Versatile graphitic nanozymes for magneto actuated cascade reaction-enhanced treatment of S. mutans biofilms
)
Download citation
1107
Views
139
Downloads
9
Crossref
9
WoS
9
Scopus
0
CSCD
Pathogenic oral biofilms especially acid-producing ones cause a variety of oral diseases such as dental caries. Given that bacteria are embedded within the biofilms matrix to prevent the penetration of therapeutic drugs, people have explored the applications of nanoparticles to treat oral diseases. However, current nanoparticle-mediated eradication has not achieved the precise treatment of biofilms, and the stabilities of nanoparticles go on strike because of acidic environment leading to poor therapeutic effectiveness. Herein, we design an integrated nanozyme, CoPt@graphene@glucose oxidase (CoPt@G@GOx), which has cascade reaction activity with two-step process. Hydrogen peroxide (H2O2) produced through the glucose oxidation by GOx serves as the substrate for peroxidase-mimic CoPt@G to produce highly toxic hydroxyl radical under acidic environment. Compared to the simple mixture of GOx and CoPt@G, CoPt@G@GOx shows around fourfold catalytic effect enhancement. Meanwhile, CoPt@G@GOx can precisely target the location of the biofilms, which ensures the minimal impact on normal soft-tissues. Relying on the advantage of the magneto-actuated cascade catalytic activity, CoPt@G@GOx reveals a superior antibacterial ability in the Streptococcus mutans biofilms model. Thus, our results provide an easy and effective method to exploit bifunctional nanozyme as a novel topical agent to prevent the prevalent biofilm-induced oral disease.
menu
Versatile graphitic nanozymes for magneto actuated cascade reaction-enhanced treatment of S. mutans biofilms
)
Abstract
Pathogenic oral biofilms especially acid-producing ones cause a variety of oral diseases such as dental caries. Given that bacteria are embedded within the biofilms matrix to prevent the penetration of therapeutic drugs, people have explored the applications of nanoparticles to treat oral diseases. However, current nanoparticle-mediated eradication has not achieved the precise treatment of biofilms, and the stabilities of nanoparticles go on strike because of acidic environment leading to poor therapeutic effectiveness. Herein, we design an integrated nanozyme, CoPt@graphene@glucose oxidase (CoPt@G@GOx), which has cascade reaction activity with two-step process. Hydrogen peroxide (H2O2) produced through the glucose oxidation by GOx serves as the substrate for peroxidase-mimic CoPt@G to produce highly toxic hydroxyl radical under acidic environment. Compared to the simple mixture of GOx and CoPt@G, CoPt@G@GOx shows around fourfold catalytic effect enhancement. Meanwhile, CoPt@G@GOx can precisely target the location of the biofilms, which ensures the minimal impact on normal soft-tissues. Relying on the advantage of the magneto-actuated cascade catalytic activity, CoPt@G@GOx reveals a superior antibacterial ability in the Streptococcus mutans biofilms model. Thus, our results provide an easy and effective method to exploit bifunctional nanozyme as a novel topical agent to prevent the prevalent biofilm-induced oral disease.
References(70)
Wade, W. G. The oral microbiome in health and disease. Pharmacol. Res. 2013, 69, 137–143.
Sampaio-Maia, B.; Caldas, I. M.; Pereira, M. L.; Pérez-Mongiovi, D.; Araujo, R. The oral microbiome in health and its implication in oral and systemic diseases. Adv. Appl. Microbiol. 2016, 97, 171–210.
Zhang, Y. H.; Wang, X.; Li, H. X.; Ni, C.; Du, Z. B.; Yan, F. H. Human oral microbiota and its modulation for oral health. Biomed. Pharmacother. 2018, 99, 883–893.
Leishman, S. J.; Do, H. L.; Ford, P. J. Cardiovascular disease and the role of oral bacteria. J. Oral Microbiol. 2010, 2, 5781.
Krishnan, K.; Chen, T.; Paster, B. J. A practical guide to the oral microbiome and its relation to health and disease. Oral Dis. 2017, 23, 276–286.
Koliarakis, I.; Messaritakis, I.; Nikolouzakis, T. K.; Hamilos, G.; Souglakos, J.; Tsiaoussis, J. Oral bacteria and intestinal dysbiosis in colorectal cancer. Int. J. Mol. Sci. 2019, 20, 4146.
Matsushita, K.; Yamada-Furukawa, M.; Kurosawa, M.; Shikama, Y. Periodontal disease and periodontal disease-related bacteria involved in the pathogenesis of Alzheimer’s disease. J. Inflamm. Res. 2020, 13, 275–283.
Read, E.; Curtis, M. A.; Neves, J. F. The role of oral bacteria in inflammatory bowel disease. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 731–742.
Selwitz, R. H.; Ismail, A. I.; Pitts, N. B. Dental caries. Lancet 2007, 369, 51–59.
Marthaler, T. M. Changes in dental caries 1953–2003. Caries. Res. 2004, 38, 173–181.
Featherstone, J. D. B. Dental caries: A dynamic disease process. Aust. Dent. J. 2008, 53, 286–291.
Pitts, N. B.; Zero, D. T.; Marsh, P. D.; Ekstrand, K.; Weintraub, J. A.; Ramos-Gomez, F.; Tagami, J.; Twetman, S.; Tsakos, G.; Ismail, A. Dental caries. Nat. Rev. Dis. Primers 2017, 3, 17030.
Silva, M. J.; Kilpatrick, N. M.; Craig, J. M.; Manton, D. J.; Leong, P.; Ho, H.; Saffery, R.; Burgner, D. P.; Scurrah, K. J. A twin study of body mass index and dental caries in childhood. Sci. Rep. 2020, 10, 568.
Listl, S.; Galloway, J.; Mossey, P. A.; Marcenes, W. Global economic impact of dental diseases. J. Dent. Res. 2015, 94, 1355–1361.
Chen, L.; Wen, Y. M. The role of bacterial biofilm in persistent infections and control strategies. Int. J. Oral Sci. 2011, 3, 66–73.
Simón-Soro, A.; Mira, A. Solving the etiology of dental caries. Trends Microbiol. 2015, 23, 76–82.
Scharnow, A. M.; Solinski, A. E.; Wuest, W. M. Targeting S. mutans biofilms: A perspective on preventing dental caries. Med. Chem. Commun. 2019, 10, 1057–1067.
Hamada, S.; Torii, M.; Kotani, S.; Tsuchitani, Y. Adherence of Streptococcus sanguis clinical isolates to smooth surfaces and interactions of the isolates with Streptococcus mutans glucosyltransferase. Infect. Immun. 1981, 32, 364–372.
Schilling, K. M.; Bowen, W. H. Glucans synthesized in situ in experimental salivary pellicle function as specific binding sites for Streptococcus mutans. Infect. Immun. 1992, 60, 284–295.
Stauder, M.; Papetti, A.; Daglia, M.; Vezzulli, L.; Gazzani, G.; Varaldo, P. E.; Pruzzo, C. Inhibitory activity by barley coffee components towards Streptococcus mutans biofilm. Curr. Microbiol. 2010, 61, 417–421.
Song, J.; Choi, B.; Jin, E. J.; Yoon, Y.; Choi, K. H. Curcumin suppresses Streptococcus mutans adherence to human tooth surfaces and extracellular matrix proteins. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 1347–1352.
Wang, S. P.; Zhang, K. K.; Zhou, X. D.; Xu, N.; Xu, H. H. K.; Weir, M. D.; Ge, Y.; Wang, S. D.; Li, M. Y.; Xu, X. et al. Antibacterial effect of dental adhesive containing dimethylaminododecyl methacrylate on the development of Streptococcus mutans biofilm. Int. J. Mol. Sci. 2014, 15, 12791–12806.
Yu, X. L.; He, J. W.; Li, S.; Liu, F.; Yang, J. M.; Deng, F. L. Preparation of experimental resin composites with an anti-adhesion effect against S. mutans using branched silicone methacrylate. J. Mech. Behav. Biomed. Mater. 2020, 101, 103414.
Hu, P.; Lv, B. B.; Yang, K. X.; Lu, Z. M.; Ma, J. Z. Discovery of myricetin as an inhibitor against Streptococcus mutans and an anti-adhesion approach to biofilm formation. Int. J. Med. Microbiol. 2021, 311, 151512.
Mohite, B. V.; Koli, S. H.; Narkhede, C. P.; Patil, S. N.; Patil, S. V. Prospective of microbial exopolysaccharide for heavy metal exclusion. Appl. Biochem. Biotechnol. 2017, 183, 582–600.
Toska, J.; Ho, B. T.; Mekalanos, J. J. Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system. Proc. Natl. Acad. Sci. USA 2018, 115, 7997–8002.
Flemming, H. C.; Wingender, J. The biofilm matrix. Nat. Rev. Microbiol. 2010, 8, 623–633.
Flemming, H. C.; Wingender, J.; Szewzyk, U.; Steinberg, P.; Rice, S. A.; Kjelleberg, S. Biofilms: An emergent form of bacterial life. Nat. Rev. Microbiol. 2016, 14, 563–575.
Wang, H.; Wan, K. W.; Shi, X. H. Recent advances in nanozyme research. Adv. Mater. 2019, 31, 1805368.
Liang, M. M; Yan, X. Y. Nanozymes: From new concepts, mechanisms, and standards to applications. Acc. Chem. Res. 2019, 52, 2190–2200.
Jiang, D. W.; Ni, D. L.; Rosenkrans, Z. T.; Huang, P.; Yan, X. Y.; Cai, W. B. Nanozyme: New horizons for responsive biomedical applications. Chem. Soc. Rev. 2019, 48, 3683–3704.
Zhang, Y. N.; Jin, Y. L.; Cui, H. X.; Yan, X. Y.; Fan, K. L. Nanozyme-based catalytic theranostics. RSC Adv. 2020, 10, 10–20.
Gao, L. Z.; Zhuang, J.; Nie, L.; Zhang, J. B.; Zhang, Y.; Gu, N.; Wang, T. H.; Feng, J.; Yang, D. L.; Perrett, S. et al. Intrinsic peroxidase-like activity of ferromagnetic nanoparticles. Nat. Nanotechnol. 2007, 2, 577–583.
Wang, X. Y.; Qin, L.; Zhou, M.; Lou, Z. P.; Wei, H. Nanozyme sensor arrays for detecting versatile analytes from small molecules to proteins and cells. Anal. Chem. 2018, 90, 11696–11702.
Weerathunge, P.; Ramanathan, R.; Torok, V. A.; Hodgson, K.; Xu, Y.; Goodacre, R.; Behera, B. K.; Bansal, V. Ultrasensitive colorimetric detection of murine norovirus using nanozyme aptasensor. Anal. Chem. 2019, 91, 3270–3276.
Mahmudunnabi, R. G.; Farhana, F. Z.; Kashaninejad, N.; Firoz, S. H.; Shim, Y. B.; Shiddiky, M. J. A. Nanozyme-based electrochemical biosensors for disease biomarker detection. Analyst 2020, 145, 4398–4420.
Zhu, Y. Y.; Wu, J. J. X.; Han, L. J.; Wang, X. Y.; Li, W.; Guo, H. C.; Wei, H. Nanozyme sensor arrays based on heteroatom-doped graphene for detecting pesticides. Anal. Chem. 2020, 92, 7444–7452.
Cheng, X. Q.; Zheng, Z. P.; Zhou, X. R.; Kuang, Q. Metal–organic framework as a compartmentalized integrated nanozyme reactor to enable high-performance cascade reactions for glucose detection. ACS Sustainable Chem. Eng. 2020, 8, 17783–17790.
Dong, Q.; Li, Z. Q.; Peng, T. H.; Chen, Z.; Tan, W. H. Progress on aptamer for cancer theranostics. Chem. J. Chin. Univ. 2020, 41, 2648–2657.
Gao, S. S.; Lin, H.; Zhang, H. X.; Yao, H. L.; Chen, Y.; Shi, J. J. Nanocatalytic tumor therapy by biomimetic dual inorganic nanozyme-catalyzed cascade reaction. Adv. Sci. 2019, 6, 1801733.
Zhang, P.; Sun, D. R.; Cho, A.; Weon, S.; Lee, S.; Lee, J.; Han, J. W.; Kim, D. P.; Choi, W. Modified carbon nitride nanozyme as bifunctional glucose oxidase-peroxidase for metal-free bioinspired cascade photocatalysis. Nat. Commun. 2019, 10, 940.
Zhang, Y.; Wang, Y. Y.; Zhou, Q.; Chen, X. Y.; Jiao, W. B.; Li, G. L.; Peng, M. L.; Liu, X. L.; He, Y.; Fan, H. M. Precise regulation of enzyme-nanozyme cascade reaction kinetics by magnetic actuation toward efficient tumor therapy. ACS Appl. Mater. Interfaces 2021, 13, 52395–52405.
Chang, K. W.; Liu, Z. H.; Fang, X. F.; Chen, H. B.; Men, X. J.; Yuan, Y.; Sun, K.; Zhang, X. J.; Yuan, Z.; Wu, C. F. Enhanced phototherapy by nanoparticle-enzyme via generation and photolysis of hydrogen peroxide. Nano Lett. 2017, 17, 4323–4329.
Wang, Z. Z.; Zhang, Y.; Ju, E. G.; Liu, Z.; Cao, F. F.; Chen, Z. W.; Ren, J. S.; Qu, X. G. Biomimetic nanoflowers by self-assembly of nanozymes to induce intracellular oxidative damage against hypoxic tumors. Nat. Commun. 2018, 9, 3334.
Zhu, Z. T.; Li, S. K.; Song, M. H.; Cai, X. Q.; Song, Z. L.; Chen, L.; Chen, Z. Recent progress of versatile metal graphitic nanocapsules in biomedical applications. Chem. J. Chin. Universities 2021, 42, 2701–2716.
Liu, Y.; Naha, P. C.; Hwang, G.; Kim, D.; Huang, Y.; Simon-Soro, A.; Jung, H. I.; Ren, Z.; Li, Y.; Gubara, S. et al. Topical ferumoxytol nanoparticles disrupt biofilms and prevent tooth decay in vivo via intrinsic catalytic activity. Nat. Commun. 2018, 9, 2920.
Sun, D.; Pang, X.; Cheng, Y.; Ming, J.; Xiang, S. J.; Zhang, C.; Lv, P.; Chu, C. C.; Chen, X. L.; Liu, G. et al. Ultrasound-switchable nanozyme augments sonodynamic therapy against multidrug-resistant bacterial infection. ACS Nano 2020, 14, 2063–2076.
Li, Y. T.; Wang, L.; Liu, H.; Pan, Y.; Li, C. N.; Xie, Z. G.; Jing, X. B. Ionic covalent-organic framework nanozyme as effective cascade catalyst against bacterial wound infection. Small 2021, 17, 2100756.
Wang, L. W.; Gao, F.; Wang, A. Z.; Chen, X. Y.; Li, H.; Zhang, X.; Zheng, H.; Ji, R.; Li, B.; Yu, X. et al. Defect-rich adhesive molybdenum disulfide/rGO vertical heterostructures with enhanced nanozyme activity for smart bacterial killing application. Adv. Mater. 2020, 32, 2005423.
Sang, Y. J.; Li, W.; Liu, H.; Zhang, L.; Wang, H.; Liu, Z. W.; Ren, J. S.; Qu, X. G. Construction of nanozyme-hydrogel for enhanced capture and elimination of bacteria. Adv. Funct. Mater. 2019, 29, 1900518.
Zhang, L.; Liu, Z. W.; Deng, Q. Q.; Sang, Y. J.; Dong, K.; Ren, J. S.; Qu, X. G. Nature-inspired construction of MOF@COF nanozyme with active sites in tailored microenvironment and pseudopodia-like surface for enhanced bacterial inhibition. Angew. Chem., Int. Ed. 2021, 60, 3469–3474.
Wu, J. J. X.; Wang, X. Y.; Wang, Q.; Lou, Z. P.; Li, S. R.; Zhu, Y. Y.; Qin, L.; Wei, H. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes (II). Chem. Soc. Rev. 2019, 48, 1004–1076.
Wei, H.; Gao, L. Z.; Fan, K. L.; Liu, J. W.; He, J. Y.; Qu, X. G.; Dong, S. J.; Wang, E. K.; Yan, X. Y. Nanozymes: A clear definition with fuzzy edges. Nano Today 2021, 40, 101269.
Zhang, R. F.; Yan, X. Y.; Fan, K. L. Nanozymes inspired by natural enzymes. Acc. Mater. Res. 2021, 2, 534–547.
Hu, Y. H.; Gao, X. J.; Zhu, Y. Y.; Muhammad, F.; Tan, S. H.; Cao, W.; Lin, S. C.; Jin, Z.; Gao, X. F.; Wei, H. Nitrogen-doped carbon nanomaterials as highly active and specific peroxidase mimics. Chem. Mater. 2018, 30, 6431–6439.
Tang, G. H.; He, J. Y.; Liu, J. W.; Yan, X. Y.; Fan, K. L. Nanozyme for tumor therapy: Surface modification matters. Exploration 2021, 1, 75–89.
Li, S. S.; Shang, L.; Xu, B. L.; Wang, S. H.; Gu, K.; Wu, Q. Y.; Sun, Y.; Zhang, Q. H.; Yang, H. L.; Zhang, F. R. et al. A nanozyme with photo-enhanced dual enzyme-like activities for deep pancreatic cancer therapy. Angew. Chem., Int. Ed. 2019, 131, 12754–12761.
Liu, X.; Wan, Y. L.; Jiang, T.; Zhang, Y. F.; Huang, P.; Tang, L. H. Plasmon-activated nanozymes with enhanced catalytic activity by near-infrared light irradiation. Chem. Commun. 2020, 56, 1784–1787.
Wei, H.; Wang, E. K. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes. Chem. Soc. Rev. 2013, 42, 6060–6093.
Ivanova, M. N.; Grayfer, E. D.; Plotnikova, E. E.; Kibis, L. S.; Darabdhara, G.; Boruah, P. K.; Das, M. R.; Fedorov, V. E. Pt-decorated boron nitride nanosheets as artificial nanozyme for detection of dopamine. ACS Appl. Mater. Interfaces 2019, 11, 22102–22112.
Zhang, L. F.; Zhang, L.; Deng, H.; Li, H.; Tang, W. T.; Guan, L. Y.; Qiu, Y.; Donovan, M. J.; Chen, Z.; Tan, W. H. In vivo activation of pH-responsive oxidase-like graphitic nanozymes for selective killing of Helicobacter pylori. Nat. Commun. 2021, 12, 2002.
Zhang, L.; Dong, Q.; Zhang, H.; Xu, J. Q.; Wang, S.; Zhang, L. F.; Tang, W. T.; Li, Z. Q.; Xia, X.; Cai, X. Q. et al. A magnetocatalytic propelled cobalt-platinum@graphene navigator for enhanced tumor penetration and theranostics. CCS Chem. 2021, 3, 2382–2395.
Xiao, J.; Klein, M. I.; Falsetta, M. L.; Lu, B. W.; Delahunty, C. M.; Yates III, J. R.; Heydorn, A.; Koo, H. The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. PLoS Pathog. 2012, 8, e1002623.
Polshin, E.; Verbruggen, B.; Witters, D.; Sels, B.; De Vos, D.; Nicolaï, B.; Lammertyn, J. Integration of microfluidics and FT-IR microscopy for label-free study of enzyme kinetics. Sensor Actuat. B:Chem. 2014, 196, 175–182.
Kim, B. C.; Jeong, E.; Kim, E.; Hong, S. W. Bio-organic–inorganic hybrid photocatalyst, TiO2 and glucose oxidase composite for enhancing antibacterial performance in aqueous environments. Appl. Catal. B:Environ. 2019, 242, 194–201.
Xiong, R.; Zhang, W. T.; Zhang, Y. F.; Zhang, Y.; Chen, Y. M.; He, Y.; Fan, H. M. Remote and real time control of an FVIO-enzyme hybrid nanocatalyst using magnetic stimulation. Nanoscale 2019, 11, 18081–18089.
Huang, Y. Y.; Ren, J. S.; Qu, X. G. Nanozymes: Classification, catalytic mechanisms, activity regulation, and applications. Chem. Rev. 2019, 119, 4357–4412.
Li, Y. Y.; Zhu, W. X.; Li, J. S.; Chu, H. T. Research progress in nanozyme-based composite materials for fighting against bacteria and biofilms. Colloids Surf. B:Biointerf. 2021, 198, 111465.
Ali, A.; Ovais, M.; Zhou, H. G.; Rui, Y. K.; Chen, C. Y. Tailoring metal–organic frameworks-based nanozymes for bacterial theranostics. Biomaterials 2021, 275, 120951.
Publication history
Copyright
Acknowledgements
This work was financially supported by the National Key Research and Development Program of China (No. 2020YFA0210800), the Science and Technology Innovation Program of Hunan Province (No. 2020RC4017), and the Science and Technology Development Fund, Macau (No. 196/2017/A3).
FEEDBACK 
TOP