Branched silica nanostructures oriented by dynamic G-quadruplex transformation

Article abstract of DOI:10.1016/j.materresbull.2010.08.008

Polymorphic G-quadruplexes including stacked G-quartet planes are potentially promising DNA templates beyond Watson-Crick duplexes to construct inorganic nanostructures. In this work, a novel G-rich oligonucleotide that can be modulated from the antiparallel G-quadruplex to multi-stranded supermolecular assemblies was designed. Based on this dynamic G-quadruplex transformation, an interesting leaf-vein silica nanostructure with regular branched intervals was constructed. The G-quadruplex assembly structure was found to play a significant role in the organization of the silica structures.

Full text of DOI:10.1016/j.materresbull.2010.08.008

Materials Research Bulletin 45 (2010) 1954–1959
Contents lists available at ScienceDirect
Materials Research Bulletin
journal homepage: www.elsevier.com/locate/matresbu
Branched silica nanostructures oriented by dynamic G-quadruplex
transformation
Jinli Zhang a, Lin Zheng a, Xian Wang a, Ying Xiao b, Yi Lu c, Wei Li b,
*
a Key Laboratory of Systems Bioengineering School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China
b Key Laboratory for Green Chemical Technology, Ministry of Education School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China
c Department of Chemistry, University of Illinois at Urbana-Champaign Urbana, IL 61801, USA
A R T I C L E I N F O
A B S T R A C T
Article history:
Polymorphic G-quadruplexes including stacked G-quartet planes are potentially promising DNA
templates beyond Watson-Crick duplexes to construct inorganic nanostructures. In this work, a novel G-
rich oligonucleotide that can be modulated from the antiparallel G-quadruplex to multi-stranded
supermolecular assemblies was designed. Based on this dynamic G-quadruplex transformation, an
interesting leaf-vein silica nanostructure with regular branched intervals was constructed. The G-
quadruplex assembly structure was found to play a significant role in the organization of the silica
structures.
Received 1 January 2010
Received in revised form 22 June 2010
Accepted 22 August 2010
Available online 27 August 2010
Keywords:
A. Inorganic compounds
A. Nanostructures
ß 2010 Elsevier Ltd. All rights reserved.
C. Atomic force microscopy
1. Introduction
wires of A15G15 [19,20], the G-lego of G11T [21], etc., have been
studied due to their advantage in generating unique nanopatterns
DNA self-assembly is increasingly recognized as an effective
way to construct well-defined nanostructures for directing the
organization of inorganic nanomaterials owing to its advantage
of programmable molecular recognition [1–6]. Several self-
assembled DNA nanopatterns based on the conventional
Watson–Crick duplex have been developed to organize the
oxide nanoparticles, such as the rod-like and circular silica fibers
[7,8], titania nanotubes [9], magnetic nanowires [10], etc.
Despite the progresses that have been made, using self-
assembled DNA templates to create hybrid nanomaterials with
increasingly complicated structures is still a principle challenge;
meeting such a challenge will not only enable precise spatial
positioning of individual units in nano-fabrication [11] but also
promote the development of bioinspired synthesis of novel
function materials [12].
over DNA duplexes. However, the potential of G-quadruplex in
constructing highly ordered oxide nanostructures has not been
fully explored.
Herein, we reported a novel asymmetric G-quadruplex G2T4G4
that can be modulated to transform into multi-stranded super-
molecular assemblies. Based on this original G-quadruplex
transformation, leaf-vein nanostructures of silica with regular
branched intervals were organized.
2. Experimental
G-rich DNA oligonucleotides of G2T4G4, G3T4G4 and G4T4G4
were purchased from the Japanese Takara Bio (Dalian) with the
purity higher than 98%. Before the experiments, all samples were
diluted to a final concentration of 40
mM in a 100 mM NaCl
One approach to meeting the above challenge is to construct
nanostructures using DNA beyond Watson–Crick duplex struc-
tures. Guanine (G)-rich oligonucleotides can self-assemble into
polymorphic quadruplexes via stacking of G-quartets comprising
of eight intermolecular hydrogen bondings (e.g., N2–Hꢀ ꢀ ꢀN7, N1–
Hꢀ ꢀ ꢀO6) between neighboring guanine residues [13–15]. Based on
the self-association of G-quadruplexes, a number of G-wire
structures involving the linear wire of G4T2G4 [16–18], the frayed
aqueous solution (pH 5.9) or 100 mM KCl as mentioned in the text.
The DNA samples were then annealed at 95 8C for 5 min, slowly
cooled to 4 8C, and holding at this temperature for several hours. To
synthesize DNA-silica hybrid nanoparticles, an ethanol solution of
3-aminopropyl trimethoxysilane (APTMS) (5
added into an aqueous solution of G-rich DNA (400
m
L, 10%, v/v) was
L, 40 M)
m
m
under stirring, with a molar ratio APTMS/DNA of 179. The mixture
was allowed to react at 20 8C for 18 h. The generated DNA-silica
nanostructures were characterized by AFM and high-resolution
transmission electron microscope (HRTEM). As a control, silica
nanoparticles were synthesized under the similar conditions in the
absence of DNA.
* Corresponding author. Tel.: +86 22 27890643; fax: +86 22 27890643.
E-mail address: liwei@tju.edu.cn (W. Li).
0025-5408/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.materresbull.2010.08.008

J. Zhang et al. / Materials Research Bulletin 45 (2010) 1954–1959
1955
CD spectra were obtained from a Jasco J-810 spectropolarimeter
equipped with a Julabo temperature controller. Thermal denatur-
ation profiles were collected in units of millidegrees as a function
of temperature. The heating rate was fixed at 1.0 8C minꢁ1. CD
stopped-flow kinetic measurements were performed with SFM300
multi-mixing instruments (Bio-logic). Time courses were recorded
in units of millidegrees at 20 8C with a sample period of 200 ms at
293 nm upon mixing the aqueous solution of G2T4G4 and APTMS-
containing ethanol solution at the volume ratio of 9:1. Data sets
from at least four experiments performed under identical
conditions were averaged and then fitted to a single-exponential
equation using Igor software (Wave-Metrics Inc., USA).
volume. 20 mL volume of the sample was deposited in a depression
slide and the spectra were recorded.
The zeta potential of the silica particles in solution formed by
APTMS hydrolysis was determined using a Zeta Plus zeta potential
analyzer (Malvern, UK).
HRTEM images were measured with a Tecnai G2 F20 field beam
electron microscope (FEI Corp.) with an acceleration voltage of
200 kV. Elemental analysis was done by energy dispersive X-ray
(EDX) spectra. The samples for HRTEM characterization were
prepared by depositing 5
mL solution on a carbon-coated copper
grid and drying at room temperature.
Native polyacrylamide gel electrophoresis (PAGE) measure-
ments were carried out to characterize the electrophoresis
mobility of DNA structures using 20% acrylamide [29:1 acrylam-
ide/bis(acrylamide)] at 10 V cmꢁ1 and 4 8C. The gel was stained in a
3. Results and discussion
3.1. Self-assembly of G-rich sequences
3
m
g mLꢁ1 Gelred solution for 30 min. The intensity of each band in
Our approach began with the design of G-rich oligonucleotide
G2T4G4 compared with the control sequences of G3T4G4 and
G4T4G4. We analyzed the self-assembly structure of G2T4G4,
G3T4G4 and G4T4G4 in the presence of 100 mM Na+ by CD, PAGE,
AFM and SER spectra measurements. CD spectra of G4T4G4 display
the typical peak at 293 nm (Fig. 1a), suggesting the formation of
dimeric antiparallel quadruplex structures involving four G-
quartet planes [23], which show a fast mobility in the native
PAGE images (Fig. 1b). When the number of guanine at 50 terminus
of the sequence decreases from 4 to 3 and then to 2, the major peak
at 293 nm still exists in CD spectra, but the melting temperature of
the sequence decreases from 67.5 to 24 8C and the electrophoresis
mobility becomes slower (Fig. 1a and b). However, the relative low
mobility band of G2T4G4 is obviously faster than the 20 bp duplex
marker. Combining with the previous work based on NMR studies
[24,25], it is suggested that G3T4G4 forms the dimmer antiparallel
G-quadruplex with overhanging guanine residues, while G2T4G4
forms the less compact antiparallel G-quadruplex with much more
the native PAGE images was determined using a GDS8000 system
(UVP, Inc., USA).
AFM measurements were carried out under constant repulsive
force mode by AFM (AJ-IIIa, Aijian nanotechnology Inc., China).
Samples were prepared for measurements by dropping 10
mL
solution onto a freshly cleaved mica substrate for 10 min,
followed by washing with water and rapidly drying by N2. All
AFM images were obtained in the tapping mode in air under
normal conditions.
SER spectra were measured with a Renishaw MKI-2000 laser
confocal microscopy Raman spectrometer with a CCD detector and
a holographic notch filter (Renishaw Ltd., Gloucestershire, UK). The
spectral resolution for this experiment was 2 cmꢁ1. Radiation of
633 nm from an air-cooled argon ion laser was used for the SER
spectra excitation. For SER spectra, citrate-reduced Au nanopar-
ticles (with an average diameter of 42 nm), prepared by a standard
protocol [22], were added into the DNA solution with equal
[(Fig._1)TD$FIG]
Fig. 1. (a) CD spectra of G2T4G4, G3T4G4, G4T4G4 in 100 mM Na+ solution (pH 5.9) at 20 8C. The inset indicates the CD melting curves of each DNA sequence. (b) Native PAGE
images of G2T4G4, G3T4G4 and G4T4G4 in 100 mM Na+ solution (pH 5.9) at 10 V cmꢁ1 and 4 8C. The first lane in the left is the 20 bp DNA marker. AFM images of self-assemblies
of (c) G2T4G4, (d) G3T4G4, (e) G4T4G4 in 100 mM Na+ solution (pH 5.9).

[
J. Zhang et al. / Materials Research Bulletin 45 (2010) 1954–1959
Fig. 2. (a) CD spectra of G2T4G4 in the absence of ions, in the presence of 100 mM Na+ and 100 mM K+ (pH 5.9). (b) CD spectra of G2T4G4 in 100 mM Na+ at different ethanol
content at 20 8C.
guanine residues overhung at the terminus. AFM images reflect the
differences of the self-assembly structures of these three G-rich
sequences. It is illustrated that G4T4G4 only forms spheres with an
average height of 2.0 nm (Fig. 1e), G3T4G4 forms a few twin-sphere
nanoparticles with an average height of 2.0 nm owing to the
potential matches between overhanging guanines, while G2T4G4
forms wire-like nanostructures with a height range of 0.6–1.4 nm
(average height 1.0 ꢂ 0.16 nm) and a length range of 0.3–1.7 mm
together with small spheres in a height of 1.1 nm (Fig. 1c). These wire-
like nanostructures of G2T4G4 are attributed to base-pairings between
the terminal overhanging guanines. SER spectra (Fig. 1S) display the
structural similarity among G4T4G4, G3T4G4 and G2T4G4, as well as a
small peak shift around 1482 cmꢁ1, which will be discussed in the
next section.
It is known that potassium ions are superior in stabilizing the G-
quadruplex rather than sodium ions [26]. We compared confor-
mational structures of G2T4G4 in the presence of potassium ions
with those in the presence of sodium ions. CD spectra of G2T4G4 in
100 mM K+ exhibit a strong positive peak around 263 nm and a
shoulder around 293 nm, suggesting the formation of both the
parallel and antiparallel G-quadruplex (Fig. 2a). As the potassium
ions increased from 1 to 400 mM, native PAGE images display a fast
mobility band corresponding to dimeric antiparallel G-quadru-
plexes and a slow band for four-stranded parallel G-quadruplexs
(Fig. S2). AFM images of G2T4G4 in 100 mM K+ appear dispersed
nanoparticles with the modal height around 1.1 and 2.5 nm,
respectively (Fig. S3).
We further find that even in the presence of Na+ the G2T4G4
assembly structure can be modulated by the solvent content. With
the increase of the ethanol content, CD spectra of G2T4G4 in the
presence of Na+ gradually show the dominated peak at 265 nm
corresponding to the parallel G-quadruplex [27] (Fig. 2b). The
ethanol induced transition has two isoelliptic points at 249.5 and
216 nm, suggesting the existence of multi-state structural transi-
tion in the system, which is consistent with the appearance of the
secondary melting temperature (Tm) in the CD melting curves as
the ethanol concentration is higher than 40% (v/v) (Fig. S4).
Similarly, Smirnov and Shafer have reported that addition of
ethanol can stabilize the G-quadruplex of thrombin binding
aptamer [28].
G2T4G4, the zeta potential of silica nanoparticles turns to be
ꢁ18 mV, illustrating the occurrence of interactions between
amino-coated silica and G2T4G4. Previous work also reported that
amino-coated silica can interact with the negatively charged DNA
molecules [7,30].
Fig. 3 shows significant variations of SER spectra and CD
spectra of G2T4G4 upon mixing with APTMS ethanol solution. SER
spectra of G2T4G4 display the typical peaks at 1238 cmꢁ1
corresponding to the base dT, 1377 cmꢁ1 for both dT and dG,
1324 and 1333 cmꢁ1 reflecting the C20-endo/syn dG and C20-endo/
anti dG conformation, as well as that at 1581 cmꢁ1 indicating the
hydrogen bonding of guanine involving exocyclic NH2 donor sites
[31–33]. It is worthwhile to mention that the peak at 1484 cmꢁ1 is
the indication of solvated guanine N7 site, while the peak at
1482 cmꢁ1 indicates the Hoogsteen N7 hydrogen bonding of
guanines [32]. As the number of 50 terminal guanine residues of
G4T4G4 reduces to 2, the peak shifts from 1482 to 1484 cmꢁ1
(Fig. S1), indicating that the conformation of G2T4G4 is not so same
as the symmetric antiparallel G-quadruplex of G4T4G4, especially
there is less Hoogsteen base-pairings between guanine residues of
G2T4G4 molecules. Upon mixing with APTMS ethanol solution, the
relative intensity of 1484 cmꢁ1 is obviously enhanced, suggesting
more solvated guanine N7 sites exist in the mixture of G2T4G4 and
silica.
CD spectra indicate diminishing of the typical G-quadruplex
peak near 293 nm after mixing with APTMS ethanol solution, but
the melting curve shows a transition temperature of 42 8C with less
cooperative, much higher than that of G2T4G4. It is illustrated that
as the hydrolysis reaction goes on the interactions between amino-
coated silica and DNA make the unstable G-quadruplex of G2T4G4
transform into a multi-stranded supermolecular structure. This
structural transformation happens simultaneously with the
hydrolysis reaction of APTMS, of which the observed rate constant
is kobs 293 nm = 0.2479 ꢂ 0.0522 sꢁ1 determined by CD stopped-flow
experiments. In previous work, the dissociation rate constant of G-
quadruplex resulted from mixing with its complementary sequence
was in the magnitude order of 10ꢁ3 sꢁ1 in the presence of sodium ions
at 20 8C [34].
DNA-silica hybrid nanostructures formed in 18 h hydrolysis
reaction of APTMS were characterized by AFM images. As shown in
Fig. 4, well-ordered leaf-vein nanostructures with regular interval
branches were observed. It was clear that both patterned trunks
and branches comprise of nanoparticles with average height of
55.5 ꢂ 11.2 nm, and the interval between neighboring major
branches is uniformly about 1.3 ꢂ 0.2 mm. Such regularly branched
DNA-silica nanostructures are quite different from the reported
fractal-patterned dendritic nanostructures of metal nanoparticles
[35,36] or polymers [37], grown under the mechanism of diffusion-
3.2. Self-organization of DNA-silica hybrid nanostructures
Upon adding APTMS ethanol solution into the aqueous
solution, the hydrolysis reaction of this organosilane occurs
immediately to form amino-coated silica nanoparticles [29], and
the zeta potential of the silica nanoparticles synthesized without
DNA was 2.5 mV at pH 5.9. When the aqueous solution contains

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J. Zhang et al. / Materials Research Bulletin 45 (2010) 1954–1959
1957
Fig. 3. (a) SER spectra, (b) CD spectra, and (c) CD melting curves of G2T4G4 (100 mM Na+, pH 5.9) before and after mixing with APTMS ethanol solution. (d) Kinetic time course
recorded at 293 nm upon mixing G2T4G4 and APTMS-containing ethanol solution at 20 8C.
limited aggregate. Further, similar branched nanostructures were
observed by HRTEM images (Fig. 5), which display the nanostructures
consisting of nanoparticles with an average diameter of 38.0 ꢂ
8.6 nm, surrounded by organic compounds, of which the intensity
gradually decreases under the irradiation of electron beams. The EDX
spectra (Fig. 5b) of the branched aggregates indicate the co-existence
of element C, N, O, P, and Si, which are major components of DNA and
the hydrolysis products of APTMS. The construction difference of
DNA-silica nanostructures between HRTEM and AFM images is
attributed to the epitaxy and electriferous property of the mica
against the copper grid of TEM [38,39]. In addition, in the absence of
DNA, silica nanoparticles grow quickly to the modal size around
95 nm after 10 min hydrolysis reaction of APTMS (Fig. S5a) and
continuously grow into large aggregates in 3 h hydrolysis reaction
[(Fig._4)TD$FIG]
Fig. 4. (a) AFM images of leaf-vein nanostructures formed under the template of G2T4G4 (100 mM Na+, pH 5.9). (b) An enlarged image of (a). (c) The height profile along the
red line in (a), the blue ladder shows the interval of the branches. (For interpretation of the references to color in this figure legend, the reader is referred to the web version
of the article.)

[
J. Zhang et al. / Materials Research Bulletin 45 (2010) 1954–1959
Fig. 5. (a) TEM images of branched G2T4G4-silica nanostructures in 100 mM Na+ (pH 5.9). (b) Elemental composition of the nanostructures in (a) determined by EDX.
(Fig. S5b). Therefore, it is concluded that the interaction between
G2T4G4 and amino-coated silica results in the formation of the
regularly branched nanostructures.
respectively, therefore it is concluded that the multi-stranded
wire-like assemblies of G2T4G4 in the presence of Na+ play an
important role in orienting the organization of leaf-vein silica
nanostructures.
Moreover, we found that the DNA-silica nanostructures were
sensitive to the conformational structure of DNA template. In the
presence of 100 mM K+, G2T4G4 mainly forms stable four-
stranded parallel G-quadruplex with the melting temperature of
73 8C. Upon adding APTMS ethanol solution into the G2T4G4-K+
aqueous solution, both CD and SER spectra (Fig. 6a and b) show
few variations except that the melting temperature decreases
from 73 to 60.5 8C, suggesting no structural transformation
occurs for the four-stranded parallel G-quadruplex. Fig. 6c
indicates the AFM image of the silica nanostructures formed in
G2T4G4-K+ solution, which were sphere particles with a height
distribution around 4 and 6 nm (Fig. S6). In combination with the
different self-assemblies of G2T4G4 in the presence of Na+ and K+,
The ethanol content can also influence the DNA-silica hybrid
structure. In the case of 40% (v/v) ethanol content, the melting
curve of G2T4G4 shows two transition temperature (39 and
54.5 8C), while the melting temperature of G2T4G4 turns to be
46 8C after mixing with APTMS ethanol solution. The intensity
of peaks at both 265 and 293 nm becomes lower in the CD
spectra (Fig. 7a and b). Fig. 7c displays AFM images of similar
branched DNA-silica nanostructures formed in 40% (v/v) ethanol
solutions, with the average height of individual nanoparticle
around 30 nm. Such smaller particle size is attributed to slower
hydrolysis reaction rate of APTMS in high ethanol content
solutions. The similarity of them demonstrated that multi-
[(Fig._6)TD$FIG]
Fig. 6. (a) CD spectra and (b) SER spectra of G2T4G4 (100 mM K+, pH 5.9) before and after mixing with APTMS ethanol solution at 20 8C. The inset: CD melting curves of G2T4G4
in the above conditions. (c) AFM images of G2T4G4-silica nanostructures formed in the presence of 100 mM K+ (pH 5.9).

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J. Zhang et al. / Materials Research Bulletin 45 (2010) 1954–1959
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Fig. 7. (a) CD spectra and (b) CD melting curves of G2T4G4 in 40% (v/v) ethanol solutions (100 mM Na+, pH 5.9) before and after mixing with APTMS ethanol solution at 20 8C. (c)
AFM images of G2T4G4-silica nanostructures formed at the ethanol content of 40% (100 mM Na+, pH 5.9).
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This work was supported by the NSFC (nos. 20776102 and
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