Influence of calcium ions on physical chemical characteristics of semiconductor quantum dots encapsulated by amphiphilic polymer and their efficiency of cellular uptake
Abstract
Here, we studied the effect of calcium ions on the physicochemical properties and cellular uptake of CdSe/ZnS quantum dots encapsulated with poly(maleic anhydride-alt-1-tetradecene), modified to a varying extent by quaternary ammonium groups. It was shown that quantum dots carrying negatively charged carboxyl groups in the polymer shell change their physicochemical and optical characteristics in the presence of Ca2+ and Ba2+ ions. As the negatively charged carboxyl groups in the shell are completely replaced by positively charged quaternary ammonium groups, these effects gradually decrease. A change in the physicochemical properties of nanoparticles leads to a change in their cellular uptake in the presence of calcium ions. Nanoparticles carrying only negatively charged groups in the shell in the presence of Ca2+ agglomerate and form conglomerates of nanoparticles and cells. The positively charged quaternary ammonium groups in the polymer shell of the nanoparticles increase their aggregative stability in the presence of Ca2+ and contribute to their uptake by cells. The mechanisms of uptake depend on nanoparticle’s charge. Nanoparticles with a positive ζ potential are absorbed by calcium-dependent mechanisms, which are suppressed by inhibition of the calcium-dependent enzyme dynamin or in the presence of calcium chelator EGTA. The uptake of nanoparticles with a negative ζ potential, in contrast, is enhanced by the chelation of calcium ions. This indicates the different role of cellular calcium-dependent mechanisms in the uptake of positively and negatively charged nanoparticles.
References
- Treuel L, Docter D, Maskos M, Stauber RH. Protein corona – from molecular adsorption to physiological complexity. Beilstein Journal of Nanotechnology. 2015;6:857–873. DOI: 10.3762/bjnano.6.88.
- Barbero F, Russo L, Vitali M, Piella J, Salvo I, Borrajo ML. Formation of the protein corona: the interface between nanoparticles and the immune system. Seminars in Immunology. 2017;34:52–60. DOI: 10.1016/j.smim.2017.10.001.
- Arruda AP, Hotamisligil GS. Calcium homeostasis and organelle function in the pathogenesis of obesity and diabetes. Cell Metabolism. 2015;22(3):381–397. DOI: 10.1016/j.cmet.2015.06.010.
- Brodskiy PA, Zartman JJ. Calcium as a signal integrator in developing epithelial tissues. Physical Biology. 2018;15(5):051001. DOI: 10.1088/1478-3975/aabb18.
- Filippini A, DʼAmore A, DʼAlessio A. Calcium mobilization in endothelial cell functions. International Journal of Molecular Sciences. 2019;20(18):4525–4538. DOI: 10.3390/ijms20184525.
- Yao CK, Liu YT, Lee IC, Wang YT, Wu PY. A Ca2+ channel differentially regulates clathrin-mediated and activity-dependent bulk endocytosis. PLoS Biology. 2020;15(4):e2000931. DOI: 10.1371/journal.pbio.2000931.
- Leitz J, Kavalali ET. Ca2+ dependence of synaptic vesicle endocytosis. The Neuroscientist. 2016;22(5):464–476. DOI: 10.1177/1073858415588265.
- Heedoo L, Groota M, Pinilla-Vera M, Fredenburgh LE, Jin Y. Identification of miRNA-rich vesicles in bronchoalveolar lavage fluid: Insights into the function and heterogeneity of extracellular vesicles. Journal of Controlled Release. 2019;294:43–52. DOI: 10.1016/j.jconrel.2018.12.008.
- Resch-Genger U, Grabolle M, Cavaliere-Jaricot S, Nitschke & Thomas Nann R. Quantum dots versus organic dyes as fluorescent labels. Nature Methods. 2008;5(9):763–775. DOI: 10.1038/nmeth.1248.
- Petrova EA, Terpinskaya TI, Fedosyuk AA, Radchanka AV, Antanovich AV, Prudnikau AV, et al. Luminescent quantum dots encapsulated by zwitterionic amphi philic polymer: surface charge-dependent interaction with cancer cells. Journal of the Belarusian State University. Chemistry. 2018;1:3–13.
- Rosenthal SJ, Mcbride J, Pennycook SJ, Feldman LC. Synthesis, surface studies, composition and structural characterization of CdSe, core/shell and biologically active nanocrystals. Surface Science Reports. 2007;62(4):111–157. DOI: 10.1016/j.surfrep.2007.02.001.
- Fedosyuk A, Radchanka A. Determination of concentration of amphiphilic polymer molecules on the surface of encapsulated semiconductor nanocrystals. Langmuir. 2016;32(8):1955–1961. DOI: 10.1021/acs.langmuir.5b04602.
- Nakamura Y. EGTA Can Inhibit Vesicular Release in the Nanodomain of Single Ca2+ Channels. Frontiers in Synaptic Neuroscience. 2019;11(26):15. DOI: 10.3389/fnsyn.2019.00026.
- Pepperell JR, Preston SL, Behrman HR. The antigonadotropic action of prostaglandin F2α is not mediated by elevated cytosolic calcium levels in rat luteal cells. Endocrinology. 1989;125(1):144–151. DOI: 10.1210/endo-125-1-144.
- Grant RL, Acosta D. Interactions of intracellular pH and intracellular calcium in primary cultures of rabbit corneal epithelial cells. In Vitro Cellular & Developmental Biology – Animal. 1996;32(1):38–45. DOI: 10.1007/bf02722992.
- Iida H, Sakaguchi S, Yagawa Y, Anraku Y. Cell cycle control by Ca2+ in Saccharomyces cerevisiae. Journal of Biological Chemistry. 1990;265(34):21216–21222.
- Timmers AC, Reiss HD, Schel JH. Digitonin-aided loading of Fluo-3 into embryogenic plant cells. Cell Calcium. 1991;12(7):515–521. DOI: 10.1016/0143-4160(91)90033-b.
- Okorokov LA, Tanner W, Lehle L. A novel primary Ca2+-transport system from Saccharomyces cerevisiae. European Journal of Biochemistry. 1993;216(2):573–577. DOI: 10.1111/j.1432-1033.1993.tb18176.x.
- Almeida JC, Benchimol M, Okorokov LA. Ca2+ sequestering in the early-branching amitochondriate protozoan Tritrichomonas foetus: an important role of the Golgi complex and its Ca2+-ATPase. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2003;1615(1–2):60–68. DOI: 10.1016/s0005-2736(03)00192-5.
- Mettlen M, Chen PH, Srinivasan S, Danuser G, Schmid SL. Regulation of clathrin-mediated endocytosis. Annual Review of Biochemistry. 2018;87:871–896. DOI: 10.1146/annurev-biochem-062917-012644.
- Mayor S, Parton RG, Donaldson JG. Clathrin-independent pathways of endocytosis. Cold Spring Harbor Perspectives in Biology. 2014;6:a016758. DOI: 10.1101/cshperspect.a016758.
- Sathe M, Muthukrishnan G, Rae J, Disanza A, Thattai M, Scita G. Small GTPases and BAR domain proteins regulate branched actin polymerisation for clathrin and dynamin-independent endocytosis. Nature Communications. 2018;9:1835–1844. DOI: 10.1038/s41467-018-03955-w.
- Fröhlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. International Journal of Nanomedicine. 2012;7:5577–5591. DOI: 10.2147/IJN.S36111.
- Donahue ND, Acar H, Wilhelm S. Concepts of nanoparticle cellular uptake, intracellular trafficking, and kinetics in nanomedicine. Advanced Drug Delivery Reviews. 2019;143:68–96. DOI: 10.1016/j.addr.2019.04.008.
- Chen Y, Deng L, Maeno-Hikichi Y, Lai M, Chang S, Chen G. Formation of an endophilin-Ca2+ channel complex is critical for clathrin-mediated synaptic vesicle endocytosis. Cell. 2003;115(1):37–48. DOI: 10.1016/s0092-8674(03)00726-8.
- Teng H, Wilkinson RS. Clathrin-mediated endocytosis in snake motor terminals is directly facilitated by intracellular Ca2+. Journal of Physiology. 2005;565(3):743–750. DOI: 10.1113/jphysiol.2005.087296.
- Zhang J, Fan J, Tian Q, Song Z, Zhang J, Chen Y. Characterization of two distinct modes of endophilin in clathrin-mediated endocytosis. Cellular Signalling. 2012;24(11):2043–2050. DOI: 10.1016/j.cellsig.2012.06.006.
- Delos Santos RC, Bautista S, Lucarelli S, Bone LN, Dayam RM, Abousawan J, et al. Selective regulation of clathrin-mediated epidermal growth factor receptor signaling and endocytosis by phospholipase C and calcium. Molecular Biology of the Cell. 2017;28(21):2747–2903. DOI: 10.1091/mbc.E16-12-0871.
- Bhattacharjee S, Ershov D, van der Gucht J, Alink GM, Rietjens IMCM, Zuilhof H. Surface charge-specific cytotoxicity and cellular uptake of tri-block copolymer nanoparticles. Nanotoxicology. 2013;7(1):71–84. DOI: 10.3109/17435390.2011.633714.
- Yameen B, Choi WI, Vilos C, Swami A, Shi J, Farokhzad OC. Insight into nanoparticle cellular uptake and intracellular targeting. Journal of Controlled Release. 2014;190:485–499. DOI: 10.1016/j.jconrel.2014.06.038.
- Schmid SL. Reciprocal regulation of signaling and endocytosis: implications for the evolving cancer cell. Journal of Cell Biology. 2017;216(9):2623–2632. DOI: 10.1083/jcb.201705017.
- Fazlollahi F, Kim YH, Sipos A, Hamm-Alvarez SF, Borok Z, Kim KJ, et al. Nanoparticle translocation across mouse alveolar epithelial cell monolayers: species-specific mechanisms. Nanomedicine. 2013;9(6):786–794. DOI: 10.1016/j.nano.2013.01.007.
Copyright (c) 2020 Journal of the Belarusian State University. Chemistry
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The authors who are published in this journal agree to the following:
- The authors retain copyright on the work and provide the journal with the right of first publication of the work on condition of license Creative Commons Attribution-NonCommercial. 4.0 International (CC BY-NC 4.0).
- The authors retain the right to enter into certain contractual agreements relating to the non-exclusive distribution of the published version of the work (e.g. post it on the institutional repository, publication in the book), with the reference to its original publication in this journal.
- The authors have the right to post their work on the Internet (e.g. on the institutional store or personal website) prior to and during the review process, conducted by the journal, as this may lead to a productive discussion and a large number of references to this work. (See The Effect of Open Access.)