Abstract
Different from most of the conventional platforms with dissatisfactory theranostic capabilities, supramolecular nanotheranostic systems have unparalleled advantages via the artful combination of supramolecular chemistry and nanotechnology. Benefiting from the tunable stimuli-responsiveness and compatible hierarchical organization, host–guest interactions have developed into the most popular mainstay for constructing supramolecular nanoplatforms. Characterized by the strong and diverse complexation property, cucurbit[8]uril (CB[8]) shows great potential as important building blocks for supramolecular theranostic systems. In this review, we summarize the recent progress of CB[8]-based supramolecular theranostics regarding the design, manufacture and theranostic mechanism. Meanwhile, the current limitations and corresponding reasonable solutions as well as the potential future development are also discussed.
Graphical Abstract
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Introduction
Improving the living quality is always the enthusiasm of human beings. However, all kinds of diseases persist in haunting people during their lives, bringing damages to bodies and sometimes even death [1]. Scientific community has committed to develop novel therapeutic medicines and approaches to boost drug effectiveness and reduce the grim side effects [2,3,4,5,6], aiming to harvest more in-depth understanding of life course and accordingly improve life quality [7,8,9].
Compared with the traditional nanotheranostic systems, supramolecular nanotheranostic systems exhibit unique properties attributing to their dynamic responsiveness of non-covalent interactions [10,11,12,13,14,15,16,17,98]. The 2:2 quaternary model (Fig. 2a-I) of TBP-CB[8] complex induced a noteworthy redshift in the absorption (from 346 to 360 nm) and phosphorescence emission (from 445 to 565 nm) (Ka = 1.54 × 106 M_1) (Fig. 2a-II). The mechanism was proposed that hydrogen bonding, diode–diode interaction and hydrophobic interaction triggered the CB[8]-directed stacking patterns, which not only efficiently restrained the molecular motion of TBP but also stably promoted the charge-transfer process with a redshifted visible-light wavelength. This unique CB[8]-mediated quaternary stacking mode allowed the visible-light excitation and tunable photoluminescence, enabling the engineered machining of multicolor hydrogels (Fig. 2a-III) and biological cell imaging (Fig. 2a-IV).
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Copyright 2019 Wiley–VCH Verlag GmbH & Co. KGaA, Weinheim. (b) Supramolecular phosphorescence-capturing assembly for NIR lysosome imaging. (I) Illustration of the establishment of RTP-capturing system featured with a delayed NIR emission. (II) Phosphorescent emission spectra of G with gradual addition of CB[8]. (III) Phosphorescent emission spectra of G⊂CB[8]. Inset: The time-resolved phosphorescence decay plot of G⊂CB[8] at 530 nm. Phosphorescent emission spectra of G⊂CB[8]@SC4AH/NiR (IV) and G⊂CB[8]@SC4AH/NiB (V) at different ratios of donor and acceptor. Reproduced with permission [99]. Copyright 2021 Wiley–VCH GmbH
(a) Room-temperature phosphorescence emissive supramolecular assembly excited by visible-light. (I) X-ray diffraction single-crystal structure of supramolecular assembly (TBP)2·CB[8]2. (II) Phosphorescent emission spectra of TBP with gradual addition of CB[8]. (III) Photographs of hydrogels with different ratios of TBP and CB[8] under daylight or UV light. (IV) CLSM images of Hela cells incubated with TBP and·CB[8] (1:1). Reproduced with permission [98].
Based on two kinds of macrocyclic molecules, CB[8] and amphiphilic calixarene p-sulfonatocalix[4]arene tetrahexyl ether (SC4AH), Liu et al. constructed a phosphorescence capturing system with a delayed NIR emission via the secondary assembly strategy (Fig. 2b-I) [99]. Because CB[8] offered an independent cavity to enhance the intramolecular charge transfer (ICT) between methoxyphenyl pyridinium salt and naphthalene (Ka = 1.26 × 107 M_1), intersystem cross (ISC) was improved and long-lived triplet state was obtained, which triggered a delayed phosphorescence emission at 530 nm (Fig. 2b-II). Moreover, owing to the further restraint of non-radiative relaxation via the secondary assembly with SC4AH, the phosphorescence emission of G⊂CB[8]@SC4AH was further enhanced (Fig. 2b-III). Interestingly, two phosphorescence-capturing systems with NIR emission at 635 (Fig. 2b-IV) and 675 nm (Fig. 2b-V), respectively, were feasibly acquired by introduction of Nile Red (NiR) or Nile Blue (NiB) as acceptor. More importantly, G⊂CB[8]@SC4AH/NiB not only held low cytotoxicity but also realized lysosome-targeted NIR imaging of tumor cells, providing a new multistage assembly approach for NIR imaging of living cells.
Liu et al. also reported other similar supramolecular assemblies emitting room-temperature phosphorescence on the basis of host–guest interaction and the secondary assembly strategy [146]. Trp was conjugated onto the surface of Fe3O4 nanoparticles and the hatchway of silica core, and drug-loaded raspberry-like nanoparticles were prepared based on the host–guest recognition between CB[8] and Trp (Fig. 6a-I). In the presence of IDO1, Trp was oxidized into N-formylkynurenine (F-Kyn), leading to the opening of channel gates of nanoparticles (Fig. 6a-II) and triggering the drug release specifically in tumor cells (Fig. 6a-III). Because of the high selectivity of nanocarrier to IDO1-overexpressed tumor cells, significant in vitro cytotoxicity and superior antitumor effects (Fig. 6a-IV) were acquired, providing a promising platform for accurate intracellular drug release.
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Copyright 2019 WILEY–VCH Verlag GmbH & Co. KGaA, Weinheim. (b) CB[8]-mediated microtubule aggregation for enhancing cell apoptosis. (I) Illustration of BP⊂CB[8]-mediated targeted microtubular aggregation. (II) TEM images of free MTs (up) and BP@MTs (down). (III) CLSM image of A549 cells treated with BP⊂CB[8]. (IV) The percentage of TUNEL-positive cells in tumor tissue of mice after different treatments. Reproduced with permission [152]. Copyright 2019 Wiley–VCH Verlag GmbH & Co. KGaA, Weinheim
(a) Trp/CB[8]-mediated hybrid nanoparticles for targeted drug delivery in IDO1-overexpressed tumor cells. (I) Illustration of the targeted release mechanism of hybrid supramolecular nanoparticles. (II) Transmission electron microscope (TEM) images of hybrid nanoparticles (left) and their collapse upon exposure to IDO1 (right). (III) Biodistribution of DOX in major organs and tumors at 24 h post-injection of free DOX and hybrid supramolecular nanoparticles. (IV) Tumor volume change of mice during treatment. Reproduced with permission [146].
Supramolecular methodology on the basis of cavity-bearing macrocycles has been proven as a powerful strategy to regulate the functions of many natural biomacromolecules [149,150,151]. Liu et al. presented a supramolecular microtubular system by combing primary tubulin–tubulin heterodimerization, specific peptide–tubulin recognition and cooperative host–guest complexation to seek the curative effect of intertubular aggregation (Fig. 6b-I) [152]. An benzylimidazolium-bearing antimitotic polypeptide (BP) with tubulin-targeting ability provided a anchoring point to complex with CB[8], exclusively inducing the dramatic morphological changes of MT from linear polymers to spherical nanoparticles (Ka = (8.66 ± 0.43) × 105 M_1) (Fig. 6b-II). After incubation with BP⊂CB[8], evident compact MTs were found in cellular environment (Fig. 6b-III) and a high level of apoptosis was induced in the tumor tissues (Fig. 6b-IV), demonstrating that orthogonal supramolecular interaction-enhanced intertubular aggregation provides a novel strategy for the fight against MT-related diseases.
Phototherapy
Compared with chemotherapy, photodynamic therapy (PDT) exhibits the non-invasiveness and high spatiotemporal controllability [153,154,155,156]. Photosensitizers (PSs) are the important component of PDT, which can use luminous energy to generate toxic reactive oxygen species (ROS) and then massively damage cells [157, 11a-I) [214]. Attributing to the CB[8]-mediated stereoisomeric engineering (Ka of (Z)- and (E)-complexs were 5.8 × 104 and 3.6 × 105 M−1, respectively), the excited state energy of photosensitizers flowed from the nonradiative decay to the ISC process and radiative decay, which led to the reinforced fluorescence intensity (Fig. 11a-II) and ROS productivity (Fig. 11a-III). Also, electropositivity endowed (Z)/(E)-TPE-EPy with mitochondrial targeting and the targeted antifungal PDT was realized. With the cationic shielding effect of CB[8], the dark toxicity of (Z)/(E)-TPE-EPy@CB[8] was dramatically reduced without sacrificing their PDT efficiency. This supramolecular assembly-assisted stereoisomeric engineering of photosensitizers opens up new doors for combating fungal infections.
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Copyright 2022, The Author(s). (b) CB[8]-mediated photoswitchable adhesion and release of bacteria on SLBs. (I) Chemical structures of different components and the illustration of the mechanism of bacteria adhesion and release. (II) The number of bacteria immobilized on supramolecular SLBs. (III) The number of residual bacteria immobilized on supramolecular SLBs. Reproduced with permission [218]. Copyright 2015 Wiley–VCH Verlag GmbH & Co. KGaA, Weinheim
(a) Supramolecular engineering of AIE photosensitizers for fungal killing. (I) Chemical structures of stereoisomers and corresponding supramolecular assemblies and the illustration of their sterilization mechanism via PDT. (II) Absorption and emission spectra of stereoisomers. (III) ROS generation assessment of stereoisomers and corresponding supramolecular assemblies. Reproduced with permission [214].
Surface immobilization technologies of bioactive ligands have accelerated the development of smart surfaces for biomedical applications [215, 216]. Current surface immobilization strategies ensure the spatial controlling of bioactive ligands [217], but temporal controlling of these ligands needs new strategies. Jonkheijm et al. developed the supramolecular supported lipid bilayers (SLBs) based on the supramolecular host–guest chemistry for spatio-temporal release of bacterial cells (Fig. 11b-I) [218]. The photoswitchable supramolecular ternary system was formed by assembling an azobenzene–mannose conjugate (Azo–Man) and CB[8] onto MV2+-functionalized liquid-state SLBs. Based on the photo-responsive conformational switching of azobenzene group, Escherichia coli (E. coli) enabled to bind onto supramolecular SLBs via cell-surface receptors (Fig. 11b-II), and meanwhile was specifically erased by UV irradiation (Fig. 11b-III), thus providing a potential to exploit reusable sensors.
Weed control
Because of the simple preparation, reversible oxidation–reduction quality and good electron deficiency, MV2+ derivants are the most used guest molecules in the CB[8]-mediated host–guest complexations [46]. In addition to this, MV2+ can cut off the electron transport from plastocyanin to nicotinamide adenine dinucleotide phosphate (NADP+) and disturb normal functioning of photosystem I (PSI), being able to perform a high herbicidal efficacy in gardening and agriculture [219,220,221].
Nevertheless, since taking a sip can be lethal and there are no valid antidotes clinically available currently, the toxicity of MV2+ to humans is always an unsolved safety problem [222]. Wang et al. reported a human-friendly, photo-responsive supramolecular herbicide via ternary host–guest self-assembly between an azobenzene derivative (Trans-G), MV2+ and CB[8] (Ka = 9.37 (± 2.37) × 104 M_1) [223]. Under sunlight or UV irradiation, Trans-G converted its configuration from trans- to cis- form, which in turn dissociated the ternary host–guest interactions and released MV2+ to perform herbicidal function (Fig. 12a-I). Due to owning the spatiotemporal controllability, this formulation afforded a safer toxicity profile on both zebrafish (Fig. 12a-II) and murine model (Fig. 12a-III) compared to free MV2+. Additionally, the herbicidal activity of supramolecular ternary complex was comparable to that of free MV2+ (Fig. 12a-IV), overcoming the safe issue of traditional MV2+-loaded antimicrobial agents.
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Copyright 2018 The Author(s). (b) DIA of supramolecular toxic nanoparticles for multifunctional applications. (I) Illustration of the preparation of MV-NPs and HA-MV-NPs. (II) The comparation of bacteriostasis rate after different treatments. (III) Tumor volume change of mice after different treatments. (IV) Weed control efficacy of different treatment methods. Reproduced with permission [224]. Copyright 2020 American Chemical Society
(a) Photo-responsive supramolecular vesicles for user-friendly herbicide. (I) Illustration of the CB[8]-mediated supramolecular complexation and photo-driven, reversible complexation and decomplexation. (II) Liver tissue observation of zebrafish after different treatments. (III) Survival curves of mice after different treatments. (IV) Weed control efficacy of different treatment methods. Reproduced with permission [223].
Based on the similar mechanism of ternary host−guest complexation, Wang et al. constructed a MV2+-sandwiched and HA-coated supramolecular nanoparticles (MV-NPs) for precisely performing bioactivity or toxicity (Fig. 12b-I) [224]. Benefiting by the HA-mediated hyaluronidase (HAase)-responsiveness and azobenzene-guided photo-responsiveness, HA lamination on MV-NPs could be peeled under multiple stimuli such as HAase, UV and IR irradiation, realizing decoating-induced activation (DIA) for selective antibacterial (Fig. 12b-II), anticancer (Fig. 12b-III) and even user-friendly herbicide (Fig. 12b-IV). This work supplied a new supramolecular formulation to tame and control the toxicity and bioactivity of nanomaterials for multifunctional biomedical applications.
Biomolecule detection
Immunosuppressive tumor microenvironment is one of the important reasons leading to the failure of tumor therapy, and IDO1 which regulates the metabolism between Trp and F-Kyn, is demonstrated to be an archcriminal for immune escape [225,226,227]. Therefore, the biocatalytic activity of IDO1 is closely associated with tumor progression. Although various methods have been developed to monitor the expression of IDO1, such as antibody-peptide conjugates, high-performance liquid chromatography (HPLC), colorimetric determination and commercialized Green Screen kit [228,229,230,231,232], but these methods need relatively strict derivatizations that are unsuitable for live cell analysis.
Hu et al. showed a supramolecular tandem method for real-time monitoring the intracellular activity of IDO1 (Fig. 13a-I) [233]. Aggregation-induced quenching dye MP was first encapsulated in the cavity of CB[8] to generate a binary complex MP⊂CB[8] with the enhanced green fluorescence (Ka > 106 M_1), then Trp bound the residual cavity of CB[8] to construct a ternary inclusion (MP·Trp)⊂CB[8], which was accompanied with the complete fluorescence quenching. Once encountering the intracellular IDO1, Trp in complex was immediately oxidized into NFK and luminous MP⊂CB[8] was released to illume cells (Fig. 13a-II). Because IDO1 was overexpressed in tumor cells but not in normal cells and supramolecular sensor was sensitive to the change of intracellular Trp concentration, this label-free method could precisely sort out tumor cells, avoiding the fussy pre-preparation and strict derivatizations.
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Copyright 2019 American Chemical Society. (b) CB[8]-based rotaxane chemosensor for optical detection of Trp in biological samples. (I) Design principle of supramolecular rotaxane 17. (II) Illustration of the analyte binding by rotaxane 17. (III) Illustration of the fluorescence imaging of Trp in blood serum by rotaxane 17-immobilizated glass surfaces. (IV) Fluorescence images of a microarray before and after treatment with Trp. (V) Emission intensity change of a sensor chip after treatment with different serums. Reproduced with permission [238]. Copyright 2023 The Author(s)
(a) An off −on supramolecular fluorescent biosensor for monitoring IDO1 activity in living cells. (I) Illustration of the detection mechanism of supramolecular fluorescent biosensor. (II) Fluorescence images of HepG2 cells with different treatments. Reproduced with permission [233].
Although some developed host–guest systems already offer new methods for the inspection of health-relevant biomarker Trp in the complicated media, these systems are usually accompanied with the sophisticated deproteinization and the low sensitivity owing to their weak binding affinities with Trp [234,235,236,237], thus realizing the accurate detection of Trp in untreated biological samples is highly pursued. Biedermann et al. constructed a rotaxane chemosensor for direct detection of Trp in blood and urine samples, in which CB[8], a reporter dye and β-CD respectively acted as macrocyclic molecule, axial component and stopper group (Fig. 13b-I) (log Ka = 0.2) [238]. Upon Trp drilling into the cavity of CB[8], a face-to-face π–π stacking occurred between electron-deficient dye and electron-rich Trp, which induced the charge-transfer interactions and significantly quenched the fluorescence of the reporter dye (Fig. 13b-II). This supramolecular chemosensor not only enabled high-throughput screen in a microwell plate but also realized chirality sensing and label-free enzyme reaction monitoring. Moreover, printed sensor chips outwardly immobilized with the rotaxane-microarrays could be used for fluorescence imaging of Trp (Fig. 13b-III–V), greatly overcoming the limitations of sensing in biofluids and inspiring the development of new supramolecular chemosensors for molecular diagnostics.
Norfloxacin (NOF), a third generation of quinolone antibiotics, has been widely used in the daily life of people. Whereas, the overuse of NOF has meanwhile caused serious environmental pollution as it has been detected in soil, surface water and even groundwater and drinking water. To date, several analytical methods including HPLC, side-flow immunoassay strip (LFIS), ELISA, surface-enhanced Raman spectroscopy (SERS) and capillary electrophoresis (CE) have been used to detect NOF, but expensive and time-consuming pretreatment and professional analysis technics are needed. **ao et al. reported a supramolecular fluorescence probe (DBXPY@CB[8]) to rapidly and sensitively detect norfloxacin based on host–guest interaction between CB[8] and dibromoxanthen-9-one phenylpyridine cationic derivative (DBXPY) (Fig. 14a-I) [239]. The addition of norfloxacin induced an obvious blue-shift of DBXPY@CB[8], and the detection of NOF was not affected by pesticides, amino acids and other antibiotics which contributed to a low detection limit (1.08 × 10−7 M) (Fig. 14a-II and III). With the help of smart phone RGB analysis, a quantitative and visual detection of norfloxacin in food and water can be realized without any precision instrument (Fig. 14a-IV), performing a great improvement over conventional techniques.
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Copyright 2023 Elsevier B.V. All rights reserved. (b) Supramolecular phosphorescent probe for determination of dodine. (I) Chemical structures of different components and the schematic illustration of the detection mechanism of supramolecular phosphorescent probe. (II) Phosphorescent emission change of CB[8]-BPCOOH after addition of different pesticides. (III) Phosphorescent photographs of CB[8]-BPCOOH-based solid film in the presence of different pesticides. (IV) Phosphorescent photographs of CB[8]-BPCOOH-based indicator paper in the presence of different concentrations of dodine. Reproduced with permission [240]. Copyright 2022 American Chemical Society
(a) A supramolecular fluorescent probe for determination of norfloxacin. (I) Schematic illustration of the self-assembly of supramolecular fluorescent probe. (II) The fluorescence emission change of DBXPY@CB[8] after addition of different drugs. (III) Fluorescence photographs of DBXPY@CB[8] after addition of various drugs, pesticides and amino acids. (IV) Schematic illustration of the detection process of supramolecular fluorescent probe. Reproduced with permission [239].
Different from the above fluorescence detections, **ao et al. developed a supramolecular charge-transfer dimer (CB[8]-BPCOOH) featuring RTP for detection of dodine (Fig. 14b-I) [240]. Benefiting by the host–guest interaction between CB[8] and BPCOOH, the molecular rotation of BPCOOH was inhibited and the water molecules and oxygen in surrounding microenvironment were isolated, which significantly improved the RTP emission behavior of BPCOOH. Interestingly, CB[8]-BPCOOH only specifically recognized dodine among other 10 pesticides (Fig. 14b-II), performing a dual detection capacity (phosphorescence quenching and meanwhile fluorescence enhancing), thus greatly improving the detection accuracy. Furthermore, CB[8]-BPCOOH could be functionalized into solid films (Fig. 14b-III) and indicator papers (Fig. 14b-IV) which were equipped with the advantages of fast identification and easy portability, providing more probabilities for cucurbit[n]uril-based RTP material.
Conclusion and outlooks
Now, a myriad of CB[8]-based supramolecular theranostic systems have been developed to improve the limitations of current medical technologies. Benefiting from the CB[8]-based host–guest chemistry, the solubility/stability, pharmacokinetics behaviors as well as the duration of activity of loaded-drugs are significantly improved, hopefully fulfilling the high requirements of personalized treatment. Owing to the “Lego-like” self-assembly modes and dynamic reversibility of host–guest chemistry, not only the synthesis and purification is easy and feasible, but also the spatial and temporal drug release can be realized, greatly enriching the theranostic functions and reducing the side effects. Despite CB[8]-based supramolecular theranostics have been vastly developed and acquired a great deal of brilliant progresses over the past years, there are still irremissible issues to be overcame.
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Compared to cyclodextrins with a good commercial availability in various sizes, CB[8] is not at an affordable cost nor commercially available on a large scale, which has hindered its applications in the field of pharmaceutical science communities and biomaterials. Therefore, this challenge requires continuous concerted efforts from synthetic chemists, pharmacist, and biologists to optimize the preparation conditions for the large-scale preparation of CB[8].
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Owing to the weak solubility both in water and organic solvents, CB[8] is quite chemically inert and its functionalization becomes a daunting task as a consequence. Considering the developments brought by CB[8] in the field of biomedical, there is no doubt that a number of possibilities remains to be explored in case that the functionalization of CB[8] can be unlocked.
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Except for cyclodextrins, almost no macrocycles including CB[8], have been approved or even used in clinical practice owing to their potential biotoxicity and immunogenicity. More attentions should be paid to the biocompatibility and degradability of CB[8] to avoid the systemic toxicity and immunotoxicities.
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Although CB[8]-based supramolecular theranostic systems have been engaged in a variety of biomedical fields, as mentioned and referenced earlier in this Review, more complicated theranostic means are not involved, such as ultrasound imaging (US), photoacoustic imaging (PA), single-photon emission computed tomography (SPECT), magnetic resonance imaging (MRI), X-ray computed tomography (CT), radiotherapy, ultrasound therapy and smart immunotherapy. It is the high time to develop more novel supramolecular theranostics via reasonably crossing chemistry, pharmacology, materials engineering, cancer biology and oncology.
In conclusion, we passionately believe that CB[8] and their derivatives are highly promising and potent candidates in constructing smart supramolecular nanotheranostics with the improved therapeutic effects. Prominent improvement and achievements will be achieved in the field of supramolecular theranostics and meaningful improvement of health services of human beings will be observed benefiting from the intelligent development of CB[8]-based biomaterials in the near future.
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Funding
This work was supported by the Natural Science Foundation of Jilin Province (JJKH20221056KJ), National Natural Science Foundation of China (No. 22305220), the China Postdoctoral Science Foundation (No. 2023M733360).
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DW, JW and DL proposed the project; all the authors carried out reference searching and data analysis; DW, JW and DL wrote the manuscript; YC, KP and XD made review and final editing. All authors read and approved the final manuscript.
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Wu, D., Wang, J., Du, X. et al. Cucurbit[8]uril-based supramolecular theranostics. J Nanobiotechnol 22, 235 (2024). https://doi.org/10.1186/s12951-024-02349-z
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DOI: https://doi.org/10.1186/s12951-024-02349-z