Bicomponent β-sheet assembly of dipeptide fluorophores of opposite polarity and sensitive detection of nitro-explosives

Article abstract of DOI:10.1039/c8cc00158h

Fluorescent hydrogels of two dipeptide-pyrene amphiphiles of opposite polarity are developed via bicomponent antiparallel β-sheet co-assembly. The helical molecular assembly resulted in the formation of fluorescent nanofibers. The sandwich-like interaction of nitroaromatics within the hydrogel matrix enabled selective and sensitive detection of toxic nitro-explosives.

Full text of DOI:10.1039/c8cc00158h

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Bicomponent β-sheet assembly of dipeptide-fluorophores of
opposite polarity and sensitive detection of nitro-explosives†
Received 00th January 20xx,
Accepted 00th January 20xx
a#
a#
a#
a*
Chilakapati Madhu, Bappaditya Roy, Pandeeswar Makam, Thimmaiah Govindaraju
DOI: 10.1039/x0xx00000x
www.rsc.org/
7
Fluorescent hydrogel of two dipeptide-pyrene amphiphiles of effects on the environment and human health. Nitroaromatic
opposite polarity is developed through bicomponent antiparallel compounds (NACs), particularly trinitroaromatics are the
β-sheet co-assembly. The helical molecular assembly resulted in known explosives widely used in military, mining as well as
the formation of fluorescent nanofibers. The sandwich-like unlawful activities.8 The NACs are known toxic pollutants
interaction of nitroaromatics within the hydrogel matix rendered present in air, water and soil. Exposure to NACs leads to severe
selective and sensitive detection of toxic nitro-explosives.
adverse effects on human health, mainly targeting the
circulatory system, liver, spleen, and immune system.
Moreover, NACs and their (bio)degradation products are
Fluorescent peptide hydrogels are emerging as novel tools for
the soft materials-based detection of various biological and
environmentally relevant analytes. Peptides and proteins are
known for their inherent ability to assemble into natural
biological architectures through noncovalent interactions
9
mutagenic and carcinogenic in nature. Therefore, sensitive
and reliable chemical sensors for the detection of NAC
explosives are in high demand to protect human health,
environment and security related issues. Among several
driven coiled-coils,1
β β
-sheets,2 -hairpins,3 and amphiphilic
approaches, chemical sensors based on fluorescence (FL)
response are widely used to detect NACs.7,10 In case of FL-
4
structures . Dipeptides, the smallest of peptides with diverse
functional groups are the versatile building blocks for
based sensors, electron transfer from excited fluorophore to
acceptor guest (NACs) results in FL change, which can be
visually detected and monitored quantitatively. FL technique is
straight forward, sensitive and reliable for the detection of
numerous analytes. Therefore, suitably preorganised
fluorophore self-assembly can be developed to detect NACs by
monitoring the FL response.
5
molecular assembly and hydrogelation. The conjugation of
functional aromatic dyes with dipeptides is advantageous to
achieve extended aromatic π-stacking interaction and thereby
6
to extract optical signalling properties. However, the design of
π-stacking systems that afford special arrangement for the
intercalation of guest of interest is a challenging task. This
requires either known specific complementary interactions
In this communication, we report a novel and efficient
florescent soft sensory system for the detection of NACs. Two
dipeptide (Ala-Ala) amphiphiles were designed and
synthesised with pyrene conjugated at C-terminus (TGM-82)
and N-terminus (TGM-83) respectively, this results in dipeptide
amphiphiles of opposite polarity (Fig. 1, Scheme S1 and S2,
ESI†). TGM-82 and TGM-83 were envisioned to undergo
bicomponent molecular assembly to form 1D nanofibers which
further entangle into 3D network and form fluorescent gel in
aqueous solution (Fig. 1 and Fig. S3). The bicomponent
assembly was effected by adding 1:1 molar ratio of TGM-82
and TGM-83 into aqueous solution at pH 7.4 (Fig. S1a). The
solution transformed into the hydrogel state at 2.0 mM total
concentration owing to the balanced hydrophilic-hydrophobic
interactions that control the physical state of the system.
Notably, the individual components (TGM-82 or TGM-83)
failed to form hydrogels under similar conditions. This in fact
supports our design strategy of customised molecular ordering
(
e.g., donor-acceptor), or choice of molecules or guests which
6
disturb the self-sorting phenomena to form co-assembly. In
this context, a pre-programmed assembly can capture small
aromatic molecules via intercalation which result in wide range
of applications viz., toxic analyte detection and pollutant
removal among others.
Fluorescent hydrogels with suitably pre-organised molecular
ordering can be used as platform to develop chemical sensor
systems and devices. Such a chemical sensor system capable of
detecting explosives is sought after, due to their harmful
aBioorganic Chemistry Laboratory, New Chemistry Unit,
Jawaharlal Nehru Centre for Advanced Scientific Research,
Jakkur P. O., Bengaluru 560064, Karnataka, India.
E-mail: tgraju@jncasr.ac.in
#These authors contributed equally to this work.
†
Electronic Supplementary Information (ESI) available: Synthesis and
characterisation, hydrogel preparation, FL spectra, FTIR, rheology, lifetime data,
and analyte detection. See DOI: 10.1039/x0xx00000x
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Fig. 1 Chemical structures of pyrene conjugated dipeptide amphiphiles (TGM-82 and TGM-83, and their bicomponent assembly supported by antiparallel β-sheet
formation via non-covalent interactions. FESEM and fluorescent optical microscopy images of 1D nanofibers in the fluorescent hydrogel (inverted gel vial). Schematic
representation of the helical bicomponent assembly of TGM-82 and TGM-83 in nanofiber. Scale bar: 1 μM and 50 μM for FESEM and FL images, respectively.
via hydrogen bonding, ionic (among carboxylate and
G՛ (ω) and loss modulus, G՛ ՛ (ω), where ω is the angular
ammonium terminals) and aromatic π-π interactions. The main frequency.12 The dynamic frequency sweep experiment
advantage of the design is that it provides a highly performed at 1% constant strain showed a wide linear
programmable 3D microenvironment to study π-electron viscoelastic region (LVR) of frequency and considerably higher
deficient NACs detection via photo-induced electron transfer modulus value (G՛/G՛՛ ~ 10) (Fig. 2b). The strain plot of the
PET) mechanism. Accordingly, we prepared a fluorescent hydrogel at 1 Hz constant frequency revealed critical strain
(
hydrogel that contains assemblies of high stiffness to observe value γ = 36·2% (Fig. S4, ESI†). This signifies higher stiffness
the effect of guest diffusion into the matrix. This is particularly opposing the monotonic collapse of the hydrogel to a quasi-
useful in developing fluorescent thin-film or chip-based device liquid state. Therefore, low yield stress (σ*, 5·4 Pa) combined
to effectively allow NACs diffusion and their co-assembly with high stiffness (G՛/G՛՛) show the low compactness of the
hydrogel and characterises it as a soft elastic material.
within the hydrogel.
The bicomponent co-assembly of TGM-82 and TGM-83 at 1:1
Circular dichroism (CD) and Fourier transform infrared (FTIR)
analysis revealed the formation of antiparallel β-sheet
85 nm (Fig. 2a, Fig. S1b, ESI†). The excimer emission is structures of the 1:1 complex at 25 ºC (Fig. 2c,d). The CD
stoichiometry showed strong pyrene-excimer band at λem
=
4
attributed to effective cofacial π-π interactions of the pyrene spectra of the independent components (TGM-82 and TGM-
chromophores in the bicomponent assembly state.11 The ionic 83) and their 1:1 complex were studied. The independent
interaction between the ammonium (–NH
3
+) and caroxylate (– components did not exhibit any significant spectral features.
−
COO ) terminals is assumed to play a key role in the assembly However, the CD spectrum of 1:1 complex showed two
−
of TGM-82 and TGM-83. The ionic (COO : NH
3
+) pair is possibly positive (355 nm and 338 nm) and a negative (287 nm) signals
the best-known intra- and intermolecular zwitterionic in the pyrene-chromophore absorption regions (Fig. S1a, ESI†)
interactions in biological systems, especially among amino
acids. Therefore, the assembly formation between TGM-82
and TGM-83 was studied at different pH (1 to 12, Fig. S2, ESI†).
The maximum excimer band intensity was observed at pH 7-9,
which confirmed possible electrostatic interaction among the
components. In addition, noncovalent interactions viz.,
hydrogen bonding and aromatic π-π interactions assisted the
molecular ordering, which is responsible for the observed high
excimer emission. However, the bicomponent molecular
system (TGM-82 and TGM-83) under pH< 7 is dominated by–
+
−
NH
3
and pH> 9 by –COO . This reduced the possible ionic
attraction between the components under highly acidic or
basic conditions.
The hydrogel was prepared at 2.0 mM total concentration of
the dipeptide amphiphiles at pH 7.4 and the gel formation was
confirmed by vial inversion experiment. The hydrogel showed
blue-green FL under the UV light (λex = 365 nm) (Fig. 1).
Supramolecular gels are viscoelastic semi-solid materials that
can store or dissipate energy, and was assessed by oscillatory
rheology. The gel state is characterised by storage modulus,
Fig. 2 (a) FL spectra of TGM-82, TGM-83 and their 1:1 complex at 0.25 mM total
concentration; (b) Frequency sweep experiment in oscillatory rheology of the
hydrogel at 2.0 mM total concentration and at 25 ºC; (c) CD spectra of the
complex at 0.25 mM total concentration and at 25 ºC; and (d) FTIR spectra of
TGM-82, TGM-83 and xerogel of 1:1 complex.
2
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which suggest the formation of right-handed (P-type) helical Detection of the NACs was achieved by monitoring the FL
bicomponent organisation. A negative CD band at 220 nm is change(ꢀ ⁄ꢀꢂ × 100%) under the UV light (λex = 365 nm) (Fig.
ꢁ
consistent with β-sheet structure formation. The CD study 3a). The NACs, viz., trinitrobenzene (TNB) and trinitrotoluene
revealed the formation of ordered molecular organisation (TNT) were found to show highest FL change (quenching of
possibly through bicomponent β-sheet structure of dipeptide excimer emission at λem = 485 nm) due to their low lying
components, in addition to aromatic and ionic interactions. To HOMO energy level (Fig. 3c). The quenching mechanism could
ascertain this notion, we performed FTIR analysis of the be ascribed to the PET from excited pyrene to the electron-
independent components and their 1:1 complex. The spectrum deficient NACs (Fig. 3b).
of bicomponent assembly exhibited strong bands at 1634,
-1
The non-NACs viz., benzene, toluene were unable to induce
675 cm-1 and a shoulder band at 1685 cm , which significant FL change (Fig. 3d). The sensing efficiency was
1
corresponds to antiparallel β-sheet structure.13 Further, the found to be below 10% for all non-NACs. However, NACs
contribution of aromatic π-π interaction to the bicomponent exhibited appreciable to very high FL quenching and simple
co-assembly was evident from the hypochromic shift in the nitrobenzene (NB) or nitrophenol (NP) showed ~50%
absorption spectra (Fig. S5, ESI†). Overall, the noncovalent efficiencies. The highest efficiencies of 90%, 94.2% and 97%
interactions driven bicomponent antiparallel β-sheet assembly were observed for TNT, Cl-DNT and TNB, respectively. The
of dipeptide amphiphiles with opposite polarity resulted in the quenching efficiency increased with the electron-acceptor
formation of nanofibers of high aspect ratio, and their entangled ability of the NACs. Cl-DNT and TNB with electron withdrawing
3
D network in aqueous solvent produced hydrogels.
The hydrogel was subsequently used as soft template for the aromatic core, showed relatively higher efficiency compared to
selective and sensitive detection of NACs via change in the FL TNT with an electron donating group (−CH ) in the core. The
2
groups (−Cl and –NO ) symmetrically positioned in the
3
intensity of the excimer emission. The detection experiment overall efficiency for NACs was found to be in the order:
was carried out in the presence of a number of analytes. TNB>Cl-DNB>TNT>DMB>NB. The electron-deficient NACs bind
to electron-rich
pyrene through
donor-acceptor
interaction in the
ground state. Upon
photo-excitation, the
excited state electrons
tunnel into the low
lying LUMO of the
acceptors
causing
non-radiative decay
that led to FL-OFF
state. The lifetime (Ƭ)
of the excited electron
(
exciton) does not
change its value in the
absence and presence
of TNT (Fig. S7, ESI†)
revealing
quenching
interactions.14
static
A
“
sandwitch-like”
complex
formation
(D-A-D)
is
considered based on
the above discussion,
which is responsible
for FL change in the
system. The efficient
Fig. 3 Selection and detection of NACs via FL quenching: (a) Schematic illustration of the hydrogel-templated detection of the analytes via
PET mechanism. Proposed “sandwich-like” conformation of pyrene-NAC-pyrene within the helical nanofiber and the potential intercalative
interactions; (b) Energy profile diagram for the PET mechanism (1-5: excitation, vibrational relaxation, electron transfer, radiative decay,
and non-radiative decay, respectively ; (c) Experimental set up for the bicomponent co-assembly coated film development NACs detection;
long-range
migration along the
extended and π-
exciton
(
d-e) The selectivity of different analytes and sensitivity of TNT was measured as a function of FL change (%Quenching), inset: film-based
NACs detection, i-iv: 100 pM, 100 nM, 1 μM, and 100 μM, respectively; (f) The chemical structures of the analytes: nitromethane (NM), NB,
NP, benzoic acid (BA), chloro-dinitrobenzene (Cl-DNB), dinitrotoluene (DNT), TNB, and TNT.
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‘
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S9, ESI†).
3
4
5
The visual detection of NAC explosives at extremely low
concentrations was achieved in a film-based experiment. The
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surroundings. We designed a film-based sensory system by
quartz-coating with bicomponent assembly-system of
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film under the UV light is established as a tool for visual
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at concentration as low as 5 nM (1 ppb) and 100 nM 27 ppb)
for both TNB and TNT, respectively (Fig. S10, ESI†).
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In summary, a fluorescent hydrogel formed by the
bicomponent assembly of two dipeptide-amphiphiles of
opposite polarity (TGM-82 and TGM-83) is developed for the
selective and sensitive detection of NACs, including the most
challenging ones such as nitrophenol, trinitrobenzene and
trinitrotoluene. The antiparallel β-sheet induced co-assembly
of the dipeptides directed the helical organisation of pyrene
chromophores that provide a suitable microenvironment to
intercalate guest NACs. The sensing mechanism of NACs is
attributed to the proposed pyrene-NAC-pyrene “sandwich-
like” interaction that allowed efficient long-range exciton
migration. The sensitivity was amplified by developing thin
film-based detection platform, which also facilitated quick and
reliable visual detection of NACs. Overall, we presented a
novel design strategy and detailed study that provides a new
insight into the design of peptide-based explosive sensors,
which are likely to be useful in protecting human health,
environment and security related issues.
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Authors thank Prof. C. N. R. Rao FRS for constant support,
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DBT (BT/PR10263/NNT/28/711/2013), Govt. of India, Shiekh
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Conflicts of interest
Authors declare no conflicts of interest.
1
1
4 Formation of
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Graphical Abstract
Bicomponent β-sheet assembly of dipeptide-fluorophores of
opposite polarity and sensitive detection of nitro-explosives
Chilakapati Madhu, Bappaditya Roy, Pandeeswar Makam,
Thimmaiah Govindaraju
Fluorescent hydrogel formed by the bicomponent β-sheet co-
assembly of dipeptide-pyrene amphiphiles of opposite polarity
provide a 3D microenvironment to detect toxic nitro-explosives.
This journal is © The Royal Society of Chemistry 20xx
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