Structural dynamics of myoglobin: FTIR-TDS study of NO migration and binding

Biochemistry

Volumn 47, Issue 3, 2008, Pages 935-948

  Nienhaus, Karin ^a   Palladino, Pasquale ^a   Nienhaus, G Ulrich ^a,b  

^a UNIVERSITY OF ULM   (Germany)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CRYOGENICS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; LIGANDS; MOLECULAR DYNAMICS; NITROGEN OXIDES; PHOTOLYSIS;

CRYOGENIC TEMPERATURES; FOURIER TRANSFORM INFRARED PHOTOLYSIS DIFFERENCE SPECTROSCOPY; LIGAND INTERACTIONS;

PROTEINS;

FERRIC ION; FERROUS ION; HEME; HISTIDINE; LIGAND; MYOGLOBIN; NITRIC OXIDE; XENON;

ARTICLE; BINDING SITE; DISSOCIATION; ILLUMINATION; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PHOTOCHEMISTRY; PHOTOLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTEIN VARIANT;

AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CARBON MONOXIDE; COLD; DARKNESS; ELECTROSTATICS; HISTIDINE; HYDROGEN-ION CONCENTRATION; IRON; LASERS; LIGHT; MYOGLOBIN; NITRIC OXIDE; OXIDATION-REDUCTION; PHOTOCHEMISTRY; PHOTOLYSIS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPERM WHALE; THERMODYNAMICS; WATER;

EID: 38549113981     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701935v     Document Type: Article

References (96)

1. Kim, S., Deinum, G., Gardner, M. T., Marletta, M. A., and Babcock, G. T. (1996) Distal Pocket Polarity in the Unusual Ligand Binding Site of Soluble Guanylate Cyclase: Implications for the Control of NO Binding, J. Am. Chem. Soc. 118, 8769-8770.
2. Boon, E. M., Huang, S. H., and Marletta, M. A. (2005) A molecular basis for NO selectivity in soluble guanylate cyclase, Nat. Chem. Biol. 1, 53-59.
3. Beltran, B., Mathur, A., Duchen, M. R., Erusalimsky, J. D., and Moncada, S. (2000) The effect of nitric oxide on cell respiration: A key to understanding its role in cell survival or death, Proc. Natl. Acad. Sci. U.S.A. 97, 14602-14607.
4. Gross, S. S., and Lane, P. (1999) Physiological reactions of nitric oxide and hemoglobin: a radical rethink, Proc. Natl. Acad. Sci. U.S.A. 96, 9967-9969.
5. Garry, D. J., Meeson, A., Yan, Z., and Williams, R. S. (2000) Life without myoglobin, Cell Mol. Life Sci. 57, 896-898.
6. Flögel, U., Merx, M. W., Gödecke, A., Decking, U. K., and Schrader, J. (2001) Myoglobin: A scavenger of bioactive NO, Proc. Natl. Acad. Sci. U.S.A. 98, 735-740.
7. Brunori, M. (2001) Nitric oxide moves myoglobin centre stage, Trends Biochem. Sci. 26, 209-210.
8. Eich, R. F., Li, T., Lemon, D. D., Doherty, D. H., Curry, S. R., Aitken, J. F., Mathews, A. J., Johnson, K. A., Smith, R. D., Phillips, G. N., Jr., and Olson, J. S. (1996) Mechanism of NO-induced oxidation of myoglobin and hemoglobin, Biochemistry 35, 6976-6983.
9. Herold, S., and Röck, G. (2003) Reactions of deoxy-, oxy-, and methemoglobin with nitrogen monoxide. Mechanistic studies of the S-nitrosothiol formation under different mixing conditions, J. Biol. Chem. 278, 6623-6634.
10. Brunori, M. (2001) Nitric oxide, cytochrome-c oxidase and myoglobin, Trends Biochem. Sci. 26, 21-23.
11. Nienhaus, K., Deng, P., Kriegl, J. M., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: The Effect of Internal Cavities on Ligand Migration and Binding, Biochemistry 42, 9647-9658.
12. Dantsker, D., Samuni, U., Friedman, A. J., Yang, M., Ray, A., and Friedman, J. M. (2002) Geminate rebinding in trehalose-glass embedded myoglobins reveals residue-specific control of intramolecular trajectories, J. Mol. Biol. 315, 239-251.
13. Samuni, U., Dantsker, D., Khan, I., Friedman, A. J., Peterson, E., and Friedman, J. M. (2002) Spectroscopically and kinetically distinct conformational populations of sol-gel-encapsulated carbonmonoxy myoglobin. A comparison with hemoglobin, J. Biol. Chem. 277, 25783-25790.
14. Scott, E. E., and Gibson, Q. H. (1997) Ligand migration in sperm whale myoglobin, Biochemistry 36, 11909-11917.
15. 2 entry into and exit from myoglobin, J. Biol. Chem. 276, 5177-5188.
16. Nienhaus, K., Deng, P., Kriegl, J. M., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: Spectroscopic and Structural Characterization of Ligand Docking Sites in Myoglobin Mutant L29W, Biochemistry 42, 9633-9646.
17. Nienhaus, K., Deng, P., Olson, J. S., Warren, J. J., and Nienhaus, G. U. (2003) Structural Dynamics of Myoglobin: Ligand Migration and Binding in Valine 68 Mutants, J. Biol. Chem. 278, 42532-42544.
18. Ostermann, A., Waschipky, R., Parak, F. G., and Nienhaus, G. U. (2000) Ligand binding and conformational motions in myoglobin, Nature 404, 205-208.
19. Brunori, M., Vallone, B., Cutruzzola, F., Travaglini-Allocatelli, C., Berendzen, J., Chu, K., Sweet, R. M., and Schlichting, I. (2000) The role of cavities in protein dynamics: crystal structure of a photolytic intermediate of a mutant myoglobin, Proc. Natl. Acad. Sci. U.S.A. 97, 2058-2063.
20. Bourgeois, D., Vallone, B., Schotte, F., Arcovito, A., Miele, A. E., Sciara, G., Wulff, M., Anfinrud, P., and Brunori, M. (2003) Complex landscape of protein structural dynamics unveiled by nanosecond Laue crystallography, Proc. Natl. Acad. Sci. U.S.A. 100, 8704-8709.
21. Hummer, G., Schotte, F., and Anfinrud, P. A. (2004) Unveiling functional protein motions with picosecond x-ray crystallography and molecular dynamics simulations, Proc. Natl. Acad. Sci. U.S.A. 101, 15330-15334.
22. Schmidt, M., Nienhaus, K., Pahl, R., Krasselt, A., Anderson, S., Parak, F., Nienhaus, G. U., and Srajer, V. (2005) Ligand migration pathway and protein dynamics in myoglobin: a time-resolved crystallographic study on L29W MbCO, Proc. Natl. Acad. Sci. U.S.A. 102, 11704-11709.
23. Schotte, F., Lim, M., Jackson, T. A., Smirnov, A. V., Soman, J., Olson, J. S., Phillips, G. N., Jr., Wulff, M., and Anfinrud, P. A. (2003) Watching a protein as it functions with 150-ps time-resolved x-ray crystallography, Science 300, 1944-1947.
24. Miller, L. M., Pedraza, A. J., and Chance, M. R. (1997) Identification of conformational substates involved in nitric oxide binding to ferric and ferrous myoglobin through difference Fourier transform infrared spectroscopy (FTIR), Biochemistry 36, 12199-12207.
25. Kim, S., Jin, G., and Lim, M. (2004) Dynamics of Geminate Recombination of NO with Myoglobin in Aqueous Solution Probed by Femtosecond Mid-IR Spectroscopy, J. Phys. Chem. B 108, 20366-20375.
26. Kim, S., and Lim, M. (2005) Protein conformation-induced modulation of ligand binding kinetics: a femtosecond mid-IR study of nitric oxide binding trajectories in myoglobin, J. Am. Chem. Soc. 127, 8908-8909.
27. Ionascu, D., Gruia, F., Ye, X., Yu, A., Rosea, F., Beck, C., Demidov, A., Olson, J. S., and Champion, P. M. (2005) Temperature-dependent studies of NO recombination to heme and heme proteins, J. Am. Chem. Soc. 127, 16921-16934.
28. Petrich, J. W., Poyart, C., and Martin, J. L. (1988) Photophysics and reactivity of heme proteins: a femtosecond absorption study of hemoglobin, myoglobin, and protoheme, Biochemistry 27, 4049-4060.
29. Olson, J. S., and Phillips, G. N., Jr. (1996) Kinetic pathways and barriers for ligand binding to myoglobin, J. Biol. Chem. 271, 17593-17596.
30. 2 and the vibrational relaxation of the six-coordinate heme species, J. Am. Chem. Soc. 124, 5914-5924.
31. Petrich, J. W., Lambry, J. C., Balasubramanian, S., Lambright, D. G., Boxer, S. G., and Martin, J. L. (1994) Ultrafast measurements of geminate recombination of NO with site-specific mutants of human myoglobin, J. Mol. Biol. 238, 437-444.
32. Petrich, J. W., Lambry, J. C., Kuczera, K., Karplus, M., Poyart, C., and Martin, J. L. (1991) Ligand binding and protein relaxation in heme proteins: a room temperature analysis of NO geminate recombination, Biochemistry 30, 3975-3987.
33. Cao, W., Christian, J. F., Champion, P. M., Rosca, F., and Sage, J. T. (2001) Water penetration and binding to ferric myoglobin, Biochemistry 40, 5728-5737.
34. Deng, P., Nienhaus, K., Palladino, P., Olson, J. S., Blouin, G., Moens, L., Dewilde, S., Geuens, E., and Nienhaus, G. U. (2007) Transient ligand docking sites in Cerebratulus lacteus mini-hemoglobin, Gene 398, 208-223.
35. Nienhaus, K., Maes, E. M., Weichsel, A., Montfort, W. R., and Nienhaus, G. U. (2004) Structural dynamics controls nitric oxide affinity in nitrophorin 4, J. Biol. Chem. 279, 39401-39407.
36. Lamb, D. C., Nienhaus, K., Arcovito, A., Draghi, F., Miele, A. E., Brunori, M., and Nienhaus, G. U. (2002) Structural dynamics of myoglobin: ligand migration among protein cavities studied by Fourier transform infrared/temperature derivative spectroscopy, J. Biol. Chem. 277, 11636-11644.
37. Nienhaus, K., and Nienhaus, G. U. (2007) Ligand Dynamics in Heme Proteins Observed by Fourier Transform Infrared Spectroscopy at Cryogenic Temperatures, Methods Enzymol., in press.
38. Tilton, R. F., Jr., Kuntz, I. D., Jr., and Petsko, G. A. (1984) Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 Å, Biochemistry 23, 2849-2857.
39. Nienhaus, G. U., and Nienhaus, K. (2002) Infrared Study of Carbon Monoxide Migration among Internal Cavities of Myoglobin Mutant L29W, J. Biol. Phys. 28, 163-172.
40. Springer, B. A., and Sligar, S. G. (1987) High-level expression of sperm whale myoglobin in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 84, 8961-8965.
41. 2O, J. Inorg. Biochem. 98, 161-166.
42. Douzou, P. (1977) Cryobiochemistry, Academic Press, New York.
43. Mourant, J. R., Braunstein, D. P., Chu, K., Frauenfelder, H., Nienhaus, G. U., Ormos, P., and Young, R. D. (1993) Ligand binding to heme proteins: II. Transitions in the heme pocket of myoglobin, Biophys. J. 65, 1496-1507.
44. Nienhaus, K., Lamb, D. C., Deng, P., and Nienhaus, G. U. (2002) The Effect of Ligand Dynamics on Heme Electronic Transition Band III in Myoglobin, Biophys. J. 82, 1059-1067.
45. Berendzen, J., and Braunstein, D. (1990) Temperature-derivative spectroscopy: a tool for protein dynamics, Proc. Natl. Acad. Sci. U.S.A. 87, 1-5.
46. Nienhaus, G. U., Mourant, J. R., Chu, K., and Frauenfelder, H. (1994) Ligand binding to heme proteins: the effect of light on ligand binding in myoglobin, Biochemistry 33, 13413-13430.
47. Austin, R. H., Beeson, K. W., Eisenstein, L., Frauenfelder, H., and Gunsalus, I. C. (1975) Dynamics of ligand binding to myoglobin, Biochemistry 14, 5355-5373.
48. Ehrenstein, D., and Nienhaus, G. U. (1992) Conformational substates in azurin, Proc. Natl. Acad. Sci. U.S.A. 89, 9681-9685.
49. Alben, J. O., Beece, D., Bowne, S. F., Doster, W., Eisenstein, L., Frauenfelder, H., Good, D., McDonald, J. D., Marden, M. C., Moh, P. P., Reinisch, L., Reynolds, A. H., Shyamsunder, E., and Yue, K. T. (1982) Infrared spectroscopy of photodissociated carboxymyoglobin at low temperatures, Proc. Natl. Acad. Sci. U.S.A. 79, 3744-3748.
50. Chu, K., Ernst, R. M., Frauenfelder, H., Mourant, J. R., Nienhaus, G. U., and Philipp, R. (1995) Light-induced and thermal relaxation in a protein, Phys. Rev. Lett. 74, 2607-2610.
51. Lehle, H., M., K. J., Nienhaus, K., Deng, P., Fengler, S., and Nienhaus, G. U. (2005) Probing Electric Fields in Protein Cavities by Using the Vibrational Stark Effect of Carbon Monoxide, Biophys. J. 88, 1978-1990.
52. Kriegl, J. M., Nienhaus, K., Deng, P., Fuchs, J., and Nienhaus, G. U. (2003) Ligand dynamics in a protein internal cavity, Proc. Natl. Acad. Sci. U.S.A. 100, 7069-7074.
53. Ansari, A., Berendzen, J., Braunstein, D., Cowen, B. R., Frauenfelder, H., Hong, M. K., Iben, I. E., Johnson, J. B., Ormos, P., Sauke, T. B., and et al. (1987) Rebinding and relaxation in the myoglobin pocket, Biophys. Chem. 26, 337-355.
54. Braunstein, D. P., Chu, K., Egeberg, K. D., Frauenfelder, H., Mourant, J. R., Nienhaus, G. U., Ormos, P., Sligar, S. G., Springer, B. A., and Young, R. D. (1993) Ligand binding to heme proteins: III. FTIR studies of His-E7 and Val-E11 mutants of carbonmonoxymyoglobin, Biophys. J. 65, 2447-2454.
55. Li, T., Quillin, M. L., Phillips, G. N., Jr., and Olson, J. S. (1994) Structural determinants of the stretching frequency of CO bound to myoglobin, Biochemistry 33, 1433-1446.
56. Müller, J. D., McMahon, B. H., Chien, E. Y., Sligar, S. G., and Nienhaus, G. U. (1999) Connection between the taxonomic substates and protonation of histidines 64 and 97 in carbonmonoxy myoglobin, Biophys. J. 77, 1036-1051.
57. 17O isotropic chemical shifts, and nuclear quadrupole coupling constants, Biophys. J. 72, 899-912.
58. Yang, F., and Phillips, G. N., Jr. (1996) Crystal structures of CO-, deoxy- and met-myoglobins at various pH values, J. Mol. Biol. 256, 762-774.
59. Tian, W. D., Sage, J. T., and Champion, P. M. (1993) Investigations of ligand association and dissociation rates in the "open" and "closed" states of myoglobin, J. Mol. Biol. 233, 155-166.
60. Vojtechovsky, J., Chu, K., Berendzen, J., Sweet, R. M., and Schlichting, I. (1999) Crystal structures of myoglobin-ligand complexes at near-atomic resolution, Biophys. J. 77, 2153-2174.
61. Johnson, J. B., Lamb, D. C., Frauenfelder, H., Müller, J. D., McMahon, B., Nienhaus, G. U., and Young, R. D. (1996) Ligand binding to heme proteins. VI. Interconversion of taxonomic substates in carbonmonoxymyoglobin, Biophys. J. 71, 1563-1573.
62. Ray, G. B., Li, X.-Y., Ibers, J. A., Sessler, J. L., and Spiro, G. S. (1994) How far can proteins bend the FeCO unit, J. Am. Chem. Soc. 116, 162-176.
63. Vogel, K. M., Kozlowski, P. M., Zgierski, M. Z., and Spiro, T. G. (1999) Determinants of the FeXO (X = C, N, O) vibrational frequencies in heme adducts from experiment and density functional theory, J. Am. Chem. Soc. 121, 9915-9921.
64. Coyle, C. M., Vogel, K. M., Rush, T. S., 3rd, Kozlowski, P. M., Williams, R., Spiro, T. G., Dou, Y., Ikeda-Saito, M., Olson, J. S., and Zgierski, M. Z. (2003) FeNO structure in distal pocket mutants of myoglobin based on resonance Raman spectroscopy, Biochemistry 42, 4896-4903.
65. Park, E. S., and Boxer, S. G. (2002) Origins of the sensitivity of molecular vibrations to electric fields: Carbonyl and Nitrosyl stretches in model compounds and proteins, J. Phys. Chem. B 106, 5800-5806.
66. Tomita, T., Hirota, S., Ogura, T., Olson, J. S., and Kitagawa, T. (1999) Resonance Raman Investigations of Fe-N-O Structure Nitrosylheme in Myoglobin and Its Mutants, J. Phys. Chem. B 103, 7044-7054.
67. Park, E. S., Thomas, M. R., and Boxer, S. G. (2000) Vibrational Stark Spectroscopy of NO bound to Heme: Effects of Protein Electrostatic fields on the NO Stretch Frequency, J. Am. Chem. Soc. 122, 12297-12303.
68. Hoffman, B. M., and Gibson, Q. H. (1978) On the photosensitivity of liganded hemoproteins and their metal-substituted analogues, Proc. Natl. Acad. Sci. U.S.A. 75, 21-25.
69. Martin, J. L., and Vos, M. H. (1994) Femtosecond measurements of geminate recombination in heme proteins, Methods Enzymol. 232, 416-430.
70. Nutt, D. R., and Meuwly, M. (2007) Ferric and Ferrous Iron in Nitroso-Myoglobin: Computer Simulations of Stable and Metastable States and Their Infrared Spectra, Chemphyschem 8, 527-536.
71. Nutt, D. R., Karplus, M., and Meuwly, M. (2005) Potential energy surface and molecular dynamics of MbNO: existence of an unsuspected FeON minimum, J. Phys. Chem. B 109, 21118-21125.
72. Cheng, L., Novozhilova, I., Kim, C., Kovalevsky, A., Bagley, K. A., Coppens, P., and Richter-Addo, G. B. (2000) First Observation of Photoinduced Nitrosyl Linkage Isomers of Iron Nitrosyl Porphyrins, J. Am. Chem. Soc. 122, 7142-7143.
73. Hartmann, H., Zinser, S., Komninos, P., Schneider, R. T., Nienhaus, G. U., and Parak, F. (1996) X-ray structure determination of a metastable state of carbonmonoxy myoglobin after photodissociation, Proc. Natl. Acad. Sci. U.S.A. 93, 7013-7016.
74. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1997) Ultrafast rotation and trapping of carbon monoxide dissociated from myoglobin, Nat. Struct. Biol. 4, 209-214.
75. Schlichting, I., Berendzen, J., Phillips, G. N., Jr., and Sweet, R. M. (1994) Crystal structure of photolysed carbonmonoxy-myoglobin, Nature 371, 808-812.
76. Teng, T. Y., Srajer, V., and Moffat, K. (1994) Photolysis-induced structural changes in single crystals of carbonmonoxy myoglobin at 40 K, Nat. Struct. Biol. 1, 701-705.
77. Lim, M., Jackson, T. A., and Anfinrud, P. A. (1995) Binding of CO to myoglobin from a heme pocket docking site to form nearly linear Fe-C-O, Science 269, 962-966.
78. Nienhaus, K., Olson, J. S., Franzen, S., and Nienhaus, G. U. (2005) The origin of Stark splitting in the initial photoproduct state of MbCO, J. Am. Chem. Soc. 127, 40-41.
79. Bredenbeck, J., Helbing, J., Nienhaus, K., Nienhaus, G. U., and Hamm, P. (2007) Multidimensional Ultrafast Spectroscopy Special Feature: Protein ligand migration mapped by nonequilibrium 2D-IR exchange spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 104, 14243-14248.
80. Park, E. S., Andrews, S. S., Hu, R. B., and Boxer, S. G. (1999) Vibrational Stark spectroscopy in proteins: A probe and calibration for electrostatic fields, J. Phys. Chem. B 103, 9813-9817.
81. Dalosto, S. D., Vanderkooi, J. M., and Sharp, K. A. (2004) Vibrational Stark Effects on Carbonyl, Nitrile, and Nitrosyl Compounds Including Heme Ligands, CO, CN, and NO, Studied with Density Functional Theory J. Phys. Chem. B 108, 6450-6457.
82. Mankoo, P. K., and Keyes, T. (2006) Classical Molecular Electrostatics: Recognition of Ligands in Proteins and the Vibrational Stark Effect, J. Phys. Chem. B 110, 25074-25079.
83. Engler, N., Prusakov, V., Ostermann, A., and Parak, F. G. (2003) A water network within a protein: temperature-dependent water ligation in H64V-metmyoglobin and relaxation to deoxymyoglobin, Eur. Biophys. J. 31, 595-607.
84. +, J. Mol. Spectrosc. 149, 559-561.
85. Agmon, N., and Hopfield, J. J. (1983) CO binding to heme proteins: A model for barrier height distributions and slow conformational changes, J. Chem. Phys. 79, 2042-2053.
86. Steinbach, P. J., Ansari, A., Berendzen, J., Braunstem, D., Chu, K., Cowen, B. R., Ehrenstein, D., Frauenfelder, H., Johnson, J. B., Lamb, D. C., Luck, S., Mourant, J. R., Nienhaus, G. U., Ormos, P., Philipp, R., Xie, A., and Young, R. D. (1991) Ligand binding to heme proteins: connection between dynamics and function, Biochemistry 30, 3988-4001.
87. Frauenfelder, H., Nienhaus, G. U., and Johnson, J. B. (1991) Rate Processes in Proteins, Ber. Bunsenges. Phys. Chem. 95, 272-278.
88. Dantsker, D., Roche, C., Samuni, U., Blouin, G., Olson, J. S., and Friedman, J. M. (2005) The position 68(E11) side chain in myoglobin regulates ligand capture, bond formation with heme iron, and internal movement into the xenon cavities, J. Biol. Chem. 280, 38740-38755.
89. Carlson, M. L., Regan, R., Elber, R., Li, H., Phillips, G. N., Jr., Olson, J. S., and Gibson, Q. H. (1994) Nitric oxide recombination to double mutants of myoglobin: role of ligand diffusion in a fluctuating heme pocket, Biochemistry 33, 10597-10606.
90. Hori, H., Masuya, F., Dou, Y., and Ikeda-Saito, M. (2000) EPR studies on the photoinduced intermediates of NO complexes in recombinant ferric-Mb trapped at low temperatures, J. Inorg. Biochem. 82, 181-187.
91. Nutt, D. R., and Meuwly, M. (2006) Studying reactive processes with classical dynamics: rebinding dynamics in MbNO, Biophys. J. 90, 1191-1201.
92. Helbing, J., Nienhaus, K., Nienhaus, G. U., and Hamm, P. (2005) Restricted Rotational Motion of CO in a Protein Internal Cavity: Evidence for Non-Separating Correlation Functions from IR Pump-Probe Spectroscopy, J. Chem. Phys. 122, 124505.
93. Nienhaus, G. U., Chu, K., and Jesse, K. (1998) Structural heterogeneity and ligand binding in carbonmonoxy myoglobin crystals at cryogenic temperatures, Biochemistry 37, 6819-6823.
94. Ford, P. C., Wink, D. A., and Stanbury, D. M. (1993) Autoxidation kinetics of aqueous nitric oxide, FEBS Lett. 326, 1-3.
95. Weiss, J. J. (1964) Nature of the Iron-Oxygen Bond in Oxyhaemoglobin, Nature 203, 182-183.
96. Herold, S. (1999) Kinetic and spectroscopic characterization of an intermediate peroxynitrite complex in the nitrogen monoxide induced oxidation of oxyhemoglobin, FEBS Lett. 443, 81-84.