Antibacterial Properties of Visible-Light-Responsive Carbon-Containing Titanium Dioxide Photocatalytic Nanoparticles against Anthrax
<p>Scanning electron microscopy and ultraviolet-visible (UV-Vis) absorption spectrum analyses. Scanning electron microscopy (<b>A</b>,<b>B</b>), X-ray photoelectron spectroscopy (XPS) analysis for the 1s atomic orbital of carbon (<b>C</b>) and UV-Vis absorption spectra (<b>D</b>) of UV100 TiO<sub>2</sub> and C200 NPs used in this study. The C200 sample absorbed light extending into the visible (>380 nm) region.</p> "> Figure 2
<p>Dose-dependent and kinetic analyses of bactericidal activity of C200 NPs against <span class="html-italic">B. subtilis</span>. Dose-dependent (<b>A</b>) and kinetic (<b>B</b>) analyses of the bactericidal activity of UV100 TiO<sub>2</sub> and C200 NPs against <span class="html-italic">B. subtilis</span> after visible-light illumination. Illumination was carried out either at different light densities (at distances of 5 cm, 10 cm and 15 cm with respective illumination intensities of 3 × 10<sup>4</sup>, 1.2 × 10<sup>3</sup> and 3 × 10<sup>2</sup> lux) for 30 min (<b>A</b>) or at a light density of 3 × 10<sup>4</sup> lux (90 mW/cm<sup>2</sup>) for different periods (<b>B</b>). Under each illumination condition, the surviving bacteria in the UV100 TiO<sub>2</sub> groups were normalized to 100%. * <span class="html-italic">P</span> < 0.05 and ** <span class="html-italic">P</span> < 0.01 compared with the respective UV100 TiO<sub>2</sub> groups. <span class="html-italic">n</span> = 6, three experiments with two replicates.</p> "> Figure 3
<p>Antibacterial properties of C200 NPs against vegetative bacteria and spores of <span class="html-italic">Bacillus</span> species. Bacteria <span class="html-italic">B. subtilis</span>, <span class="html-italic">B. thuringiensis</span>, <span class="html-italic">B. cereus</span>, and <span class="html-italic">B. anthracis</span> were photocatalyzed using UV100 TiO<sub>2</sub> and C200 NPs, respectively. All vegetative bacteria (<b>A</b>) or spores (<b>B</b>) in the UV100 TiO<sub>2</sub> groups were normalized to 100%. The relative percentages of surviving pathogens in the C200 groups are shown. The illumination intensity was 3 × 10<sup>4</sup> lux (90 mW/cm<sup>2</sup>), and the reaction time was 30 min. * <span class="html-italic">P</span> < 0.05 and ** <span class="html-italic">P</span> < 0.01 compared with respective UV100 TiO<sub>2</sub> groups. <span class="html-italic">n</span> = 6, three experiments with two replicates.</p> "> Figure 4
<p>Visible-light-responsive C200 NP-mediated inactivation of lethal toxin (LT). Macrophage J774A.1 cells were treated with LT with or without UV100 TiO<sub>2</sub> and C200 photocatalysis for 3 h, and surviving cells of untreated groups were adjusted to 100%. Columns designated UV TiO<sub>2</sub> or C200 represent that LT was pretreated with photocatalysis by using UV100 TiO<sub>2</sub> or C200 NPs, respectively, before being treated with J774A.1 cells. ** <span class="html-italic">P</span> < 0.01, compared with all other groups treated with LT (with or without additional treatments). <span class="html-italic">n</span> = 6, three experiments with two replicates.</p> "> Figure 5
<p>Surviving <span class="html-italic">B. subtilis</span> after clearance by macrophages. <span class="html-italic">B. subtilis</span> was treated with J774A.1 macrophage cells (multiplicity of infection (MOI): 0.1 bacteria/cell). Levels of surviving bacteria (colony-forming unit; CFU) harvested from macrophage cell lysate are shown. Columns designated UV TiO<sub>2</sub> and C200 represent that anthrax spores were pretreated with photocatalysis by using UV100 TiO<sub>2</sub> and C200 NPs, respectively. * <span class="html-italic">P</span> < 0.05, compared with all other groups under the 8 h treatment condition. <span class="html-italic">n</span> = 6, three experiments with two replicates.</p> ">
Abstract
:1. Introduction
2. Results
2.1. Analyses of TiO2 NPs
2.2. Dose-Dependent and Kinetic Analyses of Photocatalytic Inactivation of B. Subtilis
2.3. Antibacterial and Antispore Activities of C200 against Bacillus Species
2.4. Photocatalytic Inactivation of Anthrax LT by C200 NPs
2.5. In Vitro Phagocytic Clearance Analysis
3. Discussion
4. Materials and Methods
4.1. Preparation of Photocatalysts
4.2. Bacterial Strains and Culture
4.3. Photocatalytic Reaction and Detection of Viable Bacteria
4.4. Cytotoxicity Analysis
4.5. Phagocytosis Analysis
4.6. Statistical Analyses
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
Abbreviations
TiO2 | titanium dioxide |
TiO2(C) | carbon-containing TiO2 |
VLRP | visible-light-responsive photocatalyst |
NPs | nanoparticles |
UV | ultraviolet |
ROS | reactive oxygen species |
H2O2 | hydrogen peroxide |
•OH | hydroxyl radicals |
O2− | superoxide anions |
LT | anthrax lethal toxin |
PA | anthrax protective antigen |
LF | anthrax lethal factor |
ET | anthrax edema toxin |
MOI | multiplicity of infection |
CFU | colony-forming units |
LPS | lipopolysaccharide |
References
- World Health Organization. Anthrax in humans and animals. In Anthrax in Humans and Animals, 4th ed.; World Health Organization: Geneva, Switzerland, 2008. [Google Scholar]
- Goel, A.K. Anthrax: A disease of biowarfare and public health importance. World J. Clin. Cases 2015, 3, 20–33. [Google Scholar] [CrossRef] [PubMed]
- Doganay, M.; Demiraslan, H. Human anthrax as a re-emerging disease. Recent Pat. Antiinfect. Drug Discov. 2015, 10, 10–29. [Google Scholar] [CrossRef] [PubMed]
- Frischknecht, F. The history of biological warfare. Human experimentation, modern nightmares and lone madmen in the twentieth century. EMBO Rep. 2003, 4, S47–S52. [Google Scholar] [CrossRef] [PubMed]
- Riedel, S. Biological warfare and bioterrorism: A historical review. Proceedings 2004, 17, 400–406. [Google Scholar]
- Inglesby, T.V.; O’Toole, T.; Henderson, D.A.; Bartlett, J.G.; Ascher, M.S.; Eitzen, E.; Friedlander, A.M.; Gerberding, J.; Hauer, J.; Hughes, J.; et al. Anthrax as a biological weapon, 2002: Updated recommendations for management. JAMA 2002, 287, 2236–2252. [Google Scholar] [CrossRef] [PubMed]
- Hamburg, M.A. Bioterrorism: Responding to an emerging threat. Trends Biotechnol. 2002, 20, 296–298. [Google Scholar] [CrossRef]
- Spotts Whitney, E.A.; Beatty, M.E.; Taylor, T.H., Jr.; Weyant, R.; Sobel, J.; Arduino, M.J.; Ashford, D.A. Inactivation of bacillus anthracis spores. Emerg. Infect. Dis. 2003, 9, 623–627. [Google Scholar] [CrossRef] [PubMed]
- Maness, P.C.; Smolinski, S.; Blake, D.M.; Huang, Z.; Wolfrum, E.J.; Jacoby, W.A. Bactericidal activity of photocatalytic TiO2 reaction: Toward an understanding of its killing mechanism. Appl. Environ. Microbiol. 1999, 65, 4094–4098. [Google Scholar] [PubMed]
- Fujishima, A.; Honda, K. Electrochemical photolysis of water at a semiconductor electrode. Nature 1972, 238, 37–38. [Google Scholar] [CrossRef] [PubMed]
- Hirakawa, K.; Mori, M.; Yoshida, M.; Oikawa, S.; Kawanishi, S. Photo-irradiated titanium dioxide catalyzes site specific DNA damage via generation of hydrogen peroxide. Free Radic. Res. 2004, 38, 439–447. [Google Scholar] [CrossRef] [PubMed]
- Hearing, V.J. Biogenesis of pigment granules: A sensitive way to regulate melanocyte function. J. Dermatol. Sci. 2005, 37, 3–14. [Google Scholar] [CrossRef] [PubMed]
- Slominski, A.; Pawelek, J. Animals under the sun: Effects of ultraviolet radiation on mammalian skin. Clin. Dermatol. 1998, 16, 503–515. [Google Scholar] [CrossRef]
- Roberts, J.E. Ocular phototoxicity. J. Photochem. Photobiol. B 2001, 64, 136–143. [Google Scholar] [CrossRef]
- Wu, M.S.; Sun, D.S.; Lin, Y.C.; Cheng, C.L.; Hung, S.C.; Chen, P.K.; Yang, J.H.; Chang, H.H. Nanodiamonds protect skin from ultraviolet b-induced damage in mice. J. Nanobiotech. 2015, 13, 35. [Google Scholar] [CrossRef] [PubMed]
- Chang, W.K.; Sun, D.S.; Chan, H.; Huang, P.T.; Wu, W.S.; Lin, C.H.; Tseng, Y.H.; Cheng, Y.H.; Tseng, C.C.; Chang, H.H. Visible light responsive core-shell structured In2O3@CaIn2O4 photocatalyst with superior bactericidal property and biocompatibility. Nanomedicine 2012, 8, 609–617. [Google Scholar] [CrossRef] [PubMed]
- Cheng, C.L.; Sun, D.S.; Chu, W.C.; Tseng, Y.H.; Ho, H.C.; Wang, J.B.; Chung, P.H.; Chen, J.H.; Tsai, P.J.; Lin, N.T.; et al. The effects of the bacterial interaction with visible-light responsive titania photocatalyst on the bactericidal performance. J. Biomed. Sci. 2009, 16, 7. [Google Scholar] [CrossRef] [PubMed]
- Liou, J.W.; Chang, H.H. Bactericidal effects and mechanisms of visible light-responsive titanium dioxide photocatalysts on pathogenic bacteria. Archi. Immunol. Ther. Ex. 2012, 60, 267–275. [Google Scholar] [CrossRef] [PubMed]
- Liou, J.W.; Gu, M.H.; Chen, Y.K.; Chen, W.Y.; Chen, Y.C.; Tseng, Y.H.; Hung, Y.J.; Chang, H.H. Visible light responsive photocatalyst induces progressive and apical-terminus preferential damages on Escherichia coli surfaces. PLoS ONE 2011, 6, e19982. [Google Scholar] [CrossRef] [PubMed]
- Tseng, Y.H.; Sun, D.S.; Wu, W.S.; Chan, H.; Syue, M.S.; Ho, H.C.; Chang, H.H. Antibacterial performance of nanoscaled visible-light responsive platinum-containing titania photocatalyst in vitro and in vivo. Biochim. Biophys. Acta 2013, 1830, 3787–3795. [Google Scholar] [CrossRef] [PubMed]
- Wong, M.S.; Chen, C.W.; Hsieh, C.C.; Hung, S.C.; Sun, D.S.; Chang, H.H. Antibacterial property of Ag nanoparticle-impregnated N-doped titania films under visible light. Sci. Rep. 2015, 5, 11978. [Google Scholar] [CrossRef] [PubMed]
- Wong, M.S.; Chu, W.C.; Sun, D.S.; Huang, H.S.; Chen, J.H.; Tsai, P.J.; Lin, N.T.; Yu, M.S.; Hsu, S.F.; Wang, S.L.; et al. Visible-light-induced bactericidal activity of a nitrogen-doped titanium photocatalyst against human pathogens. Appl. Environ. Microbiol. 2006, 72, 6111–6116. [Google Scholar] [CrossRef] [PubMed]
- Wong, M.S.; Sun, D.S.; Chang, H.H. Bactericidal performance of visible-light responsive titania photocatalyst with silver nanostructures. PLoS ONE 2010, 5, e10394. [Google Scholar] [CrossRef] [PubMed]
- Kau, J.H.; Sun, D.S.; Huang, H.H.; Wong, M.S.; Lin, H.C.; Chang, H.H. Role of visible light-activated photocatalyst on the reduction of anthrax spore-induced mortality in mice. PLoS ONE 2009, 4, e4167. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.L.; Chen, Y.S.; Chan, H.; Tseng, Y.H.; Yang, S.R.; Tsai, H.Y.; Liu, H.Y.; Sun, D.S.; Chang, H.H. The use of nanoscale visible light-responsive photocatalyst TiO2-Pt for the elimination of soil-borne pathogens. PLoS ONE 2012, 7, e31212. [Google Scholar]
- Tseng, Y.H.; Kuo, C.S.; Huang, C.H.; Li, Y.Y.; Chou, P.W.; Cheng, C.L.; Wong, M.S. Visible-light-responsive nano-TiO2 with mixed crystal lattice and its photocatalytic activity. Nanotechnology 2006, 17, 2490–2497. [Google Scholar] [CrossRef] [PubMed]
- Chou, P.W.; Treschev, S.; Chung, P.H.; Cheng, C.L.; Tseng, Y.H.; Chen, Y.J.; Wong, M.S. Observation of carbon-containing nanostructured mixed titania phases for visible-light photocatalysts. Appl. Phys. Lett. 2006, 89, 131919. [Google Scholar] [CrossRef]
- Treschev, S.; Chou, P.W.; Tseng, Y.H.; Wang, J.B.; Perevedentseva, E.V.; Cheng, C.L. Photoactivities of the visible-light-activated mixed-phase carbon-containing titanium dioxide: The effect of carbon incorporation. Appl. Catal. B 2007, 79, 8–16. [Google Scholar] [CrossRef]
- Friebe, S.; van der Goot, F.G.; Burgi, J. The ins and outs of anthrax toxin. Toxins 2016, 8, 69. [Google Scholar] [CrossRef] [PubMed]
- Kau, J.H.; Sun, D.S.; Huang, H.S.; Lien, T.S.; Huang, H.H.; Lin, H.C.; Chang, H.H. Sublethal doses of anthrax lethal toxin on the suppression of macrophage phagocytosis. PLoS ONE 2010, 5, e14289. [Google Scholar] [CrossRef] [PubMed]
- Sun, D.S.; Lee, P.C.; Kau, J.H.; Shih, Y.L.; Huang, H.H.; Li, C.R.; Lee, C.C.; Wu, Y.P.; Chen, K.C.; Chang, H.H. Acquired coagulant factor VIII deficiency induced by bacillus anthracis lethal toxin in mice. Virulence 2015, 6, 466–475. [Google Scholar] [CrossRef] [PubMed]
- Chen, P.K.; Chang, H.H.; Lin, G.L.; Wang, T.P.; Lai, Y.L.; Lin, T.K.; Hsieh, M.C.; Kau, J.H.; Huang, H.H.; Hsu, H.L.; et al. Suppressive effects of anthrax lethal toxin on megakaryopoiesis. PLoS ONE 2013, 8, e59512. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Chiang, Y.W.; Lin, T.K.; Lin, G.L.; Lin, Y.Y.; Kau, J.H.; Huang, H.H.; Hsu, H.L.; Wang, J.H.; Sun, D.S. Erythrocytic mobilization enhanced by the granulocyte colony-stimulating factor is associated with reduced anthrax-lethal-toxin-induced mortality in mice. PLoS ONE 2014, 9, e111149. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Wang, T.P.; Chen, P.K.; Lin, Y.Y.; Liao, C.H.; Lin, T.K.; Chiang, Y.W.; Lin, W.B.; Chiang, C.Y.; Kau, J.H.; et al. Erythropoiesis suppression is associated with anthrax lethal toxin-mediated pathogenic progression. PLoS ONE 2013, 8, e71718. [Google Scholar] [CrossRef] [PubMed]
- Kau, J.H.; Shih, Y.L.; Lien, T.S.; Lee, C.C.; Huang, H.H.; Lin, H.C.; Sun, D.S.; Chang, H.H. Activated protein c ameliorates bacillus anthracis lethal toxin-induced lethal pathogenesis in rats. J. Biomed. Sci. 2012, 19, 98. [Google Scholar] [CrossRef] [PubMed]
- Gamage, J.; Zhang, Z. Applications of photocatalytic disinfection. Intl. J. Photoenergy 2010, 2010, 764870. [Google Scholar] [CrossRef]
- Fujishima, A. Titanium dioxide photocatalysis. J. Photochem. Photobiol. C 2000, 1, 1–21. [Google Scholar]
- Ibrahim, R.K.; Hayyan, M.; AlSaadi, M.A.; Hayyan, A.; Ibrahim, S. Environmental application of nanotechnology: Air, soil, and water. Environ. Sci. Pollut. Res. Int. 2016, 23, 13754–13788. [Google Scholar] [CrossRef] [PubMed]
- Application of Nanotechnology: Enviroment. Available online: http://www.nanocap.eu/Flex/Site/Download2e90.pdf?ID=2258 (accessed on 8 December 2016).
- Bernard, B.K.; Osheroff, M.R.; Hofmann, A.; Mennear, J.H. Toxicology and carcinogenesis studies of dietary titanium dioxide-coated mica in male and female fischer 344 rats. J. Toxicol. Environ. Health 1990, 29, 417–429. [Google Scholar] [CrossRef] [PubMed]
- Valant, J.; Drobne, D.; Novak, S. Effect of ingested titanium dioxide nanoparticles on the digestive gland cell membrane of terrestrial isopods. Chemosphere 2012, 87, 19–25. [Google Scholar] [CrossRef] [PubMed]
- Shi, H.; Magaye, R.; Castranova, V.; Zhao, J. Titanium dioxide nanoparticles: A review of current toxicological data. Part. Fibre Toxicol. 2013, 10, 15. [Google Scholar] [CrossRef] [PubMed]
- Sloan, M.; Farnsworth, S. Testing and Eevaluation of Nanoparticle Efficacy on E. Coli, and Bacillus Anthracis Spores. NSTI-Nanotech 2006, 1, 595–598. [Google Scholar]
- Lin, Y.C.; Tsai, L.W.; Perevedentseva, E.; Chang, H.H.; Lin, C.H.; Sun, D.S.; Lugovtsov, A.E.; Priezzhev, A.; Mona, J.; Cheng, C.L. The influence of nanodiamond on the oxygenation states and micro rheological properties of human red blood cells in vitro. J. Biomed. Opt. 2012, 17, 101512. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Tsai, M.F.; Chung, C.P.; Chen, P.K.; Hu, H.I.; Kau, J.H.; Huang, H.H.; Lin, H.C.; Sun, D.S. Single-step purification of recombinant anthrax lethal factor from periplasm of Escherichia coli. J. Biotechnol. 2006, 277–285. [Google Scholar] [CrossRef] [PubMed]
- Kau, J.H.; Lin, C.G.; Huang, H.H.; Hsu, H.L.; Chen, K.C.; Wu, Y.P.; Lin, H.C. Calyculin a sensitive protein phosphatase is required for bacillus anthracis lethal toxin induced cytotoxicity. Curr. Microbiol. 2002, 44, 106–111. [Google Scholar] [CrossRef] [PubMed]
- Kau, J.H.; Sun, D.S.; Tsai, W.J.; Shyu, H.F.; Huang, H.H.; Lin, H.C.; Chang, H.H. Antiplatelet activities of anthrax lethal toxin are associated with suppressed p42/44 and p38 mitogen-activated protein kinase pathways in the platelets. J. Infect. Dis. 2005, 192, 1465–1474. [Google Scholar] [CrossRef] [PubMed]
- Kort, R.; O’Brien, A.C.; van Stokkum, I.H.; Oomes, S.J.; Crielaard, W.; Hellingwerf, K.J.; Brul, S. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Appl. Environ. Microbiol. 2005, 71, 3556–3564. [Google Scholar] [CrossRef] [PubMed]
- Carrera, M.; Zandomeni, R.O.; Fitzgibbon, J.; Sagripanti, J.L. Difference between the spore sizes of bacillus anthracis and other bacillus species. J. Appl. Microbiol. 2007, 102, 303–312. [Google Scholar] [CrossRef] [PubMed]
- Sagripanti, J.L.; Bonifacino, A. Comparative sporicidal effects of liquid chemical agents. Appl. Environ. Microbiol. 1996, 62, 545–551. [Google Scholar] [PubMed]
- Chang, H.H.; Chen, P.K.; Lin, G.L.; Wang, C.J.; Liao, C.H.; Hsiao, Y.C.; Dong, J.H.; Sun, D.S. Cell adhesion as a novel approach to determining the cellular binding motif on the severe acute respiratory syndrome coronavirus spike protein. J. Virol. Methods 2014, 201, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Chang, J.C.; Chang, H.H.; Lin, C.T.; Lo, S.J. The integrin α6β1 modulation of PI3K and Cdc42 activities induces dynamic filopodium formation in human platelets. J. Biomed. Sci. 2005, 12, 881–898. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Shyu, H.F.; Wang, Y.M.; Sun, D.S.; Shyu, R.H.; Tang, S.S.; Huang, Y.S. Facilitation of cell adhesion by immobilized dengue viral nonstructural protein 1 (NS1): Arginine-glycine-aspartic acid structural mimicry within the dengue viral NS1 antigen. J. Infect. Dis. 2002, 186, 743–751. [Google Scholar] [CrossRef] [PubMed]
- Sun, D.S.; Chang, Y.C.; Lien, T.S.; King, C.C.; Shih, Y.L.; Huang, H.S.; Wang, T.Y.; Li, C.R.; Lee, C.C.; Hsu, P.N.; et al. Endothelial cell sensitization by death receptor fractions of an anti-dengue nonstructural protein 1 antibody induced plasma leakage, coagulopathy, and mortality in mice. J. Immunol. 2015, 195, 2743–2753. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Shih, K.N.; Lo, S.J. Receptor-mediated endocytosis as a selection force to enrich bacteria expressing rhodostomin on their surface. J. Biomed. Sci. 2000, 7, 42–50. [Google Scholar] [CrossRef] [PubMed]
- Leahy, M.B.; Dessens, J.T.; Nuttall, P.A. Striking conformational similarities between the transcription promoters of thogoto and influenza a viruses: Evidence for intrastrand base pairing in the 5′ promoter arm. J. Virol. 1997, 71, 8352–8356. [Google Scholar] [PubMed]
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Sun, D.-S.; Kau, J.-H.; Huang, H.-H.; Tseng, Y.-H.; Wu, W.-S.; Chang, H.-H. Antibacterial Properties of Visible-Light-Responsive Carbon-Containing Titanium Dioxide Photocatalytic Nanoparticles against Anthrax. Nanomaterials 2016, 6, 237. https://doi.org/10.3390/nano6120237
Sun D-S, Kau J-H, Huang H-H, Tseng Y-H, Wu W-S, Chang H-H. Antibacterial Properties of Visible-Light-Responsive Carbon-Containing Titanium Dioxide Photocatalytic Nanoparticles against Anthrax. Nanomaterials. 2016; 6(12):237. https://doi.org/10.3390/nano6120237
Chicago/Turabian StyleSun, Der-Shan, Jyh-Hwa Kau, Hsin-Hsien Huang, Yao-Hsuan Tseng, Wen-Shiang Wu, and Hsin-Hou Chang. 2016. "Antibacterial Properties of Visible-Light-Responsive Carbon-Containing Titanium Dioxide Photocatalytic Nanoparticles against Anthrax" Nanomaterials 6, no. 12: 237. https://doi.org/10.3390/nano6120237