutations of bacteriophage T4 lysozyme occur at sites with low mobility and low solvent accessibility in the folded protein. Biochemistry. 26:3754-3758.
32. Springer, B. A., and S. G. Sligar. 1987. High-level expression of sperm whale myoglobin in Escherichia coli. Proc. Natl. Acad. Sci. USA. 84: 8961-8965.
33. Phillips, G. N., Jr., R. M. Arduini, B. A. Springer, and S. G. Sligar. 1990. Crystal structure of myoglobin from a synthetic gene. Proteins Struct. Funct. Genet. 7:358-365.
34. Jennings, P. A., M. J. Stone, and P. E. Wright. 1995. Overexpression of myoglobin and assignment of its amide, Cα and Cβ resonances. J. Biomol. NMR. 6:271-276.
35. DeYoung, L. R., K. A. Dill, and A. L. Fink. 1993. Aggregation and denaturation of apomyoglobin in aqueous urea solutions. Biochemistry. 32:3877-3886.
36. Rossi-Fanelli, A., E. Antonini, and A. Caputo. 1958. Pure native globin from human hemoglobin: preparation and some physico-chemical properties. Biochim. Biophys. Acta. 28:221.
37. Stryer, L. 1965. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of nonpolar binding sites. J. Mol. Biol. 13:482-495.
38. Smith, M. H. 1959. Kinetics and equilibria in systems containing heme, carbon monoxide, and pyridine. Biochem. J. 73:90-101.
39. Peisach, J., and W. E. Blumberg. 1971. Specific compounds formed during the reversible and irreversible denaturation of hemoglobin and its constituent chains. Genet., Funct., Phys. Stud. Hemoglobins, Proc. 1st Inter-Amer. Symp. Hemoglobins. 199-207.
40. DiIorio, E. 1981. Hemoglobins. Methods Enzymol. 76:57-72.
41. Sato, H., V. Kathirvelu, A. J. Fielding, S. E. Bottle, J. P. Blinco, A. S. Micallef, S. S. Eaton, and G. R. Eaton. 2007. Impact of molecular size on electron spin relaxation rates of nitroxyl radicals in glassy solvents between 100 and 300 K. Mol. Phys. 105:2137-2151.
42. Zhou, Y., R. Mitri, G. R. Eaton, and S. S. Eaton. 1999. Electron spin lattice relaxation processes for molecular S = 1/2 systems in glassy matrices at temperatures between 10 and 130 K. Curr. Top. Biophys. 23:63-68.
43. 1 in a spinlabeled porphyrin. Modern Applications of EPR/ESR: From Biophysics to Materials Science, Proceedings of the Asia-Pacific EPR/ESR Symposium, 1st, Kowloon, Hong Kong, Jan. 20-24, 1997. 19-24.
44. Fielding, A. J., D. B. Back, M. Engler, B. Baruah, D. C. Crans, G. R. Eaton, and S. S. Eaton. 2007. Electron spin lattice relaxation of V(IV) complexes in glassy solutions between 15 and 70 K. ACS Symp. Ser. 974:364-375.
45. Fielding, A. J., S. Fox, G. L. Millhauser, M. Chattopadhyay, P. M. H. Kroneck, G. Fritz, G. R. Eaton, and S. S. Eaton. 2006. Electron spin relaxation of copper(II) complexes in glassy solution between 10 and 120 K. J. Magn. Reson. 179:92-104.
46. Eaton, S. S., and G. R. Eaton. 2000. Relaxation times of organic radicals and transition metal ions. In Distance Measurements in Biological Systems by EPR. L. J. Berliner, S. S. Eaton, and G. R. Eaton, editors. Kluwer Academic/Plenum Publishers, New York. 29-154.
47. Poole, C. P., and H. Farach. 1971. Relaxation in Magnetic Resonance. Academic Press, New York.
48. Kulikov, A. V., and G. I. Likhtenshtein. 1977. The use of spin relaxation phenomena in the investigation of the structure of model and biological systems by the method of spin labels. Adv. Mol. Relax. Interact. Proc. 10:47-69.
49. Salikhov, K. M., and Y. D. Tsvetkov. 1979. Electron spin-echo studies of interactions in solids. In Time Domain Electron Spin Resonance. L. Kevan and R. N. Schwartz, editors. John Wiley, New York. 232-277.
50. Zhidomirov, G. M., and K. M. Salikhov. 1969. Contribution to the theory of spectral diffusion in magnetically diluted solids. Sov. Phys. JETP. 29:1037-1040.
51. Brown, I. M. 1979. Electron spin echo studies of relaxation processes in molecular solids. In Time Domain Electron Spin Resonance. L. Kevan and R. N. Schwartz, editors. John Wiley, New York. 195-229.
52. Zecevic, A., G. R. Eaton, S. S. Eaton, and M. Lindgren. 1998. Dephasing of electron spin echoes for nitroxyl radicals in glassy solvents by non-methyl and methyl protons. Mol. Phys. 95:1255-1263.
53. Arnold, E. V., D. S. Bohle, and P. A. Jordan. 1999. Reversible and irreversible hemichrome generation by the oxygenation of nitrosylmyoglobin. Biochemistry. 38:4750-4756.
54. Peisach, J., and W. B. Mims. 1977. Linear electric field effect in electron paramagnetic resonance for two bisimidazole-heme complexes, model compounds for B and H hemichromes of hemoglobin and for cytochrome b5. Biochemistry. 16:2795-2799.
55. Kay, M. S., C. H. Ramos, and R. L. Baldwin. 1999. Specificity of native-like interhelical hydrophobic contacts in the apomyoglobin intermediate. Proc. Natl. Acad. Sci. USA. 96:2007-2012.
56. Scott, E. E., E. V. Paster, and J. S. Olson. 2000. The stabilities of mammalian apomyoglobins vary over a 600-fold range and can be enhanced by comparative mutagenesis. J. Biol. Chem. 275:27129-27136.
57. Barrick, D., and F. W. Dahlquist. 2000. Trans-substitution of the proximal hydrogen bond in myoglobin: I. Structural consequences of hydrogen bond deletion. Proteins Struct. Funct. Genet. 39:278-290.
58. Langen, R., K. J. Oh, D. Cascio, and W. L. Hubbell. 2000. Crystal structure of spin labeled T4 lysozyme mutants: implications for the interpretation of EPR spectra in terms of structure. Biochemistry. 39:8396-8405.
59. Kispert, L. D., M. K. Bowman, J. R. Norris, and M. S. Brown. 1982. Electron spin echo studies of the internal motion of radicals in crystals: phase memory vs. correlation time. J. Chem. Phys. 76:26-30.
60. Eaton, S. S., and G. R. Eaton. 2000. Distance measurements by CW and pulsed EPR. Biol. Magn. Reson. 19:1-27.
61. Baldwin, R. L. 1995. Alpha-helix formation by peptides of defined sequence. Biophys. Chem. 55:127-135.
62. Cavagnero, S., Y. Theriault, S. S. Narula, H. J. Dyson, and P. E. Wright. 2000. Amide proton hydrogen exchange rates for sperm whale myoglobin obtained from 15N-1H NMR spectra. Protein Sci. 9:186-193.
63. Feng, Z., M. C. Butler, S. L. Alam, and S. N. Loh. 2001. On the nature of conformational openings: native and unfolded-state hydrogen and thiol-disulfide exchange studies of ferric aquomoglobin. J. Mol. Biol. 314:153-166.
64. Poole, C. P., Jr., and H. A. Farach. 1971. Dipolar interaction. In Relaxation in Magnetic Resonance. C. P. Poole, Jr., and H. A. Farach, editors. Academic Press, New York. 69-71. Eqs. 66.42-66.44.