3D visualization of cellular location and cytotoxic reactions of doxorubicin, a chemotherapeutic agent

Main Article Content

Verena Richter Petra Weber Michael Wagner Herbert Schneckenburger

Abstract

Previously, we reported on the uptake and interaction of cytotoxic doxorubicin in MCF-7 breast cancer cells grown as standard 2-dimensional cell cultures. Now improved experimental techniques – including axial tomography and Light Sheet Fluorescence Microscopy (LSFM) – permit observation of single cells from any side as well as detection of individual layers in multi-cellular spheroids. Therefore, uptake of doxorubicin in the cell nucleus as well re-localization in the cytoplasm at longer incubation times is well documented. Based on a calcein-AM test, we could prove high cytotoxicity in 3D cell cultures at 48-96h after incubation. Simultaneously, disintegration of cell spheroids and formation of a degradation product became obvious. Fluorescence lifetime imaging microscopy (FLIM) is presently used to distinguish the fluorescence of doxorubicin and its degradation product, and Structured Illumination Microscopy (SIM) is suggested to improve resolution down to about 100 nm.

Keywords: fluorescence microscopy, light sheet, axial tomography, cytostatic drug, 3D cell cultures

Article Details

How to Cite
RICHTER, Verena et al. 3D visualization of cellular location and cytotoxic reactions of doxorubicin, a chemotherapeutic agent. Medical Research Archives, [S.l.], v. 6, n. 4, apr. 2018. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/1755>. Date accessed: 22 dec. 2024. doi: https://doi.org/10.18103/mra.v6i4.1755.
Section
Research Articles

References

(1) Carter, SK, Blum, RH. New chemotherapeutic agents  Bleomycin and Adriamycin, CA Cancer J. Clin., 1974, 24: 322–331. doi:10.3322/canjclin.24.6.322.
(2) Blum, RH, Carter, SK. Adriamycin. A new anticancer drug with significant clinical activity, Ann. Intern. Med., 1974, 80: 249–259. doi:10.7326/0003-4819-80-2-249.
(3) Li, ZX, Wang, TT, Wu, YT, Xu, CM, Dong, MY, Sheng, JZ, Huang, HF. Adriamycin induces H2AX phosphorylation in human spermatozoa, Asian J. Androl., 2008, 10: 749–757. doi: 10.1111/j.1745-7262.2008.00400.x.
(4) Karukstis, KK, Thompson, EH, Whiles, JA, Rosenfeld, RJ. Deciphering the fluorescence signature of daunomycin and doxorubicin, Biophys. Chem., 1998, 73: 249–263. doi: 10.1016/S0301-4622(98)00150-1.
(5) Haaland, D.M, Jones, HD, van Benthem, MH, Sinclair, MB, Melgaard, DK, Stork, CL, Pedroso, MC, Liu, P, Brasier, AR, Andrews, NL et al. Hyperspectral confocal fluorescence imaging: Exploring alternative multivariate curve resolution approaches, Appl. Spectrosc., 2009, 63: 271–279. doi:10.1366/000370209787598843.
(6) Chen, NT, Wu, CY, Chung, CY, Hwu, Y, Cheng, SH, Mou, CY, Lo, LW. Probing the dynamics of doxorubicin-DNA intercalation during the initial activation of apoptosis by fluorescence lifetime imaging microscopy (FLIM), PLoS One, 2012, 7: e44947. doi: 10.1371/journal.pone. 0044947.
(7) Bakker, GJ, Andresen, V, Hoffman, RM, Friedl, P. Fluorescence lifetime microscopy of tumor cell invasion, drug delivery, and cytotoxicity, Methods Enzymol., 2012, 504: 109–125. doi:10.1016/B978-0-12-391857-4.00005-7.
(8) Dai, X, Yue, Z, Eccleston, ME, Swartling, J, Slater, NK, Kaminski, CF. Fluorescence intensity and lifetime imaging of free and micellar-encapsulated doxorubicin in living cells, Nanomedicine, 2008, 4: 49–56. doi: 10.1016/j.nano. 2007.12.002.
(9) Weber, P, Wagner, M, Schneckenburger, H. Cholesterol dependent uptake and interaction of doxorubicin in MCF-7 breast cancer cells, Int. J. Mol. Sci., 2013, 14: 83588366. doi: 10.3390/ijms14048358.
(10) Bruns, T, Schickinger, S, Schneckenburger, H. Sample holder for axial rotation of specimens in 3D Microscopy, J. Microsc., 2015, 260(1): 30-36. doi: 10.1111/jmi.12263.
(11) Richter, V, Bruns, S, Bruns, T, Weber, P, Wagner, M, Cremer, C, Schneckenburger, H. Axial tomography in live cell laser microscopy, J. Biomed. Opt. 2017, 22(9): 091505. doi: 10.1117/1.JBO.22.9.091505.
(12) Bruns, T, Bauer, M, Bruns, S, Meyer, H, Kubin, D, Schneckenburger, H. Miniaturized modules for light sheet microscopy with low chromatic aberration, J. Microsc., 2016, 264(3): 261-267. doi: 10.1111/jmi.12439.
(13) Bratosin D, Mitrofan L, Palii C, Estaquier J, Montreuil J. Novel fluorescence assay using calcein-AM for the determination of human erythrocyte viability and aging. Cytometry A, 2005, 66(1): 78-84. doi: 10.1002/cyto.a.20152.
(14) Weber, M, Mickoleit, M, Huisken, J. Multilayer mounting for long-term light sheet microscopy of zebrafish, J. Vis. Exp., 2014, 84: e51119. doi: 10.3791/51119.
(15) Rasband, WS. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/, 1997-2016.
(16) Hovorka, O, Šubr, V, Vetvicka, D, Kovar, L., Strohalm, J, Strohalm, M, Benda, A, Hof, M, Ulbrich, K, Rihova, B. Spectral analysis of doxorubicin accumulation and the indirect quantification of its DNA intercalation, Eur. Journal of Pharmaceutics and Biopharmaceutics 2010, 76(3): 514–524. doi: 10.1016/j.ejpb.2010. 07.008.
(17) Mohapatra S, Nandi S, Chowdhury R, Das G, Ghosh S, Bhattacharyya K. Spectral mapping of 3D multi-cellular tumor spheroids: time-resolved confocal microscopy, Phys. Chem. Chem. Phys., 2016, 18(27): 18381-18390. doi: 10.1039/ c6cp02748b.
(18) Bakker, GJ, Andresen, V, Hoffman, RM, Friedl P. Fluorescence lifetime microscopy of tumor cell invasion, drug delivery, and cytotoxicity, Methods Enzymol., 2012, 504: 109-125. doi:10.1016/B978-0-12-391857-4.00005-7.
(19) Carlson M, Watson AL, Anderson L, Largaespada DA, Provenzano PP. Multiphoton fluorescence lifetime imaging of chemotherapy distribution in solid tumors, J Biomed Opt., 2017, 22(11): 1-9. doi: 10.1117/1.JBO.22.11.116010.
(20) Fei, P, Lee, J, Packard, RR, Sereti, KI, Xu, H, Ma J, Ding, Kang, Chen, H, Sung, K, Kulkarni, R, Ardehali, R, Kuo, CC, Xu, X, Ho, CM, Hsiai, TK. Cardiac Light-Sheet Fluorescent Microscopy for Multi-Scale and Rapid Imaging of Architecture and Function, Sci Rep., 2016, 6: 22489. doi: 10.1038/srep22489.
(21) Bruns, T, Schickinger, S, Schneckenburger, H. Single plane illumination module and micro-capillary approach for a wide-field microscope, J Vis Exp., 2014, 90: e51993. doi: 10.3791/51993.