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Applied Surface Science 331 (2015) 271277

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Applied Surface Science


journal homepage: www.elsevier.com/locate/apsusc

Non-covalent attachment of silver nanoclusters onto single-walled


carbon nanotubes with human serum albumin as linking molecule
Andrs Rodrguez-Galvn a,c,d, , Alejandro Heredia a , Oscar Amelines-Sarria b ,
Margarita Rivera b , Luis A. Medina c,d , Vladimir A. Basiuk a
a

Instituto de Ciencias Nucleares, Universidad Nacional Autnoma de Mxico, Circuito Exterior C.U., 04510 Mxico D.F., Mexico
Instituto de Fsica, Dpto. Materia Condensada, Universidad Nacional Autnoma de Mxico, Coyoacn, 04510 Mxico D.F., Mexico
c
Instituto de Fsica, Dpto. Fsica Experimental, Universidad Nacional Autnoma de Mxico, Coyoacn, Mxico, DF 04510, Mexico
d
Unidad de Investigacin Biomdica en Cncer INCan-UNAM, Instituto Nacional de Cancerologa, Mxico, DF 14080, Mexico
b

a r t i c l e

i n f o

Article history:
Received 18 June 2014
Received in revised form 17 October 2014
Accepted 25 October 2014
Available online 10 November 2014
Keywords:
Single-walled carbon nanotube
Silver nanoclusters
Human serum albumin
Hybrid nanomaterials

a b s t r a c t
The attachment of silver nanoclusters (AgNCs) onto single-walled carbon nanotubes (SWNTs) for the formation of integrated uorescence sites has attracted much attention due their potential applications as
biological probes and nanovectors in theragnosis. Here, we report the preparation through assembly of
uorescent quasi 1-D nanomaterial based on SWNTs and silver nanoclusters (AgNCs) non-covalently
attached to human serum albumin as biological linker. The uorescent SWNTAgNCsHSA conjugates were characterized by atomic force microscopy, high-resolution transmission electron microscopy
(HRTEM), high angle annular dark eld scanning TEM (HAADF-STEM), uorescent and UVvis spectroscopy. The above techniques conrmed that AgNCs were non-covalently attached onto the external
surface of SWNTs. In addition, it was observed that the modication did not affect the optical properties of the synthesized AgNCs since the absorption spectra and uorescence under UV irradiation
( = 365 nm) remain the same. The effect of the functionalized systems was tested on mammal red blood
cells (RBCs) and it was found that their structural integrity was compromised by the conjugates, limiting
their biological and medical applications.
2014 Elsevier B.V. All rights reserved.

1. Introduction
Single-walled carbon nanotubes (SWNTs) are quasi onedimensional (1-D) nanomaterials with unique physical and
chemical properties that can be used for applications in life
sciences and medicine [1]. Particularly, the uorescence of SWNTs
(in the near-infrared spectrum) is a promising dye in biological
applications and for the design of optical biomedical sensors
[15]. Fluorescent SWNTs has been recently explored as dyes for
targeting cancer cells and as contrast agents to enhance organs
visualization [1,2]. However, it is well known that biological
applications of bared SWNTs are restricted due to their toxicity
[6]. By using organic coatings such as chromophores containing
polymers and uorescent organic dyes onto CNTs, SWNTs become
biocompatible and, thus, an excellent alternative as uorescent

Corresponding author at: Instituto de Ciencias Nucleares, Universidad Nacional


Autnoma de Mxico, Circuito Exterior C.U., 04510 Mxico D.F., Mexico.
Tel.: +52 55 5622 4739x2224, +52 55 5622 4675; fax: +52 55 5622 4693.
E-mail address: andres.rodriguez@nucleares.unam.mx (A. Rodrguez-Galvn).
http://dx.doi.org/10.1016/j.apsusc.2014.10.164
0169-4332/ 2014 Elsevier B.V. All rights reserved.

material [79]. Another useful modication although less explored


with great potential, is the attachment of metallic nanoclusters
(NCs) onto SWNTs for the fabrication of uorescent nanotubes
[10]. NCs have been of particular interest because, in addition to
their good photostability, stability and solubility properties, they
exhibit low toxicity for biological systems [1114].
The NCs are constituted from tens to hundreds of atoms, and
due to their small size (<2 nm) their optical properties are intermediate between molecules and nanoparticles [14]. For biological
applications, the uorescence and related properties such as high
photostability, broad absorption band and a high Stokes shift are
of particular interest [13]. Different types of capping ligands ranging from small biomolecules like DNA to large molecular weight
proteins such as bovine serum albumin (BSA) have been used to
synthesize NCs [13]. Particularly, protein-stabilized silver nanoclusters (AgNCs) are receiving increasing attention due their strong
and tunable uorescence properties in the visible spectrum [15].
Among them, globular proteins such as human serum albumin
(HSA) has been extensively used as templates for the synthesis of
AgNCs because of their capability to interact and trap metal ions,
and to prevent the NCs aggregation [1619].

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It is well known HSA protein is ideal to disperse carbon nanotubes in solution because of its strong adsorption onto hydrophobic
surfaces [20,21]. The ease formation of conjugated SWNTs and HSA
has been reported [21]. The adsorption onto the SWNTs sidewalls
occurs spontaneously due to Van der Waals interactions between
the protein and the carbon nanotubes [2224]. Furthermore, HSA
has been used as linking molecules between AgNPs and multiwalled carbon nanotubes (MWNTs) to form hybrid materials under
mild conditions [23].
Herein, by using the dual hydrophobichydrophilic capability
of HSA to act as template in the molecular coupling to synthesize the AgNCs and to be easily adsorbed onto SWNTs we obtained
the rst assemblies SWNTs with uorescent AgNCs wrapped up
with the HSA as linking molecule. The method employed demonstrated the combination of unique specic molecular properties
of the three nanomaterials, resulting in an interesting molecular
aggregation with potential applications. The conjugates were characterized by UVvis spectroscopy and microscopy techniques such
as atomic force microscopy, high-resolution transmission electron microscopy and dark-eld scanning transmission electron
microscopy. Additionally, by using scanning electron microscopy
(SEM), the functionalized SWNTs were used to test the structural
integrity of the membrane of red blood cells (RBCs), in order to
explore the toxicity of these materials.

2. Materials and methods


2.1. Materials
Silver nitrate (AgNO3 ), HSA (MW 67 KDa), sodium borohydride
(NaBH4 ) and potassium hydroxide (KOH) were purchased from
Sigma-Aldrich. SWNTs (95% of purity) were purchased from ILJIN
Nanotech Co., Korea. All reagents were used as received, and for all
the experiments deionized water (18.2 M cm) was used.

2.2. AgNC synthesis with HSA


AgNCs/HSA were synthesized by the method reported by
Mathew and coworkers [15]. In brief, 100 L of HSA (50 mg/mL)
were incubated with 100 L of 10 mM AgNO3 for 5 min. Afterwards
5 L of 1 M of NaOH and left for 5 min. Finally, 4 L of 10 mM of
NaBH4 as reducing agent was added.

2.4. Effect of the conjugates on the integrity of red blood cells


(RBC)
For the blood cells, native whole blood was collected from
consenting informed healthy volunteer donors. The blood was
collected into vacutainer tubes containing 3% of sodium citrate
solution to obtain anticoagulant blood samples for uses in blood
exposure assays; the volume ratio of blood to sodium citrate solution was 9:1. The procedure for RBCs extraction and for the test was
followed as previously reported [25]. SEM characterization was carried out using a JSM-6510LV (JEOL, Japan) instrument operating at
20 kV.
2.5. Characterization
2.5.1. Ultravioletvisible and uorescence spectroscopy
UVvis spectroscopy was carried out using a Cary 100
UVvis spectrophotometer (Varian, USA) in a range between
200 and 700 nm. Fluorescence analysis was performed in a LS55 luminescence Spectrometer (PerkinElmer, USA). The emission
spectra were recorded in a range of 500700 nm upon excitation
at 510 nm.
2.5.2. High-resolution transmission electron microscopy and
dark-eld scanning transmission electron microscopy
The surface morphology and chemical composition were investigated with HAADF-STEM and HRTEM. The images were obtained
with a JEM-2010F FASTEM instrument (JEOL, Japan) coupled to a
NORAN energy dispersive spectrophotometer (EDS) operating at
20 kV. The samples were prepared by casting 5 L of the samples
onto carbon coated copper grids (Ted Pella). The solution excess
was then removed with lter paper and dried at room temperature
in the overnight. The particle/nanotube dimensions were measured
using the ImageJ version 1.40 software (NIH, Wayne Rasband).
2.5.3. Atomic force microscopy
The AFM images were recorded in tapping mode under ambient conditions on a JSPM-5200 (JEOL, Japan) microscope. 50 L of
sample was deposited onto freshly cleaved mica substrate, incubated 15 min, washed with 2 mL of deionized water and dried at
room temperature for 2 h. The images and prole analysis were
performed with the Gwyddion 2.36 software (Czech Republic).
3. Results and discussion
3.1. Decoration of SWNTs with AgNCs

2.3. Decoration of SWNTs with AgNCs to form the conjugates


For the preparation of SWNTsAgNCsHSA (referred to as conjugates hereafter), 1 mL of oxidized SWNTs (0.5 mg/mL) in water
solution was mixed with 1 mL of AgNCs (50 mg/mL) synthesized
using HSA as template and incubated for 15 min under slow stirring.
In addition, two control samples were prepared as follows:

(a) One milliliter of SWNTs (0.5 mg/mL) was mixed with 1 mL of


HSA (50 mg/mL) and sonicated for 20 min in an ultrasonic bath,
then 100 L of AgNO3 (1 M) was added gently and the pH was
adjusted to 12 with KOH. Finally 100 L of NaBH4 (10 mM) was
added as reducing agent.
(b) The second sample was prepared in a similar way as the above,
however the pH was kept neutral.

Each sample was dialyzed in PBS to eliminate the excess of


AgNO3 and NaBH4 and centrifuged at 16,000 g for 20 min.

Silver nanoclusters synthesized using HSA as biological template (Fig. 1) were incubated with SWNTs (Fig. 2a). The UVvis
absorption spectra of the conjugates showed two absorption peaks,
at 280 nm and 450 nm, assigned as HSA and AgNCs, respectively
(Fig. 3a) [15]. The absorption of HSA is attributed to the *
transition of aromatic amino acids. At the same time, it is well
known that the UVvis absorption spectra of nanoclusters exhibit
molecule-like optical transition with absorbance bands due to the
quasi-continuous electronic energy band structure and quantum
connement effects [15]. The absorption spectrum of AgNCs was
broad and low, from 400 to 500 nm, since the optical properties
of the nanoclusters were apparently affected by the protein shell
[15]. Furthermore, a different method for the formation (referred
to as control samples in Section 2, Fig. 2b) of silver nanoclusters was tested. The protein coating deposited onto the side-walls
of SWNTs was used as template for the deposition of silver ions
and then reduced with sodium borohydride. The reduction process was performed under two different pH conditions: (a) at
pH 12, since an alkaline media is required for the nanoclusters

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273

Fig. 1. Representative 3D AFM image of synthetized nanoclusters deposited on mica (a) and corresponding particle size histogram (c). HRTEM image of nanoclusters (b) and
corresponding particle size histogram (d). EDS spectrum of silver nanoclusters (inset in (b)).

synthesis under protein control [16]; and (b) at pH 7, since the


deposition of silver nanoparticles using HSA onto SWNTs has been
reported under neutral conditions [23]. The UVvis spectra of the
two control samples were similar and displayed the lack of the
AgNCs absorption band, in contrast they exhibited one peak at
420 nm (Fig. 3a), that is well known to correspond to the surface resonance plasmon of silver nanoparticles (particles with a
size > 2 nm). The physisorption of HSA onto the SWNTs surface
might explain the observed, this might restrict the native protein

dynamic for the correct interaction between lateral chains and silver ions, and furthermore this might restrict the connement effect
that is known to abolish the growing process towards nanoparticles
[22,23].
The as-prepared conjugates displayed a yellow color under
ambient light and orange color under the UV lamp (inset in Fig. 3c).
Fig. 3c shows the uorescence spectra of conjugates in aqueous
solution, as shown, they exhibit an intense absorption band centered at 480 nm and the emission spectrum displays an emission

Fig. 2. Schematic of the conjugation protocols for the non-covalent attachment of silver nanoclusters onto single-walled carbon nanotubes. The silver nanoclusters were
synthetized before their conjugation with SWNTs (a). In control samples the silver reduction was after the incubation of HSA with the SWNTs (b). The rst approach let the
formation of conjugates with AgNCs. In contrast the second way address the AgNPs formation.

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Fig. 3. Low magnication (a) and high magnication (b) of UVvis spectra of conjugates formed with AgNCs synthetized before their conjugation (purple line) and with silver
reduction was after the incubation at alkaline and basic pH (red and green line respectively). Absorption and emission spectra of conjugates formed with AgNCs synthetized
before their conjugation (c), the inserts are photographs of conjugates under ambient light and UV lamp. Emission spectra (d) of conjugates prepared at several concentrations
of SWNTs (SWNTs:AgNCs; 0.025:2.5, 0.25:2.5 and 2.5:2.5 mg/mL, purple, black and pink lines respectively). For interpretation of the references to color in this gure legend,
the reader is referred to the web version of this article.

maximum around 605 nm upon excitation at 480 nm. The emission


is known to be originated from the inter-band transitions from the
submerged and quasi-continuum 5d band to the lowest unoccupied
conduction band of Ag nanoclusters [26]. The conjugates showed
a good stability since the uorescence intensity was kept without
changes for some hours. We observe the successful formation of
conjugates needed an excess of AgNCs (SWNTs: AgNCs; 1:100),
since when the relative SWNTs concentration increased the uorescence intensity of the conjugates decreased drastically (Fig. 3d). The
SWNTs have a quenching capability for a variety of uorophores,
such as pyrenes, porphyrins and chromophores, and it is thought
that either energy transfer or electronic transfer might contribute
to the quenching effect [16]. In this work the interaction between
the nanoclusters and the surface of SWNTs might not be an explanation for the uorescence quenching, we inferred the protein shell
avoided the direct interaction. However, it was reported the interaction between metallic ions with the organic shell of protect silver
nanoclusters could promote the emission quenching [26]. Due to
the lack of information about the Ag nanoclusters at present other
factor as impurities (amorphous carbon and graphite) should be
considered [27].
3.2. Microscopic characterization
Atomic force microscopy was used to conrm the deposition of
silver nanoclusters onto SWNTs, since it is a powerful tool for the
characterization of nanomaterials. By comparing typical topography AFM images of bare SWNTs (Fig. 4a and b) with images of the
conjugates (Fig. 4c and d), it is evident the deposition of oblong
particles (high blue particles in the images) along SWNTs after
the incubation with AgNCs. The oblong particles were observed on

all the carbon nanotube samples, showing high conjugation. Comparative transversal cross sections analysis of the bare nanotubes
and their conjugates (Fig. 4b and d) conrmed the deposition. The
carbon nanotubes exhibited heights around 4 nm and a at longitudinal prole (Fig. 4e and f). In contrast, the conjugates showed
transversal proles with an increase of 3 nm and a longitudinal
prole with peaks and valleys with heights of 23 nm (Fig. 4e and
f), which correspond to the nanocluster-covered and bare surfaces
respectively [6].
Fig. 5 shows HRTEM images of pristine SWNTs, HSA-decorated
nanotubes and conjugates (a, b and c, respectively). The conjugates showed few black spots, with a size of approximately 2 nm,
embedded into a protein lm that was covering the nanotube
sidewalls (Fig. 5f). The EDS analysis revealed silver peaks that suggested the black spots might be the AgNCs. In contrast, bare and
HSA-decorated SWNTs did not exhibit black spots and showed the
absence of silver signals in EDS. A HAADF-STEM analysis was performed and interestingly contrasted with that observed in HRTEM,
the images showed a big number of AgNCs along the SWNTs surface (bright spots in Fig. 5d). This difference is explained by the
high sensitivity of HAADF-STEM, it is based in atomic number (Z)
variations of the atoms in the sample, and the sensitivity lets contrast between the protein shell and the Ag nanoclusters core. The
atomic number (Z = 47) of silver is higher than the atomic components of proteins and carbon nanotubes, namely H (Z = 1), C (Z = 6),
N (Z = 7), O (Z = 8) and S (Z = 16) [10]. In addition, it is well know
that the protein shell does not let a high resolution of AgNCs by
HRTEM [16]. Finally, it is important to remark the formation of uorescent quasi 1-D nanomaterials was successful due the use of
the SWNTs as template, since without them the AgNCs showed a
random arrangement (Fig. 5e).

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275

3.3. Effect of conjugates on RBC integrity

Fig. 4. Representative AFM images of pristine SWNTs (a, b) and conjugates (c, d)
deposited on mica, its cross section proles are marked by arrows and identied by
colors (e, f). For interpretation of the references to color in this gure legend, the
reader is referred to the web version of this article.

Nanotubes with integrated uorescence have been suggested


for biological and medical applications. However, for our known
their impact on the integrity of red blood cells, the main cellular
component in the blood and principal oxygen carriers to body tissues, has not been reported. Analysis by SEM was used to test the
structural integrity of red cells. Normal RBC typically displayed a
biconcave disk-like appearance (Fig. 6a). After their incubation with
the conjugates at a concentration of 0.025 mg/ml the RBC exhibited
a number of cells with aberrant morphology (spiculated shapes,
blue arrows) and structural damage (Fig. 6c). Furthermore, increasing the concentration up to 0.25 mg/ml the aberrant morphology
and fragmentation became more evident (Fig. 6e). SEM images of
RBCs incubated with naked SWNTs did not display noticeable damage or the transformation of echinocytes (Fig. 6g), discarding some
notable effect from hydrophobic patches form conjugates with
an incomplete protein coat as was observed in the AFM analysis
(Fig. 4d). An interesting fact resulted from the obtained SEM images
of RBCs incubated with the as-prepared AgNCs, they displayed
clear cut fragmentation and high transformation into echinocytes.
In other words, the as-prepared AgNCs promotes the erythrocyte
damage and transformation. The interaction of silver nanoparticles
with erythrocytes recently has been studied and it was found silver nanoparticles interact with the membrane of RBCs and induce a
cellular damages since block the transport channels [28], in particular the AgNPs produce an imbalance in the internal pH. It is well
known changes in the pH of RBCs to be related to the crenation
phenomena [29]. Furthermore, the interaction of PEGylated gold
nanoparticles with the membrane of RBCs has been reported to
promote the formation of echinocytes [30]. Here the SEM images
of RBCs incubated with the conjugates and with the as-prepared
AgNCs showed the presence of additional material onto the surface
of the erythrocytes (Fig. 6f and g; red arrows). Based in own results
we suggest the interaction of the AgNCs with the RBCs membrane
promotes the structural damage in the cells.
Cytotoxic drugs are between the main drugs against malign
cells, however, it is well known for some metabolic conditions as

Fig. 5. (a) HRTEM image of pristine SWNTs, SWNTs decorated with HSA (b) and conjugates (c, f). The inset shows the EDS analysis of the conjugates (c). (d) HAADF-STEM
image of conjugates and (e) AgNCs.

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study the hemo compatibility of the conjugates worked here and


their possible use in advance treatments.

Acknowledgments
The work was supported by the National Autonomous University of Mexico (grant DGAPA-IN101313) and the National
Council on Science and Technology (grant CONACyT-127299).
Andrs Rodrguez-Galvn thank CONACyT for a PhD fellowship.
O. Amelines-Sarria acknowledges nancial support of DGAPA
CJIC/CTIC/1334/2013. The authors thank Fis. Roberto Hernndez for
TEM technical assistance and to Dr. Victor Meza-Laguna for SEM
technical assistance.

References

Fig. 6. Scanning electron microscopy images of RBCs (a) incubated with conjugates
(b, c), SWNTs (d) and AgNCs (e). SEM images showing agglomeration of conjugates
(f) and AgNCs (g) over the membrane of RBCs (red arrows). All the samples were
incubated at 37 C for 2 hFor interpretation of the references to color in this gure
legend, the reader is referred to the web version of this article.

resistance to current drugs could be present [31], as the nanomaterials emerged as option to overcome these drawbacks [32].
In particular metallic nanoclusters are currently investigated as
radiosensitizers for cancer radiotherapy [33,34]. The conjugates
synthesized here could be explored for their possible use in advance
treatments.
4. Conclusions
The approach ran here showed the capability for the formation
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since the integrity of RBCs was compromised. The SEM analysis
showed a toxic effect concentration-dependency and specically
that the AgNCs were the main toxic element. Our results are not
conclusive and suggest more experiments should be addressed to

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