Photochemical NO release from nitrosyl RuII complexes with C-bound imidazoles

Article abstract of DOI:10.1016/j.ica.2008.02.052

The series of nitrosyl complexes trans-[Ru(NH₃)₄L(NO)]Cl₃, L = caffeine, theophylline, imidazole and benzoimidazole in position trans to NO were prepared and their photochemical properties studied. All complexes showed nit

Full text of DOI:10.1016/j.ica.2008.02.052

Inorganica Chimica Acta 361 (2008) 2929–2933
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Photochemical NO release from nitrosyl RuII complexes with C-bound imidazoles
Alda K.M. Holanda a, Francisco O.N. da Silva a, Jackson R. Sousa a, Izaura C.N. Diógenes a,
Idalina M.M. Carvalho a, Ícaro S. Moreira a, Michael J. Clarke b, Luiz G.F. Lopes a,
*
a Departamento de Química Orgânica e Inorgânica, Universidade Federal do Ceará, c.x. Postal 12200, Cep 60455-960 Fortaleza CE, Brazil
b Merkert Chemistry Center, Boston College, Chestnut Hill, MA 02467, USA
a r t i c l e i n f o
a b s t r a c t
Article history:
The series of nitrosyl complexes trans-[Ru(NH3)4L(NO)]Cl3, L = caffeine, theophylline, imidazole and
benzoimidazole in position trans to NO were prepared and their photochemical properties studied. All
complexes showed nitric oxide (NO) release under light irradiation at 330–440 nm. Quantum yields
for [Ru(NH3)4L(H2O)]3+ formation (/Ru(III)) were sensitive to the natures of L, kirr and pH. The major prod-
uct of the irradiation of trans-[Ru(NH3)4L(NO+)]3+ is the trans-[RuIII(NH3)4L(Cl)]2+ and NO as suggested by
UV–Vis, electrochemical, and FTIR techniques.
Received 18 October 2007
Received in revised form 15 February 2008
Accepted 23 February 2008
Available online 4 March 2008
Ó 2008 Elsevier B.V. All rights reserved.
Keywords:
NO release
Photochemical study
Ruthenium complexes
1. Introduction
syl complexes of the type trans-[Ru(NH3)4L(NO)]3+ (L = 4-pic, imN,
L-hist, py, nic, pz, isn, 4-acpy and P(OEt)3). They observed that the
In recent years, a great number of studies concerned with NO
activity in biological systems have been published [1–6]. In this
field, ruthenium complexes have been studied as NO scavengers,
or reciprocally, their nitrosyl complexes have been investigated as
NO delivery systems toward biological targets [7–20], with regard
to the design and evaluation of a number of new transition metal
complexes as NO carriers for biological applications [21–26]. Conse-
quently, metalonitrosyl complexes as agents potentially capable of
releasing NO in vivo have recently become an active area of research
[15,27–31]. One strategy is to employ a precursor that displays rel-
atively low thermal reactivity, but is photochemically active, to
yield NO when subjected to electronic excitation [10,32]. In this
context, the chemical and photochemical reactions of various metal
nitrosyl complexes and of related species are being investigated
[10,15,27–29,32,33] with the goal of developing models for NO
delivery agents in pharmaceutical applications. Complexes of the
type trans-[Ru(NH3)4(L)NO+]3+ are robust in aqueous solution and
are easily activated to release NO through electrochemical
[15,28,34,35], chemical [15,36] or photochemical monoelectronic
reduction. In this area, the photochemical behavior of several nitro-
syl metal complexes and related species [15,37,38] have been re-
ported. An interesting system is that of ruthenium ammines,
which can be modified to exhibit desired properties [12,39]. Franco
et al. [15,32] reported on the photochemical behavior of some nitro-
photolysis at higher energy than 310–370 nm light leads to the dis-
sociation of NO and trans-[Ru(NH3)4L(H2O)]3+ as products, Eq. (1).
However, the photochemistry of most nitrosyl ruthenium com-
plexes, which could act as NO delivery agents under light stimula-
tion, have been described mainly in acidic medium [15,32,33,38],
due to the nitro–nitrosyl equilibrium in basic solution
hm
trans-½RuðIIÞðNH3Þ LðNOþÞꢀ !trans-½RuðIIIÞðNH3Þ LðH2OÞꢀ3þ þNO0
3þ
4
4
ð1Þ
Contrarily, Richter-Addo have observed that the irradiation of
some iron–porphyrin containing nitrosyl and nitro ligands, at
300 < k < 500 nm, induces the linkage isomerism of both nitro and
nitrosyl ligands [40,41]. In these systems it was observed a shift in
the mNO around 150 cmꢁ1 suggesting such isomerism [40,41].
In a previous article [34], we showed that the complexes trans-
[Ru(NH3)4L(NO)]Cl3 (L = C-bonded imidazole, C-bonded caffeine
and C-bonded theophiline) are stable at physiological pH but rap-
idly release NO after NO+/NO reduction. This article describes the
photochemical properties of the trans-[Ru(NH3)4L(NO)]3+ com-
plexes where L is carbon-bound imidazole, caffeine and theophyl-
line (Fig. 1).
2. Experimental
Ultrahigh purity water purified with a Millipore system was
used throughout. RuCl3 ꢂ (H2O)x, imidazole, caffeine, benzoimidaz-
ole and theophylline were obtained from Aldrich and used without
* Corresponding author. Tel.: +55 85 33669435; fax: +55 85 33669978.
E-mail address: lopeslu@dqoi.ufc.br (L.G.F. Lopes).
0020-1693/$ - see front matter Ó 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.ica.2008.02.052

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A.K.M. Holanda et al. / Inorganica Chimica Acta 361 (2008) 2929–2933
with this assignment, these bands shifted to lower energy with
increasing pH as the imidazole proton was ionized, thereby
increasing electronic density on the RuII.
Fig. 2 presents typical changes in the UV–vis spectra of a solu-
tion of trans-[Ru(NH3)4L(NO)]3+ during the photolysis. The appear-
ance of the LMCT band in the visible region for all complexes at
different pHs values (Table 1) is clearly observed, typical of the
trans-[Ru(NH3)4LCl]2+ species generated after the release of NO,
since the photolysis experiments were carried out in chloride med-
ium [44]. Also, a change in color is observed from yellow to purple
for caffeine and theophylline complexes, characteristic of the RuIII
species [44].
Fig. 1. Structures of (A) trans-[Ru(NH3)4(imidazole)(NO)]3+ and (B) R = H trans-[R-
u(NH3)4(theophylline)(NO)]3+, R = CH3 trans-[Ru(NH3)4(caffeine)(NO)]3+
.
further purification. trans-[Ru(NH3)4L(NO)]Cl3 (L = imidazole, caf-
feine, theophylline and benzoimidazole) [34,35] complexes were
prepared according to literature procedures. Anal. Calc. for imidaz-
ole: C, 9.63; H, 4.28; N, 26.23. Found: C, 9.62; H, 4.32; N, 26.20%.
Anal. Calc. for caffeine: C, 19.21; H, 4.40; N, 25.21. Found: C,
19.02; H, 4.43; N, 24.98%. Anal. Calc. for theophylline: C, 17.28;
H, 4.12; N, 25.94. Found: C, 17.02; H, 4.18; N, 25.75%. Anal. Calc.
for benzoimidazole: C, 11.20; H, 2.40; N, 13.00. Found: C, 10.95;
H, 2.36; N, 13.23%.
The electrochemical experiments were performed at room tem-
perature by using Ag/AgCl (BAS, 3.50 mol Lꢁ1 KCl) as reference
electrode.
UV–Vis spectra were recorded on an HP-8453 diode-array spec-
trophotometer. 1H and 13C NMR spectra were obtained in 5 mm
NMR tubes on a Bruker 300 MHz FT spectrometer in D2O. IR spec-
tra were obtained in KBr pellets on a Shimadzu 283-B FT-IR
spectrophotometer.
The release of NO as a photoproduct was confirmed by differen-
tial pulse voltammetry (DPV). Fig. 3 shows the differential pulse
voltammogram obtained after 330 nm irradiation of trans-
[Ru(NH3)4(caffeine)(NO)]3+
. The anodic process observed at
0.80 V was assigned to the oxidation of the released NO. This
process was not observed when the solution of trans-[Ru(NH3)4-
(caffeine)(NO)]Cl3 was kept in the dark. Moreover, well-defined
waves appeared at potentials 0.114, 0.168, ꢁ0.083 and 0.053 V
for L = caffeine, theophylline, imidazole and benzoimidazole,
respectively. This wave is assigned to the RuII ? RuIII oxidation
process for trans-[Ru(NH3)4LCl]2+, which must be generated as a re-
sult of dissociation of NO from the original compound [34]. The
same behavior was found for several nitrosyl compounds reported
in the literature [12,45–48].
Photolysis experiments were carried out at 25.0 0.3 °C in
1.0 cm path length quartz cells capped with a rubber septum.
The complexes solutions were prepared in an 0.10 mol Lꢁ1 of NaCl
to form the characterized product as trans-[Ru(NH3)4LCl]2+. The
solutions (10ꢁ4 mol Lꢁ1 initial complex concentration) were deaer-
ated by bubbling with argon prior to photolysis and stirred during
irradiation. The solutions were photolyzed to approximately 5%
reaction to minimize inner filter effects. Simultaneous dark reac-
tions were carried out with identical solutions. As analyzed from
their UV–Vis spectra, these samples were stable in the dark on a
time scale longer than that of the photochemical experiments.
Photoproducts were identified by UV–Vis and voltammetric mea-
surements by comparison with the respective data of separately
prepared ruthenium complexes. Quantitative analyses were made
by monitoring electronic spectral changes, and it was assumed that
the quantum yield for appearance of product is equal to that of dis-
appearance of the starting material, consistent with the stoichiom-
etry indicated in Eq. (1). Quantum yields were determined from
initial spectral changes, monitoring the appearance of the trans-
[Ru(NH3)4LCl]2+ species, and were plotted versus reaction percent-
age and extrapolated back to 0% reaction to minimize inner filter
effects. The reported quantum yields are the average of, at least,
three independent experiments.
1.0
0.8
0.6
0.4
0.2
0.0
300
400
500
600
700
800
Wavelength
Fig. 2. Spectral changes of the absorption spectrum accompanying photolysis of
trans-[Ru(NH3)4(theophylline)(NO)]3+ in phosphate buffer solution, pH 7.1, l = 1.-
0 mol Lꢁ1, kirr = 330 nm.
Table 1
UV–Vis spectra data for trans-[Ru(NH3)4LCl]2+ in different pHs values
3. Results and discussion
L
pH
k (nm)
Caffeine
3.4
4.4
7.1
569
605
648
Studies of the electronic structure and electronic spectroscopy
of transition metal nitrosyl compounds have been directed to-
wards establishing the link between the molecular orbital descrip-
tion and the physical and chemical properties, especially for these
complexes as metallodrugs and in catalysis [42]. The absorption
spectra of the compounds presented here showed bands at 260
and 300 nm (Fig. 2) attributed to p ? p* transitions on the aromatic
ligands, and at 446 and 456 nm, which are assigned to p*(NO)
dp(RuII) metal to ligand charge-transfer (MLCT) transitions. These
assignments are taken by analogy to those observed for trans-
[Ru(NH3)5(NO)]3+ and related complexes [15,28,43]. Consistent
Theophylline
Imidazole
3.4
4.4
7.1
564
577
603
3.4
4.4
7.1
449
474
476
Benzoimidazole
3.4
4.4
7.1
443
475
498

A.K.M. Holanda et al. / Inorganica Chimica Acta 361 (2008) 2929–2933
2931
The process at +0.8 V is attributed the free NO0 ? NO+ oxidation
[28]. In addition, the photolysis of the compound trans-[Ru(NH3)4-
(caffeine)(NO)]3+ dispersed in KBr was performed and monitored
by IR spectroscopy (Fig. 4). Comparison of the IR spectra acquired
before and after irradiation showed a decrease in the intensity of
the mNO+ peak at 1905 cmꢁ1 and the appearance of a new peak at
1870 cmꢁ1, which can be assigned to mNO0 stretching mode
[6,15,49]. The spectrum of the final product, after exhaustive
photolysis, is identical for the trans-[Ru(NH3)4(caffeine)(Cl)]Cl2
(compared with an authentic sample) in agreement with the
formation of the RuIII species upon photolysis. Also, a change in
color is observed during the irradiation of the complexes from yel-
low to purple for L = caffeine and theophylline and from yellow to
orange for L = imidazole. These colors are characteristic of the
trans-[Ru(NH3)4(L)(Cl)]2+ complex ion. There are several studies
in the literature concerning the photochemical studies of the
metal–nitrosyl complexes. Several authors [12,45,47,48,50,51]
have carried out photochemical studies of several ruthenium
nitrosyl complexes and had observed that the irradiation at
-2
-4
-6
-8
-10
-12
Table 2
Quantum yield values (RuIII) for the photolysis of trans-[Ru(NH3)4L(NO)]3+ in aqueous
1.0
0.8
0.6
0.4
0.2
0.0
solution
Potential, V
III
Ru
L
kIrr (nm)
pH
/
Fig. 3. Differential pulse voltammogram of trans-[Ru(NH3)4(caffeine)(NO)]3+ in KCl
solution, pH 7.0; l = 1 mol Lꢁ1 at a glassy carbon electrode with platinum wire as an
auxiliary electrode and SCE as the reference electrode. The voltammogram was
taken after irradiation at 330 nm. Solid line: starting material, dashed line: after
irradiation. Potential scan started at ꢁ0.1 V with anodic sweep.
Caffeine
330
330
330
410
410
410
440
440
440
3.4
4.4
7.1
3.4
4.4
7.1
3.4
4.4
7.1
0.51 0.05
0.40 0.05
0.21 0.05
0.20 0.05
0.16 0.05
0.11 0.05
0.20 0.05
0.15 0.05
0.11 0.05
100
80
Theophylline
330
330
330
410
410
410
440
440
440
3.4
4.4
7.1
3.4
4.4
7.1
3.4
4.4
7.1
0.68 0.05
0.41 0.05
0.25 0.05
0.32 0.05
0.30 0.05
0.28 0.05
0.28 0.05
0.25 0.05
0.14 0.05
60
Imidazole
330
330
330
410
410
410
440
440
440
3.4
4.4
7.1
3.4
4.4
7.1
3.4
4.4
7.1
0.25 0.05
0.30 0.05
0.35 0.05
0.12 0.05
0.13 0.05
0.15 0.05
0.030 0.05
0.030 0.05
0.050 0.05
40
2050
2000
1950
1900
1850
1800
1750
Wave Number, cm-1
Benzoimidazole
330
330
330
3.4
4.4
7.1
0.0050 0.05
0.0060 0.05
0.0070 0.05
Fig. 4. Infrared spectra changes of trans-[Ru(NH3)4(caffeine)(NO)]3+ dispersed in
KBr as function of the irradiation process under 330 nm. Solid line: starting mate-
rial, dashed line: after photolysis.
a
b
g = 2.00
g = 2.00
2.20 2.15 2.10 2.05 2.00 1.95 1.90 1.85
g
1.90
2.15
2.10
2.05
2.00
1.95
g
Fig. 5. EPR spectrum of (a) trans-[Ru(NH3)4(caffeine)(NO)]3+ complex, kirr = 355 nm and (b) trans-[Ru(NH3)4(theophylline)(NO)]3+ complex, kirr = 440 nm, in water/ethylen-
eglycol (50%) solution, and 144 K.

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A.K.M. Holanda et al. / Inorganica Chimica Acta 361 (2008) 2929–2933
a
0.7
0.6
0.5
0.4
0.3
0.2
b
0.30
0.25
0.20
0.15
0.10
3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0
3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0
pH
pH
c
0.25
0.20
0.15
0.10
0.05
3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5
pH
Fig. 6. Plot of ØRuIII vs pH for the of trans-[Ru(NH3)4L(NO)]3+ in aqueous solution. jL = caffeine, sL = theophylline, NL = imidazole. (a) kirr = 330 nm, (b) kirr = 410 nm and (c)
kirr = 440 nm.
300 < k < 500 nm range produces the NO release from the starting
material leading to the formation of the RuIII-solvent species. The
data collected in this work suggest that the title complexes behave
by a similar mechanism.
The lowest quantum yield was found for the complex, where
L = benzoimidazole, the worst p-acceptor, and the highest quan-
tum yield was observed for L = theophylline, the best p-acceptor.
The irradiation of the complex, where L is benzoimidazole with
light at kirr > 350 nm did not lead to observable photochemistry
under the conditions used. Similar behavior was observed for other
complexes, where L is a strong r-donor such as ImN, L-Hist, py and
Isn [32].
For the compounds with L = caffeine and theophylline a de-
crease in /NO was observed with an increase in the pH of the
photolyzed solution. This can probably be explained by the more
Fig. 5 shows the in situ EPR spectrum of a solution containing
the trans-[Ru(NH3)4L(NO)]3+ after irradiation at 355 nm for L = caf-
feine and 440 nm for L = theophylline revealing the presence of a
paramagnetic photoproduct. The g = 2.00 value and observation
of the hyperfine splitting in the EPR spectrum of trans-
[Ru(NH3)4(caffeine)(NO)]3+ after irradiation suggest the formation
of a paramagnetic species containing the reduced nitric oxide rad-
ical coordinated to the metal center [52].
pronounced p-acceptor character of the protonated
L ligand
Reduction of coordinated NO+ in trans-[RuIICl(NO+)(cyclam)]2+
[49] results in trans-[RuIICl(cyclam)(NO0)]+, which undergoes a rel-
atively fast chloride labilization (k = 2.0 sꢁ1 at 8 °C) resulting in
increasing the relative charge on the RuII, thereby making it more
difficult to transfer electron density from RuII to NO+ through a
MLCT transition (see Fig. 6).
trans-[RuII(H2O)(cyclam)(NO0)]2+
,
which in turn releases NO0
slowly (k = 6.4 ꢃ 10ꢁ4 sꢁ1 at 25 °C). DFT calculations for several
RuNO complexes have shown [32,53,54] that the (dp ? NO+) MLCT
transitions lie around 330 and 450 nm, consequently the photo-
products after irradiation in this range should be trans-
[RuIII(NH3)4L(H2O)]3+ and NO. Consequently, since, in these exper-
iments, the complexes were irradiated in a (dp ? NO+) MLCT band,
it is believed that the observed EPR spectra correspond to coordi-
nated NO0 radical rather than that of a solvated one [39].
4. Conclusion
We have shown that the photolysis of trans-[Ru(NH3)4-
L(NO)]Cl3, where L is caffeine, theophylline, imidazole and benzo-
imidazole, produces NO when it is irradiated with light at
330–440 nm range. The major product of the irradiation of trans-
[Ru(NH3)4L(NO+)]3+ is an paramagnetic intermediate that in
chloride aqueous solution releases NO to produce trans-
[Ru(NH3)4L(Cl)]2+
. The quantum yield observed for the NO
formation involved in the photolysis of trans-[Ru(NH3)4L(NO)]3+
decreases with the p acceptor character of L, trans to NO+, which
is consistent with an increase in charge on NO+.
3.1. Quantum yields
Table 2 and Fig. 6a–c summarize the quantum yields for the
photoreaction depicted in Eq. (1) determined from changes in the
absorption spectrum of the aqueous solution of trans-[Ru(NH3)4-
Acknowledgements
III
L(NO)]3+ when irradiated with 330–440 nm light. / and /NO are
Ru
assumed to be the same and are sensitive to the natures of L, kIrr
and pH.
The authors acknowledge CNPq, CAPES, FINEP and FUNCAP the
Brazilian financial agencies. I.S.M. (CNPq, 308329/2006-6, 478081/

A.K.M. Holanda et al. / Inorganica Chimica Acta 361 (2008) 2929–2933
2933
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