Spectroscopic characterization of the tungsten and iron centers in aldehyde ferredoxin oxidoreductases from two hyperthermophilic archaea

Journal of the American Chemical Society

Volumn 118, Issue 49, 1996, Pages 12391-12504

  Koehler, Brian P ^a   Mukund, Swarnalatha ^a,b   Conover, Richard C ^a,c   Dhawan, Ish K ^a   Roy, Roopali ^a   Adams, Michael W W ^a   Johnson, Michael K ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b Recombinant BioCatalysis Inc   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDOREDUCTASE;

ARCHAEBACTERIUM; ARTICLE; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; THERMOPHILIC BACTERIUM; X RAY CRYSTALLOGRAPHY;

EID: 0030458581     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja962197u     Document Type: Article

References (96)

1. For recent reviews, see: (a) Molybdenum Enzymes, Cofactors. and Model Systems; Stiefel, E. I., Coucouvanis, D., Newton, W. E., Eds.; ACS Symposium Series, Vol. 535; American Chemical Society: Washington, DC, 1993. (b) Young, C. G.; Wedd, A. G. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 5, pp 2330-2346. (c) Enemark, J. H.; Young, C. G. Adv. Inorg. Chem. 1993, 40, 1-88. (d) Hille, R. Biochim. Biophys. Acta 1994, 1184, 143-169.
2. For recent reviews, see: (a) Molybdenum Enzymes, Cofactors. and Model Systems; Stiefel, E. I., Coucouvanis, D., Newton, W. E., Eds.; ACS Symposium Series, Vol. 535; American Chemical Society: Washington, DC, 1993. (b) Young, C. G.; Wedd, A. G. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 5, pp 2330-2346. (c) Enemark, J. H.; Young, C. G. Adv. Inorg. Chem. 1993, 40, 1-88. (d) Hille, R. Biochim. Biophys. Acta 1994, 1184, 143-169.
3. For recent reviews, see: (a) Molybdenum Enzymes, Cofactors. and Model Systems; Stiefel, E. I., Coucouvanis, D., Newton, W. E., Eds.; ACS Symposium Series, Vol. 535; American Chemical Society: Washington, DC, 1993. (b) Young, C. G.; Wedd, A. G. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 5, pp 2330-2346. (c) Enemark, J. H.; Young, C. G. Adv. Inorg. Chem. 1993, 40, 1-88. (d) Hille, R. Biochim. Biophys. Acta 1994, 1184, 143-169.
4. For recent reviews, see: (a) Molybdenum Enzymes, Cofactors. and Model Systems; Stiefel, E. I., Coucouvanis, D., Newton, W. E., Eds.; ACS Symposium Series, Vol. 535; American Chemical Society: Washington, DC, 1993. (b) Young, C. G.; Wedd, A. G. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 5, pp 2330-2346. (c) Enemark, J. H.; Young, C. G. Adv. Inorg. Chem. 1993, 40, 1-88. (d) Hille, R. Biochim. Biophys. Acta 1994, 1184, 143-169.
5. Johnson, J. L.; Rajagopalan, K. V. J. Biol. Chem. 1976, 251, 5505-5511.
6. May, H. D.; Patel, P. S.; Ferry, J. G. J. Bacterial. 1988, 170, 3384-3389.
7. The term pterin cofactor rather than molybdopterin is used throughout for the modified pterin that coordinates Mo or W in oxotransferases via the dithiolene group in the third ring. This avoids the need to refer to the "tungsten-molybdopterin" active site which is confusing and misleading.
8. For recent reviews, see: (a) Adams, M. W. W. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 4, pp 4284-4291. (b) Adams, M. W. W.; Kietzin, A. FEMS Microbiol. Rev. 1996, 18, 5-63. (c) Johnson, M. K.; Rees, D. C.; Adams, M. W. W. Chem. Rev. 1996, in press.
9. For recent reviews, see: (a) Adams, M. W. W. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 4, pp 4284-4291. (b) Adams, M. W. W.; Kietzin, A. FEMS Microbiol. Rev. 1996, 18, 5-63. (c) Johnson, M. K.; Rees, D. C.; Adams, M. W. W. Chem. Rev. 1996, in press.
10. For recent reviews, see: (a) Adams, M. W. W. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 4, pp 4284-4291. (b) Adams, M. W. W.; Kietzin, A. FEMS Microbiol. Rev. 1996, 18, 5-63. (c) Johnson, M. K.; Rees, D. C.; Adams, M. W. W. Chem. Rev. 1996, in press.
11. Chan, M. K.; Mukund, S.; Kletzin, A.; Adams, M. W. W.; Rees, D. C. Science 1995, 267, 1463-1469.
12. (a) Rajagopalan, K. V. Adv. Enzymol. Relat. Areas Mol. Biol. 1991, 64, 215-290.
13. (b) Rajagopalan, K. V.; Johnson, J. L. J. Biol. Chem. 1992, 267, 10199-10202.
14. Romao, M. J.; Archer, M.; Moura, I.; Moura, J. J. G.; LeGall, J.; Engh, R.; Schneider, M.; Hof, P.; Huber, R. Science 1995, 270, 1170-1176.
15. Schindelin, H.; Kisker, C.; Hilton, J.; Rajagopalan, K. V.; Rees, D. C. Science 1996, 272, 1615-1621.
16. Mukund, S.; Adams, M. W. W. J. Biol. Chem. 1990, 265, 11508-11516.
17. George, G. N.; Prince, R. C.; Mukund, S.; Adams, M. W. W. J. Am. Chem. Soc. 1992, 114, 3521-3523.
18. Mukund, S.; Adams, M. W. W. J. Biol. Chem. 1991, 266, 14208-14216.
19. George, G. N.; Mukund, S.; Roy, R.; Adams, M. W. W. Manuscript in preparation.
20. (a) Johnson, J. L.; Rajagopalan, K. V.; Mukund, S.; Adams, M. W. W. J. Biol. Chem. 1993, 268, 4848-4852.
21. (b) Mukund, S. Ph.D. Dissertation, University of Georgia, 1995.
22. (a) Johnson, M. K.; Robinson, A. E.; Thomson, A. J. In Iron-Sulfur Proteins; Spiro, T. G., Ed.; Wiley: New York, 1982; pp 367-407.
23. (b) Fu, W.; Drozdzewski, P. M.; Davies, M. D.; Sligar, S. G.; Johnson, M. K. J. Biol. Chem. 1992, 267, 15502-15510.
24. (c) Conover, R. C.; Kowal, A. T.; Fu, W.; Park, J.-B.; Aono, S.; Adams, M. W. W.; Johnson, M. K. J. Biol. Chem. 1990, 205, 8533-8541.
25. (d) Onate, Y. A.; Finnegan, M. G.; Hales, B. J.; Johnson, M. K. Biochim. Biophys. Acta 1993, 1164, 113-123.
26. (e) Finnegan, M. G.; Conover, R. C.; Park, J.-B.; Zhou, Z. H.; Adams, M. W. W.; Johnson, M. K. Inorg. Chem. 1995, 5358-5369.
27. (a) Finnegan, M. G.; Hilton, J.; Rajagopalan, K. V.; Johnson, M. K. Inorg. Chem. 1993, 32, 2616-2617.
28. (b) Benson, N.; Farrar, J. A.; McEwan, A. G.; Thomson, A. J. FEBS Lett. 1992, 307, 169-172.
29. (c) Peterson, J.; Godfrey, C.; Thomson, A. J.; George, G. N.; Bray, R. C. Biochem. J. 1986, 233, 107-110.
30. (a) Johnson, M. K. In Metal Clusters in Proteins; Que, L., Jr., Ed.; ACS Symposium Series, Vol. 372; American Chemical Society: Washington, DC, 1988; pp 326-342.
31. (b) Thomson, A. J.; Cheeseman, M. R.; George, S. J. Methods Enzymol. 1993, 226, 199-232.
32. (a) Belford, R. L.; Nilges, M. J. Computer Simulation of Powder Spectra. EPR Symposium, 21st Rocky Mountain Conference, Denver, CO, 1979.
33. (b) Nilges, M. J. Ph.D. Dissertation, University of Illinois, Urbana, IL, 1979.
34. (a) Hagen, W. R. Biochim. Biophys. Acta 1982, 708, 82-98.
35. (b) Hendrich, M. P.; Debrunner, P. G. J. Magn. Reson. 1988, 78, 133-141.
36. (c) Hendrich, M. P.; Debrunner, P. G. Biophys. J. 1989, 56, 489-506.
37. (a) Thomson, A. J.; Johnson, M. K. Biochem. J. 1980, 191, 411-420.
38. (b) Bennett, D. E.; Johnson, M. K. Biochim. Biophys. Acta 1987, 911, 71-80.
39. (a) Hagen, W. R.; Dunham, W. R.; Johnson, M. K.; Fee, J. A. Biochim. Biophys. Acta 1985, 828, 369-374.
40. (b) Werth, M. T.; Kurtz, D. M., Jr.; Howes, B. D.; Huynh, B. H. Inorg. Chem. 1989, 28, 1357-1361.
41. (c) Werth, M. T.; Johnson, M. K. Biochemistry 1989, 28, 3982-3988.
42. Hendrich, M. P.; Pearce, L. L.; Que, L., Jr.; Chasteen, N. D.; Day, E. P. J. Am. Chem. Soc. 1991, 113, 3039-3044.
43. Hendrich, M. P.; Münck, E.; Fox, B. G.; Lipscomb, J. D. J. Am. Chem. Soc. 1990, 112, 5861-5865.
44. Elgren, T. E.; Hendrich, M. P.; Que, L., Jr. J. Am. Chem. Soc. 1993, 115, 9291-9292.
45. (a) Borovik, A. S.; Hendrich, M. P.; Holman, T. R.; Münck, E.; Papaefthymiou, V.; Que, L., Jr. J. Am. Chem. Soc. 1990, 112, 6031-6038.
46. (b) Jang, H. G.; Hendrich, M. P.; Que, L., Jr. Inorg. Chem. 1993, 32, 911-919.
47. (a) Nordlund, P.; Eklund, H. Curr. Opin. Struct. Biol. 1995, 5, 758-766.
48. (b) Kurtz, D. M., Jr. In Encyclopedia of Inorganic Chemistry; King, R. B., Ed.; Wiley: U.K., 1994; Vol. 4, pp 1847-1859.
49. (a) Lindahl, P. A.; Day, E. P.; Kent, T. A.; Orme-Johnson, W. H.; Münck, E. J. Biol. Chem. 1985, 260, 11160-11173.
50. (b) Zambrano, I. C.; Kowal, A. T.; Mortenson, L. E.; Adams, M. W. W.; Johnson, M. K. J. Biol. Chem. 1989, 264, 20974-20983.
51. (c) Onate, Y. A.; Vollmer, S. J.; Switzer, R. L.; Johnson, M. K. J. Biol. Chem. 1989, 264, 18386-18391.
52. (d) Flint, D. H.; Emptage, M. H.; Finnegan, M. G.; Fu, W.; Johnson, M. K. J. Biol. Chem. 1993, 268, 14732-14742.
53. (e) George, S. J.; Armstrong, F. A.; Hatchikian, E. C.; Thomson, A. J. Biochem. J. 1989, 264, 275-284.
54. (f) Flint, D. H.; Emptage, M. H.; Guest, J. R. Biochemistry 1992, 31, 10331-10337.
55. (g) Kowal, A. T.; Werth, M. T.; Manodori, A.; Cecchini, Schröder, I.; Gunsalus, R. P.; Johnson, M. K. Biochemistry 1995, 34, 12284-12293.
56. (a) Carney, M. J.; Papaefthymiou, G. C.; Spartalian, K.; Frankel, R. B.; Holm, R.H. J. Am. Chem. Soc. 1988, 110, 6084-6095.
57. (b) Carney, M. J.; Papaefthymiou, G. C.; Whitener, M. A.; Spartalian, K.; Frankel, R. B.; Holm, R. H. Inorg. Chem. 1988, 27, 346-352.
58. (c) Carney, M. J.; Papaefthymiou, G. C.; Frankel, R. B.; Holm, R. H. Inorg. Chem. 1989, 28, 1497-1503.
59. Nelson, M. J.; Levy, M. A.; Orme-Johnson, W. H. Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 147-150.
60. (a) Holm, R. H.; Simhon, E. D. In Molybdenum Enzymes; Spiro, T. G., Ed.; John Wiley and Sons: New York, 1985; pp 1-87.
61. (b) Carney, M. J.; Kovacs, J. A.; Zhang, Y.-P.; Papaefthymiou, G. C.; Spartalian, K.; Frankel, R. B.; Holm, R. H. Inorg. Chem. 1987, 26, 719-724.
62. Meyer, J.; Gaillard, J.; Moulis, J.-M. Biochemistry 1988, 27, 6150-6156.
63. Calzolai, L.; Gorst, C. M.; Zhao, Z.-H.; Teng, Q.; Adams, M. W. W.; LaMar, G. N. Biochemistry 1995, 34, 11373-11384.
64. Hanson, G. R.; Brunette, A. A.; McDonell, A. C.; Murray, K. S.; Wedd, A. G. J. Am. Chem. Soc. 1981, 103, 1953-1959.
65. Oku, H.; Ueyama, N.; Nakamura, A. Chem. Lett. 1995, 621-622.
66. Ellis, S. R.; Collison, D.; Garner, C. D.; Clegg, W. J. Chem. Soc., Chem. Commun. 1986, 1483-1485.
67. Das, S. K.; Chaudhury, P. K.; Biswas, D.; Sarkar, S. J. Am. Chem. Soc. 1994, 116, 9061-9070.
68. W(V) species formed in situ by oxidation of W(IV) complex with 12. Oku, H.; Ueyama, N.; Nakamura, A.; Johnson, M. K. Unpublished results.
69. Dhawan, I. K.; Enemark, J. H. Inorg. Chem. 1996, 35, 4873-4882.
70. Deaton, J. C.; Solomon, E. I.; Watt, G. D.; Wetherbee, P. J.; Durfor, C. N. Biochem. Biophys. Res. Commun. 1987, 149, 424-430.
71. Schmitz, R. A.; Albracht, S. P. J.; Thauer, R. K. FEBS Lett. 1992, 309, 78-81.
72. Huber, C.; Caldeira, J.; Jongejan, J. A.; Simon, H. Arch. Microbiol. 1994, 162, 303-309.
73. Hensgens, C. M. H.; Hagen, W. R.; Hansen, T. A. J. Bacterial. 1995, 177, 6195-6200.
74. Kon, H.; Sharpless, N. E. J. Phys. Chem. 1966, 70, 105-111.
75. Carducci, M. D.; Brown, C.; Solomon, E. I.; Enemark, J. H. J. Am. Chem. Soc. 1994, 116, 11856-11868.
76. Bennett, B.; Benson, N.; McEwan, A. G.; Bray, R. C. Biochem. J. 1994, 255, 321-331.
77. George, G. N.; Hilton, J.; Rajagopalan, K. V. J. Am. Chem. Soc. 1996, 118, 1113-1117.
78. (a) Ueyama, N.; Oku, H.; Nakamura, A. J. Am. Chem. Soc. 1992, 114, 7310-7311.
79. (b) Das, S. K.; Biswas, D.; Maiti, R.; Sarkar, S. J. Am. Chem. Soc. 1996, 118, 1387-1397.
80. Xiao, Z.; Gable, R. W.; Wedd, A. G.; Young, C. G. J. Am. Chem. Soc. 1996, 118, 2912-2921 and references therein.
81. Mukund, S.; Koehler, B. P.; Roy, R.; Adams, M. W. W.; Johnson, M. K. Unpublished observations.
82. Garrett, R. M.; Rajagopalan, K. V. J. Biol. Chem. 1996, 271, 7387-7391.
83. (a) George, G. N.; Kipke, C. A.; Prince, R. C.; Sunde, R. A.; Enemark, J. H.; Cramer, S. P. Biochemistry 1989, 28, 5075-5080.
84. (b) George, G. N.; Garrett, R. M.; Prince, R. C.; Rajagopalan, K. V. J. Am. Chem. Soc. 1996, 36, 8586-8592.
85. Hilton, J. C.; Rajagopalan, K. V. Arch. Biochem. 1996, 325, 139-143.
86. Oku, H., Koehler, B. P.; Ueyama, N.; Nakamura, A.; Johnson, M. K. Manuscript in preparation.
87. (a) Pan, W.-H.; Harmer, M. A.; Halbert, T. R.; Stiefel, E. I. J. Am. Chem. Soc. 1984, 106, 459-460.
88. (b) Draganjac, M.; Simhon, E.; Chan, L. T.; Kanatzidis, M.; Baenziger, N. C.; Coucouvanis, D. Inorg. Chem. 1982, 21, 3321-3326.
89. Kletzin, A.; Mukund, S.; Kelley-Crouse, T. L.; Chan, M. K.; Rees, D. C.; Adams, M. W. W. J. Bacterial. 1995, 117, 4817-4829.
90. (a) Mukund, S.; Adams, M. W. W. J. Biol. Chem. 1993, 268, 13592-13600.
91. (b) Johnson, J. L.; Rajagopalan, K. V.; Mukund, S.; Adams, M. W. W. J. Biol. Chem. 1993, 268, 4848-4852.
92. (a) Cramer, S. P.; Liu, C.-L.; Mortenson, L. E.; Spence, J. T.; Liu, S.-M.; Yamamoto, I.; Ljungdahl, L. G. J. Inorg. Biochem. 1985, 23, 119-124.
93. (b) Yamamoto, I.; Saiki, T., Liu, S.-M.; Ljungdahl, L. G. J. Biol. Chem. 1983, 258, 1826-1832.
94. (c) Deaton, J. C.; Solomon, E. I.; Watt, G. D.; Wetherbee, P. J.; Durfor, C. N. Biochem. Biophys. Res. Commun. 1987, 149, 424-430.
95. (a) Schmitz, R. A.; Albracht, S. P. J.; Thauer, R. K. FEBS Lett. 1992, 309, 78-81.
96. (b) Hochheimer, A.; Schmitz, R. A.; Thauer, R. K.; Hedderich, R. Eur. J. Biochem. 1995, 234, 910-920.