Applications of Metal Sulfide Nanoparticles in Bioimaging

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1		Sudeshna Chandra	--	3698	2023-03-28 06:39:52	\|
2	format correct	Conner Chen	-6 word(s)	3692	2023-03-29 05:53:49	\|

This entry is adapted from the peer-reviewed paper 10.3390/molecules28062553

Applications of nanotechnology have expanded into different branches of the biomedical field. Efforts are continually being made towards the development of unique nanoparticles (=NPs) which can overcome limitations of traditional therapeutics and, hence, are able to improve management of diseases. Large surface area-to-volume ratios of NPs provide a platform for easy chemical functionalization for excellent interaction with biological systems. Among the broad range of NPs studied for biomedical applications, metal sulfide nanoparticles (=M_xS_y-NPs) have been the focus of several studies. In addition to properties found at the nanoscale, M_xS_y-NPs also exhibit favorable properties such as light conversion, Fenton catalysis, immune activation and radiation enhancement. The lower electronegativity of sulfur in comparison to oxygen makes M_xS_y-NPs naturally versatile in comparison to highly exploited metal oxide ones. The versatility of M_xS_y-NPs becomes evident by the fact that they can be successfully used for various applications including different types of imaging and therapy, often alone or in combination with other materials to enhance their intended application.

metal sulfide nanoparticles bioimaging photothermal therapy

1. Magnetic Resonance Imaging

As a result of the use of non-ionizing radiation, high spatial resolution and non-invasive magnetic resonance imaging (=MRI) has become one of the most used imaging techniques in the medical field ^[1]. MRI makes use of pulsed magnetic waves to align protons present in water and images are produced by recording radio-waves released by these protons upon their relaxation to the ground state ^[2]. Contrast agents are applied to significantly improve resolution and work by reducing the longitudinal or transverse (i.e., T₁ or T₂) relaxation time of protons in water ^[3]. Studies on NPs for MR imaging have mostly focused on metal oxides such as superparamagnetic iron oxide NPs (SPIONs); however, in recent years, researchers have begun exploring M_xS_y-NPs as well ^[4]^[5]. Examples of such studies reporting the use of M_xS_y-NPs, wherein the MR contrast is brought about by the metal sulfide itself, are highlighted below.

Iron sulfide quantum dots (=FeS QDs) were synthesized via a biomimetic route using protein bovine serum albumin (=BSA) as a template. Nanoparticles based on FeS exhibit physicochemical properties similar to that of iron oxide nanoparticles as sulfur and oxygen are congeneric elements. However, iron sulfide (FeS, Fe_1−xS, FeS₂, Fe₃S₄) exist in more phases than iron oxide (Fe₃O₄, Fe₂O₃) showing more variability and also have a smaller band gap. The authors observed a strong NIR absorption which was exploited for photoacoustic imaging, whereas quantum confinement effects enabled fluorescence imaging. The longitudinal relaxation (=r₁) value of FeS QDs (5.35 mM⁻¹ s⁻¹) was found to be higher than that of corresponding aggregates (0.2 mM⁻¹ s⁻¹), which is attributed to the template-assisted synthesis ^[6]. The resulting QDs thus showed good dispersion, higher longitudinal relaxivity, extended rotational correlation time and lower magnetization in comparison to the clinically used gadolinium-based MRI contrast agent Gd-DTPA (r₁ = 3.1 mM⁻¹ s⁻¹).

A nanohybrid (=NH), based on the sulfides of bismuth and iron was prepared by Xiong et al. via biomineralization using BSA to yield Bi₂S₃/FeS₂@BSA NHs ^[7]. BSA acted as a source of sulfur, as a template for the synthesis and as a reducing agent, whereas Fe and Bi provided the contrast for MR and computed tomography (=CT) imaging, respectively. The X-ray absorption coefficient of the NHs is 8.02 HU mM⁻¹ which increased in proportion to increasing concentrations of Bi. A similar trend was observed for MRI contrast and r₂, i.e., transverse relaxivity time was determined to 53.9 mM⁻¹ s⁻¹. In vivo, Bi₂S₃/FeS₂@BSA NHs showed accumulation in the tumor with good CT and MR imaging contrast when injected intravenously in a 4T1 tumor-bearing mice ^[7]. Fu et al. exploited magnetocaloric and MR imaging properties of iron sulfide for imaging-guided thrombolysis in celiac vein thrombosis. The author’s synthesized hydrophilic polyvinyl pyrrolidone-capped Fe₃S₄-NPs with an r₂ value of 53.1 mM⁻¹ s⁻¹ ^[8]. Through simultaneous exposure to an alternating magnetic field (=AMF) and an 808 nm laser, the NP dispersion attained a temperature higher than when exposed to AMF or laser alone. In vitro, the synergistic thermal conversion resulted in near disappearance of the thrombus, whereas individual stimulation resulted in partial dissolution. When tested in a C57 mice model of deep vein thrombosis, it resulted in the reduction of thrombus, which was visualized by MR imaging. Unpaired 3D electrons in cobalt (Co) were utilized by Lv and colleagues for T₂-weighted MRI ^[9]. Therefore, the authors prepared hollow cobalt sulfide (Co₃S₄-) NPs which were coated with a shell of N-doped carbon and encapsulated the drug doxorubicin for therapeutic (chemotherapy, photothermal therapy and photodynamic therapy) and imaging (MRI and thermal imaging) applications ^[10]. The respective NPs showed a concentration-dependent increase in MR and thermal imaging contrast. In vivo, when tested in H22 tumor bearing mice, the nanoparticles showed a good contrast as compared to pre-treatment. Huang et al. synthesized Cu₂_−xS@MnS core-shell NPs in which the Cu_2−xS-NPs are surrounded by a manganese sulfide (MnS) shell ^[11]. NIR absorption by CuS enabled photothermal treatment, whereas the presence of MnS facilitated light-triggered photodynamic therapy (PDT) and MRI. The NPs showed high photothermal conversion efficiency (47.9%) and ability to generate reactive oxygen species (=ROS) in the presence of hydrogen peroxide. With respect to MRI, T₁ contrast increased in proportion to the concentration of manganese and an r₁ value of 1.243 mM⁻¹ s⁻¹ was reported. Similarly, Chen et al. reported on the assembly of CuS-MnS₂ nanoflowers for MRI-guided photothermal-photodynamic therapy ^[12].

2. Computed Tomography

In CT imaging, differential tissue thicknesses and X-ray attenuations are exploited to generate three-dimensional and cross-sectional images ^[13]. High X-ray absorption as a consequence of high atomic numbers has resulted in the application of bismuth (Bi) and tungsten as CT contrast agents ^[14]^[15]. PEGylated-WS₂-NPs, i.e., polyethylene glycol (PEG)-coated tungsten disulfide NPs for CT-guided photothermal therapy (PTT) were prepared by Wang and colleagues ^[16]. The CT-imaging ability of the NPs was tested in 4T1 tumor-bearing mice using phosphate-buffered saline (=PBS)-treated mice as a control group. In conclusion, good photothermal stability and an effective use as CT contrast agents were reported. Similarly, Wang et al. introduced manganese dioxide (MnO₂-) coated mesoporous polydopamine nanosponges (=MPDA NSs) embedded with WS₂ nanodots (=ND), i.e., MPDA-WS₂@MnO₂ for multimodal imaging guided thermo-radiotherapy of cancer ^[17]. WS₂ NDs and MPDA NSs enabled radio-sensitization and PTT in addition to contrast for CT and multi-spectral optoacoustic tomography (=MSOT), respectively. The MnO₂ component provided MRI contrast and tumor hypoxia modulating properties. In all three imaging modalities, the contrast provided by MPDA-WS₂@MnO₂-NPs increased linearly with increasing concentration of the NPs. The authors reported a CT value of 35.3 HU L g⁻¹ and a transverse relaxation value of 6.696 mM⁻¹ S⁻¹ at pH 6.5. Post intratumoral (=i.t.) and intravenous (=i.v.) administrations. In vivo, an 8- and 2.5-fold increase in signal intensity was observed for CT and MSOT imaging, respectively. Similar results were also observed for MRI.

Nosrati et al. used bismuth sulfide (Bi₂S₃-) NPs for combination therapy including chemotherapy and radiotherapy guided by CT imaging ^[18]. The Bi₂S₃-NPs were coated with BSA to improve their stability followed by curcumin encapsulation and functionalization with folic acid to yield Bi₂S₃@BSA-FA-CUR NPs. The NPs showed sustained release of curcumin, radio-sensitization effects and a linear increase in CT contrast with increasing Bi concentration. Similarly, Bi₂S₃@MSNs, i.e., bismuth sulfide NPs coated with mesoporous silica, were synthesized to enable drug delivery in addition to NIR-responsive PTT and CT imaging ^[19]. The presence of mesoporous pores in silica enabled high drug loadings up to 99%, whereas the presence of Bi resulted in a high photothermal conversion efficiency of 37%.

Wang et al. reported the synthesis of hydrophobic Cu₃BiS₃-NPs and their use for targeted photodynamic/photothermal therapy and CT/MR dual modal imaging ^[20]. Modifications to the NPs included coating with DSPE-PEG/DSPE-PEG-NH₂ (DSPE: 1, 2-Distearoyl-sn-glycero-3-phosphoethanolamine-Poly (ethylene glycol)) for hydrophilicity, conjugation of photosensitizer chlorin e6 (=Ce6) and functionalization with folic acid for targeting. The X-ray co-efficient value of Cu₃BiS₃-NPs was calculated as 17.7 HU mmol Bi/L, whereas r₁ relaxivity was found to be twice that of Gd-DTPA, which is a clinically used T₁-MRI contrast agent. In vivo, these translated into significant CT and MR contrast which peaked at 4–6 h post-i.v. injection via the tail vein. For MRI, a 281.6% increase in signal intensity was observed 6 h post-injection, whereas a quantitative CT value of 252.3 ± 25 HU was observed. Combined, the NPs were able to successfully accumulate at the tumor site and inhibit tumor growth in vivo ^[19]. In addition, Wang et al. discussed the use of rhenium disulfide (ReS₂-) NPs as gastrointestinal (=GI) tract and tumor imaging probes, due to their excellent X-ray and NIR absorption properties ^[21]. With respect to GI tract imaging, the ReS₂-NPs showed a higher signal-to-noise ratio with increasing X-ray energy 5 min post-oral administration in Kunming mice when compared to iohexol. Similar results were also observed in 4T1 tumor-bearing mice, when ReS₂-NPs were injected intratumorally, whereby the HU value increased from 30–50 to 110–150 in the tumor region ^[22].

3. Optical Imaging

When light is used to probe molecular and cellular interactions for visualization, it is called optical imaging ^[23]. Depending on the tissue composition, when light travels through it, photons may experience absorption, reflection or scattering. These interactions can be analyzed in different types of optical imaging techniques to yield unique spectral signatures ^[24]. For example, inelastic scattering of light is measured by Raman spectroscopy, whereas absorption followed by emission of light can be in fluorescence ^[4]. Optical imaging offers advantages such as the ability to image at the microscopic level and good spatial resolution but is limited by scattering of light in biological tissues. This is often overcome using imaging probes in the NIR region as there is lower absorption and scattering by soft tissue ^[24].

NPs exploited for optical imaging mostly include QDs, as their emission is often a function of their size and can be effectively tuned. Changes in the size of nanoparticles also leads to changes in their band gap which in turn influences their imaging properties. Optical bandgap, especially of semiconductor materials is inversely proportional to nanoparticle size distribution. Thus, size of QDs often plays an important role in imaging applications. The ability of M_xS_y-NPs to absorb in the second biological window, i.e., NIR-II (1000–1700 nm), thus enabling deep tissue penetration, better signal-to-noise ratio with reduced tissue auto-fluorescence has led to their widespread application in optical imaging ^[25]. M_xS_y-NPs studied for optical imaging include semiconductor metal-based QDs especially from group II–VI elements of the periodic table of the elements such as cadmium sulfide (=CdS) and zinc sulfide (=ZnS), respectively. Group I–VI semiconductor-based silver sulfide, i.e., Ag₂S-NPs are also being increasingly used in optical imaging due to properties like absorption in the second NIR window, high signal-to-background noise ratio and good resolution ^[26]. Examples of M_xS_y-NPs used for different types of optical imaging techniques are reported below.

Awasthi et al. prepared Ag₂S QDs for fluorescence imaging due to their favorable properties including high quantum yield, good photostability and biocompatibility ^[27]. To improve hydrophilicity and dispersion of the Ag₂S QDs, they were encapsulated in a PEGylated dendrimer to yield PEG-PATU-Ag₂S QDs ^[27]. When excited with a laser at 785 nm, the appropriate QDs exhibited fluorescence at 1110 nm and intensity of fluorescence improved when the QDs attained sizes greater than 25 nm. The authors also prepared A549 cancer cells labeled with Ag₂S QDs and intravenously injected them into BALB/c mice to test in vivo tracking ability of the QDs. 2 min post-administration, fluorescence signals were observed mainly from the liver which gradually decreased over time. About 30 min following administration, fluorescence signals spread throughout the body, thus showing the distribution of tumor cells in vivo. To probe the ability of Ag₂S QDs as a vascular imaging agent, PEG₁₀₀₀ was used for modification of the QDs followed by i.v. injection into BALB/c mice. After a few seconds post-administration, the main vascular system of the mouse was clearly visible using a real-time monitoring system.

Recently, silver/silver sulfide Janus NPs (=Ag/Ag₂S JNPs) for hydrogen peroxide (=H₂O₂) triggered NIR-II fluorescence imaging were reported by Zhang et al. ^[28]. In the presence of H₂O₂, the fluorescence of Ag/Ag₂S JNPs will be “turned on”, whereas in its absence a nearly quenching effect was observed. This mechanism is attributed to an inhibited electron transfer between plasmonic Ag to semiconductor Ag₂S in the JNP when treated with H₂O₂ thus giving rise to electron deficient fluorescent Ag₂S. Because of the influence of H₂O₂ on plasmonic Ag, changes in morphology induced in the Ag/Ag₂S JNPs post-treatment by H₂O₂ was assessed. Ag/Ag₂S JNPs of size ~15 nm showed a decrease in size to ~10 nm which was in accordance with the mechanism wherein addition of H₂O₂ led to oxidation and eventual etching of plasmonic Ag in the JNP ^[29]. The authors also studied the increase in fluorescence intensity of Ag/Ag₂S JNPs treated with H₂O₂ and observed a 6-fold increase 24 h post-treatment. To confirm that fluorescence arises from the Ag₂S component, Ag and Ag₂S NPs were incubated separately with MCF-7 cells. An “always on” signal was observed in the cells in contrast to an “always off” signal solely with Ag NPs. To determine the in vivo H₂O₂-triggered fluorescing ability of Ag/Ag₂S JNP, they were injected intravenously in an AILI mice model of injured liver. PBS- and only Ag₂S NP-treated groups were chosen as control groups for the study. Whereas the Ag₂S-NP-treated group showed fluorescence that was “always on”, Ag/Ag₂S JNP treated mice showed a gradual switch from off to on fluorescence signals with progressing liver injury. Harish et al. synthesized CdS QDs coated with the biopolymer chitosan to improve its stability and biocompatibility ^[30]. To test the effect of the chitosan coating, the viability of coated and bare CdS QDs were tested in human Jurkat and erythrocyte cell lines. A reduced cytotoxicity of chitosan-coated CdS QDs was found, as compared to the same concentration of solely CdS. Moreover, it was reported that coated QDs were readily taken up by cells as observed by fluorescence imaging analysis. Biocompatibility and uptake of chitosan-coated CdS QDs was attributed to reduced leaching of Cd²⁺ ions from the respective QDs leading otherwise to cytotoxic effects. In the presence of chitosan, released Cd²⁺ ions form coordination bonds with the amino groups of chitosan thus preventing contact with the cells. In another study, Xu et al. generated two cadmium telluride/cadmium sulfide (=CdTe/CdS) core-shell QDs emitting at 545 nm and 600 nm, respectively, to visualize distribution of two chemotherapeutic drugs in a tumor ^[31]. Coating of CdS over the core resulted in improved quantum efficiency, fluorescence lifetime, stability and biocompatibility of the QDs. The 5-Fluorouracil (=5-FU) and tamoxifen (=TAM) were encapsulated into CdTe/CdS QDs emitting at 545 nm and 600 nm, respectively. To test the effect of the drugs on the tumor resistant cell line MDA-MB-231, the authors conducted a set of experiments. In the first set, the cells were incubated only with QDs-5-FU and in the second set, the cells were incubated with QDs-TAM followed by QDs-5-FU. In the first experiment, green fluorescence of QDs-5-FU was observed only on the cell membrane, whereas in the second experiment green fluorescence was observed within the cell with orange-red fluorescence observed on the cell membrane.

An approach to improve the quantum yield for fluorescence imaging results from the accessibility of QDs in an alloyed core/shell structure containing ZnS in ref. ^[32]. In this study, Shim et al. modified CIS, i.e., CuInS₂ QDs, to form a ZnS-CIS alloyed core surrounded by a ZnS shell affording ZCIS/ZnS. The authors attributed this improvement to the suppression of defect states and electronic structure evolution which, in turn, increased radiative channels. In a similar study, alloy type core/shell CdSeZnS/ZnS QDs were synthesized by Kim and colleagues for bio-imaging applications ^[33]. The authors compared the quantum yield of the CdSeZnS/ZnS QDs (=alloy QDs) against conventional multilayer CdSe/CdS/ZnS QDs (=MQDs). For alloy QDs, a 1.5-fold higher quantum yield than that of MQDs was reported which significantly improved both in vitro and in vivo imaging.

4. Photoacoustic Imaging

Photoacoustic imaging (=PAI) is a type of modified ultrasound imaging modality in which imaging signals are generated through acoustic (ultrasonic) waves caused by the photothermal effects of a PTT agent and can increase the spatial resolution and imaging depth in vivo ^[34]. The broad absorption by M_xS_y-NPs in NIR-I and NIR-II resulting from localized surface plasmon resonance has led to their applications as PTT agents and thus also as PAI contrast ^[35].

Liang et al. prepared glutathione (=GSH)-capped CuS NDs for PTT and PAI via a “one-pot” synthetic methodology ^[36]. Modification with GSH ensured good water dispersibility and size restriction of the NDs (<10 nm). Under irradiation by a 980 nm laser light, the NDs showed PA contrast three times greater than that of water with a minimal concentration of 1 mM Cu. In vitro studies were followed by in vivo testing in 4T1 tumor-bearing mice. Saline or GSH-CuS NDs were injected intratumorally as control or test, respectively, followed by irradiation at 900 nm. In a control experiment, a very weak PA signal indicating low intrinsic absorption by the tumor at 900 nm, was observed. On the other hand, a good PA signal was observed in mice treated with GSH-CuS NDs with higher contrast observed in the intratumorally injected mice as evidenced by the enhanced permeation and retention (=EPR) effect and GSH coating on the surface of the NDs. Biomimetic CuS nanoprobes coated with a melanoma cell membrane (HCuSNP@B16F10) for PAI were made accessible by Wu et al. ^[37]. They loaded HCuSNP@B16F10 with indocyanine green (=ICG) and doxorubicin (=DOX) for PTT and chemotherapy studies. Cell membrane coating was confirmed by Western blotting, and cell viability remained 70% after incubation with 150 µg mL⁻¹ for 24 h. In vivo HCuSNP@B16F10 showed a significant PA signal up to 4 h after i.v. injection. In another study, Ouyang and colleagues fabricated CuS nanoparticles trapped in a dendrimer functionalized with PEGylated-RGD (=RGD-CuS DENPs) peptide for PAI-guided PTT/gene therapy ^[38]. UV–Visible spectroscopy analysis showed good absorption by RGD-CuS DENPs in the 1000–1100 nm range with the CuS core having a diameter of 3.2 nm. The nanoparticles showed PAI contrast dependent on Cu concentration wherein PA signal peaked at 12 h post-intravenous injection in vivo.

In addition to X-ray absorption studies, strong NIR absorption has resulted in the application of Bi₂S₃ NPs for PAI as well. In this respect, Zhang et al. synthesized hollow Bi₂S₃ nanospheres with urchin-like rods (=U-BSHM) for spatio-temporal controlled drug release and PTT-PAI ^[39]. This was achieved by encapsulating the phase change material (=PCM) 1-tetradecanol and doxorubicin within the microspheres. Heat generated by U-BSHM-NPs under irradiation using an 808 nm laser melted the PCM, which in turn led to the release of DOX thus achieving controlled release. The authors reported a 65.37% release of DOX when U-BSHM-NPs attained a temperature of 43 °C or higher under laser irradiation. With respect to imaging, the NPs showed a concentration-dependent increase in the PA signal intensity by 808 nm laser irradiation. A significant PA signal was also observed when the NPs were irradiated with 700 and 900 nm lasers, respectively. Zhao et al. synthesized ultra-small Bi₂S₃-NPs using self-assembled single-stranded DNA as a template and employed them imaging probe in myocardial infarction ^[40]. As a result, thereof, a good PA signal was found when tested in vivo. Similarly, Cheng et al. synthesized Bi₂S₃ nanorods (=NR) for PTT, radiotherapy, and dual modal PA/CT imaging ^[41]. In vivo, a significant PA signal post-i.v. injection of the NRs, which peaked 24 h post-treatment, was observed. With respect to CT imaging, the NRs showed an enhanced contrast as compared to the commercially available radiocontrast agent iopromide. The authors concluded that radiotherapy and PTT acted in synergism which inhibited tumor growth as well as metastasis. AgBiS₂-NDs coated with polyethyleneimine (=PEI) were developed by Lei and colleagues for theranostic applications such as PTT and dual modal PA/CT imaging ^[42]. PEI-AgBiS₂-NDs showed photothermal conversion efficiency of 35.2% which translated to a good PAI signal in vitro. With respect to CT imaging, the authors reported a slope higher than that of iobitridol which is a commercially available radiocontrast agent. The respective in vitro imaging results were correlated with in vivo observations and maximum signal intensity for CT/PA imaging was observed at 24 h post treatment.

MoS₂ which has an extinction co-efficient higher in comparison to gold nanorods (=AuNR) and a 7.8-fold higher NIR absorbance than that of graphene oxide is increasingly being used as an NIR absorbing probe with implications in biomedicine ^[43]. In order to improve the serum stability of MoS₂, Shin and colleagues synthesized hyaluronate (=HA) and MoS₂ conjugates (=HA-MoS₂) for PAI-guided PTT ^[44]. The size of MoS₂ nanoparticles increased from 61.9 nm to 85.9 nm after conjugation with HA. DLS studies revealed no significant changes in the mean hydrodynamic size of HA-MoS₂ after 7 days in comparison to MoS₂ alone, indicative of no aggregate formation and, thus, good stability. Liu et al. synthesized MoS₂ nanosheets conjugated with the dye ICG ^[45]. The conjugation led to a red shift in the absorption peak of MoS₂ from 675 nm to 800 nm for MoS₂-ICG. As a result, a 1.35- and 1.55-fold increase in signal intensity and signal-to-noise ratio were observed at 800 nm pulsed irradiation as compared to that of 675 nm, respectively. The improved PA signal intensity and penetration depth is explained to reduced tissue scattering and absorption at 800 nm. In another study, Au et al. developed nerve growth factor (NGF) targeted AuNR coated with MoS₂ nanosheets (=anti-NGF-MoS₂-AuNR) for PAI of osteoarthritis ^[46]. MoS₂ coated AuNR resulted in a 4-fold increase in PAI signal intensity and higher biocompaibility as compared to AuNR alone. Additionally, the authors also reported stable PA intensity and morphology of MoS₂ coated AuNR following irradiation for 30 min. In vivo when anti-NGF-MoS₂-AuNR were injected intravenously into Balb/c mice, PA signal peaked at 6 h post-treatment in the synovium of osteoarthritic knee. MoS₂ nanosheets modified with CuS nanoparticles were developed by Zhang and co-workers for PAI-guided chemo-PTT ^[47]. Colloidal stability and biocompatibility of the nanocomposites were improved by attachment of PEG-thiol (=PEG-SH). CuS-MoS₂-SH-PEG showed photothermal conversion efficiency higher than that of MoS₂ alone.

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Subjects: Nanoscience & Nanotechnology

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Aishwarya Shetty

Heinrich Lang

Sudeshna Chandra

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Update Date: 29 Mar 2023

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