skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology

Abstract

This review summarizes our current understanding of the geometric and electronic structures of ferrous and ferric heme–nitrosyls, which are of key importance for the biological functions and transformations of NO. In-depth correlations are made between these properties and the reactivities of these species. Here, a focus is put on the discoveries that have been made in the last 10 years, but previous findings are also included as necessary. Besides this, ferrous heme–nitroxyl complexes are also considered, which have become of increasing interest recently due to their roles as intermediates in NO and multiheme nitrite reductases, and because of the potential role of HNO as a signaling molecule in mammals. In recent years, computational methods have received more attention as a means of investigating enzyme reaction mechanisms, and some important findings from these theoretical studies are also highlighted in this chapter.

Authors:
; ;  [1];  [2]
  1. Michigan
  2. (
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1324762
Resource Type:
Book
Resource Relation:
Related Information: Nitrosyl Complexes in Inorganic Chemistry, Biochemistry and Medicine II
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; crystallography; DFT calculations; electronic structure; heme proteins; HNO; iron porphyrins; nitric oxide; nitrosyl complexes; nitroxyl complexes; non-innocent ligands; spectroscopy

Citation Formats

Lehnert, Nicolai, Scheidt, W. Robert, Wolf, Matthew W., and Notre). Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology. United States: N. p., 2016. Web. doi:10.1007/430_2013_92.
Lehnert, Nicolai, Scheidt, W. Robert, Wolf, Matthew W., & Notre). Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology. United States. doi:10.1007/430_2013_92.
Lehnert, Nicolai, Scheidt, W. Robert, Wolf, Matthew W., and Notre). 2016. "Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology". United States. doi:10.1007/430_2013_92.
@article{osti_1324762,
title = {Structure and Bonding in Heme-Nitrosyl Complexes and Implications for Biology},
author = {Lehnert, Nicolai and Scheidt, W. Robert and Wolf, Matthew W. and Notre)},
abstractNote = {This review summarizes our current understanding of the geometric and electronic structures of ferrous and ferric heme–nitrosyls, which are of key importance for the biological functions and transformations of NO. In-depth correlations are made between these properties and the reactivities of these species. Here, a focus is put on the discoveries that have been made in the last 10 years, but previous findings are also included as necessary. Besides this, ferrous heme–nitroxyl complexes are also considered, which have become of increasing interest recently due to their roles as intermediates in NO and multiheme nitrite reductases, and because of the potential role of HNO as a signaling molecule in mammals. In recent years, computational methods have received more attention as a means of investigating enzyme reaction mechanisms, and some important findings from these theoretical studies are also highlighted in this chapter.},
doi = {10.1007/430_2013_92},
journal = {},
number = ,
volume = ,
place = {United States},
year = 2016,
month = 9
}

Book:
Other availability
Please see Document Availability for additional information on obtaining the full-text document. Library patrons may search WorldCat to identify libraries that hold this book.

Save / Share:
  • NO forms reversible complexes with non-heme ferrous enzymes and model complexes which exhibit unusual S = 3/2 ground states. These nitrosyl derivatives can serve as stable analogs of possible oxygen intermediates in the non-heme iron enzymes. Two complexes, Fe(Me[sub 3]TACN)(NO)(N[sub 3])[sub 2] and FeEDTA-NO, have been studied in detail using X-ray absorption, resonance Raman, absorption, magnetic circular dichroism. and electron paramagnetic resonance spectroscopies and SQUID magnetic susceptibility. These studies have been complemented by spin restricted and spin unrestricted SCF-X[Alpha]-SW electronic structure calculations. As these calculations have been strongly supported by experiment for the nitrosyl complexes, they have been extended tomore » possible oxygen intermediates. In parallel with the Fe[sup 3+]-NO[sup [minus]] complexes, the description of the intermediate obtained involves superoxide antiferromagnetically coupled to a high spin ferric center with a strong [sigma] donation of charge from the superoxide to the iron. These studies allow spectral data on the nitrosyl complexes to be used to estimate bonding differences in possible oxygen intermediates of different non-heme iron proteins and provide insight into the activation of superoxide by coordination to the ferric center for reaction or further reduction. 75 refs., 17 figs., 9 tabs.« less
  • Electron spin echo envelope modulation (ESEEM) spectroscopy has been used to study electron-nuclear interactions in the following isoelectronic S = 1/2 complexes: NO-Fe/sup II/(TPP) (TPP = tetraphenylporphyrin) with and without axial nitrogenous base, nitrosylhemoglobin in R and T states, and O/sub 2/-Co/sup II/(TPP) with and without axial base. Only the porphyrin pyrrole nitrogens contribute to the ESEEM of the 6-coordinate nitrosyl Fe/sup II/(TPP) complexes, nitrosylhemoglobin (R-state), and the nitrosyl complexes of ..cap alpha.. and ..beta.. chains. Pyrrole nitrogens in the 5-coordinate complex NO-Fe/sup II/(TPP) are coupled to weakly to unpaired spin and therefore do not contribute to the ESEEM. Amore » partially saturated T-state nitrosyl-hemoglobin does not exhibit echo envelope modulations characteristic of 6-coordinate nitrosyl species, which confirms that the proximal imidazole bond to heme iron is disrupted. Study of 6-coordinate O/sub 2/-Co/sup II/(TPP)(L) complexes (L = nitrogenous base) using /sup 14/N- and /sup 15/N-labeled ligands and porphyrins enabled a detailed analysis of coupling parameters for both pyrrole and axial nitrogens. The pyrrole /sup 14/N coupling frequencies are similar to those in NO-Fe/sup II/(TPP)(L). The Fermi contact couplings for axially bound nitrogen, calculated from simulation of ESEEM spectra for a series of O/sub 2/-Co/sup II/(TPP)(L) complexes (L = pyridine, 4-picoline, 4-cyanopyridine, 4-carboxypyridine, and 1-, 2-, and 4-methylimidazole) illustrate a trend toward stronger hyperfine interactions with weaker bases.« less
  • The crystal structures of nitrosyl-heme complexes of a prokaryotic nitric oxide synthase (NOS) from Bacillus subtilis (bsNOS) reveal changes in active-site hydrogen bonding in the presence of the intermediate N{sup {omega}}-hydroxy-L-arginine (NOHA) compared to the substrate L-arginine (L-Arg). Correlating with a Val-to-Ile residue substitution in the bsNOS heme pocket, the Fe(II)-NO complex with both L-Arg and NOHA is more bent than the Fe(II)-NO, L-Arg complex of mammalian eNOS. Structures of the Fe(III)-NO complex with NOHA show a nearly linear nitrosyl group, and in one subunit, partial nitrosation of bound NOHA. In the Fe(II)-NO complexes, the protonated NOHA N{sup {omega}} atommore » forms a short hydrogen bond with the heme-coordinated NO nitrogen, but active-site water molecules are out of hydrogen bonding range with the distal NO oxygen. In contrast, the L-Arg guanidinium interacts more weakly and equally with both NO atoms, and an active-site water molecule hydrogen bonds to the distal NO oxygen. This difference in hydrogen bonding to the nitrosyl group by the two substrates indicates that interactions provided by NOHA may preferentially stabilize an electrophilic peroxo-heme intermediate in the second step of NOS catalysis.« less
  • High-spin non-heme iron–nitrosyls are of direct interest to both the chemical and biological communities as these species exhibit interesting chemical properties and act as direct models for enzymatic intermediates. The electronic ground state of the ferrous NO complexes, {Fe–NO} 7, is best described as high-spin Fe III antiferromagnetically coupled to NO -, generating the spectroscopically observed S = 3/2 ground state. These species have been identified as catalytically relevant to a variety of NO-reducing enzymes such as bacterial nitric oxide reductase (NorBC) and flavo(rubredoxin) nitric oxide reductase (FNOR). Recently, the corresponding one-electron reduced {Fe–NO} 8 (nitroxyl) complexes have also beenmore » implicated as biologically significant species. In this review the available spectroscopic data for {Fe–NO} 7 and {Fe–NO} 8 mono- and dinuclear non-heme iron–nitrosyls are summarized, and the implications of these results with respect to the electronic structures and reactivities of these species, in particular towards NO reduction, are discussed.« less
  • Non-heme iron centers are present in the catalytic active sites of a large number of enzymes which are involved in the binding and activation of dioxygen. A member of this class, soybean lipoxygenase (SBL), catalyzes the reaction of 1,4-unsaturated lipids with dioxygen to form a hydroperoxide product. Nitrosyl complexes of enzymes serve as reversible analogues of possible dioxygen intermediates involved in catalysis. SBL-NO and other non-heme ferrous enzyme nitrosyl complexes (formulated as (FeNO){sup 7}) exhibit an unusual S = {sup 3}/{sub 2}{sub 3}EPR signal, which is also observed in (FeNO){sup 7} model complexes. A wide range of bonding descriptions havemore » appeared for these complexes, which include [Fe{sup +}d{sup 7}(S = 3/2)-NO{sup +}(S = O)], [Fe{sup 2+}d{sup 6}(S=2)-NO{sup 0}(S=1/2)] antiferromagnetically coupled, [Fe{sup 3+}d{sup 5}(S =1/2)-NO{sup {minus}}(S = 1)] ferromagnetically coupled, and [Fe{sup 3+}d{sup 5}(S = 3/2)-NO{sup {minus}}(S=0)]. In order for the NO derivative of these enzymes to be used as a probe of electron distribution related to dioxygen reactivity, a clear understanding of the electronic structure and associated spectral features of the S = 3/2 (FeNO){sup 7} unit is required. Spectroscopic techniques and theoretical methods have been used to study SBL-NO and two S = 3/2 ground-state model complexes, FeL-(NO)(N{sub 3}){sub 2}, where L = N,N{prime},N{double_prime}-trimethyl-1,4,7-triazacyclononane and FeEDTA-NO. 20 refs., 2 figs.« less