Light-induced N2O production from a non-heme iron-nitrosyl dimer

Article abstract of DOI:10.1021/ja504343t

Two non-heme iron-nitrosyl species, [Fe₂(N-Et-HPTB)(O₂CPh)(NO)₂](BF₄)₂ (1a) and [Fe₂(N-Et-HPTB)(DMF)₂(NO)(OH)](BF₄)₃ (2a), are characterized by FTIR and resonance Raman spectroscopy. Binding of NO is reversible in both complexes, which are prone to NO photolysis under visible light illumination. Photoproduction of N₂O occurs in high yield for 1a but not 2a. Low-temperature FTIR photolysis experiments with 1a in acetonitrile do not reveal any intermediate species, but in THF at room temperature, a new {FeNO}⁷ species quickly forms under illumination and exhibits a η(NO) vibration indicative of nitroxyl-like character. This metastable species reacts further under illumination to produce N₂O. A reaction mechanism is proposed, and implications for NO reduction in flavodiiron proteins are discussed.

Full text of DOI:10.1021/ja504343t

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Communication
2
Light-induced NO production from a nonheme iron-nitrosyl dimer
Yunbo Jiang, Takahiro Hayashi, Hirotoshi Matsumura, Loi H. Do,
Amit Majumdar, Stephen J. Lippard, and Pierre Moënne-Loccoz
J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/ja504343t • Publication Date (Web): 12 Aug 2014
Downloaded from http://pubs.acs.org on August 16, 2014
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Light-induced N2O production from a nonheme iron-nitrosyl dimer
Yunbo Jiang,1 Takahiro Hayashi,1, † Hirotoshi Matsumura,1 Loi H. Do,2, † Amit Majumdar,2, † Stephen J.
Lippard,2,* and Pierre MoënneꢀLoccoz,1,*
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1 Institute of Environmental Health, Oregon Health and Science University, Portland, Oregon 97239
2 Department of Chemistry, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139
Supporting Information Placeholder
(where
NꢀEtꢀHPTB
=
N,N,N’,N’ꢀtetrakis(2ꢀ(1ꢀ
ABSTRACT: Two nonheme iron nitrosyl species 1a [Fe2(NꢀEtꢀ
HPTB)(O2CPh)(NO)2](BF4)2 and 2a [Fe2(NꢀEtꢀ
ethylbenzimidazolyl))ꢀ2ꢀhydroxyꢀ1,3ꢀdiaminopropane) detailed a
full characterization of the model complex by single crystal Xꢀray
diffraction, UVꢀVis, infrared, and Mössbauer spectroscopy, and
magnetic susceptibility measurements. It also revealed 1a to be
stable in an acetonitrile solution for over a day at room temperaꢀ
HPTB)(DMF)2(NO)(OH)](BF4)3 are characterized by FTIR and
resonance Raman spectroscopy. Binding of NO is reversible in
both complexes and prone to NO photolysis under visible light
illumination. Photoproduction of N2O occurs in high yield for 1a
but not 2a. Low temperature FTIR photolysis experiments with 1a
in acetonitrile do not reveal any intermediate species, but in THF
at room temperature, a new {FeNO}7 species quickly forms under
illumination and exhibits a ν(NO) vibration indicative of nitroxylꢀ
like character. This metastable species reacts further under illumiꢀ
nation to produce N2O. A reaction mechanism is proposed, and
implications for NO reduction in flavodiiron proteins are disꢀ
cussed.
ture.11
A
mixed valent diironꢀmononitrosyl [Fe2(NꢀEtꢀ
HPTB)(OH)(NO)(DMF)2](BF4)3 (2a) complex containing the Nꢀ
EtꢀHPTB ligand was also isolated.12 Recently, an ironꢀnitrosyl
dimer, [Fe2(BPMP)(OPr)(NO)2](BPh4)2, where BPMP = 2,6ꢀ
bis[(bis(2ꢀpyridylmethyl)amino)methyl]ꢀ4ꢀmethylphenolate), (3a)
was structurally characterized and shown to produce N2O upon
either chemical or electrochemical reduction.13 This latter examꢀ
ple supports the notion that FMN could reduce the [{FeNO}7]2
complex in FDP and thus allow catalytic turnover without redox
cycling of the iron(II) centers. Nevertheless, activating the
{FeNO}7 unit for attack by a second NO to produce a transient
hyponitrite remains a valid alternative for the reduction of NO to
N2O.
Nitric oxide (NO) plays an important role in cellular signaling in a
wide range of biological processes. NO can also be toxic when
present at high concentration, and it participates as a key immune
defense agent against invading pathogens. Accordingly, a variety
of detoxifying enzymes has evolved in pathogens, and underꢀ
standing their microbial NO defense mechanisms may provide
new strategies for controlling infections.1ꢀ7 In anaerobic environꢀ
ments, NO detoxification occurs via the twoꢀelectron reduction of
NO to form nitrous oxide (N2O). Flavodiiron proteins (FDPs) are
flavinꢀcontaining, NOꢀdetoxifying enzymes with an active site
containing a nonheme diiron cluster (see chart 1).4 In most FDPs,8
each metal ion is coordinated by two His ligands and one terminal
monodentate carboxylate group from either Asp or Glu; a bridgꢀ
ing bidentate Asp and a waterꢀderived ligand (oxo or hydroxo)
complete the coordination sphere. An open coordination site reꢀ
mains on each iron(II). Both monoꢀ{FeNO}7 and dinitrosyl
[{FeNO}7]2 FDP adducts have been characterized.9,10 Experiꢀ
ments with a flavinꢀfree form of the enzyme reveal that N2O proꢀ
duction can occur without the flavin mononucleotide (FMN) coꢀ
factor.10 An exceptionally low frequency ν(NO) band at 1681 cmꢀ
Chart 1. Structural comparison of complexes 1, 1a, 2, 2a,
3a, and the active site of FDP
1
was detected in mononitrosyl complexes of FMNꢀfree and
FMNꢀcontaining enzymes, which suggests a nitroxylꢀlike configuꢀ
ration of the {FeNO}7 unit.9 Electrostatic interaction of this niꢀ
troxylꢀlike group with the adjacent FeII center could prime the
mononitrosyl complex for electrophilic attack by a second NO.9
In contrast, the [{FeNO}7]2 adduct persists in the FMNꢀfree enꢀ
zyme, suggesting that it either corresponds to an inactive state,10
or may be poised for reduction by FMN in the flavinated enꢀ
zyme.4
Nonheme iron synthetic models provide insight into the catalytic
mechanism of FDP proteins. The first report of a nonheme diiron
dinitrosyl compound, 1a [Fe2(NꢀEtꢀHPTB)(O2CPh)(NO)2](BF4)2
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Here we report that production of N2O by 1a can proceed under
illumination with white light at room temperature and at 15 K. We
also show that this process is preceded by simple photodissociaꢀ
tion of NO from the ironꢀnitrosyl dimer. In the case of 2a, photoꢀ
dissociation also occurs but the resulting NO does not react furꢀ
ther.
The chromophoric {FeNO}7 units in 1a and 2a display distinctive
nitrosylꢀtoꢀiron LMCT absorption bands, and these NO adducts in
acetonitrile solutions easily revert to diiron(II) compounds after
purging with Ar (Figure 1). The resonance Raman (RR) spectrum
of 1a obtained with 458ꢀnm laser excitation shows a ν(FeNO)
band at 492 cmꢀ1 with unlabeled NO that shifts to 486 with 15NO
and to 478 cmꢀ1 with 15N18O (Figure 2). Nearly identical ν(FeNO)
frequencies are observed in the RR spectra of 2a, which is conꢀ
sistent with the structural similarity of these [FeNO] units obꢀ
served by crystallography.11,12 Additional vibrations in the lowꢀ
frequency region of the RR spectra of 2a cannot be assigned with
certainty at this time, but these modes do not shift with NO labelꢀ
ing or with the addition of 20% D2O to the acetonitrile solutions
and are therefore unrelated to the nitrosyl or hydroxy ligands.
1654 cmꢀ1 is consistent with a lengthening of the C=O bond upon
coordination of DMF to metal ions.
1a
14NO
1752
15NO
2a
1784
1810
14NO
15NO
1775
1727
1706
9
15N18O
15N18O
0.02
Abs.
0.02
Abs.
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DMF
1600
1700
1800
1900
1600
1700
1800
1900
Wavenumber / cm-1
Wavenumber / cm-1
Figure 3. Room temperature FTIR spectra of 1a (left panel) and
2a (right panel) at room temperature ([1a] = 18 mM, [2a] = 20
mM).
Lowꢀtemperature FTIR spectra of 1a reproduce the ν(NO) values
observed at room temperature, but those of 2a display a signifiꢀ
cant decrease in the intensity of the ν(NO) modes that is indicaꢀ
tive of a diminished NO binding affinity at cryogenic temperaꢀ
tures (Figure S1). Previous differential FTIR photolysis experiꢀ
ments indicate that, at least within the active sites of metalloproꢀ
teins, nonheme ironꢀnitrosyl complexes can be trapped as photoꢀ
dissociated states following illumination with white light at cryoꢀ
genic temperatures.9,10,15,16 Based on these findings, "dark" minus
"illuminated" FTIR difference spectra can be used to isolate
ν(NO) bands emanating from {FeNO}7 species as positive feaꢀ
tures in the 1700ꢀcmꢀ1 region, whereas the photolyzed NO group
is detected as a weak negative band near 1870 cmꢀ1. Typically, the
buildꢀup of the photolyzed population occurs during the first few
minutes of whiteꢀlight illumination, and further illumination does
not produce any additional spectral changes. Geminate rebinding
of the photolyzed ligand requires a slight increase in sample temꢀ
perature (to ~40ꢀ80 K), and repeating the photolysis procedure at
15 K confirms the complete reversibility of these processes. Reꢀ
versible photorelease of NO from a nonheme {FeNO}7 synthetic
complex at room temperature was also reported recently.17
1200
600
520
800
400
0
400
200
0
620
degassing
with Ar
614
2a
1a
2nd exposure
to NO
1
2
500
600
700
800
500
600
700
800
Wavelength / nm
Wavelength / nm
Figure 1. Electronic spectra of 1 and 1a (left panel) and 2 and 2a
(right panel) in acetonitrile at room temperature. Also shown are
the effects of purging solutions of 1a and 2a with Ar for 3 min
(dashed lines) before repeated exposure to NO.
581
492
492
589
2a 14NO
1a 14NO
1a 15NO
1a 15N18O
550
486
479
486
478
2a 15NO
Lowꢀtemperature FTIR photolysis experiments with 2a reproduce
the behavior displayed previously by nonheme protein NO adꢀ
ducts (Figure 4). Specifically, the spectra show that the {FeNO}7
species in 2a is photolabile and that further illumination does not
produce any additional changes. In contrast, 1a reveals unique
photoreactivity. The lightꢀinduced FTIR difference spectrum of
1a at 15 K exhibits a positive band at 1787 cmꢀ1 and a weak negaꢀ
tive band at 1867 cmꢀ1 that, based on 15NOꢀisotope shifts, are
assigned to the ν(NO) of {FeNO}7 and free NO, respectively
(Figure 4). Further illumination at 15 K produces additional specꢀ
tral changes, including the appearance of a negative signal at 2239
cmꢀ1 that shifts to 2168 and 2162 cmꢀ1 with 15NO and 15N18O,
respectively. (Figures 4 and S2). The 2239ꢀcmꢀ1 signal and its
accompanying isotope shifts are characteristic of the ν(NN) mode
of N2O. This process is irreversible and can result in the complete
consumption of 1a after prolonged illumination at 15 K (Figure
S3). FTIR samples prepared by exposing 1 to substochiometric
levels of NO produce lightꢀinduced difference spectra equivalent
to those obtained with 1a, indicating that two NO molecules bind
in a cooperative fashion to 1 without significant buildup of a moꢀ
nonitrosyl species (Figure S4). Comparing the integration of the ν
(NN) signal generated from 1a after illumination at 15 K with
titration curves generated using N2Oꢀsaturated acetonitrile sugꢀ
gests that the formation of N2O proceeds with a high yield (~90%
at 15 K, Figure S5). These FTIR experiments indicate that whiteꢀ
light illumination of 1a initially produces a population of cagedꢀin
dissociated NO that can react with the diiron complex to subseꢀ
2a 15N18O
1
CH3CN
2
CH3CN
450
600
750
450
600
750
Raman shift / cm-1
Raman shift / cm-1
Figure 2. RR spectra of 1 and 1a (left panel) and 2 and 2a (right
panel) at room temperature (λexc = 458 nm, [1], [1a] = 2 mM, [2],
[2a] = 2.5 mM).
Roomꢀtemperature FTIR spectra of 1a and 2a in acetonitrile show
ν(NO) modes at 1784 and 1810 cmꢀ1, respectively, with the exꢀ
pected downshifts with 15NO and 15N18O (Figure 3). These ν(NO)
values are consistent with earlier reports11,12 and with the S =3/2
{FeNO}7 description of nonheme [FeNO] units.14 As reported
previously, 1a is composed of two {FeNO}7 units, which have
identical coordination environments and exhibit the same set of
vibrational frequencies. The ν(NO) band in 2a is upshifted by 26
cmꢀ1 relative to that in 1a and is significantly broadened, presumꢀ
ably because of the heterogeneity in the binding geometry and
environment of the nitrosyl group in 2a. The upshift of the ν(NO)
may result from substitution of the bridging benzoate in 1a by two
DMF ligands in 2a. Amideꢀlike vibrations from DMF are obꢀ
served for 2a at 1654 and 1677 cmꢀ1. The latter frequency matches
that of free DMF in acetonitrile, whereas the lower frequency at
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quently generate N2O under further illumination. Because this
reaction occurs at 15 K, an intermolecular process between two or
more 1a diiron complexes can be ruled out. In addition, decreasꢀ
ing the concentration of 1a does not significantly affect the illuꢀ
mination time required for the formation of N2O (data not shown).
cy is unusually low for a nonheme {FeNO}7 species and is remiꢀ
niscent of the 1681 cmꢀ1 band seen in the FTIR spectra of the
mononitrosyl adducts of the flavodiiron protein from Thermotoga
maritima, which also shows a 30ꢀcmꢀ1 downshift with 15NO. Such
nitrosylꢀlike character may result from semiꢀbridging interactions
of the NO group that render these mononitrosyl complexes susꢀ
ceptible to sideꢀon electrophilic attack by a second NO to produce
transient hyponitrite complexes that subsequently decay to form
N2O. Theoretical analyses of NO reduction in FDPs favor a
mechanism where the formation of a partiallyꢀreduced NO group
in a diironꢀmononitrosyl complex allows for the attack by a seꢀ
cond NO to form the NꢀN bond.18
Because the reduction of two NO molecules to N2O requires two
electrons, the other product of the photoreaction is likely to be a
diiron(III) complex. EPR spectra of 1a obtained after illumination
at 15 K showed no signal that could be assigned as iron(III) cenꢀ
ters (data not shown), suggesting antiferromagnetic coupling beꢀ
tween the two iron(III) centers. Resonance Raman spectroscopy
was used to determine whether a (ꢀꢀoxo)diiron(III) product is
formed after the release of N2O, but the results were inconclusive.
9
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1787
Abs
0.03 1786
ꢁabs
0.0005
1796
ꢁ
2a
1a 14NO
1a
illumination
14NO
14NO
1781
1873
0 min
"dark" minus "1-min illuminated"
1 min
2 min
2223
1760
1838
1867
2239
0.02
15NO
15N18O
2200
"dark" minus "7-min illuminated"
1751
1750
15NO
1695
"dark" minus "1-min illuminated"
1717
1789
1835
2168
"dark" minus "7-min illuminated"
1600
1800
2000
1600
1800
2000
2200
3 min
7 min
Wavenumber / cm-1
x2
Wavenumber / cm-1
1747
15 min
Figure 4. 15ꢀK lightꢀinduced FTIR difference spectra of 1a (left
panel, difference spectra for 1ꢀ and 7ꢀmin illuminations) and 2a
(right panel, difference spectra after completion of the photoproꢀ
cess). ([1a] = 18 mM, [2a] = 20 mM).
0 min
1 min
1a 15NO
2154 2 min
1665
Production of N2O from 1a under illumination is also observed at
room temperature in acetonitrile and in THF, although with reꢀ
duced yields compared to those at low temperature (15% and
26%, respectively). FTIR spectra of 1a in THF collected in the
dark and after consecutive 1ꢀmin illuminations reveal a loss of the
ν(NO) at 1781 cmꢀ1 in favor of a signal at 1695 cmꢀ1 that shifts to
1665 cmꢀ1 with 15NO, and a minor intensity gain in the ν(NN) of
N2O at 2223 cmꢀ1 (Figure 5, top panel). After this first two min of
irradiation, subsequent illuminations lead to a growth of the
ν(NN) signal and concurrent decreases in ν(NO) and the peak at
1695 cmꢀ1 (Figure 5, lower panel). Differential FTIR spectra for
the initial and later phases of the photoprocess also help isolate
lightꢀinduced features below 1600 cmꢀ1 that are insensitive to NOꢀ
isotope substitution and that are likely to reflect minor perturbaꢀ
tions of vibrational modes from the NꢀEtꢀHPTB ligand (Figure
S6).
Timeꢀdependent traces for the decay of the 1781ꢀcmꢀ1 ν(NO) band
from 1a and the growth of the 2223ꢀcmꢀ1 ν(NN) band from N2O
are shown in Figure 6. The intensity gain at 2223ꢀcmꢀ1 fits a single
exponential rate of 0.2 minꢀ1. The time trace for the intensity loss
of the ν(NO) of 1a requires a biexponential fit with rate constants
of 1.1 and 0.1 minꢀ1. The fast phase represents 26% of the overall
amplitude of the signal change and matches the yield of N2O;
presumably, the slower phase reflects side reactions that do not
produce N2O. Analyzing the time progression of the 1695ꢀcmꢀ1
signal is less reliable because of its weak intensity and because
expected diiron(III) products are likely to give weak signals below
1700 cmꢀ1. Nevertheless, it is worthwhile to compare the progresꢀ
sion of this signal by means of a simulation curve for an intermeꢀ
diate species with formation and decay rates that correspond to
the 1.1 minꢀ1 decay of 1a and the 0.2 minꢀ1 formation of N2O
(Figure 6).
3 min
7 min
15 min
x2
1600 1700 1800
2100 2200
Wavenumber / cm-1
Figure 5. Room temperature FTIR spectra of 1a prepared in THF
with 14NO (top traces) or 15NO (lower traces). Spectra were colꢀ
lected in the dark and after a total of 1ꢀ, 2ꢀ, 3ꢀ, 7ꢀ and 15ꢀmin
illumination periods.
100
80
100
80
60
40
20
0
1a decay
k1 = 1.1 min-1 (26 %)
k2 = 0.1 min-1 (65 %)
60
N2O formation
k1 ~ 0.2 min-1
40
ꢁabs at
20 1695 cm-1
0
0
4
8
12
16
Illumination time (min)
Figure 6. Progression of the FTIR intensity for ν(NO) of 1a
(black squares), ν(NN) of N2O (red circles) and for the 1695 cmꢀ1
signal (open blue squares) (see Supporting Information for deꢀ
tails).
The 1695ꢀcmꢀ1 FTIR signal and its 30ꢀcmꢀ1 downshift with 15NO
are consistent with a ν(NO) from an ironꢀnitrosyl complex with
[FeIIIꢀNOꢀ] nitroxylꢀlike character. However, this ν(NO) frequenꢀ
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fellowship for H.M., and a Vertex pharmaceutical scholarship for
T.H. We thank Mik Minier for helpful discussions.
Scheme 1. Possible mechanistic steps for the light-induced
production of N2O from 1a19
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REFERENCES
From these data, we propose that the metastable nitroxylꢀlike
mononitrosyl complex observed in THF at room temperature is a
competent intermediate in the lightꢀinduced formation of N2O via
electrophilic attack by a second NO molecule (Scheme 1).
Whereas light activation is not required for catalytic activity in
FDPs, and a recent preꢀsteady state study of FDP favors a diferꢀ
rousꢀdinitrosyl intermediate as the precursor to NꢀN bond forꢀ
mation20, characterizing nonꢀequilibrium states in synthetic modꢀ
els provides insight on possible reaction mechanisms and transiꢀ
tion states that enzymes may stabilize to optimize their catalytic
activity. Efforts are underway in our laboratories to further charꢀ
acterize this chemistry using monochromatic laser illuminations
as a possible mean to better control the formation and decay steps
of the 1695ꢀcmꢀ1 species. In addition, we will explore the possible
role of protons in the reduction of NO as we did previously for the
dioxygen activation reaction of these diiron models.21
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residue only (Frazao, C., Silva, G., Gomes, C. M., Matias, P., Coelho, R.,
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(10) Hayashi, T.; Caranto, J. D.; Wampler, D. A.; Kurtz, D. M., Jr.;
MoënneꢀLoccoz, P. Biochemistry 2010, 49, 7040.
(11) Feig, A. L.; Bautista, M. T.; Lippard, S. J. Inorg. Chem. 1996, 35,
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(19) The FTIR data do not distinguish whether visible illumination of 1a
dissociates both nitrosyl ligands to produce a dynamic population of
dinitrosyl and diferrous states or whether mononitrosyl species are
produced after dissociation of only one NO molecule.
(20) Caranto, J. D.; Writz, A.; Hendrich, M. P.; Kurtz, B. M., Jr. J. Am.
Chem. Soc. 2014, 136, 7981.
ASSOCIATED CONTENT
Supporting Information
FTIR spectra of 1a and 2a at 15 K; lightꢀinduced FTIR difference
spectra of 1a prepared with NO, 15NO, and 15N18O; room temꢀ
perature UVꢀvis spectra of 1a before and after prolonged illumiꢀ
nation at 15 K; 15ꢀK FTIR spectra of N2O in acetonitrile; room
temperature FTIR difference spectra of 1a prepared with NO and
15NO, after 2ꢀmin and 15ꢀmin illumination periods. This material
is available free of charge via Internet at http://pubs.acs.org.
AUTHOR INFORMATION
Corresponding Author
*moennelo@ohsu.edu, lippard@mit.edu
Present Addresses
†T.H. Department of Synthetic Chemistry and Biological Chemꢀ
istry, Graduate School of Engineering, Kyoto Univeristy, Katsura,
Kyoto 615ꢀ8510, Japan.
†L.H.D. Department of Chemistry, University of Houston, Houꢀ
ston, Texas 77204
†A.M. Department of Inorganic Chemistry, Indian Association for
the Cultivation of Science, Jadavpur, Kolkataꢀ700032, India.
Notes
The authors declare no competing financial interests.
(21) Do, L. H.; Hayashi, T.; MoënneꢀLoccoz, P.; Lippard, S. J. J. Am.
Chem. Soc. 2010, 132, 1273.
ACKNOWLEDGMENT
This work was supported by NIH grants GM074785 (P.M.L.) and
GM032114 (S.J.L.) from the National Institute of General Medi
cal Science, the National Science Foundation (S.J.L.), a JSPS
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