Studies of ferric heme proteins with highly anisotropic/highly axial low spin (S = 1/2) electron paramagnetic resonance signals with bis-histidine and histidine-methionine axial iron coordination

Biopolymers - Peptide Science Section

Volumn 91, Issue 12, 2009, Pages 1064-1082

  Zoppellaro, Giorgio ^a   Bren, Kara L ^b   Ensign, Amy A ^b   Harbitz, Espen ^a   Kaur, Ravinder ^b   Hersleth, Hans Petter ^a   Ryde, Ulf ^c   Hederstedt, Lars ^c   Andersson, K Kristoffer ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITY OF ROCHESTER   (United States)

^c LUND UNIVERSITY   (Sweden)

Author keywords

1H NMR; Cytochrome; DFT calculation; EPR; Ligand field anisotropy

Indexed keywords

AXIAL LIGAND; AXIAL LIGATION; COORDINATION ENVIRONMENT; CYTOCHROME; CYTOCHROME C; DFT CALCULATION; ELECTRON PARAMAGNETIC RESONANCE; ELECTRON-TRANSFER REACTIONS; HEME GROUP; HEME PROTEINS; LIGAND-FIELD; LINEAR CORRELATION; METHYL GROUP; TYPE II;

ANISOTROPY; ELECTRON RESONANCE; ELECTRON SPIN RESONANCE SPECTROSCOPY; FLUORINE CONTAINING POLYMERS; HYDROCARBONS; IRON; LIGANDS; NUCLEAR MAGNETIC RESONANCE; PARAMAGNETIC MATERIALS; PARAMAGNETIC RESONANCE; PARAMAGNETISM; PORPHYRINS; PROBABILITY DENSITY FUNCTION; QUANTUM THEORY; SPIN DYNAMICS; STRONTIUM COMPOUNDS; PHOSPHATASES;

HEMOGLOBIN;

ANION; BACTERIAL PROTEIN; COORDINATION COMPOUND; CYTOCHROME C; FERRIC ION; FERROCHELATASE; FERROUS ION; HEME; HISTIDINE; IRON DERIVATIVE; LIGAND; METHIONINE; METHYL GROUP; MITOCHONDRIAL PROTEIN; POLYPEPTIDE; PROTEIN DERIVATIVE; HEMOPROTEIN; IRON; FERRICHROME;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; ANALYTIC METHOD; ANALYTICAL PARAMETERS; ANISOTROPY; BACTERIAL STRAIN; CHEMICAL REACTION; COVALENT BOND; CRYSTAL STRUCTURE; ELECTROCHEMICAL ANALYSIS; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; EUKARYOTE; HYDROGEN BOND; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MICROBIAL ACTIVITY; NONHUMAN; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN VARIANT; PROTON NUCLEAR MAGNETIC RESONANCE; RESPIRATORY CHAIN; REVIEW; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; ALGORITHM; ANIMAL; CHEMISTRY; METHODOLOGY; OXIDATION REDUCTION REACTION; CORRELATION FUNCTION; PROTEIN ANALYSIS; SIGNAL DETECTION;

ALGORITHMS; ANIMALS; ANISOTROPY; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEMEPROTEINS; HISTIDINE; IRON; METHIONINE; OXIDATION-REDUCTION;

EID: 71749110766     PISSN: 00063525     EISSN: 10970282     Source Type: Journal    
DOI: 10.1002/bip.21267     Document Type: Review

References (120)

1. Bikiel, D. E.; Boechi, L.; Capece, L.; Crespo, A.; De Biase, P. M.; Di Lella, S.; Lebrero, M. C. G.; Marti, M. A.; Nadra, A. D.; Perissinotti, L. L.; Scherlis, D. A.; Estrin, D. A. Phys Chem Chem Phys 2006, 8, 5611-5628.
2. Dolphin, D., Ed. The Porphyrins; Academic Press: London, 1979.
3. Poulos, T. L.; Li, H. Y.; Raman, C. S. Curr Opin Chem Biol 1999, 3, 131-137.
4. Igarashi, N.; Moriyama, H.; Fujiwara, T.; Fukumori, Y.; Tanaka, N. Nat Struct Biol 1997, 4, 276-284.
5. Hersleth, H. P.; Varnier, A.; Harbitz, E.; Rohr, A. K.; Schmidt, P. P.; Sorlie, M.; Cederkvist, F. H.; Marchal, S.; Gorren, A. C. F.; Mayer, B.; Uchida, T.; Schünemann, V.; Kitagawa, T.; Trautwein, A. X.; Shimizu, T.; Lange, R.; Gorbitz, C. H.; Andersson, K. K. Inorg Chim Acta 2008, 361, 831-843.
6. Hersleth, H. P.; Uchida, T.; Rohr, A. K.; Teschner, T.; Schünemann, V.; Kitagawa, T.; Trautwein, A. X.; Gorbitz, C. H.; Andersson, K. K. J Biol Chem 2007, 282, 23372-23386.
7. Hersleth, H. P.; Ryde, U.; Rydberg, P.; Gorbitz, C. H.; Andersson, K. K. J Inorg Biochem 2006, 100, 460-476.
8. Bertini, I.; Gori, G.; Luchinat, C.; Vila, A. J. Biochemistry 1993, 32, 776-783.
9. La Mar, G. N.; Jackson, J. T.; Dugad, L. B.; Cusanovich, M. A.; Bartsch, R. G. J Biol Chem 1990, 265, 16173-16180.
10. Margoliash, E.; Schejter, A. Trends Biochem Sci 1984, 9, 364-367.
11. Keilin, D. Proc R Soc Lond B 1925, 98, 312-339.
12. Sigfridsson, E.; Olsson, M. H. M.; Ryde, U. J Phys Chem B 2001, 105, 5546-5552.
13. Blumberg, W. E.; Peisach J. Adv Chem Ser 1971, 100, 271-291.
14. Allen, J. W. A.; Barker, P. D.; Daltrop, O.; Stevens, J. M.; Tomlinson, E. J.; Sinha, N.; Sambongi, Y.; Ferguson, S. J. Dalton Trans 2005, 21, 3410-3418.
15. Hooper, A. B.; Dispirito, A. A. Microbiol Rev 1985, 49, 140-157.
16. Wood, P. M. FEBS Lett 1983, 164, 223-226.
17. Bowman, S. E. J.; Bren, K. L. Nat Prod Rep 2008, 25, 1118-1130.
18. Berry, E. A.;Walker, F. A. J Biol Inorg Chem 2008, 13, 481-498.
19. Palmer, G. Biochem Soc Trans 1985, 13, 548-560.
20. McGarvey, B. R. Coord Chem Rev 1998, 170, 75-92.
21. Palmer, G. In Physical Methods in Bioinorganic Chemistry; L. Q., Jr., Ed.; University Sciences Books: Sausalito, California, 2000; pp 121-184.
22. Zoppellaro, G.; Harbitz, E.; Kaur, R.; Ensign, A. A.; Bren, K. L.; Andersson, K. K. J Am Chem Soc 2008, 130, 15348-15360.
23. Walker, F. A. Chem Rev 2004, 104, 589-615.
24. Griffith, J. S. Proc R Soc Lond A 1956, 235, 23-36.
25. Taylor, C. P. S. Biochim Biophys Acta 1977, 491, 137-149.
26. Alonso, P. J.; Martinez, J. I.; Garcia-Rubio, I. Coord Chem Rev 2007, 251, 12-24.
27. Walker, F. A.; Huynh, B. H.; Scheidt, W. R.; Osvath, S. R. J Am Chem Soc 1986, 108, 5288-5297.
28. Scheidt, W. R.; Kirner, J. F.; Hoard, J. L.; Reed, C. A. J Am Chem Soc 1987, 109, 1963-1968.
29. Gadsby, P. M. A.; Thomson, A. J. J Am Chem Soc 1990, 112, 5003-5011.
30. Walker, F. A. Coord Chem Rev 1999, 185-186, 471-534.
31. Huynh, B. H.; Emptage, M. H.; Munck, E. Biochim Biophys Acta 1978, 534, 295-306.
32. Zoppellaro, G.; Teschner, T.; Harbitz, E.; Schünemann, V.; Karlsen, S.; Arciero, D. M.; Ciurli, S.; Trautwein, A. X.; Hooper, A. B.; Andersson, K. K. Chem Phys Chem 2006, 7, 1258-1267.
33. Cheesman, M. R.; Greenwood, C.; Thomson, A. J. Adv Inorg Chem 1991, 36, 201-255.
34. Portis, A. M. Phys Rev 1953, 91, 1071-1078.
35. Walker, F. A.; Nasri, H.; TurowskaTyrk, I; Mohanrao, K.; Watson, C. T.; Shokhirev, N. V.; Debrunner, P. G.; Scheidt, W. R. J Am Chem Soc 1996, 118, 12109-12118.
36. Rivera, M.; Caignan, G. A.; Astashkin, A. V.; Raitsimring, A. M.; Shokhireva, T. K.; Walker, F. A. J Am Chem Soc 2002, 124, 6077-6089.
37. Peisach, J.; Blumberg, W. E.; Adler, A. Ann N Y Acad Sci 1973, 206, 310-327.
38. De Vries, S.; Albracht, S. P. J. Biochim Biophys Acta 1979, 546, 334-340.
39. De Vries, S.; Albracht, S. P. J.; Leeuwerik, F. J. Biochim Biophys Acta 1979, 546, 316-333.
40. Salerno, J. C. J Biol Chem 1984, 259, 2331-2336.
41. Paul, M. A.; Gadsby, P. M. A.; Thomson, A. J. FEBS Lett 1986, 197, 253-257.
42. Migita, C. T.; Iwaizumi, M. J Am Chem Soc 1981, 103, 4378-4381.
43. Orme-Johnson, N. R.; Hansen, R. E.; Beinert, H. Biochem Biophys Res Commun 1971, 45, 871-878.
44. Friden, H.; Cheesman, M. R.; Hederstedt, L.; Andersson, K. K.; Thomson, A. J. Biochim Biophys Acta 1990, 1041, 207-215.
45. Hederstedt, L.; Andersson, K. K. J Bacteriol 1986, 167, 735-739.
46. Tsai, A. L.; Palmer, G. Biochem Biophys Acta 1982, 681, 484-495.
47. Tsai, A. L.; Palmer, G. Biochim Biophys Acta 1983, 722, 349-363.
48. Schünemann, V.; Trautwein, A. X.; Illerhaus, J.; Haehnel, W. Biochemistry 1999, 38, 8981-8991.
49. Zatsman, A. I.; Zhang, H. M.; Gunderson, W. A.; Cramer, W. A.; Hendrich, M. P. J Am Chem Soc 2006, 128, 14246-14247.
50. Dou, Y.; Admiraal, S. J.; Ikedasaito, M.; Krzywda, S.; Wilkinson, A. J.; Li, T. S.; Olson, J. S.; Prince, R. C.; Pickering, I. J.; George, G. N. J Biol Chem 1995, 270, 15993-16001.
51. Arciero, D. M.; Hooper, A. B. J Biol Chem 1994, 269, 11878-11886.
52. Arciero, D. M.; Peng, Q. Y.; Peterson, J.; Hooper, A. B. FEBS Lett 1994, 342, 217-220.
53. Harbitz, E., Cand. Scient. Thesis, University of Oslo, Norway, 2003.
54. Brautigan, D. L.; Feinberg, B. A.; Hoffman, B. M.; Margoliash, E.; Peisach, J.; Blumberg,W. E. J Biol Chem 1977, 252, 574-582.
55. Ambler, R. P.; Dalton, H.; Meyer, T. E.; Bartsch, R. G.; Kamen, M. D. Biochem J 1986, 233, 333-337.
56. Hägerhäll, C.; Aasa, R.; von Wachenfeldt, C.; Hederstedt, L. Biochemistry 1992, 31, 7411-7421.
57. Unden, G.; Hackenberg, H.; Kroger, A. Biochim Biophys Acta 1980, 591, 275-288.
58. Crouse, B. R.; Yu, C. A.; Yu, L.; Johnson, M. K. FEBS Lett 1995, 367, 1-4.
59. Yu, L.; Xu, J. X.; Haley, P. E.; Yu, C. A. J Biol Chem 1987, 262, 1137-1143.
60. Kita, K.; Vibat, C. R. T.; Meinhardt, S.; Guest, J. R.; Gennis, R. B. J Biol Chem 1989, 264, 2672-2677.
61. Peterson, J.; Vibat, C.; Gennis, R. B. FEBS Lett 1994, 355, 155-156.
62. Hägerhäll, C. Biochim Biophys Acta 1997, 1320, 107-141.
63. Hederstedt, L. Science 1999, 284, 1941-1942.
64. Hägerhäll, C.; Hederstedt, L. FEBS Lett 1996, 389, 25-31.
65. Bertero, M. G.; Rothery, R. A.; Palak, M.; Hou, C.; Lim, D.; Blasco, F.; Weiner, J. H.; Strynadka, N. C. J. Nat Struct Biol 2003, 10, 681-687.
66. Bertero, M. G.; Rothery, R. A.; Boroumand, N.; Palak, M.; Blasco, F.; Ginet, N.; Weiner, J. H.; Strynadka, N. C. J. J Biol Chem 2005, 280, 14836-14843.
67. Huang, L. S.; Shen, J. T.; Wang, A. C.; Berry, E. A. Biochim Biophys Acta 2005, 1757, 1073-1083.
68. DeLano, W. L. DeLano Scientific, San Carlos, CA, USA, 2002. Available at: http://www.pymol.org.
69. Schirawski, J.; Unden, G. Eur J Biochem 1998, 257, 210-215.
70. Schnorpfeil, M.; Janausch, I. G.; Biel, S.; Kroger, A.; Unden, G. Eur J Biochem 2001, 268, 3069-3074.
71. Matsson, M.; Tolstoy, D.; Aasa, R.; Hederstedt, L. Biochemistry 2000, 39, 8617-8624.
72. Smirnova, I. A.; Hägerhäll, C.; Konstantinov, A. A.; Hederstedt, L. FEBS Lett 1995, 359, 23-26.
73. Hägerhäll, C.; Friden, H.; Aasa, R.; Hederstedt, L. Biochemistry 1995, 34, 11080-11089.
74. Jormakka, M.; Tornroth, S.; Byrne, B.; Iwata, S. Science 2002, 295, 1863-1868.
75. Becke, A. D. Phys Rev A 1988, 38, 3098-3100.
76. Perdew, J. P. Phys Rev B 1986, 33, 8822-8824.
77. Weigend, F.; Ahlrichs, R. Phys Chem Chem Phys 2005, 7, 3297-3305.
78. Ahlrichs, R.; Bär, M.; Häser, M.; Horn, H.; Kölmel, C. Chem Phys Lett 1989, 162, 165-169.
79. Svensson, B.; Andersson, K. K.; Hederstedt, L. Eur J Biochem 1996, 238, 287-295.
80. Mogi, T.; Saiki, K.; Anraku, Y. Mol Microbiol 1994, 14, 391-398.
81. Brown, K. R.; Allan, B. A.; Do, P.; Hegg, E. L. Biochemistry 2002, 41, 10906-10913.
82. Hederstedt, L.; Lewin, A.; Throne-Holst, M. J Bacteriol 2005, 187, 8361-8369.
83. Lewin, A.; Hederstedt, L. FEBS Lett 2006, 580, 5351-5356.
84. Lewin, A.; Hederstedt, L. FEBS Lett 2008, 582, 1330-1334.
85. Orme-Johnson, N. R.; Hansen, R. E.; Beinert, H. J Biol Chem 1974, 249, 1928-1939.
86. Bushnell, G. W.; Louie, G. V.; Brayer, G. D. J Mol Biol 1990, 214, 585-595.
87. Matsuura, Y.; Takano, T.; Dickerson, R. E. J Mol Biol 1982, 156, 389-409.
88. Travaglini-Allocatelli, C.; Gianni, S.; Dubey, V. K.; Borgia, A.; Di Matteo, A.; Bonivento, D.; Cutruzzola, F.; Bren, K. L.; Brunori, M. J Biol Chem 2005, 280, 25729-25734.
89. Benini, S.; Gonzalez, A.; Rypniewski, W. R.; Wilson, K. S.; Van Beeumen, J. J.; Ciurli, S. Biochemistry 2000, 39, 13115-13126.
90. Timkovich, R.; Bergmann, D.; Arciero, D. M.; Hooper, A. B. Biophys J 1998, 75, 1964-1972.
91. Shokhirev, N. V.; Walker, F. A. J Am Chem Soc 1998, 120, 981-990.
92. Banci, L.; Bertini, I.; Luchinat, C.; Pierattelli, R.; Shokhirev, N. V.; Walker, F. A. J Am Chem Soc 1998, 120, 8472-8479.
93. Turner, D. L. Eur J Biochem 1995, 227, 829-837.
94. Turner, D. L. Eur J Biochem 1993, 211, 563-568.
95. Bertini, I.; Luchinat, C.; Parigi, G. Eur J Inorg Chem 2000, 12, 2473-2480.
96. Walker, F. A. Inorg Chem 2003, 42, 4526-4544.
97. Bren, K. L.; Kellogg, J. A.; Kaur, R.; Wen, X. Inorg Chem 2004, 43, 7934-7944.
98. La Mar, G. N.; Satterlee, J. D.; De Ropp, J. S.; Nuclear Magnetic Resonance of Hemoproteins. In: Kadish, K. M.; Smith, K. M.; Guilard, R., Eds; The Porphyrin Handbook. Vol.5. Academic Press: San Diego, CA, 2000, 185-298.
99. Zhong, L. H.; Wen, X.; Rabinowitz, T. M.; Russell, B. S.; Karan, E. F.; Bren, K. L. Proc Natl Acad Sci USA 2004, 101, 8637-8642.
100. Russell, B. S.; Melenkivitz, R.; Bren, K. L. Proc Natl Acad Sci USA 2000, 97, 8312-8317.
101. Wen, X.; Bren, K. L. Inorg Chem 2005, 44, 8587-8593.
102. Bertini, I.; Luchinat, C.; Aime, S. Coord Chem Rev 1996, 150, 1-293.
103. McConnell, H. M.; Robertson, R. E. J Chem Phys 1958, 29, 1361-1365.
104. Kurland, R. J.; McGarvey, B. R. J Mag Res 1970, 2, 286-301.
105. Shokhirev, N. V.; Walker, F. A. J Biol Inorg Chem 1998, 3, 581-594.
106. Senn, H.; Wüthrich, K. Quart Rev Biophys 1985, 18, 111-134.
107. Santos, H.; Turner, D. L. Magn Reson Chem 1993, 31, S90-S95.
108. Karan, E. F.; Russell, B. S.; Bren, K. L. J Biol Inorg Chem 2002, 7, 260-272.
109. Timkovich, R.; Cai, M. L.; Zhang, B. L.; Arciero, D. M.; Hooper, A. B. Eur J Biochem 1994, 226, 159-168.
110. Neese, F. Curr Opin Chem Biol 2003, 7, 125-135.
111. Ye, T.; Kaur, R.; Wen, X.; Bren, K. L.; Elliott, S. J. Inorg Chem 2005, 44, 8999-9006.
112. Battistuzzi, G.; Borsari, M.; Sola, M. Antioxid Redox Signal 2001, 3, 279-291.
113. Benini, S.; Borsari, M.; Ciurli, S.; Dikiy, A.; Lamborghini, M. J Biol Inorg Chem 1998, 3, 371-382.
114. Bertini, I.; Luchinat, C.; Macinai, R.; Martinuzzi, S.; Pierattelli, R.; Viezzoli, M. S. Inorg Chim Acta 1998, 269, 125-134.
115. Cheesman, M. R.; Ferguson, S. J.; Moir, J. W. B.; Richardson, D. J.; Zumft, W. G.; Thomson, A. J. Biochemistry 1997, 36, 16267-16276.
116. van Wonderen, J. H.; Knight, C.; Oganesyan, V. S.; George, S. J.; Zumft, W. G.; Cheesman, M. R. J Biol Chem 2007, 282, 28207-28215.
117. Saraiva, L. M.; Denariaz, G.; Liu, M. Y.; Payne, W. J.; Legall, J.; Moura, I. Eur J Biochem 1992, 204, 1131-1139.
118. Teschner, T.; Yatsunyk, L.; Schünemann, V.; Paulsen, H.; Winkler, H.; Hu, C. J.; Scheidt, W. R.; Walker, F. A.; Trautwein, A. X. J Am Chem Soc 2006, 128, 1379-1389.
119. Geremia, S.; Garau, G.; Vaccari, L.; Sgarra, R.; Viezzoli, M. S.; Calligaris, M.; Randaccio, L. Protein Sci 2002, 11, 6-17.
120. Salemme, F. R. Annu Rev Biochem 1977, 46, 299-329.