A multinuclear ENDOR study of the C-cluster in CO dehydrogenase from Clostridium thermoaceticum: Evidence for H(x)O and histidine coordination to the [Fe4S4] center

Journal of the American Chemical Society

Volumn 120, Issue 34, 1998, Pages 8767-8776

  DeRose, Victoria J ^a   Telser, Joshua ^b,c   Anderson, Mark E ^a   Lindahl, Paul A ^a   Hoffman, Brian M ^b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c ROOSEVELT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE DEHYDROGENASE; FERRIC ION; HISTIDINE; LIGAND;

ARTICLE; CATALYSIS; CHEMICAL STRUCTURE; CLOSTRIDIUM; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; ENZYME ANALYSIS; MOLECULAR INTERACTION; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN BINDING; REACTION ANALYSIS;

EID: 0032475404     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja9731480     Document Type: Article

References (79)

1. m, moderately coupled proton(s); rf, radio frequency; fwhm, full-width at half-maximum height.
2. Bonam, D.; Ludden, P. W. J. Biol. Chem. 1987, 262, 2980-2987.
3. Kerby, R. L.; Hong, S. S.; Ensign, S. A.; Coppoc, L. J.; Ludden, P. W.; Roberts, G. P. J. Bacteriol. 1992, 174, 5284-5294 .
4. Ragsdale, S. W.; Kumar, M. Chem. Rev. 1996, 96, 2515-2539.
5. Hu, Z.; Spangler, N. J.; Anderson, M. E.; Xia, J.; Ludden, P. W.; Lindahl, P. A.; Münck, E. J. Am. Chem. Soc. 1996, 118, 830-845.
6. Anderson, M. E.; Lindahl, P. A. Biochemistry 1994, 33, 8702-8711.
7. Anderson, M. E.; DeRose, V. J.; Huffman, B. M.; Lindahl, P. A. J. Inorg. Biochem. 1993, 51, Abstract B149.
8. Anderson, M. A.; DeRose, V. J.; Hoffman, B. M.; Lindahl, P. A. J. Am. Chem. Soc. 1993, 115, 12204-12205.
9. Kumar, M.; Lu, W.-P.; Liu, L.; Ragsdale, S. W. J. Am. Chem. Soc. 1993, 115, 11646-11647.
10. The C-cluster also has been investigated by resonance Raman spectroscopy (ref 11), but these papers recently have been retracted (ref 12) and so are not discussed here.
11. (a) Qiu, D.; Kumar, M.; Ragsdale, S. W.; Spiro, T. G. J. Am. Chem. Soc. 1995, 117, 2653-2654.
12. (b) Qiu, D.; Kumar, M.; Ragsdale, S. W.; Spiro, T. G. J. Am. Chem. Soc. 1996, 118, 10429-10435.
13. J. Am. Chem. Soc. 1997, 119, 11134.
14. red1 state.
15. (b) Beinert, H.; Kennedy, M. C.; Stout, C. D. Chem. Rev. 1996, 96, 2335-2373.
16. (c) Ciurli, S.; Carrié, M.; Weigel, J. A.; Carney, M. J.; Stack, T. D. P.; Papaefthymiou, G. C.; Holm, R. H. J. Am. Chem. Soc. 1990, 112, 2654-2664.
17. (a) Ensign, S. A.; Bonam, D.; Ludden, P. W. Biochemistry 1989, 28, 4968-4973.
18. (b) Ensign, S. A.; Campbell, M. J.; Ludden, P. W. Biochemistry 1990, 29, 2162-2168.
19. Spangler, N. J.; Lindahl, P. A.; Bandarian, V.; Ludden, P. W. J. Biol. Chem. 1996, 271, 7973-7977.
20. Lindahl, P. A.; Ragsdale, S. W.; Münck, E. J. Biol. Chem. 1990, 265, 3880-3888.
21. Lindahl, P, A.; Münck, E.; Ragsdale, S. W. J. Biol. Chem. 1990, 265, 3873-3879.
22. Tan, G. O.; Ensign, S. A.; Ciurli, S.; Scott, M. J.; Hedman, B.; Holm, R. H.; Ludden, P. W.; Korszun, Z. R.; Stephens, P. J.; Hodgson, K. O. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 4427-4431.
23. Anderson, M. E.; Lindahl, P. A. Biochemistry 1996, 35, 8371-8380.
24. m′ = -530 mV) and so was rejected by Anderson and Lindahl (ref 19).
25. Seravalli, J.; Kumar, M.; Lu, W.-P.; Ragsdale, S. W. Biochemistry 1995, 34, 7879-7888.
26. Kumar, M.; Lu, W.-P.; Smith, A.; Ragsdale, S. W.; McCracken, J. J. Am. Chem. Soc. 1995, 117, 2939-2944.
27. Hoffman, B. M.; DeRose, V. J.; Doan, P. E.; Gurbiel, R. J.; Houseman, A. L. P.; Telser, J. In EMR of Paramagnetic Molecules; Biological Magnetic Resonance 13; Berliner, L. J., Reuben, J., Eds.; Plenum Press: New York, 1993; pp 151-218.
28. DeRose, V. J.; Hoffman, B. M. In Methods in Enzymology; Sauer, K., Ed.; Academic Press: New York, 1995; Vol. 246, pp 554-589.
29. Telser, J.; Smith, E. T.; Adams, M. W. W.; Conover, R. C.; Johnson, M. K.; Hoffman, B. M. J. Am. Chem. Soc. 1995, 117, 5133-5140.
30. Lowe, D. J. Prog. Biophys. Mol. Biol. 1992, 57, 1-22.
31. Fan, C.; Gorst, C. M.; Ragsdale, S. W.; Hoffman, B. M. Biochemistry 1991, 30, 431-435.
32. (a) Lundie, L. L.; Drake, H. L. J. Bacteriol 1984, 159, 700-703.
33. (b) Ragsdale, S. W.; Wood, H. G. J. Biol. Chem. 1985, 260, 3970-3977.
34. (c) Raybuck, S. A.; Bastian, N. R.; Orme-Johnson, W. H.; Walsh, C. T. Biochemistry 1988, 27, 7698-7702.
35. (d) Ramer, S. E.; Raybuck, S. A.; Orme-Johnson, W. H.; Walsh, C. T. Biochemistry 1989, 28, 4675-4680.
36. Shin, W.; Lindahl, P. A. Biochemistry 1992, 31, 12870-12875.
37. Pelley, J. W.; Garner, C. W.; Little, G. H. Anal. Biochem. 1978, 86, 341-343.
38. Glasoe, P. K.; Long, F. A. J. Phys. Chem. 1960, 64, 188-190.
39. Werst, M. M.; Kennedy, M. C.; Beinert, H.; Huffman, B. M. Biochemistry 1990, 29, 10526-10532.
40. DeRose, V. J.; Liu, K. E.; Lippard, S. J.; Huffman, B. M. J. Am. Chem. Soc. 1996, 118, 121-134.
41. Hoffman, B. M.; DeRose, V. J.; Ong, J.-L.; Davoust, C. E. J. Magn. Reson. Ser. A 1994, 110, 52-57.
42. Mims, W. B. Proc. R. Soc. London 1965, 283, 452-457.
43. Davoust, C. E.; Doan, P. E.; Hoffman, B. M. J. Magn. Reson. 1996, 119, 38-44.
44. In many reported X-band EPR spectra, temperature and power variations have been used to separate the CODH EPR signals on the basis of their different relaxation properties. Under the low-temperature rapid-passage conditions used in this study, all of the species present contribute to the absorption-like EPR envelope. ENDOR spectra at any field value would be the sum of features due to each contributing species in the EPR spectrum.
45. m, (data not shown),
46. (b) Willems, J.-P.; Lee, H.-I.; Burdi, D.; Doan, P. E.; Stubbe, J.; Hoffman, B. M. J. Am. Chem. Soc. 1997, 119, 9816-9824.
47. (c) Doan, P. E.; Hoffman, B. M. Chem. Phys. Lett. 1997, 269, 208-214.
48. (a) Doan, P. E.; Fan, C.; Hoffman, B. M. J. Am. Chem. Soc. 1994, 116, 1033-1041.
49. (b) Mouesca, J.-M.; Rius, G.; Lamotte, B. J. Am. Chem. Soc. 1993, 115, 4714-4731.
50. Fan, C.; Teixeira, M.; Moura, J.; Moura, I.; Huynh, B.-H.; Le Gall, J.; Peck, H. D., Jr.; Huffman, B. M. J. Am. Chem. Soc. 1991, 113, 20-24.
51. Fann, Y.-C.; Gerber, N. C.; Osmulski, P. A.; Hager, L. P.; Sligar, S. G., Hoffman, B. M. J. Am. Chem. Soc. 1994, 116, 5989-5990.
52. Mouesca, J.-M.; Noodleman, L.; Case, D. A.; Lamotte, B. Inorg. Chem. 1995, 34, 4347-4359.
53. i = 0.99≈1.
54. s. (a) Mulks, C. F.; Scholes, C. P.; Dickinson, L. C.; Lapidot, A. J. Am. Chem. Soc. 1979, 101, 1645-1653. (b) LoBrutto, R.; Scholes, C. P.; Wagner, G. C.; Gunsalus, I. C.; Debrunner, P. G. J. Am. Chem. Soc. 1980, 102, 1167-1170.
55. s. (a) Mulks, C. F.; Scholes, C. P.; Dickinson, L. C.; Lapidot, A. J. Am. Chem. Soc. 1979, 101, 1645-1653. (b) LoBrutto, R.; Scholes, C. P.; Wagner, G. C.; Gunsalus, I. C.; Debrunner, P. G. J. Am. Chem. Soc. 1980, 102, 1167-1170.
56. 1H) = 16 MHz, which is larger than the previously reported value of 8 MHz (ref 32).
57. 14N in the two states.
58. (b) Ashby, C. I. H.; Cheng, C. P.; Brown, T. L. J. Am. Chem. Soc. 1978, 100, 6057-6067.
59. Gurbiel, R. J.; Batie, C. J.; Sivaraja, M.; True, A. E.; Fee, J. A.; Hoffman, B. M.; Ballou, D. P. Biochemistry 1989, 28, 4861-4871.
60. Gurbiel, R. J.; Doan, P. E.; Gassner, G. T.; Macke, T. J.; Case, D. A.; Ohnishi, T.; Fee, J. A.; Ballou, D. P.; Huffman, B. M. Biochemistry 1996, 35, 7834-7845.
61. Houseman, A. L. P.; Oh, B.-H.; Kennedy, M. C.; Fan, C.; Werst, M. M.; Beinert, H.; Markley, J. L.; Hoffman, B. M. Biochemistry 1992, 31, 2073-2080.
62. Adman, E.; Watenpaugh, K. D.; Jensen, L. H. Proc. Natl. Acad. Sci. U.S.A. 1975, 72, 4854-4848.
63. 14N Δm = ±2 "double quantum" transitions previously observed by Q-band ENDOR for other Fe-S centers that lack direct nitrogen ligands (ref 49).
64. Volbeda, A.; Charon, M.-H.; Piras, C.; Hatchikian, E. C.; Frey, M.; Fontecilla-Camps, J. C. Nature 1995, 373, 580-587.
65. Telser, J.; Benecky, M. J.; Adams, M. W. W.; Mortenson, L. E.; Hoffman, B. M. J. Biol. Chem. 1986, 261, 13536-13541.
66. Telser, J.; Benecky, M. J.; Adams, M. W. W.; Mortenson, L. E.; Hoffman, B. M. J. Biol. Chem. 1987, 262, 6589-6594.
67. (a) Pollock, R. C.; Lee, H.-I.; Cameron, L. M.; DeRose, V. J.; Hales, B. J.; Orme-Johnson, W. H.; Hoffman, B. M. J. Am. Chem. Soc. 1995, 117, 8686-8687.
68. (b) Lee, H.-I.; Cameron, L. M.; Hales, B. J.; Hoffman, B. M. J. Am. Chem. Soc. 1997, 119, 10121-10126.
69. Trumpower, B. L.; Gennis, R. B. Annu. Rev. Biochem. 1994, 675-716.
70. Roberts, L. M.; Lindahl, P. A. J. Am. Chem. Soc. 1995, 117, 2565-2572.
71. Teixeira, M.; Moura, I.; Xavier, A. V.; Moura, J. J.; LeGall, J.; DerVartanian, D. V.; Peck, H. D., Jr.; Huynh, B. H. J. Biol. Chem. 1989, 264, 16435-16450.
72. 4 center of the C-cluster. Bridging two metals seems less likely for hydroxide that is involved in catalysis as a nucleophile, but it is possible that the status of the bridging ligand changes, for example by CO binding, during catalysis.
73. Macgregor, S. A.; Lu, Z.; Eisenstein, O.; Crabtree, R. H. Inorg. Chem. 1994, 33, 3616-18.
74. Mt. Their conclusion was based on a previous study in which preparations of the isolated αε dimer (called the Ni/Fe-S component) exhibited the NiFeC EPR signal of CO-reduced A-cluster (ref 61c). However, the quantified NiFeC signal intensity in their samples was only ∼1/6 that exhibited by the intact complex, raising the possibility that their samples contained a small amount of intact complex and that it was this complex that gave rise to the signal.
75. (b) Maupin-Furlow, J. A.; Ferry, J. G. J. Bacteriol. 1996, 178, 6849-6856.
76. (c) Lu, W.-P.; Jablonski, P. E.; Rasche, M.; Ferry, J. G.; Ragsdale, S. W. J. Biol. Chem. 1994, 269, 9736-9742.
77. 2: while the other bound one of the oxygen atoms. This arrangement dramatically enhanced the rate of catalysis relative to the corresponding mononuclear complex.
78. (b) Steffey, B. D.; Curtis, C. J.; DuBois, D. L. Organometallics 1995, 14, 4937-4943.
79. Ensign, S. A.; Hyman, M. R.; Ludden, P. W. Biochemistry 1989, 28, 4973-4979.