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Polydopamine-encapsulated FeO with an adsorbed HSP70 inhibitor for improved photothermal inactivation of bacteria Dongdong Liu, Liyi Ma, Lidong Liu, Lu Wang, Yuxin Liu, Qi Jia, Quanwei Guo, Ge Zhang, and Jing Zhou ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.6b08119 • Publication Date (Web): 01 Sep 2016 Downloaded from http://pubs.acs.org on September 2, 2016

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ACS Applied Materials & Interfaces

Polydopamine-encapsulated Fe3O4 with an adsorbed HSP70 inhibitor for improved photothermal inactivation of bacteria Dongdong Liu †‡, Liyi Ma †, Lidong Liu †, Lu Wang †, Yuxin Liu †, Qi Jia †, Quanwei †

†

†

Guo , Ge Zhang , Jing Zhou * † Department of Chemistry, Capital Normal University, Beijing 100048, People’s Republic of China ‡ College of Resource Environment and Tourism, Capital Normal University, Beijing 100048, People’s Republic of China E-mail: [email protected]

Keywords: photothermal, polydopamine, HSP70 inhibitor, bacteria, magnetic nanoparticles

Abstract Photothermal treatment, a new approach for inactivation of bacteria and pathogens that does not depend on traditional therapeutic approaches, has recently received much attention. In this study, a new type of nanoplatform (PDA@Fe3O4+PES) was fabricated by using polydopamine (PDA, a photothermal conversion agent) to encapsulate Fe3O4 (a magnetic nanoparticle) and support 2-phenylethynesulfonamide (PES, an inhibitor of heat shock protein 70 (HSP70)). Upon near-infrared light irradiation, the increased temperature weakens π-π and hydrogen bonding

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interactions and PES is released from the PDA@Fe3O4+PES. The released PES inhibits the function of HSP70, reducing bacterial tolerance to photothermal therapy and improving the therapeutic effect against infectious bacterial pathogens. After treatment, PDA@Fe3O4+PES can be recovered using the magnetic property of the Fe3O4 cores. Consequently, PDA@Fe3O4+PES

possesses

the

potential

to

be

a

recyclable

photothermal agent for enhanced photothermal bacterial inactivation without causing secondary pollution.

1. INTRODUCTION Pathogens,

including

Staphylococcus

aureus

(S.

aureus)

and

Escherichia coli (E. coli), are well known as food contaminants that cause bacterial infectious diseases.1 Preventing outbreaks of pathogens are very important for their biological diversity and high infectivity.2 As the most effective therapeutic approach, antibiotics, such as penicillin, have a long-period and wide application in infections treatment. However, frequent and excessive use of conventional antibiotics has caused extensive multidrug resistance in pathogens and bacteria.3 The difficulty of developing completely new antibiotics has led to new approaches such as photothermal treatment4-9, received much attention in the field of infectious pathogens and bacteria inactivation.10-16 Upregulation of heat shock proteins (HSPs) has been proved to enable


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cells to acquire tolerance to particular stress.17 Heat shock protein 70 (HSP70), as a member of HSP family and an ATP-dependent molecular chaperone, can be encoded by an evolutionarily conserved gene family that is widely found in organisms from bacteria to mammals. It plays a supporting role in polypeptides (or proteins) folding and refolding, proteins complex formation or aggregation, and protein transporting promotion. Also, as an important apoptotic regulator of signaling pathways, HSP70 can be induced by stress and accumulate in cells to provide protection from severe living conditions, such as overheat. The 2-phenylethynesulfonamide (PES), a stable HSP70 inhibitor, has low cytotoxicity to living system and can selectively interact with HSP70, which can interfere the normal function of HSP70 in different kinds of cell signaling pathways.18-20 Our recent work has shown that PES can be released from nanogel under near-infrared (NIR) irradiation, which can further improve the therapeutic effect in tumor-bearing mice model, and hence improve the photothermal therapy depth.21 The presence of the free PES is expected to reduce bacterial cells’ tolerance to heat, resulting in improved photothermal inactivation of the bacteria. Magnetic nanoparticles generate an induced magnetic dipole allowing selective control of location and motion with a magnetic field applied externally.22-23 Recently, magnetic nanoparticle-based nanoplatforms have been intensively developed for magnetic resonance imaging (MRI)24,



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magnetically guided drug delivery25-27, hyperthermia treatment28-30, and selective

separation

or

targeting31-34.

Moreover,

magnetic

nanoparticle-based antibacterial materials can be recovered and reused35, avoiding secondary pollution. In this work, a novel nanoplatform (PDA@Fe3O4+PES) was fabricated by loading PES onto the surface of polydopamine-coated Fe3O4 nanoparticles. Upon near infrared irradiation, PES is released from the PDA@Fe3O4+PES, enabling inhibition of HSP70 and reduction of bacterial tolerance to heat. The ablation effect on bacteria, recovery properties and toxicity of the nanoplatform were evaluated. 2. EXPERIMENTAL SECTION 2.1. Preparation of PDA@Fe3O4+PES nanoplatform 2.1.1. Preparation of Fe3O4 nanoparticles (Fe3O4) The Fe3O4 nanoparticles (Fe3O4) were prepared via a polyol progress as previously reported.24 In a typical procedure, sodium acetate trihydrate (2.0 g), trisodium citrate (0.5 g), and FeCl3•6H2O (1.1 g) were added into ethylene glycol (33 mL) with stirring until the solution is clear. Then, a sealed Teflon-lined autoclave was used for the hydrothermal treatment of the obtained solution at 200 °C for 10 h. After that, the system in the sealed autoclave was allowed to naturally cool down to room temperature (R. T.). The brownish-black precipitates were collected after been washed with ethanol and deionized water to obtain Fe3O4.


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2.1.2. Preparation of PDA-encapsulated Fe3O4 nanocomposites (PDA@Fe3O4) According to a typical procedure, the obtained Fe3O4 (7 mg) were scattered in 40 mL 10 mM Tris-HCl buffer solution (pH = 8.5) by sonication, and 32 mg FeCl3•6H2O and 40 mg dopamine hydrochloride were then dissolved into the above suspension under generous stirring. After stirring at R. T. for another 4 h, polydopamine (PDA)-encapsulated Fe3O4 nanocomposites (PDA@Fe3O4) were prepared successfully. The obtained products were centrifugated and washed to remove the unreacted reagents. 2.1.3. Preparation of PES-loaded PDA@Fe3O4 nanocomposites (PDA@Fe3O4+PES) To study the adsorption properties of PES onto the PDA@Fe3O4, PES loading experiments were performed at R. T.. Typically, PES solution (1.25 mL, 1.2 mg mL−1) and PDA@Fe3O4 (2.5 mL, 1.0 mg mL−1) were mixed in PBS buffer (pH = 7.4) under stirring and gently stirred for another 12 h at R. T.. The PES-loaded PDA@Fe3O4 (PDA@Fe3O4+PES) was collected by centrifugation (12000 rpm, 3 min) from the dispersion. With the help of the ninhydrin method, the amount of loaded PES was calculated. By means of the given computing method, the entrapment efficiency

and

loading

Encapsulation efficiency =

content

were

accounted.

weight of PES in PDA @ Fe3O 4 + PES initial weight of PES


(1)


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Loading content =

weight of PES in PDA @ Fe3O 4 + PES weight of PDA @ Fe3O 4 + PES

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(2)

2.2. PES release studies To determine the property of PES releasing, PDA@Fe3O4+PES solution (1.5 mL, 0.53 mg mL−1) was treated with water bath to simulate the condition of NIR irradiation. After been treated with different kinds of hydrothermal pretreatment (37 °C, 40 °C, 50 °C, and 60 °C for 1 h), the supernatant were then collected by centrifugation at 12800 rpm for 4 min, respectively. Taking advantage of the amino group in PES, the PES release amount was verified by the ninhydrin method.

2.3. Photothermal inactivation of bacteria Bacteria (S. aureus and E. coli) were transferred to PBS buffer (pH = 7.4), PDA@Fe3O4 (100 µL, 500 µg mL−1) and PDA@Fe3O4+PES (100 µL, 500 µg mL−1) solution were cultured at 37 °C for 24 h under gentle rotation, respectively. Sterile water was used to dilute the bacteria until 105 cfu mL−1. The acquired solution was exposed to the irradiation of 785 nm laser for 300 s (0.5 W cm−2). After that, spread plate method was used to place the solution to solid medium. After being cultured for 24 h, the bacteria colonies number was calculated. Blank group and material only group (PDA@Fe3O4+PES) were set as control.

2.4. Separation efficiency measurement The concentrations of PDA@Fe3O4+PES remained in supernatant solutions

were

calculated

by

ultraviolet-visible-near-infrared


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(UV-vis-NIR) absorption spectra. Then PDA@Fe3O4+PES removal efficiency (R) was determined according to the following equations36.

R = V (C 0 − Ce ) / m

(3)

where C0 and Ce represent the concentrations of PDA@Fe3O4+PES in aqueous solution before and after the separation, separately; m represents the mass of PDA@Fe3O4+PES and V represents the aqueous solution volume.

2.5. Recycling property study Bacteria (S. aureus and E. coli) were transferred to PDA@Fe3O4+PES solution (100 µL, 500 µg mL−1) and cultured at 37 °C with middle speed of rotation, respectively. After 24 h, the bacterial suspension was diluted with PBS buffer (pH = 7.4) until 105 cfu mL−1. Photothermal inactivation experiments were then carried out by exposing the obtained mixture to the irradiation of 785 nm laser for 300 s (0.5 W cm−2). After inactivation, PDA@Fe3O4 solution was attracted to the wall of the tube by a magnetic field and the supernatant was removed. The separated PDA@Fe3O4 was cleaned by pure water for several times and retested in the following antibacterial application. The photothermal inactivation effect on bacteria of each circle was evaluated by spread plate method and counting the bacteria colonies number after photothermal inactivation.

3. RESULTS AND DISCUSSION



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Scheme 1. Scheme of the preparation of PDA@Fe3O4+PES (a) for enhancing photothermal inactivation effect on bacteria and could be recovered for recycle usage (b).

3.1. Preparation and characterization Uniform Fe3O4 cores were prepared using a modified polyol method24 and showed good dispersibility in water as a result of citrate capping groups on the nanoparticle surface. As the transmission electron


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microscopy (TEM) image reveals, the Fe3O4 cores exhibited a nearly spherical shape when dropped on the copper grid. Narrow particle size distribution can be observed to be ~140 nm (Figure 1a). Polydopamine (PDA)-encapsulated

Fe3O4

nanocomposites

(PDA@Fe3O4)

were

synthesized by dispersion of Fe3O4 in dopamine hydrochloride solution (pH = 8.5) with gentle stirring at R. T. for 4 h (Scheme 1). A TEM image showed that PDA@Fe3O4 was successfully systhesised with a 5-10 nm of PDA shell. (Figures 1b, 1c). The hydrodynamic diameter of the PDA@Fe3O4 was measured to be ~230 nm (Figure 1d), which is obtained by dynamic light scattering (DLS) data. Compared with the Fourier transform infrared spectrum (FTIR) of Fe3O4, an absorption peak at 1290 cm−1 was present in Fe3O4@PDA and PDA spectra (Figure 2a). As the X-ray photoelectron spectroscopy (XPS) demonstrated, the obtained nanopaltform (PDA@Fe3O4) were composed by Fe, O, N and possibly H elements (Figure S1a). Likewise, on the observation of the thermogravimetric analysis (TGA) analysis, weight loss behavior of PDA@Fe3O4 demonstrated that PDA@Fe3O4 has been synthesized successfully (Figure S1b). These results demonstrated that the Fe3O4 cores were well coated with PDA. The zeta-potential of PDA@Fe3O4 in aqueous solution (pH = 7.0) was −30 mV (Figure 2b), indicating their high dispersibility in aqueous solution.



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Figure 1. TEM images of Fe3O4 (a) and PDA@Fe3O4 (b), scale bar: 50 nm. The size characterization (c) and the hydrodynamic diameter (d) of PDA@Fe3O4.


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Figure 2. (a) FTIR spectra of Fe3O4, PDA, and PDA@Fe3O4. (b) The zeta-potential of PDA@Fe3O4 solution (pH = 7.0). (c) UV-vis-NIR spectra of the Fe3O4 and PDA@Fe3O4 solution. (d) Temperature variation of different concentrations of PDA@Fe3O4 solution vs irradiation time.

3.2. Measurement of photothermal properties Polydopamine (PDA) coatings can be easily formed on many different kinds of substrates, giving excellent biocompatibility, and causing no immune response.37-38 Moreover, for its ability of converting NIR to heat energy, PDA has the prospect to be a photothermal agent for therapeutic use.21, 39-40 With its layer of PDA, PDA@Fe3O4 is expected to kill bacteria by absorption of NIR light and producing cytotoxic heat within minutes. Hence, the absorption and photothermal properties of PDA@Fe3O4 were ACS Paragon Plus Environment


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studied. The UV-vis-NIR spectrum of PDA@Fe3O4 solution exhibited broad absorbance in the 500–900 nm region (Figure 2c), showing higher NIR absorbance compared with Fe3O4. A PDA@Fe3O4 solution (0.25 mg mL−1) was also exposed to a 785 nm laser (0.5 W cm−2) to determine the photothermal properties of the nanoplatform. As shown in Figure 3a, the photothermal images changed as the time going on, and indicated that the temperature of the PDA@Fe3O4 solution came up to 47 °C from 25.7 °C within 800 s (Figure 3b). These results demonstrated that PDA@Fe3O4 has efficient photo-heat conversion ability under substantial irradiation of NIR. Upon the same NIR irradiation, the temperature rose higher as the concentration of PDA@Fe3O4 increased (Figure 2d). Therefore, the temperature of the PDA@Fe3O4 solution will continuously increase as the concentration of the solution increased. In addition, the photothermal conversion efficiency of the PDA@Fe3O4 was ~57% (Figures 3b, 3c). Further, under NIR irradiation for five on/off cycles, PDA@Fe3O4 demonstrated excellent photostability (Figure 4a). The absorption study of PDA@Fe3O4 also suggested an excellent photostability (Figure 4b). Above all, with excellent photothermal conversion efficiency and stability, PDA@Fe3O4 has the potential to be used in the domain of bioapplication as a coupling agent for photothermal ablation.


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Figure 3. (a) Photothermal images for the PDA@Fe3O4 solution (0.25 mg mL−1) with different irradiation time (785 nm, 0.5 W cm−2, 0-15 min). (b) Photothermal temperature change curve of the PDA@Fe3O4 solution (on-off period). (c) Cooling time vs –lnθ obtained from (b).



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Figure 4. (a) The on-off temperature curve of the PDA@Fe3O4 solution (0.25 mg mL−1) under the irradiation of 785 nm laser (0.5 W cm−2). (b) The UV-vis-NIR spectra of PDA@Fe3O4 solution under different NIR irradiated conditions. (c) Magnetic hysteresis curves of PDA@Fe3O4 at 300 K. Inset: digital image of PDA@Fe3O4 solution alongside a magnet. (d) HCT116 cells viability with PDA@Fe3O4 (0, 0.2, 0.4, 0.6, 0.8, 1.0 mg mL−1) treatment for 12 and 24 h.

3.3. Measurement of magnetic properties As a consequence of the Fe3O4 cores, with a nearby magnetic field, the PDA@Fe3O4 solution became clear and the nanocomposites could be attracted to the bottle wall within 5 min (Figure 4c inset and Figure S2). Also, when the magnetic field was removed, the PDA@Fe3O4 could be ACS Paragon Plus Environment

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redispersed in water after gentle shaking. To explore the magnetic properties of PDA@Fe3O4, the magnetization curve was determined using a vibrating sample magnetometer (VSM). The magnetic hysteresis curve suggested the superparamagnetic behavior of PDA@Fe3O4, for displaying no evident remanence or coercivity at 300 K (Figure 4c). The saturation magnetization value of PDA@Fe3O4 was 56.2 emu g−1, which was strong enough to facilitate their recovery with the help of a magnet. What is worth mentioned is that the presence of the PDA shell did not strongly weaken the magnetic properties of Fe3O4 (Figure S3), since the coated PDA on the Fe3O4 cores was only 5-10 nm (Figures 1a, 1b). These results clearly demonstrated that PDA@Fe3O4 had excellent magnetic properties and prospect for practical use in selective separation.

3.4. Toxicity studies Biocompatibility is a serious concern for any nanoplatform which is designed to be used in the biological field. Methylthiazolyltetrazolium (MTT) assays on the human colon cancer cell line (HCT116) cells were implemented to determine the toxicity of PDA@Fe3O4. As shown in Figure 4d, it can be seen that the PDA@Fe3O4 caused no significant apoptosis of HCT116 cells which was cultured with different concentrations of the nanoparticles (0–1.0 mg mL–1) for 12 or 24 h. These findings suggest that thanks to the advantages of low toxicity and high biocompatibility, PDA@Fe3O4 nanoparticles showed a bright future for



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potential bioapplication.

3.5. HSP70 inhibitor loading and laser-controlled release The functional groups on PDA including catechol, amine and imine enhanced the special abilities of the PDA-functionalized nanoparticles for absorption and separation.41-42 The PDA-functionalized nanoparticles have already been exploited as reusable adsorbents of lanthanum (III) and copper ions, separation of organic mixed dyes, and adsorption of lysozyme.36,

43-47

The

small

molecule

HSP70

inhibitor,

2-phenylethynesulfonamide (PES), could break the normal function of HSP70 in different kinds of cell signaling pathways which would cause the cells less tolerant to external injuries, such as overheat. Here, PES was loaded onto the PDA@Fe3O4 via π-π stacking and/or hydrogen binding to form a nanoplatform which can be abbreviated as PDA@Fe3O4+PES (Scheme 1A). The adsorption and desorption capacities of PDA@Fe3O4+PES were further examined. Based on detection of amino group on PES using the ninhydrin method, the PES encapsulation efficiency came up to 97.27% by calculating, and the loading content was measured to be 36.85%. The PDA@Fe3O4+PES nanocomposite was dissolved in PBS buffer (pH = 7.4), 5% glucose solution, 0.9% NaCl solution, and serum solution. After been rest at room temperature for 14 days, the UV-vis-NIR spectra of the solution mentioned above were compared with that of the PDA@Fe3O4+PES


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nanocomposite dissolved in deionized water. The result demonstrated the stability of the nanocomposite after loading PES (Figure S4). Under the irradiation of NIR, the temperature of PDA@Fe3O4+PES solution increased and the loaded PES can be expected to release. By the ninhydrin method, the PES-releasing percentages were 15.89% at 37 °C, 16.83% at 40 °C, 18.03% at 50 °C, and 19.23% at 60 °C (Figure S5). The release of PES with 5-min laser irradiation was measured, and the results showed that the PES release amount was 13.3%. The experiments demonstrated a controlled PES release upon NIR irradiation and NIR irradiation can improve the release of PES as a result of the rise in temperature. According to a previous report, the released PES could then interact selectively with HSP70 and exert a cooperative effect with photothermal

therapy.18

Considering

the

photothermal

and

laser-controlled release features, the PDA-based nanoparticles could act as photothermal coupling and delivery carriers at the same time, with utility for inactivation of bacteria as described below.

3.6. Photothermal inactivation of bacteria The photothermal effect of the PDA@Fe3O4+PES was further explored by assessing its ablation efficiency on bacteria (Gram-negative (E. coli) and (Gram-positive (S. aureus)). In detail, bacteria were incubated with PBS buffer (pH = 7.4), PDA@Fe3O4, or PDA@Fe3O4+PES solution, and then irradiated with NIR for 5 min (0.5 W cm−2). A blank group and



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material only (PDA@Fe3O4+PES) group were used as controls. As a comparison, the effect of the PES alone and conventional heating on bacteria ablation was measured. As shown in Figure 5a and Figure S6, a large number of bacterial colonies could be observed in the blank, PDA@Fe3O4+PES and PBS+NIR groups, a few colonies could be seen in the PDA@Fe3O4+NIR group, whereas very few colonies were seen in the PDA@Fe3O4+PES+NIR group. In summary, the best photothermal therapeutic effect was observed with PDA@Fe3O4+PES+NIR against E. coli. Under consistent conditions, the ablation effect on S. aureus (Figure 5c and Figure S6) identified with those on E. coli. The introduction of PES enhanced the inactivation effect of PDA@Fe3O4 on bacteria. The Kruskal Wallis Test and SPSS 16.0 IBM software were introduced to evaluate the significant differences among these groups and analyzed the data. As for statistically significant, P-values < 0.05 were considered. As Figure 5b shown, there were no significant (P > 0.05) effects of PDA@Fe3O4+PES, PBS+NIR, or PDA@Fe3O4+NIR group on E. coli. Nevertheless, a confidence level of 99.9% (P < 0.001) confirmed the significant difference between the PDA@Fe3O4+PES+NIR group and the blank group, which was revealed by the Kruskal Wallis Test. Similar results were observed for S. aureus (Figures 5c, 5d). P value < 0.01 was obtained between the PDA@Fe3O4+NIR group and the blank group, and P value < 0.001 was obtained between the blank group and the


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PDA@Fe3O4+PES+NIR group. Given these findings, the released PES from PDA@Fe3O4+PES made bacteria less tolerant to photothermal inactivation. It could be assumed that the released PES from PDA@Fe3O4+PES could enhance the photothermal effect at relatively low temperature. In summary, the PDA@Fe3O4+PES could be used as a novel photothermal coupling agent with enhanced inactivation properties in antibacterial applications.

Figure 5. Photographs (a, c) and bacteria viability (b, d) of the colonies of E. coli (a, b) and S. aureus (c, d) under different incubated conditions. Note: *p < 0.05, **p < 0.01, ***p < 0.001.



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3.7. Separation efficiency after photothermal inactivation Following

photothermal

inactivation,

we

explored

whether

PDA@Fe3O4 could be separated from water for recycling, avoiding secondary pollution and reducing consumption of raw material. Comparative data before and after adsorption were determined after separation of PDA@Fe3O4+PES with a magnetic field at 25 °C for 30 min. The concentrations of PDA@Fe3O4+PES remaining in supernatant solutions were confirmed by UV-vis-NIR using the absorption at 425 nm of

PES

(Figure

S7).

After

removal,

the

concentration

of

PDA@Fe3O4+PES (originally 500 µg mL−1) decreased to 111 µg mL−1. Therefore, the PDA@Fe3O4+PES removal efficiency (R) was calculated to be 77.8% (Figure S8). While in the practical application, the magnet with stronger magnetic field intensity can be applied to enhance the collection and removal efficiency. Antibacterial activity of recycled PDA@Fe3O4+PES was further explored. As Figure 6 shown, bacterial mortality of S. aureus and E. coli after the photothermal inactivation with PDA@Fe3O4+PES was relatively high in all three cycles. The results demonstrated that the antibacterial efficiency of PDA@Fe3O4+PES can be guaranteed while avoiding secondary pollution. In our experiment of bacteria inactivation, the amount of the released PES was calculated to be 35.43 µg mL−1 in 60 °C. Part of the released PES will interact with bacteria to improve photothermal inactivation, so the amount of the


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released PES into water can be guaranteed lower than 35.43 µg mL−1. Moreover, with the advantages of not causing extensive multidrug resistance, excellent selectivity, the PES-loaded nanoplatform reported by us could be an effective and promising antibacterial agent to reduce water pollution caused by PES. It is very important for understanding how the retained PES after previous antibacterial treatment impact the reloading of free PES and the antibacterial potency of the reloaded nanoplatform, and more works to investigate the PES encapsulation efficiency in the recycled nanoplatform will be included in our subsequent work.

Figure

6.

Recyclable

antibacterial

study of

PDA@Fe3O4+PES

nanocomposite. (a) Schematic illustration of the recyclable antibacterial application of PDA@Fe3O4+PES. (b) Photo image of PDA@Fe3O4+PES ACS Paragon Plus Environment


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treated bacteria suspension (left) and the separation of PDA@Fe3O4+PES in the bacteria suspension with a magnetic field (right). Bacterial mortality of E. coli (c) and S. aureus (d) after the photothermal inactivation of continuous three-times-recycled PDA@Fe3O4+PES.

4. CONCLUSIONS In this study, PDA@Fe3O4 nanoparticles were successfully synthesized and loaded with a small molecule HSP70 inhibitor, PES, to form a novel nanoplatform for HSP70-inhibitory and photothermal

synergistic

antibacterial application. Irradiated with a NIR laser, PES can be released from PDA@Fe3O4+PES and specifically interfere the function of bacterial HSP70, which can result in improving inactivation effect by reducing the bacterial tolerance to thermal damage. With the advantages of low toxicity, and good recovery properties, this work come up with a novel strategy for enhancing the effect of NIR irradiation-immediated photothermal inactivation and has the prospect to be used in routine antibacterial applications and industrial manufacture without secondary pollution. ASSOCIATED CONTENT Supporting Information XPS spectrum, Fe3O4 aqueous solution images, magnetic hysteresis curves, UV-vis-NIR spectra, the standard curves, the amidoge concentrations of the released PES, bacteria viability. Acknowledgements


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We thank Dr. Jun Lu, an engineer from IOP-CAS, for his help on magnetic measurements. The authors thank the funding of National Natural Science Foundation of China (21301121), Scientific Research Base Development Program of the Beijing Municipal Commission of Education (KM201410028008), Beijing talent foundation outstanding young individual project (2015000026833ZK02)

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Polydopamine-Encapsulated Fe - ACS Publications - American

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