ENDOR of NO-ligated cytochrome c′

Journal of the American Chemical Society

Volumn 128, Issue 15, 2006, Pages 5021-5032

  Usov, Oleg M ^a   Choi, Peter S T ^b   Shapleigh, James P ^b   Scholes, Charles P ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b Cornell University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER CONCENTRATION; DENITRIFICATION; DEUTERIUM; NITROGEN; TENSORS;

CYTOCHROME; EPR LINE SHAPE; G-TENSOR AXIS; NO-BOUND HEME;

PIGMENTS;

ARGININE; CYTOCHROME C'; DEUTERIUM; HEME; NITRIC OXIDE; NITROGEN; PHENYLALANINE; PROTON;

ARTICLE; DENSITY; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; HYDROGEN BOND; RHODOBACTER SPHAEROIDES;

CYTOCHROMES C'; ELECTRON SPIN RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NITRIC OXIDE; NITROGEN ISOTOPES; RHODOBACTER SPHAEROIDES; THERMODYNAMICS;

EID: 33646121774     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja055323f     Document Type: Article

References (72)

1. Denninger, J. W.; Marletta, M. A. Biochim. Biophys. Acta 1999, 1411, 334-350.
2. Wasser, I. M.; de Vries, S.; Moenne-Loccoz, P.; Schroder, I.; Karlin, K. D. Chem. Rev. 2002, 102, 1201-1234.
3. Ballou, D. P.; Zhao, Y.; Brandish, P. E.; Marletta, M. A. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 12097-12101.
4. Zhao, Y.; Hoganson, C.; Babcock, G. T.; Marletta, M. A. Biochemistry 1998, 37, 12458-12464.
5. Zhao, Y.; Brandish, P. E.; Ballou, D. P.; Marletta, M. A. Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 14753-14758.
6. Lawson, D. M.; Stevenson, C. E.; Andrew, C. R.; George, S. J.; Eady, R. R. Biochem. Soc. Trans. 2003, 31, 553-557.
7. Lawson, D. M.; Stevenson, C. E.; Andrew, C. R.; Eady, R. R. EMBO J. 2000, 19, 5661-5671.
8. Mayburd, A. L.; Kassner, R. J. Biochemistry 2002, 41, 11582-11591.
9. Stone, J. R.; Marletta, M. A. Biochemistry 1994, 33, 5636-5640.
10. Stone, J. R.; Sands, R. H.; Dunham, W. R.; Marletta, M. A. Biochem. Biophys. Res. Commun. 1995, 207, 572-577.
11. Zhao, Y.; Marletta, M. A. Biochemistry 1997, 36, 15959-15964.
12. Zhao, Y.; Schelvis, J. P.; Babcock, G. T.; Marletta, M. A. Biochemistry 1998, 37, 4502-4509.
13. Zhao, Y.; Brandish, P. E.; DiValentin, M.; Schelvis, J. P.; Babcock, G. T.; Marletta, M. A. Biochemistry 2000, 39, 10848-10854.
14. Choi, P. S.-T. Insights into nitric oxide metabolism by the denitrifier Rhodobacter sphaeroides 2.4.3″. Ph.D., Cornell, 2004.
15. Choi, P. S.; Grigoryants, V. M.; Abruna, H. D.; Scholes, C. P.; Shapleigh, J. P. J. Bacteriol. 2005, 187, 4077-4085.
16. Ellison, M. K.; Scheidt, W. R. J. Am. Chem. Soc. 1997, 119, 7404-7405.
17. Hayes, R. G.; Ellison, M. K.; Scheidt, W. R. Inorg. Chem. 2000, 39, 3665-3668.
18. Ramirez, L. M.; Axelrod, H. L.; Herron, S. R.; Rupp, B.; Allen, J. P.; Kantardjieff, K. A. Journal of Chemical Crystallography 2003, 33, 413-424.
19. Scholes, C. P. ENDOR on Hemes and Hemoproteins. In Multiple Electron Resonance Spectroscopy; Dorio, M., Freed, J. H., Eds., Plenum Press: New York, 1979; pp 297-329.
20. Scholes, C. P.; Lapidot, A.; Mascarenhas, R.; Inubushi, T.; Isaacson, R. A.; Feher, G. J. Am. Chem. Soc. 1982, 104, 2724-2735.
21. Scholes, C. P.; Falkowski, K. M.; Chen, S.; Bank, J. J. Am. Chem. Soc. 1986, 108, 1660-1671.
22. Usov, O. M.; Choi, P. S.-T.; Shapleigh, J. P.; Scholes, C. P. J. Am. Chem. Soc. 2005, 127, 9485-9494.
23. Dickinson, L. C.; Chien, J. C. J. Am. Chem. Soc. 1971, 93, 5036-5040.
24. Dickinson, L. C.; Chien, J. C. Biochem. Biophys. Res. Commun. 1974, 59, 1292-1297.
25. Hori, H.; Ikeda-Saito, M.; Yonetani, T. J. Biol. Chem. 1981, 256, 7849-7855.
26. LoBrutto, R.; Wei, Y. H.; Mascarenhas, R.; Scholes, C. P.; King, T. E. J. Biol. Chem. 1983, 258, 7437-7448.
27. LoBrutto, R.; Wei, Y. H.; Yoshida, S.; Van Camp, H. L.; Scholes, C. P.; King, T. E. Biophys. J. 1984, 45, 473-479.
28. Hüttermann, J.; Burgard, C.; Kappl, R. J. Chem. Soc., Faraday Trans. 1994, 90, 3077-3087.
29. Hohn, M.; Hüttermann, J.; Chien, J. C. W.; Dickinson, L. C. J. Am. Chem. Soc. 1983, 105, 109-115.
30. Kappl, R.; Hüttermann, J. Israel Journal of Chemistry 1989, 29, 73-84.
31. Flores, M.; Wajnberg, E.; Bemski, G. Biophys. J. 2000, 78, 2107-2115.
32. Zhang, Y.; Gossman, W.; Oldfield, E. J. Am. Chem. Soc. 2003, 125, 16387-16396.
33. Zeng, Z.; Guenzburger, D.; Ellis, D. E. THEOCHEM 2004, 678, 145-156.
34. Gilbert, D. C.; Doetschman, D. C. Chemical Physics 2001, 269, 125-135.
35. Scheidt, W. R.; Frisse, M. E. J. Am. Chem. Soc. 1975, 97, 17-21.
36. SIMPIPM is an extension of PIP which is an extension of QPOW. Nilges, M. J., Belford, R. L., and Francesconi, L. C. Simulation of strain in EPR spectra using the method of gradients; 40th Rocky Mountain Conference on Analytical Chemistry, Denver, Colorado, July 1998. For QPOW, see: Nilges, M. J., Thesis, University of Illinois, Urbana, 1979.
37. Sienkiewicz, A.; Smith, B. G.; Veselov, A.; Scholes, C. P. Rev. Sci. Instrum. 1996, 67, 2134-2138.
38. Veselov, A.; Olesen, K.; Sienkiewicz, A.; Shapleigh, J. P.; Scholes, C. P. Biochemistry 1998, 37, 6095-6105.
39. Veselov, A. V.; Osborne, J. P.; Gennis, R. B.; Scholes, C. P. J. Am. Chem. Soc. 2000, 122, 8712-8716.
40. Zhao, Y.; Lukoyanov, D. A.; Toropov, Y. V.; Wu, K.; Shapleigh, J. P.; Scholes, C. P. Biochemistry 2002, 41, 7464-7474.
41. Hoffman, B. M.; DeRose, V. J.; Doan, P. E.; Gurbiel, R. J.; Houseman, A. L. P.; Telser, J. In Biological Magnetic Resonance, Vol. 13: EMR of Paramagnetic Molecules; Berliner, L. J., Reuben, J., Eds.; Plenum: New York, 1993; Vol. 13.
42. Werst, M. M.; Davoust, C. E.; Hoffman, B. M. J. Am. Chem. Soc. 1991, 113, 1533-1538.
43. Carrington, A.; McLachlan, A. D. Introduction to Magnetic Resonance with Applications to Chemistry and Chemical Physics; Harper & Row: New York, 1967.
44. Flores, M.; Wajnberg, E.; Bemski, G. Biophys. J. 1997, 73, 3225-3229.
45. Hoffmann, R.; Chen, M. M. L.; Elian, M.; Rossi, A. R.; Mingos, D. M. P. Inorg. Chem. 1974, 13, 2666-2675.
46. Patchkovskii, S.; Ziegler, T. Inorg. Chem. 2000, 39, 5354-5364.
47. Dousmanis, C. Phys. Rev. 1955, 97, 967-970.
48. -3 (Hartree, D. R.; Hartree, W. Proc. R. Soc. London, Ser. A 1949, 193, 299-304.) is the 2s wave function at the nitrogen nucleus, and h is Planck's constant.
49. p = 144.9 MHz.
50. Zhang, Y.; Mao, J.; Godbout, N.; Oldfield, E. J. Am. Chem. Soc. 2002, 124, 13921-13930.
51. Tyryshkin, A. M.; Dikanov, S. A.; Reijerse, E. J.; Burgard, C.; Huettermann, J. Am. Chem. Soc. 1999, 121, 3396-3406.
52. Gilbert, D. C.; Dikanov, S. A.; Doetschman, D. C.; Smeija, J. A. Chem. Phys. Lett. 1999, 315, 43-48.
53. Mulks, C. F.; Scholes, C. P.; Dickinson, L. C.; Lapidot, A. J. Am. Chem. Soc. 1979, 101, 1645-1654.
54. At the extreme high field edge of the EPR line shape (Spectrum 5G) the shoulder (d,d′) emerged, and it is thus plausible that the tensor direction for the lowest g-value has tilt with respect to the heme normal in the FeNO plane. Since there is also evidence for these shoulders (d,d′) from Fe(OEP)-(NO), their existence appears intrinsic to an Fe(heme)(NO) having mesoprotons and is not due to interaction with the protein environment.
55. Hoffman, B. M.; Martinsen, J.; Venters, R. A. J. Magn. Reson. 1984, 59, 110-123.
56. Hoffman, B. M.; Venters, R. A.; Martinsen, J. J. Magn. Reson. 1985, 62, 537-542.
57. Hoffman, B. M.; Gurbiel, R. J. J. Magn. Reson. 1989, 82, 309-317.
58. inter, range two broad proton hyperfine peaks separated by about 1.2 MHz.
59. Walker, F. A. Inorg. Chem. 2003, 42, 4526-4544.
60. 2u (π) orbital, an overlap which, in the case of high and intermediate spin ferric hemes (Cheng, R.-J.; Chen, P.-Y. Chemistry-A European Journal 1999, 5, 1708-1715.
61. Cheng, R.-J.; Chen, P.-Y.; Lovell, T.; Liu, T.; Noodleman, L.; Case, D. A. J. Am. Chem. Soc. 2003, 125, 6774-6783.
62. Walker, F. A. Inorg. Chem. 2003, 42, 4526-4544.
63. Usov, O. M.; Choi, P. S.-T.; Shapleigh, J. P.; Scholes, C. P. J. Am. Chem. Soc. 2005, 127, 9485-9494.), equired iron out-of-planarity. The Fe of NO-Cyt c′ is 0.31 Å out of the average pyrrole nitrogen plane toward the NO ligand
64. (Lawson, D. M.; Stevenson, C. E.; Andrew, C. R.; Eady, R. R. EMBO J. 2000, 19, 5661-5671.); whereas the iron out-of-planarity for ferric Cyt c′ is 0.25 Å
65. (Ramirez, L. M.; Axelrod, H. L.; Herron, S. R.; Rupp, B.; Allen, J. P.; Kantardjieff, K. A. Journal of Chemical Crystallography 2003, 33, 413-424.)
66. 3 = (+)2.07 MHz, values which still show pπ spin density on the mesocarbon and a ∼20% larger anisotropic coupling than predicted by the point dipolar interaction.
67. Mao, J.; Zhang, Y.; Oldfield, E. J. Am. Chem. Soc. 2002, 124, 13911-13920.
68. Andrew, C. R.; Kemper, L. J.; Busche, T. L.; Tiwari, A. M.; Kecskes, M. C.; Stafford, J. M.; Croft, L. C.; Lu, S.; Moenne-Loccoz, P.; Huston, W.; Moir, J. W.; Eady, R. R. Biochemistry 2005, 44, 8664-8672.
69. Marti, M. A.; Capece, L.; Crespo, A.; Doctorovich, F.; Estrin, D. A. J. Am. Chem. Soc. 2005, 127-.
70. George, S. J.; Andrew, C. R.; Lawson, D. M.; Thorneley, R. N.; Eady, R. R. J. Am. Chem. Soc. 2001, 123, 9683-9684.
71. Andrew, C. R.; George, S. J.; Lawson, D. M.; Eady, R. R. Biochemistry 2002, 41, 2353-2360.
72. Andrew, C. R.; Rodgers, K. R.; Eady, R. R. J. Am. Chem. Soc. 2003, 125, 9548-9549.