Molecular "light switch" for G-quadruplex DNA: Cycling the switch on and off

Article abstract of DOI:10.1039/c2dt30076a

We report a new G-quadruplex DNA "light switch", where the light switch can be cycled on and off through the successive introduction of G-quadruplex DNA and [Fe(CN)₆]^4- ions.

Full text of DOI:10.1039/c2dt30076a

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COMMUNICATION
Molecular “light switch” for G-quadruplex DNA: cycling the switch
on and off†
Shuo Shi,* Juan Zhao, Xing Gao, Chunyan Lv, Li Yang, Jian Hao, Hailiang Huang, Junliang Yao,
Wenliang Sun, Tianming Yao* and Liangnian Ji
Received 11th January 2012, Accepted 26th March 2012
DOI: 10.1039/c2dt30076a
2
+
We report a new G-quadruplex DNA “light switch”,
where the light switch can be cycled on and off through
the successive introduction of G-quadruplex DNA and
and off processes by successive additions of Co ions and
9
EDTA, respectively. Recently, Li reported a metallointercalator-
based luminescent DNA film and the light-switch behaviour of
the cast film through chemical modulation of the solid–liquid
4
−
[Fe(CN)6] ions.
10
interface. The principle of the emission can be “turned off” by
coordination of various foreign metal ions to a vacant multiden-
tate ligand. These DNA “light switch” complexes may prove to
be useful in applications such as molecular-scale logic gates,
DNA sensing, the detection of mismatches and the signaling of
Since the structure of the DNA double helix was proposed by
Watson and Crick in 1953, new structures of nucleic acids have
continued to emerge at an ever-increasing rate. Among the
different noncanonical DNA motifs, quadruplex DNA structures
are probably the most extensively studied. Such structures are
1
11
DNA–protein binding. However, as the unique properties of
metal complexes have been successfully used to probe duplex
DNA, it is important to note that these complexes are only in the
beginning stages of development and are not as evolved as metal
complexes that bind G-quadruplex DNA. Recently, our labora-
made up of G-quartet subunits, where four coplanar guanines
2
(
G) are linked together by Hoogsteen hydrogen bonds. It has
been suggested that these secondary DNA structures could be
3
involved in the regulation of several key biological processes.
2+
For example, the G-quadruplex has been suggested to act as a
negative regulator of telomere elongation by telomerase in vivo
and is currently considered as a potential target for cancer
tory found that [Ru(phen) (dppz)] can serve as a prominent
2
molecular “light switch” for both G-quadruplexes and i-motif
DNA, which prefers binding to G-quadruplexes over the
4
12
therapy. In addition, many promoter elements within the human
i-motif. Herein, we describe the first example of a new G-quad-
ruplex DNA “light switch” complex, which can be repeatedly
cycled on and off through the addition of external agents.
Scheme 1 illustrates how the switch can be cycled through the
genome contain G-rich sequences that are thought to be involved
3
,5
in controlling gene expression.
These potential roles of
G-quadruplex DNA structures have stimulated the search for
specific molecules that may serve either as biological probes for
these structures or perhaps as therapeutic agents.
4−
successive introduction of [Fe(CN)6] ions and G-quadruplex
DNA. The synthetic routes for the preparation of the [Ru-
2+
The interaction of nucleic acids with small molecules has
been a primary area of interest and research for over half a
(
bpy) (dppzi)] complex are shown in Scheme 2 ((dppzi) =
2
dipyrido[3,2-a:2′,3′-c]phenazine-10,11-imidazole). Human telo-
meric fragments of 5′-AGGGTTAGGGTTAGGGTTAGGG-3′
6
century. Among these small molecules, polypyridyl complexes
incorporating planar aromatic ligands have attracted much atten-
7
8
tion. The pioneering work of Murphy and Barton has provided
detailed information about the recognition and reactions of
double helical DNA by transition metal complexes. They first
2
+
reported the luminescence of [Ru(L) (dppz)] ((L) = bpy (2,2′-
2
bipyridine) or phen = (1,10-phenanthroline) and dppz = (dipyr-
ido[3,2-a:2′,3′-c] phenazine)) to be almost non-emissive in water
but “switched on” in the presence of duplex DNA. Since then,
many efforts have focused on the design and development of
molecular “light switch” complexes. Dunbar and Turro have
achieved chemical cycling of the molecular “light switch” on
Department of Chemistry, Tongji University, Shanghai, China. E-mail:
shishuo@tongji.edu.cn, tmyao@tongji.edu.cn; Fax: +86-21-6598-2287;
Tel: +86-21-6598-3292
†
Electronic supplementary information (ESI) available: synthetic pro-
2+
cedures for [Ru(bpy)
2
(dppzi)] and details of the experimental materials
Scheme 1 Schematic illustration of the light switching behaviour of
and methods. See DOI: 10.1039/c2dt30076a
the ruthenium complex in the presence of G-quadruplex DNA (G-4).
This journal is © The Royal Society of Chemistry 2012
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Scheme 2 The synthetic routes for the preparation of the [Ru-
2
+
(
2
bpy) (dppzi)] complex.
(denoted 22AG) were chosen for this investigation, of which the
crystal and solution structures are known. The structure and the
stability of the G-quadruplex depend on the monocations; the
NMR structure of 22AG in the presence of Na is known to be
2+
Fig. 1 Absorption spectra of [Ru(bpy)
2
2
(dppzi)] in the presence of
+
+
2AG in (a) K and (b) Na buffer (100 mM KCl/NaCl, 10 mM Tris,
pH 7.0) ([Ru] = 10 μM, [DNA] = 0–100 μM). Insets: plots of (ε
(ε − ε ) vs. [DNA] for the titration of the Ru(II) complexes.
+
a
f
− ε )/
an antiparallel basket quadruplex; however, the same sequence
favors a mixed parallel/antiparallel structure in the presence of a
b
f
+
13
K solution.
The electronic spectra of [Ru(bpy) (dppzi)]
2
+
have been
Hypochromism and red shifting indicates the strong interactions
between the DNA bases and the complex. The intrinsic binding
constants, K , of [Ru(bpy) (dppzi)] and the antiparallel basket
quadruplex and mixed parallel/antiparallel quadruplex were
determined to be 9.5 × 10 M (s = 1.3) and 5.1 × 10 M
2
characterized by an intense ligand-centered (LC) transition in the
UV region and a metal-to-ligand charge transfer (MLCT) in the
visible region, which are typical of polypyridylruthenium(II)
2+
b
2
14
5
−1
5
−1
complexes. The ultraviolet bands around 287 nm for [Ru-
2
+
2+
(
bpy) (dppzi)] can be attributed to the (bpy) π → π* transition;
(s = 1.0), respectively. That is to say, [Ru(bpy) (dppzi)] prefer-
2
2
2
+
the band at 430 nm for [Ru(bpy) (dppzi)] can be attributed to
entially binds to the mixed parallel/antiparallel quadruplex over
the antiparallel basket quadruplex. The exact data are shown in
Table S1 (ESI†).
To gain insight into the interaction between [Ru-
(bpy) (dppzi)] and the G-quadruplex, we examined the ability
to stabilize G-quadruplex DNA by
thermal denaturation profiles. In accordance with previous
studies, 295 nm was chosen to study the influence of the
2
the overlap of Ru(dπ) → bpy (π*) and Ru(dπ) → dppzi (π*).
Apart from these, the absorption band around 386 nm can be
assigned to the intraligand (IL) transition of dppzi.
+
+
2+
The interaction with G-quadruplex DNA in either a K or Na
2
2+
buffer was evident from the absorption titration spectra. The
changes in the spectral profiles during titration are shown in
Fig. 1. The hypochromism and red shift in the intraligand
absorption band (∼386 nm) of the dppzi ligand, as well as the
MLCT band, are a little more pronounced for the mixed parallel/
of [Ru(bpy) (dppzi)]
2
15
complex on the stability of the G-quadruplex. As expected, the
+
+
melting profiles of 22AG in the absence of K and Na showed
almost no transition (data not shown), suggesting that it did not
form a stable G-quadruplex structure. As for the dissociation of
+
antiparallel G-quadruplex (K buffer) compared to the form
+
bound to the antiparallel basket G-quadruplex DNA (Na
+
buffer). For example, the addition of 22AG to a solution of [Ru-
the G-quadruplex, the Tm of the monovalent K ion induced
intramolecular G-quartet structure of the 22AG sequence was
more stable than its Na counterpart. Concentration-dependent
melting curves for each G-quadruplex DNA upon binding to
2+
+
(
bpy) (dppzi)] in K buffer led to a 3 nm red shift and 40.2%
2
+
hypochromism of the band at 386 nm (Fig. 1a) and addition of
+
antiparallel basket G-quadruplex DNA in Na buffer led to the
2+
same red shift and 35.0% hypochromism of the band at 386 nm
[Ru(bpy) (dppzi)] are shown in Fig. 2. Upon the addition of
2
(Fig. 1b). The isosbestic points are located at 322 and 477 nm.
the complex, i.e., changing the [Ru]/[DNA] ratio of 1 : 1 to 3 : 1
5790 | Dalton Trans., 2012, 41, 5789–5793
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2
+
2
Fig. 3 Emission spectra of [Ru(bpy) (dppzi)] in the presence of
Fig. 2 Normalized UV melting curves for 5 μM of the antiparallel
4−
increasing amounts of (a) [Fe(CN)
[Ru] = 5 μM, [DNA] = 0–50 μM in 100 mM K buffer. The arrows
6
]
or (b) G-quadruplex DNA;
G-quadruplex (a) and the mixed-hybrid G-quadruplex (b) in the absence
+
2
+
and the presence of [Ru(bpy)
2
(dppzi)] at different [Ru]/[DNA] ratios
4−
show the emission intensity changes upon increasing [Fe(CN)
G-quadruplex DNA concentrations.
6
]
ion or
(DNA alone (■), 1 : 1 ( ), 3 : 1( ), 5 : 1 ( )). The stability of the
G-quadruplex DNAwas assessed by UVabsorbance at 295 nm.
intensity of the complex is quenched again. Interestingly, by
adding an excess of G-quadruplex DNA to the buffer system
and 5 : 1, the Tm of the G-quadruplex DNA increased dramati-
2+
cally, which is comparable to that observed for classic G-quadru-
containing G-quadruplex DNA-bound [Ru(bpy) (dppzi)] with
2
16
2+
4−
plex binders. At a ratio of 5 : 1 ([Ru(bpy) (dppzi)] to 22AG),
[Fe(CN)6] ions, the emission intensity can be recovered again.
A similar phenomenon was observed in the Na buffered sol-
2
+
the transition temperature of the G-quadruplex increased from
+
5
5.3 to 64.3 °C in Na buffer and increased from 65.3 to 79.4 °C
ution as well. Therefore, it is interesting to investigate whether
+
2+
in K buffer, in which an increase in the melting temperature of
the quadruplex indicated an effective stabilizing effect.
In the absence of G-quadruplex DNA, [Ru(bpy) (dppzi)]
the photoluminescence of DNA-bound [Ru(bpy) (dppzi)]
could be tuned by the successive introduction of [Fe(CN)6]
2
1
6
4−
2+
2
ions and G-quadruplex DNA. In an appropriate buffer (100 mM
+
+
can emit luminescence at the excited wavelength of 440 nm in a
buffer solution at ambient temperature and its maximum appears
K or Na ) and at a ratio of 1 : 1 (ruthenium to nucleotide), the
emission was monitored at the emission maxima of the complex
4−
4−
at 625 nm. Upon addition of [Fe(CN) ] ions, the luminescence
at various concentrations of [Fe(CN)6]
and G-quadruplex
6
2+
of [Ru(bpy) (dppzi)] can be fully quenched in the absence of
DNA at 20 °C. Fig. 4 shows the changes in the relative emission
2
2
+
the G-quadruplex (Fig. 3a). The quenching is due to a reductive
intensity of [Ru(bpy) (dppzi)] bound to G-quadruplex DNA as
2
17
4−
electron transfer. The results of the emission titrations for [Ru-
[Fe(CN)6] ions and G-quadruplex DNA are added succes-
2
+
(
bpy) (dppzi)]
with G-quadruplex DNA are illustrated in
sively, thus flipping the DNA “light switch” on and off over a
series of cycles. In this system the emission quenching and
recovery is observed immediately following the addition of
2
+
Fig. 3b. Upon addition of G-quadruplex DNA in 100 mM K
buffer, the emission intensities of the [Ru(bpy) (dppzi)]
2+
2
4
−
complex increase to around 2.46 times larger than the original.
either [Fe(CN)6] ions or G-quadruplex DNA, respectively.
To perform a detailed thermodynamic study of G-quadruplex
2
+
This implies that [Ru(bpy) (dppzi)] can interact with G-quad-
2
2
+
ruplex DNA and be protected by DNA efficiently. Upon addition
DNA molecules and [Ru(bpy) (dppzi)] , fluorimetric titrations
2
4
−
+
18
of [Fe(CN)6] ions into the 100 mM K buffer system contain-
were performed at 15, 30, 37 and 45 °C. The binding constants
2
+
2+
ing [Ru(bpy) (dppzi)] with G-quadruplex DNA, the emission
(K ) for the complex formed between [Ru(bpy) (dppzi)] and
2
b
2
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Fig. 5 The minimized model of the complex between [Ru-
2
+
(bpy)
2
(dppzi)] and the 22AG antiparallel G-quadruplex (a) and the
mixed-hybrid G-quadruplex (b). G is shown in green, A is shown in red,
2
+
2
+
T is shown in cyan and [Ru(bpy)
2
(dppzi)] is shown in brown and blue.
Fig. 4 The relative emission intensity of [Ru(bpy)
2
(dppzi)] upon
4−
successive additions of G-quadruplex DNA (G-4) and [Fe(CN)
6
]
in
+
2+
1
00 mM K buffer.
To compare the DNA binding of [Ru(bpy) (dppzi)] for G-
2
quadruplex DNA and duplex DNA, emission titrations for [Ru
2
+
G-quadruplex DNA were determined from a complete titration at
the particular temperature. The values of the binding constant
were found to be comparable to the values obtained from the
(bpy) (dppzi)] with calf thymus DNA (CT-DNA) were per-
2
formed and are presented in Fig. S1 (ESI†). Upon addition of
CT-DNA in 100 mM K buffer, the emission intensities of the
[Ru(bpy) (dppzi)] complex increase to around 2.03 times that
of the original. This implies that [Ru(bpy) (dppzi)] can interact
with CT-DNA and also be protected by DNA efficiently. Though
[Ru(bpy) (dppzi)] showed a prominent G-quadruplex binding
+
0
0
2+
absorption titration. The thermodynamic parameters, ΔG , ΔS
2
0
2+
and ΔH , were calculated from the van’t Hoff equation and are
reported in Table S2 (ESI†). It can be seen that the binding of
2
2+
2+
[
Ru(bpy) (dppzi)] to G-quadruplex DNA is characterized by
2
2
negative enthalpy and negative entropy changes. The negative
ΔG values suggest that the energy of the complex–DNA adduct
affinity, a modest selectivity for the quadruplex over the duplex
was observed. It still suffered from the classic drawback of lack
of specificity for the quadruplex. On the other hand, a dramatic
preference for the quadruplex over the i-motif was observed.
Upon addition of i-motif DNA in the same buffer, the fluor-
escence of the complex hardly increased at all (Fig. S2) (ESI†),
0
is lower than the sum of the energies of the free complex and
0
DNA. The negative ΔH values suggest that the binding of the
complex to DNA is exothermic and driven by enthalpy. The
negative entropy values indicate that the degree of freedom of
the Ru(II) complex is decreased after binding and that the DNA
conformational freedom is also reduced upon complex–DNA
binding.
2+ 12
which is similar to star molecular [Ru(phen) (dppz)] .
2
Molecular docking studies were carried out to determine the
2+
binding mode between [Ru(bpy) (dppzi)] and the G-quadru-
2
22
Small molecules can potentially bind to a G-quadruplex DNA
by externally stacking on the G-quartets, intercalating between
the quartets or non-specifically binding to some random location
plex, which corroborates the experimental results. The antipar-
allel basket NMR G-quadruplex structure (PDB 143D) and a
26-mer mixed hybrid-type NMR G-quadruplex structure (PDB
2HY9) were used as templates for the docking studies. To
compare both conformations, we removed two adenines from
19
on the DNA strand. Molecules bound to the surface of the
helix or quartets will be accessible to the quencher, while those
intercalating inside the helix or quartets will be protected from
23
each end of the mixed hybrid-type structure. As shown in
20
the quencher. Ferrocyanide ions proved to be excellent quench-
Fig. 5, the docking study confirms that each intramolecular G-
4
−
2+
ers for the complex in the presence of DNA. The [Fe(CN)6]
quadruplex molecule binds to one [Ru(bpy) (dppzi)] molecule.
2
ion will be prevented from entering the helix due to an electro-
static barrier as a result of the phosphate group and, conse-
quently, very little quenching will be observed in the case of true
intercalators. As illustrated in Fig. 4, the luminescence of DNA-
It has previously been shown that G-quadruplex binders can
3,4,22,23
stack on the surface of both terminal G-quartet planes.
2+
[Ru(bpy) (dppzi)] contains a square π-aromatic surface and the
2
dppzi ligand prefers to stack in the center of the terminal G-
quartet end. For the antiparallel basket G-quadruplex structure,
both diagonal loop and parallel loop binding positions were con-
2
+
bound [Ru(bpy) (dppzi)] could be tuned by the successive
2
4
−
introduction of [Fe(CN)6] ions and G-quadruplex DNA. These
results therefore suggest that the binding modes of [Ru-
2+
sidered. When [Ru(bpy) (dppzi)] binds in the diagonal loop
2
2+
(
bpy) (dppzi)] may not be intercalative. Given the large and
position, π–π stacking becomes less stable than in the parallel
2
flat aromatic moiety of the dppzi ligand and the structures of the
loop binding position, as shown by energy calculations. So [Ru-
2
+
2+
G-quadruplex, we propose that [Ru(bpy) (dppzi)] stacks on
(bpy) (dppzi)] prefers to stack on the center between the paral-
2
2
the ends of the G-quadruplexes like a similar complex,
lel loop and the terminal G-quartet (Fig. 5a). The predicted
II
21
2+
[
Pt (dppz-COOH)(NΛC)]CF SO , does. This binding mode is
favorable binding site between [Ru(bpy) (dppzi)] and the
3
3
2
4
−
not very strong and both G-quadruplex DNA and [Fe(CN) ]
can access the [Ru(bpy) (dppzi)] complex easily. The environ-
ment of [Ru(bpy) (dppzi)] will change depending on the
amount of G-quadruplex DNA and [Fe(CN) ] and the lumi-
mixed-hybrid G-quadruplex DNA was found to be stacking on
the external G-quartets at the 5′ end of the oligonucleotide
(Fig. 5b). The modeling study revealed that the complex binds to
the mixed-hybrid G-quadruplex and antiparallel basket G-quad-
ruplex with a calculated binding energy of ca. −13.4 and
6
2
+
2
2
+
2
4
−
6
2
+
nescence of the [Ru(bpy) (dppzi)] complex can thus be tuned.
2
5792 | Dalton Trans., 2012, 41, 5789–5793
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1
−
10.0 kcal mol− , respectively, which is comparable with the
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energies obtained from the fluorimetric titration Table S2 (ESI†).
It was also noteworthy that [Ru(bpy) (dppzi)] possessed a
2
+
2
much more favorable binding interaction (lower binding free
energy) with the hybrid-type G-quadruplex than the antiparallel
basket G-quadruplex. Such reliable end-stacking of compounds
onto the G-quartet are in agreement with previously reported
aromatic quadruplex ligands. Thus, the molecular modeling
studies explained why the photoluminescence of [Ru-
bpy) (dppzi)] can be tuned by the successive introduction of
2
Fe(CN)6] ions and G-quadruplex DNA and confirmed the
excellent complementarity in the binding modes.
In summary, cycling of the G-quadruplex DNA “light switch”
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(
[
4
−
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5
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2+
off and on has been accomplished for [Ru(bpy) (dppzi)]
2
4
−
through the successive introduction of [Fe(CN)6] ions and G-
quadruplex DNA, respectively. To the best of our knowledge,
this work presents the first example of a reversible G-quadruplex
DNA light switch. Furthermore, the mechanism of cycling of the
G-quadruplex DNA “light switch” in this work is different from
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9
,10
the mechanism reported in other “light switches”.
The switch
4−
can be cycled through the competition of [Fe(CN)6] ions and
G-quadruplex DNA. The discovery of the binding features of
2
+
[
Ru(bpy) (dppzi)]
with G-quadruplex DNA may show
2
promise for probing G-quadruplex DNA and provide a more
comprehensive understanding of the molecular recognition of
G-quadruplex DNA.
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1
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This work was supported by the National Natural Science Foun-
dation of China (20901060, 31170776, 20871094, 81171646)
and the Fundamental Research Funds for the Central
Universities.
1
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Dalton Trans., 2012, 41, 5789–5793 | 5793