Solution NMR characterization of the electronic structure and magnetic properties of high-spin ferrous heme in deoxy myoglobin from Aplysia limacina

Journal of the American Chemical Society

Volumn 125, Issue 28, 2003, Pages 8494-8504

  Ma, Dejian ^a   Musto, Raffaella ^b   Smith, Kevin M ^a,c   La Mar, Gerd N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTRONIC STRUCTURE; MAGNETIC ANISOTROPY; NUCLEAR MAGNETIC RESONANCE; SOLUTIONS; TENSORS;

MOLECULAR ORBITAL;

PROTEINS;

FERROUS DEOXYMYOGLOBIN; HEME; HEMOPROTEIN; MYOGLOBIN; UNCLASSIFIED DRUG;

ANISOTROPY; APLYSIA; ARTICLE; CORRELATION FUNCTION; ELECTROCHEMISTRY; MAGNETISM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROTEIN ANALYSIS; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS;

ANIMALS; APLYSIA; BINDING SITES; DEUTERIUM; FERROUS COMPOUNDS; HEME; ISOTOPE LABELING; MAGNETICS; MYOGLOBIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SOLUTIONS;

EID: 0038713861     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja035256u     Document Type: Article

References (78)

1. La Mar, G. N.; de Ropp, J. S. Biol. Magn. Reson. 1993, 18, 1-79.
2. Bertini, I.; Luchinat, C. Coord. Chem. Rev. 1996, 150, 1-296.
3. Banci, L.; Bertini, I.; Luchinat, C.; Turano, P. In The Porphyrin Handbook; Kadish, K. M., Smith, K. M., Guilard, R., Eds.; Academic Press: Boston, 1999; Vol. 5, pp 323-350.
4. Bertini, I.; Turano, P.; Vila, A. J. Chem. Rev. 1993, 93, 2833-2933.
5. La Mar, G. N.; Satterlee, J. D.; de Ropp, J. S. In The Porphyrins Handbook; Kadish, K. M., Smith, K. M., Guilard, R., Eds.; Academic Press: San Diego, 1999, Vol. 5, pp 185-298.
6. Shulman, R. G.; Glarum, S. H.; Karplus, M. J. Mol. Biol. 1971, 57, 93-115.
7. Traylor, T. G.; Berzinis, A. P. J. Am. Chem. Soc. 1980, 102, 2844-2846.
8. Williams, G.; Moore, G. R.; Porteous, R.; Robinson, M. N.; Soffe, N.; Williams, R. J. P. J. Mol. Biol. 1985, 183, 409-428.
9. Yamamoto, Y.; Nanai, N.; Chujo, R.; Suzuki, T. FEBS Lett. 1990, 264, 113-116.
10. Emerson, S. D.; La Mar, G. N. Biochemistry 1990, 29, 1556-1566.
11. Turner, D. L. Eur. J. Biochem. 1993, 211, 563-568.
12. Brennan, L.; Turner, D. L. Biochim. Biophys. Acta 1997, 1342, 1-12.
13. Banci, L.; Bertini, I.; Luchinat, C.; Pierattelli, R.; Shokhirev, N. V.; Walker, F. A. J. Am. Chem. Soc. 1998, 120, 8472-8479.
14. Louro, R. O.; Correia, I. J.; Brennan, L.; Coutinho, I. B.; Xavier, A. V.; Turner, D. L. J. Am. Chem. Soc. 1998, 120, 13240-13247.
15. Shokhirev, N. V.; Walker, F. A. J. Biol. Inorg. Chem. 1998, 3, 581-594.
16. Turner, D. L. J. Biol. Inorg. Chem. 2000, 5, 328-332.
17. Rajarathnam, K.; La Mar, G. N.; Chiu, M. L.; Sligar, S. G.; Singh, J. P.; Smith, K. M. J. Am. Chem. Soc. 1991, 113. 7886-7892.
18. Banci, L.; Bertini, I.; Turano, P.; Vicens Oliver, M. Eur. J. Biochem. 1992, 204, 107-112.
19. Bertini, I.; Gori, B.; Luchinat, C.; Vila, A. J. Biochemistry 1993, 32 (2), 776-783.
20. Clark, K.; Dugad, L. B.; Bartsch, R. G.; Cusanovich, M. A.; Lamar, G. N. J. Am. Chem. Soc. 1996, 118, 4654-4664.
21. Caffrey, M.; Simorre, J.-P.; Brutscher, B.; Cusanovich, M.; Marion, D. Biochemistry 1995, 34, 5904-5912.
22. Asokan, A.; de Ropp, J. S.; Newmyer, S. L.; Ortiz de Montellano, P. R. J. Am. Chem. Soc. 2001, 123, 4243-4254.
23. Déméné, H.; Tsan, P.; Gans, P.; Marion, D. J. Phys. Chem. B 2000, 104, 2559-2569.
24. Kao, Y.-H.; Lecomte, J. T. J. J. Am. Chem. Soc. 1993, 115, 9754-9762.
25. Antonini, E.; Brunori, M. In Hemoglobin and Myoglobin and Their Reactions with Ligands; Elsevier: North-Holland Publishing: Amsterdam, 1971; pp 40-54.
26. Ho, C.; Perussi, J. R. Methods Enzymol. 1994, 232, 97-138.
27. Moore, G. R.; Pettigrew, G. W. In Cytochromes c, Evolutionary, Structural and Physiochemical Aspects; Rich, A., Ed.; Springer-Verlag: New York, 1990: pp 197-204.
28. Ortiz de Montellano, P. R. Acc. Chem. Res. 1987, 20, 289-294.
29. Ortiz de Montellano, P. R.; Wilks, A. Adv. Inorg. Chem. 2001, 51, 359-407.
30. Williams, G.; Clayden, N. J.; Moore, G. R.; Williams, R. J. P. J. Mol. Biol. 1985, 183, 447-460.
31. Wüthrich, K.; Hochmann, J.; Keller, R. M.; Wagner, G.; Brunori, M.; Giacometti, G. J. Magn. Reson. 1975, 19, 111-117.
32. Emptage, M. H.; Xavier, A. V.; Wood, J. M.; Alsaadi, B. M.; Moore, G. R.; Pitt, R. C.; Williams, R. J. P.; Ambler, R. P.; Bartsch, R. G. Biochemistry 1981, 20, 58-64.
33. La Mar, G. N.; Jackson, J. T.; Bartsch, R. G. J. Am. Chem. Soc. 1981, 103, 4405-4410.
34. La Mar, G. N.; Jackson, J. T.; Dugad, L. B.; Cusanovich, M. A.; Bartsch, R. G. J. Biol. Chem. 1990, 265, 16173-16180.
35. Yamamoto, Y.; Iwafune, K.; Chujo, R.; Inoue, Y.; Imai, K.; Suzuki, T. J. Biochem. Tokyo 1992, 112, 414-420.
36. Banci, L.; Bertini, I.; Turano, P.; Oliver, M. V. Eur. J. Biochem. 1992, 204, 107-112.
37. Banci, L.; Bertini, I.; Marconi, S.; Pierattelli, R. Eur. J. Biochem. 1993, 215, 431-437.
38. La Mar, G. N.; Dalichow, F.; Zhao, X.; Dou, Y.: Ikedo-Saito, M.; Chiu, M. L.; Sligar, S. G. J. Biol. Chem. 1994, 288, 29629-29635.
39. Busse, S. C.; Jue, T. Biochemistry 1994, 33, 10934-10943.
40. Bougault, C. M.; Dou, Y.; Ikeda-Saito, M.; Langry, K. C.: Smith, K. M.; La Mar, G. N. J. Am. Chem. Soc. 1998, 120, 2113-2123.
41. Bertini, I.; Dikiy, A.; Luchinat, C.; Macinai, R.; Viezzoli, M. S. Inorg. Chem. 1998, 37, 4814-4821.
42. Tsan, P.; Caffrey, M.; Daku, M. L.; Cusanovich, M.; Marion, D.; Gans, P. J. Am. Chem. Soc. 1999, 121, 1795-1805.
43. Abbreviations used: Mb, myoglobin; Hb, hemoglobin; NOE, nuclear Overhauser effect; NOESY, two-dimensional nuclear Overhauser spectroscopy; TOCSY, two-dimensional total correlation spectroscopy; DSS, 2,2-dimethyl-2-silapentane-5-sulfonate; MO, molecular orbital.
44. La Mar, G. N.; Anderson, R. R.; Budd, D. L.; Smith, K. M.; Langry, K. C.; Gersonde, K.; Sick, H. Biochemistry 1981, 20, 4429-4436.
45. Kent, T. A.; Spartalian, K.; Lang, G. J. Chem. Phys. 1979, 71, 4899-4908.
46. Winkler, H.; Ding, X.-Q.; Burkardt, M.; Trautwein, A.; Parak, F. Hyperfine Interact. 1994, 71, 875-878.
47. Bolognesi, M.; Onesti, S.; Gatti, G.; Coda, A.; Ascenzi, P.; Giacometti, A.; Brunori, M. J. Mol. Biol. 1989, 205, 529-544.
48. Kuriyan, J.; Wilz, S.; Karplus, M.; Petsko, G. A. J. Mol. Biol. 1986, 192, 133-154.
49. Bolognesi, M.; Coda, A.; Frigero, F.; Gatti, G.; Ascenzi, P.; Brunori, M. J. Mol. Biol. 1989, 205, 529-544.
50. Mattevi, A.; Gaffi, G.; Coda, A.; Rizzi, M.; Ascenzi, P.; Brunori, M.; Bolognesi, M. J. Mol. Recognit. 1991, 4, 1-6.
51. Conti, C.; Moser, C.; Rizzi, M.; Mattevi, A.; Lionetti, C.; Coda, A.; Ascenzi, P.; Brunori, M.; Bolognesi, M. J. Mol. Biol. 1993, 233, 498-508.
52. Cutruzzola, F.; Allocatelli, C. T.; Brancaccio, A.; Brunori, M. Biochem. J. 1996, 314, 83-90.
53. Teale, F. W. J. Biochim. Biophys. Acta 1959, 35, 543.
54. Pande, U.; La Mar, G. N.; Lecomte, J. T. J.; Ascoli, F.; Brunori, M.; Smith, K. M.; Pandey, R. K.; Parish, D. W.; Thanabal, V. Biochemistry 1986, 25, 5638-5646.
55. Banci, L.; Bertini, I.; Luchinat, C. Nuclear and electronic relaxation; VCH: Weinheim, 1991.
56. Gupta, R. K. J. Magn. Reson. 1976, 24, 461-465.
57. Thanabal, V.; de Ropp, J. S.; La Mar, G. N. J. Am. Chem. Soc. 1987, 109, 7516-7525.
58. Jeener, J.; Meier, B. H.; Bachmann, P.; Ernst, R. R. J. Chem. Phys. 1979, 71, 4546-4553.
59. Griesinger, C.; Otting, G.; Wüthrich, K.; Ernst, R. R. J. Am. Chem. Soc. 1988, 110, 7870-7872.
60. Bundi, A.; Wüthrich, K. Biopolymers 1979, 18, 285-297.
61. Wishart, D. S.; Sykes, B. D.; Richards, F. M. J. Mol. Biol. 1991, 222, 311-333.
62. Cross, K. J.; Wright, P. E. J. Magn. Reson. 1985, 64, 220-231.
63. Neuhaus, D.; Williamson, M. The Nuclear Overhauser Effect; VCH Publishers: New York, 1989.
64. Peyton, D. H.; La Mar, G. N.; Pande, U.; Ascoli, F.; Smith, K. M.; Pandey, R. K.; Parish, D. W.; Bolognesi, M.; Brunori, M. Biochemistry 1989, 28, 4880-4887.
65. Nguyen, B. D.; Xia, Z.; Cutruzzolá, F.; Travaglini Allocatelli, C.; Brancaccio, A.; Brunori, M.; La Mar, G. N. J. Biol. Chem. 2000, 275, 742-751.
66. Gueron, M. J. Magn. Reson. 1975, 19, 58-66.
67. Johnson, M. E.; Fung, L. W.-M.; Ho, C. J. Am. Chem. Soc. 1977, 99, 1245-1250.
68. Qin, J.; La Mar, G. N. J. Biomol. NMR 1992, 2, 597-618.
69. La Mar, G. N. In Biological Applications of Magnetic Resonance; Shulman, R. G., Ed.; Academica Press: New York, 1979; pp 305-343.
70. Bolognesi, M.; Coda, A.; Frigerio, F.; Gatti, G.; Ascenzi, P.; Brunori, M. J. Mol. Biol. 1990, 213, 621-625.
71. 2θ - 1), for the majority of residues.
72. Wüthrich, K. NMR of Proteins and Nucleic Acids; Wiley & Sons: New York, 1986.
73. Tahirov, T. H.; Misaki, S.; Meyer, T. E.; Cusanovich, M. A. J. Mol. Biol. 1996, 259, 467-479.
74. La Mar, G. N.; Walker, F. A. In The Porphyrins: Dolphin, D., Ed.; Academic Press: New York, 1978; Vol. IV, pp 61-157.
75. Walker, F. A. In The Porphyrin Handbook; Kadish, K. M., Smith, K. M., Guilard, R., Eds.; Academic Press: Boston, 1999; Vol. 5, pp 81-183.
76. Bertini, I.; Luchinat, C.; Parigi, G.; Walker, F. A. J. Biol. Inorg. Chem. 1999, 4, 515-519.
77. Turner, D. L.; Brennan, L.; Messias, A. C.; Teodoro, M. L.; Xavier, A. V. Euro. Biophys. J. 2000, 29, 104-112.
78. Johansson, M. P.; Sundholm, D.; Gerfen, G.; Wilkström, M. J. Am. Chem. Soc. 2002, 124, 11771-11780.