Article pubs.acs.org/Langmuir
L‑Phenylalanine-Tethered,
Naphthalene Diimide-Based, AggregationInduced, Green-Emitting Organic Nanoparticles
Pritam Choudhury, Krishnendu Das, and Prasanta Kumar Das* Department of Biological Chemistry, Indian Association for the Cultivation of Science, Jadavpur, Kolkata − 700032, India S Supporting Information *
ABSTRACT: The present article delineates the formation of green fluorescent organic nanoparticle through supramolecular aggregation of naphthalene diimide (NDI)-based, carboxybenzyl-protected, L-phenylalanine-appended bola-amphiphile, NDI-1. The amphiphilic molecule is soluble in DMSO, and, with gradual addition of water within the DMSO solution, the amphiphile starts to self-assemble via H-type aggregation to form spherical nanoparticles. These self-assembly of NDI-1 in the presence of a high amount of water exhibited aggregationinduced emission (AIE) through excimer formation. Notably, in the presence of 99% water content, the amphiphile forms spherical aggregated nanoparticles as confirmed from microscopic investigations and dynamic light scattering study. Interestingly, the emission maxima of molecularly dissolved NDI-1 (weak blue fluorescence) red-shifted upon aggregation with increase in water concentration and led to the formation of green-emitting fluorescent organic nanoparticles (FONPs) at 99% water content. These green-emitting FONPs were utilized in cell imaging as well as for efficient transportation of anticancer drug curcumin inside mammalian cells.
1. INTRODUCTION
Generally, FONPs are formed by controlled self-assembly of monodisperse π-conjugated oligomers or chromophores in mixtures of various organic solvents and water.28−30 Tuning in the structural motif of amphiphile plays a crucial role in the surfactant like self-assembly of π-conjugated oligomers toward the formation of spherical aggregates.26,31 However, aggregation-caused quenching (ACQ) weakens the fluorescence intensity of these organic nanoparticles that restricts its applications particularly in biosensing and bioimaging.18 Encouragingly, few self-assembled systems were reported to exhibit aggregation-induced emission (AIE) due to restricted intramolecular rotation of the small organic molecules.32 Since then variety of organic dyes like tetraphenylethene, siloles, cyano-substituted diarylethene and distyrylanthracene derivatives are used for synthesis of FONPs.17−19,33 In this context, naphthalene diimide (NDI) derivatives could be of great interest for synthesizing FONPs because of their extended π surface.27,34,35 NDI derivatives have been used in the designing of artificial photosynthetic systems, white light-emitting systems, light-harvesting triads, as well as pH-responsive fluorescent sensors.36−40,41 However, unlike perylenebisimide (PBI) and other mentioned dyes, the use of unsubstituted NDI derivatives as bioprobes is limited due to their poor quantum yield and low association constant of small aromatic core.42−44
Molecular self-assembly designates the spontaneous organization of small molecules to diversified structures at different scale. In this context, self-aggregation of low molecular mass amphiphiles results in the formation of different supramolecular assemblies like vesicles, liposomes, micelles, low molecular weight gels, and other noncovalent aggregates.1−16 Fluorescent organic nanoparticles (FONPs) are another fascinating manifestation of supramolecular organization where selfassembly plays the key role to construct the nanostructured spherical aggregates.17−19 Easy synthesis and flexible tuning of the intrinsic fluorescence have made FONPs a potent candidate for its exploitation across scientific disciplines.18 Over the past few decades, fluorescent bioprobes have received notable attention considering their importance primarily in different sensing applications that include environmental monitoring to chemosensing, biosensing, disease diagnosis, and others.20−22 Fluorescent probes based on inorganic nanoparticles, proteins, and organic dyes have been fabricated and explored in biomedical applications.23,24 In spite of having photostability and tunable photoluminescence, fluorescent inorganic nanoparticles (FINs) have some major limitations due to their potential toxicity and nonbiodegradability.25 In the course of overcoming these thorny issues, fluorescent organic nanoparticles (FONPs) are finding noteworthy interest in biomedicine, possibly because of their potential biodegradability and cytocompatibility.17,26,27 © 2017 American Chemical Society
Received: February 9, 2017 Revised: April 20, 2017 Published: April 24, 2017 4500
DOI: 10.1021/acs.langmuir.7b00452 Langmuir 2017, 33, 4500−4510
Article
Langmuir
to remove the organic solvent followed by drying in a vacuum pump. The crude mass was dissolved in ethyl acetate (EtOAc) and washed two times with 10% Na2CO3 aqueous solution followed by drying the organic part over dry Na2SO4. The organic part was evaporated in a rotary evaporator to obtain 2. In the final step, 1,4,5,8-naphthalenetetracarboxylic dianhydride (1.0 equiv) and 2 (2.2 equiv) was heated at 110 °C for 12 h in dry N,N-dimethylformamide (DMF) under refluxing conditions. After removal of DMF, the reaction mixture was extracted with DCM and washed with water. The organic layer was dried with anhydrous Na2SO4, and the solvent was evaporated in rotary evaporator. The final compound (NDI-1) was purified using column chromatography (100−200 mesh silica gel, 1% methanol in chloroform as an eluent), followed by precipitation in diethyl ether. NDI-1 was characterized by 1H NMR and MALDI-TOF mass spectrometry (Supporting Information). UV−Visible Study. UV−vis spectra were recorded on a PerkinElmer Lambda 25 spectrophotometer. We have taken the UV−vis spectra of NDI-1 (20 μM) in different solvent mixtures of DMSO−water varying the volume of DMSO (non-self-aggregated solvent) from 100% to 1%, i.e., (1:99 v/v) DMSO−water (selfaggregated solvent). Temperature-dependent UV−vis spectroscopic study of NDI-1 was also performed in (1:3 v/v) DMSO−water ([NDI-1] = 20 μM) to investigate the self-aggregation behavior of NDI-1. Photoluminescence Study. The emission spectra of NDI-1 solution were recorded at an excitation wavelength (λex) 350 nm with a Varian Cary Eclipse luminescence spectrometer. NDI-1 stock solution was prepared in DMSO. The required amount of NDI-1 stock solution was added to different solvent mixtures of DMSO−water so that the final concentration of NDI-1 was 5 μM. Concentrationdependent emission spectra of NDI-1 were also obtained in different solvent mixtures of DMSO−water i.e., (3:1 v/v), (1:1 v/v), and (1:99 v/v) DMSO−water. Quantum Yield (QY) Measurement. QYs are generally measured relative to an optical dilute standard fluorophore solution that exhibits a well-known quantum yield (ϕs). The quantum yields of the unknown fluorophore (ϕu) were determined by using the Parker− Rees method.
Also, it is crucial to develop AIE luminogens in a solvent systems having maximum possible water content considering their potential in biomedicine. The present study describes the synthesis and development of the N-substituted NDI-based, carboxybenzyl-protected, Lphenylalanine-appended bola-amphiphile, NDI-1 (Figure 1),
Figure 1. Structure of NDI-1.
which formed spherical organic nanoparticles through selfaggregation in a (1:99, v/v) dimethyl sulfoxide (DMSO)− water binary solvent mixture. The presence of an extended aromatic NDI core and the phenyl rings of the terminal chiral amino acid present in the bola-amphiphile may facilitate the self-aggregation through π−π stacking. Importantly, in binary mixtures of DMSO and water, the NDI-1 amphiphile showed aggregation-induced emission (AIE) through excimer formation in solution as well as in solid phase, leading to the development of green-emitting FONPs. The emitting property of this NDI based FONPs was aptly utilized in bioimaging of mammalian cells. Considering the water dispersibility and cytocompatibility of the developed FONPs, these spherical aggregates were also used as a cellular transporter for delivery of curcumin within the mammalian cells.
2. EXPERIMENTAL SECTION Materials and Methods. Silica gel of 60−120 mesh and 100−200 mesh, L-phenylalanine, N,N- dicyclohexylcarbodiimide (DCC), 4-N,N(dimethylamino) pyridine (DMAP), N-hydroxybenzotriazole (HOBT), trifluoroacetic acid (TFA), di-tert-butyldicarbonate (BOCanhydride), solvents, and all other reagents were purchased from SRL, India. Milli-Q water was used throughout the study. Thin layer chromatography (TLC) was performed on Merck precoated silica gel 60-F254 plates. Sodium hydroxide (NaOH) pellets and sodium carbonate were bought from Spectrochem, India. 1,4,5,8-Naphthalenetetracarboxylic dianhydride, 2,2′-(ethylenedioxy) bis(ethylamine), carboxybenzoyl chloride (Cbz-Cl), curcumin, thiazolyl blue tetrazolium bromide (MTT), and all deuterated solvents for NMR and Fourier transform infrared spectroscopy (FTIR) were procured from Sigma-Aldrich. Dulbecco’s Modified Eagle’s Medium (DMEM), heatactivated fetal bovine serum (FBS), and trypsin from procine pancreas were obtained from Hi-Media, India. 1H NMR spectra were recorded on an AVANCE 500 MHz (Bruker) and 300 MHz (Bruker) spectrometer. A MALDI-TOF spectrum was obtained on a Bruker spectrometer with 2,5-dihydroxy benzoic acid (DHB) as the matrix. Synthesis of NDI-1. Naphthalene diimide-based, carboxybenzylprotected, L-phenylalanine-appended amphiphile was synthesized by the methods mentioned below (Scheme S1, Supporting Information). To synthesize NDI-1, first mono-BOC-protected 2,2′-(ethylenedioxy) bis(ethylamine) (1.2 equiv) and carboxybenzyl-protected L-phenylalanine (1.0 equiv) were coupled together using DCC (1.1 equiv) as the coupling reagent in the presence of DMAP (1.1 equiv) and HOBT (1.1 equiv) in dry dichloromethane (DCM) under nitrogen atmosphere. The reaction mixture was stirred for 12 h, and after that, the organic layer was washed two times with 1(N) HCl followed by drying of the organic solvent over anhydrous sodium sulfate. Organic solvent was then evaporated, and compound 1 (Scheme S1, Supporting Information) was purified by column chromatography using 100−200 mesh silica gel. BOC group was deprotected from the coupled product 1 using TFA (1.5 equiv) in dry DCM. After 4 h of stirring, the reaction mixture was concentrated in a rotary evaporator
2 ϕu = (A sFun u 2 /A u Fn s s )ϕs
(1)
Here, Au = the absorbance of unknown sample at the excitation wavelength, As = the absorbance of reference sample at the excitation wavelength, Fu = the total area of integrated fluorescence intensity for the unknown sample when excited at the same excitation wavelength, and Fs = the area of the integrated fluorescence intensity for the known sample when excited at the same excitation wavelength. We used a solution with similar absorbance (80%) of curcumin loaded NDI-1 FONPs (in DMSO-water, 1:99 v/v) (Figure S13a, Supporting Information). Figure S13b (Supporting Information) also demonstrates that most of the curcumin molecules are retained in the NDI-1 FONPs formulation with time in 10% FBS-supplemented DMEM media. A very minute amount of drug (11%) leaked out from the drug-loaded formulation after 18 h, indicating the stable formation of curcumin-loaded NDI-1 FONPs. After successful loading of drug, we investigated the killing effect of both the native curcumin (in DMSO) and curcuminloaded NDI-1 FONPs toward the mammalian cell lines for 12 h over a concentration range 5−50 μM of curcumin (NDI-1 concentration was varied accordingly). With increasing concentration of curcumin loaded FONPs, steady increase in the killing of mammalian cells was noted (Figure 8c). The killing efficiency of curcumin loaded NDI-1 FONPs was notably higher toward the cancer cells (B16F10) than the noncancer cells (NIH3T3). At 50 μM of curcumin loaded on NDI-1 FONPs, more than 80% B16F10 cells got killed in contrast to 47% of NIH3T3 cells, whereas only around 35% mammalian cells were killed with native curcumin (50 μM in DMSO) (Figure 8c). The morphological changes in the cells shape was also investigated upon incubation of 50 μM native curcumin (in DMSO) and curcumin-loaded NDI-1 FONPs with B16F10 cells for 4 h. Bright field images of cells clearly depicts an initiation of morphological damage of cells after incubation of curcumin loaded FONPs (Figure 9a), whereas comparatively healthy cells were observed with native curcumin (Figure 9c). Also green fluorescence was noted within the damaged cells in case of curcumin loaded FONPs due to the internalization of FONP (Figure 9b). On the other hand, no notable fluorescence was found in the case of native curcumin,
4. CONCLUSION In summary, N-substituted naphthalene diimide (NDI)-based amphiphilic molecule (NDI-1) was synthesized which formed spherical shaped aggregated nanoparticles through selfassembly in 1:99 v/v DMSO−water binary solvent mixtures. The spectroscopic studies revealed the AIE of NDI-1 through excimer formation in both solution as well as solid phase, resulting in the formation of strong green fluorescent organic nanoparticles. Extended aromatic π-moiety of the NDI chromophore facilitated the formation of self-assembled nanostructures in the mixed solvent via H-type aggregation. These newly developed green FONPs, having good water dispersibility and cytocompatibility, were successfully utilized in cell imaging and as drug delivery vehicles. Hence, NDI derivative-based FONPs will have wide horizon to be exploited in biomedicine along with other scientific disciplines.
■
ASSOCIATED CONTENT
* Supporting Information S
This material is available free of charge via the Internet at http://pubs.acs.org/. The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.7b00452. Synthetic scheme of NDI-1, 1H NMR, 13C NMR, and MALDI-TOF mass spectroscopic data of NDI-1, CD spectra of NDI-1, AFM image of NDI-1 FONPs, FTIR spectra of NDI-1, solvent- and concentration-dependent 1 H NMR study of NDI-1, XRD spectrum of NDI-1, suspension stability index of NDI-1 FONPs, MTT assay of NDI-1, spectroscopic study of curcumin loading in NDI-1 FONPs, calibration graph of curcumin, and suspension stability index of curcumin loaded NDI-1 FONPs (PDF)
■
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Prasanta Kumar Das: 0000-0002-0203-8446 Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS P.K.D. is thankful to the Council of Scientific and Industrial Research (CSIR), India (ADD, CSC0302), for financial assistance. P.C. and K.D. acknowledge CSIR, India, for Research Fellowships.
■
Figure 9. Bright field and fluorescence microscopic images of B16F10 cells after 4 h of incubation with 50 μM native curcumin and curcumin-loaded NDI-1 FONPs. (a,b) B16F10 cells incubated with curcumin-loaded NDI-1 FONPs; (c, d) B16F10 cells incubated with native curcumin.
REFERENCES
(1) Xu, Y. X.; Wang, G. T.; Zhao, X.; Jiang, X. K.; Li, Z. T. SelfAssembly of vesicles from amphiphilic aromatic amide-based oligomers. Langmuir 2009, 25, 2684−2688. (2) Cuomo, F.; Ceglie, A.; Piludu, M.; Miguel, M. G.; Lindman, B.; Lopez, F. Loading and protection of hydrophilic molecules into
4508
DOI: 10.1021/acs.langmuir.7b00452 Langmuir 2017, 33, 4500−4510
Article
Langmuir liposome-templated polyelectrolyte nanocapsules. Langmuir 2014, 30, 7993−7999. (3) Vieira, V. M. P.; Liljestrom, V.; Posocco, P.; Laurini, E.; Pricl, S.; Kostiainen, M. A.; Smith, D. K. Emergence of highly-ordered hierarchical nanoscale aggregates on electrostatic binding of selfassembled multivalent (SAMul) cationic micelles with polyanionic heparin. J. Mater. Chem. B 2017, 5, 341−347. (4) Nalluri, S. K. M.; Ulijn, R. V. Discovery of energy transfer nanostructures using gelation-driven dynamic combinatorial libraries. Chem. Sci. 2013, 4, 3699−3705. (5) Nalluri, S. K. M.; Berdugo, C.; Javid, N.; Frederix, P. W. J. M.; Ulijn, R. V. Biocatalytic self-assembly of supramolecular chargetransfer nanostructures based on n-type semiconductor-appended peptides. Angew. Chem., Int. Ed. 2014, 53, 5882−5887. (6) Bai, S.; Debnath, S.; Javid, N.; Frederix, P. W. J. M.; Fleming, S.; Pappas, C.; Ulijn, R. V. Differential self-assembly and tunable emission of aromatic peptide bola-amphiphiles containing perylene bisimide in polar solvents including water. Langmuir 2014, 30, 7576−7584. (7) Okesola, B. O.; Smith, D. K. Applying low-molecular weight supramolecular gelators in an environmental setting self-assembled gels as smart materials for pollutant removal. Chem. Soc. Rev. 2016, 45, 4226−4251. (8) Versluis, F.; van Elsland, D. M.; Mytnyk, S.; Perrier, D. L.; Trausel, F.; Poolman, J. M.; Maity, C.; le Sage, V. A. A.; van Kasteren, S. I.; van Esch, J. H.; Eelkema, R. Negatively charged lipid membranes catalyze supramolecular hydrogel formation. J. Am. Chem. Soc. 2016, 138, 8670−8673. (9) Zhang, K.; Glazer, P. J.; Jennings, L.; Vedaraman, S.; Oldenhof, S.; Wang, Y.; Schosseler, F.; van Esch, J. H.; Mendes, E. A facile approach for the fabrication of 2D supermicelle networks. Chem. Commun. 2016, 52, 12360−12363. (10) Sittko, I.; Kremser, K.; Roth, M.; Kuehne, S.; Stuhr, S.; Tiller, J. C. Amphiphilic polymer conetworks with defined nanostructure and tailored swelling behavior for exploring the activation of an entrapped lipase in organic solvents. Polymer 2015, 64, 122−129. (11) Krumm, C.; Harmuth, S.; Hijazi, M.; Neugebauer, B.; Kampmann, A. L.; Geltenpoth, H.; Sickmann, A.; Tiller, J. C. Antimicrobial poly(2-methyloxazoline)s with bioswitchable activity through satellite group modification. Angew. Chem., Int. Ed. 2014, 53, 3830−3834. (12) Bhosale, S. V.; Jani, C. H.; Lalander, C. H.; Langford, S. J.; Nerush, I.; Shapter, J. G.; Villamaina, D.; Vauthey, E. Supramolecular construction of vesicles based on core-substituted naphthalene diimide appended with triethyleneglycol motifs. Chem. Commun. 2011, 47, 8226−8228. (13) Bhosale, S. V.; Jani, C.; Lalander, C. H.; Langford, S. J. Solvophobic control of core substituted naphthalene diimide nanostructures. Chem. Commun. 2010, 46, 973−975. (14) Dinda, S.; Ghosh, M.; Das, P. K. Spontaneous formation of a vesicular assembly by a trimesic acid based triple tailed amphiphile. Langmuir 2016, 32, 6701−6712. (15) Choudhury, P.; Mandal, D.; Brahmachari, S.; Das, P. K. Hydrophobic end-modulated amino-acid-based neutral hydrogelators: structure-specific inclusion of carbon nanomaterials. Chem. - Eur. J. 2016, 22, 5160−5172. (16) Mandal, D.; Mandal, S. K.; Ghosh, M.; Das, P. K. Phenylboronic acid appended pyrene-based low-molecular-weight injectable hydrogel: glucose-stimulated insulin release. Chem. - Eur. J. 2015, 21, 12042− 12052. (17) Leung, C. W. T.; Hong, Y.; Chen, S.; Zhao, E.; Lam, J. W.; Tang, B. Z. A photostable aie luminogen for specific mitochondrial imaging and tracking. J. Am. Chem. Soc. 2013, 135, 62−65. (18) Hong, Y.; Lam, J. W. Y.; Tang, B. Z. Aggregation-induced emission: phenomenon, mechanism and applications. Chem. Commun. 2009, 4332−4353. (19) An, B. K.; Kwon, S. K.; Jung, S. D.; Park, S. Y. Enhanced emission and its switching in fluorescent organic nanoparticles. J. Am. Chem. Soc. 2002, 124, 14410−14415.
(20) Wu, J.; Liu, W.; Ge, J.; Zhang, H.; Wang, P. New sensing mechanisms for design of fluorescent chemosensors emerging in recent years. Chem. Soc. Rev. 2011, 40, 3483−3495. (21) Kong, B.; Zhu, A.; Ding, C.; Zhao, X.; Li, B.; Tian, Y. Carbon dot-based inorganic−organic nanosystem for two-photon imaging and biosensing of ph variation in living cells and tissues. Adv. Mater. 2012, 24, 5844−5848. (22) Kobayashi, H.; Ogawa, M.; Alford, R.; Choyke, P. L.; Urano, Y. New strategies for fluorescent probe design in medical diagnostic imaging. Chem. Rev. 2010, 110, 2620−2640. (23) Das, K.; Sarkar, S.; Das, P. K. Fluorescent indicator displacement assay: ultrasensitive detection of glutathione and selective cancer cell imaging. ACS Appl. Mater. Interfaces 2016, 8, 25691−25701. (24) Zhang, X.; Zhang, X.; Wang, S.; Liu, M.; Zhang, Y.; Tao, L.; Wei, Y. Facile incorporation of aggregation-induced emission materials into mesoporous silica nanoparticles for intracellular imaging and cancer therapy. ACS Appl. Mater. Interfaces 2013, 5, 1943−1947. (25) Peynshaert, K.; Manshian, B. B.; Joris, F.; Braeckmans, K.; De Smedt, S. C.; Demeester, J.; Soenen, S. J. Exploiting intrinsic nanoparticle toxicity: The pros and cons of nanoparticle-induced autophagy in biomedical research. Chem. Rev. 2014, 114, 7581−7609. (26) Kumar, M.; George, S. J. Green fluorescent organic nanoparticles by self-assembly induced enhanced emission of a naphthalene diimide bolaamphiphile. Nanoscale 2011, 3, 2130−2133. (27) Li, K.; Qin, W.; Ding, D.; Tomczak, N.; Geng, J.; Liu, R.; Liu, J.; Zhang, X.; Liu, H.; Liu, B.; Tang, B. Z. Photostable fluorescent organic dots with aggregation-induced emission (AIE dots) for noninvasive long-term cell tracing. Sci. Rep. 2013, 3, 1150. (28) Hoeben, F. J. M.; Jonkheijm, P.; Meijer, E. W.; Schenning, A. P. H. J. About supramolecular assemblies of π-conjugated systems. Chem. Rev. 2005, 105, 1491−1546. (29) Babu, S. S.; Praveen, V. K.; Ajayaghosh, A. Functional π-gelators and their applications. Chem. Rev. 2014, 114, 1973−2129. (30) Bell, T. D. M.; Bhosale, S. V.; Forsyth, C. M.; Hayne, D.; Ghiggino, K. P.; Hutchison, J. A.; Jani, C. H.; Langford, S. J.; Lee, M. A. P.; Woodward, C. P. Melt-induced fluorescent signature in a simple naphthalenediimide. Chem. Commun. 2010, 46, 4881−4883. (31) Zhang, X.; Rehm, S.; Safont-Sempere, M. M.; Wurthner, F. Vesicular perylene dye nanocapsules as supramolecular fluorescent pH sensor systems. Nat. Chem. 2009, 1, 623−629. (32) Luo, J.; Xie, Z.; Lam, J. W. Y.; Cheng, L.; Chen, H.; Qiu, C.; Kwok, H. S.; Zhan, X.; Liu, Y.; Zhu, D.; Tang, B. Z. Aggregationinduced emission of 1-methyl-1,2,3,4,5-pentaphenylsilole. Chem. Commun. 2001, 1740−1741. (33) Zhang, X.; Chi, Z.; Zhang, J.; Li, H.; Xu, B.; Li, X.; Liu, S.; Zhang, Y.; Xu, J. Piezofluorochromic Properties and mechanism of an aggregation-induced emission enhancement compound containing nhexyl-phenothiazine and anthracene moieties. J. Phys. Chem. B 2011, 115, 7606−7611. (34) Kumar, M.; George, S. J. Spectroscopic probing of the dynamic self-assembly of an amphiphilic naphthalene diimide exhibiting reversible vapochromism. Chem. - Eur. J. 2011, 17, 11102−11106. (35) Kulkarni, C.; George, S. J. Carbonate linkage bearing naphthalenediimides: self- assembly and photophysical properties. Chem. - Eur. J. 2014, 20, 4537−4541. (36) Wasielewski, M. R. Self-Assembly strategies for integrating light harvesting and charge separation in artificial photosynthetic systems. Acc. Chem. Res. 2009, 42, 1910−1921. (37) Molla, M. R.; Ghosh, S. Hydrogen-bonding-mediated Jaggregation and white-light emission from a remarkably simple, single-component, naphthalenediimide chromophore. Chem. - Eur. J. 2012, 18, 1290−1294. (38) Wu, S.; Zhong, F.; Zhao, J.; Guo, S.; Yang, W.; Fyles, T. Broadband visible light-harvesting naphthalenediimide (ndi) triad: study of the intra-/intermolecular energy/electron transfer and the triplet excited state. J. Phys. Chem. A 2015, 119, 4787−4799. (39) Doria, F.; Nadai, M.; Sattin, G.; Pasotti, L.; Richter, S. N.; Freccero, M. Water soluble extended naphthalene diimides as pH 4509
DOI: 10.1021/acs.langmuir.7b00452 Langmuir 2017, 33, 4500−4510
Article
Langmuir fluorescent sensors and G-quadruplex ligands. Org. Biomol. Chem. 2012, 10, 3830−3840. (40) Kobaisi, M. A.; Bhosale, S. V.; Latham, K.; Raynor, A. M.; Bhosale, S. V. Functional naphthalene diimides: synthesis, properties, and applications. Chem. Rev. 2016, 116, 11685−11796. (41) Wurthner, F. Perylene bisimide dyes as versatile building blocks for functional supramolecular architectures. Chem. Commun. 2004, 1564−1579. (42) Bhosale, S. V.; Jani, C. H.; Langford, S. J. Chemistry of naphthalene diimides. Chem. Soc. Rev. 2008, 37, 331−342. (43) Cubberley, M. S.; Iverson, B. L. 1H nmr investigation of solvent effects in aromatic stacking interactions. J. Am. Chem. Soc. 2001, 123, 7560−7563. (44) Shao, H.; Parquette, J. R. A π-conjugated hydrogel based on an Fmoc-dipeptide naphthalene diimide semiconductor. Chem. Commun. 2010, 46, 4285−4287. (45) Brouet, I.; Ohshima, H. Curcumin, an anti-tumor promoter and anti-inflammatory agent, inhibits induction of nitric oxide synthase in activated macrophages. Biochem. Biophys. Res. Commun. 1995, 206, 533−540. (46) Anand, P.; Kunnumakkara, A. B.; Newman, R. A.; Aggarwal, B. B. Bioavailability of curcumin: problems and promises. Mol. Pharmaceutics 2007, 4, 807−818. (47) Li, H.; Zhang, N.; Hao, Y.; Wang, Y.; Jia, S.; Zhang, H.; Zhang, Y.; Zhang, Z. Formulation of curcumin delivery with functionalized single-walled carbon nanotubes: characteristics and anticancer effects in vitro. Drug Delivery 2014, 21, 379−387.
4510
DOI: 10.1021/acs.langmuir.7b00452 Langmuir 2017, 33, 4500−4510
