Cationic and Anionic Antimicrobial Agents Co-Templated Mesostructured Silica Nanocomposites with a Spiky Nanotopology and Enhanced Biofilm Inhibition Performance
Corresponding Author: Chengzhong Yu
Nano-Micro Letters,
Vol. 14 (2022), Article Number: 83
Abstract
Silica-based materials are usually used as delivery systems for antibacterial applications. In rare cases, bactericidal cationic surfactant templated silica composites have been reported as antimicrobial agents. However, their antibacterial efficacy is limited due to limited control in content and structure. Herein, we report a “dual active templating” strategy in the design of nanostructured silica composites with intrinsic antibacterial performance. This strategy uses cationic and anionic structural directing agents as dual templates, both with active antibacterial property. The cationic-anionic dual active templating strategy further contributes to antibacterial nanocomposites with a spiky surface. With controllable release of dual active antibacterial agents, the spiky nanocomposite displays enhanced anti-microbial and anti-biofilm properties toward Staphylococcus epidermidis. These findings pave a new avenue toward the designed synthesis of novel antibacterial nanocomposites with improved performance for diverse antibacterial applications.
Highlights:
1 A ‘dual active templating’ strategy is firstly reported, using cationic and anionic bactericidal agents as co-templates for the preparation of antibacterial silica nanocomposite with spiky nanotopography.
2 The spiky nanocomposite exhibited enhanced antibacterial and biofilm inhibition performance, compared to pure antimicrobial cationic agent templated smooth silica nanocomposite.
Keywords
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- T. Yanagisawa, T. Shimizu, K. Kuroda, C. Kato, The preparation of alkyltrimethylammonium–kanemite complexes and their conversion to microporous materials. Bull. Chem. Soc. Jpn. 63(4), 988–992 (1990). https://doi.org/10.1246/bcsj.63.988
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- J.S. Beck, J.C. Vartuli, W.J. Roth, M.E. Leonowicz, C.T. Kresge et al., A new family of mesoporous molecular sieves prepared with liquid crystal templates. J. Am. Chem. Soc. 114(27), 10834–10843 (1992). https://doi.org/10.1021/ja00053a020
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- Y. Yang, C. Yu, Advances in silica based nanops for targeted cancer therapy. Nanomed. Nanotechnal. Bio. Med. 12(2), 317–332 (2015). https://doi.org/10.1016/j.nano.2015.10.018
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- B. Tian, Y. Liu, Antibacterial applications and safety issues of silica-based materials: a review. Int. J. Appl. Ceram. Technol. 18(2), 289–301 (2021). https://doi.org/10.1111/ijac.13641
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- C.A. Schütz, L. Juillerat-Jeanneret, H. Mueller, I. Lynch, M. Riediker, Therapeutic nanops in clinics and under clinical evaluation. Nanomedicine 8(3), 449–467 (2013). https://doi.org/10.2217/nnm.13.8
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- D. Niu, Z. Ma, Y. Li, J. Shi, Synthesis of core-shell structured dual-mesoporous silica spheres with tunable pore size and controllable shell thickness. J. Am. Chem. Soc. 132(43), 15144–15147 (2010). https://doi.org/10.1021/ja1070653
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- Q. Lin, J.Y.C. Lim, K. Xue, P.Y.M. Yew, C. Owh et al., Sanitizing agents for virus inactivation and disinfection. View 1(2), e16 (2020). https://doi.org/10.1002/viw2.16
- W. Li, E.S. Thian, M. Wang, Z. Wang, L. Ren, Surface design for antibacterial materials: from fundamentals to advanced strategies. Adv. Sci. 8(9), 2100368 (2021). https://doi.org/10.1002/advs.202100368
- H. Koo, R.N. Allan, R.P. Howlin, P. Stoodley, L. Hall-Stoodley, Targeting microbial biofilms: current and prospective therapeutic strategies. Nat. Rev. Microbiol. 15(12), 740–755 (2017). https://doi.org/10.1038/nrmicro.2017.99
- Y. Wang, Y. Yang, Y. Shi, H. Song, C. Yu, Antibiotic-free strategies: antibiotic-free antibacterial strategies enabled by nanomaterials: progress and perspectives. Adv. Mater. 32(18), 2070138 (2020). https://doi.org/10.1002/adma.202070138
- V.K. Truong, R. Lapovok, Y.S. Estri, E.P. Lvanova, The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31(13), 3674–3683 (2010). https://doi.org/10.1016/j.biomaterials.2010.01.071
- E.P. Ivanova, N. Mitik-Dineva, R.J. Crawford, Staleya guttiformis attachment on poly(tert-butylmethacrylate) polymeric surfaces. Micron 39(8), 1197–1204 (2008). https://doi.org/10.1016/j.micron.2008.04.009
- E.P. Ivanova, Y. Niu, S. Karmakar, L. Zhou, C. Xu et al., Bactericidal activity of black silicon. Nat. Commun. 4(1), 2838 (2013). https://doi.org/10.1038/ncomms3838
- Y.A. Nor, Y. Niu, S. Karmakar, L. Zhou, C. Xu et al., Shaping nanops with hydrophilic compositions and hydrophobic properties as nanocarriers for antibiotic delivery. ACS Cent. Sci. 1(6), 328–334 (2015). https://doi.org/10.1021/acscentsci.5b00199
- Y. Wang, Y. Wang, L. Su, Y. Luan, X. Du et al., Effect of surface topology morphologies of silica nanocarriers on the loading of Ag nanops and antibacterial performance. J. Alloys Compd. 783, 136–144 (2019). https://doi.org/10.1016/j.jallcom.2018.12.284
- W. Wang, P. Wang, X. Tang, A.A. Elzatahry, S. Wang et al., Facile synthesis of uniform virus-like mesoporous silica nanops for enhanced cellular internalization. ACS Cent. Sci. 3(8), 839–846 (2017). https://doi.org/10.1021/acscentsci.7b00257
- Y. Niu, M. Yu, S.B. Hartono, J. Yang, H. Xu et al., Nanops: nanops mimicking viral surface topography for enhanced cellular delivery. Adv. Mater. 25(43), 6232–6232 (2013). https://doi.org/10.1002/adma.201302737
- C. Xu, Y. Niu, A. Popat, S. Jambhrunkar, S. Karmakar et al., Rod-like mesoporous silica nanops with rough surfaces for enhanced cellular delivery. J. Mater. Chem. B 2(3), 253–256 (2014). https://doi.org/10.1039/c3tb21431a
- D. Kaplan, Effect of sodium salicylate on the antibacterial activity of glucose oxidase. Chemotherapy 19(4), 235–242 (1973). https://doi.org/10.1159/000221460
- C.T.D. Price, I.R. Lee, J.E. Gustafson, The effects of salicylate on bacteria. Int. J. Biochem. Cell Biol. 32(10), 1029–1043 (2000). https://doi.org/10.1016/S1357-2725(00)00042-X
- Y. Yang, S. Bernardi, H. Song, J. Zhang, M. Yu et al., Anion assisted synthesis of large pore hollow dendritic mesoporous organosilica nanops: understanding the composition gradient. Chem. Mater. 28(3), 704–707 (2016). https://doi.org/10.1021/acs.chemmater.5b03963
- Y. Zhang, Z.Y. Gu, Y. Liu, W.L. Hu, C. Liu et al., Benzene-bridged organosilica modified mesoporous silica nanops via an acid-catalysis approach. Langmuir 37(8), 2780–2786 (2021). https://doi.org/10.1021/acs.langmuir.0c03541
- D. Kharaghani, D. Dutta, P. Gitigard, Y. Tamada, A. Katagiri et al., Development of antibacterial contact lenses containing metallic nanops. Polym. Test. 79, 106034 (2019). https://doi.org/10.1016/j.polymertesting.2019.106034
- R.G. Dinis-Oliveira, P.G. Pinho, A.C.S. Ferreirad, A.M.S. Silvae, C. Afonso et al., Reactivity of paraquat with sodium salicylate: formation of stable complexes. Toxicology 249(2), 130–139 (2008). https://doi.org/10.1016/j.tox.2008.04.014
- J. Pernak, I. Mirska, R. Kmiecik, Antimicrobial activities of new analogues of benzalkonium chloride. Eur. J. Med. Chem. 34(9), 765–771 (1999). https://doi.org/10.1016/S0223-5234(99)00216-0
- L.R. Bennison, C.N. Miller, R.J. Summers, A.M.B. Minnis, G. Sussman et al., The pH of wounds during healing and infection: a descriptive literature review. Wound Manag. Prev. 25(2), 63–69 (2017). https://doi.org/10.3316/informit.927380056251808
- X. Hong, X. Zhong, G. Du, Y. Hou, Y. Zhang et al., The pore size of mesoporous silica nanops regulates their antigen delivery efficiency. Sci. Adv. 6(25), 4462 (2020). https://doi.org/10.1126/sciadv.aaz4462
- C. Lei, Y.X. Cao, S. Hosseinpour, F. Gao, C. Xu, Hierarchical dual-porous hydroxyapatite doped dendritic mesoporous silica nanops based scaffolds promote osteogenesis in vitro and in vivo. Nano Res. 14(3), 770–777 (2020). https://doi.org/10.1007/s12274-020-3112-2
- J.W. Bartholomew, H. Finkelstein, Crystal violet binding capacity and the Gram reaction of bacterial cells. J. Bacteriol. Res. 67(6), 689–691 (1954). https://doi.org/10.1128/jb.67.6.689-691.1954
References
T. Yanagisawa, T. Shimizu, K. Kuroda, C. Kato, The preparation of alkyltrimethylammonium–kanemite complexes and their conversion to microporous materials. Bull. Chem. Soc. Jpn. 63(4), 988–992 (1990). https://doi.org/10.1246/bcsj.63.988
C.T. Kresge, M.E. Leonowicz, W.J. Roth, J.C. Vartuli, J.S. Beck, Ordered mesoporous molecular sieves synthesized by a liquid-crystal template mechanism. Nature 359, 710–712 (1992). https://doi.org/10.1038/359710a0
J.S. Beck, J.C. Vartuli, W.J. Roth, M.E. Leonowicz, C.T. Kresge et al., A new family of mesoporous molecular sieves prepared with liquid crystal templates. J. Am. Chem. Soc. 114(27), 10834–10843 (1992). https://doi.org/10.1021/ja00053a020
D. Zhao, J. Feng, Q. Huo, N.A. Melosh, G.H. Fredrickson et al., Triblock copolymer syntheses of mesoporous silica with periodic 50 to 300 angstrom pores. Science 279(5350), 548–552 (1998). https://doi.org/10.1126/science.279.5350.548
M. Kalantari, M. Yu, Y. Yang, E. Strounina, Z. Gu et al., Tailoring mesoporous-silica nanops for robust immobilization of lipase and biocatalysis. Nano Res. 10(2), 605–617 (2017). https://doi.org/10.1007/s12274-016-1320-6
T. Zhang, B. Huang, A.A. Elzatahry, A. Alghamdi, Q. Yue et al., Synthesis of podlike magnetic mesoporous silica nanochains for use as enzyme support and nanostirrer in biocatalysis. ACS Appl. Mater. Interfaces 12(15), 17901–17908 (2020). https://doi.org/10.1021/acsami.0c03220
Y. Yang, C. Yu, Advances in silica based nanops for targeted cancer therapy. Nanomed. Nanotechnal. Bio. Med. 12(2), 317–332 (2015). https://doi.org/10.1016/j.nano.2015.10.018
Y. Yang, Y. Lu, P.L. Abbaraju, J. Zhang, M. Zhang et al., Multi-shelled dendritic mesoporous organosilica hollow spheres: roles of composition and architecture in cancer immunotherapy. Angew. Chem. Int. Ed. 56(29), 8446–8450 (2017). https://doi.org/10.1002/anie.201701550
H. Song, Y.A. Nor, M. Yu, Y. Yang, J. Zhang et al., Silica nanopollens enhance adhesion for long-term bacterial inhibition. J. Am. Chem. Soc. 138(20), 6455–6462 (2016). https://doi.org/10.1021/jacs.6b00243
B. Tian, Y. Liu, Antibacterial applications and safety issues of silica-based materials: a review. Int. J. Appl. Ceram. Technol. 18(2), 289–301 (2021). https://doi.org/10.1111/ijac.13641
V. Vedarethinam, L. Huang, W. Xu, R. Zhang, D.D. Gurav et al., Bacteria inhibition: detection and inhibition of bacteria on a dual-functional silver platform. Small 15(3), 1970020 (2019). https://doi.org/10.1002/smll.201970020
M.S. Rana, L. Xu, J. Cai, V. Vedarethinam, Y. Teng et al., Zirconia hybrid nanoshells for nutrient and toxin detection. Small 16(46), 2003902 (2020). https://doi.org/10.1002/smll.202003902
S. Savic, K. Vojisavljevic, M. Počuča-Nešić, K. Zivojevic, M. Mladenovic et al., Hard template synthesis of nanomaterials based on mesoporous silica. Metall. Mater. Eng. 24(4), 225–241 (2018). https://doi.org/10.30544/400
S.H. Wu, C.Y. Mou, H.P. Lin, Synthesis of mesoporous silica nanops. Chem. Soc. Rev. 42(9), 3862–3875 (2013). https://doi.org/10.1039/c3cs35405a
I.I. Slowing, B.G. Trewyn, V.S.Y. Lin, Mesoporous silica nanops for intracellular delivery of membrane-impermeable proteins. J. Am. Chem. Soc. 129(28), 8845–8849 (2007). https://doi.org/10.1021/ja0719780
R.R. Castillo, M. Vallet-Regí, Recent advances toward the use of mesoporous silica nanops for the treatment of bacterial infections. Int. J. Nanomed. 16, 4409–4430 (2021). https://doi.org/10.2147/IJN.S273064
C.A. Schütz, L. Juillerat-Jeanneret, H. Mueller, I. Lynch, M. Riediker, Therapeutic nanops in clinics and under clinical evaluation. Nanomedicine 8(3), 449–467 (2013). https://doi.org/10.2217/nnm.13.8
M. Michailidis, I.S. Bellido, W.A. Adamidou, Y.A. Diaz-Fernandez, J. Aveyard, Modified mesoporous silica nanops with a dual synergetic antibacterial effect. ACS Appl. Mater. Interfaces 9(44), 38364–38372 (2017). https://doi.org/10.1021/acsami.7b14642
K. Khorsandi, R. Hosseinzadeh, H.S. Esfahani, S. Keyvani-Ghamsari, S.U. Rahman, Nanomaterials as drug delivery systems with antibacterial properties: current trends and future priorities. Expert Rev. Anti Infect. Ther. 19(10), 1299–1323 (2021). https://doi.org/10.1080/14787210.2021.1908125
D. Hu, L. Zou, Y. Gao, Q. Jin, J. Ji, Emerging nanobiomaterials against bacterial infections in postantibiotic era. View 1(3), 20200014 (2020). https://doi.org/10.1002/VIW.20200014
Y. Wang, H. Song, M.H. Yu, C. Xu, Y. Liu et al., Room temperature synthesis of dendritic mesoporous silica nanops with small sizes and enhanced mRNA delivery performance. J. Mater. Chem. B 6(24), 4089–4095 (2018). https://doi.org/10.1039/c8tb00544c
D. Niu, Z. Ma, Y. Li, J. Shi, Synthesis of core-shell structured dual-mesoporous silica spheres with tunable pore size and controllable shell thickness. J. Am. Chem. Soc. 132(43), 15144–15147 (2010). https://doi.org/10.1021/ja1070653
V. Dubovoy, A. Ganti, T. Zhang, H. Al-Tameemi, J.D. Cerezo et al., One-pot hydrothermal synthesis of benzalkonium-templated mesostructured silica antibacterial agents. J. Am. Chem. Soc. 140(42), 13534–13537 (2018). https://doi.org/10.1021/jacs.8b04843
Q. Lin, J.Y.C. Lim, K. Xue, P.Y.M. Yew, C. Owh et al., Sanitizing agents for virus inactivation and disinfection. View 1(2), e16 (2020). https://doi.org/10.1002/viw2.16
W. Li, E.S. Thian, M. Wang, Z. Wang, L. Ren, Surface design for antibacterial materials: from fundamentals to advanced strategies. Adv. Sci. 8(9), 2100368 (2021). https://doi.org/10.1002/advs.202100368
H. Koo, R.N. Allan, R.P. Howlin, P. Stoodley, L. Hall-Stoodley, Targeting microbial biofilms: current and prospective therapeutic strategies. Nat. Rev. Microbiol. 15(12), 740–755 (2017). https://doi.org/10.1038/nrmicro.2017.99
Y. Wang, Y. Yang, Y. Shi, H. Song, C. Yu, Antibiotic-free strategies: antibiotic-free antibacterial strategies enabled by nanomaterials: progress and perspectives. Adv. Mater. 32(18), 2070138 (2020). https://doi.org/10.1002/adma.202070138
V.K. Truong, R. Lapovok, Y.S. Estri, E.P. Lvanova, The influence of nano-scale surface roughness on bacterial adhesion to ultrafine-grained titanium. Biomaterials 31(13), 3674–3683 (2010). https://doi.org/10.1016/j.biomaterials.2010.01.071
E.P. Ivanova, N. Mitik-Dineva, R.J. Crawford, Staleya guttiformis attachment on poly(tert-butylmethacrylate) polymeric surfaces. Micron 39(8), 1197–1204 (2008). https://doi.org/10.1016/j.micron.2008.04.009
E.P. Ivanova, Y. Niu, S. Karmakar, L. Zhou, C. Xu et al., Bactericidal activity of black silicon. Nat. Commun. 4(1), 2838 (2013). https://doi.org/10.1038/ncomms3838
Y.A. Nor, Y. Niu, S. Karmakar, L. Zhou, C. Xu et al., Shaping nanops with hydrophilic compositions and hydrophobic properties as nanocarriers for antibiotic delivery. ACS Cent. Sci. 1(6), 328–334 (2015). https://doi.org/10.1021/acscentsci.5b00199
Y. Wang, Y. Wang, L. Su, Y. Luan, X. Du et al., Effect of surface topology morphologies of silica nanocarriers on the loading of Ag nanops and antibacterial performance. J. Alloys Compd. 783, 136–144 (2019). https://doi.org/10.1016/j.jallcom.2018.12.284
W. Wang, P. Wang, X. Tang, A.A. Elzatahry, S. Wang et al., Facile synthesis of uniform virus-like mesoporous silica nanops for enhanced cellular internalization. ACS Cent. Sci. 3(8), 839–846 (2017). https://doi.org/10.1021/acscentsci.7b00257
Y. Niu, M. Yu, S.B. Hartono, J. Yang, H. Xu et al., Nanops: nanops mimicking viral surface topography for enhanced cellular delivery. Adv. Mater. 25(43), 6232–6232 (2013). https://doi.org/10.1002/adma.201302737
C. Xu, Y. Niu, A. Popat, S. Jambhrunkar, S. Karmakar et al., Rod-like mesoporous silica nanops with rough surfaces for enhanced cellular delivery. J. Mater. Chem. B 2(3), 253–256 (2014). https://doi.org/10.1039/c3tb21431a
D. Kaplan, Effect of sodium salicylate on the antibacterial activity of glucose oxidase. Chemotherapy 19(4), 235–242 (1973). https://doi.org/10.1159/000221460
C.T.D. Price, I.R. Lee, J.E. Gustafson, The effects of salicylate on bacteria. Int. J. Biochem. Cell Biol. 32(10), 1029–1043 (2000). https://doi.org/10.1016/S1357-2725(00)00042-X
Y. Yang, S. Bernardi, H. Song, J. Zhang, M. Yu et al., Anion assisted synthesis of large pore hollow dendritic mesoporous organosilica nanops: understanding the composition gradient. Chem. Mater. 28(3), 704–707 (2016). https://doi.org/10.1021/acs.chemmater.5b03963
Y. Zhang, Z.Y. Gu, Y. Liu, W.L. Hu, C. Liu et al., Benzene-bridged organosilica modified mesoporous silica nanops via an acid-catalysis approach. Langmuir 37(8), 2780–2786 (2021). https://doi.org/10.1021/acs.langmuir.0c03541
D. Kharaghani, D. Dutta, P. Gitigard, Y. Tamada, A. Katagiri et al., Development of antibacterial contact lenses containing metallic nanops. Polym. Test. 79, 106034 (2019). https://doi.org/10.1016/j.polymertesting.2019.106034
R.G. Dinis-Oliveira, P.G. Pinho, A.C.S. Ferreirad, A.M.S. Silvae, C. Afonso et al., Reactivity of paraquat with sodium salicylate: formation of stable complexes. Toxicology 249(2), 130–139 (2008). https://doi.org/10.1016/j.tox.2008.04.014
J. Pernak, I. Mirska, R. Kmiecik, Antimicrobial activities of new analogues of benzalkonium chloride. Eur. J. Med. Chem. 34(9), 765–771 (1999). https://doi.org/10.1016/S0223-5234(99)00216-0
L.R. Bennison, C.N. Miller, R.J. Summers, A.M.B. Minnis, G. Sussman et al., The pH of wounds during healing and infection: a descriptive literature review. Wound Manag. Prev. 25(2), 63–69 (2017). https://doi.org/10.3316/informit.927380056251808
X. Hong, X. Zhong, G. Du, Y. Hou, Y. Zhang et al., The pore size of mesoporous silica nanops regulates their antigen delivery efficiency. Sci. Adv. 6(25), 4462 (2020). https://doi.org/10.1126/sciadv.aaz4462
C. Lei, Y.X. Cao, S. Hosseinpour, F. Gao, C. Xu, Hierarchical dual-porous hydroxyapatite doped dendritic mesoporous silica nanops based scaffolds promote osteogenesis in vitro and in vivo. Nano Res. 14(3), 770–777 (2020). https://doi.org/10.1007/s12274-020-3112-2
J.W. Bartholomew, H. Finkelstein, Crystal violet binding capacity and the Gram reaction of bacterial cells. J. Bacteriol. Res. 67(6), 689–691 (1954). https://doi.org/10.1128/jb.67.6.689-691.1954