Phosphorus(V)-corrole: Synthesis, spectroscopic properties, theoretical calculations, and potential utility for in vivo applications in living cells

Article abstract of DOI:10.1021/ic402347w

The synthesis and properties of phosphorus(V) 5,10,15-tris(4- methoxycarbonylphenyl)corrole (1) have been investigated, and its potential utility for bioimaging applications in living cells has been explored. As would normally be anticipated for corrole complexes, the intensity of the Q(0,0) bands of 1 is greater than those of comparable phosphorus(V) tetraphenylporphyrins, but the Φ_F values (0.25 for 1) are found to be comparable. A detailed analysis of the electronic structure of the complex was carried out by comparing electronic absorption and MCD spectral data to the results of TD-DFT calculations. The meso-aryl substituents, which enhance the lipophilicity of 1 and hence result in its localization in intracellular membranes during HeLa cell experiments, are predicted to result in a narrowing of the HOMO-LUMO gap and hence a red shift of the Q(0,0) bands toward the optical window in biological tissues.

Full text of DOI:10.1021/ic402347w

Article
pubs.acs.org/IC
Phosphorus(V)-Corrole: Synthesis, Spectroscopic Properties,
Theoretical Calculations, and Potential Utility for in Vivo Applications
in Living Cells
Xu Liang,†,‡ John Mack,†,§ Li-Min Zheng,‡ Zhen Shen,‡ and Nagao Kobayashi*,†
†Department of Chemistry, Graduate School of Science, Tohoku University, Sendai 980-8578, Japan
‡State Key Laboratory of Coordination Chemistry, Nanjing University, Nanjing 210093, People’s Republic of China
§Department of Chemistry, Rhodes University, Grahamstown 6140, South Africa
S
* Supporting Information
ABSTRACT: The synthesis and properties of phosphorus(V)
5,10,15-tris(4-methoxycarbonylphenyl)corrole (1) have been
investigated, and its potential utility for bioimaging applica-
tions in living cells has been explored. As would normally be
anticipated for corrole complexes, the intensity of the Q(0,0)
bands of 1 is greater than those of comparable phosphorus(V)
tetraphenylporphyrins, but the ΦF values (0.25 for 1) are
found to be comparable. A detailed analysis of the electronic
structure of the complex was carried out by comparing
electronic absorption and MCD spectral data to the results of
TD-DFT calculations. The meso-aryl substituents, which
enhance the lipophilicity of 1 and hence result in its
localization in intracellular membranes during HeLa cell
experiments, are predicted to result in a narrowing of the HOMO−LUMO gap and hence a red shift of the Q(0,0) bands
toward the optical window in biological tissues.
research focus on the use of corroles as functional ligands,
largely due to their ability to stabilize higher oxidation states of
the coordinated metal such as Cr(V), Fe(IV), Co(IV), and
even Mn(V) or Co(V).6 Although much of the research has
focused on the complexes of first-row transition metal ions,7
which tend to be nonfluorescent due to the presence of low-
lying charge transfer states associated with the central metal, the
potential utility of sulfonated Ga(III) corroles for combined
photodynamic therapy and bioimaging applications in living
cells has recently been explored.8 There has been comparatively
little research on the corrole complexes of other main group
ions relative to the porphyrins due primarily to difficulties faced
in their syntheses and isolation.7,9 P(V) corrole complexes have
been prepared by reacting metal-free corroles with a P(V)
reagent.7,10 There is an intensification of the Q band relative to
those of analogous P(V) porphyrins,11 and it lies at similar
wavelength to those of P(V) tetraphenylporphyrins between
590 and 610 nm.11c Phosphous(V) porphyrins have been
reported to have low biological toxicity, and satisfactory results
have been reported in biological systems for the photo-
sensitized formation of singlet oxygen.12 It seems reasonable to
anticipate that structural analogues such as corroles will have
similar properties in this regard.
INTRODUCTION
■
The porphyrinoid complexes of nonmetals have received a
considerable amount of attention in recent years, since their
optical and biological properties could lead to applications as
functional dyes in a number of different high-technology fields,
such as organic solar cells, photodynamic therapy, heat
absorbers, and organic catalysis.1 Porphyrins tend to have
high fluorescence quantum yields due to their rigid planar
structures and emission bands that lie at the red end of the
visible region in the optical window in biological tissues
between 650 and 1000 nm, making them potentially suitable
for bioimaging applications.2 Ideally a bioimaging dye molecule
should absorb and emit strongly in the red/near-infrared (NIR)
spectral region with narrow spectra bands, large Stokes shifts,
long excited-state lifetimes, excellent photostability, and low
biotoxicity. The main disadvantage of porphyrins in this regard
is that their lowest energy π → π* band (usually referred to as
the Q band) tends to be relatively weak with molar extinction
coefficients of >104 L mol−1 cm−1,3 so the bioimaging
properties of structural analogues such as chlorins,4 which
absorb more strongly at the red end of the visible region, have
also been studied.
Corroles are porphyrin analogues with a direct pyrrole−
pyrrole bond and an extra NH proton on the inner ligand
perimeter, best known for forming the basic structure in
vitamin B12.5 In recent decades, there has been a strong
Received: September 17, 2013
Published: March 5, 2014
© 2014 American Chemical Society
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Scheme 1. Synthetic Procedure for the Formation of the P(V) 5,10,15-Tris(4-methoxycarbonylphenyl)corrole Derivative (1)
Figure 1. UV−visible absorption and MCD spectra of 1, with the fluorescence intensity in the Q band intensity provided as an inset.
In this paper
a
novel P(V) 5,10,15-tris(4-
contain a strong parent peak at m/z 746.23 [calcd [M + H]+
= 746.19], providing direct evidence that the target molecule
was obtained. The 1H NMR spectrum of the phosphorus
corrole is also typical of a metallocorrolate; the four peaks from
9.47, 9.19, 9.16, and 8.88 ppm are associated with the pyrrole β-
methoxycarbonylphenyl)corrole has been prepared to study
trends in the electronic structure and spectroscopic properties
of P(V) corrole complexes and their potential utility for
bioimaging applications in living cells. The ester groups on the
meso-substituents were expected to enhance the lipophilicity
and hence enhance cellular uptake, since a lipophilic 4,4-
difluoro-4-bora-3a,4a-diaza-s-indacene (BODIPY) methyl ester
has successfully been developed for use as a counterstain for
cells and tissues that express green fluorescent protein.13
1
protons and were assigned by H−1H COSY experiment. The
31P NMR spectrum contains a peak at −100.93 ppm, which is
similar to other meso-substituted phosphorus(V)-corroles but is
significantly different from the peaks reported previously for
phosphorus porphyrins, which lie at ca. −200 ppm,16 due to the
complexes being six- rather than five-coordinate.
RESULTS AND DISCUSSION
The optical spectroscopy of corroles can be described in
■
terms of perturbations to an ML = 0, 1, 2, 3, 4, 5, 6,
Free base 5,10,15-tris(4-methoxycarbonylphenyl)corrole was
prepared according to literature procedures, Scheme 1.14
Reaction of the free base corrole with PCl3 in pyridine at 100
°C produces the target molecule 1 in a yield of 92% (for details
see Supporting Information). The central atom of 1 was
oxidized, P(III) to P(V), due to the ability of porphyrinoids to
coordinate O2 as an axial ligand.15 The P(III) complex is
typically only observed as an intermediate during the
phosphorus insertion reaction. The UV−visible absorption
spectrum of 1 is similar to those reported previously for
transition metal complexes.6 The MALDI-TOF MS data
3−
7 sequence of MOs associated with the parent C15H15
perimeter for the 15-atom 18-π-electron system of the inner
ligand perimeter. Moffitt17 and Michl18 demonstrated that
when the symmetry of aromatic and heteroaromatic π-systems
are lowered by perturbations to the structure, the alignments of
the nodal patterns of the MOs of the parent perimeter are
retained. This can be used to predict the effect of structural
perturbations on the relative energies of the frontier π-MOs.
The HOMO and LUMO of the parent C15H153− perimeter for
corroles have ML = 4 and 5 properties, respectively. By
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Table 1. Calculated Electronic Excitation Spectra of the P(O) Corrole and P(O) 5,10,15-Triphenylcorrole Model
Complexes and 1 Based on TD-DFT Calculations Using the B3LYP Functional
P(O) Corrole (Cs)
a
b
c
d
e
f
band
no.
sym
calc
exp
wave function
1
2
3
4
5
1A′
ground state
Q
Q
B
1A″
1A′
1A″
1A′
20.3
20.3
28.1
28.4
492
491
356
353
0.03
0.03
0.61
0.51
60% s → −a; 39% a → −s; ...
61% a → −a; 39% s → −s; ...
44% a → −s; 19% s → −a; ...
36% s → −s; 19% 2a″ → −a; 15% a → −a; ...
B
P(O) 5,10,15-Triphenylcorrole (C1)
a
b
c
d
e
f
band
no.
sym
calc
exp
wave function
1
2
3
4
5
1A
1A
1A
1A
1A
ground state
Q
Q
B
19.3
19.7
26.6
26.9
518
507
376
372
0.11
0.01
1.06
0.78
65% s → −a; 33% a → −s; ...
58% a → −a; 43% s → −s; ...
52% a → −s; 15% s → −a; ...
40% s → −s; 22% a → −a; ...
B
1 (C1)
a
b
c
d
e
f
band
no.
sym
calc
exp
wave function
1
2
3
4
5
1A
1A
1A
1A
1A
ground state
Q
Q
B
19.1
524
514
395
394
0.15
16.7
17.6
23.3
24.2
600
568
429
414
65% s → −a; 32% a → −s; ...
57% a → −a; 42% s → −s; ...
33% s → −s; 20% s → 4a; 15% a → −a; ...
19.5
25.3
0.01
0.65
1.02
B
25.4
b
43% a → −s; 20% s → 5a; 12% s → −a; ...
a
c
Band assignment described in the text. The number of the state assigned in terms of ascending energy within the TD-DFT calculation. State
d
e
symmetry. Calculated band energies (103 cm−1), wavelengths (nm), and oscillator strengths. Observed energies (103 cm−1) and wavelengths (nm).
f
Wave functions based on the eigenvectors predicted by TD-DFT. One-electron transitions associated with the four frontier π-MOs of Michl’s
perimeter model14 are highlighted in bold.
analogy with Gouterman’s four-orbital model3 it can be
demonstrated that this leads to allowed B and forbidden Q
bands based on allowed ΔML = 1 and forbidden ΔML =
9
transitions. The absorption spectrum of 1 contains bands at
600, 562, and 528 nm in the Q band region and an intense B
(or Soret) band at 418 nm, Figure 1. The additional
information provided by the MCD technique19−21 is derived
from three highly characteristic spectral features, the Faraday
(
1, )0, and *0 terms.18,21−23 The oppositely signed coupled
pair of Faraday )0 terms observed at 600 and 568 nm in the
MCD spectrum, Figure 1, can be readily assigned as the Q(0,0)
bands, since no other electronic bands are predicted in this
portion of the spectrum, Table 1. In the spectra of low-
symmetry porphyrinoids, pairs of coupled oppositely signed
Faraday )0 terms replace the derivative-shaped
(
terms that
1
are observed in the spectra of radially symmetric metal
porphyrinoid complexes.21a
Michl18 referred to the two frontier MOs derived from the
HOMO and LUMO of the parent perimeter in which nodal
planes lie on the y-axis as a and −a, respectively, while the
corresponding MOs that lie on antinodes are referred to as s
and −s, Figure 2. In contrast with the analogous porphyrin
complex, there is a minor splitting of the −a and −s MOs of
P(O) corrole for symmetry reasons, due to there being 15
rather than 16 atoms on the perimeter. When phenyl
substituents are added at the three meso-carbons, there is a
narrowing of the HOMO−LUMO gap due to a relative
destabilization of the s MO, which has large MO coefficients on
all three meso-carbons, Figures 2 and 3. This leads to a marked
red shift of the Q and B bands, Figure 4 and Table 1. There is a
further narrowing of the HOMO−LUMO gap when electron-
withdrawing −CO2Me groups are introduced at the para-
Figure 2. Nodal patterns and energies of the frontier MOs of P(O)
corrole, P(O) 5,10,15-triphenylcorrole model complexes, and 1 at
an isosurface value of 0.03 au. The a, s, −a, and −s nomenclature is
derived from Michl’s perimeter model18 and refers to four MOs
3−
derived from the HOMO and LUMO of a C15H15 parent
hydrocarbon perimeter, based on whether there is a nodal plane or
a large MO coefficient on the meso-carbon atom which is aligned with
the y-axis. This nomenclature simplifies the comparison of structurally
related molecules of different symmetry.
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coefficients on the three meso-carbons and at the para-positions
of the phenyl rings.18d This is predicted to cause a further red
shift of the Q band toward the biological window for tissue
penetration, Figure 4 and Table 1, making the compound more
suitable for bioimaging applications. The separation of the MOs
derived from the LUMO of the parent perimeter (the ΔLUMO
value to use Michl’s terminology18) is greater than those
derived from the HOMO level of the parent perimeter (the
ΔHOMO value). This results in an intensification of the Q
band of 1 relative to what is observed with analogous porphyrin
complexes,11 due to a mixing of the allowed and forbidden
properties of the Q and B bands. Although the Q band remains
relatively weak relative to what has been observed in the spectra
of the tetraaza analogues of corroles and tetrabenzocorroles19,20
due to the small |ΔLUMO − ΔHOMO| value,18 the solubility
of the complex is greatly enhanced by the presence of the meso-
aryl groups, which hinder the aggregation effects due to π−π
stacking that are often observed with phthalocyanine analogues
and tend to lead to a quenching of their fluorescence
properties.24
An intense fluorescence band is observed with a maximum at
610 nm and significant intensity in the 650−700 nm region,
Figure 1, and a Stokes shift of 124 cm−1 (see Supporting
Information). In the absence of a high oxidation state transition
metal ion, the lower energy Q(0,0) band of 1 is associated with
the S1 state. The fluorescence quantum value of 0.25 in CHCl3
is similar to that of P(V) tetraphenylporphyrin (ΦF = 0.28 in
ethanol).12b The increased intensity of the Q(0,0) bands makes
1 a suitable candidate for use in the imaging of living cells.
HeLa cells are the oldest and most commonly used human cell
line type in scientific research.25 HeLa cells were stained with a
10 μM solution of 1 in PBS solution for 10 min at 37 °C and
were then studied by confocal fluorescence microscopy (for
details see the Supporting Information). Significant intracellular
fluorescence was observed, Figure 5. No fluorescence was
observed upon irradiation with the lamp of an Olympus
FV1000 laser scanning confocal microscope. Only the outlines
of the cells are observed in the “bright-field” microscopy images
(Figure 5a) since absorbance of incident light identifies dense
areas within the sample. Significant intracellular fluorescence
was observed upon irradiation with laser light at λ = 543 nm
(Figure 5b), however.
Figure 3. Energies of the frontier π-MOs of the P(O) corrole and
P(O) 5,10,15-triphenylcorrole model complexes and 1. The a, s, −a,
and −s nomenclature is derived from Michl’s perimeter model18 and
refers to four MOs derived from the HOMO and LUMO of a
3−
C15H15 parent hydrocarbon perimeter, based on whether there is a
nodal plane or a large MO coefficient on the meso-carbon atom which
is aligned with the y-axis. The HOMO−LUMO gap values are plotted
against a secondary axis and, as would normally be anticipated, exhibit
the same trend that is observed in the calculated energies for the Q
and B bands, Figure 4
Figure 4. Calculated TD-DFT spectra for the P(O) corrole and
P(O) 5,10,15-triphenylcorrole model complexes and 1.
positions of the aryl substituents, due to a relative stabilization
of the −a and −s MOs, Figure 3, which is related to the
interaction between the π-systems of the aryl groups and the
corrole macrocycle and differences in the size of the MO
Overlays of the fluorescence and bright-field images revealed
that this fluorescence signal was selectively located in the
Figure 5. Confocal image luminescence intensity profile (left), the bright-field microscopy image (middle), and overlayed images of HeLa cells
incubated with 1 for 10 min at 37 °C with 10 μM in PBS (λex = 543 nm).
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intracellular region (Figure 5c). The localization of 1 in the
nucleus of HeLa cells demonstrates its potential utility for
biomaging. More importantly, counterstain results for 1 and
4′,6-diamidino-2-phenylindole (DAPI), Figure 6, demonstrate
Figure 6. Confocal luminescence imaging of the living HeLa cells. (a)
Images of HeLa cells incubated with 0.5 μg/mL DAPI for 5 min at 37
°C (excited at λ = 405 nm). (b) Confocal luminescence images of
HeLa cells incubated with compound 1 for 10 min at 37 °C (λex = 543
nm). (c) Bright-field images of living HeLa cells. (d) Overlayed
luminescence and bright-field pictures.
Figure 7. Photobleaching of 1 during LSCM imaging.
the parent corrole ligand, resulting in a red shift of the Q(0,0)
bands toward the biological window. There is scope to make
further structural modifications, such as fused-ring-expansion of
the ligand, to shift the Q bands further to the red through a
process of rational design assisted by theoretical calculations.
Experiments with HeLa cells demonstrate that P(O) 5,10,15-
tris(4-methoxycarbonylphenyl)corrole is biocompatible and
cell-permeable with fluorescence that can be easily discrimi-
nated from other types of functional dyes that are used in
bioimaging. This suggests that P(V) corroles are potentially
useful for applications in this regard and merit further
investigation for use in bioimaging.
that the intense fluorescence from the nucleoli and cytoplasm
can be easily discriminated from the blue fluorescence in the
nuclear zone. This demonstrates that 1 has very good
counterstain compatibility with 4′,6-DAPI, which tends to
pass through cell membranes, and hence that 1 has good
coexistence properties with other types of functional dyes that
are used during the bioimaging of living cells. Similar results
have recently been reported for a BODIPY methyl ester, which
preferentially accumulates in intracellular membranes due to its
lipophilic character.26 Photobleaching studies by laser scanning
confocal microscope (LSCM) measurements were also carried
out to investigate the photostability of 1 in living cells, Figure 7.
The fluorescence signal was detected immediately with no
delayed response, and the fluorescence signal is still present
after 600 s. Stable output is required for bioimaging agents, so
P(V) corroles appear to be potentially useful in this regard. The
quantization of the fluorescence intensity profiles of cells
stained with 1 is shown in Figure S3.
ASSOCIATED CONTENT
■
S
* Supporting Information
1
The experimental details, H and 31P NMR spectra, and the
quantization of the fluorescence intensity spectra are available
free of charge via the Internet at http://pubs.acs.org.
AUTHOR INFORMATION
Corresponding Author
*E-mail: nagaok@m.tohoku.ac.jp. Tel/Fax: +81-22-795-7719.
■
CONCLUSIONS
Notes
■
The authors declare no competing financial interest.
The introduction of a P(V) ion into the central cavity of the
corrole ligand results in a complex that is potentially suitable for
bioimaging applications, since the loss of one of the meso-
carbons enhances the intensity of the Q band relative to those
of tetraphenylporphyrins, and the absence of a high oxidation
state transition metal ion results in high ΦF values. A narrowing
of the HOMO−LUMO gap of P(O) 5,10,15-tris(4-
methoxycarbonylphenyl)corrole is predicted relative to that of
ACKNOWLEDGMENTS
■
This work has been supported by Grants-in-Aid for Exploratory
Research (No. 25620019) and for Scientific Research
Exploratory (B) (No. 23350095) to N.K. from the Ministry
of Education, Culture, Sports, Science and Technology, Japan.
The theoretical calculations were performed at the Centre for
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High Performance Computing in Cape Town, South Africa. We
thank Prof. Dr. Fuyou Li (Fudan University, P. R. China) for
his help with the living cell bioimaging measurements.
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