Abstract
Overproduction of reactive oxygen species (ROS) is an unwanted phenomenon, leading to cellular damages. The aim of this study was to investigate the ability of neat and surface-modified iron oxide nanoparticles (IONs) to eliminate ROS produced by immune cells. The employed coating included heparin (ION@Hep) or heparin and chitosan grafted with phenolic compounds famous for antioxidant properties, i.e., gallic acid (ION@Ch-G) or phloroglucinol (ION@CH-P). A total peroxyl radical-trapping potential assay showed that both types of the phenolic compounds-modified IONs exhibited superior radical scavenging activity over the neat and ION@Hep particles at 100 μg/mL. Up to ~ 75 μg/mL, the particles were non-toxic towards RAW 264.7 macrophages. Capability of the particles to limit ROS production was investigated in vitro on polymorphonuclear (PMN) cells isolated from human whole blood and expressed as an ability to reduce the oxidative burst in the stimulated cells, as well as a potential to increase the viability of bacteria cultivated with the PMN cells. The highest viability of bacteria was observed for the neat and ION@Ch-G, while the ION@Ch-G particles also the most effectively inhibited the oxidative burst. The results indicated that ROS scavenging depend on the presence of polymer and selection of phenols, enriching the IONs.
Similar content being viewed by others
Data Availability
The data that support the findings of this study are available from the corresponding author, MŚ, upon reasonable request.
Code Availability
Not applicable.
References
J. K. Patra, G. Das, L. F. Fraceto, E. V. R. Campos, M. del Pilar Rodriguez Torres, L. S. Acosta-Torres, L. A. Diaz-Torres, R. Grillo, M. K. Swamy, S. Sharma, S. Habtemariam, and H.-S. Shin (2018). J. Nanobiotechnol. 16, 71. https://doi.org/10.1186/s12951-018-0392-8.
X. Han, K. Xu, O. Taratula, and K. Farsad (2019). Nanoscale 11, 799. https://doi.org/10.1039/C8NR07769J.
S. van Rijt and P. Habibovic (2017). J. R. Soc. Interface 14, 20170093. https://doi.org/10.1098/rsif.2017.0093.
C.-Y. Zhao, R. Cheng, Z. Yang, and Z.-M. Tian (2018). Molecules 23, 826. https://doi.org/10.3390/molecules23040826.
V. F. Cardoso, A. Francesko, C. Ribeiro, M. Bañobre-López, P. Martins, and S. Lanceros-Mendez (2018). Adv. Healthc. Mater. 7, 1700845. https://doi.org/10.1002/adhm.201700845.
J. Kudr, Y. Haddad, L. Richtera, Z. Heger, M. Cernak, V. Adam, and O. Zitka (2017). Nanomaterials 7, 243. https://doi.org/10.3390/nano7090243.
D. Lachowicz, W. Górka, A. Kmita, A. Bernasik, J. Żukrowski, W. Szczerba, M. Sikora, C. Kapusta, and S. Zapotoczny (2019). J. Mater. Chem. B 7, 2962–2973. https://doi.org/10.1039/C9TB00029A.
L. Yang, L. Ma, J. Xin, A. Li, C. Sun, R. Wei, B. W. Ren, Z. Chen, H. Lin, and J. Gao (2017). Chem. Mater. 29, 3038–3047. https://doi.org/10.1021/acs.chemmater.7b00035.
H. Zeng, J. Li, Z. L. Wang, J. P. Liu, and S. Sun (2004). Nano Lett. 4, 187–190. https://doi.org/10.1021/nl035004r.
E. A. Kwizera, E. Chaffin, Y. Wang, and X. Huang (2017). RSC Adv. 7, 17137–17153. https://doi.org/10.1039/C7RA01224A.
S. M. Dadfar, K. Roemhild, N. I. Drude, S. von Stillfried, R. Knüchel, F. Kiessling, and T. Lammers (2019). Adv. Drug Deliv. Rev. 138, 302. https://doi.org/10.1016/j.addr.2019.01.005.
A. L. Cortajarena, D. Ortega, S. M. Ocampo, A. Gonzalez-García, P. Couleaud, R. Miranda, C. Belda-Iniesta, and A. Ayuso-Sacido (2014). Nanomedicine 1, 1. https://doi.org/10.5772/58841.
G. Jarockyte, E. Daugelaite, M. Stasys, U. Statkute, V. Poderys, T.-C. Tseng, S.-H. Hsu, V. Karabanovas, and R. Rotomskis (2016). Int. J. Mol. Sci. 17, 1193. https://doi.org/10.3390/ijms17081193.
P. Mathieu, Y. Coppel, M. Respaud, Q. T. Nguyen, S. Boutry, S. Laurent, D. Stanicki, C. Henoumont, F. Novio, J. Lorenzo, D. Motpeyó, and C. Amiens (2019). Molecules 24, 4629. https://doi.org/10.3390/molecules24244629.
Y. Wu, Z. Lu, Y. Li, J. Yang, and X. Zhang (2020). Nanomaterials 10, 1441. https://doi.org/10.3390/nano10081441.
L. M. Armijo, S. J. Wawrzyniec, M. Kopciuch, Y. I. Brand, A. C. Rivera, N. J. Withers, N. C. Cook, D. L. Huber, T. C. Monson, H. Smyth, and M. Osiński (2020). J. Nanobiotechnol. 18, 35. https://doi.org/10.1186/s12951-020-0588-6.
D. Zhao, S. Yu, B. Sun, S. Gao, S. Guo, and K. Zhao (2018). Polymers 10, 462. https://doi.org/10.3390/polym10040462.
M. A. Matica, F. L. Aachmann, A. Tøndervik, H. Sletta, and V. Ostage (2019). Int. J. Mol. Sci. 20, 5889. https://doi.org/10.3390/ijms20235889.
J. Liu, G. Pu, S. Liu, J. Kan, and C. Jin (2017). Carbohydr. Polym. 174, 999–1017. https://doi.org/10.1016/j.carbpol.2017.07.014.
C. A. Prauchner (2017). Burns 43, 471. https://doi.org/10.1016/j.burns.2016.09.023.
J. Roy, J. M. Galano, T. Durand, J. T. Le Guennec, and J. C. Lee (2017). FASEB J. 31, 3729–3745. https://doi.org/10.1096/fj.201700170R.
M. Świętek, Y.-C. Lu, R. Konefał, L. P. Ferreira, M. M. Cruz, Y.-H. Ma, and D. Horák (2019). Beilstein J. Nanotechnol. 10, 1073. https://doi.org/10.3762/bjnano.10.108.
W. Kim, C.-Y. Suh, S.-W. Cho, K.-M. Roh, H. Kwon, K. Song, and I.-J. Shon (2012). Talanta 94, 348. https://doi.org/10.1016/j.talanta.2012.03.001.
M. A. Legodi and D. de Waal (2007). Dyes Pigm. 74, 161. https://doi.org/10.1016/j.dyepig.2006.01.038.
O. N. Shebanova and P. Lazor (2003). J. Raman Spectrosc. 34, 845. https://doi.org/10.1002/jrs.1056.
L. Slavov, M. V. Abrashev, T. Merodiiska, C. Gelev, R. E. Vandenberghe, I. Markova-Deneva, and I. Nedkov (2010). J. Magn. Magn. Mater. 322, 1904. https://doi.org/10.1016/j.jmmm.2010.01.005.
A. M. Jubb and H. C. Allen (2010). ACS Appl. Mater. Interface 2, 2804. https://doi.org/10.1021/am1004943.
M. Hanesch (2009). Geophys. J. Int. 177, 941. https://doi.org/10.1111/j.1365-246X.2009.04122.x.
S. T. Shah, W. A. Yehya, O. Saad, K. Simarani, Z. Chowdhury, A. A. Alhadi, and L. A. Al-Ani (2017). Nanomaterials 7, 306. https://doi.org/10.3390/nano7100306.
A. M. Pisoschi and G. P. Negulescu (2011). Biochem. Anal. Biochem. 1, 106. https://doi.org/10.4172/2161-1009.1000106.
K. J. Patra, S. Ali, I.-G. Oh, and K.-H. Baek (2016). Artif. Cell. Nanomed. Biotechnol. 45, 349. https://doi.org/10.3109/21691401.2016.1153484.
H. Wu, J.-J. Yin, W. G. Wamer, M. Zeng, and Y. M. Lo (2014). J. Food Drug Anal. 22, 86. https://doi.org/10.1016/j.jfda.2014.01.007.
F. Yu, Y. Huang, A. J. Cole, and V. C. Yang (2009). Biomaterials 30, 4716. https://doi.org/10.1016/j.biomaterials.2009.05.005.
E. Fröhlich (2012). Int. J. Nanomed. 7, 5577. https://doi.org/10.2147/IJN.S36111.
M. A. Voinov, J. O. S. Pagán, E. Morrison, T. I. Smirnova, and A. I. Smirnov (2011). J. Am. Chem. Soc. 133, 35. https://doi.org/10.1021/ja104683w.
L. S. Arias, J. P. Pessan, A. P. M. Vieira, T. M. Toito de Lima, A. C. B. Delbem, and D. R. Monteiro (2018). Antibiotics 7, 46. https://doi.org/10.3390/antibiotics7020046.
O. Lunov, T. Syrovets, B. Büchele, X. Jiang, C. Röcker, K. Tron, G. U. Nienhaus, P. Walther, V. Mailänder, K. Landfester, and T. Simmet (2010). Biomaterials 31, 5063. https://doi.org/10.1016/j.biomaterials.2010.03.023.
N. S. Ghandi and R. L. Mancera (2008). Chem. Biol. Drug Des. 72, 455. https://doi.org/10.1111/j.1747-0285.2008.00741.x.
L. Ternent, D. A. Mayoh, M. R. Lees, and G.-L. Davies (2016). J. Mater. Chem. B 4, 3065. https://doi.org/10.1039/C6TB00832A.
S. Shukla, A. Jadaun, V. Arora, R. K. Sinha, N. Biyani, and V. K. Jain (2015). Toxicol. Rep. 2, 27. https://doi.org/10.1016/j.toxrep.2014.11.002.
G. Cairo, S. Recalcati, A. Mantovani, and M. Locati (2011). Trends Immunol. 32, 241. https://doi.org/10.1016/j.it.2011.03.007.
A. Laskar, J. Eilertsen, W. Li, and X.-M. Yuan (2013). Biochem. Biophys. Res. Commun. 441, 737. https://doi.org/10.1016/j.bbrc.2013.10.115.
J. M. Rojas, L. Sanz-Ortega, V. Mulens-Arias, L. Gutiérrez, S. Pérez-Yagüe, and D. F. Barber (2016). Nanomed. Nanotechnol. 12, 1127–1138. https://doi.org/10.1016/j.nano.2015.11.020.
D. Gonnissen, Y. Qu, K. Langer, C. Öztürk, Y. Zhao, C. Chen, G. Seebohm, M. Düfer, H. Fuchs, H.-J. Galla, and K. Riehemann (2016). Int. J. Nanomed. 11, 5221. https://doi.org/10.2147/IJN.S106540.
O. M. Ighodaro (2018). Biomed. Pharmacol. 108, 656. https://doi.org/10.1016/j.biopha.2018.09.058.
C. N. Paiva and M. T. Bozza (2014). Antioxid. Redox Signal. 20, 1000. https://doi.org/10.1089/ars.2013.5447.
Z. Chen, J.-J. Yin, Y.-T. Zhou, Y. Zhang, L. Song, M. Song, S. Hu, and N. Gu (2012). ACS Nano 6, 4001. https://doi.org/10.1021/nn300291r.
R. Castañeda-Arriaga, A. Pérez-González, M. Reina, J. R. Alvarez-Idaboy, and A. Galano (2018). J. Phys. Chem. B 122, 6198. https://doi.org/10.1021/acs.jpcb.8b03500.
Funding
This study was supported by the Czech Science Foundation No. 20-02177J. The Polish authors thank the EU Project POWR.03.02.00-00-I004/16.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Świętek, M., Gunár, K., Kołodziej, A. et al. Surface Effect of Iron Oxide Nanoparticles on the Suppression of Oxidative Burst in Cells. J Clust Sci 34, 323–334 (2023). https://doi.org/10.1007/s10876-022-02222-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10876-022-02222-9