Abstract
Silver nanoparticles (AgNPs) are a potential class of nanomaterial for antibiosis and chemotherapeutic effects against human carcinoma cells. However, the DNA-damaging ability of free AgNPs pose the critical issues in their biomedical applications. Herein, we demonstrated a facile method to capture Ag+ ions and reduce them into active AgNPs within Zr-based metal-organic frameworks (MOFs) of UiO-66 with a mild reductant of DMF (AgNPs@UiO-66(DMF)). The average diameters of UiO-66 carriers and AgNPs were facilely controlled to be 140 and 10 nm, respectively. The obtained UiO-66 nanocarriers exhibited excellent biocompatibility and could be effectively endocytosed by cancer cells. Additionally, the AgNPs@UiO-66(DMF) could rapidly release Ag+ ions and efficiently inhibit the growth of cancer cells. The half maximal inhibitory concentration (IC50) values of the encapsulated AgNPs were calculated to be 2.7 and 2.45 μg mL−1 for SMMC-7721 and HeLa cells, respectively, which were much lower than those of free AgNPs in the reported works. Therefore, the developed AgNPs@UiO-66(DMF) not only maintained the therapeutic effect against cancer cells but also reduced the dosage of free AgNPs in chemotherapy treatment.
A mild reduction process was developed for the fabrication of AgNPs@UiO-66, which exhibited efficient induction of apoptosis in cancer cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmed I, Jhung SH (2015) Effective adsorptive removal of indole from model fuel using a metal-organic framework functionalized with amino groups. J Hazard Mater 283:544–550. https://doi.org/10.1016/j.jhazmat.2014.10.002
Ahamed M, AlSalhi MS, Siddiqui M (2010) Silver nanoparticle applications and human health. Clin Chim Acta 411(23–24):1841–1848. https://doi.org/10.1016/j.cca.2010.08.016
Akhavan O, Abdolahad M, Abdi Y, Mohajerzadeh S (2011) Silver nanoparticles within vertically aligned multi-wall carbon nanotubes with open tips for antibacterial purposes. J Mater Chem 21:387–393. https://doi.org/10.1039/C0JM02395G
AshaRani PV, Low Kah Mun G, Hande MP, Valiyaveettil S (2009) Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano 3:279–290. https://doi.org/10.1021/nn800596w
Barreto JC, Smith GS, Strobel NHP, McQuillin PA, Miller TA (1994) Terephthalic acid: a dosimeter for the detection of hydroxyl radicals in vitro. Life Sci 56:PL89–PL96. https://doi.org/10.1016/0024-3205(94)00925-2
Cavka JH, Jakobsen S, Olsbye U, Guillou N, Lamberti C, Bordiga S, Lillerud KP (2008) A new zirconium inorganic building brick forming metal organic frameworks with exceptional stability. J Am Chem Soc 130(42):13850–13851. https://doi.org/10.1021/ja8057953
Chen X, Huang X, Zheng C, Liu Y, Xu T, Liu J (2015) Preparation of different sized nano-silver loaded on functionalized graphene oxide with highly effective antibacterial properties. J Mater Chem B 3:7020–7029. https://doi.org/10.1039/C5TB00280J
Chen X-C, Tao T, Wang Y-G, Peng Y-X, Huang W, Qian H-F (2012) Azo-hydrazone tautomerism observed from UV-vis spectra by pH control and metal-ion complexation for two heterocyclic disperse yellow dyes. Dalton Trans 41:11107–11115. https://doi.org/10.1039/C2DT31102J
Chernousova S, Epple M (2013) Silver as antibacterial agent: ion, nanoparticle, and metal. Angew Chem Int Ed 52(6):1636–1653. https://doi.org/10.1002/anie.201205923
Deng K, Hou Z, Li X, Li C, Zhang Y, Deng X, Cheng Z, Lin J (2015) Aptamer-mediated up-conversion core/MOF shell nanocomposites for targeted drug delivery and cell imaging. Sci Rep 5(7851). https://doi.org/10.1038/srep07851
Ehdaie B (2007) Application of nanotechnology in cancer research: review of progress in the National Cancer Institute’s Alliance for Nanotechnology. Int J Biol Sci 3(2):108–110
Feng Q, Wu J, Chen G, Cui F, Kim T, Kim J (2000) A mechanistic study of the antibacterial effect of silver ions on Escherichia coli and Staphylococcus aureus. J Biomed Mater Res 52(4):662–668
Férey G (2008) Hybrid porous solids: past, present, future. Chem Soc Rev 37(1):191–214. https://doi.org/10.1039/B618320B
Ferrari M (2005) Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer 5:161–171. https://doi.org/10.1038/nrc1566
Foldbjerg R, Dang DA, Autrup H (2011) Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch Toxicol 85(7):743–750. https://doi.org/10.1007/s00204-010-0545-5
Gong C, Shen Y, Chen J, Song Y, Chen S, Song Y, Wang L (2017) Microperoxidase-11@PCN-333 (Al)/three-dimensional macroporous carbon electrode for sensing hydrogen peroxide. Sens Actuators, B: Chemical 239:890–897. https://doi.org/10.1016/j.snb.2016.08.108
Gopinath P, Gogoi SK, Sanpui P, Paul A, Chattopadhyay A, Ghosh SS (2010) Signaling gene cascade in silver nanoparticle induced apoptosis. Colloids Surf, B 77(2):240–245. https://doi.org/10.1016/j.colsurfb.2010.01.033
Gurunathan S, Han JW, Dayem AA, Eppakayala V, Park JH, Cho SG, Lee KJ, Kim JH (2013) Green synthesis of anisotropic silver nanoparticles and its potential cytotoxicity in human breast cancer cells (MCF-7). J Ind Eng Chem 19:1600–1605. https://doi.org/10.1016/j.jiec.2013.01.029
He Y, du, Tang, Zheng, Zhang, Zhao, Lv, Qianfa J (2013) Green synthesis of silver nanoparticles by Chrysanthemum morifolium Ramat. Extract and their application in clinical ultrasound gel. Int J Nanomedicine 8:1809–1815. https://doi.org/10.2147/IJN.S43289
Hsin Y-H, Chen C-F, Huang S, Shih T-S, Lai P-S, Chueh PJ (2008) The apoptotic effect of nanosilver is mediated by a ROS-and JNK-dependent mechanism involving the mitochondrial pathway in NIH3T3 cells. Toxicol Lett 179(3):130–139. https://doi.org/10.1016/j.toxlet.2008.04.015
Igaz N, Kovács D, Rázga Z, Kónya Z, Boros IM, Kiricsi M (2016) Modulating chromatin structure and DNA accessibility by deacetylase inhibition enhances the anti-cancer activity of silver nanoparticles. Colloids Surf B: Biointerfaces 146:670–677. https://doi.org/10.1016/j.colsurfb.2016.07.004
Jeyaraj M, Rajesh M, Arun R, MubarakAli D, Sathishkumar G, Sivanandhan G, Dev GK, Manickavasagam M, Premkumar K, Thajuddin N, Ganapathi A (2013) An investigation on the cytotoxicity and caspase-mediated apoptotic effect of biologically synthesized silver nanoparticles using Podophyllum hexandrum on human cervical carcinoma cells. Colloids Surf B 102:708–717. https://doi.org/10.1016/j.colsurfb.2012.09.042
Jose Ruben M, Jose Luis E, Alejandra C, Katherine H, Juan BK, Jose Tapia R, Miguel Jose Y (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16(10):2346–2353
Kathiravan V, Ravi S, Ashokkumar S (2014) Synthesis of silver nanoparticles from Melia dubia leaf extract and their in vitro anticancer activity. Spectrochim Acta A 130(15):116–121. https://doi.org/10.1016/j.saa.2014.03.107
Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3(1):95–101. https://doi.org/10.1016/j.nano.2006.12.001
Kim J, Yeo S, Jeon J-D, Kwak S-Y (2015) Enhancement of hydrogen storage capacity and hydrostability of metal–organic frameworks (MOFs) with surface-loaded platinum nanoparticles and carbon black. Microporous Mesoporous Mater 202:8–15. https://doi.org/10.1016/j.micromeso.2014.09.025
Kitagawa S, Kitaura R, Si N (2004) Functional porous coordination polymers. Angew Chem Int Ed 43(18):2334–2375. https://doi.org/10.1002/anie.200300610
Kovács D, Szőke K, Igaz N, Spengler G, Molnár J, Tóth T, Madarász D, Rázga Z, Kónya Z, Boros IM, Kiricsi M (2016) Silver nanoparticles modulate ABC transporter activity and enhance chemotherapy in multidrug resistant cancer. Nanomedicine 12:601–610. https://doi.org/10.1016/j.nano.2015.10.015
Liu J, Sonshine DA, Shervani S, Hurt RH (2010) Controlled release of biologically active silver from nanosilver surfaces. ACS Nano 4:6903–6913. https://doi.org/10.1021/nn102272n
Manikandan R, Manikandan B, Raman T, Arunagirinathan K, Prabhu NM, Jothi Basu M, Perumal M, Palanisamy S, Munusamy A (2015) Biosynthesis of silver nanoparticles using ethanolic petals extract of Rosa indica and characterization of its antibacterial, anticancer and anti-inflammatory activities. Spectrochim Acta A 138:120–129. https://doi.org/10.1016/j.saa.2014.10.043
Marudhupandi T, Ajith Kumar TT, Lakshmanasenthil S, Suja G, Vinothkumar T (2015) In vitro anticancer activity of fucoidan from Turbinaria conoides against A549 cell lines. Int J Biol Macromol 72:919–923. https://doi.org/10.1016/j.ijbiomac.2014.10.005
Orellana-Tavra C, Baxter EF, Tian T, Bennett TD, Slater NK, Cheetham AK, Fairen-Jimenez D (2015) Amorphous metal–organic frameworks for drug delivery. Chem Commun 51(73):13878–13881. https://doi.org/10.1039/C5CC05237H
Pu S, Xu L, Sun L, Du H (2015) Tuning the optical properties of the zirconium–UiO-66 metal–organic framework for photocatalytic degradation of methyl orange Inorg. Chem Commun 52:50–52. https://doi.org/10.1016/j.inoche.2014.12.015
Sanpui P, Chattopadhyay A, Ghosh SS (2011) Induction of apoptosis in cancer cells at low silver nanoparticle concentrations using chitosan nanocarrier. ACS Appl Mater Interfaces 3(2):218–228. https://doi.org/10.1021/am100840c
Sarkar K, Banerjee SL, Kundu PP, Madras G, Chatterjee K (2015) Biofunctionalized surface-modified silver nanoparticles for gene delivery. J Mat Chem B 3(26):5266–5276. https://doi.org/10.1039/C5TB00614G
Schaate A, Roy P, Godt A, Lippke J, Waltz F, Wiebcke M, Behrens P (2011) Modulated synthesis of Zr-based metal–organic frameworks: from nano to single crystals. ChemEur J 17(24):6643–6651. https://doi.org/10.1002/chem.201003211
Shen L, Liang R, Luo M, Jing F, Wu L (2015) Electronic effects of ligand substitution on metal-organic framework photocatalysts: the case study of UiO-66 Phys. Chem Chem Phys 17:117–121. https://doi.org/10.1039/C4CP04162C
Sen Karaman D et al (2016) Shape engineering boosts antibacterial activity of chitosan coated mesoporous silica nanoparticle doped with silver: a mechanistic investigation. J Mat Chem B 4(19):3292–3304. https://doi.org/10.1039/C5TB02526E
Singh RP, Ramarao P (2012) Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles. Toxicol Lett 213:249–259. https://doi.org/10.1016/j.toxlet.2012.07.009
Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci 275(1):177–182. https://doi.org/10.1016/j.jcis.2004.02.012
Song Y, Chen J, Liu H, Song Y, Xu F, Tan H, Wang L (2015a) Conformation, bioactivity and electrochemical performance of glucose oxidase immobilized on surface of gold nanoparticles. Electrochim Acta 158:56–63. https://doi.org/10.1016/j.electacta.2015.01.114
Song Y, Wei C, He J, Li X, Lu X, Wang L (2015b) Porous co nanobeads/rGO nanocomposites derived from rGO/co-metal organic frameworks for glucose sensing. Sensors Actuators B 220:1056–1063. https://doi.org/10.1016/j.snb.2015.06.052
Sotiriou GA, Pratsinis SE (2010) Antibacterial activity of nanosilver ions and particles. Environ Sci Technol 44:5649–5654. https://doi.org/10.1021/es101072s
Sriram MI, Kanth SBM, Kalishwaralal K, Gurunathan S (2010) Antitumor activity of silver nanoparticles in Dalton’s lymphoma ascites tumor model. Int J Nanomedicine 5:753–762. https://doi.org/10.2147/IJN.S11727
Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267(5203):1456–1462. https://doi.org/10.1126/science.7878464
Wang J, Chen D, Li B, He J, Duan D, Shao D, Nie M (2016) Fe-MIL-101 exhibits selective cytotoxicity and inhibition of angiogenesis in ovarian cancer cells via downregulation of MMP. Sci Rep 6:26126. https://doi.org/10.1038/srep26126
Wei L, Lu J, Xu H, Patel A, Chen Z-S, Chen G (2015) Silver nanoparticles: synthesis, properties, and therapeutic applications. Drug Discov Today 20(5):595–601. https://doi.org/10.1016/j.drudis.2014.11.014
Xia QH, Ma YJ, Wang JW (2016) Biosynthesis of silver nanoparticles using Taxus yunnanensis Callus and their antibacterial activity and cytotoxicity in human cancer cells. Nano 6(9):160. https://doi.org/10.3390/nano6090160
Xiong R, Lu C, Wang Y, Zhou Z, Zhang X (2013) Nanofibrillated cellulose as the support and reductant for the facile synthesis of Fe3O4/Ag nanocomposites with catalytic and antibacterial activity. J Mat Chem A 1(47):14910–14918. https://doi.org/10.1039/C3TA13314A
Xiu Z-m, Zhang Q-b, Puppala HL, Colvin VL, Alvarez PJ (2012) Negligible particle-specific antibacterial activity of silver nanoparticles. Nano Lett 12(8):4271–4275. https://doi.org/10.1021/nl301934w
Xu W-X, Li J, Liu R-P, Zhou W-X, Ma W-Y, Zhang F-X (2013) A novel 1D linear zinc(II) coordination polymer based 2, 2′-bipyridine-4, 4′-dicarboxylic acid: synthesis, crystal structure and photoluminescence property. Inorganic Chem Commun 28:12–15. https://doi.org/10.1016/j.inoche.2012.11.008
Yaghi OM, O'Keeffe M, Ockwig NW, Chae HK, Eddaoudi M, Kim J (2003) Reticular synthesis and the design of new materials. Nature 423:705–714. https://doi.org/10.1038/nature01650
Yang J, Chen X, Li Y, Zhuang Q, Liu P, Gu J (2017a) Zr-based MOFs shielded with phospholipid bilayers: improved biostability and cell uptake for biological applications. Chem Mater 29(10):4580–4589. https://doi.org/10.1021/acs.chemmater.7b01329
Yang X, Li L, He D, Hai L, Tang J, Li H, He X, Wang K (2017b) A metal-organic framework based nanocomposite with co-encapsulation of Pd@Au nanoparticles and doxorubicin for pH- and NIR-triggered synergistic chemo-photothermal treatment of cancer cells. J Mater Chem B 5(24):4648–4659. https://doi.org/10.1039/C7TB00715A
Yezhelyev MV, Gao X, Xing Y, Al-Hajj A, Nie S, O'Regan RM (2006) Emerging use of nanoparticles in diagnosis and treatment of breast cancer. The Lancet Oncology 7:657–667. https://doi.org/10.1016/S1470-2045(06)70793-8
Wang H, Yuan X, Zeng G, Wu Y, Liu Y, Jiang Q, Gu S (2015) Three dimensional graphene based materials: synthesis and applications from energy storage and conversion to electrochemical sensor and environmental remediation. Adv Colloid Interf Sci 221:41–59. https://doi.org/10.1016/j.cis.2015.04.005
Wang S, Li G, Huo Q, Liu Y (2013) Syntheses, crystal structures of two coordination polymers constructed from imidazole-based dicarboxylate ligands containing alkyl group. Inorg Chem Commun 30:115–119. https://doi.org/10.1016/j.inoche.2013.01.005
Zhan H, Zhou X, Cao Y, Jagtiani T, Chang T-L, Liang JF (2017) Anti-cancer activity of camptothecin nanocrystals decorated by silver nanoparticles. J Mater Chem B 5(14):2692–2701. https://doi.org/10.1039/C7TB00134G
Zhang Z, Miao L, Lv C, Sun H, Wei S, Wang B, Huang C, Jiao B (2013) Wentilactone B induces G2/M phase arrest and apoptosis via the Ras/Raf/MAPK signaling pathway in human hepatoma SMMC-7721 cells. Cell Death & Dis 4(6):e657. https://doi.org/10.1038/cddis.2013.182
Zhao H-X, Zou Q, Sun S-K, Yu C, Zhang X, Li R-J, Fu Y-Y (2016) Theranostic metal-organic framework core-shell composites for magnetic resonance imaging and drug delivery. Chem Sci 7(8):5294–5301. https://doi.org/10.1039/C6SC01359G
Zhu X, Gu J, Wang Y, Li B, Li Y, Zhao W, Shi J (2014) Inherent anchorages in UiO-66 nanoparticles for efficient capture of alendronate and its mediated release. Chem Commun 50(63):8779–8782. https://doi.org/10.1039/C4CC02570A
Acknowledgments
This work was financially supported by the Natural Science Foundation of China (51072053, 51372084), the Innovation Program of Shanghai Municipal Education Commission (13zz040), the Nano-Special Foundation for Shanghai Committee of Science and Technology (12 nm0502600), and the 111 Project (B14018).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interest.
Electronic supplementary material
ESM 1
TEM images, Nitrogen adsorption-desorption isotherms, Fluorescence spectra, Flow cytometric analysis, EDS spectrum, Confocal images and the cumulate release profile of Ag+, Table S1 and Table S2. (DOCX 1344 kb)
Rights and permissions
About this article
Cite this article
Han, C., Yang, J. & Gu, J. Immobilization of silver nanoparticles in Zr-based MOFs: induction of apoptosis in cancer cells. J Nanopart Res 20, 77 (2018). https://doi.org/10.1007/s11051-018-4187-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11051-018-4187-5