Anatomy of a red copper center: Spectroscopic identification and reactivity of the copper centers of bacillus subtilis Sco and its Cys-to-ala variants

Journal of the American Chemical Society

Volumn 132, Issue 14, 2010, Pages 5215-5226

  Siluvai, Gnana S ^a   Mayfield, Mary ^a   Nilges, Mark J ^b   Debeer George, Serena ^c   Blackburn, Ninian J ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b Illinois EPR Research Center   (United States)

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOREDUCTION; BACILLUS SUBTILIS; BOND STRENGTH; COPPER BONDS; COPPER CENTERS; COPPER PROTEINS; COPPER-CYSTEINE; COVALENCIES; CU COMPLEXES; CUPREDOXINS; CYS RESIDUES; CYTOCHROME C OXIDASE; EDGE DATA; ELECTRON PARAMAGNETIC RESONANCE; ELECTRON-TRANSFER; EXTENDED X-RAY ABSORPTION FINE STRUCTURES; NITROSOCYANIN; OXYGEN LIGANDS; RESONANCE RAMAN SPECTROSCOPY; SIDE CHAINS; SPECTROSCOPIC IDENTIFICATION; TETRAGONAL ARRAYS; THIOLATES; WILD TYPES;

ABSORPTION; ABSORPTION SPECTROSCOPY; BACTERIOLOGY; LIGANDS; OXYGEN; PARAMAGNETIC RESONANCE; PHOSPHATASES; PROTEINS; RAMAN SPECTROSCOPY; RESONANCE; X RAY ABSORPTION;

COPPER;

ALANINE; AMINO ACID; BACTERIAL PROTEIN; COPPER; COPPER COMPLEX; CUPREDOXIN; CYSTEINE; CYTOCHROME C OXIDASE; EDETIC ACID; LIGAND; NITRITE REDUCTASE; OXYGEN; RED COPPER PROTEIN; SULFUR; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; EXTENDED X RAY ABSORPTION SPECTROSCOPY; METAL BINDING; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; OXIDATION REDUCTION REACTION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN STABILITY; RAMAN SPECTROMETRY; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY; XANES SPECTROSCOPY;

ALANINE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; COPPER; CYSTEINE; GENETIC VARIATION; LIGANDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; SPECTROPHOTOMETRY, ULTRAVIOLET; SPECTRUM ANALYSIS, RAMAN; SULFHYDRYL COMPOUNDS; X-RAY ABSORPTION SPECTROSCOPY;

EID: 77950794316     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja910759v     Document Type: Article

References (62)

1. Gray, H. B., Malmstrom, B. G., and Williams, R. J. J. Biol. Inorg. Chem. 2000, 5, 551-559
2. Holm, R. H., Kennepohl, P., and Solomon, E. I. Chem. Rev. 1996, 96, 2239-2314
3. Andrew, C. R., Yeom, H., Valentine, J. S., Karlsson, B. G., van Pouderoyen, G., Canters, G. W., Loehr, T. M., Sanders-Loehr, J., and Bonander, N. J. Am. Chem. Soc. 1994, 116, 11489-11498
4. Andrew, C. R. and Sanders-Loehr, J. Acc. Chem. Res. 1996, 29, 365-372
5. Basumallick, L., Sarangi, R., DeBeer George, S., Elmore, B., Hooper, A. B., Hedman, B., Hodgson, K. O., and Solomon, E. I. J. Am. Chem. Soc. 2005, 127, 3531-3544
6. LaCroix, L. B., Shadle, S. E., Wang, Y., Averill, B. A., Hedman, B., Hodgson, K. O., and Solomon, E. I. J. Am. Chem. Soc. 1996, 118, 7755-7768
7. Solomon, E. I. Inorg. Chem. 2006, 45, 8012-8025
8. Savelieff, M. G., Wilson, T. D., Elias, Y., Nilges, M. J., Garner, D. K., and Lu, Y. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 7919-7924
9. Shadle, S. E., Penner-Hahn, J. E., Schugar, H. J., Hedman, B., Hodgson, K. O., and Solomon, E. I. J. Am. Chem. Soc. 1993, 115, 767-776
10. Randall, D. W., Gamelin, D. R., LaCroix, L. B., and Solomon, E. I. J. Biol. Inorg. Chem. 2000, 5, 16-29
11. Glaser, T., Hedman, B., Hodgson, K. O., and Solomon, E. I. Acc. Chem. Res. 2000, 33, 859-868
12. Solomon, E. I., Szilagyi, R. K., DeBeer George, S., and Basumallick, L. Chem. Rev. 2004, 104, 419-458
13. Solomon, E. I., Hedman, B., Hodgson, K. O., Dey, A., and Szilagyi, R. K. Coord. Chem. Rev. 2005, 249, 97-129
14. Arciero, D. M., Pierce, B. S., Hendrich, M. P., and Hooper, A. B. Biochemistry 2002, 41, 1703-1709
15. Lieberman, R. L., Arciero, D. M., Hooper, A. B., and Rosenzweig, A. C. Biochemistry 2001, 40, 5674-5681
16. Balatri, E., Banci, L., Bertini, I., Cantini, F., and Ciofi-Baffoni, S. Structure 2003, 11, 1431-1443
17. Banci, L., Bertini, I., Calderone, V., Ciofi-Baffoni, S., Mangani, S., Martinelli, M., Palumaa, P., and Wang, S. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 8595-8600
18. Banci, L., Bertini, I., Ciofi-Baffoni, S., Gerothanassis, I. P., Leontari, I., Martinelli, M., and Wang, S. Structure 2007, 15, 1132-1140
19. Andruzzi, L., Nakano, M., Nilges, M. J., and Blackburn, N. J. J. Am. Chem. Soc. 2005, 127, 16548-16558
20. Horng, Y. C., Leary, S. C., Cobine, P. A., Young, F. B., George, G. N., Shoubridge, E. A., and Winge, D. R. J. Biol. Chem. 2005, 280, 34113-34122
21. Abriata, L. A., Banci, L., Bertini, I., Ciofi-Baffoni, S., Gkazonis, P., Spyroulias, G. A., Vila, A. J., and Wang, S. Nat Chem Biol 2008, 4, 599-601
22. Mattatall, N. R., Jazairi, J., and Hill, B. C. J. Biol. Chem. 2000, 275, 28802-28809
23. Nittis, T., George, G. N., and Winge, D. R. J. Biol. Chem. 2001, 276, 42520-42526
24. Chinenov, Y. V. J. Mol. Med. 2000, 78, 239-242
25. Ye, Q., Imriskova-Sosova, I., Hill, B. C., and Jia, Z. Biochemistry 2005, 44, 2934-2942
26. Williams, J. C., Sue, C., Banting, G. S., Yang, H., Glerum, D. M., Hendrickson, W. A., and Schon, E. A. J. Biol. Chem. 2005, 280, 15202-15211
27. Siluvai, G. S., Nakano, M., Mayfield, M., Nilges, M. J., and Blackburn, N. J. Biochemistry 2009, 48, 12133-12144
28. Blackburn, N. J., Ralle, M., Gomez, E., Hill, M. G., Patsuszyn, A., Sanders, D., and Fee, J. A. Biochemistry 1999, 38, 7075-7084
29. Cutting, S. M. and Youngman, P. Methods for General and Molecular Biology; ASM Press: Washington, DC, 1994.
30. George, G. N.; Stanford Synchrotron Radiation Laboratory: Menlo Park, CA, 1995.
31. George, G. N.; Stanford Synchrotron Radiation Laboratory: Menlo Park, CA, 1990.
32. Binsted, N., Gurman, S. J., and Campbell, J. W.; 9.2 ed.; Daresbury Laboratory: Warrington, England, 1998.
33. Gurman, S. J., Binsted, N., and Ross, I. J. Phys. C 1984, 17, 143-151
34. Gurman, S. J., Binsted, N., and Ross, I. J. Phys. C 1986, 19, 1845-1861
35. Binsted, N. and Hasnain, S. S. J. Synchrotron Rad. 1996, 3, 185-196
36. Blackburn, N. J., Rhames, F. C., Ralle, M., and Jaron, S. J. Biol. Inorg. Chem. 2000, 5, 341-353
37. Nilges, M. J.; Illinois EPR Research Center (IERC), University of Illinois: Urbana-Champaign, 1979.
38. Hedman, B., Frank, P., Gheller, S. F., Roe, A. L., Newton, W. E., and Hodgson, K. O. J. Am. Chem. Soc. 2002, 110, 3798-3805
39. van Amsterdam, I. M., Ubbink, M., van den Bosch, M., Rotsaert, F., Sanders-Loehr, J., and Canters, G. W. J. Biol. Chem. 2002, 277, 44121-44130
40. Han, J., Loehr, T. M., Lu, Y., Valentine, J. S., Averill, B. A., and Sanders-Loehr, J. J. Am. Chem. Soc. 1993, 115, 4256-4263
41. Lu, Y., Roe, J. A., Bender, C. J., Peisach, J., Banci, L., Bertini, I., Gralla, E. B., and Valentine, J. S. Inorg. Chem. 1996, 35, 1692-1700
42. Mandal, S., Das, G., Singh, R., Shukla, R., and Bharadwaj, P. K. Coord. Chem. Rev. 1997, 160, 191-235
43. Cawthorn, T. R., Poulsen, B. E., Davidson, D. E., Andrews, D., and Hill, B. C. Biochemistry 2009, 48, 4448-4454
44. Wang, X., Ang, M. C., and Lu, Y. J. Am. Chem. Soc. 1999, 121, 2947-2948
45. Ralle, M., Lutsenko, S., and Blackburn, N. J. J. Biol. Chem. 2003, 278, 23163-23170
46. Pickering, I. J., George, G. N., Dameron, C. T., Kurz, B., Winge, D. R., and Dance, I. G. J. Am. Chem. Soc. 1993, 115, 9498-9505
47. Kau, L. S., Spira-Solomon, D., Penner-Hahn, J. E., Hodgson, K. O., and Solomon, E. I. J. Am. Chem. Soc. 1987, 109, 6433-6422
48. Himes, R. A., Park, Y. G., Barry, A. N., Blackburn, N. J., and Karlin, K. D. J. Am. Chem. Soc. 2007, 129, 5352-5353
49. Chen, K., Yuldasheva, S., Penner-Hahn, J. E., and OHalloran, T. V. J. Am. Chem. Soc. 2003, 125, 12088-12089
50. Ralle, M., Cooper, M. J., Lutsenko, S., and Blackburn, N. J. J. Am. Chem. Soc. 1998, 120, 13525-13526
51. Pufahl, R. A., Singer, C. P., Peariso, K. L., Lin, S.-J., Schmidt, P. J., Fahrni, C. J., Cizewski Culotta, V., Penner Hahn, J. E., and OHalloran, T. V. Science 1997, 278, 853-856
52. An additional factor which must be taken into consideration when comparing the S-K edge data with results from other spectroscopy is a possible difference induced by measuring the data at different temperatures. Due to experimental considerations the S-K edge data were measured at 4 °C rather than the low temperature (10-110 K) used for EXAFS, EPR and resonance Raman data. Phosphate buffers are known to shift downwards in pH by up to 2 pH units upon freezing to 77 K, due to the insolubility of the dibasic salt at low temperature (see: Williams-Smith, D. L., Bray, R. C., Barber, M. J., Tsopanakis, A. D., and Vincent, S. P. Biochem. J. 1977, 167, 593-600). Therefore we measured the pH dependence of the UV/vis spectrum of the WT BSco from pH 2 to pH 10. Only very minor differences in extinction were observed between pH 7 and pH 2, indicating that the structure of the Cu(II) site remains essentially unchanged over this pH range. A plot of the UV/vis spectrum of BSco vs pH is shown as Supporting Information Figure S8.
53. Han, J., Adman, E. T., Beppu, T., Codd, R., Freeman, H. C., Huq, L., Loehr, T. M., and Sanders-Loehr, J. Biochemistry 1991, 30, 10904-10913
54. Dave, B. C., Germanas, J. P., and Czernuszewicz, R. S. J. Am. Chem. Soc. 1993, 115, 12175-12176
55. den Blaauwen, T., Hoitink, C. W. G., Canters, G. W., Ham, J., Loehr, T. M., and Sanders-Loehr, J. Biochemistry 1993, 32, 12455-12464
56. Anemueller, S., Bill, E., Schaefer, G., Trautwein, A. X., and Teixeira, M. Eur. J. Biochem. 1992, 210, 133-138
57. Blair, D. F., Campbell, D. W., Schoonover, D. R., Chan, S. I., Gray, H. B., Malmstrom, B. G., Pecht, I., Swanson, B. I., Woodruff, W. H., Cho, W. K., English, A. M., Fry, H. A., Lum, V., and Norton, K. A. J. Am. Chem. Soc. 1985, 107, 5755-5766
58. John, E., Bharadwaj, P. K., Potenza, J. A., and Schugar, H. J. Inorg. Chem. 1986, 25, 3065-3069
59. Stibrany, R. T., Fikar, R., Brader, M., Potenza, M. N., Potenza, J. A., and Schugar, H. J. Inorg. Chem. 2002, 41, 5203-5215
60. Penfield, K. W., Gewirth, A. A., and Solomon, E. I. J. Am. Chem. Soc. 1985, 107, 4519-4529
61. Karlsson, B. G., Tsai, L. C., Nar, H., Sanders-Loehr, J., Bonander, N., Langer, V., and Sjolin, L. Biochemistry 1997, 36, 4089-4095
62. Kroes, S. J., Salgado, J., Parigi, G., Luchinat, C., and Canters, G. W. J. Inorg. Biol. Chem. 1996, 1, 551-559