Abstract
Cerium oxide nanoparticles (CONPs), widely used in catalytic applications owing to their robust redox reaction, are now being considered in therapeutic applications based on their enzyme mimetic properties such as catalase and super oxide dismutase (SOD) mimetic activities. In therapeutic applications, the emerging demand for CONPs with low cytotoxicity, high cost efficiency, and high enzyme mimetic capability necessitates the exploration of alternative synthesis and effective material design. This study presents a room temperature aqueous synthesis for low-cost production of shape-selective CONPs without potentially harmful organic substances, and additionally, investigates cell viability and catalase and SOD mimetic activities. This synthesis, at room temperature, produced CONPs with particular planes: {111}/{100} nanopolyhedra, {100} nano/submicron cubes, and {111}/{100} nanorods that grew in [110] longitudinal direction. Enzymatic activity assays indicated that nanopolyhedra with a high concentration of Ce4+ ions promoted catalase mimetic activity, while nanocubes and nanorods with high Ce3+ ion concentrations enhanced SOD mimetic activity. This is the first study indicating that shape and facet configuration design of CONPs, coupled with the retention of dominant, specific Ce valence states, potentiates enzyme mimetic activities. These findings may be utilized for CONP design aimed at enhancing enzyme mimetic activities in therapeutic applications.
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Pirmohamed, T.; Dowding, J. M.; Singh, S.; Wasserman, B.; Heckert, E.; Karakoti, A. S.; King, J. E.; Seal, S.; Self, W. T. Nanoceria exhibit redox state-dependent catalase mimetic activity. Chem. Commun. 2010, 46, 2736–2738.
Korsvik, C.; Patil, S.; Seal, S.; Self, W. T. Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanoparticles. Chem. Commun. 2007, 1056–1058.
Heckert, E. G.; Karakoti, A. S.; Seal, S.; Self, W. T. The role of cerium redox state in the SOD mimetic activity of nanoceria. Biomaterials 2008, 29, 2705–2709.
Li, Y. Y.; He, X.; Yin, J. J.; Ma, Y. H.; Zhang, P.; Li, J. Y.; Ding, Y. Y.; Zhang, J.; Zhao, Y. L.; Chai, Z. F. et al. Acquired superoxide-scavenging ability of ceria nanoparticles. Angew. Chem., Int. Ed. 2015, 54, 1832–1035.
Xia, T.; Kovochich, M.; Liong, M.; Mädler, L.; Gilbert, B.; Shi, H. B.; Yeh, J. I.; Zink, J. I.; Nel, A. E. Comparison of the mechanism of toxicity of zinc oxide and cerium oxide nanoparticles based on dissolution and oxidative stress properties. ACS Nano 2008, 2, 2121–2134.
Xu, M. S.; Fujita, D.; Kajiwara, S.; Minowa, T.; Li, X. L.; Takemura, T.; Iwai, H.; Hanagata, N. Contribution of physicochemical characteristics of nano-oxides to cytotoxicity. Biomaterials 2010, 31, 8022–8031.
Batinic-Haberle, I.; Tovmasyan, A.; Roberts, E. R. H.; Vujaskovic, Z.; Leong, K. W.; Spasojevic, I. SOD therapeutics: Latest insights into their structure-activity relationships and impact on the cellular redox-based signaling pathways. Antioxid. Redox Signal. 2014, 20, 2372–2415.
Chen, J. P.; Patil, S.; Seal, S.; McGinnis, J. F. Rare earth nanoparticles prevent retinal degeneration induced by intracellular peroxides. Nat. Nanotechnol. 2006, 1, 142–150.
Heckman, K. L.; DeCoteau, W.; Estevez, A.; Reed, K. J.; Costanzo, W.; Sanford, D.; Leiter, J. C.; Clauss, J.; Knapp, K.; Gomez, C. et al. Custom cerium oxide nanoparticles protect against a free radical mediated autoimmune degenerative disease in the brain. ACS Nano 2013, 7, 10582–10596.
Pagliari, F.; Mandoli, C.; Forte, G.; Magnani, E.; Pagliari, S.; Nardone, G.; Licoccia, S.; Minieri, M.; Di Nardo, P.; Traversa, E. Cerium oxide nanoparticles protect cardiac progenitor cells from oxidative stress. ACS Nano 2012, 6, 3767–3775.
Wason, M. S.; Colon, J.; Das, S.; Seal, S.; Turkson, J.; Zhao, J.; Baker, C. H. Sensitization of pancreatic cancer cells to radiation by cerium oxide nanoparticle-induced ROS production. Nanomedicine 2013, 9, 558–569.
Celardo, I.; De Nicola, M.; Mandoli, C.; Pedersen, J. Z.; Traversa, E.; Ghibelli, L. Ce3+ ions determine redox-dependent anti-apoptotic effect of cerium oxide nanoparticles. ACS Nano 2011, 5, 4537–4549.
Zhang, D. S.; Du, X. J.; Shi, L. Y.; Gao, R. H. Shapecontrolled synthesis and catalytic application of ceria nanomaterials. Dalton Trans. 2012, 41, 14455–14475.
Conesa, J. C. Computer modeling of surfaces and defects on cerium dioxide. Surf. Sci. 1995, 339, 337–352.
Jiang, Y.; Adams, J. B.; van Schilfgaarde, M. Densityfunctional calculation of CeO2 surfaces and prediction of effects of oxygen partial pressure and temperature on stabilities. J. Chem. Phys. 2005, 123, 064701.
Sayle, T. X. T.; Parker, S. C.; Catlow, C. R. A. The role of oxygen vacancies on ceria surfaces in the oxidation of carbon monoxide. Surf. Sci. 1994, 316, 329–336.
Zhang, J.; Kumagai, H.; Yamamura, K.; Ohara, S.; Takami, S.; Morikawa, A.; Shinjoh, H.; Kaneko, K.; Adschiri, T.; Suda, A. Extra-low-temperature oxygen storage capacity of CeO2 nanocrystals with cubic facets. Nano Lett. 2011, 11, 361–364.
Mai, H. X.; Sun, L. D.; Zhang, Y. W.; Si, R.; Feng, W.; Zhang, H. P.; Liu, H. C.; Yan, C. H. Shape-selective synthesis and oxygen storage behavior of ceria nanopolyhedra, nanorods, and nanocubes. J. Phys. Chem. B 2005, 109, 24380–24385.
Wu, Z. L.; Li, M. J.; Overbury, S. H. On the structure dependence of CO oxidation over CeO2 nanocrystals with well-defined surface planes. J. Catal. 2012, 285, 61–73.
Liu, X. W.; Zhou, K. B.; Wang, L.; Wang, B. Y.; Li, Y. D. Oxygen vacancy clusters promoting reducibility and activity of ceria nanorods. J. Am. Chem. Soc. 2009, 131, 3140–3141.
Agarwal, S.; Lefferts, L.; Mojet, B. L.; Ligthart, D. A. J.; Hensen, E. J. M.; Mitchell, D. R. G.; Erasmus, W. J.; Anderson, B. G.; Olivier, E. J.; Neethling, J. H. et al. Exposed surfaces on shape-controlled ceria nanoparticles revealed through AC-TEM and water-gas shift reactivity. ChemSusChem 2013, 6, 1898–1906.
Si, R.; Flytzani-Stephanopoulos, M. Shape and crystal-plane effects of nanoscale ceria on the activity of Au-CeO2 catalysts for the water-gas shift reaction. Angew. Chem., Int. Ed. 2008, 47, 2884–2887.
Wang, S. P.; Zhao, L. F.; Wang, W.; Zhao, Y. J.; Zhang, G. L.; Ma, X. B.; Gong, J. L. Morphology control of ceria nanocrystals for catalytic conversion of CO2 with methanol. Nanoscale 2013, 5, 5582–5588.
Zhang, Y.; Zhou, K. B.; Zhai, Y. W.; Qin, F.; Pan, L. L.; Yao, X. Crystal plane effects of nano-CeO2 on its antioxidant activity. RSC Adv. 2014, 4, 50325–50330.
Pan, C. S.; Zhang, D. S.; Shi, L. Y.; Fang, J. H. Template-free synthesis, controlled conversion, and CO oxidation properties of CeO2 nanorods, nanotubes, nanowires, and nanocubes. Eur. J. Inorg. Chem. 2008, 15, 2429–2436.
Xu, J. X.; Li, G. S.; Li, L. P. CeO2 nanocrystals: Seed-mediated synthesis and size control. Mater. Res. Bull. 2008, 43, 990–995.
Chen, H. I.; Chang, H. Y. Synthesis of nanocrystalline cerium oxide particles by the precipitation method. Ceram. Int. 2005, 31, 795–802.
Chang, H. Y.; Chen, H. I. Morphological evolution for CeO2 nanoparticles synthesized by precipitation technique. J. Cryst. Growth. 2005, 283, 457–468.
Vantomme, A.; Yuan, Z. Y.; Du, G. H.; Su, B. L. Surfactant-assisted large-scale preparation of crystalline CeO2 nanorods. Langmuir 2005, 21, 1132–1135.
Yang, S. W.; Gao, L. Controlled synthesis and self-assembly of CeO2 nanocubes. J. Am. Chem. Soc. 2006, 128, 9330–9331.
Zhang, J.; Ohara, S.; Umetsu, M.; Naka, T.; Hatakeyama, Y.; Adschiri, T. Colloidal ceria nanocrystals: A tailor-made crystal morphology in supercritical water. Adv. Mater. 2007, 19, 203–206.
Wu, Q.; Zhang, F.; Xiao, P.; Tao, H. S.; Wang, X. Z.; Hu, Z.; Lü, Y. N. Great influence of anions for controllable synthesis of CeO2 nanostructures: From nanorods to nanocubes. J. Phys. Chem. C 2008, 112, 17076–17080.
Du, N.; Zhang, H.; Chen, B. D.; Ma, X. Y.; Yang, D. R. Ligand-free self-assembly of ceria nanocrystals into nanorods by oriented attachment at low Temperature. J. Phys. Chem. C 2007, 111, 12677–12680.
Sreeremya, T. S.; Krishnan, A.; Remani, K. C.; Patil, K. R.; Brougham, D. F.; Ghosh, S. Shape-selective oriented cerium oxide nanocrystals permit assessment of the effect of the exposed facets on catalytic activity and oxygen storage capacity. ACS Appl. Mater. Interfaces 2015, 7, 8545–8555.
Maitarad, P.; Han, J.; Zhang, D. S.; Shi, L. Y.; Namuangruk, S.; Rungrotmongkol, T. Structure–activity relationships of NiO on CeO2 nanorods for the selective catalytic reduction of NO with NH3: Experimental and DFT studies. J. Phys. Chem. C 2014, 118, 9612–9620.
Tsunekawa, S.; Sivamohan, R.; Ito, S.; Kasuya, A.; Fukuda, T. Structural study on monosize CeO2–x nano-particles. Nanostruct. Mater. 1999, 11, 141–147.
Deshpande, S.; Patil, S.; Kuchibhatla, S. V.; Seal, S. Size dependency variation in lattice parameter and valency states in nanocrystalline cerium oxide. Appl. Phys. Lett. 2005, 87, 133113.
Holgado, J. P.; Munuera, G.; Espinós, J. P.; González-Elipe, A. R. XPS study of oxidation processes of CeOx defective layers. Appl. Surf. Sci. 2000, 158, 164–171.
Chen, L.; Fleming, P.; Morris, V.; Holmes, J. D.; Morris, M. A. Size-related lattice parameter changes and surface defects in ceria nanocrystals. J. Phys. Chem. C 2010, 114, 12909–12919.
Naganuma, T.; Traversa, E. Stability of the Ce3+ valence state in cerium oxide nanoparticle layers. Nanoscale 2012, 4, 4950–4953.
Naganuma, T.; Traversa, E. Air, aqueous and thermal stabilities of Ce3+ ions in cerium oxide nanoparticle layers with substrates. Nanoscale 2014, 6, 6637–6645.
Naganuma, T.; Traversa, E. The effect of cerium valence states at cerium oxide nanoparticle surfaces on cell proliferation. Biomaterials 2014, 35, 4441–4453.
Vayssieres, L. On the effect of nanoparticle size on water-oxide interfacial chemistry. J. Phys. Chem. C 2009, 113, 4733–4736.
Nolan, M.; Parker, S. C.; Watson, G. W. The electronic structure of oxygen vacancy defects at the low index surfaces of ceria. Surf. Sci. 2005, 595, 223–232.
Chueh, W. C.; McDaniel, A. H.; Grass, M. E.; Hao, Y.; Jabeen, N.; Liu, Z.; Haile, S. M.; McCarty, K. F.; Bluhm, H.; Gabaly, F. E. Highly enhanced concentration and stability of reactive Ce3+ on doped CeO2 surface revealed in operando. Chem. Mater. 2012, 24, 1876–1882.
Sayle, T. X. T.; Inkson, B. J.; Karakoti, A.; Kumar, A.; Molinari, M.; Möbus, G.; Parker, S. C.; Seal, S.; Sayle, D. C. Mechanical properties of ceria nanorods and nanochains; the effect of dislocations, grain-boundaries and oriented attachment. Nanoscale 2011, 3, 1823–1837.
Zhang, F.; Chan, S. W.; Spanier, J. E.; Apak, E.; Jin, Q.; Robinson, R. D.; Herman, I. R. Cerium oxide nanoparticles: Size-selective formation and structure analysis. Appl. Phys. Lett. 2002, 80, 127–129.
Wu, L. J.; Wiesmann, H. J.; Moodenbaugh, A. R.; Klie, R. F.; Zhu, Y. M.; Welch, D. O.; Suenaga, M. Oxidation state and lattice expansion of CeO2–x nanoparticles as a function of particle size. Phys. Rev. B 2004, 69, 125415.
Hailstone, R. K.; DiFrancesco, A. G.; Leong, J. G.; Allston, T. D.; Reed, K. J. A study of lattice expansion in CeO2 nanoparticles by transmission electron microscopy. J. Phys. Chem. C 2009, 113, 15155–15159.
Paun, C.; Safonova, O. V.; Szlachetko, J.; Abdala, P. M.; Nachtegaal, M.; Sa, J.; Kleymenov, E.; Cervellino, A.; Krumeich, F.; van Bokhoven, J. A. Polyhedral CeO2 nanoparticles: Size-dependent geometrical and electronic structure. J. Phys. Chem. C 2012, 116, 7312–7317.
Torrente-Murcianoa, L.; Gilbank, A.; Puertolas, B.; Garcia, T.; Solsona, B.; Chadwick, D. Shape-dependency activity of nanostructured CeO2 in the total oxidation of polycyclic aromatic hydrocarbons. Appl. Catal. B 2013, 132–133, 116–122.
Tana; Zhang, M. L.; Li, J.; Li, H. J.; Li, Y.; Shen, W. J. Morphology-dependent redox and catalytic properties of CeO2 nanostructures: Nanowires, nanorods and nanoparticles. Catal. Today 2009, 148, 179–183.
Ho, C. M.; Yu, J. C.; Kwong, T.; Mak, A. C.; Lai, S. Morphology-controllable synthesis of mesoporous CeO2 nano- and microstructures. Chem. Mater. 2005, 17, 4514–4522.
Tang, B.; Zhuo, L. H.; Ge, J. C.; Wang, G. L.; Shi, Z. Q.; Niu, J. Y. A surfactant-free route to single-crystalline CeO2 nanowires. Chem. Commun. 2005, 3565–3567.
Bugayeva, N.; Robinson, J. Synthesis of hydrated CeO2 nanowires and nanoneedles. Mater. Sci. Technol. 2007, 23, 237–241.
Mandoli, C.; Pagliari, F.; Pagliari, S.; Forte, G.; Di Nardo, P.; Licoccia, S.; Traversa, E. Stem cell aligned growth induced by CeO2 nanoparticles in PLGA scaffolds with improved bioactivity for regenerative medicine. Adv. Funct. Mater. 2010, 20, 1617–1624.
Wang, G. F.; Peng, Q.; Li, Y. D. Lanthanide-doped nanocrystals: Synthesis, optical-magnetic properties, and applications. Acc. Chem. Res. 2011, 44, 322–332.
LaMer, V. K.; Dinegar, R. H. Theory, production and mechanism of formation of monodispersed hydrosols. J. Am. Chem. Soc. 1950, 72, 4847–4854.
Djuričić, B.; Pickering, S. Nanostructured cerium oxide: Preparation and properties of weakly-agglomerated powders. J. Eur. Ceram. Soc. 1999, 19, 1925–1934.
Vincent, A.; Inerbaev, T. M.; Babu, S.; Karakoti, A. S.; Self, W. T.; Masunov, A. E.; Seal, S. Tuning hydrated nanoceria surfaces: Experimental/theoretical investigations of ion exchange and implications in organic and inorganic interactions. Langmuir 2010, 26, 7188–7198.
Acknowledgments
This work was funded by The Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan under the auspices of the WPI Program. Technical support by NIMS Molecule & Material Synthesis Platform in “Nanotechnology Platform Project” operated by MEXT is gratefully acknowledged.
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Naganuma, T. Shape design of cerium oxide nanoparticles for enhancement of enzyme mimetic activity in therapeutic applications. Nano Res. 10, 199–217 (2017). https://doi.org/10.1007/s12274-016-1278-4
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DOI: https://doi.org/10.1007/s12274-016-1278-4