Helical polycarbodiimide cloaking of carbon nanotubes enables inter-nanotube exciton energy transfer modulation

Article abstract of DOI:10.1021/ja505529n

The use of single-walled carbon nanotubes (SWCNTs) as near-infrared optical probes and sensors require the ability to simultaneously modulate nanotube fluorescence and functionally derivatize the nanotube surface using noncovalent methods. We synthesized a small library of polycarbodiimides to noncovalently encapsulate SWCNTs with a diverse set of functional coatings, enabling their suspension in aqueous solution. These polymers, known to adopt helical conformations, exhibited ordered surface coverage on the nanotubes and allowed systematic modulation of nanotube optical properties, producing up to 12-fold differences in photoluminescence efficiency. Polymer cloaking of the fluorescent nanotubes facilitated the first instance of controllable and reversible internanotube exciton energy transfer, allowing kinetic measurements of dynamic self-assembly and disassembly.

Full text of DOI:10.1021/ja505529n

Article
pubs.acs.org/JACS
Helical Polycarbodiimide Cloaking of Carbon Nanotubes Enables
Inter-Nanotube Exciton Energy Transfer Modulation
†
†
†
,†,‡
Januka Budhathoki-Uprety, Prakrit V. Jena, Daniel Roxbury, and Daniel A. Heller*
†Memorial Sloan Kettering Cancer Center, New York, New York 10065, United States
‡Weill Cornell Medical College, New York, New York 10065, United States
*
S Supporting Information
ABSTRACT: The use of single-walled carbon nanotubes
SWCNTs) as near-infrared optical probes and sensors require
(
the ability to simultaneously modulate nanotube fluorescence
and functionally derivatize the nanotube surface using
noncovalent methods. We synthesized a small library of
polycarbodiimides to noncovalently encapsulate SWCNTs
with a diverse set of functional coatings, enabling their
suspension in aqueous solution. These polymers, known to
adopt helical conformations, exhibited ordered surface cover-
age on the nanotubes and allowed systematic modulation of
nanotube optical properties, producing up to 12-fold differences in photoluminescence efficiency. Polymer cloaking of the
fluorescent nanotubes facilitated the first instance of controllable and reversible internanotube exciton energy transfer, allowing
kinetic measurements of dynamic self-assembly and disassembly.
INTRODUCTION
resulting in a polymer chain with a regular array of functional
17
■
side groups. The tunable nature of the system permits the
synthesis of polycarbodiimides to promote multivalent π−π
interactions between the polymer and the nanotube surface to
form stable, photoluminescent, polymer-cloaked nanotube
complexes with diverse functionalities.
Semiconducting single-walled carbon nanotubes emit photo-
stable fluorescence in the near-infrared (nIR) region (ca. 900−
600 nm) of the electromagnetic spectrum. Due to their
unique photophysical properties, interest exists in using
SWCNTs for biological applications. Noncovalent functional-
1
1
2
ization of SWCNTs via encapsulation in amphiphilic polymers
preserves the optical properties of SWCNTs in solution.
EXPERIMENTAL SECTION
■
3
4
5
Biopolymers, such ssDNA, peptides, and proteins, and
Synthesis of Polymers. Polymers were synthesized following the
6
7
18
synthetic polymers, such as polyfluorenes, polycarbazoles,
reported procedure with slight modifications [details in the
8
Supporting Information (SI)]. Briefly, the catalyst, R-BINOL-
titanium(IV)-diisopropoxide, either neat or dissolved in chloroform
0.2 mL per 500 mg of monomer), was added to the alkyne-
substituted monomer at room temperature and under inert
atmosphere. The reaction mixture turned into a dark red viscous
liquid and solidified to an orange red solid (ca. 24 h). The completion
of the polymerization process was confirmed by disappearance of IR
aryleneethynylene polymers polyethylene glycol (PEG)
derivatives, and dextran-based polymers, have been inves-
tigated to encapsulate nanotubes for diverse applications,
9
10
(
11
including their use as optical probes and bioanalytical
1
2
sensors. The ease of synthesis, scale-up, and greater control
over functionalization of synthetic polymers, as compared to
nucleic acids and peptides, allows the development of
functionally diverse polymer−nanotube complexes for a wide
range of applications. We endeavor to rationally design
encapsulating materials to produce nanotube suspensions
resulting in environmentally responsive, multiplexed, and
photostable nIR probes.
−1
signals from carbodiimide (∼2140−2120 cm ) and appearance of
−1
new IR absorption at ∼1620−1640 cm due to formation of the
polymer backbone. The solid polymer was dissolved in chloroform,
precipitated in methanol, separated, and dried to obtain a light yellow
solid. The alkyne-substituted polymers were then postmodified via a
Cu(I)-catalyzed alkyne−azide cycloaddition reaction to couple organic
azide compounds (details in the SI).
Synthetic helical polymers incorporate similar structural
motifs as the biomolecules used to encapsulate carbon
nanotubes; however, they allow for greater structural
Amine-Poly-5 and Amine-Poly-7 were acidified with a few drops of
dilute HCl to increase water solubility. Carboxy-Poly-6 was treated
with a few drops of a saturated solution of NaHCO . Acidic and basic
polymer solutions were then filtered through centrifugal filters
Amicon Ultracel, MWCO 3K Da, Merck Millipore Ltd.) to remove
residual small molecules and washed with water until free from free
3
1
3
modularity. We explored a helical polymer system, poly-
carbodiimides, with a semirigid backbone that allows a large
(
14
degree of control over size and pendant groups, to develop
stable and water-soluble polymer−nanotube complexes. Recent
studies on polycarbodiimides demonstrated precise control
Received: June 2, 2014
1
5,16
over the polymer microstructure
and postmodifications,
©
XXXX American Chemical Society
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Scheme 1. Synthesis of Polycarbodiimide Polymers (Poly-1−7)
acid or base, as tested with litmus paper. The polymers were then used
to suspend SWCNTs in water.
immediately after mixing, and after incubation for 40 h (Figure 3).
In dynamic studies (Figure 4A−C), photoluminescence (PL) from
nanotubes was continuously monitored (excitation 669 nm) for a
specified time period. To disaggregate the nanotubes, an aqueous
solution of amine-functionalized polycarbodiimide hydrochloride salt
solution (0.5 mg/mL) was added to the mixture of polycarbodiimide−
SWCNT complexes and the suspension was mixed thoroughly by
pipetting it up and down.
TEM. A 2−4 μL aqueous solution of polymer−SWCNTs (∼5 mg/L,
nanotube concentration) was dropped onto a carbon-coated copper
TEM grid (Ted Pella) and allowed to stand for 10 min. SWCNTs on
air-dried grids were observed using a JEOL 1200 EX transmission
electron microscope operated at 80 kV.
AFM. A 10 μL aqueous solution of polymer−SWCNTs (2−5 mg/L,
nanotube concentration) was dropped onto a freshly cleaved mica
surface (Pelco Mica Disc, V1, Ted Pella) and allowed to stand for 45 s.
The mica surface was rinsed with deionized water two times to remove
unbound carbon nanotubes. The mica surface was air-dried at room
temperature prior to AFM imaging. AFM images were collected using
an Asylum MFD-3D-BIO in ac mode using AC240TS and AC160TS
tips (Asylum Research). The typical scan size was 2−5 μm and the
scan rate was 0.25 Hz−0.5 Hz. The images were processed with Igor
software.
Preparation and Characterization of Polycarbodiimide−
SWCNT Complexes in Water. SWCNTs (1 mg, Unidym HiPCO
SWCNTs) were added to aqueous solutions of polymer (4 mg in 1.0
mL water), and the mixture was probe sonicated (eight-tip probe, 750
W, 20 kHz, 40% Amplitude, SONICS VibraCell) at low temperature
for 20 min using a CoolRack M30 PF (BioCision) kept at −20 °C
prior to use. The solution was centrifuged (SORVALL Discovery
90SE, HITACHI) at 280 000 g for 30 min at room temperature to
remove unsuspended nanotubes and carbon impurities. After
centrifugation, ca. 80% of the supernatant was collected and filtered
through a 100 kDa molecular weight cutoff centrifugal filter (Millipore
Amicon) to remove excess of polymer, washed with water two more
times, and resuspended in water. Solutions were diluted with water as
required prior to characterization by ultraviolet−visible−near-infrared
(
UV−vis−nIR) absorbance and fluorescence spectroscopies. Absorp-
tion and fluorescence spectra were compared to those from sodium
deoxycholate (SDC)-suspended SWCNTs. Ultrapure water (18.2
mΩ) was used for all aqueous solutions.
The UV−vis−nIR absorption spectra were measured with a JASCO
V-670 spectrophotometer. Near infrared fluorescence measurements
were performed on a home-built instrument consisting of an IsoPlane
SCT 320 spectrograph and PioNIR InGaAs detector (both Princeton
Instruments) connected to an Olympus IX71 inverted microscope. A
RESULTS AND DISCUSSION
■
20× objective was used. SWCNTs were excited using a SuperK
Alkyne polycarbodiimides (Poly-1, Mn = 13 kDa, PDI = 1.29,
and Poly-2, Mn = 36 kDa, PDI = 1.35; see the SI) were
synthesized and organic azides were subsequently coupled to
terminal alkyne groups in these polymers via Cu(I)-catalyzed
alkyne−azide cycloaddition, as depicted in Scheme 1, following
Extreme supercontinuum laser connected to a Varia variable bandpass
filter (both NKT Photonics), and emission from 915 to 1354 nm was
recorded. LightField software (Princeton Instruments) was used to
collect and process data. Photoluminescence excitation/emission (PL)
measurements were performed (details in the SI) on the same
spectrograph. The excitation wavelength was varied from 491 to 824
nm, and the emission was recorded from 915 to 1354 nm. Data were
collected using a custom Labview (National Instruments) automation
program. These data were then analyzed and plotted using Matlab
1
8
a previously reported procedure. Side chains in these
polymers, such as primary amines, carboxylic acids, and
oligoethylene glycols, were incorporated to mimic side chains
in biopolymers, such as polylysines and polyglutamic acids, and
to increase water solubility. In addition, aromatic groups were
incorporated on each monomer substituent 3 and 4 (Scheme
(The MathWorks) code.
Internanotube Exciton Energy Transfer (INEET) in Poly-
carbodiimide−SWCNTs. Amine-Poly-5−SWCNTs (18 mg/L nano-
tubes, 100 μL) was mixed with Carboxy-Poly-6−SWCNTs (18 mg/L
nanotubes, 100 μL) in a 96-well plate (96W plate, μClear, chimney
style, clear bottom, TC, sterile, Greiner Bio-One) at room temper-
ature. 2D PL measurements were performed prior to mixing,
1
9
1
) to promote multivalent π−π interactions between the
polymer and the graphitic sidewall of SWCNTs.
Raw SWCNTs (Unidym, HiPCO) were sonicated in the
presence of a polycarbodiimide from the library (Poly-3−7) to
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Figure 1. Polycarbodiimide encapsulation of SWCNTs. (A) Scheme showing the preparation of polymer−SWCNT aqueous suspensions. (B)
Atomic force micrograph of Amine-Poly-7−SWCNT complexes showing periodic banding along the nanotube surface. (C) Magnified AFM image of
a single Amine-Poly-7−SWCNT complex. (D) Height profile of a single polymer−nanotube complex; direction is denoted by the red arrow in image
C.
2
1
render them soluble in an aqueous solution. The insoluble
materials were pelleted via ultracentrifugation and removed,
yielding a dark, aqueous supernatant (Figure 1A). Excess free
polymer was then removed from the suspensions by centrifugal
filtration. The aqueous suspensions were stable under ambient
conditions for several months, with no visible aggregation.
Atomic force microscopy (AFM) and transmission electron
microscopy (TEM) were conducted to characterize poly-
carbodiimide−SWCNT morphology. Images from both TEM
and AFM microscopies showed well-dispersed nanotubes (SI,
Figure S1). AFM images of Amine-Poly-7−SWCNTs (Figure
interactions, we suggest that the polymer also likely helically
encapsulated the nanotubes.
Absorption spectra of all polycarbodiimide−SWCNT com-
plexes (Figure 2A) showed characteristic E22 and E11 transition
22
features of semiconducting SWCNTs. Sharp, discrete peaks in
the absorption spectra are indicative of well-dispersed nano-
tubes. The photoluminescence efficiencies of the polymer−
nanotube complexes varied with the encapsulating polymer.
Photoluminescence intensities from polycarbodiimide−
SWCNTs (16 mg/L nanotubes, in all cases with identical
exposure conditions) differed by up to 12-fold, depending on
the polymer substituent functional group as well as the polymer
microstructure (Figure 2B). Such trends are similar to findings
1B,C), deposited and dried on freshly cleaved mica surface,
showed a distinct, periodic banding pattern along the nanotube
surface. The patterns exhibited a periodic spacing of ∼20 nm
along the nanotube axis and band heights up to ∼0.8−0.5 nm
above the surface of the nanotubes (Figure 1D). A similar
periodic pattern is observed in nanotube complexes dispersed
using carboxy- and PEG-functionalized polycarbodiimides as
well (SI, Figure S1). These observations, coupled with the long-
term stability of the polymer−nanotube suspension, suggest a
uniform conformation of these aromatic polymers along the
SWCNTs. These AFM micrographs are comparable to those
from DNA-encapsulated SWCNTs, for which a regular banding
pattern of DNA strands with a pitch of 14−20 nm along the
23
reported for DNA-encapsulated SWCNTs.
Two-dimensional photoluminescence excitation/emission
PL) spectroscopy was conducted on polycarbodiimide−
(
SWCNTs by recording emission spectra upon varying the
excitation wavelength (details in the SI). Fourteen distinct
nanotube species detected in 2D PL plots for polycarbodi-
mide−SWCNT complexes (SI, Figure S2) were assigned (n,m)
22
chirality indices according to Bachilo et al. and Weisman and
2
4
Bachilo. Excitation and emission wavelength maxima,
collected from the PL plots, fell within a narrow range that
was red-shifted relative to surfactant-suspended SWCNT
emission (Figure 2C).
Exciton energy transfer (EET) in SWCNTs has been
observed between adjacent semiconducting nanotubes in van
der Waals contact wherein large band gap donors transfer
20
nanotubes has been reported. On the basis of this regular
pattern and the similarity to the pattern of DNA−SWCNTs,
which are predicted [by all atom molecular dynamics (MD)
simulations] to helically wrap nanotubes via the π−π
25
energy to smaller band gap acceptors. In small bundles, a
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Figure 2. Optical properties of polycarbodiimide−SWCNTs. (A) Vis−nIR absorption spectra, (B) nIR emission spectra of polycarbodiimide−
SWCNTs excited at 659 nm, and (C) center wavelengths of nanotube emission peaks collected from photoluminescence excitation/emission profiles
of polycarbodiimide−SWCNTs and surfactant-suspended SWCNTs.
Figure 3. Reversible internanotube exciton energy transfer (INEET) in polycarbodiimide−SWCNTs. (A) Schematic representation of the EET
process and its reversal upon addition of amine-functionalized polycarbodiimide. (B) Photoluminescence excitation−emission (PL) map of Amine-
Poly-5−SWCNTs, Carboxy-Poly-6−SWCNTs, a mixture of Amine-Poly-5−SWCNTs and Carboxy-Poly-6−SWCNTs, and the mixture after
subsequent addition of amine-polymer.
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Figure 4. Observation of INEET dynamics in polycarbodiimide-encapsulated SWCNTs. (A) Individual spectra acquired during a time-course
acquisition of EET kinetic data. Intensity was normalized to the area under the curve. (B) EET dynamics show a monotonic relative PL intensity
increase in small band gap nanotubes (peaks 4 and 5) and simultaneous relative PL intensity decrease in large band gap nanotubes (peaks 1−3). (C)
INEET ratio, plotted using peak 5 as the acceptor and peak 1 as the donor. The final data point was acquired after initiating disaggregation using an
amine-polymer.
center to center distance of 1−4 nm between nanotubes was
aggregation, amine-functionalized polycarbodiimide polymer
was introduced. Addition of the free polymer resulted in a
recovery of the original relative PL intensities (Figure 3B and
SI, Figure S3A) concomitant with the disappearance of large
aggregates (SI, Movie S2). Plotting the net recovery of (n,m)
intensities showed a semimonotonic trend with emission
wavelength (SI, Figure S3C). The results from these experi-
ments demonstrated that inter-nanotube EET can be triggered
between nanotubes that are individually encapsulated with their
own functional coatings.
26
shown to optimize energy transfer. Recent studies have
shown that exciton energy transfer rates in SWCNTs vary
depending on a number of factors, including surface
2
7
28
functionalization, and ranges from picoseconds to femto-
2
9
seconds. With a functionally diverse set of polymer−
SWCNTs in hand, we first investigated the possibility of
initiating internanotube exciton energy transfer (INEET)
events. Figure 3A illustrates a schematic representation of the
process. Figure 3B shows 2D PL plots of two oppositely
charged polymer−nanotube complexes (ζ-potential values
Next, we investigated transient INEET events in aqueous
suspensions of polymer−SWCNT complexes. Dynamic meas-
urements of INEET dynamics (Figure 4) illustrate that the
process is spontaneous, controllable, and reversible. Upon
mixing the aforementioned oppositely charged nanotubes, the
photoluminescence intensities of large band gap nanotubes
exhibited a monotonic decrease [e.g., (8,3), (6,5), etc. species,
peaks 1−3], while small band gap nanotube emission exhibited
a simultaneous relative increase [e.g., (8,7), (9,5), etc. species,
peaks 4 and 5; Figure 4A). The relative fluorescence intensities
of each peak, plotted over time, illustrate INEET dynamics
between large and small band gap nanotubes (Figure 4B).
Each intensity−time curve was fit with the logistic function as
this function has been used to approximate the kinetics of
6
1
7.93 ± 2.73 mV for Amine-Poly-5−SWCNTs and −62.93 ±
.28 mV for Carboxy-Poly-6−SWCNTs) and the resulting
mixture after incubation for 40 h at room temperature.
Complexes were chosen to take advantage of strong Coulombic
attraction between primary amine groups (cationic protonated
form, SI) and carboxylic acid groups (anionic carboxylate form,
SI) to bring nanotubes encapsulated in corresponding polymers
into a favorable distance for INEET, without creating
irreversible van der Waals bundles. Mixing the two polymer−
SWCNT complexes resulted in an overall emission decrease in
PL measurements (SI, Figure S3A), yet the emission of smaller
band gap SWCNTs [e.g.; (8,7) and (9,5) species] increased
with respect to that of large band gap SWCNTs [e.g.; (8,3),
(
6,5), and (7,5) species, Figure 3B], suggesting exciton energy
transfer from large band gap donor nanotubes to smaller band
gap acceptor nanotubes. The relative intensity increase was
found to exhibit an (n,m) dependence that was virtually
monotonic with emission wavelength (SI, Figure S3B).
Photoluminescence quenching in the SWCNT-EET process
31
protein aggregation (SI, Figure S6A). The kinetics of peaks 1
and 5 also fit well as the reactant and the final product in a
series of first-order forward reactions, respectively (SI, Figure
S6B). The first-order behavior suggests that the larger band gap
nanotubes within peak 1 act almost purely as energy donors
and the smaller band gap nanotubes within peak 5 as energy
acceptors. Using the above information, the INEET ratio,
plotted as I /(I + I ), where I is the acceptor intensity and I is
25
has been reported3 and was attributed to the presence of
0
metallic SWCNTs. In our study, charge-induced clustering of
the two polymer−SWCNT complexes in the mixture likely
brought metallic tubes closer to semiconducting tubes, resulting
in the overall decrease in photoluminescence intensity. Upon
mixing the suspensions, nanotubes coalesced into free-floating
aggregates that remained for several days without precipitating.
In separate experiments, we confirmed that fluorescent
aggregates of various sizes were formed upon mixing the two
polymer−SWCNT suspensions (SI, Figure S4 and Movie S1).
After mixing, emission peaks in the short-wavelength
excitation/long-wavelength emission range, which could not
be assigned to known (n,m) species, were enhanced (SI, Figure
S5), a signature of energy transfer in semiconducting SWCNTs
a
a
d
a
d
the donor intensity, was obtained using peak 5 as the acceptor
and peak 1 as the donor (Figure 4C). The INEET ratio shows a
gradual increase and apparent plateauing after ca 80 min. To
test reversibility, amine-functionalized polycarbodiimide poly-
mer salt solution (0.5 mg/mL) was added at 110 min time
point and the reaction was gently mixed. A near-instantaneous
reversal of INEET back to the initial ratio occurred. Movies
confirm the gradual aggregation upon mixing polymer−
nanotube complexes and the rapid disaggregation upon
addition of a free polymer (SI, Movies S1 and S2).
30
as described in the literature. In order to disrupt the
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Schmidt, H. K.; Weisman, R. B.; Engel, P. S. Carbon 2007, 45 (12),
CONCLUSIONS
■
2
(
388−2393.
We report the noncovalent functionalization of SWCNTs
through encapsulation in helical polycarbodiimides to form
water-soluble, well-dispersed polymer−nanotube complexes
with nIR emission that are stable under ambient conditions.
The polymers facilitated the intensity modulation of nanotube
fluorescence and enabled INEET between individually
encapsulated nanotubes. This is the first instance of EET
produced spontaneously between nanotubes due to Coulombic
attraction between the encapsulating polymers and displays
directed reversibility. The finding portends the measurement of
dynamic processes and a potential mechanism for switchable
molecular probes and sensors.
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Supporting Information
Supporting figures, movies, and methods, including material
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B.; Dieckmann, G. R.; Draper, R. K.; Baughman, R. H.; Musselman, I.
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Corresponding Author
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ACKNOWLEDGMENTS
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This work was supported by the NIH Director’s New Innovator
Award (DP2-HD075698), the Louis V. Gerstner Jr. Young
Investigator’s Fund, the Frank A. Howard Scholars Program,
the Alan and Sandra Gerry Metastasis Research Initiative, and
the Center for Molecular Imaging and Nanotechnology at
Memorial Sloan Kettering Cancer Center. D.R. was supported
by an American Cancer Society 2013 Roaring Fork Valley
Research Fellowship. The authors would like to thank core
facilities at Memorial Sloan Kettering Cancer Center: the
Molecular Cytology Core Facility for AFM imaging (Core
Grant P30 CA008748), the Electron Microscopy Core facility
for TEM imaging, and the Analytical Core Facility for NMR
data, FTIR instruments, and HRMS data.
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