1. pubs.acs.org/JPCL
Protein Dispersant Binding on Nanotubes Studied by NMR
Self-Diffusion and Cryo-TEM Techniques
Anton E. Frise,† Eran Edri,‡ Istvn Furo,† and Oren Regev*,‡
a
‡
Department of Chemical Engineering and the Ilse Katz Institute for Meso and Nanoscale Science and Technology, Ben-Gurion
University of the Negev, 84105 Beer-Sheva, Israel, and †Division of Physical Chemistry, Department of Chemistry,
Royal Institute of Technology, SE-10044 Stockholm, Sweden
ABSTRACT Carbon nanotubes can be dispersed by a variety of molecules. We
investigate the dynamics of protein-assisted carbon nanotube dispersion in water.
We find that in equilibrium, only a small fraction of the dispersants is indeed
adsorbed to the nanotube surface, while there is a fast exchange process between
the adsorbed and free protein molecules. Self-diffusion NMR spectroscopy in
combination with cryo-transmission electron microscopy imaging are employed.
SECTION Nanoparticles and Nanostructures
arbon nanotubes (CNTs) possess unique electrical,
C
on the nanotubes surface remains, among other issues,
mechanical, and optical properties and are hence ambiguous.27,28
implemented in applications ranging from nanoelec- As concerns dispersion mechanisms, for polymer-type
tronics1-3 through biosensors4 to drug delivery.5 A major dispersants, it was suggested that a weak, long-ranged en-
drawback of as-produced CNTs is their bundling due to strong tropic repulsion among polymer-decorated tubes acts as a
van-der-Waals interactions. Therefore, the advantages with the steric barrier preventing the tubes from approaching the
high aspect ratio (1000) and other unique properties of attractive part of the intertube potential.7,29 Others suggested
individual single-wall carbon nanotubes (SWNTs) are lost. a wrapping-type mechanisms.12,30 However, while there is
Hence, substantial effort has been devoted to dispersing and plenty of data on the conformation of the dispersing agent in
debundling CNTs through either covalently grafting dispersing dry samples,31,32 there is lack of experimental information on
molecules onto the CNT surface6 or noncovalently adsorbing it the dispersant configuration or the density of dispersant
on the CNT surface.7 To preserve the original CNT structure molecules on the nanotube in situ. For surfactants, various
together with the associated electrical and mechanical proper- anchoring possibilities on nanotubes were suggested, primar-
ties, the hybridization of the carbon atoms should be minimally ily involving hydrophobic interactions.33
perturbed during the debundling process, which calls for Interactions involved in protein adsorption on NT sur-
noncovalent dispersion. Moreover, the noncovalent approach, faces can be electrostatic and hydrophobic. While some
investigated here, does not require chemical reactions. researchers suggest that hydrophobic interactions20,34
While the noncovalent dispersion and exfoliation of CNTs dominantly control protein adsorption, others35 claim that
with surfactants,8-10 polysaccharides,7,11 and polymers12,13 is the electrostatic contribution is the major one. Recently, the
well-established, biomaterials such as proteins are rather new distribution of the dispersant-dispersant distance on
candidates for dispersing NTs. Nonetheless, proteins gain a the nanotubes (L) (Figure 1) has been reported for BSA as
rapidly growing interest as an alternative route for the de- the dispersant.36
bundling and dispersion of CNTs, especially for biomedical Despite significant research, little is known on the nature of
applications. This stems from the hope that they also enhance noncovalent dispersion of nanotubes by protein or other
the biocompatibility of SWNTs.14-16 Lately, an efficient up- dispersants. How much dispersant is adsorbed on a nano-
take of protein (drug)-dispersed SWNT by cells, probably via tube? What is the fraction of surface area covered? Are the
an endocytosis17 pathway, has been reported. Here, the CNT-adsorbed molecules in equilibrium with the freely dis-
SWNTs are employed as molecular transporters for various persed ones? These questions are extremely relevant to
cargos.18 applications where nanotubes are exploited as transporters
Indeed, natural water-soluble proteins are reported of drugs (proteins) to cells.17 In many studies, one assumed a
to successfully disperse NTs through noncovalent inter- full coverage,28,33 which is, however, difficult to prove experi-
actions.19-22 Short synthetic peptides were also shown to mentally.
successfully exfoliate, debundle, and disperse nanotubes via
specifically designed adsorption23,24 or helical-like wrap-
ping.25 Indeed, the use of peptides and proteins has opened Received Date: March 16, 2010
a door to many potential applications.26 However, the dis- Accepted Date: April 8, 2010
persant (e.g., surfactant, polymer, or protein) configuration Published on Web Date: April 14, 2010
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BSA in an aqueous solution has been found to adsorb to within the approximately (2% statistical error) water diffu-
CNTs.36 The proposed mechanism is that the protein partly sion coefficients in all measured solutions (for more details,
unfolds and exposes some of its hydrophobic amino acids, see Experimental Methods section).
which interact with the surface of the CNTs.37,38 The binding The validity of the assumption of fast exchange was
of protein to the surface introduces steric repulsion and will confirmed by comparing the BSA spectral integrals obtained
disperse CNTs. in conventional single-pulse experiments for solution A on
In this paper, we show that in the dispersed state, the one hand and those for solutions B1 and B2 on the other hand.
protein molecules cover only a very small fraction of the In the case of slow exchange, proteins binding to the NTs
nanotube surface and exchange quickly with the pool of would experience very slow tumbling that would lead to the
unadsorbed proteins. loss of their signal because of the very large broadening.
Samples were prepared by mixing protein and nanotubes, However, no such reduction in the signal could be found, and
sonicating and extracting the supernatant by centrifugation the assumption of fast exchange should therefore hold for this
(for details, see Supporting Information). The concentrations system. (Alternatively, if there were slow exchange, the frac-
of NTs in the dispersion were determined by UV-vis-based tion of NT-bound BSA should be lower that the 2-3%
chemometric techniques22 and are presented in Table 1 along accuracy of the NMR intensity measurements). As an addi-
with the initial mixing concentrations. As concerns the protein tional indication, the BSA line widths were slightly larger in
component, BSA concentrations as provided by NMR spectral solutions B1 and B2 as compared to those in solution A. This
intensities of BSA were identical (within the experimental behavior is as expected for BSA molecules in fast exchange
error of a few percent) before and after centrifugation. between sites with slow (in solution) and fast (bound to NTs)
We first present the results of our self-diffusion measure- transverse relaxation.
ments and then relate to our cryo-TEM micrographs, including In fast exchange, the observed BSA diffusion coefficient
calculations of area per adsorbed protein molecule. (Dobs) in solutions B1 and B2 becomes the population average
Self-Diffusion Study. Previous studies of self-diffusion of NT of the diffusion coefficients in the bound and free states.42
systems concerned the diffusion of gases and liquids confined Dobs ¼ Dfree 3 pfree þ Dbound 3 ð1 - pfree Þ ð1Þ
inside of the NTs.39,40 Our use of the molecular diffusion here is
entirely different since we exploit self-diffusion NMR to report Considering that the diffusion of BSA in its NT-bound state is
on the ratio of BSA bound to CNTs versus that free in the negligibly small, Dfree . Dbound, this expression simplifies to
solution. It is assumed that these are the only states that the Dobs = Dfree 3 pfree, from which the fraction of bound BSA
protein takes and also that the exchange between the two molecules can be estimated as
states is fast on the NMR time scale. A third assumption is that Dobs
when the protein is bound to CNTs, its diffusion becomes pbound ¼ 1 - pfree ¼ 1 - ð2Þ
Dfree
negligible. This is reasonable considering that the NTs are
100-1000 times larger than the proteins, and their movement The fractions and resulting absolute concentrations Cbound of
should therefore be correspondingly slower. Finally, we as- NT-bound BSA as provided by eq 2 are presented in Table 1.
sume that the obstruction41 on diffusion by the NTs is negli- For both SWNTs and MWNTs, we find that the bound fractions
gible, which is validated by the identical (1.90 Â 10-9 m2/s are small, on the order of only a few percent. Unfortunately,
this and the comparable magnitude of the precision of the
diffusion data also mean that the obtained relative error of
pbound is high.
We use the obtained Cbound and the total dispersed con-
centration of NT, CNT, from chemometric measurements22 to
calculate the area per one BSA molecule on NT, ABSA(NT). First,
the number of bound BSA molecules per volume unit is
obtained as
Cbound
Figure 1. The dispersant-dispersant distance (L) in the arrange- NBSA ¼ NA ð3Þ
ment of dispersant molecules (dotted) adsorbed on a nanotube. MWBSA
Table 1. Initial NT and BSA Mixing Weights and Final (for solutions B1 and B2) NT Concentrations after Sonication and Centrifugationa
sample compound initial conc. [mg/mL] CNT [mg/mL]b Dobs [Â10-11 m2/s] Pboundc Cboundd [mg/mL]
A BSA 4 5.22 ( 0.13
B1 BSA 4 5.03 ( 0.05 0.04 ( 0.03 0.16 ( 0.12
SWNT 2 0.24 ( 0.01
B2 BSA 4 4.74 ( 0.13 0.09 ( 0.05 0.36 ( 0.20
MWNT 2 0.02
a
NT concentrations were obtained by chemometric-based experiments on UV-vis spectroscopy,22 and NMR spectral intensities indicate identical
BSA concentrations before and after centrifugation. b Dispersed concentration in the supernatant. c Fraction of NT-bound BSA. d The concentration of
NT-bound BSA.
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it seems that the surface density should, if anything, be higher
for MWNTs than that for SWNTs and that low values of R
provide peculiarly high surface density values (more than
monolayer coverage, under the assumption of adsorption on
the external surface of the outermost tube).
Electron Microscopy Study. The BSA molecules have insuffi-
ciently low contrast in cryo-TEM measurements (Figure 2A).
To enhance the contrast, we attached an 8 nm gold nanopar-
ticle (GNP) to the individual BSA molecules (Figure 2B).
We have previously shown that the GNP-BSA complex
disperses the SWNTwithout changing the conformation of the
protein.36 The measured distribution of the dispersant-
dispersant distance (L; see Figure 1) for the BSA-GNP com-
plex as imaged by cryo-TEM indicates an average distance of
ÆLæ=77 ( 55 nm for SWNT solutions36 (Figure 2B) in order-of-
magnitude agreement with the NMR findings above. In the
cryo-TEM image (Figure 2B), L has a rather wide polydisper-
sity. Similar images in the corresponding MWNT system
demonstrate binding, but we refrain from a quantitative
analysis (see discussion above).
The area per adsorbed BSA molecule, ABSA(NT), is obtained
via eq 6 as ABSA(SWNT) = 360 ( 260 nm2.36 Since the
concentration of the GNP-BSA was lower than the BSA
concentration in the NMR experiments (see discussion
above), this value is consistent with that derived from the
NMR experiments.
Figure 2. Cryo-TEM micrographs of SWNTs (A,B) and MWNTs First, it should be noted that due to the low BSA contrast in
(C,D) dispersed by unlabeled BSA (A,C) and by BSA labeled by 8 nm
gold nanoparticles (B,D). It is impossible to see any unlabeled TEM, the NMR and cryo-TEM measurements are not con-
adsorbed BSA molecules. The spots in A and C marked by arrows ducted on exactly the same system; (1) the GNP introduced
are due to surface contamination during vitrification and transfer into the cryo-TEM preparation are not added in the NMR
to the electron microscope. Bar = 100 nm.
experiments, and (2) the BSA concentration in the cryo-TEM
where MWBSA=67100 Da is the molar mass of BSA and NA is measurement is much lower than that in the NMR experi-
the Avogadro number. The total surface area of NTs (per ments (see Experimental Methods section). Therefore, in
volume) in the solution, ANT, is obtained as Figure 2, we mostly see GNP-BSA that are bound (in close
ANT ¼ CNT 3 SSA ð4Þ proximity) to the SWNT, which is in contrast to the NMR
finding of most BSA being not bound. This contradiction can
where SSA is the reported specific surface area of the NTs. be resolved by considering the low GNP-BSA concentration.
For SWNT, available values are SSA(SWNT) = 24843,44 or Here, the NMR findings can be considered as quantitatively
283 m2/g.45 Hence, the area per adsorbed BSA molecule is accurate, while the cryo-TEM observations can primarily be
ANT seen as rough verifications of the finding of the small amount
ABSA ðSWNTÞ ¼ ¼ 80 ( 60 nm2 ð5Þ of CNT-bound protein.
NBSA
In this context, there is no easy way to perform the NMR
This area yields, via and cryo-TEM experiments on the same system because
ABSA ðNTÞ ¼ πDNT ÆLæ ð6Þ binding the gold nanoparticles broadens the NMR signal to
close undetectability. Even if the 1H NMR signal from
and the known diameter of SWNT (DNT=1.5 nm), the average GNP-BSA were detectable, the diffusion coefficient for them
dispersant-dispersant distance (L; see Figure 1) on the order in the free state would be much lower, which would decrease
of ÆLæ ≈ 20 nm, in agreement with reported values in the the sensitivity of NMR experiments to binding. Since our
literature.31 current sensitivity is barely enough to detect binding, diffu-
The active surface area per weight (available for ad- sion experiments with GNP-BSA are not feasible.
sorption) for a MWNT is plausibly lower than the one obtained Despite all possible shortcoming of our experiments, our
by BET measurements (233 m2/g46) if we assume that only current observations together with some earlier ones36 pro-
the external surface of the outermost tube is accessible for vide two significant findings. First, the most striking feature is
adsorption of a protein molecule. Since (i) the reported values that only a very small fraction of the dispersing molecules
for the ratio of the active surface area/total surface area, R, for (a few percent; see Table 1) are actually adsorbed on the NT
MWNTs are scattered within a very wide range of surface at a given instance. This is true for both the SWNTand
0.1-0.001.47,48 and (ii) there is a large polydispersity in MWNT (Table 1). However, if one attempts to disperse the NTs
MWNT width and the number of layers, we cannot provide by initially adding only that much BSA that corresponds to the
a surface density estimate for the MWNT solutions. However, pbound (that is, for example, preparing a SWNT dispersion by
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Figure 3. Schematics of the dynamic equilibrium between adsorbed and free BSA molecules (red). According to our results, most BSA
molecules are in the free state at any given instance, and the exchange is fast, on a time scale 50 ms.
adding 0.2 mg/mL BSA instead of 4 mg/mL; see Table 1) with
the same initial amount of NT (2 mg/mL), no SWNT will be
dispersed.21 Therefore, BSA molecules seem to be in a
dynamic equilibrium and exchange between bound and free
states, similar to surfactant molecules in a micelle above the
CMC and as illustrated in Figure 3. This process can take place
and can take place quickly (50 ms, which is the time scale of
our NMR diffusion experiments) since the BSA adsorbs on the
NT via a nonwrapping mechanism.49 Indeed, for other pro-
teins or other dispersants with different adsorption energies,
the situation could be completely different, especially for
certain polymers as dispersants.
Our second finding is that the area per adsorbed BSA
molecule seems to differ for SWNTs and MWNTs. Unfortu-
nately, we could not quantify the extent of this difference. One
possible reason for such a difference is different curvatures for
Figure 4. Normalized signal amplitudes of stimulated echo de-
SWNTs and MWNTs. cays versus the Stejskal-Tanner factor (b = (γgδ)2(Δ - δ/3),
Upon dispersing NTs by a dispersant, part of the NTs are where γ is the magnetogyric ratio of 1H) of BSA in solutions
indeed dispersed, but some precipitate. After centrifugation, without (A; see Table 1) and with added carbon nanotubes (B1
we decant the supernatant,9 where a stable NT dispersion is and B2). Spectra obtained in pulsed field gradient spin-echo
experiments in aqueous solutions of BSA. The solid lines are linear
obtained. It has been recently reported that there is a thresh- fits to the decay data with adjusted R2 values higher than 0.99.
old of dispersant concentration, above which a dispersion is
obtained.28 This value depends on the dispersant as well as
would therefore be to study different dispersants to clarify
the solvent. Increasing the dispersant concentration above
these issues.
this threshold value for a given NTconcentration will not bring
more nanotubes to the dispersed solution50 and may even
EXPERIMENTAL METHODS
reduce the concentration of the dispersed NT.21 Intuitively, it
could then be assumed that in the dispersed state, most The diffusion coefficients of BSA were measured with
dispersing molecules are indeed adsorbed on the NT surface. pulsed gradient spin-echo (PGSE) NMR using the stimulated
This is clearly not the case, as we have shown in this Letter. echo pulse sequence.51 The gradient strength ( g) was in-
The protein molecules bound to the dispersed nanotubes creased in 10 steps from 0.5 to 3.9 T m-1. At each step, 128
are only a very small fraction of the available protein mole- scans were acquired. The diffusion time (Δ) was set constant
cules in the system. The free and bound protein molecules are to 50 ms and gradient pulse duration (δ) was set to
in fast exchange between these two states. These findings 1 ms, with 1 ms stabilization time between the gradient and
provide new insights and an alternative to the previously radio frequency pulses. The diffusion coefficients were ex-
depicted scenario of persistent dispersant-NT complexes in tracted by fitting the conventional Stejskal-Tanner expres-
solution. For BSA adsorbed on SWNTs, a protein-to-protein sion52 to the observed diffusional decays (see Figure 4). The
distance of 5-30 nm is estimated from NMR measurements, longitudinal relaxation time (T1) of BSA was estimated by
and its order of magnitude is confirmed by cryo-TEM mea- inversion recovery to ∼0.5 s, and the recycle delay between
surements. two acquisitions was therefore set to 3 s. The diffusion
We cannot tell if the reported dynamic equilibrium picture measurements were repeated three times for the free protein
inferred in this system is true as well for other systems with (solution A) and five times for protein in the NT dispersion
different adsorption energies or curvatures. Our next step (solutions B1 and B2); the results given in Table 1 are
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5. pubs.acs.org/JPCL
arithmetic means, and the error bars are estimates of preci- (4) Chen, R. J.; Bangsaruntip, S.; Drouvalakis, K. A.; Kam, N. W. S.;
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SUPPORTING INFORMATION AVAILABLE Description of Smalley, R. E.; Schmidt, J.; Talmon, Y. Individually Suspended
the materials and sample preparation procedures. This material is Single-Walled Carbon Nanotubes in Various Surfactants.
available free of charge via the Internet at http://pubs.acs.org. Nano Lett. 2003, 3, 1379–1382.
(14) Shim, M.; Kam, N. W. S.; Chen, R. J.; Li, Y. M.; Dai, H. J.
AUTHOR INFORMATION Functionalization of Carbon Nanotubes for Biocompatibility
and Biomolecular Recognition. Nano Lett. 2002, 2, 285–288.
Corresponding Author: (15) Magrez, A.; Kasas, S.; Salicio, V.; Pasquier, N.; Seo, J. W.; Celio,
*To whom correspondence should be addressed. E-mail: oregev@ M.; Catsicas, S.; Schwaller, B.; Forro, L. Cellular Toxicity of
bgu.ac.il. Carbon-Based Nanomaterials. Nano Lett. 2006, 6, 1121–
1125.
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It Again! Carbon Nanotubes Hoax Scientists in Viability
ACKNOWLEDGMENT This work has been supported by the Assays. Nano Lett. 2006, 6, 1261–1268.
Israeli Science Foundation Grant 8003 and by the Swedish (17) Kam, N. W. S.; Jessop, T. C.; Wender, P. A.; Dai, H. J. Nanotube
Research Council VR. Pola Goldberg and Margarita Ruvinsky are Molecular Transporters: Internalization of Carbon Nanotu-
acknowledged for valuable discussions, electron microscopy work, be-Protein Conjugates into Mammalian Cells. J. Am. Chem.
and image analysis. Soc. 2004, 126, 6850–6851.
(18) Pantarotto, D.; Briand, J. P.; Prato, M.; Bianco, A. Transloca-
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r 2010 American Chemical Society 1419 DOI: 10.1021/jz100342c |J. Phys. Chem. Lett. 2010, 1, 1414–1419