How cytochromes with different folds control heme redox potentials

Biochemistry

Volumn 42, Issue 33, 2003, Pages 9829-9840

  Mao, Junjun ^a   Hauser, Karin ^a   Gunner, M R ^a  

^a CITY COLLEGE OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROMES;

COMPLEXATION; ELECTROSTATICS; FREE ENERGY; OXIDATION; PEROXIDES; PH EFFECTS; PROTEINS; STRUCTURE (COMPOSITION);

ELECTROCHEMISTRY;

GLOBIN; HEME; PEROXIDASE; PROPIONIC ACID;

ARTICLE; CALCULATION; CORRELATION ANALYSIS; ELECTROCHEMISTRY; ENERGY; ENZYME ACTIVITY; ENZYME CONFORMATION; EQUILIBRIUM CONSTANT; OXIDATION REDUCTION REACTION; PH; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN MOTIF; PROTON TRANSPORT; REACTION ANALYSIS; SOLVATION; STRUCTURE ANALYSIS; THERMODYNAMICS;

BACTERIA; CYTOCHROMES; ELECTROCHEMISTRY; GLOBINS; HEME; MODELS, MOLECULAR; OXIDATION-REDUCTION; PROTEIN FOLDING; THERMODYNAMICS;

EID: 0041972670     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi027288k     Document Type: Article

References (142)

1. Pettigrew, G. W., and Moore, G. R. (1987) Cytochromes c: Biological Aspects, Springer-Verlag, Berlin.
2. Moore, G. R., and Pettigrew, G. W. (1990) Cytochromes c: Evolutionary, Structural and Physiochemical Aspects, Springer-Verlag, Berlin.
3. Martin, A. C. R., Orengo, C. A., Hutchinson, E. G., Jones, S., Karmirantzou, M., Laskowski, R. A., Mitchell, J. B. O., Taroni, C., and Thornton, J. M. (1998) Structure 6, 875-884.
4. Lemberg, R., and Barrett, J. (1973) Cytochromes, Academic Press, London.
5. Cusanovich, M. A., Meyer, T. E., and Tollin, G. (1988) Heme Proteins 7, 37-91.
6. Moore, G. R. (1996) in Protein Electron Transfer (Bendall, D. S., Ed.) pp 189-216, Bios, Cambridge.
7. Churg, A. K., Weiss, R. M., Warshel, A., and Takano, T. (1983) J. Phys. Chem. 87, 1683-1694.
8. Gunner, M. R., and Honig, B. (1991) Proc. Natl. Acad. Sci. U.S.A. 88, 9151-9155.
9. Rabenstein, B., Ullmann, G. M., and Knapp, E. W. (1998) Biochemistry 57, 2488-2495.
10. Rabenstein, B., Ullmann, G. M., and Knapp, E. W. (2000) Biochemistry 39, 10487-96.
11. Alexov, E., and Gunner, M. (1999) Biochemistry 38, 8253-8270.
12. Stephens, P. J., Jollie, D. R., and Warshel, A. (1996) Chem. Rev. 96, 2491-2513.
13. Eidsness, M. K., Burden, A. E., Richie, K. A., Kurtz, D. M., Jr., Scott, R. A. S., E. T., Ichiye, T., Beard, B., Min, T., and Kang, C. (1999) Biochemistry 38, 14803-14809.
14. Ullmann, G. M., Noodleman, L., and Case, D. A. (2002) J. Biol. Inorg. Chem. 7, 632-639.
15. Noodleman, L., Lovell, T., Liu, T., Himo, F., and Torres, R. A. (2002) Cur. Opin. Struct. Biol. 6, 259-273.
16. Simonson, T. (2001) Curr. Opin. Struct. Biol. 11, 243-252.
17. Cutler, R. L., Davies, A. M., Creighton, S., Warshel, A., Moore, G. R., Smith, M., and Mauk, A. G. (1989) Biochemistry 28, 3188-3197.
18. Sham, Y. Y., Chu, Z. T., Tao, H., and Warshel, A. (2000) Proteins 39, 393-407.
19. Simonson, T. (1998) J. Am. Chem. Soc. 120, 4873-4878.
20. Soares, C. M., Martel, P. J., Mendes, J., and Carrondo, M. A. (1998) Biophys. J. 74, 1708-1721.
21. Olsson, M. H., Hong, G., and Warshel, A. (2003) J. Am. Chem. Soc. 125, 5025-5039.
22. Friesner, R. A., and Dunietz, B. D. (2001) Acc. Chem. Res 34, 351-358.
23. Gunner, M. R., Saleh, M., Cross, E., ud-Doula, A., and Wise, M. (2000) Biophys. J. 78, 1126-1144.
24. Muegge, I., Qi, P. X., Wand, A. J. W., Chu, Z. T., and Warshel, A. (1997) J. Phys. Chem. 101, 825-836.
25. Simonson, T. (2002) Proc. Natl. Acad. Sci. U.S.A. 99, 6544-6549.
26. Warshel, A. (1981) Biochemistry 20, 3167.
27. Bashford, D., and Karplus, M. (1991) J. Phys. Chem. 95, 9556-9561.
28. Yang, A.-S., Gunner, M. R., Sampogna, R., Sharp, K., and Honig, B. (1993) Proteins 15, 252-265.
29. Antosiewicz, J., McCammon, J. A., and Gilson, M. K. (1996) Biochemistry 35, 7819-7833.
30. Alexov, E. G., and Gunner, M. R. (1997) Biophys. J. 72, 2075-2093.
31. Mehler, E. L., and Guarnieri, F. (1999) Biophys. J. 77, 3-22.
32. Schutz, C. N., and Warshel, A. (2001) Proteins 44, 400-417.
33. Georgescu, R. E., Alexov, E. G., and Gunner, M. R. (2002) Biophys J. 83, 1731-1748.
34. Warshel, A., and Russell, S. T. (1984) Q. Rev. Biophys. 17, 283-422.
35. Warshel, A., and Churg, A. K. (1983) J. Mol. Biol 168, 687-694.
36. Churg, A. K., and Warshel, A. (1986) Biochemistry 25, 1675-1681.
37. Warwicker, J. (1986) J. Theor. Biol 121, 199-210.
38. Honig, B., and Nicholls, A. (1995) Science 268, 1144-1149.
39. Warshel, A., and Papazyan, A. (1998) Curr. Opin. Struct. Biol. 8, 211-217.
40. Mauk, A. G., and Moore, G. R. (1997) J. Biol. Inorg. Chem. 2, 119-125.
41. Springs, S. L., Bass, S. E., McLendon, G. L. (2000) Biochemistry 39, 6075-6082.
42. Springs, S. L., Bass, S. E., Bowman, G., Nodelman, I., Schutt, C. E., and McLendon, G. L. (2002) Biochemistry 47, 4321-4328.
43. Bertini, I., Gori-Savellini, G., and Luchinat, C. (1997) J. Biol. Inorg. Chem. 2, 109-113.
44. Battistuzzi, G., Borsari, M., and Sola, M. (2001) Antioxid. Redox Signal 3, 279-91.
45. Battistuzzi, G., Borsari, M., Cowan, J. A., Ranieri, A., and Sola, M. (2002) J. Am. Chem. Soc. 124, 5315-5324.
46. Zhou, H. X. (1997) J. Biol. Inorg. Chem. 2, 109-113.
47. Gunner, M. R., Alexov, E., Torres, E., and Lipovaca, S. (1997) J. Biol. Inorg. Chem. 2, 126-134.
48. Warshel, A., Papazyan, A., and Muegge, I. (1997) J. Biol. Inorg. Chem. 2, 143-152.
49. Baptista, A. M., Martel, P. J., and Peterson, S. B. (1997) Proteins: Struct., Funct., Genet. 27, 523-544.
50. Baptista, A., Martel, P. J., and Soares, C. M. (1999) Biophys. J. 76, 2978-2998.
51. Martel, P. J., Soares, C. M., Baptista, A. M., Fuxreiter, M., Naray-Szabo, G., Louro, R. O., and Carrondo, M. A. (1999) J. Biol. Inorg. Chem. 4, 73-86.
52. Zaric, S. D., Popovic, D. M., and Knapp, E. W. (2001) Biochemistry 40, 7914-7928.
53. Kassner, R. J. (1972) Proc. Natl. Acad. Sci. U.S.A. 69, 2263-2267.
54. Kassner, R. J. (1973) J. Am. Chem. Soc. 95, 2674-2676.
55. Warwicker, J., and Watson, H. C. (1982) J. Mol. Biol. 157, 671-679.
56. Rogers, N. K., Moore, G. R., and Sternberg, M. J. (1985) J. Mol. Biol. 182, 613-616.
57. Rogers, N. K., and Moore, G. R. (1988) FEBS Lett. 228, 69-73.
58. Ullmann, G. M. (2000) J. Phys. Chem. B 104, 6923-6301.
59. Teixeira, V. H., Soares, C. M., and Baptista, A. M. (2002) J. Biol. Inorg. Chem. 7, 200-216.
60. Rau, H. K., DeJonge, N., and Haehnel, W. (1998) Proc. Natl. Acad. Sci. U.S.A. 95, 11526-11531.
61. Gunner, M. R., and Alexov, E. (2000) Biochim. Biophys. Acta 1458, 63-87.
62. Antosiewicz, J., McCammon, J. A., and Gilson, M. K. (1994) J. Mol. Biol. 238, 415-436.
63. You, T. J., and Bashford, D. (1995) Biophys. J. 69, 1721-1733.
64. Beroza, P., and Case, D. (1996) J. Phys. Chem. 100, 20156-20163.
65. Nielsen, J. E., Anderson, K. V., Honig, B., Hooft, R. W. W., Klebe, G., Vriend, G., and Wade, R. C. (1999) Prot. Eng. 12, 657-662.
66. Sham, Y. Y., Muegge, I., and Warshel, A. (1998) Biophys. J. 74, 1744-1753.
67. Sham, Y. Y., Chu, Z. T., and Warshel, A. (1997) J. Phys. Chem. B 101, 4458-4472.
68. Sridharan, S., Nicholls, A., and Honig, B. (1992) Biophys. J. 61, A174.
69. Bharadwaj, R., Windemuth, A., Sridharan, S., Honig, B., and Nicholls, A. (1995) J. Comput. Chem. 16, 898-913.
70. Gu, Z., Ridenoor, C. F., Bronnimann, C. E., Iwashita, T., and McDermott, A. (1996) J. Am. Chem. Soc. 118, 822-829.
71. Nicholls, A., and Honig, B. (1991) J. Comput. Chem. 12, 435-445.
72. Sitkoff, D., Sharp, K. A., and Honig, B. (1994) J. Phys. Chem. 98, 1978-1988.
73. Kashiwagi, H., and Obara, S. (1981) Int. J. Quantum Chem. 20, 843-59.
74. Harbury, H. A., and Loach, P. A. (1960) J. Biol. Chem. 255, 3640-3645.
75. Harbury, H. A., and Loach, P. A. (1960) J. Biol. Chem. 235, 3646-3653.
76. Wilson, G. S. (1974) Bioelectrochem. Bioenerg. 1, 172-179.
77. Adams, P. A., Baldwin, D. A., and Marques, H. M. (1996) in Cytochrome c (Scott, R. A., and Mauk, A. G., Eds.) pp 635-692, University Science Books, Sausalito, CA.
78. Tezcan, F. A., Winkler, J. R., and Gray, H. B. (1998) J. Am. Chem. Soc. 120, 13383-13388.
79. Harbury, H. A., Cronin, J. R., Fanger, M. W., Hettinger, T. P., Murphy, A. J., Meyer, Y. P., and Vinogradov, S. N. (1965) Proc. Natl. Acad. Sci. U.S.A. 54, 1658-1664.
80. Wallace, C. J. A., and Clark-Lewis, I. (1992) J. Biol. Chem. 1992, 3852-3861.
81. Raphael, A. L., and Gray, H. B. (1989) Proteins 6, 338-340.
82. Miller, G. T., Zhang, B., Hardman, J. K., and Timkovich, R. (2000) Biochemistry 39, 9010-9017.
83. Wu, J., Gan, J. H., Xia, Z. X., Wang, Y. H., Wang, W. H., Xue, L. L., Xie, Y., and Huang, Z. X. (2000) Proteins 40, 249-57.
84. Durley, R. C. E., and Mathews, F. S. (1996) Acta Crystallogr., Sect. D: Biol. Crystallogr. 52, 65.
85. Xue, L., Wang, Y., Xie, Y., Yao, P., Wang, W., Qian, W., and Huang, Z. (1999) Biochemistry 38, 11961-11972.
86. Lide, D. R. (1990) CRC Handbook of Chemistry and Physics, CRC Press, Boca Raton, FL.
87. Cramer, W. A., and Knaff, D. B. (1991) Energy Transduction in Biological Membranes: A Textbook of Bioenergetics, Springer-Verlag, New York.
88. Das, D. K., and Medhi, O. K. (1998) J. Inorg. Biochem. 70, 83-90.
89. Barker, P. D., Butler, J., Oliveira, P., Hill, H. A., and Hunt, N. I. (1996) Inorg. Chim. Acta 252, 71-77.
90. Moore, G. R., Williams, R. J. P., Peterson, J., Thomson, A. J., and Mathews, S. (1985) Biochim. Biophys. Acta 829, 83-96.
91. Moore, G. R., Pettigrew, G. W., Pitt, R. C., and Williams, R. J. P. (1980) Biochim. Biophys. Acta 590, 261-271.
92. Marcus, R. A., and Sutin, N. (1985) Biochim. Biophys. Acta 811, 265-322.
93. Langen, R., Brayer, G. D., Berghuis, A. M., McLendon, G., Sherman, F., and Warshel, A. (1992) J. Mol. Biol. 224, 589-600.
94. Sharp, A. S. (1998) Biophys. J. 73, 1241-1250.
95. Parson, W. W., Chu, Z. T., and Warshel, A. (1998) Biophys. J. 74, 182-91.
96. Wirtz, M., Oganesyan, V., Zhang, X., Studer, J., and Rivera, M. (2000) Faraday Discuss. 116, 221-34.
97. Meyer, T. E., Watkins, J. A., Przysiecki, C. T., Tollin, G., and Cusanovich, M. A. (1984) Biochemistry 23, 4761-4767.
98. Meyer, T. E., and Kamen, M. D. (1982) Adv. Prot. Chem. 35, 105-212.
99. Northup, S. H. (1996) in Protein Electron Transfer (Bendall, D. S., Ed.) pp 69-98, Bios, Cambridge.
100. Benini, S., Borsari, M., Ciurli, S., Dikiy, A., and Lamborghinin, M. (1998) J. Biol. Inorg. Chem. 3, 371-382.
101. Rivera, M., Seetharaman, R., Girdhar, D., Wirtz, M., Zhang, X., Wang, X., and White, S. (1998) Biochemistry 37, 1485-1494.
102. Meyer, T. E., Cheddar, G., Bartsch, R. G., Getzoff, E. D., Cusanovich, M. A., and Tollin, G. (1986) Biochemistry 25, 1383-1390.
103. Yamaanka, T. (1992) Group c Cytochromes, Japan Scientific Societies Press, Tokoyo.
104. Maroti, P., and Wraight, C. A. (1988) Biochim. Biophys. Acta 934, 329-347.
105. Garcia, A. E., and Hummer, G. (1999) Proteins 36, 175-191.
106. Schlereth, D. D., and Mantele, W. (1993) Biochemistry 32, 1118-1126.
107. Berghuis, A. M., Guillemette, J. G., McLendon, G., Sherman, F., Smith, M., and Brayer, G. D. (1994) J. Mol. Biol. 236, 786-799.
108. Safo, M. K., Nesset, M. J. M., Walker, F. A., Debrunner, P. G., and Scheidt, W. R. (1997) J. Am. Chem. Soc. 117, 9438-9448.
109. Sarma, S., Dangi, B., Yan, C., DiGate, R. J., Banville, D. L., and Guiles, R. D. (1997) Biochemistry 36, 5645-5657.
110. Obrien, P., and Sweigart, D. A. (1985) Inorg. Chem. 24, 1405-1409.
111. Kassner, R. J. (1991) Biochim. Biophys. Acta 1058, 8-12.
112. Nesset, M. J. M., Shokhirev, N. V., Enemark, P. D., Jacobson, S. E., and Walker, F. A. (1996) Inorg. Chem. 35, 5188-5200.
113. Ubbink, M., Campos, A. P., Teixeira, M., Hunt, N. I., Hill, H. A. O., and Canters, G. W. (1994) Biochemistry 33, 10051-10059.
114. Kadish, K. M., and Bottomley, L. A. (1980) J. Inorg. Chem. 19, 832-836.
115. Stellwagen, E. (1978) Nature 275, 73-74.
116. Fantuzzi, A., Sadeghi, S., Valentti, F., Rossi, G. L., and Gilardi, G. (2002) Biochemistry 41, 8718-8724.
117. Weyermann, P., and Diederich, F. (2002) Helv. Chima. Acta 85, 571-597.
118. Smith, H. T., Staudenmayer, N., and Millett, F. (1977) Biochemistry 16, 4977-4974.
119. Rees, D. C. (1980) J. Mol. Biol. 141, 323-326.
120. Tiede, D. M., Vashishta, A.-C., and Gunner, M. R. (1993) Biochemistry 32, 4515-4531.
121. Lo, T. P., Komar-Panicucci, S. Sherman, F., McLendon, G., and Brayer, G. D. (1995) Biochemistry 34, 5259-5268.
122. Kannt, A., Pfitzner, U., Ruitenberg, M., Hellwig, P., Ludwig, B., Mantele, W., Fendler, K., and Michel, H. (1999) J. Biol. Chem. 274, 37974-81.
123. Langen, R., Braver, G. D., Berghuis, A. M., McLendon, G., Sherman, F., and Warshel, A. (1992) J. mol. Biol. 224, 589-600.
124. Saraiva, L. M., Salgueiro, C. A., da Costa, P. N., Messias, A. C., LeGall, J., van Dongen, W. M., and Xavier, A. V. (1998) Biochemistry 37, 12160-5.
125. Wang, Z. Q., Wang, Y. H., Wang, W. H., Xue, L. L., Wu, X. Z., Xie, Y., and Huang, Z. X. (2000) Biophys Chem 83, 3-17.
126. Cesareni, G., Spiedel, D., Jones, M. R., and Robert, B. (2002) FEBS Lett. 527, 171-175.
127. Schlarb-Ridley, B. G., Bendall, D. S., and Howe, C. J. (2002) Biochemistry 41, 3279-85.
128. Alexov, E., Miksovska, J., Baciou, L., Schiffer, M., Hanson, D., Sebban, P., and Gunner, M. R. (2000) Biochemistry 39, 5940-5952.
129. Springs, S. L., Mao, J., Hauser, K., Gunner, M. R., and McLendon, G. Proc. Natl. Acad. Sci. U.S.A., submitted.
130. Sarma, S., DiGate, R. J., Goodin, D. B., Miller, C. J., and Guiles, R. D. (1997) Biochemistry 36, 5658-5668.
131. Gong, X. S., Wen, J. Q., and Gray, J. C. (2000) Eur. J. Biochem. 267, 1732-42.
132. Zhao, D., Hutton, H. M., Gooley, P. R., MacKenzie, N. E., and Cusanovich, M. A. (2000) Protein Sci. 9, 1828-37.
133. Harrenga, A., Reincke, B., Ruterians, H., Ludwig, B., and Michel, H. (2000) J. Mol. Biol. 295, 667-78.
134. Iverson, T. M., Arciero, D. M., Hooper, A. B., and Rees, D. C. (2001) J. Biol. Inorg. Chem. 6, 390-7.
135. Banci, L., Bertini, I., Ferroni, F., and Rosato, A. (1997) Eur. J. Biochem. 249, 270-9.
136. Amesano, F.,Banci, L., Bertini, I., Felli, I. C. (1998) Biochemistry 37, 173-184.
137. Martinez, S. E., Huang, D., Ponomarev, M., Cramer, W. A., and Smith, J. L. (1996) Protein Sci. 5, 1081-1092.
138. Ponamarev, M. V., and Cramer, W. A. (1998) Biochemistry 37, 17199-208.
139. Sainz, G., Carrell, C. J., Ponamarev, M. V., Soriano, G. M., Cramer, W. A., and Smith, J. L. (2000) Biochemistry 39, 9164-9175.
140. Arnesano, F., Banci, L., Bertini, I., Faraone-Mennella, J., Rosato, A., Barker, P. D., and Fersht, A. R. (1999) Biochemistry 38, 865-770.
141. Behr, J., Hellwig, P., Mantele, W., and Michel, H. (1998) Biochemistry 37, 7400-7406.
142. Cai, M., and Timkovich, R. (1992) FEBS Lett. 311, 213-6.