Heme versus non-heme iron-nitroxyl {FeN(H)O}8 complexes: Electronic structure and biologically relevant reactivity

Accounts of Chemical Research

Volumn 47, Issue 4, 2014, Pages 1106-1116

  Speelman, Amy L ^a   Lehnert, Nicolai ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERROUS ION; HEME; NITRIC-OXIDE REDUCTASE; NITROGEN OXIDE; NITROXYL; OXIDOREDUCTASE;

CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; THERMODYNAMICS;

FERROUS COMPOUNDS; HEME; MODELS, CHEMICAL; MODELS, MOLECULAR; NITROGEN OXIDES; OXIDOREDUCTASES; THERMODYNAMICS;

EID: 84898858903     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400256u     Document Type: Article

References (49)

1. Moncada, S.; Palmer, R. M.; Higgs, E. A. Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol. Rev. 1991, 43, 109-142
2. Ignarro, L.: Nitric Oxide: Biology and Pathobiology; Academic Press: San Diego, 2000.
3. Lehnert, N.; Berto, T. C.; Galinato, M. G. I.; Goodrich, L. E.: The Role of Heme-Nitrosyls in the Biosynthesis, Transport, Sensing, and Detoxification of Nitric Oxide (NO) in Biological Systems: Enzymes and Model Complexes. In The Handbook of Porphyrin Science; Kadish, K. M.; Smith, K. M.; Guilard, R., Eds.; World Scientific: Hackensack, NJ, 2011; Vol. 14; Chap. 63, pp 1-247.
4. Gladwin, M. T.; Grubina, R.; Doyle, M. P. The New Chemical Biology of Nitrite Reactions with Hemoglobin: R-State Catalysis, Oxidative Denitrosylation, and Nitrite Reductase/Anhydrase Acc. Chem. Res. 2009, 42, 157-167
5. Miranda, K. M. The chemistry of nitroxyl (HNO) and implications in biology Coord. Chem. Rev. 2005, 249, 433-455
6. Bartberger, M. D.; Liu, W.; Ford, E.; Miranda, K. M.; Switzer, C.; Fukuto, J. M.; Farmer, P. J.; Wink, D. A.; Houk, K. N. The reduction potential of nitric oxide (NO) and its importance to NO biochemistry Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 10958-10963
7. Kumar, M. R.; Fukuto, J. M.; Miranda, K. M.; Farmer, P. J. Reactions of HNO with Heme Proteins Inorg. Chem. 2010, 49, 6283-6292
8. Fukuto, J. M.; Cisneros, C. J.; Kinkade, R. L. A comparison of the chemistry associated with the biological signaling and actions of nitroxyl (HNO) and nitric oxide (NO) J. Inorg. Biochem. 2013, 118, 201-208
9. 2 Analogue: Long-Lived HNO Adducts of Ferrous Globins Biochemistry 2009, 48, 5018-5025
10. Enemark, J. H.; Feltham, R. D. Principles of Structure, Bonding, and Reactivity for Metal Nitrosyl Complexes Coord. Chem. Rev. 1974, 13, 339-406
11. Nakahara, K.; Tanimoto, T.; Hatano, K.; Usuda, K.; Shoun, H. Cytochrome P-450 55A1 (P-450dNIR) acts as nitric oxide reductase employing NADH as the direct electron donor J. Biol. Chem. 1993, 268, 8350-8355
12. Obayashi, E.; Takahashi, S.; Shiro, Y. Electronic Structure of Reaction Intermediate of Cytochrome P450nor in Its Nitric Oxide Reduction J. Am. Chem. Soc. 1998, 120, 12964-12965
13. nor J. Inorg. Biochem. 2002, 88, 343-352
14. Lehnert, N.; Praneeth, V. K. K.; Paulat, F. Electronic Structure of Iron(II)-Porphyrin Nitroxyl Complexes: Molecular Mechanism of Fungal Nitric Oxide Reductase (P450nor) J. Comput. Chem. 2006, 27, 1338-1351
15. Riplinger, C.; Neese, F. The Reaction Mechanism of Cytochrome P450 NO Reductase: A Detailed Quantum Mechanics/Molecular Mechanics Study ChemPhysChem 2011, 12, 3192-3203
16. 2O generation by bacterial nitric oxide reductase Science 2010, 330, 1666-1670
17. Berto, T. C.; Speelman, A.; Zheng, S.; Lehnert, N. Mono- and Dinuclear Non-Heme Iron-Nitrosyl Complexes: Models for Key Intermediates in Bacterial Nitric Oxide Reductases Coord. Chem. Rev. 2013, 257, 244-259
18. 2O Generation in Bacterial Nitric Oxide Reductase: A Quantum Chemical Study Biochemistry 2012, 51, 5173-5186
19. Kurtz, D. M., Jr. Flavo-diiron enzymes: nitric oxide or dioxygen reductases? J. Chem. Soc., Dalton Trans. 2007, 4115-4121
20. Hayashi, T.; Caranto, J. D.; Matsumura, H.; Kurtz, D. M.; Moënne-Loccoz, P. Vibrational Analysis of Mononitrosyl Complexes in Hemerythrin and Flavodiiron Proteins: Relevance to Detoxifying NO Reductase J. Am. Chem. Soc. 2012, 134, 6878-6884
21. Hayashi, T.; Caranto, J. D.; Wampler, D. A.; Kurtz, D. M.; Moënne-Loccoz, P. Insights into the Nitric Oxide Reductase Mechanism of Flavodiiron Proteins from a Flavin-Free Enzyme Biochemistry 2010, 49, 7040-7049
22. 2 Provides Insight into the Mechanism of Flavodiiron NO Reductases J. Am. Chem. Soc. 2013, 135, 4902-4905
23. Einsle, O.; Messerschmidt, A.; Huber, R.; Kroneck, P. M. H.; Neese, F. Mechanism of the Six-Electron Reduction of Nitrite to Ammonia by Cytochrome c Nitrite Reductase J. Am. Chem. Soc. 2002, 124, 11737-11745
24. Bykov, D.; Neese, F. Reductive activation of the heme iron-nitrosyl intermediate in the reaction mechanism of cytochrome c nitrite reductase: A theoretical study J. Biol. Inorg. Chem. 2012, 17, 741-760
25. Murphy, W. R., Jr.; Takeuchi, K. J.; Meyer, T. J. Interconversion of Nitrite and Ammonia: Progress toward a Model for Nitrite Reductase J. Am. Chem. Soc. 1982, 104, 5817-5819
26. Liu, Y.; Ryan, M. D. The electrochemical reduction of iron porphyrin nitrosyls in the presence of weak acids J. Electroanal. Chem. 1994, 368, 209-219
27. 8 Porphyrin Model Complexes: New Insight from a Bis-Picket Fence Porphyrin Inorg. Chem. 2013, 52, 7766-7780
28. Lançon, D.; Kadish, K. M. Electrochemical and spectral characterization of iron mono- and dinitrosyl porphyrins J. Am. Chem. Soc. 1983, 105, 5610-5617
29. Choi, I.-K.; Liu, Y.; Feng, D.; Paeng, K.-J.; Ryan, M. D. Electrochemical and Spectroscopic Studies of Iron Porphyrin Nitrosyls and Their Reduction Products Inorg. Chem. 1991, 30, 1832-1839
30. 8 in a Heme Model J. Am. Chem. Soc. 2010, 132, 989-995
31. 8 complex: properties and biological reactivity of reduced MNO systems Chem. Sci. 2012, 3, 364-369
32. 9 Metal Nitrosyls in Relation to Nitroxyl Coordination Chemistry Struct. Bonding (Berlin, Ger.) 2013, 10.1007/430-2012-87
33. Lehnert, N.; Scheidt, W. R.; Wolf, M. W. Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology Struct. Bonding (Berlin, Ger.) 2013, 10.1007/430-2013-92
34. Goodrich, L. E.; Paulat, F.; Praneeth, V. K. K.; Lehnert, N. Electronic Structure and Reactivity of Heme-Nitrosyls and Its Significance for Nitric Oxide Sensing, Transport, and Catalysis in Biological Systems Inorg. Chem. 2010, 49, 6293-6316
35. Traylor, T. G.; Sharma, V. S. Why NO? Biochemistry 1992, 31, 2847-2849
36. Praneeth, V. K. K.; Näther, C.; Peters, G.; Lehnert, N. Spectroscopic Properties and Electronic Structure of Five- and Six-Coordinate Iron(II) Porphyrin NO Complexes: Effect of the Axial N-Donor Ligand Inorg. Chem. 2006, 45, 2795-2811
37. Lehnert, N.; Sage, J. T.; Silvernail, N. J.; Scheidt, W. R.; Alp, E. E.; Sturhahn, W.; Zhao, J. Oriented Single-Crystal Nuclear Resonance Vibrational Spectroscopy of [Fe(TPP)(MI)(NO)]: Quantitative Assessment of the trans Effect of NO Inorg. Chem. 2010, 49, 7197-7215
38. 1+/0 Couple of the Fe Protein from Azotobacter vinelandii J. Am. Chem. Soc. 2002, 124, 12100-12101
39. Farmer, P. J.; Sulc, F. Coordination chemistry of the HNO ligand with hemes and synthetic coordination complexes J. Inorg. Biochem. 2005, 99, 166-184
40. Zapata, A. L.; Kumar, M. R.; Pervitsky, D.; Farmer, P. J. A singular value decomposition approach for kinetic analysis of reactions of HNO with myoglobin J. Inorg. Biochem. 2013, 118, 171-178
41. Immoos, C. E.; Sulc, F.; Farmer, P. J.; Czarnecki, K.; Bocian, D. F.; Levina, A.; Aitken, J. B.; Armstrong, R. S.; Lay, P. A. Bonding in HNO-Myoglobin as Characterized by X-ray Absorption and Resonance Raman Spectroscopies J. Am. Chem. Soc. 2005, 127, 814-815
42. Ling, Y.; Mills, C.; Weber, R.; Yang, L.; Zhang, Y. NMR, IR/Raman, and Structural Properties in HNO and RNO (R = Alkyl and Aryl) Metalloporphyrins with Implication for the HNO-Myoglobin Complex J. Am. Chem. Soc. 2010, 132, 1583-1591
43. Goodrich, L. E.; Lehnert, N. The trans effect of nitroxyl (HNO) in ferrous heme systems: Implications for soluble guanylate cyclase activation by HNO J. Inorg. Biochem. 2013, 118, 179-186
44. Yi, J.; Morrow, B. H.; Campbell, A. L. O. C.; Shen, J. K.; Richter-Addo, G. B. Nitric oxide coupling mediated by iron porphyrins: the N-N bond formation step is facilitated by electrons and a proton Chem. Commun. 2012, 48, 9041-9043
45. Tonzetich, Z. J.; Héroguel, F.; Do, L. H.; Lippard, S. J. Chemistry of Nitrosyliron Complexes Supported by a β-Diketiminate Ligand Inorg. Chem. 2011, 50, 1570-1579
46. 8 Complex: Implications for the Reactivity of Iron Nitroxyl Species in Biology Angew. Chem., Int. Ed. 2013, 52, 12283-12287
47. B Center of Bacterial Nitric Oxide Reductase (NorBC) J. Am. Chem. Soc. 2011, 133, 16714-16717
48. 8 Species J. Am. Chem. Soc. 2010, 132, 4739-4751
49. 2+/+/0 J. Am. Chem. Soc. 2004, 126, 5138-5153