Breaking the proximal Fe II-N His bond in heme proteins through local structural tension: Lessons from the heme b proteins nitrophorin 4, nitrophorin 7, and related site-directed mutant proteins

Biochemistry

Volumn 50, Issue 40, 2011, Pages 8559-8575

  He, Chunmao ^a   Neya, Saburo ^b   Knipp, Markus ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

^b CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BOND BREAKAGE; COORDINATION SITES; FERROHEME; HEME POCKETS; HEME PROTEINS; MUTANT PROTEINS; NEUTRAL PH; NITROPHORIN; NITROPHORIN-4; NO BINDING; RESONANCE RAMAN SPECTROSCOPY; SITE DIRECTED MUTAGENESIS; SOLUBLE GUANYLATE CYCLASE (SGC); SPATIAL ARRANGEMENTS; SPECTROSCOPIC INVESTIGATIONS; STRUCTURAL DETERMINANTS; TRANS EFFECT; UV-VIS ABSORBANCE; VINYL SUBSTITUENTS;

AMINO ACIDS; PORPHYRINS; RAMAN SPECTROSCOPY;

PROTEINS;

GLUTAMINE; HEMOPROTEIN; HISTIDINE; IRON; ISOPROTEIN; NITRIC OXIDE; NITROPHORIN 2; NITROPHORIN 4; NITROPHORIN 7; PHENYLALANINE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL BOND; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; SITE DIRECTED MUTAGENESIS; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; BINDING SITES; FERROUS COMPOUNDS; HEME; HEMEPROTEINS; HISTIDINE; HUMANS; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PROTEIN BINDING; SALIVARY PROTEINS AND PEPTIDES;

EID: 80053615330     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi201073t     Document Type: Article

References (111)

1. 6 f complex of oxygenic photosynthesis: Tuning the cavity Science 302, 1009-1014 (Pubitemid 37386186)
2. Ribeiro, J. M. C. and Francischetti, I. M. B. (2003) Role of arthropode saliva in blood feeding: Sialome and post-sialome perspectives Annu. Rev. Entomol. 48, 73-88 (Pubitemid 37365386)
3. Ignarro, L. J. (1990) Biosynthesis and metabolism of endothelium-derived nitric oxide Annu. Rev. Pharmacol. Toxicol. 30, 535-560
4. Soares, A. C., Carvalho-Tavares, J., Gontijo, N. d. F., dos Santos, V. C., Teixeira, M. M., and Pereira, M. H. (2006) Salivation pattern of Rhodnius prolixus (Reduviidae; Triatominae) in mouse skin J. Insect Physiol. 52, 468-472 (Pubitemid 44268995)
5. Weichsel, A., Andersen, J. F., Champagne, D. E., Walker, F. A., and Montfort, W. R. (1998) Crystal structures of a nitric oxide transport protein from a blood-sucking insect Nat. Struct. Biol. 5, 304-309 (Pubitemid 28164883)
6. 6 complex J. Inorg. Biochem. 99, 216-236 (Pubitemid 39646483)
7. Hoshino, M., Maeda, M., Konishi, R., Seki, H., and Ford, P. C. (1996) Studies on the reaction mechanism for reductive nitrosylation for ferrihemoproteins in buffer solutions J. Am. Chem. Soc. 118, 5702-5707 (Pubitemid 26233658)
8. Berry, R. E., Shokhirev, M. N., Ho, A. Y. W., Yang, F., Shokhireva, T. K., Zhang, H., Weichsel, A., Montfort, W. R., and Walker, F. A. (2009) Effect of mutation of carboxyl side-cahin amino acids near the heme on the midpoint potentials and ligand binding constants of nitrophorin 2 and its NO, histamine, and imidazole complexes J. Am. Chem. Soc. 131, 2313-2327
9. Shokhireva, T. K., Berry, R. E., Uno, E., Balfour, C. A., Zhang, H., and Walker, F. A. (2003) Electrochemical and NMR spectroscopic studies of distal pocket mutants of nitrophorin 2: Stability, structure, and dynamics of axial ligand complexes Proc. Natl. Acad. Sci. U.S.A. 100, 3778-3783 (Pubitemid 36418107)
10. Ding, X. D., Weichsel, A., Andersen, J. F., Shokhireva, T. K., Balfour, C., Pierik, A. J., Averill, B. A., Montfort, W. R., and Walker, F. A. (1999) Nitric oxide binding to the ferri- and ferroheme states of nitrophorin 1, a reversible NO-binding heme protein from the saliva of the blood-sucking insect, Rhodnius prolixus J. Am. Chem. Soc. 121, 128-138 (Pubitemid 29047130)
11. Enemark, J. H. and Feltham, R. D. (1974) Principles of structure, bonding, and reactivity for metal nitrosyl complexes Coord. Chem. Rev. 13, 339-406
12. Berry, R. E., Ding, X. D., Shokhireva, T. K., Weichsel, A., Montfort, W. R., and Walker, F. A. (2004) Axial ligand complexes of the Rhodnius nitrophorins: Reduction potentials, binding constants, EPR spectra, and structures of the 4-iodopyrazole and imidazole complexes of NP4 J. Biol. Inorg. Chem. 9, 135-144 (Pubitemid 38327309)
13. Berry, R. E., Shokhireva, T. K., Filippov, I., Shokhirev, M. N., Zhang, H., and Walker, F. A. (2007) The effect of the N-terminus on heme cavity structure, ligand equilibrium and rate constants and reduction potentials of nitrophorin 2 from Rhodnius prolixus Biochemistry 46, 6830-6843 (Pubitemid 46906413)
14. Knipp, M., Yang, F., Berry, R. E., Zhang, H., Shokhirev, M. N., and Walker, F. A. (2007) Spectroscopic and functional characterization of nitrophorin 7 from the blood-feeding insect Rhodnius prolixus reveals an important role of its isoform-specific N-terminus for proper protein function Biochemistry 46, 13254-13268 (Pubitemid 350139255)
15. Traylor, T. G. and Sharma, V. S. (1992) Why NO? Biochemistry 31, 2847-2849
16. 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 (Pubitemid 39258204)
17. Benabbas, A., Ye, X., Kubo, M., Zhang, Z., Maes, E. M., Montfort, W. R., and Champion, P. M. (2010) Ultrafast dynamics of diatomic ligand binding to nitrophorin 4 J. Am. Chem. Soc. 132, 2811-2820
18. Maes, E. M., Roberts, S. A., Weichsel, A., and Montfort, W. R. (2005) Ultrahigh resolution structures of nitrophorin 4: Heme distortion in ferrous CO and NO complexes Biochemistry 44, 12690-12699 (Pubitemid 41379399)
19. Ribeiro, J. M. C. (1996) Salivary thiol oxidase activity of Rhodnius prolixus Insect Biochem. Mol. Biol. 26, 899-905 (Pubitemid 27091756)
20. Daff, S. (2010) NO synthase: Structures and mechanisms Nitric Oxide 23, 1-11
21. Poulos, T. L. (2006) Soluble guanylate cyclase Curr. Opin. Struct. Biol. 16, 736-743 (Pubitemid 44834471)
22. Gladwin, M. T., Grubina, R., and Doyle, M. P. (2009) The new chemical biology of nitrite reactions with hemoglobin: R-state catalysis, oxidative denitrosylation, and nitrite reductase/anhydrase Acc. Chem. Res. 42, 157-167
23. 3 by the concerted nitrite reductase and anhydrase activity of hemoglobin Nat. Chem. Biol. 3, 785-794 (Pubitemid 350126874)
24. Creutz, C. and Sutin, N. (1973) Reduction of ferricytochrome c by dithionite ion: Electron transfer by parralel adjacent and remote pathways Proc. Natl. Acad. Sci. U.S.A. 70, 1701-1703
25. Knipp, M., Braun, O., and Vašák, M. (2005) Searching for DDAH inhibitors: S -Nitroso- l -homocysteine is a chemical lead J. Am. Chem. Soc. 127, 2372-2373 (Pubitemid 40327784)
26. Braun, O., Knipp, M., Chesnov, S., and Vašák, M. (2007) Specific reactions of S -nitrosothiols with cysteine hydrolases: A comparative study between dimethylargininase-1 and CTP synthetase Protein Sci. 16, 1522-1534 (Pubitemid 47195680)
27. Neya, S., Suzuki, M., Hoshino, T., Ode, H., Imai, K., Komatsu, T., Ikezaki, A., Nakamura, M., Furutani, Y., and Kandori, H. (2010) Molecular insights into intrinsic heme distortion in ligand binding in hemoprotein Biochemistry 49, 5642-5650
28. cam by the dithionite anion monomer J. Biol. Chem. 255, 7317-7325
29. Wang, W. and Malcolm, B. A. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis BioTechniques 26, 680-682
30. Knipp, M., Zhang, H., Berry, R. E., and Walker, F. A. (2007) Overexpression in Escherichia coli and functional reconstitution of the liposome binding ferriheme protein nitrophorin 7 from the blood sucking bug Rhodnius prolixus Protein Expression Purif. 54, 183-191 (Pubitemid 46636327)
31. Yang, F., Zhang, H., and Knipp, M. (2009) A one-residue switch reverses the orientation of a heme b cofactor. Investigations on the ferriheme NO transporters nitrophorin 2 and 7 from the blood-feeding insect Rhodnius prolixus Biochemistry 48, 235-241
32. Knipp, M., Taing, J. J., and He, C. (2011) Reduction of the lipocalin type heme containing protein nitrophorin: Sensitivity of the fold-stabilizing cysteine disulfides toward routine heme-iron reduction J. Inorg. Biochem. doi: 10.1016/j.jinorgbio.2011.07.009
33. Andersen, J. F., Ding, X. D., Balfour, C., Shokhireva, T. K., Champagne, D. E., Walker, F. A., and Montfort, W. R. (2000) Kinetics and equilibria in ligand binding by nitrophorins 1-4: Evidence for stabilization of a nitric oxide-ferriheme complex through a ligand-induced conformational trap Biochemistry 39, 10118-10131 (Pubitemid 30663033)
34. Knipp, M. and He, C. (2011) Nitrophorins: Nitrite disproportionation reaction and other novel functionalities of insect heme-based nitric oxide transport proteins IUBMB Life 63, 304-312
35. Palaniappan, V. and Bocian, D. F. (1994) Acid-induced transformations of myoglobin. Characterization of a new equilibrium heme-pocket intermediate Biochemistry 33, 14264-14274 (Pubitemid 24382373)
36. Tang, Q., Kalsbeck, W. A., Olson, J. S., and Bocian, D. F. (1998) Disruption of the heme iron-proximal histidine bond requires unfolding of deoxymyoglobin Biochemistry 37, 7047-7056 (Pubitemid 28228143)
37. Spiro, T. G. and Li, X.-Y. (1988) Resonance Raman spectroscopy of metalloporphyrins. In Resonance Raman Spectra of Heme and Metalloproteins (Spiro, T. G., Ed.) 1st ed., pp 1-38, John Wiley & Sons, New York.
38. Spiro, T. G. and Czernuszewicz, R. S. (2000) Resonance Raman Spectroscopy. In Physical Methods in Bioinorganic Chemistry: Spectroscopy and Magnetism (Que, L., Jr., Ed.) 1st ed., pp 59-119, University Science Books, Sausalito, CA.
39. Maes, E. M., Walker, F. A., Montfort, W. R., and Czernuszewicz, R. S. (2001) Resonance Raman spectroscopic study of nitrophorin 1, a nitric oxide-binding heme protein from Rhodnius prolixus, and its nitrosyl and cyano adducts J. Am. Chem. Soc. 123, 1164-1172
40. Kincaid, J. R. (2000) Resonance Raman spectra of heme proteins and model compounds. In The Porphyrin Handbook (Kadish, K. M., Smith, K. M., and Guilard, R., Eds.) 1st ed., pp 225-291, Academic Press, San Diego.
41. Andersson, L. A., Mylrajan, M., Sullivan, E. P., Jr., and Strauss, S. H. (1989) Modeling low-pH hemoproteins J. Biol. Chem. 264, 19099-19102 (Pubitemid 19285816)
42. Kitagawa, T., Kyogoku, Y., Iizuka, T., and Saito, M. I. (1976) Nature of the iron-ligand bond in ferrous low spin hemoproteins studied by resonance Raman scattering J. Am. Chem. Soc. 98, 5169-5173
43. Spiro, T. G., Stong, J. D., and Stein, P. (1979) Porphyrin core expansion and doming in heme proteins. New evidence from resonance Raman spectra of six-coordinate high-spin iron(III) hemes J. Am. Chem. Soc. 101, 2648-2655
44. Sage, J. T., Morikis, D., and Champion, P. M. (1991) Spectroscopic studies of myoglobin at low pH: Heme structure and ligation Biochemistry 30, 1227-1237
45. Vetter, S. W., Terentis, A. C., Orsborne, R. L., Dawson, J. H., and Goodin, D. B. (2009) Replacement of the axial histidine heme ligand with cysteine in nitrophorin 1: Spectroscopic and crystallographic characterization J. Inorg. Biol. Chem. 14, 179-191
46. He, C. and Knipp, M. (2009) Formation of nitric oxide from nitrite by the ferriheme b protein nitrophorin 7 J. Am. Chem. Soc. 131, 12042-12043
47. Sun, J., Loehr, T. M., Wilks, A., and Ortiz de Montellano, P. R. (1994) Identification of histidine 25 as the heme ligand in human liver heme oxygenase Biochemistry 33, 13734-13740 (Pubitemid 24381936)
48. Kitagawa, T., Ozaki, Y., Kyogoku, Y., and Horio, T. (1977) Resonance Raman study of the pH-dependent and detergent-induced structural alterations in the heme moiety of Rhodospirillum rubrum cytochrome c ′ Biochim. Biophys. Acta 495, 1-11 (Pubitemid 8215084)
49. Hobbs, J. D., Larsen, R. W., Meyer, T. E., Hazzard, J. H., Cusanovich, M. A., and Ondrias, M. R. (1990) Resonance Raman characterization of Chromatium vinosum cytochrom c ′. Effect of pH and comparison of equilibrium and photolyzed cabron monoxide species Biochemistry 29, 4166-4174 (Pubitemid 20145654)
50. 13C NMR spectroscopic study of the ferriheme resonances of three low-spin complexes of wild-type nitrophorin 2 and nitrophorin2(V24E) as a function of pH J. Biol. Inorg. Chem. 14, 1077-1095
51. Decatur, S. M., Franzen, S., DePillis, G. D., Dyer, R. B., Woodruff, W. H., and Boxer, S. G. (1996) Trans effect in nitric oxide binding to myoglobin cavity mutant H93G Biochemistry 35, 4939-4944 (Pubitemid 26126710)
52. Ford, P. C. (2010) Reactions of NO and nitrite with heme models and proteins Inorg. Chem. 49, 6226-6239
53. Praneeth, V. K. K., Näther, C., Peters, G., and Lehnert, N. (2006) Spectroscopic properties and electronic structure of five- and six-coordinate iron(II) porphyrin NO complexes: Effect of the axial N-donor ligand Inorg. Chem. 45, 2795-2811
54. Scheidt, W. R. and Ellison, M. K. (1999) The synthetic and structural chemistry of heme derivatives with nitric oxide ligands Acc. Chem. Res. 32, 350-359
55. Ibrahim, M., Xu, C., and Spiro, T. G. (2006) Differential sensing of protein influences by NO and CO vibrations in heme addcuts J. Am. Chem. Soc. 128, 16834-16845 (Pubitemid 46032759)
56. Reynolds, M. F., Parks, R. B., Burstyn, J. N., Shelver, D., Thorsteinsson, M. V., Kerby, R. L., Roberts, G. P., Vogel, K. M., and Spiro, T. G. (2000) Electronic absorption, EPR, and resonance Raman spectroscopy of CooA, a CO-sensing transcription activator from R. rubrum, reveals a five-coordinate NO-heme Biochemistry 39, 388-396 (Pubitemid 30056474)
57. Tomita, T., Ogura, T., Tsuyama, S., Imai, Y., and Kitagawa, T. (1997) Effects of GTP on bound nitric oxide of soluble guanylate cyclase probed by resonance Raman spectroscopy Biochemistry 36, 10155-10160 (Pubitemid 27357725)
58. Mukaiyama, Y., Uchida, T., Sato, E., Sasaki, A., Sato, Y., Igarashi, J., Kurokawa, H., Sagami, I., Kitagawa, T., and Shimizu, T. (2006) Spectroscopic and DNA-binding characterization of the isolated heme-bound basic helix-loop-helix-PAS-A domain of neuronal PAS protein 2 (NPAS2), a transcription activator associated with circadian rythms FEBS J. 273, 2528-2539 (Pubitemid 43736664)
59. Schade, D., Kotthaus, J., and Clement, B. (2010) Modulating the NO generating system from a medicinal chemistry perspective: Current trends and therapeutic options in cardiovascular disease Pharmacol. Ther. 126, 279-300
60. Tomita, T., Hirota, S., Ogura, T., Olson, J. S., and Kitagawa, T. (1999) Resonance raman investigation of Fe-N-O structure of nitrosylheme in myoglobin and its mutants J. Phys. Chem. B 103, 7044-7054 (Pubitemid 129702490)
61. Sawai, H., Makino, M., Mizutani, Y., Ohta, T., Sugimoto, H., Uno, T., Kawada, N., Yoshizato, K., Kitagawa, T., and Shiro, Y. (2005) Structural characterization of the proximal and distal histidine environment of cytoglobin and neuroglobin Biochemistry 44, 13257-13265 (Pubitemid 41429450)
62. Lukat-Rodgers, G. S. and Rodgers, K. R. (1997) Characterization of ferrous FixL-nitric oxide adducts by resonance raman spectroscopy Biochemistry 36, 4178-4187 (Pubitemid 27171590)
63. Tomita, T., Gonzalez, G., Chang, A. L., Ikeda-Saito, M., and Gilles-Gonzalez, M. A. (2002) A comparative resonance Raman analysis of heme-binding PAS domains: Heme iron coordination structures of the Bj FixL, Ax PDEA1, Ec Dos, and Mt Dos proteins Biochemistry 41, 4819-4826 (Pubitemid 34298648)
64. Andrew, C. R., George, S. J., Lawson, D. M., and Eady, R. R. (2002) Six- to five-coordinate heme-nitrosyl conversion in cytochrome c ′ and its releveance to guanylate cyclase Biochemistry 41, 2353-2360 (Pubitemid 34160897)
65. Andrew, C. R., Kemper, L. J., Busche, T. L., Tiwari, A. M., Kecskes, M. C., Stafford, J. M., Croft, L. C., Lu, S., Moënne-Loccoz, P., Huston, W., Mior, J. W. B., and Eady, R. R. (2005) Accessibility of the distial heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c ′: Evidence from spectroscopic studies Biochemistry 44, 8664-8672 (Pubitemid 40840432)
66. 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
67. Deinum, G., Stone, J. R., Babcock, G. T., and Marletta, M. A. (1996) Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy Biochemistry 35, 1540-1547 (Pubitemid 26055288)
68. Stone, J. R. and Marletta, M. A. (1994) Soluble guanylate cyclase from bovine lung: Activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states Biochemistry 33, 5636-5640 (Pubitemid 24163003)
69. Lukat-Rodgers, G. S., Correia, C., Botuyan, M. V., Mer, G., and Rodgers, K. R. (2010) Heme-based sensing by the mammalian circadian protein CLOCK Inorg. Chem. 49, 6349-6365
70. Vogel, K. M., Hu, S., Spiro, T. G., Dierks, E. A., Yu, A. E., and Burstyn, J. N. (1999) Variable forms of soluble guanylyl cyclase: Protein-ligand interactions and the issue of activation by carbon monoxide J. Biol. Inorg. Chem. 4, 804-813
71. Yu, A. E., Hu, S., Spiro, T. G., and Burstyn, J. N. (1994) Resonance Raman Spectroscopy of Soluble Guanylyl Cyclase Reveals Displacement of Distal and Proximal Heme Ligands by NO J. Am. Chem. Soc. 116, 4117-4118
72. 1H NMR spectroscopy: Comparison to structural data obtained from X-ray crystallography Inorg. Chem. 46, 170-178
73. 13C NMR spectroscopy: Comparison to structural data obtained from X-ray crystallography Inorg. Chem. 46, 2041-2056
74. 13C NMR spectroscopy and comparison to nitrophorin 2: Heme pocket structural similarities and differences Inorg. Chim. Acta 361, 925-940
75. 6 f complex Photochem. Photobiol. 84, 1349-1358
76. Barbieri, S., Murphy, L. M., Sawers, R. G., Eady, R. R., and Hasnain, S. S. (2008) Modulation of NO binding to cytochrome c ′ by distal and proximal haem pocket residues J. Biol. Inorg. Chem. 13, 531-540
77. Sharma, V. S. and Madge, D. (1999) Activation of soluble guanylate cyclase by carbon monoxide and nitric oxide: A mechanistic model Methods 19, 494-505 (Pubitemid 30025793)
78. Hobbs, A. J. (1997) Soluble guanylate cyclase: The forgotten sibling Trends Pharmacol. Sci. 18, 484-491
79. Goodrich, L. E., Paulat, F., Praneeth, V. K. K., and Lehnert, N. (2010) Electronic structure of heme-nitrosyls and its significance for nitric oxide reactivity, sensing, transport, and toxicity in biological systems Inorg. Chem. 49, 6293-6316
80. Yoshimura, T. and Siuzuki, S. (1988) The pH dependence of the stereochemistry around the heme group in NO-cytochrome c (horse heart) Inorg. Chim. Acta 152, 241-249
81. Duprat, A. F., Traylor, T. G., Wu, G.-Z., Coletta, M., Sharma, V. S., Walda, K. N., and Magde, D. (1995) Myoglobin-NO at low pH: Free four-coordinate heme in the protein pocket Biochemistry 34, 2634-2644
82. Pellicena, P., Karow, D. S., Boon, E. M., Marletta, M. A., and Kuriyan, J. (2004) Crystal structure of an oxygen-binding heme domain related to soluble guanylate cyclases Proc. Natl. Acad. Sci. U.S.A. 101, 12854-12859 (Pubitemid 39167547)
83. Suzuki, S., Yoshimura, T., Nakahara, A., Iwasaki, H., Shidara, S., and Matsubara, T. (1987) Electronic and magnetic circular dichroism spectra of pentacoordinate nitrosylhemes in cytochromes c ′ from nonphotosynthetic bacteria and their model complexes Inorg. Chem. 26, 1006-1008
84. Iwasaki, H., Yoshimura, T., Suzuki, S., and Shidara, S. (1991) Spectral properties of Achromobacter xylosoxidans cytochrome c ′ and their NO complexes Biochim. Biophys. Acta 1058, 79-82
85. Yoshimura, T., Fujii, S., Kamada, H., Yamaguchi, K., Suzuki, S., Shidara, S., and Takakuwa, S. (1996) Spectroscopic characterization of nitrosylheme in nitric oxide complexes of ferric and ferrous cytochrome c ′ from photosynthetic bacteria Biochim. Biophys. Acta 1292, 39-46
86. Lawson, D. M., Stevenson, C. E. M., Andrew, C. R., and Eady, R. R. (2000) Unprecedented proximal binding of nitric oxide to heme: Implications for guanylate cyclase EMBO J. 19, 5661-5671
87. Kharitonov, V. G., Sharma, V. S., Magde, D., and Koesling, D. (1997) Kinetics of nitric oxide dissociation from five- and six-coordinate nitrosyl hemes and heme proteins, including soluble guanylate cyclase Biochemistry 36, 6814-6818 (Pubitemid 27242342)
88. Pinakoulaki, E., Gemeinhardt, S., Saraste, M., and Varotsis, C. (2002) Nitric-oxide reductase: Structure and properties of the catalytic site from resonance Raman scattering J. Biol. Chem. 277, 23407-23413 (Pubitemid 34952172)
89. Xu, C. and Spiro, T. G. (2008) Ambidentate H-bonding by heme-bound NO: Structural and spectral effects of -O versus -N H-bonding J. Biol. Inorg. Chem. 13, 613-621
90. Ma, X., Sayed, N., Beuve, A., and van den Akker, F. (2007) NO and CO differentially activate soluble guanylate cyclase via a heme pivot-bend mechanism EMBO J. 26, 578-588 (Pubitemid 46160957)
91. Zhong, F., Wang, H., Ying, T., Huang, Z.-X., and Tan, X. (2010) Efficient expression of human soluble guanylate cyclase in Escherichia coli and its signaling-related interaction with nitric oxide Amino Acids 39, 399-408
92. Kitagawa, T. (1988) in Biological Applications of Raman Spectroscopy (Spiro, T. G., Ed.) pp 97-131, John Wiley & Sons, New York.
93. Coyle, C. M., Vogel, K. M., Rush, T. S., III, 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 (Pubitemid 36532041)
94. Hough, M. A., Antonyuk, S. V., Barbieri, S., Rustage, N., McKay, A. L., Servid, A. E., Eady, R. R., Andrew, C. R., and Hasnain, S. S. (2011) Distal-to-proximal NO conversion in hemoproteins: The role of the proximal pocket J. Mol. Biol. 405, 395-409
95. Scheidt, W. R. and Frisse, M. E. (1975) Nitrosylmetalloporphyrins. II. Synthesis and molecular sterochemistry of nitrosyl-α,β,γ, δ-tetraphenylporphinatoiron(II) J. Am. Chem. Soc. 97, 17-21
96. Spiro, T. G. and Wasbotten, I. H. (2005) CO as a vibrational probe of heme protein active sites J. Inorg. Biochem. 99, 34-44 (Pubitemid 39642970)
97. Wyllie, G. R. A., Schulz, C. E., and Scheidt, W. R. (2003) Five- to six-coordination in (nitrosyl)iron(II) porphyrinates: Effects of binding the sixth ligand Inorg. Chem. 42, 5722-5734
98. Scheidt, W. R. and Piciulo, P. L. (1976) Nitrosylmetalloporphyrins. III. Synthesis and molecular stereochemistry of nitrosyl-α,β,γ, δ-tetraphenylporphinato(1-methylimidazole)iron(II) J. Am. Chem. Soc. 98, 1913-1919
99. Silvernail, N. J., Pavlik, J. W., Noll, B. C., Schulz, C. E., and Scheidt, W. R. (2008) Reversible NO motion in crystaline [Fe(porphy)(1-MeIm)(NO) ] derivatives Inorg. Chem. 47, 912-920
100. Copeland, D. N., Soares, A. S., West, A. H., and Richter-Addo, G. B. (2006) Crystal structures of the nitrite and nitric oxide complexes of horse heart myoglobin J. Inorg. Biochem. 100, 1413-1425 (Pubitemid 43996961)
101. Brucker, E. A., Olson, J. S., Ikeda-Saito, M., and Phillips, G. N., Jr. (1998) Nitric oxide myoglobin: Crystal structure and analysis of ligand geometry Proteins: Struct., Funct., Genet. 30, 352-356 (Pubitemid 28117655)
102. Copeland, D. N., West, A. H., and Richter-Addo, G. B. (2003) Crystal structure of ferrous horse heart myoglobin complexed with nitric oxide and nitrosoethane Proteins: Struct., Funct., Genet. 53, 182-192 (Pubitemid 37193814)
103. II-NO] yielded 150°: Rich, A. M., Armstrong, R. S., Ellis, P. J., and Lay, P. A. (1998) Determination of the Fe-Ligand Bond Lengths and Fe-N-O bond angles in horse heart ferric and ferrous nitrosylmyoglobin using multiple-scattering XAFS analyses J. Am. Chem. Soc. 120, 10827-10836 (Pubitemid 28507427)
104. Tangen, E., Savadberg, A., and Ghosh, A. (2005) Toward modeling H-NOX domains: A DFT study of heme-NO complexes as hydrogen bond acceptors Inorg. Chem. 44, 7802-7805 (Pubitemid 41619082)
105. Lehnert, N., Sage, J. T., Silvernail, N., Scheidt, W. R., Alp, E. E., Sturhahn, W., and Zhao, J. (2010) Oriented single-crystal nuclear resonance vibration spectroscopy of [Fe(TPP)(MI)(NO)]: Quantitative assessment of the trans effect of NO Inorg. Chem. 49, 7197-7215
106. 2 by myoglobin J. Biol. Inorg. Chem. 4, 99-110 (Pubitemid 29113817)
107. Ribeiro, J. M. C. (1998) Rhodnius prolixus salivary nitrophorins display heme-peroxidase activity Insect Biochem. Mol. Biol. 28, 1051-1057 (Pubitemid 29022134)
108. Karow, D. S., Pan, D., Tran, R., Pellicena, P., Presley, A., Mathies, R. A., and Marletta, M. A. (2004) Spectroscopic characterization of the soluble guanylate cyclase-like heme domains from Vibrio cholerae and Thermoanaerobacter tengcongensis Biochemistry 43, 10203-10211 (Pubitemid 39030911)
109. Mukaiyama, Y., Uchida, T., Sato, E., Sasaki, A., Sato, Y., Igarashi, J., Kurikawa, H., Sagami, I., Kitagawa, T., and Shimizu, T. (2006) Spectroscopic and DNA-binding characterozation of the isolated heme-bound basic helix-loop-helix-PAS-A domain of neuronal PAS protein 2 (NPAS2), a transcription activator protein associated with circadian rythms FEBS J. 273, 2528-2539 (Pubitemid 43736664)
110. Igarashi, J., Sato, A., Kitagawa, T., Yoshimura, T., Yamauchi, S., Sagami, I., and Shimizu, T. (2004) Activation of heme-regulated eukaryotic initiator factor 2α kinase by nitric oxide is induced by the formation of a five-coordinate NO-heme complex. Optical absorption, electron spin resonance, and resonance Raman spectral studies J. Biol. Chem. 279, 15752-15762 (Pubitemid 38509260)
111. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual Molecular Dynamics J. Mol. Graphics 14, 33-38 (Pubitemid 26152973)