Self-redox reaction driven in situ formation of Cu2O/Ti3C2Tx nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound

Hsu, Ya-Ju; Nain, Amit; Lin, Yu-Feng; Tseng, Yu-Ting; Li, Yu-Jia; Sangili, Arumugam; Srivastava, Pavitra; Yu, Hui-Ling; Huang, Yu-Fen; Huang, Chih-Ching; Chang, Huan-Tsung

doi:10.1186/s12951-022-01428-3

Self-redox reaction driven in situ formation of Cu₂O/Ti₃C₂T_x nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound

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Published: 19 May 2022

Volume 20, article number 235, (2022)
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Self-redox reaction driven in situ formation of Cu₂O/Ti₃C₂T_x nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound

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Ya-Ju Hsu¹^na1,
Amit Nain¹^na1,
Yu-Feng Lin¹,
Yu-Ting Tseng¹,
Yu-Jia Li¹,
Arumugam Sangili¹,
Pavitra Srivastava²,
Hui-Ling Yu¹,
Yu-Fen Huang³,
Chih-Ching Huang ORCID: orcid.org/0000-0002-0363-1129^4,5 &
…
Huan-Tsung Chang¹

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Abstract

Background

MXenes with interesting optical and electrical properties have been attractive in biomedical applications such as antibacterial and anticancer agents, but their low photogeneration efficiency of reactive oxygen species (ROS) and poor stability are major concerns against microbial resistance.

Methods

Water-dispersible single layer Ti₃C₂T_x-based MXene through etching tightly stacked MAX phase precursor using a minimally intensive layer delamination method. After addition of Cu(II) ions, the adsorbed Cu(II) ions underwent self-redox reactions with the surface oxygenated moieties of MXene, leading to in situ formation of Cu₂O species to yield Cu₂O/Ti₃C₂T_x nanosheets (heterostructures).

Results

Under NIR irradiation, the Cu₂O enhanced generation of electron–hole pairs, which boosted the photocatalytic production of superoxide and subsequent transformation into hydrogen peroxide. Broad-spectrum antimicrobial performance of Cu₂O/Ti₃C₂T_x nanosheets with sharp edges is attributed to the direct contact-induced membrane disruption, localized photothermal therapy, and in situ generated cytotoxic free radicals. The minimum inhibitory concentration of Cu₂O/Ti₃C₂T_x nanosheets reduced at least tenfold upon NIR laser irradiation compared to pristine Cu₂O/Ti₃C₂T_x nanosheets. The Cu₂O/Ti₃C₂T_x nanosheets were topically administrated on the methicillin-resistant Staphylococcus aureus (MRSA) infected wounds on diabetic mice.

Conclusion

Upon NIR illumination, Cu₂O/Ti₃C₂T_x nanosheets eradicated MRSA and their associated biofilm to promote wound healing. The Cu₂O/Ti₃C₂T_x nanosheets with superior catalytic and photothermal properties have a great scope as an effective antimicrobial modality for the treatment of infected wounds.

Graphical Abstract

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Background

Infectious diseases pose a serious threat to humankind and global economy [1]. Antimicrobial resistance (AMR), gave rise to the situation of global health emergency [2]. Once bacteria come in contact with an exposed wound, they consume nutrients from surrounding and initiate the formation of biofilm at an alarming rate, which is much faster in diabetic patients [3]. Conventional antibiotics such as streptomycin and vancomycin combat bacterial infections by causing irreparable damage to the bacteria through various mechanisms like inhibition of essential proteins [4]. Antibiotics not only treat microbial infections but also play an indispensable role in preventing severe infections in chronically ill patients such as diabetes and renal disease or who have had complex surgeries [5, 6]. Emergence of AMR along with massive reports of overdose or misuse of administered antibiotics are responsible for impotency of existing antibiotics [7]. From the year of 2050, microbial infections will account for the death of more than 10 million people per year [8]. Moreover, multidrug resistance (MDR) bacteria can produce enzymes to degrade or inactivate antibiotics, or to alter bacterial efflux pumps, targeting binding sites, and entry ports to inhibit antibiotics [9]. With the deteriorating efficiency of currently available antibiotics and growing AMR, it is of great importance to discover alternative strategies against infectious diseases.

To circumvent the challenges associated with AMR, various carbon-, metal/metal oxide-, and two-dimensional (2D) nanomaterial-based antimicrobial modalities have been developed to disintegrate bacteria via complex mechanisms, including disruption of bacterial membranes, proteolysis, degradation of DNA, or elevated oxidative stress [10,11,12,14,15,16]. These nanomaterials that are often recognized as “endogenous antimicrobial” can delay bacterial damage, and thus repeated administration inevitably leads to AMR [17]. In addition, cytotoxicity of metal ions leached out from nanoparticle surfaces is also a concern [18]. Although surface passivation is feasible using small organic ligands, polymers, and biomacromolecules, antibacterial activity is compromised [19]. Therefore, development of biocompatible nanomaterials that offer multiple routes of biocidal action in vivo systems or clinical settings is a colossal challenge.

Ultrathin 2D nanomaterials with the lateral size larger than 100 nm and thickness of only a single- or few-atoms thick (< 5 nm) represent an emerging class of antimicrobials, mainly due to their huge specific surface and faster electron transfer ensuring sufficient surface-active sites [20,21,22]. For example, Zhao et al. reported highly catalytic reduced graphene oxide nanosheets for antimicrobial therapies [23]. The nanosheets provided therapeutic potency against MDR bacteria; however, they were non-responsive to near-infrared (NIR) irradiation, and thus they do not allow in-depth tissue penetration and generation of localized heat (> 50 °C) to inactivate the bacteria. Another report, Ding et al. showed the synthesis of CuS/graphitic carbon nitride (g-C3N4) heterojunctions for NIR-laser irradiation-assisted photothermal therapy [24]. Although the heterojunctions induced faster electron transfer to promote photocatalytic performance, they could not generate H₂O₂.

Currently, MXene is a fast-growing family of 2D materials, comprised of transition metal carbides, carbonitride, and nitrides with a general formula of M_n+1X_nT_x, where M is an early transition metal (e.g., Sc, Ti, V, Cr, Zr, Nb, Mo, Hf), X is carbon and/or nitrogen, and T_x is a surface terminal group (–F, –OH, –O, etc.) [25,Full size image

Results

In situ formation of Cu₂O on Ti₃C₂T_x MXene nanosheets

Rough surfaces of tightly stacked Ti₃AlC₂ flakes (i.e., commercially purchased MAX phase; Additional file 1: Fig. S1A) were etched with a freshly prepared mixture of hydrofluoric acid and lithium fluoride to remove aluminum to yield multilayer Ti₃C₂T_x nanosheets (i.e., MXene; Fig. S1B), which were then subjected to sonication to form well-dispersed single or few layers of Ti₃C₂T_x MXene nanosheets (Fig. S1C) [34]. Selected area electron diffraction (SAED) analysis revealed a distinct (002) plane of hexagonal Ti₃C₂T_x nanosheets (Additional file 1: Fig. S2A) [35]. The X-ray diffraction (XRD) pattern of Ti₃C₂T_x nanosheets exhibits a characteristic peak centered at 6.3º ascribing to (002) basal plane of MXene (Fig. 1B) [36]. The MXene nanosheets were further incubated with CuCl₂ at an ambient temperature for 1 h to deposit Cu(II) ions onto Ti₃C₂T_x nanosheets (Fig. 1A). The XRD pattern (Fig. 1B) shows a gradual decrease in the signal intensity of (002) plane upon increasing Cu(II) concentration, indicating disruption of the crystal structure probably due to in situ self-oxidation of MXene to form Cu₂O and TiO₂ species [37]. The X-ray photoelectron spectroscopy (XPS) analysis of Ti₃C₂T_x MXene (17.2%/47.0%/21.2%) shows that relative abundance of Ti⁺/Ti²⁺/Ti³⁺ is significantly reduced after Cu deposition (Additional file 1: Fig. S3A), whereas Ti⁴⁺ (i.e., TiO₂) is greatly increased [1Db).

Generation of O₂ ^•−/H₂O₂ by Cu₂O/Ti₃C₂T_x heterostructures

First, we demonstrated the capacity of Cu₂O/Ti₃C₂T_x nanosheets to generate NIR-induced electron−hole pairs (Fig. 2A) [41]. Ti₃C₂T_x MXene could not generate photocurrent due to their intrinsic metallic/metal-like behavior upon NIR irradiation (808 nm, 0.53 W cm⁻²) [42]. On the other hand, Cu₂O/Ti₃C₂T_x nanocomposites showed obvious photocurrent responses as compared to a bare electrode, mainly due to the formation of semiconducting Cu₂O on the surface of nanosheets. The photocurrent (~ 1.83 × 10⁻⁶ A) produced by the Cu₂O/Ti₃C₂T_x nanosheets ([Cu(II)] = 25 µg mL⁻¹) is at least 2.4-fold higher than those (7.75 × 10⁻⁷ A) nanosheets prepared using 10 µg mL⁻¹ of Cu(II), suggesting that amplified photocurrent response of Cu₂O/Ti₃C₂T_x is attributed to the formation of heterostructures formed by the coupling of Cu₂O with TiO₂/Ti₃C₂T_x [43]. Further increase in Cu(II) concentration i.e., 50 or 100 µg mL⁻¹ (in terms of Cu) resulted in a significant drop in the photocurrent, probably due to higher degree oxidation of Ti₃C₂T_x MXene (TiO₂ > 94%, Additional file 1: Fig. S2). The presence of Cu₂O in crystalline Ti₃C₂T_x nanosheets created an energy barrier (i.e., Schottky junction), which restricted the electron–hole pair recombination and facilitated the faster transfer of photogenerated electrons to the surface, leading to the enhanced photocurrent response [44]. Due to the substantial photoactivity through modulating electrons-holes, we further investigated the catalytic formation of hydrogen peroxide (H₂O₂) under NIR irradiation. Efficient generation of H₂O₂ was demonstrated through a combination of Amplex Red (AR) and horseradish peroxidase (HRP) assays [45]. HRP decomposes H₂O₂ to facilitate an electron transfer induced AR-oxidation to yield a highly fluorescent product resorufin (7-hydroxy-3H-phenoxazin-3-one; quantum yield: 0.83) [46]. As-prepared Cu₂O/Ti₃C₂T_x heterostructures generated a comparable amount of H₂O₂ (10 μM), which is ~ fivefold higher than that of the Ti₃C₂T_x MXene at an ambient temperature under dark condition (Fig. 2B). Interestingly, the amount of H₂O₂ generated by Cu₂O/Ti₃C₂T_x was further improved twofold when coupled with NIR irradiation (808 nm, 0.54 W cm⁻², 10 min). In control experiments, reaction carried at 58 ºC (equivalent to the NIR induced temperature) with Cu₂O/Ti₃C₂T_x nanosheets revealed a similar trend to that of NIR laser, indicating that spontaneous formation of H₂O₂ can be ascribed to the NIR induced in situ thermal gradients (Fig. 2B) [47].

The electron spin resonance (ESR) spectra of Cu₂O/Ti₃C₂T_x heterostructures using 5,5-dimethyl-1pyrroline-N-oxide (DMPO) as a spin trap exhibited mixture of signals, corresponding to hydroxyl (⋅OH) and hydroperoxyl/superoxide (⋅OOH/O₂^•–) (Fig. 2C) [48]. In addition, a weak signal corresponding to methyl radical (H₃C⋅) was also observed, ascribing to the copper-induced oxidation of DMPO. Upon incubation at an ambient temperature for 5 min, the peak for ⋅OH quartet (1:2:2:1) became more intense, and disappeared in the presence of catalase, suggesting the ⋅OH originated from H₂O₂ (Fig. 2C) [49]. Nevertheless, the ESR spectra show weak intensity sextet ascribing to ⋅OOH/O₂^•– in the absence of NIR, under parallel conditions (Additional file 1: Fig. S6). Control group (only Cu(II)) did not reveal any obvious peak after incubating with DMPO in the absence or presence of NIR (data not shown). To confirm the formation of O₂^•– as an intermediate for subsequent formation of H₂O₂, we employed a tetrazolium dye MTT [3-(4,5-dimethyl-thiazol-2-yl) 2,5-diphenyl tetrazolium bromide] reduction method to form it’s colored formazan, as reported previously [50]. Additional file 1: Fig. S7 indicates that Cu₂O/Ti₃C₂T_x (Abs₅₇₆ ~ 0.22) produced at least fourfold higher O₂^•– as compared to the control (Abs₅₇₆ ~ 0.05) without NIR irradiation, which is consistent with the low-intensity ESR peaks shown in Additional file 1: Fig. S6. In addition, spontaneous production of O₂^•– was further improved threefold under NIR irradiation (Abs₅₇₆ ~ 0.61), which is comparable to that provided by potassium dioxide (positive control; 0.5 mg mL⁻¹).

2D structures with ultrafast charge carriers, huge surface area for redox reactions, broad-band absorption profile, and presence of heteroatom are the features of a modern photocatalyst [51]. Electrochemical behaviors of Cu₂O/Ti₃C₂T_x heterostructures were studied by cyclic voltammetry (CV). The CV curves in a wide potential window were recorded to determine the position of valence band (VB; Fig. 2Da) and conduction band (CB; Fig. 2Db) [52, 53]. The energy band gap (E_g) was calculated as 1.16 eV using Eq. (3):

$${\text{E}}_{{{\text{VB}}}} \left( {{\text{eV}}} \right) = - \left( {{\text{E}}_{{{\text{oxidation}}}} \,vs\,{\text{Ag/AgCl}} + 0.197 + 4.74} \right)$$

(1)

$${\text{E}}_{{{\text{CB}}}} \left( {{\text{eV}}} \right) = - \left( {{\text{E}}_{{{\text{reduction}}}} \,vs\,{\text{Ag/AgCl}} + 0.197 + 4.74} \right)$$

(2)

$${\text{E}}_{{\text{g}}} = {\text{E}}_{{{\text{CB}}}} - {\text{E}}_{{{\text{VB}}}}$$

(3)

As shown in Fig. 2E, Cu₂O/Ti₃C₂T_x nanosheets can promote the thermodynamically favorable formation of O₂^•– (O₂ + e⁻ → O₂^•– E⁰ = − 0.33 V) upon NIR illumination, which were subsequently converted into H₂O₂ (O₂^•– + e⁻ + 2H⁺ → H₂O₂ E⁰ = + 0.89 V) by superoxide dismutase-like Cu₂O species on the MXene surface [10,11,12,20,21,22,23]. However, r-GO was inable to provide in-depth tissue penetration or localized thermal effect to inactivate bacteria. Owing to various structural properties, MXene comes to light as a potential candidate [28, 29]. An appreciable amount of work has been going on the heterojunctions and inducing defects in these structures, but the drawback lies in using the aqueous solution with low ionic strength because of poor stability in biologically complex fluids [33]. Our developed Cu₂O/Ti₃C₂T_x nanosheets have several advantages such as facile synthesis Cu₂O/Ti₃C₂T_x nanosheets conducted at room temperature, and as-prepared nanosheets exhibited remarkable biocompatibility mainly due to their high aqueous dispersibility and low toxic natures of Cu and Ti. The Cu₂O/Ti₃C₂T_x nanosheets possess high photo-to-heat conversion efficiency and characteristic NIR absorbance, which allowed the development of a lower energy-based bacterial eradication from infected wounds. Thus they have a great scope as an antimicrobial modality for various biomedical applications.

Conclusions

We demonstrated a self-redox reaction of CuCl₂ and Ti₃C₂T_x MXene to form TiO₂ and Cu₂O species in situ on the surfaces of Ti₃C₂T_x nanosheets. Under NIR irradiation, the surface Cu₂O species on Cu₂O/Ti₃C₂T_x nanosheets boost the production of H₂O₂. In addition, temperature rise in response to low energy photons acted as a thermal gradient, which contributed to the production of H₂O₂. The MIC₉₀ values of as-prepared Cu₂O/Ti₃C₂T_x nanosheets under NIR irradiation against tested bacteria was > tenfold lower than pristine Ti₃C₂T_x MXene. Broad-spectrum antimicrobial susceptibility to various bacteria, including MDR bacteria, was achieved due to systematically generated therapeutic response, at first, sharp-edges of nanosheets physically attacked bacterium membrane (direct contact-mediated bacterial disintegration), then, NIR irradiation induced localized heat (~ 58 °C, photothermal therapy), and enhanced ROS production (catalytic therapy). The Cu₂O/Ti₃C₂T_x nanosheets showed insignificant cytotoxicity and negligible hemolytic activity against human skin cells (NIH-3T3 skin cells) and RBCs, respectively. In vivo efficacy of Cu₂O/Ti₃C₂T_x nanosheets was proven by treating the MRSA-infected surgical wounds created on diabetic mice under photoirradiation. Topically administered Cu₂O/Ti₃C₂T_x nanosheets efficiently eliminated microbial pathogenesis caused by MRSA to accelerate wound healing via angiogenesis, epithelialization, and collagen deposition. Intrinsic radical scavenging capabilities of MXene may contribute to accelerated wound healing. Anti-oxidant properties of MXene and the role of Cu₂O in enhanced stimulation of immune cells is currently under investigation. Our developed, Cu₂O/Ti₃C₂T_x nanosheets possess superior biocompatibility, photothermal efficiency, and catalytic properties, which makes them an ideal candidate for the treatment of infectious diseases and wound healing applications.

Methods

Synthesis of MXene and Cu₂O/Ti₃C₂T_x nanosheets

Nanosheets were prepared through a previously reported minimally intensive layer delamination (MILD) method, with minor modifications [34]. 40 mL of HCl (9 M) was added slowly into a PTFE bottle containing 4 g of LiF, which was then stirred for 30 min (600 r.p.m.) at ambient temperature. To which, 4 g of Ti₃AlC₂ MAX powder was slowly added over the course of 30 min. Then, the mixture was heated at 40 °C under constant stirring for 24 h and then subjected to centrifugation at a relative centrifugal force (RCF) of 3000g (10 min, 25 °C) to collect the etched multi-layered MXene in the pellet. The obtained residues were repeatedly washed with ultrapure water until the pH value reached to ~ 6.0. The delamination of purified multi-layered MXene was carried out by probe sonicator (Pulse 150 Ultrasonic Homogenizer, Thomas Scientific, Swedesboro, NJ, USA) in degassed water, under a flow of argon (Ar) gas for 4 h. During sonication, the surrounding temperature was maintained at 4 °C, while the frequency was set to 37 kHz, and the power of amplitude was 80%. The resulting solution was then centrifuged (RCF 3000×g, 5 min, 27 °C) to separate the delaminated flakes (dark green; monolayer Ti₃C₂T_x or MXene) from the unexfoliated sheets and larger particles. The concentration of purified MXene (in terms of mg mL⁻¹) was determined using freeze-drying method. Freshly prepared monolayer MXene (1.0 mg mL⁻¹, 0.5 mL) dispersed in sodium phosphate buffer (20 mM, pH 7.0) was separately incubated with CuCl₂ solutions (20, 50, 100, 200 μg mL⁻¹, in terms of Cu; 0.5 mL in water) for 1 h under continuous shaking (100 r.p.m.) at ambient temperature to obtain Cu₂O/Ti₃C₂T_x nanosheets.

Photoresponsive properties of Cu₂O/Ti₃C₂T_x nanosheets

A continuous NIR laser (808 nm) with DPSSL driver II (Tangyu Precision Machinery Industry Co., Ltd., Taipei, Taiwan) was used to evaluate photocatalytic and photothermal performances of nanosheets. Temperature profiles of 50 µg mL⁻¹ (in terms of Ti₃C₂T_x) of as-prepared Ti₃C₂T_x MXene and Cu₂O/Ti₃C₂T_x MXene dispersed in phosphate-buffered saline (PBS, pH 7.4, containing 137 mM NaCl, 2.7 mM KCl, 10 mM Na₂HPO₄, and 2.0 mM KH₂PO₄; 1 mL) solution under NIR laser irradiation (0.54 W cm⁻²) were continuously recorded using a TFC–305A Type K single input thermocouple thermometer (Yi Chun Electrics Co., Ltd., Taipei, Taiwan) for 10 min.

A freshly prepared Amplex Red (AR; 50 µM) was added into a 1.0 mL vial containing Ti₃C₂T_x or Cu₂O/Ti₃C₂T_x nanosheets (50 µg mL⁻¹; in terms of Ti₃C₂T_x) dispersed in PBS solution with horseradish peroxidase (HRP; 0.1 unit mL⁻¹) to estimate the catalytic generation of H₂O₂ [65]. The aliquots were then incubated at 0 °C, 58 °C, and at ambient temperature separately in dark and under NIR irradiation (808 nm, 0.54 W cm⁻²) for 10 min. Afterwards, the mixtures were subjected to measure the fluorescence intensity at an excitation/emission of 540/590 nm using a monochromatic microplate spectrophotometer (Synergy 4, Biotek Instruments, Winooski, VT, USA). We employed 5,5-dimethyl-1-pyrroline-N-oxide (DMPO) as a spin trap to perform Electron Spin Resonance (ESR) spectroscopy analysis for the detection of ROS. The ESR parameters are as follows: microwave power, 15 mW; microwave frequency, 9.8 gHz; scan range, 100 G; time constant, 0.328 s; sampling time, 20 ms; receiver gain, 30; modulation frequency, 100 kHz; g-factor, 2.00627; modulation amplitude, 0.1 mT.

Determination of superoxide free radical

A freshly prepared MTT (1.0 mM) was added into a 1.0 mL vial containing Cu₂O/Ti₃C₂T_x nanosheets (50 µg mL⁻¹; in terms of Ti₃C₂T_x) dispersed in PBS solution (pH 7.4) to assess the formation of MTT-formazan in the absence and presence of NIR irradiation (808 nm, 0.54 W cm⁻², 10 min). MTT incubated with KO₂ (0.5 mg mL⁻¹) served as a positive control. Afterwards, as obtained purple-colored precipitates were dissolved in 50% isopropanol (1:1) and the absorbance at 576 nm was recorded immediately using a monochromatic microplate spectrophotometer (Synergy 4).

Bacterial growth

Staphylococcus aureus (BCRC10781) and E. coli (BRBC 12438) were separately grown in Luria Bertani (LB) media, while MRSA (ATCC 43300) and GREC (BRCG 20703) were cultured individually in 1% penicillin and gentamicin containing LB broth, respectively. A single colony of each strain was plucked from solidified agar plates and inoculated in LB medium (1.0 mL). The cultures were then incubated at 37 °C under continuous shaking (200 r.p.m.), until the absorbance at 600 nm (OD₆₀₀) reached to 1.0 (optical path length: 1.0 cm). Each of the bacterial suspension was centrifuged (RCF 3000×g, 10 min, 25 °C) and washed thrice with PBS solution. Finally, 100 μL of the E. coli suspension [5.0 × 10³ colony-forming unit (CFU) mL⁻¹] was spread onto the solidified LB agar plates for the assessment of colony formation assay.

In vitro antibacterial assays

The standard broth microdilution method determined the MIC₉₀ (minimal inhibitory concentrations required to kill > 90% of total bacteria population) values against four different bacterial strains. Bacterial suspensions (1.0 × 10⁴ CFU mL⁻¹) were incubated separately with CuCl₂, Ti₃C₂T_x, or Cu₂O/Ti₃C₂T_x nanosheets in PBS solution (pH 7.4) at 37 °C under continuous shaking (250 r.p.m.) for 1 h and further incubated for 10 min at ambient temperature without and with NIR irradiation (808 nm, 0.54 Wcm⁻², 10 min). Then, each of the diluted bacterial mixtures (100 μL) was spread onto the solidified LB agar plates, and CFUs were counted manually after 24 h incubation at 37 °C.

Treatment of infected wounds using Cu₂O/Ti₃C₂T_x nanosheets

The in vivo eradication of MRSA by Cu₂O/Ti₃C₂T_x nanosheets was demonstrated using BKS Cg–Dock7^m +/+ Leprdb/J (db/db) male mice (5–6 weeks old, weighing 35–45 g). All animal experiments were conducted in accordance with the institutional guidelines of Care and Use of Laboratory Animals of National Taiwan University and granted by the Institutional Animal Care and Use Committee of the National Laboratory Animal Center, Taipei, Taiwan (IACUC Approval No. IACUC2012-037). The mice were anesthetized using a mixture of xylazine (117 mg kg^–1) and Zoletil (5 mg kg⁻¹). After shaving the dorsal skin of mice, the skin was disinfected using 70% ethyl alcohol (v/v) before aseptic surgery. An incision created circular wounds of ~ 10 mm in diameter on the skin of each mouse with a sterile stainless-surgical scissors. Microbial infection was induced by incubating the MRSA suspensions (1 × 10⁸ CFU mL⁻¹; 50 µL) onto the wound site for 6 h. 14 days post-surgery, the wound sites were swabbed using a sterile cotton swab and cultured on LB agar plates for 24 h at 37 °C to confirm the MRSA infection. Then, Cu₂O/MXene nanosheets were topically administered onto the wound site under NIR laser irradiation (808 nm, 0.54 W cm⁻², 5 min; every other day). To evaluate the in vivo antimicrobial activity of as-prepared Cu₂O/MXene nanosheets, tissue fluid (~ 10 µL) was swabbed from infectious wound site untreated and treated with Cu₂O/Ti₃C₂T_x nanosheets without or with NIR laser irradiation on day 0, 2, 4, 6, 8, 10, 12, 14, 16, and 18 and separately grown on the LB agar plates to monitor the bacteria growth through colony formation assay. Photographs of the wound area were captured using a digital camera to observe the real-time progress of the infected wounds. Tissue sections containing the entire wound including surrounding healthy skin (dermis and subcutaneous tissue) were surgically removed on postoperative day 14 for histological evaluation. Collagen formation and skin histology of wounded tissue were studied by Masson’s trichrome and Hematoxylin and eosin (H&E) staining, respectively.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This study was supported by the Ministry of Science and Technology, Taiwan, under the contracts 110-2113-M-002-005-MY3 and 110-2622-M-002-001. Thanks to Ms. Chia-Ying Chien of Ministry of Science and Technology (National Taiwan University) for the assistance in TEM and EDS experiments. The authors gratefully acknowledge Mr. Jui-Chin Lee for the use of electron spectroscopy for chemical analysis (PHI-5000) provided by the Instrument Center of National Cheng Kung University.

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Ya-Ju Hsu and Amit Nain contributed equally to this work

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Department of Chemistry, National Taiwan University, Taipei, 10617, Taiwan
Ya-Ju Hsu, Amit Nain, Yu-Feng Lin, Yu-Ting Tseng, Yu-Jia Li, Arumugam Sangili, Hui-Ling Yu & Huan-Tsung Chang
School of Basic Sciences, Indian Institute of Technology, Kamand campus, Mandi, Himachal Pradesh, 175005, India
Pavitra Srivastava
Institute of Analytical and Environmental Sciences, National Tsing Hua University, Hsinchu, 30013, Taiwan
Yu-Fen Huang
Department of Bioscience and Biotechnology and Center of Excellence for the Oceans, National Taiwan Ocean University, Keelung, 202301, Taiwan
Chih-Ching Huang
School of Pharmacy, College of Pharmacy, Kaohsiung Medical University, Kaohsiung, 80708, Taiwan
Chih-Ching Huang

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Ya-Ju Hsu
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Amit Nain
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Yu-Feng Lin
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Yu-Ting Tseng
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Yu-Jia Li
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Hui-Ling Yu
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Yu-Fen Huang
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Contributions

C-CH, and H-TC supervised the execution of project from the beginning to the end and assisted in manuscript preparation. Y-JH carried out most experiments. AN interpreted the results, mechanism, and prepared the first draft of the manuscript. AS and Y-FL performed electrochemical experiments. H-LY prepared MXenes. Y-JL and Y-TT carried out in vivo experiments. All authors discussed the results and contributed to the manuscript. All authors read and approved the final manuscript.

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Correspondence to Chih-Ching Huang or Huan-Tsung Chang.

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Hsu, YJ., Nain, A., Lin, YF. et al. Self-redox reaction driven in situ formation of Cu₂O/Ti₃C₂T_x nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound. J Nanobiotechnol 20, 235 (2022). https://doi.org/10.1186/s12951-022-01428-3

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Received: 23 November 2021
Accepted: 20 April 2022
Published: 19 May 2022
DOI: https://doi.org/10.1186/s12951-022-01428-3

Self-redox reaction driven in situ formation of Cu2O/Ti3C2Tx nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound

Abstract

Background

Methods

Results

Conclusion

Graphical Abstract

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Background

Results

In situ formation of Cu2O on Ti3C2Tx MXene nanosheets

Generation of O2 •−/H2O2 by Cu2O/Ti3C2Tx heterostructures

Conclusions

Methods

Synthesis of MXene and Cu2O/Ti3C2Tx nanosheets

Photoresponsive properties of Cu2O/Ti3C2Tx nanosheets

Determination of superoxide free radical

Bacterial growth

In vitro antibacterial assays

Treatment of infected wounds using Cu2O/Ti3C2Tx nanosheets

Data availability

References

Acknowledgements

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Contributions

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Supplementary Information

Additional file 1.

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Self-redox reaction driven in situ formation of Cu₂O/Ti₃C₂T_x nanosheets boost the photocatalytic eradication of multi-drug resistant bacteria from infected wound

In situ formation of Cu₂O on Ti₃C₂T_x MXene nanosheets

Generation of O₂ ^•−/H₂O₂ by Cu₂O/Ti₃C₂T_x heterostructures

Synthesis of MXene and Cu₂O/Ti₃C₂T_x nanosheets

Photoresponsive properties of Cu₂O/Ti₃C₂T_x nanosheets

Treatment of infected wounds using Cu₂O/Ti₃C₂T_x nanosheets