The cell membrane as the barrier in the defense against nanoxenobiotics: Zinc oxide nanoparticles interactions with native and model membrane of melanoma cells.
cytotoxicity
melanoma
model membrane
zinc oxide
Journal
Journal of applied toxicology : JAT
ISSN: 1099-1263
Titre abrégé: J Appl Toxicol
Pays: England
ID NLM: 8109495
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
revised:
01
06
2021
received:
09
04
2021
accepted:
17
06
2021
pubmed:
9
7
2021
medline:
16
2
2022
entrez:
8
7
2021
Statut:
ppublish
Résumé
Currently, we are dealing with ever-increasing pollution of the environment with metal and metal oxide nanoparticles. One type of these, zinc oxide nanoparticles (ZnO-NPs), are increasingly used in areas such as cosmetology, electrical engineering, medicine, and even in the food and textile industries. As a consequence, ZnO-NPs may enter the human body in many ways. Their influence on the body is still not clear. Here, we define the mechanism of the initial toxicity of ZnO-NPs to cells based on interaction with the lipid part of the native and model cell membrane. The selected cell lines react differently to contact with nanoparticles. We found a disruption of the native membranes of B16-F0 cells and to a lesser extent of COLO 679. In turn, the membrane of COLO 679 cells was more peroxidated, and cell viability was much lower. A model of the lipid part of the membrane was created for B16-F0 cells and compared with previously published studies on immune cells. On the basis of physicochemical parameters obtained for individual lipids and a mix representing the native membrane of the tested cells, we concluded that exposure to nanoparticles resulted in a change within the model membranes (specifically with the polar parts of lipids). The greatest interaction has been noticed between ZnO-NPs and zwitterionic phospholipids (PC and PE), cholesterol, and negatively charged phosphatidylglycerol. Assessing the interactions between the membrane and nanoparticles will help to better understand the first steps of its toxicity mechanism.
Substances chimiques
Zinc Oxide
SOI2LOH54Z
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
334-341Informations de copyright
© 2021 John Wiley & Sons, Ltd.
Références
Angelikopoulos, P., Sarkisov, L., Cournia, Z., & Gkeka, P. (2017). Self-assembly of anionic, ligand-coated nanoparticles in lipid membranes. Nanoscale, 9(3), 1040-1048. https://doi.org/10.1039/C6NR05853A
Athukorala, Y., Ahn, G. N., Jee, Y.-H., Kim, G.-Y., Kim, S.-H., Ha, J.-H., … Jeon, Y.-J. (2009). Antiproliferative activity of sulfated polysaccharide isolated from an enzymatic digest of Ecklonia cava on the U-937 cell line. Journal of Applied Phycology, 21, 307-314. https://doi.org/10.1007/s10811-008-9368-7
Baek, M., Chung, H.-E., Yu, J., Lee, J.-A., Kim, T.-H., Oh, J.-M., … Choi, S.-J. (2012). Pharmacokinetics, tissue distribution, and excretion of zinc oxide nanoparticles. International Journal of Nanomedicine, 7, 3081-3097. https://doi.org/10.2147/IJN.S32593
Barbasz, A., Kreczmer, B., Dyba, B., Filek, M., & Rudolphi-Szydło, E. (2016). The direct action of hyaluronic acid on human U-937 and HL-60 cells-Modification of native and model membranes. Biologia, 71, 1304-1314. https://doi.org/10.1515/biolog-2016-0157
Brown, D., Donaldson, K., & Stone, V. (2004). Effects of PM10 in human peripheral blood monocytes and J774 macrophages. Respiratory Research, 5, 29. https://doi.org/10.1186/1465-9921-5-29
Buschiazzo, J., Ialy-Radio, C., Auer, J., Wolf, J.-P., Serres, C., Lefèvre, B., & Ziyyat, A. (2013). Cholesterol depletion disorganizes oocyte membrane rafts altering mouse fertilization. PLoS ONE, 8, e62919. https://doi.org/10.1371/journal.pone.0062919
Cevc, G. (1990). Membrane electrostatics. Biochimica et Biophysica Acta, 1031(3), 311-382. https://doi.org/10.1016/0304-4157(90)90015-5
Chen, K. L., & Bothun, G. D. (2014). Nanoparticles meet cell membranes: Probing nonspecific interactions using model membranes. Environmental Science & Technology, 48, 873-880. https://doi.org/10.1021/es403864v
Costin, I. S., & Barnes, G. T. (1975). Two-component monolayers. II. Surface pressure-area relations for the octadecanol-docosyl sulphate system. Journal of Colloid and Interface Science, 51, 106-121. https://doi.org/10.1016/0021-9797(75)90088-0
Czyżowska, A., & Barbasz, A. (2020a). A review: Zinc oxide nanoparticles-Friends or enemies? International Journal of Environmental Health Research, 1-17. https://doi.org/10.1080/09603123.2020.1805415
Czyżowska, A., & Barbasz, A. (2020b). Cytotoxicity of zinc oxide nanoparticles to innate and adaptive human immune cells. Journal of Applied Toxicology, 1-13. https://doi.org/10.1002/jat.4133
Czyżowska, A., Dyba, B., Rudolphi-Szydło, E., & Barbasz, A. (2020). Structural and biochemical modifications of model and native membranes of human immune cells in response to the action of zinc oxide nanoparticles. Journal of Applied Toxicology, 41(3), 458-469. https://doi.org/10.1002/jat.4057
Dyba, B., Rudolphi-Szydło, E., Barbasz, A., Czyżowska, A., Hus, K., Petrilla, V., … Bocian, A. (2021). Effects of 3FTx protein fraction from Naja ashei venom on the model and native membranes: Recognition and implications for the mechanisms of toxicity. Molecules, 26, 2164. https://doi.org/10.3390/molecules26082164
Edidin, M. (2003). Lipids on the frontier: A century of cell-membrane bilayers. Nature Reviews Molecular Cell Biology, 4(5), 414-418. https://doi.org/10.1038/nrm1102
Flasiński, M., Hąc-Wydro, K., Wydro, P., & Dynarowicz-Łątka, P. (2014). Influence of platelet-activating factor, lyso-platelet-activating factor and edelfosine on Langmuir monolayers imitating plasma membranes of cell lines differing in susceptibility to anti-cancer treatment: The effect of plasmalogen level. Journal of the Royal Society Interface, 11, 20131103. https://doi.org/10.1098/rsif.2013.1103
Gao, H., & He, Q. (2014). The interaction of nanoparticles with plasma proteins and the consequent influence on nanoparticles behavior. Expert Opinion on Drug Delivery, 11(3), 409-420. https://doi.org/10.1517/17425247.2014.877442
Gkeka, P., Angelikopoulos, P., Sarkisov, L., & Cournia, Z. (2014). Membrane partitioning of anionic, ligand-coated nanoparticles is accompanied by ligand snorkeling, local disordering, and cholesterol depletion. PLoS Computational Biology, 10(12), e1003917. https://doi.org/10.1371/journal.pcbi.1003917
Gong, K., Feng, S.-S., Go, M. L., & Soew, P. H. (2002). Effects of pH on the stability and compressibility of DPPC/cholesterol monolayers at the air-water interface. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 207, 113-125. https://doi.org/10.1016/S0927-7757(02)00043-2
Guttà, C., Rahman, A., Aura, C., Dynoodt, P., Charles, E. M., Hirschenhahn, E., … Rehm, M. (2020). Low expression of pro-apoptotic proteins Bax, Bak and Smac indicates prolonged progression-free survival in chemotherapy-treated metastatic melanoma. Cell Death & Disease, 11(2), 1-12. https://doi.org/10.1038/s41419-020-2309-3
Hąc-Wydro, K., & Dynarowicz-Łątka, P. (2008). Biomedical applications of the Langmuir monolayer technique. Annales Universitatis Mariae Curie-Skłodowska, sectio AA - Chemia, 63, 47-60. https://doi.org/10.2478/v10063-008-0027-2
Jiang, Y.-S., Jin, Z.-X., Umehara, H., & Ota, T. (2010). Cholesterol-dependent induction of dendrite formation by ginsenoside Rh2 in cultured melanoma cells. International Journal of Molecular Medicine, 26, 787-793. https://doi.org/10.3892/ijmm-00000526
Jun, H.-S., Park, T., Lee, C. K., Kang, M. K., Park, M. S., Kang, H. I., … Kim, O. H. (2007). Capsaicin induced apoptosis of B16-F10 melanoma cells through down-regulation of Bcl2. Food and Chemical Toxicology: An International Journal Published for the British Industrial Biological Research Association, 45(5), 708-715. https://doi.org/10.1016/j.fct.2006.10.011
Kohli, A. K., & Alpar, H. O. (2004). Potential use of nanoparticles for transcutaneous vaccine delivery: Effect of particle size and charge. International Journal of Pharmaceutics, 275(1-2), 13-17. https://doi.org/10.1016/j.ijpharm.2003.10.038
Ładniak, A., Jurak, M., & Wiącek, A. E. (2019). Langmuir monolayer study of phospholipid DPPC on the titanium dioxide-chitosan-hyaluronic acid subphases. Adsorption, 25(3), 469-476. https://doi.org/10.1007/s10450-019-00037-1
Larpin, Y., Besançon, H., Babiychuk, V. S., Babiychuk, E. B., & Köffel, R. (2021). Small pore-forming toxins different membrane area binding and Ca2+ permeability of pores determine cellular resistance of monocytic cells. Toxins (Basel), 13. https://doi.org/10.3390/toxins13020126
Leroueil, P. R., Berry, S. A., Duthie, K., Han, G., Rotello, V. M., McNerny, D. Q., … Holl, M. M. B. (2008). Wide varieties of cationic nanoparticles induce defects in supported lipid bilayers. Nano Letters, 8, 420-424. https://doi.org/10.1021/nl0722929
Maksoudian, C., Saffarzadeh, N., Hesemans, E., Dekoning, N., Buttiens, K., & Soenen, S. J. (2020). Role of inorganic nanoparticle degradation in cancer therapy. Nanoscale Advances, 2, 3734-3763. https://doi.org/10.1039/D0NA00286K
Marsh, D. (1996). Lateral pressure in membranes. Biochimica et Biophysica Acta, 1286, 183-223. https://doi.org/10.1016/s0304-4157(96)00009-3
Maurer-Jones, M. A., Gunsolus, I. L., Murphy, C. J., & Haynes, C. L. (2013). Toxicity of engineered nanoparticles in the environment. Analytical Chemistry, 85(6), 3036-3049. https://doi.org/10.1021/ac303636s
McLaughlin, S. (1989). The electrostatic properties of membranes. Annual Review of Biophysics and Biophysical Chemistry, 18(1), 113-136. https://doi.org/10.1146/annurev.bb.18.060189.000553
Noei, H., Qiu, H., Wang, Y., Löffler, E., Wöll, C., & Muhler, M. (2008). The identification of hydroxyl groups on ZnO nanoparticles by infrared spectroscopy. Physical Chemistry Chemical Physics, 10(47), 7092-7097. https://doi.org/10.1039/b811029h
Nowack, B. (2009). The behavior and effects of nanoparticles in the environment. Environmental Pollution (Barking, Essex: 1987), 157(4), 1063-1064. https://doi.org/10.1016/j.envpol.2008.12.019
Pike, L. J. (2004). Lipid rafts: Heterogeneity on the high seas. Biochemical Journal, 378, 281-292. https://doi.org/10.1042/BJ20031672
Rudolphi-Szydło, E., Filek, M., Dyba, B., Miszalski, Z., & Zembala, M. (2020). Antioxidative action of polyamines in protection of phospholipid membranes exposed to ozone stress. Acta Biochimica Polonica, 67, 259-262. https://doi.org/10.18388/abp.2020_5230
Schroeder, F., & Gardiner, J. M. (1984). Membrane lipids and enzymes of cultured high-and low-metastatic B16 melanoma variants. Cancer Research, 44(8), 3262-3269.
Skierski, J. (2008). Cytotoxic assays of chemical substances. Postępy Biologii Komórki, 35(24), 147-163.
Taghavi, S. M., Momenpour, M., Azarian, M., Ahmadian, M., Souri, F., Taghavi, S. A., … Karchani, M. (2013). Effects of nanoparticles on the environment and outdoor workplaces. Electronic Physician, 5(4), 706-712. https://doi.org/10.14661/2013.706-712
Teicher, B. A. (Ed.) (2011). Tumor models in cancer research. Humana Press. https://doi.org/10.1007/978-1-59259-100-8
Velikonja, A., Perutkova, Š., Gongadze, E., Kramar, P., Polak, A., Maček-Lebar, A., & Iglič, A. (2013). Monovalent ions and water dipoles in contact with dipolar zwitterionic lipid headgroups-Theory and MD simulations. International Journal of Molecular Sciences, 14(2), 2846-2861. https://doi.org/10.3390/ijms14022846
Vincent, K. M., & Postovit, L.-M. (2017). Investigating the utility of human melanoma cell lines as tumour models. Oncotarget, 8(6), 10498-10509. https://doi.org/10.18632/oncotarget.14443
Walker, G. J., Soyer, H. P., Terzian, T., & Box, N. F. (2011). Modelling melanoma in mice. Pigment Cell & Melanoma Research, 24(6), 1158-1176. https://doi.org/10.1111/j.1755-148x.2011.00923.x
Wang, R., Bi, J., Ampah, K.K., Ba, X., Liu, W., & Zeng, X. (2013). Lipid rafts control human melanoma cell migration by regulating focal adhesion disassembly. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1833, 3195-3205. https://doi.org/10.1016/j.bbamcr.2013.09.007
Westphal, D., Dewson, G., Czabotar, P. E., & Kluck, R. M. (2011). Molecular biology of Bax and Bak activation and action. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1813(4), 521-531. https://doi.org/10.1016/j.bbamcr.2010.12.019
Wingett, D., Louka, P., Anders, C. B., Zhang, J., & Punnoose, A. (2016). A role of ZnO nanoparticle electrostatic properties in cancer cell cytotoxicity. Nanotechnology, Science and Applications, 9, 29-45. https://doi.org/10.2147/NSA.S99747
Wong, K., Field, M., Ou, J., Latham, K., Spencer, M., Yarovsky, I., & Kalantar-zadeh, K. (2012). Interaction of hydrogen with ZnO nanopowders-Evidence of hydroxyl group formation. Nanotechnology, 23, 015705. https://doi.org/10.1088/0957-4484/23/1/015705
Yanagida, M., Nakayama, H., Yoshizaki, F., Fujimura, T., Takamori, K., Ogawa, H., & Iwabuchi, K. (2007). Proteomic analysis of plasma membrane lipid rafts of HL-60 cells. Proteomics, 7, 2398-2409. https://doi.org/10.1002/pmic.200700056
Yeagle, P. L. (1989). Lipid regulation of cell membrane structure and function. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 3(7), 1833-1842. https://doi.org/10.1096/fasebj.3.7.2469614
Zbinden, G., & Flury-Roversi, M. (1981). Significance of the LD50-test for the toxicological evaluation of chemical substances. Archives of Toxicology, 47(2), 77-99. https://doi.org/10.1007/bf00332351