TMDC Nanozymes: Application Perspective: History
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Subjects: Cell & Tissue Engineering | Immunology | Toxicology
Contributor:
Birendra Behera

Applications of TMDC NZs in different fields—starting from biosensing to different treatment fields like antibacterial, anti-inflammation activity and cancer therapy—are discussed in more details. 

  • nanozymes
  • transition metal dichalcogenides
  • biosensing
  • anticancer
  • antimicrobial
  • cytoprotection

1. Biosensing Applications

A biosensor is an analytical system that can detect a specific biological analyte and translate presence and/or concentration information into analytical data, such as electrical, optical, and thermal signals, using a simple, low-cost, and time-effective operation [1][2][3]. With the advent of nanotechnology, NZ biosensors, including TMDC-based, have witnessed enormous applicability in biomedical domain, particularly diagnostics, due to their intrinsic enzymatic capabilities [1]. To date, TMDC NZs have been used to detect a variety of biochemical analytes, including tiny biomolecules (such as glucose, cholesterol, glutathione (GSH), and cysteine) as well as macromolecules (e.g., proteins).
TMDC NZ-based biosensing strategies primarily take advantage of their POD-like activity, in which they can oxidize chromogenic substrates (such as TMB, ABTS, and OPD) in the presence of H2O2 to produce colored products that can be measured colorimetrically [4][5][6]. This NZ-based H2O2 biosensing is frequently coupled with analyte-specific oxidases such as glucose oxidase (GOx), cholesterol oxidase (ChOx), xanthine oxidase (XOx), and uricase to detect glucose, cholesterol, xanthine, and uric acid, respectively, in biological samples. First, a specific oxidase enzyme metabolizes the bioanalyte in the presence of oxygen to produce a specific acidic product and H2O2 as a byproduct. This H2O2 is further sensed colorimetrically by NZs as mentioned above. Notably, within the linear detection range, the intensity of color correlates directly with the amount of bioanalyte present in the samples. The GOx/WS2 biosensor system, for example, was used to detect glucose with a linear range of 5–300 μM and a detection limit of 2.9 μM [7]. Similarly, cholesterol was successfully detected at concentrations as low as 15 μM using a ChOx/Au nanoparticle-laden MoS2 nanoribbon system [8], whereas uricase/MoS2 nanoflakes sensor could detect uric acid within a range of 0.5–100 μM in human serum samples [9].
On the contrary, the detection regimes for cysteine and glutathione (GSH) differ substantially. The ability of these materials to prevent oxidation of colorimetric substrates or revert the oxidized colored product (produced via POD-/OD-like activity of NZs) to its pristine unoxidized form is the basis for their sensing [10]. The color intensity of the reaction mix is inversely proportional to the amount of cysteine or GSH present. Previously, WS2 nanomaterial with POD-like activity was used to estimate GSH levels as low as 0.061 nM and a linear detection range of 0.1–10 nM. GSH levels in human serum samples could be measured easily and without interference from other substances [10]. Similarly, cysteine was quantified using Hg2+ stimulated OD-like activity of MoS2 QDs-Ag NPs in the 1–100 μM range [11].
TMDC NZs can also be used to detect biomacromolecules, such as proteins, in a simple and label-free manner. To date, protein biosensing has been approached in a variety of ways. For instance, lipase was found to prevent POD-like activity of MoS2, allowing its detection at concentrations as low as 5 nM [12]. Other TMDC NZs-based protein detection strategies utilize nucleic acid aptamer probes due to their target (proteins or other biomolecules) selectivity, chemical stability, and ability to be synthesized in vitro [13]. ssDNA aptamer probe/MoS2 nanosheet system was used to detect carcinoembryonic antigen (CEA). In comparison to bare MoS2 nanosheets, the POD-like activity of aptamer/MoS2 was ~4.3 times higher, enabling greater oxidation of TMB substrate and consequently higher color intensity. However, when the target analyte, CEA, is present, the attached aptamer probe releases from the MoS2 nanosheet’s surface and binds with the protein, showing a reduced TMB oxidation. This drop in color intensity can be measured and is inversely proportional to the CEA concentration. Using this method, CEA could be detected in a linear range of 50–1000 ng/mL with the detection limit of 50 ng/mL [14]. Aptamer-anchored MoS2/PtCu nanocomposites with strong OD-like activity were used to detect mucin 1 positive cells with high sensitivity and selectivity. Cells such as MCF-7 and A549, which have mucin 1 overexpression, could be detected even in populations as small as 300 cells. The use of NZs with OD-like activity, as in this case, is often advantageous because it surpasses the use of cytotoxic H2O2, thus improving the biocompatibility and allowing the biosensor to be used in conjunction with living cells [15]. Besides, protein-specific antibodies [16] or antibody/aptamer probes [17] were also physically/chemically conjugated onto TMDC NZs to detect Salmonella typhimurium-specific surface proteins and human epididymis-specific protein 4 (HE4) proteins, respectively.
Table 1 summarizes some of the recent TMDC-based NZs that have been used for molecular and macromolecular biosensing so far.
Table 1. TMDC NZs for biosensing applications.
Analyte Detected Nanozyme System Activity Assisting Enzyme Detection Type Substrate Employed Linear Range Detection Limit Stability Biological Samples Ref.
H2O2 MoS2 POD-like   Colorimetric TMB 0.125–1.75 μM 0.08 μM   Lake water [18]
H2O2 N-Doped MoS2 POD-like   Colorimetric TMB     6 months   [19]
H2O2 Au NRs-anchored MoS2/C POD-like   Colorimetric TMB 10–200 μM 1.82 μM   Cancer cells [20]
H2O2 MoS2/Ppy POD-like   Colorimetric TMB 50–2000 μM 45 μM     [21]
Glucose MoS2 POD-like GOx Colorimetric TMB 5–150 μM 1.2 μM   Human serum [22]
Glucose MoS2 QDs POD-like GOx Fluorometric   10–1500 μM 5.16 μM   Fetal bovine serum [23]
Glucose PTCA-MoS2 POD-like GOx Colorimetric TMB 20–800 µM 18.3 μM 2 months (at 4 °C) Human serum [24]
Glucose MoS2-MIL-101(Fe) POD-like GOx Colorimetric TMB 0.01−15 μM 0.01 μM 1 month Human serum [25]
Glucose MoS2@MgFe2O4 POD-like GOx Colorimetric TMB, ABTS 5–200 μM 2 μM 1 month Human serum [26]
Glucose Cysteine- MoS2 NF POD-like GOx Colorimetric ABTS 50–1000 μM 33.51 μM   Human serum [27]
Glucose Dextran-MoSe2 POD-like GOx Colorimetric TMB 40–400 µM 28 µM 10 days Human serum [28]
Glucose Chitosan-MoSe2 POD-like GOx Colorimetric TMB 5–60 µM 0.71 μM >1 month Human serum [29]
Glucose SDS–MoS2 POD-like GOx Colorimetric TMB 5–500 μM 0.57 μM   Human serum [30]
Glucose AuNPs@MoS2 QD POD-like GOx Colorimetric TMB 20–400 μM 0.068 μM 12 days Human serum, tear and saliva [31]
Glucose PVP-MoS2 NPs POD-like GOx Colorimetric TMB 1000–10,000 μM 320 μM   Fetal bovine serum [32]
Glucose WS2 POD-like GOx Colorimetric TMB 5–300 μM 2.9 μM   Human serum [33]
Glucose WS2 NS + Ag NCs POD-like GOx Chemiluminescence Sodium bicarbonate 0.03–20 μM 0.0013 μM   Human serum [34]
Glucose Hemin-WS2 POD-like GOx Colorimetric TMB 5–200 µM 1.5 μM   Human serum [35]
Glucose WSe2 POD-like GOx Colorimetric TMB 10–60 μM 10 μM     [36]
Glucose VS2 POD-like GOx Colorimetric TMB 5–250 µM 1.5 µM     [37]
Cholesterol MoS2 NS POD-like ChOx Colorimetric TMB 2–200 μM 0.76 μM   Human serum [38]
Cholesterol MoS2 nanoribbons–AuNPs POD-like ChOx Colorimetric TMB 40–1000 μM 15 μM   Human serum [39]
Cholesterol Oxidized GSH-modified MoS2 NSs POD-like ChOx Colorimetric TMB 5.36–800 μM 5.36 μM   Mouse serum [40]
GSH WS2 NSs POD-like   Colorimetric TMB 0.1–10 nM 0.061 nm   Human serum [41]
Uric acid MoS2 NFs POD-like Uricase Colorimetric TMB 0.5–100 μM 0.3 μM   Human serum [42]
Xanthine MoSe2 POD-like XOx Colorimetric TMB 10–320 µM 1.964 μM   Human serum [43]
Cysteine MoS2 QDs-Ag NPs (stimulated by Hg (II) ion) OD-like   Colorimetric TMB 1–100 μM 0.82 μM 1 month Human serum [44]
CEA Aptamer/MoS2 NSs POD-like   Colorimetric TMB 50–1000 ng/mL 50 ng/mL   Human serum [45]
Lipase MoS2 NPs POD-like   Colorimetric TMB 5–200 nM 4.8 nM     [46]
Mucin 1 Aptamer-MoS2/PtCu OD-like NA Colorimetric TMB NA 300 cells of MCF-7   MCF-7, A549, HEK293, and HepG2 [47]

2. Therapeutics

2.1. Antibacterial Activity

The annual increase in the cases of bacterial infections is one of the most challenging aspects of the global public health and safety [48]. In particular, an alarming rise in bacterial drug resistance—as a result of uncontrolled use of antibiotics—has heightened concerns in this context [49]. Significant efforts are being made to overcome this challenge through the development of novel antibacterial agents with greater efficacy and specificity than conventional antibiotics. Recently, a new type of antibacterial therapy with broadband antimicrobial capability, known as nanozyme-mediated antibacterial therapy (NABT), has been introduced. It entails the use of NZs, including TMDC-based, with POD-/OD-like enzymatic activities to regenerate ROS, which then exerts antibacterial effects via oxidation of the bacterial membrane’s polysaccharides, proteins, and lipids [50].
The antibacterial activity of TMDC NZs, along with their relatively biocompatible nature, may be advantageous during the wound healing process. Bacterial infections have already been shown to delay healing by increasing inflammatory responses at the wound site [51]. As a result, using appropriate antibacterial agents could help to restore and balance the accurate healing microenvironment and avoid any delays. MoSe2 nanosheets/carboxyl-modified silk fibroin based wound dressing exerted considerable antibacterial effects on Escherichia coli and Bacillus subtilis due to their POD-like activity. The studies were conducted both in vitro and in vivo in E. coli-infected full-skin defect mice model in the presence of low amounts of H2O2 [52]. Another study used lysozyme, an enzyme capable of hydrolyzing bacterial cell wall peptidoglycan, as an exfoliating agent to generate MoS2 nanosheets. These nanomaterials demonstrated enhanced antibacterial activity against ampicillin-resistant E. coli and B. subtilis, which was attributed synergistically to the antibacterial activity of lysozyme and the POD-like activity of MoS2 nanosheets [53].
Another intriguing study was conducted by Niu and his colleagues, who used a combination of citraconic anhydride-modified polyethyleneimine (PEI)-MoS2 nanosheets and a photoacid generator molecule, 2-nitrobenzaldehyde (2-NBA). When 2-NBA was exposed to 365 nm light, the pH of the solution decreased, which activated the POD-like activity of the NZs to produce ROS and impart antibacterial effects. Furthermore, the irradiation time changed the charge of the nanomaterial from negative to positive, thanks to the photoreactive characteristics of citraconic anhydride, allowing Gram selectivity for the developed antimicrobial system [54].
Multimodal therapy is usually considered to be more efficient and effective at imparting antibacterial effects. NZs were combined with photothermal and chemotherapy in a study by encapsulating WS2 quantum dots (WS2 QDs) and vancomycin in a thermal-sensitive liposome. The use of WS2 QDs benefited in two ways: (i) their POD-like activity allowed the generation of ROS and (ii) their photothermal property resulted in heat generation (via 808 nm NIR laser irradiation), causing liposomal rupturing at the targeted site, resulting in a reduction in drug doses required. This anti-biofilm agent demonstrated excellent anti-biofilm activity, eradicating both E. coli and Mu50 (vancomycin-intermediate Staphylococcus aureus strain) both in vitro and in vivo [55]. Owing to POD-like activity and photothermal properties, PEG-functionalized MoS2 nanoflowers imparted an efficient antimicrobial effect and improved wound healing rate in ampicillin-resistant E. coli-infected full-skin defect mice models [56]. Another study used mesoporous ruthenium nanoparticle that was loaded and capped with ascorbic acid prodrug and hyaluronic acid, respectively. Ciprofloxacin-coated MoS2 nanosheets were further bound to the outer surface of the nanocomposite. Post-administration, hyaluronidase enzyme (produced by bacteria) would reduce the hyaluronic acid capping degradation and release of ascorbic acid and MoS2 at the infected wound site. Ascorbic acid/MoS2-mediated reactive radical generation, and ruthenium nanoparticles-mediated photothermal therapy, could synergistically eliminate multidrug-resistant bacterial strains in vitro. Furthermore, this therapeutic agent demonstrated promising efficacy in S. aureus-infected mice models (tested for biofilm dispersion inhibition) and S. aureus and Pseudomonas aeruginosa infected mice models (tested for wound healing). On the other hand, Ciprofloxacin loading did not affect the antibacterial potency of these nanocomposites [18].

2.2. Cancer Therapy

Cancer is one of the leading causes of death due to its late diagnosis and insufficient effects of currently available treatments (e.g., chemotherapy, radiation therapy, and surgical treatment) [29]. NZs, including those based on TMDC, have recently gained prominence in cancer treatment. NZ-mediated cancer therapy, like antibacterial systems, uses POD-/OD-like activities to generate ROS and cause cancer cells to die [57].
NZ-mediated cancer therapy is often limited by the lower availability of intra-tumoral H2O2. To address this challenge, recently, MoSe2/CoSe2@PEG nanosheets were synthesized. Using dissolved O2 and photoexcited electrons, this system was able to produce H2O2 via a sequential single-electron transfer mechanism. Furthermore, this NZ system showed potent dual POD- and CAT-like activities, which ensured efficient generation of ●OH and O2, respectively. ●OH caused mitochondrial damage, whereas O2 alleviated hypoxia and served as a source of H2O2. The anticancer effects were amplified by the nanomaterial’s excellent photothermal characteristics, as well as redox disruptions (through intracellular GSH reduction). Besides, biodegradability and urinal/fecal elimination (within two weeks post-administration) are other notable features of this therapeutic system [58].
In another study, a glucose-responsive, H2O2 self-supplying nano-catalytic reactor was developed by self-assembly of GOx, tirapazamine (TPZ) and chitosan on the surface of MoS2 nanosheets. The catalytic mechanisms involved in the cascade are as follows: (i) catalysis of intra-tumoral glucose by GOx (in the presence of O2) to produce H2O2 and lower the pH; (ii) utilization of H2O2 by POD-like activity of MoS2 nanosheets to produce ROS—to damage the cancer cells. Meanwhile, depletion of O2 would activate TPZ, whereas MoS2 could utilize GSH to disturb cellular redox balance, further amplifying the anticancer effects. This therapeutic agent demonstrated potent anticancer effects on A549 cells in vitro and A549 tumor-bearing mice models in vivo. In contrast, even at concentrations as high as 100 g/mL, no cytotoxicity was observed in normal human umbilical vein endothelial cells (HUVEC). Furthermore, under in vivo conditions, these nanomaterials did not accumulate in normal organs, but instead degraded and were cleared out of the body, indicating minimal toxicity to normal tissues [59].
Another significant challenge in the field of nanomedicine is the development of advanced theranostic platforms with both therapeutic and diagnostic capabilities. In this regard, 3D porous MoS2 nanoflowers were synthesized, then loaded with doxorubicin and coated with PEG-PEI (conjugated with LIM Kinase 2 protein (LMP) nucleolar translocation signal peptide). LMP peptide improved the nanomaterials’ nuclear targetability in cancer cells. Thus, these materials were able to specifically target the cancer cells and could exert potent anticancer effects both in vitro (4T1 cells) and in vivo (4T1 tumor bearing mice model) through pH-responsive/NIR-enhanced doxorubicin delivery into the tumor cells, NIR-induced photothermal effects along with ROS generation due to POD-like activity of MoS2 nanoflowers. Furthermore, the excellent photoacoustic properties of these materials allowed for real-time tracking post-intravenous in the 4T1 tumor bearing mice models [60]. A smart hybrid NZ based on MoS2-coated bipyramidal gold nanostructure was developed for anticancer therapy and two-photon bioimaging. This hybrid nanomaterial produced considerable ROS due to the POD-like activity of MoS2, which was augmented further by irradiation with 808 nm NIR laser due to localized plasmonic effects. Such synergistic ROS generation exerted significant anticancer effects in HeLa cells, as confirmed by two-photon luminescence imaging [61].

2.3. Anti-Inflammatory Effect

Apart from the applications listed above, TMDC NZs, particularly those with CAT/SOD-like activity, have also been used as antioxidant materials to provide cytoprotective effects and treat inflammatory diseases/conditions such as osteoarthritis and neurodegeneration [62][63][64]. For example, MoS2 nanosheets with CAT/SOD-like activity were synthesized those were able to quench and reduce the levels of free radicals like nitric oxide (●NO), ●OH, and nitrogen-centered free radicals (●DPPH). Furthermore, treating H2O2-exposed A549 cells with these nanomaterials dramatically reduced oxidative stress [63]. Fullerene-like MoS2 (F-MoS2) is another interesting TMDC-NZs with CAT-/SOD-like activities under physiological settings that appropriate it for using for the non-surgical treatment of osteoarthritis. F-MoS2 was able to catalyze ●O2– into H2O2 and then produce water and O2. Interestingly F-MoS2 was used to protect HUVEC cells from oxidative stress induced by H2O2. Besides, F-MoS2, when coupled with hyaluronic acid (HA), could reduce the excess of ROS and prevent the depolymerization of HA in artificial synovial fluid [64]. TMDC NZ with CAT-/SOD-like activity was used to mitigate the pathology of Alzheimer’s disease by targeting neuronal mitochondria with (3-carboxypropyl)triphenyl-phosphonium bromide-conjugated 1,2-distearoyl-sn-glycero-3-phosphoethanolamine-N-[amino(PEG)-2000]-functionalized MoS2 QDs. When tested in vitro in murine-derived microglia BV2 cells, this nano-formulation dramatically decreased oxidative stress, downregulated pro-inflammatory cytokines, and elevated anti-inflammatory cytokines. Furthermore, in vitro (in BV2 cells) and in vivo (in an Alzheimer’s disease mouse model) tests revealed that these nanomaterials were able to reduce amyloid-beta (Aβ) aggregation-mediated neurotoxicity and eliminate Aβ aggregates. These were attributed to switching microglial polarization from pro-inflammatory M1 to anti-inflammatory M2, presenting a novel pathway to mitigate Alzheimer’s disease pathology [28].
Table 2. TMDC NZs for therapeutic applications.
Applications TMDCs Material Activity Mimics Targeting Molecule (if Any) Therapeutic Mechanism Therapeutic Mediators Light Characteristics (if Involved) Activity Assessed Against In Vivo Evaluation Ref.
Microbial Cells Mammalian Cells
Disinfection and wound healing MoS2/rGO POD-like, OD-like, CAT-like   ROS-mediated H2O2 Xenon lamp (100 mW/cm2) Chloramphenicol-resistant E. coli and S. aureus   S. aureus-infected full-skin defect mice models [50]
Fe3O4@MoS2-Ag POD-like   Ag+ ion-mediated toxicity, ROS-mediated, PTT H2O2, Ag+ ions NIR (808 nm, 1 W/cm2) E. coli     [43]
citraconic anhydride modified PEI-MoS2 POD-like   Disruption of surface charge, ROS-mediated H2O2, 2-nitrobenzaldehyde UV light (365 nm) E. coli and S. aureus   E. coli and S. aureus-infected full-skin defect mice models [54]
WS2 QDs-Van@lipo POD-like, OD-like   ROS-mediated, PTT, Chemotherapy H2O2, vancomycine NIR (808 nm, 1 W/cm2) E. coli and Mu50 (vancomycin-intermediate S. aureus strain)   Mice models with Mu50-infected abscess [55]
Cu NW-supported MoS2 NS POD-like   ROS-mediated, PTT H2O2 NIR (808 nm, 1 W/cm2) E. coli and S. aureus   MRSA-infected full-skin defect mice models [36]
N-doped MoS2, N-doped WS2 POD-like   ROS-mediated H2O2   Ampicillin resistant E. coli and B. subtilis   Ampicillin resistant E. coli-infected full-skin defect mice models [65]
Lysozyme exfoliated MoS2 NSs POD-like   ROS-mediated H2O2   Ampicillin-resistant E. coli and B. subtilis     [53]
PEG-MoS2 NFs POD-like   ROS-mediated, Photothermal therapy (PTT) H2O2 NIR (808 nm, 1 W/cm2) Ampicillin-resistant E. coli and B. subtilis   Ampicillin resistant E. coli-infected full-skin defect mice models [56]
CMSF-MoSe2 NSs POD-like   ROS-mediated H2O2   E. coli and B. subtilis   E. coli-infected full-skin defect mice models [52]
Anticancer therapy Glucose responsive, TMZ-loaded chitosan-MoS2 POD-like   ROS-mediated, GSH depletion, hypoxia induced TPZ activation H2O2 and TPZ     A549 cells A549 tumor-bearing mice models [59]
AuNBPs@MoS2 POD-like   ROS-mediated, PTT H2O2 NIR laser (808 nm, 2.0 W/cm2)   HeLa cells   [61]
LNP-PEG-PEI coated, Dox loaded MoS2 NFs POD-like LNP nucleolar translocation signal peptide ROS-mediated, CT, PTT, PDT Dox NIR laser (808 nm, 3.0 W/cm2)   4T1 cells 4T1 tumor-bearing mice models [60]
MoSe2/CoSe2@PEG POD-like, CAT-like   ROS-mediated, GSH depletion, PTT H2O2 NIR laser (808 nm, 1.0 W/cm2)   HepG2 cells Tumor-bearing mice models [58]
Cytoprotection MoS2 NS CAT-like, SOD-like, POD-like   Scavenging oxidative stress species     E. coli and S. aureus A549 cells   [63]
Neurodegeneration TPP-MoS2 QDs CAT-like, SOD-like TPP (mitochondrial targeting) Scavenging oxidative stress species       BV-2 cells Amyloid precursor protein/presenilin 1 (APP/PS1) double transgenic mice [28]
Osteoarthritis Fullerene-like MoS2 CAT-like, SOD-like   Scavenging oxidative stress species       HUVECs   [64]

This entry is adapted from the peer-reviewed paper 10.3390/ma15010337

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