Magnetic interactions sense changes in distance between heme bL and the iron-sulfur cluster in cytochrome bc1

Biochemistry

Volumn 48, Issue 24, 2009, Pages 5708-5720

  Sarewicz, Marcin ^a   Dutka, Małgorzata ^a   Froncisz, Wojciech ^a   Osyczka, Artur ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC CORE; COFACTORS; CYTOCHROME C; DIPOLAR COUPLINGS; DIPOLAR RELAXATION; DYNAMIC DISTRIBUTION; EQUILIBRIUM DISTRIBUTIONS; EQUILIBRIUM POSITIONS; FROZEN SOLUTIONS; GLASS STATE; IRON-SULFUR CLUSTERS; KEY ENZYMES; LIQUID PHASE; MAGNETIC INTERACTIONS; PHASE RELAXATION; POTENTIAL GRADIENTS; SPECTROSCOPIC PARAMETERS;

CATALYTIC OXIDATION; ENERGY CONVERSION; HEMOGLOBIN; PORPHYRINS; SULFUR; SYNTHETIC METALS;

MAGNETIC DOMAINS;

GLASS; HEME; IRON SULFUR PROTEIN; UBIQUINOL CYTOCHROME C REDUCTASE;

ARTICLE; CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; FREEZING; MAGNETISM; MUTATION; OXIDATION; PRIORITY JOURNAL; SPECTROSCOPY;

BINDING SITES; CATALYTIC DOMAIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX III; HEME; IRON; MODELS, MOLECULAR; OXIDATION-REDUCTION; RHODOBACTER CAPSULATUS; SULFUR;

EID: 67649229861     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900511b     Document Type: Article

References (70)

1. Berry, E. A., Guergova-Kuras, M., Huang, L., and Crofts, A. R. (2000) Structure and function of cytochrome bc complexes. Annu. Rev. Biochem. 69, 1005-1075.
2. 1 complex from bovine heart mitochondria. Science 277, 60-66.
3. 1 complex. Science 281, 64-71.
4. 1. Nature 392, 677-684.
5. v fragment. Structure 8, 669-684.
6. 1: comparison with its mitochondrial and chloroplast counterparts. Photosynth. Res. 81, 251-275.
7. 1 from the photosynthetic bacterium Rhodobacter sphaeroides. J. Biol. Chem. 283, 2846-2857.
8. 6f complex of oxygenic photosynthesis: tuning the cavity. Science 302, 1009-1014.
9. 6f complex. Nature 426, 413-418.
10. Mitchell, P. (1975) The protonmotive Q cycle: a general formulation. FEBS Lett. 59, 137-139.
11. Osyczka, A., Moser, C. C., Daldal, F., and Dutton, P. L. (2004) Reversible redox energy coupling in electron transfer chains. Nature 427, 607-612. (Pubitemid 38248474)
12. Rich, P. R. (2004) The quinone chemistry of bc complexes. Biochim. Biophys. Acta 1658, 165-171.
13. Osyczka, A., Moser, C. C., and Dutton, P. L. (2005) Fixing the Q cycle. Trends Biochem. Sci. 30, 176-182.
14. Cape, J. L., Bowman, M. K., and Kramer, D. M. (2006) Understanding the cytochrome bc complexes by what they don't do. The Q cycle at 30. Trends Plant Sci. 11, 46-55.
15. 1 complex: a new gating mechanism that prevents short circuits. Biochim. Biophys. Acta 1757, 1019-1034.
16. 1 complex: reaction mechanism and prevention of short-circuiting. Biochim. Biophys. Acta 1709, 5-34.
17. 1: a new device for electron transfer in proteins. Trends Biochem. Sci. 26, 445-451.
18. 1 complex. Biochim. Biophys. Acta 1365, 261-268.
19. 1 complex. J. Mol. Biol. 341, 281-302.
20. 1 and its implications for energy conversion. Proc. Natl. Acad. Sci. U.S.A. 97, 4567-4572.
21. o site catalysis. J. Biol. Chem. 277, 3471-3476.
22. 1 complex by the formation of an intersubunit disulfide bond between cytochrome b and the iron-sulfur protein. J. Biol. Chem. 275, 38597-38604.
23. 1 complex. Biochemistry 44, 10520-10532.
24. Brugna, M., Rodgers, S., Schricker, A., Montoya, G., Kazmeier, M., Nitschke, W., and Sinning, I. (2000) A spectroscopic method for observing the domain movement of the Rieskie iron-sulfur protein. Proc. Natl. Acad. Sci. U.S.A. 97, 2069-2074.
25. 6f complex "Rieske" iron-sulfur protein domain movements. Biochemistry 41, 4070-4079.
26. o site occupants and the head domain position of the Fe-S protein subunit. Biochemistry 43, 2217-2227.
27. 1. Biochemistry 48, 1888-1899.
28. Hung, S. C., Grant, C. V., Peloquin, J. M., Waldeck, A. R., Britt, R. D., and Chan, S. I. (2000) Electron spin-lattice relaxation measurement of the 3Fe-4S (S-3) cluster in succinate:ubiquinone reductase from Paracoccus denitrificans. A detailed analysis based on a dipole-dipole interaction model. J. Phys. Chem. A 104, 4402-4412.
29. Kulikov, A. V., and Likhtenshtein, G. I. (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. Processes 10, 47-69.
30. Goodman, G., and Leigh, J. S. (1985) Distance between the visible copper and cytochrome a in bovine heart cytochrome oxidase. Biochemistry 24, 2310-2317. (Pubitemid 15009486)
31. Hirsh, D. J., Beck, W. F., Innes, J. B., and Brudvig, G. W. (1992) Using saturation-recovery EPR to measure distances in proteins: applications to photosystem II. Biochemistry 31, 532-541.
32. Zhou, Y., Bowler, B. E., Lynch, K., Eaton, S. S., and Eaton, G. R. (2000) Interspin distances in spin-labeled metmyoglobin variants determined by saturation recovery EPR. Biophys. J. 79, 1039-1052. (Pubitemid 30626195)
33. Ulyanov, D., Bowler, B. E., Eaton, G., and Eaton, S. S. (2008) Electron-electron distances in spin-labeled low-spin metmyoglobin variants by relaxation enhancement. Biophys. J. 95, 5306-5316.
34. Rakowsky, M. H., More, K. M., Kulikov, A. V., Eaton, G. R., and Eaton, S. S. (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.
35. Fielding, A. J., Usselman, R. J., Watmough, N., Simkovic, M., Frerman, F. E., Eaton, G. R., and Eaton, S. S. (2008) Electron spin relaxation enhancement measurements of interspin distances in human, porcine, and Rhodobacter electron transfer flavoprotein-ubiquinone oxidoreductase (ETF-QO). J. Magn. Reson. 190, 222-232.
36. Fajer, F. G. (2005) Site directed spin labelling and pulsed dipolar electron paramagnetic resonance (double electron-electron resonance) of force activation in muscle. J. Phys.: Condens. Matter 17, 1459-11459
37. o site catalysis. Biochemistry 39, 3285-3296.
38. Lyubenova, S., Siddiqui, M. K., Penning, M. J. M., Ludwig, B., and Prisner, T. F. (2007) Protein-protein interactions studied by EPR relaxation measurements: cytochrome c and cytochrome c oxidase. J. Phys. Chem. B 11, 3839-3846.
39. 2 states. Phys. Chem. Chem. Phys. 6, 4890-4896.
40. Ohnishi, T., Schagger, H., Meinhardt, S. W., LoBrutto, R., Link, T. A., and von Jagow, G. (1989) Spatial organization of redox active centers in the bovine heart ubiquinol-cytochrome c oxidoreductase. J. Biol. Chem. 264, 735-744.
41. 1 complex and for photosynthetic growth of Rhodobacter capsulatus. Proc. Natl. Acad. Sci. U.S.A. 88, 492-496.
42. o) site with purified Fe-S protein subunit. Biochemistry 37, 16242-16251.
43. Williams-Smith, D. L., Bray, R. C., Barber, M. J., Tsopanakis, A. D., and Vincent, S. P. (1977) Changes in apparent pH on freezing aquenous buffer solutions and their relevance to biochemical electronparamagnetic-resonance spectroscopy. Biochem. J. 167, 593-600. (Pubitemid 8240975)
44. Hirsh, D. J., and Brudvig, G. W. (2007) Measuring distances in proteins by saturation-recovery EPR. Nat. Protoc. 2, 1770-1781.
45. Telser, J., Hoffman, B. M., LoBrutto, R., Ohnishi, T., Tsai, A. L., Simpkin, D., and Palmer, G. (1987) Evidence forNcoordination to Fe in the [2Fe-2S] center in yeast mitochondrial complex III. Comparison with similar findings for analogous bacterial [2Fe-2S] proteins. FEBS Lett. 214, 117-121.
46. Huber, M., Lindgren, M., Hammarstrom, P., Martensson, L. G., Carlsson, U., Eaton, G. R., and Eaton, S. S. (2001) Phase memory relaxation times of spin labels in human carbonic anhydrase II: pulsed EPR to determine spin label location. Biophys. Chem. 94, 245-256.
47. Eichel, R. A., Granwehr, J., and Schweiger, A. (2003) Measurement of spin-lattice relaxation times in EPR with enhanced orientation selectivity. J. Magn. Reson. 162, 380-384.
48. Lindsey, C. P., and Patterson, G. D. (1980) Detailed comparision of the Williams-Watts and Cole-Davidson functions. J. Chem. Phys. 73, 3348-3357.
49. Zhidomirov, G. M., and Salikhov, K. M. (1969) Contribution to the theory of spectral diffusion in magnetically diluted solids. Sov. Phys. JETP 29, 1037-1040.
50. Salerno, J. C. (1984) Cytochrome electron spin resonance line shapes, ligand fields, and components stoichiometry in ubiquinol-cytochrome c oxidoreductase. J. Biol. Chem. 259, 2331-2336.
51. 1 complex. Biochemistry 43, 430-436.
52. Stoll, S., and Schweiger, A. (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J. Magn. Reson. 178, 42-55.
53. Beinert, H. (2000) Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem. 5, 2-15.
54. 1 complex. Biochemistry 34, 15979-15996.
55. o site model. Biochemistry 31, 3144-3158.
56. 2 oxidoreductase from Rhodobacter capsulatus: definition of a minimal, functional isolated preparation. Biochemistry 32, 1310-1317.
57. 1 complex). FEBS Lett. 431, 423-426.
58. 2+ EPR spectra. J. Chem. Phys. 73, 3123-3131.
59. Zu, Y., Fee, J. A., and Hirst, J. (2002) Breaking and re-forming the disulfide bond at the high-potential respiratory-type Rieske [2Fe2S] center of Thermus thermophilus: characterization of the sulfhydryl state by protein-film voltammetry. Biochemistry 41, 14054-14065. (Pubitemid 35364878)
60. Martínez, M. C., and Torre, J. G. (1987) Brownian dynamics simulation of restricted rotational diffusion. Biophys. J. 52, 303-310.
61. Prosser, R. S., and Davis, J. H. (1994) Dynamics of an integral membrane peptide: a deuteriumNMRrelaxation study of gramicidin. Biophys. J. 66, 1429-1440. (Pubitemid 24145140)
62. Budil, D. E., Sale, K. L., Khairy, K. A., and Fajer, P. G. (2006) Calculating slow-motional electron paramagnetic resonance spectra from molecular dynamics using a diffusion operator approach. J. Phys. Chem. A 110, 3703-3713.
63. 1 complex. Proc. Natl. Acad. Sci. U.S.A. 103, 13045-13050.
64. o site for reaction with oxygen. Biochemistry 47, 12365-12370.
65. 1 complex from bovine heart. Proc. Natl. Acad. Sci. U.S.A. 95, 8026-8033.
66. i site. Biochemistry 42, 9067-9080.
67. 1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. J. Mol. Biol. 351, 573-597.
68. 1 complex: effects of inhibitors and mutations. Biochemistry 39, 15484-15492.
69. 1 complex: the advantages of being a twin. Biochim. Biophys. Acta 1777, 1079-1091.
70. 1 complexes of phototrophic bacteria: introducing the activated Q-cycle. Photochem. Photobiol. Sci. 6, 19-34.