Multiple wavelength anomalous diffraction (MAD) crystal structure of rusticyanin: A highly oxidizing cupredoxin with extreme acid stability

Journal of Molecular Biology

Volumn 263, Issue 5, 1996, Pages 730-751

  Walter, Richard L ^a,e   Ealick, Steven E ^a   Friedman, Alan M ^b,e   Blake II, Robert C ^c   Proctor, Peter ^d   Shoham, Menachem ^d  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b YALE UNIVERSITY   (United States)

^c XAVIER UNIVERSITY OF LOUISIANA   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

Acid stability; Crystal structure; Cupredoxins; MAD phasing; Rusticyanin; Type 1 copper binding proteins

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; COPPER ION; METALLOPROTEIN; RUSTICYANIN;

ACIDITHIOBACILLUS FERROOXIDANS; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PH; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; STEREOCHEMISTRY; X RAY CRYSTALLOGRAPHY;

ACIDITHIOBACILLUS FERROOXIDANS; BACTERIA (MICROORGANISMS); THIOBACILLUS;

EID: 0030589040     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0612     Document Type: Article

References (82)

1. Adman, E. T. (1991). Copper protein structures. Advan. Protein Chem. 43, 145-197.
2. Adman, E. T., Turley, S., Bramson, R., Petratos, K., Banner, D., Tsernoglou, D., Beppu, T. & Watanabe, H. (1989). A 2.0 Å structure of the blue copper protein (cupredoxin) from Alcaligenes faecalis S-6*. J. Biol. Chem. 264, 87-99.
3. Adman, E. T., Canters, G. W., Hill, H. A. O. & Kitchen, N. A. (1982). The effect of pH and temperature on the structure of the active site of azurin from Pseudomonas aeruginosa. FEBS Letters, 143, 287-292.
4. Bagby, S., Driscoll, P. C., Harvey, T. S. & Hill, H. A. O. (1994). High-resolution solution structure of reduced parsley plastocyanin. Biochemistry, 33, 6611-6622.
5. Baker, E. N. (1988). Structure of azurin from Alcaligenes denitrificans. Refinement at 1.8 Å resolution and comparison of the two crystallographically independent molecules. J. Mol. Biol. 203, 1071-1095.
6. Barrick, D., Hughson, F. M. & Baldwin, R. L. (1994). Molecular mechanisms of acid denaturation: the role of histidine residues in the partial unfolding of apomyoglobin. J. Mol. Biol. 237, 588-601.
7. Bashford, D. & Karplus, M. (1990). pKas of ionizable groups in proteins: atomic detail from a continuum electrostatic model. Biochemistry, 29, 10219-10225.
8. Blake, R. C., II & Shute, E. A. (1987). Respiratory enzymes of Thiobacillus ferrooxidans: a kinetic study of electron transfer between iron and rusticyanin in sulfate media. J. Biol. Chem. 262, 14983-14989.
9. Blake, R. C., II, Shute, E. A., Waskovsky, J. & Harrison, A. P., Jr (1992). Respiratory components in acidophilic bacteria that respire on iron. Geomicrobiol. J. 10, 173-192.
10. Brünger, A. T. (1992a). X-PLOR, Version 3.1, A System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
11. Brünger, A. T. (1992b). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
12. Brünger, A. T., Kuriyan, J. & Karplus, M. (1987). Crystallographic R-factor refinement by molecular dynamics. Science, 235, 458-460.
13. Canters, G. W. & van Pouderoyen, G. (1994). Engineering of electron transfer properties of metallo-proteins. Biosensors Bioelectronics, 9, 637-645.
14. Carson, M. & Bugg, C. E. (1986). Algorithm for ribbon models of proteins. J. Mol. Graph. 4, 121-122.
15. 1H nuclear magnetic resonance spectrum of French bean plastocyanin. J. Mol. Biol. 202, 623-636.
16. Chen, L., Durley, R., Poliks, B. J., Hamada, K., Chen, Z., Mathews, F. S., Davidson, V. L., Satow, Y., Huizinga, E., Vellieux, F. M. D. & Hol, W. G. J. (1992). Crystal structure of an electron-transfer complex between methylamine dehydrogenase and amicyanin. Biochemistry, 31, 4959-4964.
17. 2+ and the preliminary characterization of rusticyanin, a novel 'blue' copper protein. FEBS Letters, 60, 29-33.
18. Collaborative Computational Project, Number 4 (1994). The CCP4 suite: programs for protein crystallography. Acta. Crystallog. sect. D, 50, 760-763.
19. Collyer, C. A., Guss, J. M., Sugimura, Y., Yoshizaki, F. & Freeman, H. C. (1990). Crystal structure of plastocyanin from a green alga, Enteromorpha prolifera. J. Mol. Biol. 211, 617-632.
20. Colman, P. M., Freeman, H. C., Guss, J. M., Murata, M., Norris, V. A., Ramshaw, J. A. M. & Venkatappa, M. P. (1978). X-ray crystal structure analysis of plastocyanin at 2.7 Å resolution. Nature, 272, 319-324.
21. Cowtan, K. (1994). In Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography, 31, 34.
22. Cox, J. C. & Boxer, D. H. (1978). The purification and some properties of rusticyanin, a blue copper protein involved in iron(II) oxidation from Thiobacillus ferro-oxidans. Biochem. J. 174, 497-502.
23. 2+ oxidation at pH 2.0. FEBS Letters, 93, 157-160.
24. Cromer, D. T. (1983). Calculation of anomalous scattering factors at arbitrary wavelengths. J. Appl. Crystallog. 16, 437.
25. Djebli, A., Proctor, P., Blake, R. C., II & Shoham, M. (1992). Crystallization and preliminary X-ray crystallographic studies of rusticyanin from Thiobacillus ferrooxidans. J. Mol. Biol. 227, 581-582.
26. Durley, R., Chen, L., Lim, L. W., Mathews, F. S. & Davidson, V. L. (1993). Crystal structure analysis of amicyanin and apoamicyanin from Paracoccus denitrificans at 2.0 Å and 1.8 Å resolution. Protein Sci. 2, 739-752.
27. Durley, R. C. E., Cunane, L. M., Chen, Z.-W., Tarng, W. & Mathews, F. S. (1995). "Just doing its job": comparison of the oxidized and reduced structures of an electron transfer protein. Abstract W087 from the Annual American Crystallographic Association Meeting in Montreal, Quebec, Canada.
28. Engh, R. A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein-structure refinement. Acta Crystallog. sect. A, 47, 392-400.
29. Fink, A. L., Calciano, L. J., Goto, Y., Kurotsu, T. & Palleros, D. R. (1994). Classification of acid denaturation of proteins: intermediates and unfolded states. Biochemistry, 33, 12504-12511.
30. Friedman, A. M., Fischmann, T. O., Shamoo, Y. & Ealick, S. (1994). MADPRB: A new suite of programs for MAD data analysis incorporating robust estimation, maximum likelihood and Bayesian inference. Abstract TRN07 from the Annual American Crystallographic Association Meeting in Atlanta, Georgia.
31. Gross, E. L. (1993). Plastocyanin: structure and function. Photosynthesis Res. 37, 103-116.
32. Grossmann, J. G., Ingledew, W. J., Harvey, I., Strange, R. W. & Hasnain, S. S. (1995). X-ray absorption studies and homology modeling define the structural features that specify the nature of the copper site in rusticyanin. Biochemistry, 34, 8406-8414.
33. Guss, J. M. & Freeman, H. C. (1983). Structure of oxidized poplar plastocyanin at 1.6 Å resolution. J. Mol. Biol. 169, 521-563.
34. Guss, J. M., Bartunik, H. D. & Freeman, H. C. (1992). Accuracy and precision in protein structure analysis: restrained least-squares refinement of the structure of poplar plastocyanin at 1.33 Å resolution. Acta Crystallog. sect. B, 48, 790-811.
35. I) poplar plastocyanin at six pH values. J. Mol. Biol. 192, 361-387.
36. Guss, J. M., Merritt, E. A., Phizackerley, R. P., Hedman, B., Murata, M., Hodgson, K. O. & Freeman, H. C. (1988). Phase determination by multiple-wavelength X-ray diffraction: Crystal structure of a basic "blue" copper protein from cucumbers. Nature, 272, 806-811.
37. Hemmingsen, J. M., Gernert, K. M., Richardson, J. S. & Richardson, D. C. (1994). The tyrosine corner: a feature of most Greek key β-barrel proteins. Protein Sci. 3, 1927-1937.
38. Hendrickson, W. A. (1985). Analysis of protein structure from diffraction measurements at multiple wavelengths. Trans. Am. Crystallog. Assoc. 21, 11-21.
39. Hendrickson, W. A. (1991). Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science, 254, 51-58.
40. Hendrickson, W. A., Smith, J. L., Phizackerley, R. P. & Merritt, E. A. (1988). Crystallographic structure analysis of lamprey hemoglobin from anomalous dispersion of synchrotron radiation. Proteins, 4, 77-88.
41. Hibino, T., Lee, B. H., Takabe, T. & Takabe, T. (1995). Expression and characterization of Met92Gln mutant plastocyanin from Silene pratensis. J. Biochem. 117, 101-106.
42. 47 for structure and reactivity of azurin from Alcaligenes denitrificans as studied by site-directed mutagenesis and spectroscopy. J. Biol. Chem. 267, 13836-13842.
43. Holt, S. D., Piggott, B., Ingledew, W. J., Feiters, M. C. & Diakun, G. P. (1990). EXAFS of the type-1 copper site of rusticyanin. FEBS Letters, 269, 117-121.
44. 1N resonance assignments and global fold of rusticyanin: insights into the ligation and acid stability of the blue copper site. J. Mol. Biol. 244, 370-384.
45. Ingledew, W. J. & Cobley, J. G. (1980). A potentiometric and kinetic study on the respiratory chain of ferrous-iron-grown Thiobacillus ferrooxidans. Biochim. Biophys. Acta, 590, 141-158.
46. Inoue, T., Shibata, N., Nakanishi, H., Koyama, S., Ishii, H., Kai, Y., Harada, S., Kasai, N., Ohshiro, Yl, Suzuki, S., Kohzuma, T., Yamaguchi, K., Shidara, S. & Iwasaki, H. (1994). Structure of Azurin from Achromobacter xylosoxidans NCIB11015 at 2.5 Å resolution. J. Biochem. 116, 1193-1197.
47. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
48. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
49. Kalverda, A. P., Wymenga, S. S., Lommen, A., van de Ven, F. J. M., Hilbers, C. W. & Canters, G. W. (1994). Solution structure of the Type 1 blue copper protein amicyanin from Thiobacillus versutus. J. Mol. Biol. 240, 358-371.
50. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
51. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26, 283-291.
52. Lee, B. & Richards, F. M. (1971). The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
53. Luzatti, V. (1952). Traitement statistique des erreurs dans la détermination des structures cristallines. Acta Crystallog. 5, 802-810.
54. Malmström, B. G. (1994). Rack-induced bonding in blue-copper proteins. Eur. J. Biochem. 223, 711-718.
55. Moore, G. R., Pettigrew, G. W. & Rogers, N. K. (1986). Factors influencing redox potentials of electron transfer proteins. Proc. Natl Acad. Sci. USA, 83, 4998-4999.
56. Moore, J. M., Case, D. A., Chazin, W. J., Gippert, G. P., Havel, T. F., Powls, R. & Wright, P. E. (1988). Three-dimensional solution structure of plastocyanin from the green alga Scenedesmus obliquus. Science, 240, 314-317.
57. Moratal, M., Romero, A., Salgado, J., Perales-Alarcon, A. & Jimènez, H. R. (1995). The crystal structure of nickel(II)-azurin. Eur. J. Biochem. 228, 653-657.
58. Murphy, L. M., Strange, R. W., Karlsson, B. G., Lundberg, L. G., Pascher, T., Reinhammar, B. & Hasnain, S. S. (1993). Structural characterization of azurin from Pseudomonas aeruginosa and some of its methionine-121 mutants. Biochemistry, 32, 1965-1975.
59. Nar, H., Messerschmidt, A., Huber, R., van de Kamp, M. & Canters, G. (1991a). X-ray crystal structure of the two site-specific mutants His35Gln and His35Leu of azurin from Pseudomonas aeruginosa. J. Mol. Biol. 218, 427-447.
60. Nar, H., Messerschmidt, A., Huber, R., van de Kamp, M. & Canters, G. W. (1991b). Crystal structure analysis of oxidized Pseudomonas aeruginosa azurin at pH 5.5 and pH 9.0. A pH-induced conformational transition involves a peptide bond flip. J. Mol. Biol. 221, 765-772.
61. Nar, H., Messerschmidt, A., Huber, R., van de Kamp, M. & Canters, G. W. (1992). Crystal structure of Pseudomonas aeruginosa apo-azurin at 1.85 Å. FEBS Letters, 306, 119-124.
62. Norris, G. E., Anderson, B. F. & Baker, E. N. (1983). Structure of azurin from Alcaligenes denitrificans at 2.5 Å resolution. J. Mol. Biol. 165, 501-521.
63. Omura, T. (1961). Studies on laccases of lacquer trees. IV. Purification and properties of a blue protein obtained from latex of Rhus vernicifera. J. Biochem. (Tokyo), 50, 394-399.
64. Otwinowski, Z. (1993). In Data Collection and Processing (Sawyer, L., Isaacs, N., Bailey, S., eds), pp. 56-62, SERC Daresbury Laboratory, Warrington, U.K.
65. Petratos, K., Dauter, Z. & Wilson, K. S. (1988). Refinement of the structure of pseudoazurin from Alcaligenes faecalis S-6 at 1.55 Å resolution. Acta Crystallog. sect. B, 44, 628-636.
66. Pronk, J. T. & Johnson, D. B. (1992). Oxidation and reduction of iron by acidophilic bacteria. Geomicrobiol. J. 10, 153-171.
67. Ramachandran, G. N., Ramakrishnan, C. & Sasisekharan, V. (1963). Stereochemistry of polypeptide chain configurations. J. Mol. Biol. 7, 95-99.
68. Redinbo, M. R. & Yeates, T. O. (1993). Structure determination of plastocyanin from a specimen with a hemihedral twinning fraction of one-half. Acta Crystallog. sect. D, 49, 375-380.
69. Redinbo, M. R., Cascio, D., Choukair, M. K., Rice, D., Merchant, S. & Yeates, Y. O. (1993). The 1.5 Å crystal structure of plastocyanin from the green alga Chlamydomonas reinhardtii. Biochemistry, 32, 10560-10567.
70. Rees, D. C. (1985). Electrostatic influence on energetics of electron transfer reactions. Proc. Natl Acad. Sci. USA, 82, 3082-3085.
71. Romero, A., Hoitink, C. W. G., Nar, H., Huber, R., Messerschmidt, A. & Nar, H. (1993). X-ray analysis and spectroscopic characterization of M121Q azurin. J. Mol. Biol. 229, 1007-1021.
72. Romero, A., Nar, H., Huber, R., Messerschmidt, A., Kalverda, A. P., Canters, G. W., Durley, R. & Mathews, F. S. (1994). Crystal structure analysis and refinement at 2.15 Å resolution of amicyanin, a type 1 blue copper protein, from Thiobacillus versutus. J. Mol. Biol. 243, 1196-1211.
73. Sack, J. S. (1987). CHAIN - a crystallographic modeling program. J. Mol. Graph. 6, 224-225.
74. Shepard, W. E. B., Kingston, R. L., Anderson, B. F. & Baker, E. N. (1993). Structure of apo-azurin from Alcaligenes denitrificans at 1.8 Å resolution. Acta Crystallog. sect. D, 49, 331-343.
75. Sjölin, L., Tsai, L.-C., Langer, V., Pascher, T., Karlsson, G., Nordling, M. & Nar, H. (1993). Structure of Pseudomonas aeruginosa zinc-azurin mutant asn47asp at 2.4 Å resolution. Acta Crystallog. sect. D, 49, 449-457.
76. Skyes, A. G. (1991). Active-site properties of the blue copper proteins. Advan. Inorg. Chem. 36, 377-408.
77. Strange, R. W., Reinhammar, B., Murphy, L. M. & Hasnain, S. S. (1995). Structural and spectroscopic studies of the copper site of stelllacyanin. Biochemistry, 34, 220-231.
78. 13C assignments for recombinant Cu(I) rusticyanin: prediction of secondary structure from patterns of chemical shifts. FEBS Letters, 365, 35-41.
79. Tsai, L.-C., Sjölin, L., Langer, V., Pascher, T. & Nar, H. (1995). Structure of the azurin mutant phe114ala from Pseudomonas aeruginosa at 2.6 Å resolution. Acta Crystallog. sect. D, 51, 168-176.
80. Vakoufari, E., Wilson, K. S. & Petratos, K. (1994). The crystal structures of reduced pseudoazurin from Alcaligenes faecalis S-6 at two pH values. FEBS Letters, 347, 203-206.
81. Wilmot, C. M. & Thornton, J. M. (1988). Analysis and prediction of the different types of β-turn in proteins. J. Mol. Biol. 203, 221-232.
82. Yang, A.-S., Honig, B. (1993). On the pH dependence of protein stability. J. Mol. Biol. 231, 459-474.