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Biomimetic synthesis of vaterite CaCO3 microspheres under threonine for preparation of pH-responsive antibacterial biofilm

Published online by Cambridge University Press:  17 July 2020

Tingyu Yang ,
Yu Wu ,
Xiaoqing Yue ,
Cuiyan Wang  and
Jianbin Zhang Open the ORCID record for Jianbin Zhang [Opens in a new window]
Tingyu Yang
Affiliation:
College of Chemical Engineering, Inner Mongolia University of Technology, Hohhot010051, China Inner Mongolia Engineering Research Center for CO2 Capture and Utilization, Hohhot010051, China
Yu Wu
Affiliation:
College of Chemical Engineering, Inner Mongolia University of Technology, Hohhot010051, China Inner Mongolia Engineering Research Center for CO2 Capture and Utilization, Hohhot010051, China
Xiaoqing Yue
Affiliation:
College of Chemical Engineering, Inner Mongolia University of Technology, Hohhot010051, China Inner Mongolia Engineering Research Center for CO2 Capture and Utilization, Hohhot010051, China
Cuiyan Wang
Affiliation:
College of Chemical Engineering, Inner Mongolia University of Technology, Hohhot010051, China Inner Mongolia Engineering Research Center for CO2 Capture and Utilization, Hohhot010051, China
Jianbin Zhang*
Affiliation:
College of Chemical Engineering, Inner Mongolia University of Technology, Hohhot010051, China Inner Mongolia Engineering Research Center for CO2 Capture and Utilization, Hohhot010051, China
*
a)Address all correspondence to this author. e-mail: [email protected]
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Abstract

The synthesis of antibacterial biomaterial with specific functions responsive to specific bacterial growth environments is of significant importance to achieve effective sterilization and reduce the resistant bacteria. Herein, inspired by biomineralization, we develop a one-pot, threonine (Thr)-mediated biomineralization method using a CO2 bubbling procedure to green, simply and quickly prepare vaterite CaCO3 microspheres as a platform for antibacterial Sanguinarine (SAN) delivery. The loading capacity of vaterite CaCO3 microspheres for SAN drugs reached 159.8 mg/g, corresponding to the loading efficiency of 83.7%. And for the first time, a novel Sanguinarine@calcium carbonate (SAN@CaCO3) organic–inorganic hybrid antibacterial biofilm was constructed by using vaterite CaCO3 microspheres with pH-responsive and high SAN drug-loading. Importantly, the film showed bacteria-triggered, pH-responsive SAN release properties and strong bactericidal ability (96.19%) for Staphylococcus aureus (S. aureus). Meanwhile, it also had antibacterial capabilities in real environments. In 7 days, it can significantly inhibit the adhesion and growth of bacteria in the air. The biomineralized synthetic vaterite CaCO3 microspheres and the application in the construction of pH-responsive antibacterial biofilm have bright future in resisting bacterial infections and reducing the production of resistant bacteria.

Keywords

biomaterialcompoundfilm
Type
Article
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Journal of Materials Research , Volume 35 , Issue 18 , 28 September 2020 , pp. 2427 - 2440
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Copyright © Materials Research Society 2020

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References

Diekema, D.J., Pfaller, M.A., Schmitz, F.J., Smayevsky, J., Bell, J., Jones, R.N., and Beach, M.: Survey of infections due to Staphylococcus species: Frequency of occurrence and antimicrobial susceptibility of isolates collected in the United States, Canada, Latin America, Europe, and the Western Pacific region for the SENTRY antimicrobial surveillance program, 1997-1999. Clin. Infect. Dis. 32, S114–S132 (2001).CrossRefGoogle ScholarPubMed
Maya, S., Indulekha, S., Sukhithasri, V., Smitha, K.T., Nair, S.V., Jayakumar, R., and Biswas, R.: Efficacy of tetracycline encapsulated O-carboxymethyl chitosan nanoparticles against intracellular infections of Staphylococcus aureus. Int. J. Biol. Macromol. 51, 392–399 (2012).CrossRefGoogle ScholarPubMed
Samanipour, A., Dashti-Khavidaki, S., Abbasi, M.R., and Abdollahi, A.: Antibiotic resistance patterns of microorganisms isolated from nephrology and kidney transplant wards of a referral academic hospital. J. Res. Pharm. Pract. 5, 43–51 (2016).Google ScholarPubMed
Cochis, A., Azzimonti, B., Della Valle, C., De Giglio, E., Bloise, N., Visai, L., Cometa, S., Rimondini, L., and Chiesa, R.: The effect of silver or gallium doped titanium against the multidrug resistant Acinetobacter baumannii. Biomaterials 80, 80–95 (2015).CrossRefGoogle ScholarPubMed
Lu, Y., Wu, Y., Liang, J., Libera, M.R., and Sukhishvili, S.A.: Self-defensive antibacterial layer-by-layer hydrogel coatings with pH-triggered hydrophobicity. Biomaterials 45, 64–71 (2015).CrossRefGoogle ScholarPubMed
Hao, X.P., Wang, W.H., Yang, Z.Q., Yue, L.F., Sun, H.Y., Wang, H.F., Guo, Z.H., Cheng, F., and Chen, S.G.: pH responsive antifouling and antibacterial multilayer films with self-healing performance. Chem. Eng. J. 356, 130–141 (2019).CrossRefGoogle Scholar
Wang, W.H., Hao, X.P., Chen, S.G., Yang, Z.Q., Wang, C.Y., Yan, R., Zhang, X., Liu, H., Shao, Q., and Guo, Z.H.: pH-responsive capsaicin@chitosan nanocapsules for antibiofouling in marine applications. Polymer 158, 223–230 (2018).CrossRefGoogle Scholar
Li, S.K. and D'Emanuele, A.: On-off transport through a thermoresponsive hydrogel composite membrane. J. Control. Release 75, 55–67 (2001).CrossRefGoogle ScholarPubMed
Albright, V., Zhuk, I., Wang, Y., Selin, V., van de Belt-Gritter, B., Busscher, H.J., van der Mei, H.C., and Sukhishvili, S.A.: Self-defensive antibiotic-loaded layer-by-layer coatings: Imaging of localized bacterial acidification and pH-triggering of antibiotic release. Acta Biomater. 6, 66–74 (2017).CrossRefGoogle Scholar
Kiprono, S.J., Ullah, M.W., and Yang, G.: Surface engineering of microbial cells: Strategies and applications. Eng. Sci. 1, 33–45 (2018).Google Scholar
Wang, B.L., Liu, H.H., Wang, Z.F., Shi, S., Nan, K.H., Xu, Q.W., Yea, Z., and Chen, H.: A self-defensive antibacterial coating acting through the bacteria-triggered release of a hydrophobic antibiotic from layer-by-layer films. J. Mater. Chem. B 5, 1498–1506 (2017).CrossRefGoogle ScholarPubMed
Xu, Q.W., Li, X., Jin, Y.Y., Sun, L., Ding, X.X., Liang, L., Wang, L., Nan, K.H., Ji, J., Chen, H., and Wang, B.L.: Bacterial self-defense antibiotics release from organic-inorganic hybrid multilayer films for long-term anti-adhesion and biofilm inhibition properties. Nanoscale 9, 19245–19254 (2017).CrossRefGoogle ScholarPubMed
Svenskaya, Y.I., Genina, E.A., Parakhonskiy, B.V., Lengert, E.V., Talnikova, E.E., Terentyuk, G.S., Utz, S.R., Gorin, D.A., Tuchin, V.V., and Sukhorukov, G.B.: A simple non-invasive approach toward efficient transdermal drug delivery based on biodegradable particulate system. ACS Appl. Mater. Inter. 11, 17270–17282 (2019).CrossRefGoogle ScholarPubMed
Choukrani, G., Maharjan, B., Park, C.H., Kim, C.S., and Sasikala, A.R.K.: Biocompatible superparamagnetic sub-micron vaterite particles for thermo-chemotherapy: From controlled design to in vitro anticancer synergism. Mater. Sci. Eng. C 106, 110226 (2020).CrossRefGoogle ScholarPubMed
Guo, Y.M., Jia, W.L., Li, H., Shi, W.K., Zhang, J., Feng, J., and Yang, L.: Facile green synthesis of calcium carbonate/folate porous hollow spheres for the targeted pH-responsive release of anticancer drugs. J. Mater. Chem. B 4, 5650–5653 (2016).CrossRefGoogle ScholarPubMed
Trushina, D.B., Bukreeva, T.V., Kovalchuk, M.V., and Antipina, M.N.: CaCO3 vaterite microparticles for biomedical and personal care applications. Mater. Sci. Eng. C 45, 644–658 (2014).CrossRefGoogle ScholarPubMed
Wang, A.H., Yang, Y., Zhang, X.M., Liu, X.C., Cui, W., and Li, J.B.: Gelatin-assisted synthesis of vaterite nanoparticles with higher surface area and porosity as anticancer drug containers in vitro. ChemPlusChem 81, 194–201 (2016).CrossRefGoogle ScholarPubMed
Guo, Y.M., Fang, Q.L., Li, H., Shi, W.K., Zhang, J., Feng, J., Jia, W.L., and Yang, L.: Hollow silica nanospheres coated with insoluble calcium salts for pH-responsive sustained release of anticancer drugs. Chem. Commun. 52, 10652–10655 (2016).CrossRefGoogle ScholarPubMed
Liu, L.J., Zhang, X.L., Liu, X., Liu, J., Lu, G.Z., Kaplan, D.L., Zhu, H.S., and Lu, Q.: Biomineralization of stable and monodisperse vaterite microspheres using silk nanoparticles. ACS Appl. Mater. Inter. 7, 1735–1745 (2015).CrossRefGoogle ScholarPubMed
Klevens, R.M., Edwards, J.R., Richards, C.L., Horan, T.C., Gaynes, R.P., Pollock, D.A., and Cardo, D.M.: Estimating health care associated infections and deaths in US hospitals, 2002. Public Health Rep. 122, 160–166 (2007).CrossRefGoogle Scholar
Du, L., Wang, Y.J., and Luo, G.S.: In situ preparation of hydrophobic CaCO3 nanoparticles in a gas-liquid microdispersion process. Particuology 11, 421–427 (2013).CrossRefGoogle Scholar
Chuajiw, W., Takatori, K., Igarashi, T., Hara, H., and Fukushima, Y.: The influence of aliphatic amines, diamines, and amino acids on the polymorph of calcium carbonate precipitated by the introduction of carbon dioxide gas into calcium hydroxide aqueous suspensions. J. Cryst. Growth 386, 119–127 (2014).CrossRefGoogle Scholar
Sun, B.C., Wang, X.M., Chen, J.M., Chu, G.W., Chen, J.F., and Shao, L.: Synthesis of nano-CaCO3 by simultaneous absorption of CO2 and NH3 into CaCl2 solution in a rotating packed bed. Chem. Eng. J 168, 731–736 (2011).CrossRefGoogle Scholar
Domingo, C., García-Carmona, J., Loste, E., Fanovich, A., Fraile, J., and Gómez-Morales, J.: Control of calcium carbonate morphology by precipitation in compressed and supercritical carbon dioxide media. J. Cryst. Growth 271, 268–273 (2004).CrossRefGoogle Scholar
Zhang, C.X., Zhang, J.L., Feng, X.Y., Li, W., Zhao, Y.J., and Han, B.X.: Influence of surfactants on the morphologies of CaCO3 by carbonation route with compressed CO2. Colloids Surf. A 324, 167–170 (2008).CrossRefGoogle Scholar
Demichelis, R., Raiteri, P., Gale, J.D., and Dovesi, R.A.: New structural model for disorder in vaterite from first-principles calculations. CrystEngComm 14, 44–47 (2012).CrossRefGoogle Scholar
Kato, T., Sugawara, A., and Hosoda, N.: Calcium carbonate-organic hybrid materials. Adv. Mater. 14, 869–877 (2002).3.0.CO;2-E>CrossRefGoogle Scholar
Nehrke, G. and Van Cappellen, P.: Framboidal vaterite aggregates and their transformation into calcite: A morphological study. J. Cryst. Growth 287, 528–530 (2006).CrossRefGoogle Scholar
Qiao, L. and Feng, Q.L.: Study on twin stacking faults in vaterite tablets of freshwater lacklustre pearls. J. Cryst. Growth 304, 253–256 (2007).CrossRefGoogle Scholar
Soldati, A.L., Jacob, D.E., Wehrmeister, U., and Hofmeister, W.: Structural characterization and chemical composition of aragonite and vaterite in freshwater cultured pearls. Mineral. Mag. 72, 579–592 (2008).CrossRefGoogle Scholar
Aizenberg, J., Lambert, G., Addadi, L., and Weiner, S.: Stabilization of amorphous calcium carbonate by specialized macromolecules in biological and synthetic precipitates. Adv. Mater. 8, 222–226 (1996).CrossRefGoogle Scholar
Aizenberg, J., Lambert, G., Weiner, S., and Addadi, L.: Factors involved in the formation of amorphous and crystalline calcium carbonate: A study of an ascidian skeleton. J. Am. Chem. Soc. 124, 32–39 (2002).CrossRefGoogle ScholarPubMed
Tong, H., Ma, W., Wang, L., Wan, P., Hu, J., and Cao, L.: Control over the crystal phase, shape, size and aggregation of calcium carbonate via a L-aspartic acid inducing process. Biomaterials 25, 3923–3929 (2004).CrossRefGoogle Scholar
Malkaj, P. and Dalas, E.: Calcium carbonate crystallization in the presence of aspartic acid. Cryst. Growth Des. 4, 721–723 (2004).CrossRefGoogle Scholar
Hou, W.T. and Feng, Q.L.: Morphologies and growth model of biomimetic fabricated calcite crystals using amino acids and insoluble matrix membranes of Mytilus edulis. Cryst. Growth Des. 6, 1086–1090 (2006).CrossRefGoogle Scholar
Gao, Z.Z., Kan, J.L., Chen, L.X., Bai, D., Wang, H.Y., Tao, Z., and Xiao, X.: Binding and selectivity of essential amino acid guests to the inverted cucurbit[7]uril host. ACS Omega 2, 5633–5640 (2017).CrossRefGoogle ScholarPubMed
Fujii, H., Zhang, X.H., and Yoshida, T.: Essential amino acid residues controlling the unique regioselectivity of heme oxygenase in Pseudomonas aeruginosa. J. Am. Chem. Soc. 126, 4466–4467 (2004).CrossRefGoogle ScholarPubMed
Beuria, T.K., Santra, M.K., and Panda, D.: Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44, 16584–16593 (2005).CrossRefGoogle ScholarPubMed
Qing, Z.X., Yang, P., Tang, Q., Cheng, P., Liu, X.B., Zheng, Y.J., and Zeng, J.G.: Isoquinoline alkaloids and their antiviral, antibacterial, and antifungal activities and structure-activity relationship. Curr. Org. Chem. 21, 1920–1934 (2017).CrossRefGoogle Scholar
Yang, S.B., Han, X.G., Yang, Y., Qiao, H., Yu, Z.F., Liu, Y., Wang, J., and Tang, T.T.: Bacteria-targeting nanoparticles with microenvironment responsive antibiotic release to eliminate intracellular Staphylococcus aureus and associated infection. ACS Appl. Mater. Inter. 10, 14299–14311 (2018).CrossRefGoogle ScholarPubMed
Fraunholz, M. and Sinha, B.: Intracellular Staphylococcus aureus: live-in and let die. Front. Cell. Infect. Microbiol. 2, 43 (2012).CrossRefGoogle ScholarPubMed
Yang, C., Krishnamurthy, S., Liu, J., Liu, S., Lu, X., Coady, D.J., Cheng, W., De Libero, G., Singhal, A., Hedrick, J.L., and Yang, Y.Y.: Broad-spectrum antimicrobial star polycarbonates functionalized with mannose for targeting bacteria residing inside immune cells. Adv. Healthc. Mater. 5, 1272–1281 (2016).CrossRefGoogle ScholarPubMed
Guo, B., Zhao, T.X., Sha, F., Zhang, F., Li, Q., Zhao, J., and Zhang, J.B.: Synthesis of vaterite CaCO3 micro-spheres by carbide slag and a novel CO2-storage material. J. CO2 Util 18, 23–29 (2017).CrossRefGoogle Scholar
Zhao, T.X., Guo, B., Zhang, F., Sha, F., Li, Q., and Zhang, J.B.: Morphology control in the synthesis of CaCO3 microspheres with a novel CO2-storage material. ACS Appl. Mater. Inter. 7(29), 15918–15927 (2015).CrossRefGoogle ScholarPubMed
Kontoyannis, C.G. and Vagenas, N.V.: Calcium carbonate phase analysis using XRD and FT-Raman spectroscopy. Analyst 125, 251–255 (2000).CrossRefGoogle Scholar
Tas, A.C.: Monodisperse calcium carbonate microtablets forming at 70°C in prerefrigerated CaCl2-gelatin-urea solutions. Int. J. Appl. Ceram. Technol. 6, 53–59 (2009).CrossRefGoogle Scholar
Xu, A.W., Antonietti, M., Cölfen, H., and Fang, Y.P.: Uniform hexagonal plates of vaterite CaCO3 mesocrystals formed by biomimetic mineralization. Adv. Funct. Mater. 16, 903–908 (2010).CrossRefGoogle Scholar
Zhou, G.T., Yao, Q.Z., Fu, S.Q., and Guan, Y.B.: Controlled crystallization of unstable vaterite with distinct morphologies and their polymorphic transition to stable calcite. Eur. J. Mineral. 22, 259–269 (2010).CrossRefGoogle Scholar
Sarkar, A. and Mahapatra, S.: Synthesis of all crystalline phases of anhydrous calcium carbonate. Cryst. Growth Des. 10, 2129–2135 (2010).CrossRefGoogle Scholar
Pouget, E.M., Bomans, P.H.H., Dey, A., Frederik, P.M., With, G.D., and Sommerdijk, N.A.J.M.: The development of morphology and structure in hexagonal vaterite. J. Am. Chem. Soc. 132, 11560–11565 (2010).CrossRefGoogle ScholarPubMed
Li, J., Jiang, H.K., Ouyang, X., Han, S.H., Wang, J., Xie, R., Zhu, W.T., Ma, N., Wei, H., and Jiang, Z.Y.: CaCO3/tetraethylenepentamine-graphene hollow microspheres as biocompatible bone drug carriers for controlled release. ACS Appl. Mater. Inter. 8, 30027–30036 (2016).CrossRefGoogle ScholarPubMed
Picker, A., Kellermeier, M., Seto, J., Gebauer, D., and Co¨lfen, H.: The multiple effects of amino acids on the early stages of calcium carbonate crystallization. Z. Kristallogr. Cryst. Mater. 227, 744–757 (2012).CrossRefGoogle Scholar
Borukhin, S., Bloch, L., Radlauer, T., Hill, A.H., Fitch, A.N., and Pokroy, B.: Screening the incorporation of amino acids into an inorganic crystalline host: The case of calcite. Adv. Funct. Mater. 22, 4216–4224 (2012).CrossRefGoogle Scholar
Zhou, X.L., Liu, W.Z., Zhang, J., Wu, C., Ou, X.W., Tian, C., Lin, Z., and Dang, Z.: Biogenic calcium carbonate with hierarchical organic-inorganic composite structure enhancing the removal of Pb(II) from wastewater. ACS Appl. Mater. Inter. 9, 35785–35793 (2017).CrossRefGoogle ScholarPubMed
Cai, H.Y., Wang, P., and Zhang, D.: pH-responsive linkages-enabled layer-by-layer assembled antibacterial and antiadhesive multilayer films with polyelectrolyte nanocapsules as biocide delivery vehicles. J. Drug Deliv. Sci. Technol. 54, 101251–101266 (2019).CrossRefGoogle Scholar
Wang, X.H., Song, L.J., Zhao, J., Zhou, R.T., Luan, S.F., Huang, Y.B., Yin, J.H., and Khan, A.F.: Bacterial adaptability of enzyme and pH dual-responsive surface for infection resistance. J. Mater. Chem. B 6, 7710–7718 (2018).CrossRefGoogle ScholarPubMed
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