Multiclawed SiO<sub>2</sub> Nano-Antibacterial Agent Based on Charge Inversed Ce6 Ionic Liquid Polymers for Combating Oral Biofilm Infection

Jiao, Ziyi; Teng, Yonggang; Zhan, Chunjing; Qiao, Youbei; Ma, Yuying; Wang, Chaoli; Wu, Hong

doi:https://doi.org/10.1155/2022/2468104

Journal of Nanomaterials

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Abstract Introduction Materials and Methods Results and Discussion Conclusions Data Availability Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2022 | Article ID 2468104 | https://doi.org/10.1155/2022/2468104

Multiclawed SiO₂ Nano-Antibacterial Agent Based on Charge Inversed Ce6 Ionic Liquid Polymers for Combating Oral Biofilm Infection

Ziyi Jiao,¹Yonggang Teng,²Chunjing Zhan,¹Youbei Qiao,¹Yuying Ma,³Chaoli Wang,¹and Hong Wu¹

Academic Editor: Iaroslav Gnilitskyi

Received10 Aug 2021

Accepted20 Nov 2021

Published12 Jan 2022

Abstract

Photodynamic antimicrobial chemotherapy (PACT) is a promising therapy against biofilm infection. However, due to the saliva clearance and obstacle of biofilm, the photosensitizer is difficult to concentrate in the infection site; then, the PACT is less effective on oral biofilm infection. In this article, we report a special nano-antibacterial agent (SiO₂-P_Ce6-IL) to solve the bottleneck problem of PACT in treatment of oral biofilm infections. The SiO₂-P_Ce6-IL was composed of SiO₂ and poly ionic liquid photosensitizer (P_Ce6-IL) and had tri-fold features of eliminate biofilm infection: high binding ability, breaking biofilm barriers, and enrichment photosensitizer in infection site. In oral biofilm, the SiO₂-P_Ce6-IL changed to SiO₂-P_IL⁺ like claws of octopus that could hold tightly with biofilm. Then, the poly-dodecyl on the SiO₂-P_IL⁺ broke down the barrier of biofilm. The results of HR-MS and zeta potential indicated that SiO₂-P_Ce6-IL could change to positive (SiO₂-P_IL⁺) in acidic environment. The interaction forces and morphology results proved that the SiO₂-P_IL⁺ had a higher affinity to biofilm and could destroy the biofilm structure. Then, the photosensitizer was enriched in biofilm at sites of infection. The in vitro and in vivo experiments showed that SiO₂-P_Ce6-IL could effectively eradicate oral biofilm infections and control of dental caries.

1. Introduction

Oral biofilm infection is most important pathogenic factor of dental caries [1, 2]. Thus, eliminating biofilm on the tooth surface is a primary strategy to prevent and treat dental caries [3]. However, with the protection, bacteria in the biofilm is difficult to eradicate by common strategy of mechanical cleaning combined antibiotics. In this background, it is urgently to develop new treatment against oral biofilm infection. One promising therapy is PACT [4]. Compared with traditional treatment, PACT could efficiently control of bacteria and bacterial biofilm infection. However, owing to rapid clearance by saliva and barrier of biofilm, the photosensitizers are not concentrated in the infection site, and the efficacy of PACT against oral biofilm infections is limited [5]. Faced with the dilemma, the concentration of photosensitizer in the site of oral biofilm is the key to improve the PACT efficiency.

An understanding of oral biofilms matrix could offer opportunities to exploit photosensitizer delivery systems [6]. Because oral biofilm develop when microbes accumulate and form structured communities encapsulated within an extracellular matrix such as exopolysaccharides (EPS) [7, 8], the sugars are fermented by bacteria within the EPS matrix, then created highly acidic microenvironments and negative charge. The pH values often reach pH~4.5 or even lower in oral biofilm and particularly after exposure to sucrose, starch, and other cariogenic food products [9]. So, photosensitizer delivery system that could response to lower pH microenvironments is an effective method to improve delivery efficiency. Furthermore, many researches on cationic polymers [10], especially on the charge-reversal polymers, indicated that positively charged polymers could combine with extracellular polymeric substances (EPS) [11] and increase concentration of photosensitizer in biofilm. However, due to the dense and thick structure of biofilm, the photosensitizers difficultly penetrated into biofilm; then, photochemical reaction initiated by photosensitizer occurs mainly in the outermost layers of biofilm. The PACT efficiency was not significantly improved.

To overcome these challenges, polyionic liquid that composed of polycation and anion is introduced in previous studies [12, 13]. Inspired by octopus claws, the polyionic liquid photosensitizer nanoparticle (SiO₂-P_Ce6-IL) like arms of octopus was prepared in this work. In acid microenvironment of oral biofilm, the SiO₂-P_Ce6-IL could change to nano-claws SiO₂-P_IL⁺ and firmly combine to negatively charged EPS to overcome the saliva cleaning. Then, the dodecyl on the SiO₂-P_IL⁺ could pierce through the biofilm and break down the barrier of biofilm. Finally, the photosensitizer was highly concentrated in oral biofilm, and the biofilm infection was eliminated. The high binding energy between positively charged SiO₂-P_Ce6-IL and oral biofilm, excellent breaking ability of polydodecyl, and effective enrichment of photosensitizer were the key factors to effectively eliminate oral biofilm. The mechanism of SiO₂-P_Ce6-IL against oral biofilm is showed in Figure 1.

2. Materials and Methods

2.1. Materials

Ce6 was purchased from Frontier Scientific. KOH, methanol, methanol, absolute ethanol, cyclohexane, ammonia solution, hexanol, trimethylamine, Triton x-100, and 1,3-diphenylisobenzofuran (DPBF) were purchased from Sinopharm Chemical Reagent Co., Ltd. Artificial saliva was purchased from Beijing Regan Biotechnology Co., Ltd. Tetraethyl orthosilicate (TEOS), 3-aminopropyl triethoxysilane (APTES), CuCl, 2-bromoisobutyryl bromide, and N,N,N,N,N-pentamethyldiethylenetriamine were purchased from Aladdin. Streptococcus mutans (S. mutans, ATCC 700610) was purchased from ATCC. Brain Heart Infusion Broth (BHIB) was purchased from Beijing Land Bridge Technology Co., Ltd. The live/dead Baclight bacterial viability kit (L7012) was purchased from Invitrogen. Hydroxyapatite tablets were purchased from National Biomedical Materials Engineering Technology Research Center (China). Alexa Fluor 647 was purchased from Thermo Fisher Scientific.

2.2. The Synthesis and Characterization of Multiclawed SiO₂-P_Ce6-IL

The preparation of SiO₂-Br was similar with previous research [14], except the 2.4 mL of triethylamine and 2-bromoisobutyryl bromide (1.2 mL) were added to prepare SiO₂-Br. The multiclawed SiO₂-P_Ce6-IL was prepared by ATRP. Briefly, 10 mg Ce6-IL and SiO₂-Br dispersed into a mixture solution of ethanol and distilled water (5 : 1, ) for stirring 10 min at 800 rpm. 200 μL of PMDETA and 30 mg of CuCl were quickly transferred into the flask for reaction 8 h at 35°C. The SiO₂-P_Ce6-IL was washed with ethanol, distilled water.

The morphology of SiO₂-P_Ce6-IL was examined by TEM and SEM. The change of SiO₂-P_Ce6-IL zeta potentials in pH 4.5 and 7.4 was measured by a Delsa Nano C particle analyzer (Beckman Coulter Ireland Inc.).

The UV absorption of 5.0 mg·mL^-1SiO₂-P_Ce6-IL was measured by UV-vis (MAPADA). The Ce6 loading efficiency () was calculated as formula:

was SiO₂-P_Ce6-IL loading efficiency; was the concentration of Ce6 (mg·mL^-1); was solution volume (mL); was the weight of SiO₂-P_Ce6-IL (mg).

The Ce6 released in acidic microenvironment of oral biofilm (pH 4.5) was quantified by UV-vis. Briefly, 10 mg multiclawed SiO₂-P_Ce6-IL was placed in pH 4.5 solution 10 min and separated by centrifugation. The concentration of Ce6 in supernatant was examined by UV-vis.

DPBF was used to measure the generation of ¹O₂ [15]. Briefly, 2.0 mL DMSO solution containing SiO₂-P_Ce6-IL (equalled 100 μM Ce6) and 100 μM DPBF was irradiated by 660 nm light with a power density of 0.5 W·cm^-2. The absorbance of DPBF at about 410 nm was taken to record at 1 and 2 min.

2.3. Binding Ability of SiO₂-P_Ce6-IL to Oral Biofilm

Hydroxyapatite tablets (6.0 mm in diameter, 1.5 mm in thickness) were washed twice with PBS and incubated with artificial saliva to obtain saliva-coated hydroxyapatite. The S. mutans biofilm was formed on hydroxyapatite surfaces in BHIB medium which contained S. mutans (10⁶) and 2% sucrose () for incubated 72 h at 37°C.

The binding capacity of SiO₂-P_Ce6-IL to the hydroxyapatite and S. mutans biofilm was measured by UV-vis. The 0.1 mM multiclawed SiO₂-P_Ce6-IL was incubated with hydroxyapatite and biofilm in pH 4.5 and 7.4 solutions for 10 min at 37°C, and then, the concentration of SiO₂-P_Ce6-IL was measured before and after adsorption to calculated binding capacity.

In order to examine the binding ability of SiO₂-P_Ce6-IL to oral biofilm, the interaction between SiO₂-P_Ce6-IL with S. mutans biofilm was measured by AFM. The procedure was as follows: the AFM tip (NP-O10, Bruker) contacted with epoxy. After waiting for 10 min, 1 μL SiO₂-P_Ce6-IL (0.1 mM) was put on the tip and heated to completely cure epoxy. Then, the AFM tip was put in ultrapure water and ultrasonicated for 30 s to get rid of unattached SiO₂-P_Ce6-IL. The SEM was used to check the AFM tip modified with SiO₂-P_Ce6-IL.

2.4. Photosensitizer Concentration in Biofilm

The S. mutans biofilm was stained with Alexa Fluor 647. Briefly, 1 μM Alexa Fluor 647 was added to the S. mutans biofilms for 6 h. 20 μL of SiO₂-P_Ce6-IL or Ce6 (120 μM) was added onto the S. mutans biofilm interaction for 30 min, and then, wash with PBS 3 times to remove unconjugated SiO₂-P_Ce6-IL or Ce6. The laser scanning confocal microscopy (LSCM, Leica TCS SP8 STED 3X Super-resolution Confocal Microscope, Germany) was used to examine the concentration of Ce6 in biofilm.

2.5. Antibiofilm Activity

The S. mutans biofilm was treated with PBS, SiO₂-P_Ce6-IL, and Ce6. The biofilm incubated with BacLight live/dead dye in the dark after illumination for 15 min to observe dead/live bacteria. The CLSM images were taken to analyze the live and dead bacteria.

2.6. In Vivo Efficacy

Animal experiments were performed on a well-established model of dental caries disease as described in previous literatures [16]. Briefly, rats with two weeks old were purchased from animal center of the Air Force Medical University and screened for infection with S. mutans. Any rats infected with S. mutans prior to inoculation were removed. The animals were infected orally using an actively growing culture of S. mutans by oral swabbing three times a day for 2 weeks. Infected animals were randomly placed into three treatment groups of , and their teeth treated topically once daily. The treatment groups included (1) PBS, (2) SiO₂-P_Ce6-IL (amount to 0.1 mM Ce6) using a 660 nm LED light (0.5 W/cm²) for 15 min, and (3) free Ce6 (0.1 mM Ce6) using a 660 nm LED light (0.5 W/cm²) for 15 min. Each group was provided the National Institutes of Health cariogenic diet 2000 and 5% sucrose water ad libitum. The experiment proceeded for 2 weeks; all animals were weighed weekly. At the end of the experimental period, animals were sacrificed, and the teeth were observed by SEM. Finally, the heart, liver, spleen, lung, and kidney were harvested for histological sections (H&E staining analysis on a Leica SP8 microscope).

2.7. Cell Viability Assays

The cell viability of SiO₂-P_Ce6-IL was evaluated by CCK-8 assays. L929 fibroblast cells were used as model cells and seeded into 96-well plates (6000 cells per well) with 180 μL of DMEM culturing medium in each well for 24 h. SiO₂-P_Ce6-IL solution with concentrations from 0.2974, 0.5587, and 1.1173 mM was added to the cells and irradiated by LED light (0.5 W/cm²) for 15 min. After being incubated for 48 h, 200 μL of MTT solution (0.5 μg/mL) was added to each well and cultured for another 2 h. 200 μL DMSO was added and shook for 10 min to dissolve the crystal. Then, the absorbance was recorded at 490 nm by a microplate reader (model 550, BioRad).

2.8. Hemolysis Assay

The red blood cells washed with PBS until the supernatant was pellucid and was diluted to 2 vol% by PBS. The Ce6 and SiO₂-P_Ce6-IL (0.1 mM) were immersed into 2 vol% red blood cell solutions (5 mL for each tube) and incubated at 37°C for 3 h, respectively. Then, the samples were centrifuged at 1500 rpm for 10 min, and the OD values were recorded at 545 nm. The red blood cells treated with water as the positive control, while the red blood cells treated with PBS as negative control. The hemolysis rate was determined by the equation (2):

Besides hemolysis rate, the major organs including the hearts, livers, spleens, lungs, and kidneys were collected and stained with H&E for further evaluation of biocompatibility as previously reported [17].

3. Results and Discussion

3.1. Characterization of SiO₂-P_Ce6-IL

In order to strong interaction, the 8.92% Br of ATRP grafted on SiO₂ (Figure 2(d)). As showed in Figure 2(a), the size of SiO_2-P_Ce6-IL was about 70 nm, and the surface was more rough after initiated by CuCl. Element analysis displayed that N elements of P_Ce6-IL were on the SiO₂. The location of Si and N elements was further analyzed by the Spherical Aberration Corrected Transmission Electron Microscope (ACTEM) analysis software. The analysis results showed that the N element was on the surface of Si (Figure 2(b)). These results indicated that the P_Ce6-IL was successful grafted on the surface of SiO₂.

(a)

(b)

(c)

(d)

Because ¹O₂ was a major factor in photodynamic therapy [18], the ¹O₂ production of SiO₂-P_Ce6-IL was examined by DPBF. For the reaction of DPBF with ¹O₂ decreased the absorption of DPBF at 410 nm, the consumption rate of DPBF corresponds to the ¹O₂ production. Compared to the reduced absorbance of DPBF treated by Ce6 (from 3.15 to 1.75), ¹⁴ the absorbance of DPBF treated by SiO₂-P_Ce6-IL reduced from 2.69 to 0.24, and the consumption of DPBF was 2.45 (Figure 2(c)). The SiO₂-P_Ce6-IL had higher ¹O₂. More ¹O₂ production indicated that SiO₂-P_Ce6-IL had strong oxidation capacity and high PACT efficacy.

3.2. Binding Ability of SiO₂-P_Ce6-IL with Oral Biofilm

The Streptococcus mutans (S. mutans) is one of the primary pathogenic bacteria that cause caries. In this work, S. mutans biofilm as model was used to study antibacterial ability of SiO₂-P_Ce6-IL. To mimic the bacterial biofilm on the teeth, bacteria were grown for 72 h on hydroxyapatite disks. Due to acid microenvironment of S. mutans biofilm, the Ce6 was protonated and released; then, SiO₂-P_Ce6-IL changed to positive charged SiO₂-P_IL⁺. The biofilm had anions such as carboxyl, phosphoryl, and glycerate at the proteins or polysaccharides would produce negatively charge [19]. The electrostatic interactions would occur between SiO₂-P_IL⁺ and S. mutans biofilm. In order to detect interaction strength, the AFM was used to detect the interaction between SiO₂-P_IL⁺ and S. mutans biofilm. As showed in Figure 3(a), the SiO₂-P_Ce6-IL has been successfully modified on the AFM probe. The interaction between SiO₂-P_Ce6-IL with S. mutans biofilm was 954.02 nN which contributed by imidazolium cation and dodecyl in the SiO₂-P_IL⁺. However, the interaction of Ce6 with S. mutans biofilm was only 23.35 nN, and this weak force was difficult to resist saliva cleaning. This strong interaction was also proved by SEM. As showed in Figure 4(c), the SiO₂-P_IL⁺ like multiclawed octopus and could firmly adsorb on the S. mutans biofilm (EPS). Along with massive positive charges of SiO₂-P_IL⁺, the surface potential of S. mutans biofilm changed from -117 to 35 mV, and the adhesion of S. mutans biofilm was decreased from -76 nN to -25 nN. However, the adhesion of S. mutans biofilm treated by Ce6 alone was -45 nN. Due to the strong adhesion, the oral biofilm infection was difficult to eradicate. So, the decreased adhesion of SiO₂-P_Ce6-IL will be beneficial to eliminating biofilm infection.

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)

Figure 4

(a) (A) S. mutans biofilm; (B) S. mutans biofilm treated with Ce6; (C) S. mutans biofilm treated with SiO₂-P_Ce6-IL; (b) live (green) and dead (red) results; (A) control group; (B) treated with Ce6; (C) treated with SiO₂-P_Ce6-IL; (c) (A–C) the morphology of S. mutans biofilm; (D, E) the morphology of S. mutans biofilm treated with Ce6; (F, G) the morphology of S. mutans biofilm treated with SiO₂-P_Ce6-IL; (H) the morphology of S. mutans biofilm combined with SiO₂-P_Ce6-IL; (I) the pores in the EPS.

3.3. Antibacterial Activity In Vitro

As a result of strong interaction, the SiO₂-P_IL⁺ combined with biofilm firmly and the problem of saliva cleaning was solved. But the barrier of biofilm also severely restricted the PACT efficacy against oral biofilm. As showed in Figure 4(a), the blue was S. mutans biofilm, and the red Ce6 was difficult to enter the biofilm (Figure 4(a)). Limited by lifetime and diffusion distance of ¹O₂ [20], the Ce6 was difficult to damage protected bacteria outside biofilm. As showed in Figure 4(b), green represented live bacteria, and red represented dead bacteria. Most bacteria were alive after treated by Ce6 alone. So it is very important to destroy the dense structure of biofilm to improve the Ce6 concentration in biofilm. Compared to Ce6, SiO₂-P_Ce6-IL had hydrophobic dodecyl chain which like suckers on the arm of octopus and could destroy the structure of biofilm. In order to examine the membrane breaking effect of SiO₂-P_Ce6-IL, the morphology of S. mutans biofilm was characterized by SEM. As showed in Figure 4(c), the pores were created in the S. mutans biofilm. Once the biofilm was broken, the Ce6 was highly concentrated in biofilm (Figure 4(a)). After illumination for 15 min, most of S. mutans in the biofilm were killed by SiO₂-P_Ce6-IL (Figure 4(c)). The SiO₂-P_Ce6-IL greatly improved the PACT efficacy and could effectively eliminate of S. mutans biofilm.

3.4. In Vivo Antibiofilm Assessment

The in vitro results revealed that multiclawed SiO₂-P_Ce6-IL had excellent efficacy against S. mutans biofilms. To further verify these conclusions, the in vivo experiments were designed. The infected mice were divided into three groups: treated with PBS, Ce6 with illumination for 15 min, and SiO₂-P_Ce6-IL with illumination for 15 min. The therapeutic effects of SiO₂-P_Ce6-IL were evaluated by SEM. As showed in Figure 5, the treatment with SiO₂-P_Ce6-IL was very effective in preventing the development of dental caries and completely blocked extensive enamel damage. In contrast, treatment with Ce6 alone was no significant effect and resulted in enamel loss and damage, then led to dental caries.

3.5. Biocompatibility Evaluation

Although SiO₂-P_Ce6-IL could effective combine with oral biofilm and almost impossible to transport into the stomach from the mouth, it was important to evaluate their biocompatibility. So the cytotoxicity, hemolysis rate, and the histological section of main organs including the heart, liver, spleen and lung, and kidney were examined. The results show that no abnormal effects or damages were observed in these organs (Figure 6), and the body weights of rats treated with SiO₂-P_Ce6-IL were similarly to healthy rats. The hemolysis rate and cytotoxicity were 4.2% (limit of clinical hemolysis ) [21] and above 90% within therapeutic concentration (Figure 6). The SiO₂-P_Ce6-IL was a potential safe material for clinical applications in oral biofilm infection.

4. Conclusions

In this work, the SiO₂-P_Ce6-IL with charge reversal and high binding ability was prepared. The potential measurements showed that SiO₂-P_Ce6-IL could turn into positive and combine with EPS firmly in the acidic microenvironment of oral biofilm. The morphology of S. mutans biofilm results showed that SiO₂-P_Ce6-IL could combine with EFS and destroy the structure of biofilm. The laser scanning confocal microscopy results found that the concentration of Ce6 in S. mutans biofilm was greatly improved, and most of bacteria in biofilm were killed. In vivo experiments showed that the SiO₂-P_Ce6-IL was a highly desirable property for oral biofilm infection and had high quality in the prevention of dental caries. Most importantly, SiO₂-P_Ce6-IL had good biocompatibility in therapeutic effective concentrations.

Data Availability

The experimental data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

Authors’ Contributions

Ziyi Jiao and Yonggang Teng contributed equally to this work.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Nos. 31771087 and 32171388), the Innovation Capability Support Plan of Shaanxi Province (No. 2020TD-041), and the Shaanxi Natural Science (Nos. 2021JM-238 and 2021JQ-334).

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Copyright © 2022 Ziyi Jiao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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