Luminescent cell-penetrating pentadecanuclear lanthanide clusters

Article abstract of DOI:10.1021/ja403539t

A novel pentadecanuclear lanthanide hydroxy cluster [{Ln ₁₅(μ₃-OH)₂₀(PepCO₂) ₁₀(DBM)₁₀Cl}Cl₄] (Ln = Eu (1), Tb (2)) featuring the first example with peptoids as supporting ligands was prepared and fully characterized. The solid-state structures of 1 and 2 were established via single-crystal X-ray crystallography. ESI-MS experiments revealed the retention of the cluster core in solution. Although OH groups are present, 1 showed intense red fluorescence with 11(1)% absolute quantum yield, whereas the emission intensity and the quantum yield of 2 were significantly weaker. In vitro investigations on 1 and 2 with HeLa tumor cells revealed an accumulation of the clusters in the endosomal-lyosomal system, as confirmed by confocal microscopy in the TRLLM mode. The cytotoxicity of 1 and 2 toward the HeLa cells is moderate.

Full text of DOI:10.1021/ja403539t

Communication
pubs.acs.org/JACS
Luminescent Cell-Penetrating Pentadecanuclear Lanthanide Clusters
Dominique T. Thielemann,† Anna T. Wagner,† Esther Rosch,‡ Dominik K. Kolmel,‡ Joachim G. Heck,†
̈
̈
Birgit Rudat,‡ Marco Neumaier,† Claus Feldmann,† Ute Schepers,*,§ Stefan Brase,*,‡,§
̈
and Peter W. Roesky*,†
†Institute of Inorganic Chemistry and ‡Institute of Organic Chemistry, Karlsruhe Institute of Technology, 76131 Karlsruhe, Germany
§Institute of Toxicology and Genetics, Karlsruhe Institute of Technology, 76344 Eggenstein-Leopoldshafen, Germany
S
* Supporting Information
mononuclear complexes, semiconductor nanoparticles such as
ABSTRACT: A novel pentadecanuclear lanthanide hy-
droxy cluster [{Ln15(μ3-OH)20(PepCO2)10(DBM)10Cl}-
Cl4] (Ln = Eu (1), Tb (2)) featuring the first example
with peptoids as supporting ligands was prepared and fully
characterized. The solid-state structures of 1 and 2 were
established via single-crystal X-ray crystallography. ESI-MS
experiments revealed the retention of the cluster core in
solution. Although OH groups are present, 1 showed
intense red fluorescence with 11(1)% absolute quantum
yield, whereas the emission intensity and the quantum
yield of 2 were significantly weaker. In vitro investigations
on 1 and 2 with HeLa tumor cells revealed an
accumulation of the clusters in the endosomal−lyosomal
system, as confirmed by confocal microscopy in the
TRLLM mode. The cytotoxicity of 1 and 2 toward the
HeLa cells is moderate.
quantum dots (QDs) have attracted a number of researchers,
since their luminescence is not as prone to quenching effects as is
the case for Ln metal complexes. QDs show characteristic size-
and composition-dependent luminescence which can be tuned
precisely.10 The third class of compounds that has been proposed
as optical markers are rare-earth metal-based nanoparticles.11 In
comparison to QDs, they have a much longer fluorescence
lifetime, and the fluorescence wavelength of Ln(III) ions is not
sensitive to particle size.11
Obviously there is a large gap in size between well-defined
mononuclear lanthanide complexes and polynuclear nano-
particles. The size of the latter can only be controlled within a
certain range, resulting in a particle size distribution instead of
defined structures. Between these two extremes, oligonuclear
lanthanide clusters are accommodated. Such cluster compounds
are much larger than mononuclear compounds but still exhibit a
well-defined size and composition.12 As a result of these
properties, the study of the function and properties of these
compounds is simplified when compared with that of nano-
particles. Today a range of lanthanide hydroxy clusters exhibiting
various nuclearities has been established, highlighting the ease of
preparation and good yields.12 Although some of these
compounds were studied in terms of their magnetic properties,13
the photophysical properties of only very few lanthanide hydroxy
clusters were investigated.14 To the best of our knowledge,
oligonuclear clusters of the rare-earth metals have hitherto not
been used for any biological application. Based on this
consideration, we were interested in synthesizing rare-earth
metal-based clusters having luminescent properties for living cell
penetration. To reach this goal, the anchoring of a cell-
penetrating agent onto a structurally well-defined rare-earth
metal cluster is necessary. Recently, Schiff-base-ligated hexa-
nuclear zinc macrocycles were evaluated against several cell lines
with respect to their toxicity, providing an example of metal
clusters being investigated with regard to their potential as anti-
tumor drugs or cellular localization probes.15
uminescent materials were used in past decades in cell
Lbiology and biochemistry to get a better understanding of
the structure and function of biological systems through methods
that involve minimal perturbation of the system. As luminescent
materials, organic fluorophores,1 recombinant proteins,2 semi-
conductor nanoparticles,3 and emissive metal complexes were
used.4 The drawback of organic dyes is that they are not stable
against bleaching, have a poor extinction coefficient or quantum
yield, and are sometimes toxic to cells. Regarding nanoparticles
and emissive metal complexes, rare-earth metal-based materials
have been studied intensively because trivalent rare-earth metal
ions have useful properties as optical probes,5 since the f−f
emission lines of Pr(III), Sm(III), Eu(III), Tb(III), Dy(III), and
Tm(III) ions are in the visible range.6 Moreover, the emission
lines of the rare-earth metals are sharp because the excitation of
an electron into a 4f orbital of higher energy is almost not
influenced by the ligands in a metal complex. Most work that has
been published in the area of luminescent rare-earth metal
complexes deals with Eu(III) and Tb(III) because the excited
states of these ions are less sensitive to vibrational quenching by
intra- or intermolecular energy transfer to adjacent high-energy
vibrators such as hydroxyl groups.7 The advantage of using
mononuclear rare-earth metal complexes as cellular probes in
general is their rational design.4,8 However, the susceptibility of
rare-earth metal and in particular lanthanide(III) (Ln(III)) ion
luminescence to quenching effects caused by water or hydroxyl
groups is a drawback of such mononuclear complexes.9 Besides
In 1994, the intrinsic cell-penetrating peptide (CPP) research
began with the identification of the polycationic homeoprotein
Antennapedia from Drosophila melanogaster.16 The currently used
CPPs consist of 10−30 α-amino acids. It was shown that they can
carry cargos into the cell-like peptides and proteins up to 120
kDaoligonucleotides,17 liposomes,18 and nanoparticles.19 The
Received: April 9, 2013
Published: May 7, 2013
© 2013 American Chemical Society
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Communication
a
Scheme 1. Synthesis of Eu and Tb Clusters 1 and 2
a
Keto−enol tautomerization of DBMH is omitted for clarity.
fast cellular uptake and the defined structure make CPPs very
attractive, but their applicability is also restricted since they are
prone to enzymatic degradation. To circumvent the latter aspect,
peptidomimetics such as cell-penetrating peptoids (CPPos) are
increasingly used.20 CPPos are based on oligo-N-alkylglycine
varying in different side chains connected to the N-atom of the
backbone. Peptoids are stable against proteases in vivo and in
vitro, and they exhibit antibiotic properties. Furthermore, they
possess a binding affinity to certain receptors or proteins.20d
Herein we report on pentadecanuclear europium and terbium
hydroxy clusters which are ligated by CPPo monomers. Owing to
the distinct biological compatibility of the peptoids, the obtained
clusters feature a pronounced propensity to cell penetration.
Reaction of the CPPo monomer 2-[{3-(((tert-butoxycarbonyl)-
amino)methyl)benzyl}amino]acetic acid hydrochloride (Pep-
CO2H·HCl) with [LnCl3·(H2O)6] (Ln = Eu, Tb) and
dibenzoylmethane (DBMH) in the presence of potassium tert-
butoxide in methanol resulted in the formation of the
pentadecanuclear lanthanide hydroxy cluster [Ln15(μ3-
OH)20(PepCO2)10(DBM)10Cl]Cl4 (Ln = Eu (1), Tb (2)) in
40% (1) and 33% (2) single-crystalline yield, respectively
(Scheme 1).
Compounds 1 and 2 were characterized by standard analytical
and spectroscopic techniques (Supporting Information). The
solid-state structures were determined by single-crystal X-ray
diffraction (Figure 1). Although the X-ray data collected from 1
were very poor, its composition was deduced. The composition
was also established by ESI-MS (see below). The [Ln15(μ3-
OH)20(PepCO2)10(DBM)10Cl]4+ cation consists of five
{Ln4(μ3-OH)4}8+ heterocubane subunits, which are fused to a
pentagonal ring structure by an edge-sharing arrangement. The
cyclic shape of this metal hydroxide scaffold is additionally
stabilized by a centered μ5-bridging Cl-atom. The 10
dibenzoylmethanide (DBM) ligands are bidentate and coor-
dinate uniformly in a chelating κ2-mode to those rare-earth metal
atoms which do not act as linking points between adjacent
heterocubane subunits. All DBM ligands are aligned coplanar
with the pentagonal ring. In contrast, the CPPo monomer
(PepCO2) ligands act exclusively as tridentate ligands and are
arranged perpendicular to the ring. Each PepCO2 ligand
coordinates with both carboxylate O-atoms and the glycinic N-
atom to three metal centers, giving a μ3:κ2:κ1-mode. Although a
similar central structural core of formula {Ln15(μ3-OH)20Cl}24+
has been reported,21 coordination of CPPo monomers to such an
inorganic core structure is, to the best of our knowledge, unique.
Although numerous rare-earth metal hydroxy clusters can be
found in literature,12 almost nothing is known about their
structure in solution.22 To investigate the stability in solution,
ESI-MS spectra of 1 and 2 were recorded from different solvents.
For all compounds the [{Ln15(μ3-OH)20(PepCO2)10(DBM)10-
Cl}Cl2]2+ (M02+) cation could be unambiguously detected from
various alcoholic solvents (Figures 2, S4, and S5) and DMF; i.e.,
in the chosen medium the dissolution process of 1 is
accompanied by the dissociation of two non-coordinating
Figure 1. Top: Front view of solid-state structure of [Tb15(μ3-
OH)20(PepCO2)10(DBM)10Cl]Cl4 (2). Bottom: view of the inorganic
{Tb15(μ3-OH)20Cl}24+ core with all ligand-derived coordinating
heteroatoms. H-atoms are omitted for clarity.
chloride anions. Figures 2 and S5 show cutouts of the ESI-MS
spectra of 1 and 2 from ethanol solution, and the insets highlight
the agreement between calculated and experimentally found m/z
ratio as well as the expected isotopic distribution of the dication
M02+. As can be seen from Figures 2 and S4, adjacent signal sets
with identical isotopic distribution shifted to higher m/z ratios
are indicative of an exchange reaction, which is attributed to
substitution of hydroxy bridges by ethanol-derived ethoxy
groups. Upon this exchange process, the cluster scaffold is
retained, as illustrated by the corresponding sum formula
[{Ln15(μ3-OH)20−n(OEt)n(PepCO2)10(DBM)10Cl}Cl2]2+
(Mn2+) with n = 1−3, showing that 1−3 hydroxy bridges are
substituted in M02+. These degradation processes were found to
occur consecutively (for 1, refer to Figure S4).
Compound 1 showed intense red fluorescence with the
characteristic Eu3+-related f→f transitions at 580−700 nm
(Figure 3). Considering the direct coordination of the
luminescent center to hydroxide anions, the quantum yield at
room temperature is surprisingly high. Thus, values of 19(1)%
relative to YVO4:Eu (λexc. = 365 nm) as a reference and of
16(1)% (λexc. = 400 nm) for absolute counting of photons were
obtained (cf. Supporting Information). Most often the emission
of rare-earth ions is quenched via vibronic transitions in the
presence of hydroxyl or aqua ligands.23 Compound 2 showed
typical f→f emission lines of Tb3+ (550−650 nm). In comparison
to 1, the emission intensity and the quantum yield (<3%) are,
however, significantly weaker (Figure S6).
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Figure 2. Cationic electrospray (ESI+) spectrum of 1 from ethanol. The
Figure 4. Cellular uptake of 1 and 2 in HeLa cells: 1 × 104 HeLa wt cells
were treated with 0.1 μM 1 (A−D), 2 (E−H), or [TbCl3·(H2O)6] (I−
L) for 24 h at 37 °C. [EuCl3·(H2O)6] showed the same result as shown
in panels I−L. Eventually, the cells are analyzed with time-resolved
luminescence confocal imaging. Images D, H, and L show the merging of
the bright-field channel with the emission channels (A−C, E−G, and I−
K, respectively) for the luminescence using the PMTs with emission of
420−480 (A,E), 480−600 (F,J), and 500−700 nm (B), and the bright-
field channel (C,G,K). Due to the weak luminescence of 2, images F and
H were taken from 32 accumulated frames. Scale bar = 25 μm.
2+
ion signal for M0 at m/z = 3946.09 can clearly be assigned to the
dicationic species [{Eu15(μ3-OH)20(PepCO2)10(DBM)10Cl}Cl2]2+.
Peaks marked with an asterisk are due to adduct formation through a
PepCO2H ligand (either from solution or due to the electrospray
process). Inset: Comparison of the calculated (top) and measured
2+
(bottom) isotopic distribution of M0
.
the cells, the intracellular luminescence of the clusters was
measured.
Cluster 1 showed a strong luminescence, while the images of 2
were taken by 32-fold frame accumulation to detect the signal
due to the rather weak luminescence of 2. Compounds 1 and 2
were distributed within the cytoplasm and the nucleus (Figure
4). Additionally, they show a strong accumulation within the
endosomal−lysosomal system. This suggests an endocytotic
uptake and an endosomal escape, accompanied by a subsequent
distribution to the cytoplasmic and nuclear compartments
(Figure 4). To elucidate whether the uptake of the lanthanide
clusters is based on energy-dependent endocytic processes,
cellular uptake was studied for 4 h at 4 °C. Energy depletion at
4 °C severely reduced the uptake, giving rise to the assumption
that endocytosis was involved in the cellular uptake of clusters 1
and 2. Further studies have to be undertaken to pinpoint the
exact endocytic pathway. Using [EuCl3·(H2O)6] and
[TbCl3·(H2O)6] instead of the cluster compounds 1 and 2 as
rare-earth element sources under the same incubation conditions
did not result in any uptake into the cells. To prove the uptake of
the clusters within the cells, a xyλ-scan was performed. By using
confocal microscopy in the TRLLM mode, a xyλ-scan showed
main luminescence emission peaks at about 617 nm for 1 and
493, 553, and 595 nm for 2, which were slightly shifted to higher
wavelengths. This bathochromic shift can be due to aggregation
within the cells or solvent issues (Figure S8). These emission
peaks indicate the presence of clusters 1 and 2 in the cells’
interior; i.e., the cluster molecules are not just adsorbed on the
surface of the cell walls. By using a related method applying z-axis
scanning, it was recently shown that oligonucleotide-templated
silver nanoclusters enter MCF-7 human breast cancer cells.27
In conclusion, a novel structurally defined CPPo monomer-
ligated pentadecanuclear lanthanide hydroxy cluster of formula
[Ln15(μ3-OH)20(PepCO2)10(DBM)10Cl]Cl4 (Ln = Eu (1), Tb
(2)) was prepared and structurally characterized. ESI-MS of
these compounds revealed the retention of the cluster core when
dissolved in alcohols or DMF; however, in EtOH an exchange of
Figure 3. Excitation/emission spectra of 1 and photograph of the
compound in daylight and under 366 nm excitation.
To date, luminescent lanthanide complexes are increasingly
being used as luminescent labels for bioimaging24 as well as for
simultaneous labeling of biological structures in electron
microscopy or magnetic resonance imaging (MRI).25 Europium
and terbium clusters 1 and 2 were tested for their applicability as
luminescent probes in cell culture. To monitor their cellular
uptake and the intracellular routing, we used conventional
fluorescent confocal microscopy and time-resolved long-lived
luminescent microscopy (TRLLM), which is capable of gating
out the undesirable cell-derived short-lived luminescence.26
Although there are many publications on luminescent lanthanide
complexes, only a few of them have yet been used for
luminescence microscopy via TRLLM, since the imaging
requires kinetic stability in water and a so-called sensitizing
unit that generates an efficient antenna effect.26 To determine a
suitable working concentration in cell culture, a MTT viability
assay was performed (Figure S7). The clusters are moderately
toxic, with LD50 = 13.62 μM for 1 and 4.61 μM for 2 in human
cervial carcinoma (HeLa) cells. Eventually, 1 and 2 were applied
in cell culture experiments at 0.1−1 μM concentration using
HeLa cells. By gating out the short-lived autofluorescence from
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ASSOCIATED CONTENT
* Supporting Information
Synthesis and characterization; luminescence data, xyλ-scans,
and viability essay; full citation for ref 20c. This material is
available free of charge via the Internet at http://pubs.acs.org.
■
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AUTHOR INFORMATION
Corresponding Author
roesky@kit.edu
■
Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS
■
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We acknowledge the financial support provided by the Deutsche
Forschungsgemeinschaft (DFG) and the DFG-Center for
Functional Nanostructures (CFN) within Research Area C.
The German Business Foundation (SDW) (fellowship for E.R.),
the Fonds der Chemischen Industrie (fellowship to D.K.K.), and
the Karlsruhe School of Optics & Photonics (KSOP) (fellowship
to D.K.K. and B.R.) are acknowledged.
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