Multiphoton imaging of melanoma 3D models with plasmonic nanocapsules

Acta Biomaterialia - Tập 142 - Trang 308-319 - 2022
Paula Zamora-Perez1, Can Xiao1, Marcos Sanles-Sobrido1, Muriel Rovira-Esteva1, José Javier Conesa2, Vladimir Mulens-Arias1, Daniel Jaque3,4, Pilar Rivera-Gil1
1Integrative Biomedical Materials and Nanomedicine Lab, Department of Experimental and Health Sciences (DCEXS), Pompeu Fabra University, PRBB, Carrer Doctor Aiguader 88, 08003 Barcelona, Spain
2Department of Structure of Macromolecules, Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas (CNB-CSIC), Cantoblanco, 28049, Madrid, Spain. Mistral Beamline, Experiment Division, ALBA Synchrotron (ALBA-CELLS), Barcelona, Spain
3Nanomaterials for Bioimaging Group (NanoBIG), Departamento de Física de Materiales, Universidad Autónoma de Madrid, C/Francisco Tomás y Valiente 7, 28049 Madrid, Spain
4Nanomaterials for Bioimaging Group (NanoBIG), Instituto Ramón y Cajal de Investigación Sanitaria, Ctra de Colmenar Viejo Km 9,100, Madrid, 28034 Spain

Tài liệu tham khảo

Ong, 2010, Engineering a scaffold-free 3D tumor model for in vitro drug penetration studies, Biomaterials, 31, 1180, 10.1016/j.biomaterials.2009.10.049 Ravi, 2017, Contributions of 3D Cell Cultures for Cancer Research, J. Cell. Physiol., 232, 2679, 10.1002/jcp.25664 Duval, 2017, Modeling Physiological Events in 2D vs. 3D Cell Culture, Physiology, 32, 266, 10.1152/physiol.00036.2016 Rodrigues, 2018, Emerging tumor spheroids technologies for 3D in vitro cancer modeling, Pharmacol. Ther., 184, 201, 10.1016/j.pharmthera.2017.10.018 Zanoni, 2016, 3D tumor spheroid models for in vitro therapeutic screening: a systematic approach to enhance the biological relevance of data obtained, Sci. Rep., 6, 19103, 10.1038/srep19103 Nunes, 2019, 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs, Biotechnol. Bioeng., 116, 206, 10.1002/bit.26845 Jarockyte, 2018, 3D cellular spheroids as tools for understanding carboxylated quantum dot behavior in tumors, Biochim. Biophys. Acta - Gen. Subj., 1862, 914, 10.1016/j.bbagen.2017.12.014 Costa, 2016, 3D tumor spheroids: an overview on the tools and techniques used for their analysis, Biotechnol. Adv., 34, 1427, 10.1016/j.biotechadv.2016.11.002 Olejniczak, 2018, In vitro characterization of spheres derived from colorectal cancer cell lines, Int. J. Oncol., 52, 599 Qin, 2016, Hypoxia-driven mechanism of vemurafenib resistance in melanoma, Mol. Cancer Ther., 15, 2442, 10.1158/1535-7163.MCT-15-0963 Huber, 2016, Tumour hypoxia promotes melanoma growth and metastasis via High Mobility Group Box-1 and M2-like macrophages, Sci. Rep., 6, 29914, 10.1038/srep29914 Liu-Smith, 2014, Updates of reactive oxygen species in melanoma etiology and progression, Arch. Biochem. Biophys., 563, 51, 10.1016/j.abb.2014.04.007 Paardekooper, 2019, Radical stress is more cytotoxic in the nucleus than in other organelles, Int. J. Mol. Sci., 20, 4147, 10.3390/ijms20174147 Fu, 2014, Mechanisms of nanotoxicity: generation of reactive oxygen species, J. Food Drug Anal., 22, 64, 10.1016/j.jfda.2014.01.005 Lu, 2018, Multicellular Tumor Spheroids (MCTS) as a 3D In Vitro Evaluation Tool of Nanoparticles, Small, 14, 10.1002/smll.201702858 Wong, 2018, Emerging In Vitro 3D Tumour Models in Nanoparticle-Based Gene and Drug Therapy, Trends Biotechnol., 36, 477, 10.1016/j.tibtech.2018.02.002 Zhao, 2017, Influence of nanoparticle shapes on cellular uptake of paclitaxel loaded nanoparticles in 2D and 3D cancer models, Polym. Chem., 8, 3317, 10.1039/C7PY00385D Tchoryk, 2019, Penetration and uptake of nanoparticles in 3D tumor spheroids, Bioconjug. Chem., 30, 1371, 10.1021/acs.bioconjchem.9b00136 van den Brand, 2018, Penetration in 3D tumor spheroids and explants: adding a further dimension to the structure-activity relationship of cell-penetrating peptides, Biochim. Biophys. Acta - Biomembr., 1860, 1342, 10.1016/j.bbamem.2018.03.007 Priwitaningrum, 2016, Tumor stroma-containing 3D spheroid arrays: a tool to study nanoparticle penetration, J. Control. Release., 244, 257, 10.1016/j.jconrel.2016.09.004 Agarwal, 2015, Effect of Shape, Size, and Aspect Ratio on Nanoparticle Penetration and Distribution inside Solid Tissues Using 3D Spheroid Models, Adv. Healthc. Mater., 4, 2269, 10.1002/adhm.201500441 Lin, 2019, Recent advances in multiphoton microscopy combined with nanomaterials in the field of disease evolution and clinical applications to liver cancer, Nanoscale, 11, 19619, 10.1039/C9NR04902A Larson, 2011, Multiphoton microscopy, Nat. Photonics., 5, 1, 10.1038/nphoton.an.2010.2 Sandoval, 2017, Intravital multiphoton microscopy as a tool for studying renal physiology and pathophysiology, Methods, 128, 20, 10.1016/j.ymeth.2017.07.014 Sarder, 2013, All-near-infrared multiphoton microscopy interrogates intact tissues at deeper imaging depths than conventional single- and two-photon near-infrared excitation microscopes, J. Biomed. Opt., 18, 10.1117/1.JBO.18.10.106012 Vickers, 2018, Two-Photon Photoluminescence and Photothermal Properties of Hollow Gold Nanospheres for Efficient Theranostic Applications, J. Phys. Chem. C., 122, 13304, 10.1021/acs.jpcc.7b09055 Shen, 2016, Two-photon excitation nanoparticles for photodynamic therapy, Chem. Soc. Rev., 45, 6725, 10.1039/C6CS00442C Huang, 2015, Controlled Au-Polymer Nanostructures for Multiphoton Imaging, Prodrug Delivery, and Chemo-Photothermal Therapy Platforms, ACS Appl. Mater. Interfaces., 7, 25259, 10.1021/acsami.5b07110 Ardekani, 2017, Two-photon excitation triggers combined chemo-photothermal therapy via doped carbon nanohybrid dots for effective breast cancer treatment, Chem. Eng. J., 330, 651, 10.1016/j.cej.2017.07.165 Melentiev, 2015, Giant enhancement of two photon induced luminescence in metal nanostructure, Opt. Express., 23, 11444, 10.1364/OE.23.011444 Liu, 2015, Two-photon microscopy in pre-clinical and clinical cancer research, Front. Optoelectron., 8, 141, 10.1007/s12200-014-0415-5 Xu, 1996, Multiphoton fluorescence excitation: new spectral windows for biological nonlinear microscopy, Proc. Natl. Acad. Sci. U. S. A., 93, 10763, 10.1073/pnas.93.20.10763 Shanmugam, 2014, Near-infrared light-responsive nanomaterials in cancer therapeutics, Chem. Soc. Rev., 43, 6254, 10.1039/C4CS00011K Wagner, 2019, Quantum dots in biomedical applications, Acta Biomater., 94, 44, 10.1016/j.actbio.2019.05.022 Austin, 2014, The optical, photothermal, and facile surface chemical properties of gold and silver nanoparticles in biodiagnostics, therapy, and drug delivery, Arch. Toxicol., 88, 1391, 10.1007/s00204-014-1245-3 Yuan, 2012, In vivo particle tracking and photothermal ablation using plasmon-resonant gold nanostars, Nanomedicine Nanotechnology, Biol. Med., 8, 1355, 10.1016/j.nano.2012.02.005 Olesiak-Banska, 2019, Two-photon absorption and photoluminescence of colloidal gold nanoparticles and nanoclusters, Chem. Soc. Rev., 48, 4087, 10.1039/C8CS00849C Suarasan, 2019, Intracellular Dynamic Disentangling of Doxorubicin Release from Luminescent Nanogold Carriers by Fluorescence Lifetime Imaging Microscopy (FLIM) under Two-Photon Excitation, ACS Appl. Mater. Interfaces., 11, 7812, 10.1021/acsami.8b21269 Chen, 2012, Creation and luminescence of size-selected gold nanorods, Nanoscale, 4, 5017, 10.1039/c2nr30324h Gordel, 2014, Shell-thickness-dependent nonlinear optical properties of colloidal gold nanoshells, J. Mater. Chem. C., 2, 7239, 10.1039/C4TC01210K Hutter, 2010, Microglial response to gold nanoparticles, ACS Nano, 4, 2595, 10.1021/nn901869f Liu, 2015, A plasmonic gold nanostar theranostic probe for in vivo tumor imaging and photothermal therapy, Theranostics, 5, 946, 10.7150/thno.11974 Zhang, 2017, A surface plasmon enhanced FLIM-FRET imaging approach based on Au nanoparticles, Med. Devices Diagnostic Eng., 2, 78, 10.15761/MDDE.1000119 Basuki, 2013, Using fluorescence lifetime imaging microscopy to monitor theranostic nanoparticle uptake and intracellular doxorubicin release, ACS Nano, 7, 10175, 10.1021/nn404407g Boreham, 2016, Time-Resolved Fluorescence Spectroscopy and Fluorescence Lifetime Imaging Microscopy for Characterization of Dendritic Polymer Nanoparticles and Applications in Nanomedicine, Molecules, 22, 17, 10.3390/molecules22010017 Zamora-Perez, 2018, Hyperspectral-enhanced dark field microscopy for single and collective nanoparticle characterization in biological environments, Materials (Basel), 11, 10.3390/ma11020243 Rane, 2016, Two-photon microscopy analysis of gold nanoparticle uptake in 3D cell spheroids, PLoS One, 11, 10.1371/journal.pone.0167548 Olesiak-Banska, 2019, Two-photon absorption and photoluminescence of colloidal gold nanoparticles and nanoclusters, Chem. Soc. Rev., 48, 4087, 10.1039/C8CS00849C Morales-Dalmau, 2019, Quantification of gold nanoparticle accumulation in tissue by two-photon luminescence microscopy, Nanoscale, 11, 11331, 10.1039/C9NR01198F Bedogni, 2009, Hypoxia, melanocytes and melanoma - Survival and tumor development in the permissive microenvironment of the skin, Pigment Cell Melanoma Res., 22, 166, 10.1111/j.1755-148X.2009.00553.x Meierjohann, 2014, Oxidative stress in melanocyte senescence and melanoma transformation, Eur. J. Cell Biol., 93, 36, 10.1016/j.ejcb.2013.11.005 Cheli, 2012, Hypoxia and MITF control metastatic behaviour in mouse and human melanoma cells, Oncogene, 31, 2461, 10.1038/onc.2011.425 Jackson, 2010, Potential dependent superiority of gold nanoparticles in comparison to iodinated contrast agents, Eur. J. Radiol., 75, 104, 10.1016/j.ejrad.2009.03.057 Sanles-sobrido, 2014, 2699 Javier, 2008, Uptake of colloidal polyelectrolyte-coated particles and polyelectrolyte multilayer capsules by living cells, Adv. Mater., 20, 4281, 10.1002/adma.200703190 Rivera-Gil, 2009, Intracellular processing of proteins mediated by biodegradable polyelectrolyte capsules, Nano Lett., 9, 4398, 10.1021/nl902697j Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods., 9, 676, 10.1038/nmeth.2019 Mastronarde, 2017, Automated tilt series alignment and tomographic reconstruction in IMOD, J. Struct. Biol., 197, 102, 10.1016/j.jsb.2016.07.011 Carzaniga, 2014, Cryo-soft X-ray tomography: a journey into the world of the native-state cell, Protoplasma, 251, 449, 10.1007/s00709-013-0583-y Chiappi, 2016, Cryo-soft X-ray tomography as a quantitative three-dimensional tool to model nanoparticle: cell interaction, J. Nanobiotechnology., 14, 10.1186/s12951-016-0170-4 Zamora Perez, 2021, Hyperspectral enhanced darkfield imaging of individual and collective hyperthermia-driven gold-copper sulfide nanoparticles, Nanoscale, 13, 13256, 10.1039/D0NR08256B Sant, 2017, The production of 3D tumor spheroids for cancer drug discovery, Drug Discov. Today Technol., 23, 27, 10.1016/j.ddtec.2017.03.002 Yang, 2015, Gold Nanomaterials at Work in Biomedicine, Chem. Rev., 115, 10410, 10.1021/acs.chemrev.5b00193 Dreaden, 2012, The golden age: gold nanoparticles for biomedicine, Chem. Soc. Rev., 41, 2740, 10.1039/C1CS15237H Wu, 2019, Gold nanoparticles in biological optical imaging, Nano Today, 24, 120, 10.1016/j.nantod.2018.12.006 R. Datta, T.M. Heaster, J.T. Sharick, A.A. Gillette, M.C. Skala, Fluorescence lifetime imaging microscopy: fundamentals and advances in instrumentation, analysis, and applications, Https://Doi.Org/10.1117/1.JBO.25.7.071203. 25 (2020) 071203. https://doi.org/10.1117/1.JBO.25.7.071203. Berezin, 2010, Fluorescence lifetime measurements and biological imaging, Chem. Rev., 110, 2641, 10.1021/cr900343z Wagner, 2019, Quantum dots in biomedical applications, Acta Biomater., 94, 44, 10.1016/j.actbio.2019.05.022 Peteiro-Cartelle, 2009, One example on how colloidal nano- and microparticles could contribute to medicine, Nanomedicine, 4, 967, 10.2217/nnm.09.84 Rivera-Gil, 2013, The challenge to relate the physicochemical properties of colloidal nanoparticles to their cytotoxicity, Acc. Chem. Res., 46, 743, 10.1021/ar300039j Carregal-Romero, 2012, Subcellular carrier-based optical ion-selective nanosensors, Front. Pharmacol., 10.3389/fphar.2012.00070 Petryayeva, 2011, Localized surface plasmon resonance: nanostructures, bioassays and biosensing-A review, Anal. Chim. Acta., 706, 8, 10.1016/j.aca.2011.08.020 Sagle, 2011, Advances in localized surface plasmon resonance spectroscopy biosensing, Nanomedicine, 6, 1447, 10.2217/nnm.11.117 Foroozandeh, 2018, Insight into Cellular Uptake and Intracellular Trafficking of Nanoparticles, Nanoscale Res. Lett., 13, 1, 10.1186/s11671-018-2728-6 Canton, 2012, Endocytosis at the nanoscale, Chem. Soc. Rev., 41, 2718, 10.1039/c2cs15309b Oh, 2014, Endocytosis and exocytosis of nanoparticles in mammalian cells, Int. J. Nanomed., 9, 51 Schweiger, 2012, Quantification of the internalization patterns of superparamagnetic iron oxide nanoparticles with opposite charge, J. Nanobiotechnol., 10, 28, 10.1186/1477-3155-10-28 Kastl, 2013, Multiple internalization pathways of polyelectrolyte multilayer capsules into mammalian cells, ACS Nano, 7, 6605, 10.1021/nn306032k Durymanov, 2019, Role of Endocytosis in Nanoparticle Penetration of 3D Pancreatic Cancer Spheroids, Mol. Pharm., 16, 1074, 10.1021/acs.molpharmaceut.8b01078 Achilli, 2014, Multilayer spheroids to quantify drug uptake and diffusion in 3D, Mol. Pharm., 11, 2071, 10.1021/mp500002y Sorrentino, 2015, MISTRAL: a transmission soft X-ray microscopy beamline for cryo nano-tomography of biological samples and magnetic domains imaging, J. Synchrotron Radiat., 22, 1112, 10.1107/S1600577515008632 Chiappi, 2016, Cryo-soft X-ray tomography as a quantitative three-dimensional tool to model nanoparticle: cell interaction, J. Nanobiotechnology., 14, 15, 10.1186/s12951-016-0170-4 Conesa, 2016, Intracellular nanoparticles mass quantification by near-edge absorption soft X-ray nanotomography, Sci. Rep., 6, 22345, 10.1038/srep22354 Idée, 2004, Prophylaxis of iodinated contrast media-induced nephropathy: a pharmacological point of view, Invest. Radiol., 39, 155, 10.1097/01.rli.0000101483.60710.2c Criddle, 2006, Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells, J. Biol. Chem., 281, 40485, 10.1074/jbc.M607704200 Lequeux, 2019, Impact of hypoxic tumor microenvironment and tumor cell plasticity on the expression of immune checkpoints, Cancer Lett., 458, 13, 10.1016/j.canlet.2019.05.021 Riffle, 2017, Modeling tumor cell adaptations to hypoxia in multicellular tumor spheroids, J. Exp. Clin. Cancer Res., 36, 10.1186/s13046-017-0570-9 Däster, 2017, Induction of hypoxia and necrosis in multicellular tumor spheroids is associated with resistance to chemotherapy treatment, Oncotarget, 8, 1725, 10.18632/oncotarget.13857 Benien, 2014, 3D tumor models: history, advances and future perspectives, Futur. Oncol., 10, 1311, 10.2217/fon.13.274 Reynolds, 2017, Breast Cancer Spheroids Reveal a Differential Cancer Stem Cell Response to Chemotherapeutic Treatment, Sci. Rep., 7, 10382, 10.1038/s41598-017-10863-4 Luca, 2013, Impact of the 3D Microenvironment on Phenotype, Gene Expression, and EGFR Inhibition of Colorectal Cancer Cell Lines, PLoS One, 8, e59689, 10.1371/journal.pone.0059689 Rivera-Gil, 2013, Plasmonic nanoprobes for real‐time optical monitoring of nitric oxide inside living cells, Angewandte Chemie International Edition, 52, 13694, 10.1002/anie.201306390