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Impairment of the autophagy-related lysosomal degradation pathway by an anticancer rhenium(i) complex.
Journal of Photochemistry and Photobiology 8 (2021) 100078
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Journal of Photochemistry and Photobiology
journal homepage: www.sciencedirect.com/journal/journal-of-photochemistry-and-photobiology
Photophysical properties of a β-Carboline Rhenium (I) complex. Solvent
effects on excited states and their redox reactivity
Iván Maisuls a, b, Ezequiel Wolcan a, Pedro M. David-Gara c, Franco M. Cabrerizo b,
Guillermo J. Ferraudi d, Gustavo T. Ruiz a, *
a
Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas (INIFTA, UNLP, CCT La Plata-CONICET), Diag. 113 y 64, Sucursal 4, C.C. 16, (B1906ZAA) La Plata,
Argentina
Instituto Tecnológico de Chascomús (INTECH, UNSAM, CONICET), Intendente Marino Km 8.2, CC 164 (B7130IWA), Chascomús, Argentina
c
Centro de Investigaciones Ópticas (CIOP, CONICET, CIC), Universidad Nacional de La Plata, CC.3, (1897), La Plata, Argentina
d
Radiation Research Building, University of Notre Dame, Notre Dame, IN 46556, United States
b
A R T I C L E I N F O
A B S T R A C T
Keywords:
Rhenium tricarbonyl complexes
Singlet oxygen generation
Photophysics
Photochemistry
Norharmane – TD-DFT
Pulse radiolysis
The photochemical and photophysical properties of a Re(I) tricarbonyl complex, ClRe(CO)3(nHo)2, where nHo =
9H-pyrido[3,4-b] indole (norharmane), were investigated in solution phase by a combination of steady state
emission spectroscopy, laser flash photolysis (LFP) and pulse radiolysis (PR) techniques. These results allowed us
to identify and study the reactivity of the β-carboline (nHo) Rhenium(I) complex main excited states. The ab
sorption spectrum as well as the steady-state and time-resolved luminescence of the complex exhibits a marked
dependence with the solvent properties. These experimentally observed results were corroborated by quantum
chemical calculations, TD-DFT. The most important electronic transitions present in the spectrum in all solvents
are MLLCTRe(CO)3→nHo1, nHo2 along with a mixture of ILnHo and LLCTCl→nHo transitions. The relationship between
the dipole moment and the polarity of the solvent was rationalized in terms of the electron density inside and
outside the complex. While the luminescence of the complex is mainly attributed to the emitting 1ILnHo state, in
LFP experiments a MLCT excited state was also detected. The species generated in either reductive or oxidative
conditions in LFP experiments were compared with those obtained in PR. Also, the quenching rate constant (kq)
of the excited state with MV+2 was calculated. The excited state of the complex can efficiently generate singlet
oxygen in acetonitrile yielding a ΦΔ = 0.25 ± 0.02. Optoacoustic measurements showed that, after photonic
excitation, almost all the absorbed energy by the complex is released to the medium as prompt heat. The
investigated photophysical and photochemical properties of ClRe(CO)3(nHo)2 are of significant importance in
relation to the use of this β-carboline Rhenium(I) complex in several biomedical fields, such as photodynamic
therapy and photoactivated chemotherapy as well as new alternative therapies such as regional hyperthermia.
1. Introduction
β-Carbolines (βCs) are a group of alkaloids widely spread in nature.
Their presence has been suggested in several plant and animal species,
displaying a pharmacological functions including antioxidants, anti
tumor, antiviral and antimicrobial activities, among many others
[1–10]. In addition, these biological activities can be enhanced or trig
gered by light [11–17].
As it is widely known, the combination of light-sensitive bioactive
ligands such as βCs with transition metals permits the design of inno
vative compounds that can optimize or enhance the intrinsic
photochemical, photophysical, or photobiological properties of the noncoordinated βC molecules [18–22]. Recent work from a few research
groups has shown the potential anticancer properties of different
β-carboline metal complexes [23]. The nature of metal core strongly
modulates the multi-mechanistic anticancer activities as well as the se
lective toxicity against different cancer cell lines. In addition, the type of
transition metal bound to the βC derivative induce distinctive photo
physical properties [24–28]. In particular, Rhenium (I) tricarbonyl
complexes with different polypyridines as bidentate ligands, in addition
to on βC moiety placed as an ancillary ligand, represent a set of metal
complexes with quite promising photophysical and photobiological
* Corresponding author.
E-mail address: gruiz@inifta.unlp.edu.ar (G.T. Ruiz).
https://doi.org/10.1016/j.jpap.2021.100078
Received 27 June 2021; Received in revised form 29 September 2021; Accepted 21 October 2021
Available online 28 October 2021
2666-4690/© 2021 The Authors.
Published by Elsevier B.V. This is an open
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
access
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I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
properties. We have shown, for example, the differential capabilities of
this kind of complexes to induce (or photoinduce) DNA damage [29,30].
In general, Re(I) complexes offer numerous advantages over other metal
coordination compounds such as thermal and photochemical stability
and an exceptionally rich excited-state and thermal redox chemistry
behavior, among others [29,31–35]. In addition, the accessible excited
states of Re(I) tricarbonyl complexes, such as metal to ligand charge
transfer (MLCTRe→L) and/or intraligand (IL) excited states, are generally
long-lived and luminescent at room temperature [36–39]. These con
ditions allow us to investigate the photophysical processes in which
these excited states are involved as well as their redox reactivity [29,
40–43]. Besides, Re(I) complexes has been proposed, also, as promising
candidates in anticancer treatments and as biological probes [44–50].
While there are scarcely reported Re(I) complexes with βCs as ligands
present in the bibliography, in all the recorded complexes the photo
physical properties of the compounds were commanded by the bidentate
accompanying luminophore [25,26,51]. In those complexes, the βC
derivative was acting only as a spectator ligand, with a minor photo
physical role when compared with the other moieties.
Therefore, in this work, we undertook a deep photophysical and
photochemical study of a Re(I) complex with βCs as the only type of
constitutive ligand, ClRe(CO)3(nHo)2 where nHo = norharmane, to
avoid the influence of any additional ligands, (Scheme 1) [25].
Although we have recently shown that the most important electronic
transitions present in the absorption spectrum of this complex are metal
to ligand charge transfer (MLCTRe–>nHo) along with a mixture of intra
ligand (ILnHo) and ligand to ligand charge transfer (LLCTCl–>nHo) tran
sitions by TDDFT calculations [25], in this work we extend the studies
on the experimental photophysical behavior of solutions of ClRe
(CO)3(nHo)2 complex in solvents of different polarity. We also present
their photoluminescence properties (such as excited state photo
luminescence lifetimes, emission spectra, and quantum yields) in
different solvents, and these experimental results were complemented
through theoretical calculations. With the assistance of laser flash
photolysis (LFP) and pulse radiolysis (PR) techniques, we performed a
full analysis of the possible excited state species and/or radicals derived
from the complex after a pulse of light or electrons. Furthermore, the
excited state´s redox properties of the complex were examined by both
reductive and oxidative quenching. Finally, the ability of the complex to
generate singlet oxygen was evaluated as well as their skill to release
heat through laser-induced optoacoustic spectroscopy (LIOAS)
measurements.
available from previous works [25,52]. Norharmane, 2-hydroxybenzo-
phenone and phenalenone were purchased from Sigma Aldrich at the
highest purity available and were used as received. Spectrograde and
HPLC grade acetonitrile (ACN), dichloromethane (DCM), ethanol
(EtOH), dimethylsulfoxide (DMSO), tetrahydrofuran (THF), toluene
(Tol), acetone (Ace) and triethylamine (TEA) were purchased to
Sigma-Aldrich and used without further purification. Methanol (MeOH),
benzene (BzH) and carbon tetrachloride (CCl4) were purchased to Merck
and K2HPO4 to J.T. Baker.
2.2. Solutions with methyl-viologen
Methanolic solutions of Re(nHo)2 with different concentrations of
MV+2 were prepared by adding different volumes of MV+2 (10−4 M) to
the complex solution, reaching a final volume of 10 ml. The concen
tration of the complex (10−5 M) was kept constant in all experiments.
2.3. Photochemical and photophysical measurements
UV−vis spectra were recorded on a Shimadzu UV-1800 spectro
photometer. Emission spectra were obtained with a computer-interfaced
Near-IR Fluorolog-3 Research Spectrofluorometer and were corrected
for differences in spectral response and light scattering. Solutions were
deaerated with O2-free N2 in a gas-tight cell before recording the spectra.
Luminescence lifetime measurements were carry out using a nanoLED,
λex = 341 nm, as excitation source. Photoluminescence quantum yields,
ΦF, were calculated using eq. (1).
∅F =
Aref IF n2F
∅ref
AF Iref n2ref
(1)
where A is the absorbance of the sample, I is the intensity of the lumi
nescence calculated as the integral under the entire emission spectra,
Φref is the quantum yield of the reference and n is the refractive index of
the solvent. For the experiments, nHo (Φref = 0.30 in MeOH) was used as
reference [53–55].
2.4. Flash photolysis and pulse radiolysis
Absorbance changes, ΔA, occurring in a time scale longer than 10 ns
were investigated with a flash photolysis apparatus described elsewhere
[56,57]. In these experiments, 10 ns flashes of 351 nm light were
generated with a Lambda Physik SLL −200 excimer laser. The energy of
the laser flash was attenuated to values equal to or less than 20 mJ/pulse
by absorbing some of the laser light in a filter solution of Ni(ClO4)2
having the desired optical transmittance, T = It /I0 where I0 and It are
respectively the intensities of the light arriving to and transmitted from
the filter solution. The transmittance, T = 10−A, was routinely calculated
by using the spectrophotometrically measured absorbance, A, of the
filter solution. A right-angle configuration was used for the pump and
the probe beams. Concentrations of the photolytes were adjusted to
provide homogeneous concentrations of photogenerated intermediates
over the optical path, l = 1 cm, of the probe beam. To satisfy this optical
condition, solutions were made with an absorbance equal to or less than
0.8 over the 0.2 cm optical path of the pump.
Pulse radiolysis experiments were carried out with a model TB-8/
16–1S electron linear accelerator, LINAC. The instrument and comput
erized data collection for time-resolved UV–Vis spectroscopy and reac
tion kinetics have been described elsewhere in the literature [58,59].
Thiocyanate dosimetry was carried out at the beginning of each exper
imental session. The details of the dosimetry have been reported else
where [60]. The procedure is based on the concentration of (SCN)2●̶
radicals generated by the electron pulse in a N2O saturated 10−2 M SCN¡
solution. In the procedure, the calculations were made with G = 6.13
and an extinction coefficient, ε = 7.58 × 103 M − 1 cm−1 at 472 nm, for
the (SCN)2●̶ radicals [58,60]. In general, the experiments were carried
2. Methods and materials
2.1. General
ClRe(CO)3(nHo)2 (Re(nHo)2) and Methyl-Viologen (MV+2) were
Scheme 1. Structure of ClRe(CO)3(nHo)2 (Re(nHo)2).
2
I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
out with doses that in N2 saturated aqueous solutions resulted in (2.0 ±
0.1) × 10−6 M to (6.0 ± 0.3) × 10−6 M concentrations of e¡solv. In all the
experiments, solutions in methanol were deaerated under vacuum in a
gas-tight cell. In methanolic solutions, the radiolytic pulse yield e¡solv
and C●H2OH radicals according to the following reactions scheme 2:
Thereby, in pulse radiolysis of methanolic solutions under an N2
atmosphere, the main reducing species formed are e¡solv and C●H2OH
[60]. As these species have large reduction potentials (−0.92 V for
C●H2OH and −2.8 V for e¡solv, both against NHE [61]) they have been
used for the study of both electron transfer and reduction reactions of
different species like coordination complexes of different transition
metals. The G-value of e¡solv in MeOH (G ≈ 1.2) is approximately
one-third part of the yield in the radiolysis of H2O (G ≈ 2.8). When the
e¡solv is scavenged with N2O, the C●H2OH radical is the predominant
product (yield >90%) of the reaction between O●¡ and CH3OH. The
reaction kinetics were investigated by following the absorbance change
at given wavelengths of the spectrum and incorporating those changes in
the dimensionless parameter ξ, according to eq. (2).
ξ=
ΔAinf − ΔAt
ΔAinf − ΔA0
LIOAS signals, eq. (3) was used, which relates the peak to peak ampli
tude of the first optoacoustic signal (H) with the fraction of the excita
tion laser fluence (F) absorbed by the sample [66].
)
(
(3)
H = K αF 1 − 10−A
where K is the experimental constant that contains the thermo-elastic
parameters of the solution as well as instrumental factors, A is the
absorbance of the sample at λex and a is the fraction of the energy
released to the medium as prompt heat within the time resolution of the
experiment.
3. Results and discussion
3.1. UV–Vis spectroscopy
Fig. 1 shows the solvent dependence of the spectral features of Re
(nHo)2 in solvents of different polarities. As observed, the intense band
centered at λmax ~ 240 nm is practically not affected by the solvent, as
depicted also in Table 1. In contrast, the lower energy absorption band
experiences a bathochromic shift and an intensity decrease as the
dielectric constant (ε) drops. The latter fact was further explored with an
additional group of solvents, showing a clear correlation between the
wavelength of the lower energy band with the solvent dielectric constant
(Figure S1a). Similar spectroscopic behavior observed previously in the
non-coordinated nHo indicates a strong interaction of the solvent with
the ligand [53,67] .
A comparative analysis of the absorption spectra of the complex in
methanolic solutions with those recorded for non-coordinated neutral
(nHo) and protonated (nHoH+) norharmane (Fig. 1), clearly evidenced
that, despite other electronic transitions, both nHo-like (probably to a
greater extent) and nHoH+-like βC’s rings contribute, at least in part, to
the overall absorption of Re(nHo)2 [25,53,67,68]. In addition, new
charge transfer transitions must be present also at λ > 300 nm due to the
coordination of the βC molecule to Re(I) metal.
It should be noted that although the recorded spectra show that the
highest energy band is rather insensitive to the polarity of the solvent
while the band centered at ~310 nm experiences a bathochromic shift
when the polarity of the solvent decreases, this effect is not seen with
DMSO (Figure S1a). This fact pinpoints to a probable specific interaction
between DMSO and the Re(I) complex which was not taken account in
the theoretical calculations presented below.
(2)
where ΔA0, ΔAt and ΔAinf are the absorbance changes at the beginning of
the reaction, at a given time t, and at the end of the reaction,
respectively.
2.5. Singlet oxygen production and optoacoustic measurements
The experimental details of this technique have been published
previously [62]. Briefly, quantum yields of photosensitized singlet ox
ygen production, ΦΔ, were obtained using the third harmonic of a
Q-switched Nd-YAG laser as the excitation source (λex = 355 nm,
Surelite II- Continuum), looking at the 1270 nm 1O2 phosphorescence
with a Ge-photodiode (Applied Detector Corporation, resolution time of
1 μs). Measurements were performed in air-equilibrated solutions. The
averages of signals generated by 64 laser shots were recorded to improve
the signal-to-noise ratio. Single exponential analysis of emission decays
was performed with the exclusion of the initial part of the signal. ΦΔ was
determined by measuring its phosphorescence intensity using an opti
cally matched solution of a reference sensitizer. In acetonitrile, the
reference used was phenalenone (ΦΔ =0.975) [63].
Photoacoustic measurements were performed by using a set-up
already described [62]. The resolution time in our experimental
set-up, tR, was ca. 800 ns [62]. 2-hydroxybenzo-phenone was used as
calorimetric reference (CR) compounds in ACN solutions [64,65]. Ex
periments were performed under a controlled atmosphere, bubbling N2
or O2 in the solution, for 15 min. In principle, all the excited species with
lifetimes t ≤ ⅕ tR release their heat content as prompt heat, whereas
excited species with a lifetime of τ ≥ 5 tR function as heat storage within
the time resolution of the LIOAS experiment. For the handling of the
Fig. 1. Normalized UV–Vis spectra of Re(nHo)2 in different solvents (solid
lines). For comparison, non-coordinated nHo and nHoH+ in neutral and acidic
organic solvent (green and blue dotted lines, respectively) are also shown.
Absorption coefficients are displayed in Figure S1b.
Scheme 2. Generated MeOH-derived species after the radiolytic pulse.
3
I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
centered on nHo2 and nHo1, respectively. H-2 is very similar in shape to
H-1. Therefore, all the electronic transitions in vacuo in this region of
wavelengths are MLLCT(Re(CO)3→nHo1, nHo2). MO shapes in BzH are very
similar to MO shapes in vacuo. In THF, however, H and H-1 have in
addition significant contributions from nHo1 and nHo2, respectively.
On the other hand, L and L + 1 have in THF even contributions from
nHo1 and nHo2 and those MOs are widespread between both ligands. In
DMSO, the charge density is widespread between Re, COs, nHo1, and
nHo2 in H and H-1. The solvent effect on MOs charge density is
responsible for a decrease of the percentage of charge-transfer transi
tion, CT%, as polarity increases, from 48% in vacuo to nearly 32% in
DMSO (see definition of CT% in Supporting Material and Table S6).
The decrease in CT% as polarity increases also explains the bath
ochromic shift of the calculated MLLCTRe(CO)3→nHo1, nHo2 wavelength
(λcalc) as solvent polarity decreases. As the charge density over Re is
lower in DMSO than in BzH, the energy of the MLLCTRe(CO)3→nHo1, nHo2 is
higher in DMSO than in BzH and the charge transfer process becomes
energetically less feasible. As observed in the previous figures, our cal
culations are in agreement with the negative solvatochromism observed
in less polar solvents. The direction of the solvent dependence is asso
ciated with a reduced (and reversed) molecular dipole in their MLCT
excited states, as stated in the bibliography [70]. As depicted in the
Fig. 4, the molecular dipole moment, µ, increases with the increase on
the dielectric constant, εr. Moreover, the vector of the dipole moment is
directed between the two nHo ligands.
The solvent effect on the dipole moment can be interpreted in terms
of electron density plots (Figure S2). In vacuo, the electron density is
more concentrated inside the “shape” of the molecule. However, when
the polarity of the solvent increases, the electron density becomes more
diffuse and it is enhanced outside the molecular limits. Therefore, µ
increases.
Table 1
λmax of Re(nHo)2 in different solvents and dipole moment (μ) and dielectric
constant (ε) of the solvents [69].
Solvent
λmax, nm
λmax, nm
μ, D (debye)
ε at 25 ◦ C
CH3CN
CH3OH
CH2Cl2
CCl4
239
241
241
—
305
307
309
315
3.53 (at 25 ◦ C)
2.87 (at 20 ◦ C)
1.14
0
35.94
32.66
8.93
2.23
3.2. Quantum chemistry of Re(nHo)2
To get a deeper understanding of the absorption spectrum of Re
(nHo)2 and its dependence with the solvent described above, a system
atic TD-DFT theoretical study is present herein. To this aim, spectra were
simulated under 10 different solvents (i.e., PCM = DMSO, ACN, MeOH,
EtOH, Ace, DCM, THF, Tol, BzH and CCl4) with different intensive
properties. A set of MLCT, LLCT and IL electronic transitions was taken
into account in the calculations. The calculations were carried out at the
M06/6–311 G/6–311G*/LanL2TZ(f)/PCM level of theory.
Fig. 2 depicts the UV–visible absorption spectra of Re(nHo)2 simu
lated under both vacuo and the 10 different solvents mentioned above
(Figure S1a). The calculated absorption spectra follow the experimental
trend showing a clear bathochromic shift of the lowest energy absorp
tion band as the polarity of the solvent decreases while the higher energy
band experiences hardly any shift. In addition, the highest energy band
in vacuo is only blue-shifted by 7 nm relative to the solvent media while
the lowest energy band in vacuo is displaced by 20–40 nm to the red
relative to its position under the PCM. Electronic transitions results
calculated at the same level of theory in vacuo, BzH, and DMSO are
summarized in Tables S1-S3. The most relevant MOs which are
responsible for the electronic transitions in the absorption spectroscopy
of Re(nHo)2 in the 230–500 nm wavelength range are: HOMO, LUMO,
and the groups of MOs H-10 through H-1 and L + 1 through L + 6. The
percentage compositions of those MOs were obtained from Mulliken
population analysis with the aid of AOMIX program from contributions
of five fragments: (i) Re atom, (ii) the three carbonyls, (iii) nHo-1
molecule, (iv) nHo-2 molecule, and (v) Cl atom. Tables S4-S5 show
the calculated% compositions of all fragments at each MO for Re(nHo)2
in BzH and DMSO.
In the 330–500 nm region, the most relevant electronic transitions
are H→L, H→L + 1, H-1→L, H-2→L, and H-2→L + 1. Fig. 3 shows the
spatial plots of a selection of those MOs of Re(nHo)2 in vacuo, BzH, THF,
and DMSO, which give insight into the electronic transitions. Fig. 3
shows that in vacuo, H and H-1 are MOs mostly centered on the Re atom
with contributions from the three CO while L and L + 1 are MOs
3.3. Photophysical and photochemical measurements of Re(nHo)2
3.3.1. Luminescence measurements
The emission spectra of Re(nHo)2 were recorded in MeOH, ACN, and
DCM (Fig. 5). For comparative purposes, spectra of non-coordinated
nHo recorded under different solvent or pH conditions are also shown.
Luminescence spectra of both Re(nHo)2 and non-coordinated nHo,
showed a strong solvent dependence. Briefly, a set of three emission
bands centered 370–400 nm, 400–480 nm, and 480–550 nm. While the
lowest energy transition could be associated to MLCT transitions, the
spectrum of non-coordinated nHo suggests a dominant contribution of
ILnHo transition [25,67,72]. When Re(nHo)2 is dissolved in a non-protic
solvent with a low polarity like ACN, the only evident emission band is
the one attributed to an intraligand excited state, ILnHo, where the
emission spectrum of the complex is quite similar to the emission
spectrum of the non-coordinated nHo ligand, with no spectral contri
butions at wavelength larger than 450 nm. On the contrary, emission
spectrum of Re(nHo)2 recorded in methanolic solution (Fig. 5, left)
shows two broad bands. The highest energy bands (λ ~ 360 – 390 nm)
are attributed to the radiative decay of ILnHo electronic states [68,73,
74]. The emission centered at λ ~ 440 nm, has been previously attrib
uted to an ILnHo excited state where the n electrons of the pyridinic N are
compromised, as in the cationic form of nHo (nHoH+) [67,72]. In
addition, a shoulder spans the 480 – 600 nm region of the spectra. As it
was previously established, when an organic molecule is part of a
transition metal complex, nonbonding electrons of the N atoms of the
ligands, that contributed the nπ* excited state, is turned into a charge
transfer (CT) excited state. Bearing this in mind we can assume that this
effect could explain the similarities observed in the luminescence
spectra in ACN and MeOH namely where interaction of solvent mole
cules with the nonbonding electrons is strong [53]. Conversely in DCM,
the emission spectrum of non-coordinated nHo does not resemble the
spectra of the complex. While the nHo emission band (ILnHo excited
state) is located at λmax = 380 nm, a band centered at λmax = 450 nm was
Fig. 2. Simulation of the UV/Vis spectra of Re(nHo)2 in 10 different solvents
and vacuo. Inset: Amplification of the band centered in λ~350 nm.
4
I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
Fig. 3. Spatial plots of most representative MOs of Re(nHo)2 (isovalue = 0.02).
Photoluminescence quantum yields (ΦF), as well as the photo
luminescence excited state lifetimes (τ) of Re(nHo)2, were measured in
ACN, DCM, and MeOH, and the results are depicted in Table 2. Lumi
nescence lifetime were recorded at different wavelengths, depending on
the prominent emission bands of the complex.
As shown in Table 2, both ΦF and τ also depend in a certain way on
the solvent. From the obtained values of τ, two main points can be
discussed. First, as depicted, there is a mild dependency on the presence
of O2, as expected for this kind of compounds and their ability to interact
with 3O2 to generate 1O2, (see below). Second, the obtained values for
the two main ILnHo emission bands closely resemble the τ previously
reported for the excited states of non-coordinated nHo molecule [53,
67]. This outcome suggests once more, that the main emitting excited
states in Re(nHo)2 are mainly ILnHo.
3.3.2. Photochemical reactions induced by laser flash photolysis (LFP)
LFP measurements were carried out using a XeF laser (λex = 351 nm).
Fig. 6 shows the transient spectra obtained when either Re(nHo)2 or
non-coordinated nHo solutions (10−5 M) were flash photolyzed in
MeOH. As it can be observed, the main transient absorption band
observed with Re(nHo)2 solution is centered at λmax ~ 555 nm (blue).
However, the main absorption band with the nHo solution is centered at
λmax ~ 500 nm (red). The latter spectral feature was previously attrib
uted to an excited state of the nHo [68]. The spectra obtained are dis
similar and, therefore, the transient of Re(nHo)2 should not be assigned
to an intrinsic ILnHo excited state.
Besides, the decay of the transient of the complex after the irradia
tion adjusts perfectly to a monoexponential decay (τ = 75 ns), sug
gesting that only one species is present. This lifetime is much longer than
the luminescence lifetime of Re(nHo)2 (Table 2), and is markedly
shorter than the reported (and also measured in this work) for the
transient decay of non-coordinated nHo (τ = 2 μs), as it is shown in the
supplementary information (Figure S3) [53,68,72]. These differences
Fig. 4. Molecular dipole moment, μ, of Re(nHo)2 as a function of the dielectric
constant, εr.
observed to Re(nHo)2. Under acidic conditions, when the n electrons of
the pyridinic N of the free nHo are compromised, as in nHoH+, a λmax of
450 nm is observed. This equivalence between the spectra of the nHoH+
and Re(nHo)2 in DCM suggests that in this solvent the complex exper
iments a charge distribution where an electronic deficiency over the nHo
is obtained and therefore the spectral features of an ILnHo
electron-deficient excited state is observed. In this sense, the nature of
the excited state responsible for the luminescence at λ ~ 450 nm could
be attributed to a protonated-like ILnHo excited state [67]. The changes
in the electronic density, along with the “heavy atom effect” caused by
the Re atom can lead to an electronic distribution like the free nHoH+,
giving as a result similar emission spectral features.
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I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
Fig. 5. Left: normalized emission spectra of Re(nHo)2 (dash lines) and nHo (dotted lines) in ACN (red) and MeOH (black). Right: normalized emission spectra of Re
(nHo)2, nHo in DCM and nHo in DCM + H+ (dotted line and dashed line, respectively) λex = 320 nm. Emission spectra of non-coordinated nHo are in agreement with
that reported in the literature [53,68,71].
Table 2
Photoluminescence excited state lifetimes and emission quantum yields of Re(nHo)2in different solvents.
Solvent
ΦF
τ Re(nHo)2 λem = 380 nm/air
τ Re(nHo)2 λem = 380 nm/N2
τ Re(nHo)2 λem = 450 nm/air
τ Re(nHo)2 λem = 450 nm/N2
ACN
DCM
0.010
0.025
τ = 3.06 ± 0.02
τ = 2.56 ± 0.02
τ = 3.84 ± 0.02
τ = 2.71 ± 0.02
–
–
MeOH
0.018
τ = 3.77 ± 0.01
τ = 4.51 ± 0.02
equilibrated/ns
equilibrated/ns
equilibrated/ns
τ1 = 1.25 ± 0.03 (93%)
τ2 = 20.4 ± 0.3 (7%)
τ1 = 3.65 ± 0.04 (76%)
τ2 = 18.5 ± 0.1 (24%)
equilibrated/ns
τ1 = 1.41 ± 0.06 (81%)
τ2 = 17.2 ± 0.2 (19%)
τ1 = 4.36 ± 0.06 (72%)
τ2 = 26.2 ± 0.1 (28%)
flash irradiated in a neat MeOH solution (10−5 M) containing also 0.1 M
TEA. The transient spectrum recorded is shown in Fig. 7.
This transient spectrum is very similar to the one observed in the
absence of TEA Fig. 6). In addition, the decay lifetime of the transient
observed was longer lived (τ = 6.04 μs) than excited state decay. These
results suggest that the similarity between the excited state and the
transient in Fig. 7 spectral features is the result of the charge separation
established in the complex when an excited state MLCTRe→nHo is popu
lated (formally Re(II) and a ligand radical anion) and the net location of
an electron in the ligand, i.e., forming the reduced radical generated by
reaction of the MLCT with TEA, Eq. (4) and ((5).
Fig. 6. LFP spectra for non-coordinated nHo (red) and Re(nHo)2 complex
(blue) recorded in MeOH.
are explained by assuming that some excited states in the Re(nHo)2
complex are different than those present in the non-coordinated nHo, as
observed previously in different coordination complexes with nHo as
ligand [29].
The ability of the excited states to participate in redox reactions it is
well documented in the literature [29,56,75,76]. The electron transfer
reactions between the excited states of Re(I) complexes with the sacri
ficial electron donor triethylamine (TEA) as well as with the electron
acceptor methyl viologen (MV+2) are often used to probe their redox
reactivity. Reductive quenching with amines, in particular, it is used for
the identification of MLCT excited states. They react generating a
reduced radical of complex. In this work, the Re(nHo)2 complex was
Fig. 7. LFP spectra of Re(nHo)2 with an excess of TEA in MeOH (λex = 351
nm). Inset: oscillographic trace recorded at λob = 550 nm showing the decay of
the transient absorbance (ΔA), with a lifetime τ = 6.04 μs.
6
I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
[
] hv [
]∗
ClReI (CO)3 (nHo)2 → ClReII (CO)3 (nHo)(nHo•− )
(4)
[
]∗ +TEA [
]
ClReII (CO)3 (nHo)(nHo•− ) ̅̅̅̅→
ClReI (CO)3 (nHo)(nHo•− )
•+
(5)
−TEA
The quenching rate constant (kq) was calculated from the slope of the
plot kd vs MV+2, yielding the value kq = 4.8 × 109 M − 1s−1 (Fig. 9). This
value of kq is in within the order of magnitude of kq constants in the
literature for structurally related complexes [29,77,78]. Furthermore, it
is 2.3 to 34.3 times greater than those reported for the relative com
plexes [(nHo)Re(CO)3(L)]+, where L = bidentate N,N´-ligands [29]. In
sum, the excited state oxidation reaction of Re(nHo)2 occurs with
greater ease than those complexes with bidentate ligands. Such a greater
ease is probably due to steric effects that energetically optimize the re
action path for monodentate ligands.
Thus, contrasting what is observed in a non-coordinated nHo solu
tion, an MLCT excited state is generated when a solution of Re(nHo)2
was flash photolyzed.
3.3.3. Pulse radiolysis (PR)
The pulse radiolysis technique was used also to generate the reduced
radical of Re(nHo)2 complex by reaction mainly with solvated electrons,
e¡solv, (experimental conditions MeOH/N2, see 2.4 section).
Fig. 8 shows that the spectrum for the reduced species of Re(nHo)2,
(blue), consist of a narrow band at λ ~ 390 nm along with a broad band
at λ ~ 550 nm, both bands nearly with the same intensity. The same
spectral features are observed in the reduction of non-coordinated nHo
(red). Hence, the complex is reduced by the thermal reaction with e−solv
producing a radical, eq. (6).
[
] e−solv [
)]
ClReI (CO)3 (nHo)2 → ClReI (CO)3 (nHo)(nHo•−
3.3.4. Singlet oxygen generation and optoacoustic measurements
Singlet oxygen generation by the Re(nHo)2 complex in ACN solu
tions was analyzed by time-resolved phosphorescence measurements
(1270 nm). The phosphorescence showed clear evidence of singlet ox
ygen formation. Linear correlations were obtained from the plots of the
dependence of the singlet oxygen phosphorescence intensity emission at
zero time, S(0), as a function of the laser energy for the complex and the
reference. From these slopes (Figure S5) and the usual procedure
described elsewhere [62,79], the determined quantum yield of singlet
oxygen production was ΦΔ = 0.25 ± 0.02. This result is similar to values
of ΦΔ of Re(I) complexes which have similar structures or with nHo as
ligand [30,62,80].
As observed in Fig. 10, the photoacoustic signal of Re(nHo)2, as well
as the reference in ACN solutions, showed the same behavior: no time
shift or changes of shape, with respect to the calorimetric reference
signal (inset of Fig. 10). Linear relationships in both solvents were ob
tained between the amplitude of the first optoacoustic signal (H) and the
excitation fluence (F) for samples and references at various A, in a flu
ence range between 1 and 10 J/m2. The ratio between the slopes of these
lines for sample and reference yielded the values of α for the samples.
From these plots, considering that aR = 1 for CR, the a value = 0.89 ±
0.04 was obtained for Re(nHo)2 complex. Consequently, this complex
released to the medium almost all the absorbed energy as prompt heat
(integrated by the transducer) in processes faster than τR/5. These
values, combined with the photochemical data, were satisfactorily
adjusted to the energy balance [62,66], where the molar exciting energy
from the laser photon (Eλ = 80.5 kcal/mol at 355 nm) provides the sum
of the fraction of energy dissipated as prompt heat, plus the energy lost
in rapid radiative processes, e.g. fluorescence, and the energy "stored" in
long-lived transient species, such as a singlet oxygen.
(6)
The high spectral resemblance between the spectrum generated by
PR and the spectrum recorded by LFP in the reductive quenching with
TEA (Fig. 7), confirms the Re(nHo)2 role of electron acceptor in the
photoinduced process in which the participation of a MLCTRe→nHo
excited state must be required [29].
Oxidative quenching of Re(nHo)2 was investigated by the LFP gen
eration of the excited states of the complex in the presence of MV+2. The
latter species oxidize the excited state of the complex producing the
radical MV●+. Such a radical exhibits a characteristic absorption at λ ~
600 nm (Figure S4). The redox process must involve the photo
generation of MLCT, eq. (4), followed by its reaction with MV+2, eq. (7).
[
)]∗
]+
[
ClReII (CO)3 (nHo)(nHo•−
+ MV+2 → ClReII (CO)3 (nHo)2 + MV•+
(7)
Solutions of the complex with MV were flash irradiated at 351 nm.
The rate constants of the quenching reactions were determined by
varying the concentration of MV+2 while keeping the complex concen
tration constant. The kinetics of the reactions was investigated under a
pseudo-first-order regime in MV+2 concentration. A single exponential
decay of the excited state with a rate constant (kd), eq. (8), corre
sponding to a pseudo-first-order dependence on MV+2 concentration
was obtained [29,76].
+2
−kd t
ΔAt = ΔA0 e
4. Conclusions
(8)
The photophysical and photochemical properties of ClRe
(CO)3(nHo)2 were studied in solution phase. These results allowed us to
Fig. 8. Pulse radiolysis spectra of Re(nHo)2 (blue) and non-coordinated nHo
(red) of N2 deaerated solutions (10−5 M, MeOH).
Fig. 9. Plot of kd vs [MV+2]. kq is represented as the slope of the linear fit.
7
I. Maisuls et al.
Journal of Photochemistry and Photobiology 8 (2021) 100078
112–2013–01–00236CO), ANPCyT (PICT 2018–03193 and PICT
2018–03341) and UNLP (11/X779 and 11/X679) Argentina. F.M.C, E.
W. and G.T.R. are Research Members of CONICET (Argentina). P.D.G. is
a Research Member of CICBA (Argentina). I.M. thanks ANPCyT, CONI
CET and the Fulbright Program for research scholarships. Part of this
work was also carried out in the Notre Dame Radiation Laboratory
(NDRL). The NDRL is supported by the Division of Chemical Sciences,
Geosciences and Biosciences, Basic Energy Sciences, Office of Science,
United States Department of Energy through grant number DEFC02–04ER15533. This is contribution number NDRL 5320.
Supplementary materials
Supplementary material associated with this article can be found, in
the online version, at doi:10.1016/j.jpap.2021.100078.
References
Fig. 10. Amplitude of the photoacoustic signals as a function of laser fluence
for ACN solutions: 2-Hydroxybenzophenone (2-HBP, •), Re(nHo)2 complex
( ). Inset: Normalized photoacoustic signals of ACN solutions for 2-HBP (black
line) and the Re(nHo)2 complex (red line) with matched absorbances (0.158
± 0.002).
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identify and study the reactivity of the β-carboline Rhenium(I) complex
main excited states. The absorption spectrum as well as the steady-state
and time-resolved luminescence of Re(nHo)2 complex exhibits a marked
dependence with the solvent properties. TD-DFT calculations estab
lished that the most important electronic transitions present in the low
energy region of the spectrum in all solvents are MLLCTRe(CO)3→nHo1,
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attributed to the emitting 1ILnHo state although overlapping emission
from 3MLCT states in the low energy region cannot be ruled out. How
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(nHo)2 complex can efficiently generate singlet oxygen as well as
reduced radicals or oxidized species of Re(II) reactive against substrates
present, for example, in cellular environments. These photophysical
properties suggest the potential application of Re(nHo)2 complex in
photodynamic therapy (PDT) or photoactivated chemotherapy (PACT),
antioxidant activity, or photocytotoxicity. In this sense, the cellular
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cytotoxicity against these human carcinoma lung cells, acquire even
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therapies such as regional hyperthermia that allows counteracting
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photobiological action that could be modulated by the difference in the
polarity of the different cell compartments.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgments
This
work
was
supported
in
part
by
CONICET
(PIP
8
Journal of Photochemistry and Photobiology 8 (2021) 100078
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