Simultaneous binding of fluoride and NO to the nonheme iron of photosystem II: Quantitative EPR evidence for a weak exchange interaction between the semiquinone Q(A)- and the iron-nitrosyl complex

Journal of the American Chemical Society

Volumn 121, Issue 39, 1999, Pages 9155-9164

  Sanakis, Yiannis ^a   Petasis, Doros ^a   Petrouleas, Vasili ^b   Hendrich, Michael ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b INSTITUTE OF MATERIALS SCIENCE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE ION; COORDINATION COMPOUND; FLUORIDE; IRON COMPLEX; NITRIC OXIDE; NITROSO DERIVATIVE; NONHEME IRON PROTEIN; RADICAL; SEMIQUINONE;

ARTICLE; CHEMICAL BINDING; CHEMICAL INTERACTION; COMPLEX FORMATION; ELECTRON SPIN RESONANCE; ILLUMINATION; PHOTOSYSTEM II; THYLAKOID MEMBRANE;

EID: 0032879508     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja990533b     Document Type: Article

References (71)

1. B, the primary and secondary plastoquinone electron acceptors of PSII, respectively; EPR, electron paramagnetic resonance; MES, 4-morpholineethanesulfonic acid; Tris, 2-amino-2-hydroxymethylpropane-1,3-diol; EDTA; ethylenediaminetetraacetate.
2. Diner, B. A.; Babcock, G. T. In Advances in Photosynthesis: Oxygenic Photosynthesis: The Light Reactions; Ort, D. R., Yocum, C. F., Eds; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996; Vol. 4, pp 213-247.
3. (b) Diner, B. A.; Petrouleas, V.; Wendoloski, J. J. Physiol. Plant 1991, 81, 423-436.
4. Deisenhofer, J.; Michel, H. EMBO J. 1989, 8, 2149-2169.
5. Petrouleas, V.; Diner, B. A. Biochim. Biophys. Acta 1990, 1015, 131-140.
6. (b) Diner, B. A.; Petrouleas, V. Biochim. Biophys. Acta 1990, 1015, 141-149.
7. (c) Hienerwadel, R.; Berthomieu, C. Biochemistry 1995, 34, 16288-16297.
8. 7 nomenclature refers to the covalent FeNO complex which has seven d-electrons.
9. Deligiannakis, Y.; Petrouleas, V.; Diner, B. A. Biochim. Biophys. Acta 1994, 1188, 260.
10. (b) Petrouleas, V.; Deligiannakis, Y.; Diner, B. A Biochim. Biophys. Acta 1994, 1188, 271.
11. Vermaas, W. F. J.; Rutherford, A. W. FEBS Lett. 1984, 175, 243.
12. Koulougliotis, D.; Kostopoulos, T.; Petrouleas, V.; Diner, B. A. Biochim. Biophys. Acta 1141, 1993, 275-282.
13. (b) Sanakis, Y.; Petrouleas, V.; Diner, B. A. Biochemistry 1994, 33, 9922-9928.
14. Rutherford, A. W.; Zimmerman, J. L. Biochim. Biophys. Acta 1984, 767, 168-175.
15. (b) Nugent, J. H. A.; Diner, B. A.; Evans, M. C. W. FEBS Lett. 1981, 124, 241-244.
16. (c) Nugent, J. H. A.; Doetschman, D. C.; MacLachlan, D. J. Biochemistry 1992, 31, 2935-2941.
17. Petrouleas, V.; Sanakis, Y.; Deligiannakis, Y.; Diner, B. A. In Research in Photosynthesis; Murata, N., Ed.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1992, Vol. II, pp 119-122.
18. Dutton, P. L.; Leigh, J. S.; Reed, E. W. Biochim. Biophys. Acta 1973, 292, 654-664.
19. Butler, W. F.; Calvo, R.; Fredkin, D. R.; Isaacson, R. A.; Okamura, M. Y.; Feher, G. Biophys. J. 1984, 45, 947-973.
20. (b) Dismukes, G. C.; Frank, H. A.; Friesner, R.; Sauer, K. Biochim. Biophys. Acta 1984, 764, 253-271.
21. Berthold, D. A.; Babcock, G. T.; Yocum, C. F. FEBS Lett. 1981, 134, 231-234.
22. (b) Ford, R. C.; Evans, M. C. W. FEBS Lett. 1983, 160, 159-164.
23. For a review on the treatments affecting the Mn-complex of PSII, see Debus, R. J. Biochim. Biophys. Acta 1992, 1102, 269-352.
24. Petasis, D. T.; Hendrich, M. P. J. Magn. Reson. 1999, 136, 200-206.
25. Klimov, V. V.; Dolan, E.; Shaw, E. R.; Ke, B. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 7227-7231.
26. Pilbrow, J. R. Transition Ion Electron Paramagnetic Resonance; Clarendon Press: Oxford, U.K., 1990; pp 211-259, 341, 631-638.
27. z is also not measurable.
28. Van Camp, H. L.; Scholes, C. P.; Mulks, C. F.; Caughey, W. S. J. Am. Chem. Soc. 1977, 99, 8283-8290.
29. (b) Morimoto, H.; Kotani, M. Biochim. Biophys. Acta 1966, 126, 176-178.
30. For a review on usual EPR signals from PSII, see Miller, A.-F.; Brudvig, G. W. Biochim. Biophys. Acta 1991, 1056, 1-8.
31. Diner, B. A.; Petrouleas, V. Biochim. Biophys. Acta 1987, 893, 138-148.
32. D. Koulougliotis, Diploma Thesis, NCSR Democritos, unpublished results.
33. Allen, J. P.; Feher, G.; Yeates T. O.; Komiya, H.; Rees, D. C. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 8487-8491.
34. (b) El-Kabbani, O.; Chang, C.-H.; Tiede, D.; Noms J.; Schiffer, M. Biochemistry 1991, 30, 5361-5369.
35. (c) Emler, U.; Fritzsch, G.; Buchanan, S. K.; Michel, H. Structure 1994, 2 925-936.
36. DeRose, V. J.; Latimer, M. J.; Zimmermann, J.-L.; Mikerji, I.; Yachandra, V. K.; Sauer, K.; Klein, M. P. Chem. Phys. 1995, 194, 443-459.
37. Britt, R. D. In Advances in Photosynthesis: Oxygenic Photosynthesis: The Light Reactions; Ort, D. R., Yocum, C. F., Eds; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1996; Vol. 4, pp 113-136.
38. (b) Lindberg K.; Andreasson L.-E. Biochemistry 1996, 35, 14259-14267.
39. Stemler, A.; Murphy, J. Plant Physiol. 1985, 77, 974-977.
40. Brown, C. A.; Pavlosky, M. A.; Westre, T. E.; Zhang, Y.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1995, 117, 715-732.
41. Ray, M.; Golombek, A. P.; Hendrich, M. P.; Yap, G. P.; Liable-Sands, L. M.; Rheingold, A. L.; Borovik, A. S. Inorg. Chem. 1999, 38, 3110-3115.
42. 1 suggesting a 7-coordinated iron ion was considered unlikely.
43. Nocek, J. M.; Kurtz, D. M., Jr.; Sage, J. T.; Xia, Y.-M.; Debrunner, P.; Shiemke, A. K.; Sanders-Loehr, J.; Loehr, T. M. Biochemistry 1988, 27, 1014-1024.
44. Owen, J.; Thornley, J. H. M. Rep. Prog. Phys. 1966, 29, 675-728.
45. (b) Abragam, A.; Bleaney, B. Electron Paramagnetic Resonance of Transition Ions; Clarendon Press: Oxford, U.K., 1970.
46. Wertz, J. E.; Bolton, J. R. Electron Spin Resonance; Chapman and Hall, New York, 1986, p 498.
47. Hoffman, B. M.; Martinsen, J.; Venters, R. A. J. Magn. Res. 1984, 58, 110-123.
48. Hall, T. P. P.; Hayes, W.; Stevenson, R. W. H.; Wilkens, J. J. Chem. Phys. 1963, 38, 1977-1984.
49. (b) Radnell, C. J.; Pilbrow, J. R.; Subramanian S.; Rogers, M. T. J. Chem. Phys. 1975, 12, 4948-4952.
50. Arciero, D. M.; Orville, A. M.; Lipscomb, J. D. J. Biol. Chem. 1985, 260, 14035-14044.
51. (b) Orville, A. M.; Lipscomb, J. D. J. Biol. Chem. 1993, 268, 8596-8607.
52. Koehler, B. P.; Mukund, S.; Conover, R. C.; Dhawan, I. K.; Roy, R.; Adams, M. W. W.; Johnson, M. K. J. Am. Chem. Soc. 1996, 118, 12391-12405.
53. 2 = 1/2 species can be found in Kundalika, M. M.; Eaton, G. R.; Eaton, S. S. Inorg. Chem. 1986, 25, 2638-2646.
54. Ogasenyan, V. S.; Butler, C. S.; Watmough, N. J.; Greenwood, C.; Thomson, A. J.; Cheesman, M. R. J. Am. Chem. Soc. 1998, 120, 4232-4233.
55. Hendrich, M. P.; Debrunner, P. G. Biophys. J. 1989, 56, 489-506.
56. Euler, W. B. Inorg. Chem. 1986, 25, 1871-1875.
57. Calvo, R.; Passeggi, M. C. G.; Isaacson, R. A.; Okamura, M. Y.; Feher, G. Biophys. J. 1990 58, 149-165.
58. Allen, J. P.; Feher, G.; Yeates T. O.; Komiya, H.; Rees, D. C. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 8487-8491.
59. (b) El-Kabbani, O.; Chang, C.-H.; Tiede, D.; Norris J.; Schiffer, M. Biochemistry 1991, 30, 5361-5369.
60. (c) Emler, U.; Fritzsch, G.; Buchanan, S. K.; Michel, H. Structure 1994, 2, 925-936.
61. Bosch, M. K.; Gast, P.; Hoff., A. J.; Spoyalov, A. P.; Tsvetkov, Y. D. Chem. Phys. Lett. 1995, 239, 306-312.
62. Astashkin, A. V.; Kawamori, A.; Kodera, Y.; Kuroiwa, S.; Akabori, K. J. Chem. Phys. 1995, 102, 5583.
63. (b) Deligiannakis, Y.; Jegerschold, C.; Rutherford, A. W. Chem. Phys. Lett. 1997, 270, 564-572.
64. (c) Astashkin, A. V.; Hara, H.; Kuroiwa, S.; Kawamori, A.; Akabori, K. J. Chem. Phys. 1998, 108, 10143-10151.
65. (d) Noguchi, T.; Inoue, Y.; Tang, X.-S. Biochemistry 1999, 38, 399-403
66. (e) Peloquin, J. M.; Tang, X.-S.; Diner, B. A.; Britt, R. D. Biochemistry 1999, 38, 2057-2067.
67. Coffmann, R. E.; Buettner, G. R. J. Phys. Chem. 1979, 83, 2387-2392.
68. - sample is retained, then we must increase the distance in order to eliminate the dipolar effects.
69. Guigliarelli, B.; Guillaussier, J.; More, C.; Setif, P.; Bottin; H.; Bertrand, P. J. Biol. Chem. 1993, 268, 900-908.
70. (b) Bertrand, P.; More, C.; Guigliarelli, B.; Fournel, A.; Bennett, B.; Howes, B. J. Am. Chem. Soc. 1994, 116, 3078-3086.
71. Analogous theoretical treatment has been carried out for the excited, [3/2] state. We find that either no transitions can be induced between the energy levels or the transition probabilities are negligible.