Versions
- 24-10-2023 (3)
- 24-10-2023 (2)
- 19-07-2023 (1)
Keywords
3D cell culture
gold nanoparticles
nanotechnology
oncology
How to Cite
Abstract
The creation of cell cultures for scientific purposes has made it possible to obtain new knowledge and consequently to make discoveries in the field of cell biology or biophysics. In vitro studies allow for the observation of cell lines as well as interactions with introduced substances or materials. They have an invaluable contribution to the development of nanomedicine, which is attracted a lot of interest. Gold nanoparticles (GNPs) are particularly popular and promising, especially in terms of cancer therapy. This is due to the specific (e.g. electrical, magnetic, optical, mechanical) properties of nanoparticles, significantly different from gold particles of macro size. Unfortunately, the results of in vitro studies are sometimes inconsistent with in vivo studies. Nanoparticles that work well at the cellular level are not always as effective in animal models. The reason for this is the multiplicity of complex metabolic processes occurring in the body during in vivo studies. Most cell studies are performed on two-dimensional structures that approximate real-world conditions. Currently, none of the in vitro techniques is able to reflect the identical physiological conditions prevailing in animal models. However, modern science can map them more precisely using 3D culture, which is much more complex and less efficient. When designing new studies, the advantages and disadvantages of each of the mentioned cell culture methods should be considered. The purpose of this publication is to present the differences between two-dimensional and three-dimensional (3D) cell cultures, taking into account the use of gold nanoparticles.
References
Patra JK, Das G, Fraceto LF, Campos EVR, Rodriguez-Torres M del P, Acosta-Torres LS, et al. Nano based drug delivery systems: recent developments and future prospects. J Nanobiotechnol. 2018 Dec;16(1):71.
Alkilany AM, Murphy CJ. Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J Nanopart Res. 2010 Sep;12(7):2313–33.
Bouché M, Hsu JC, Dong YC, Kim J, Taing K, Cormode DP. Recent Advances in Molecular Imaging with Gold Nanoparticles. Bioconjugate Chem. 2020 Feb 19;31(2):303–14.
Retif P, Pinel S, Toussaint M, Frochot C, Chouikrat R, Bastogne T, et al. Nanoparticles for Radiation Therapy Enhancement: the Key Parameters. Theranostics. 2015;5(9):1030–44.
Musielak M, Piotrowski I, Suchorska WM. Superparamagnetic iron oxide nanoparticles (SPIONs) as a multifunctional tool in various cancer therapies. Reports of Practical Oncology & Radiotherapy. 2019 Jul;24(4):307–14.
Bromma K, Dos Santos N, Barta I, Alexander A, Beckham W, Krishnan S, et al. Enhancing nanoparticle accumulation in two dimensional, three dimensional, and xenograft mouse cancer cell models in the presence of docetaxel. Sci Rep. 2022 Aug 5;12(1):13508.
Amendola V, Pilot R, Frasconi M, Maragò OM, Iatì MA. Surface plasmon resonance in gold nanoparticles: a review. J Phys: Condens Matter. 2017 May 24;29(20):203002.
Zhao X, Pan J, Li W, Yang W, Qin L, Pan Y. Gold nanoparticles enhance cisplatin delivery and potentiate chemotherapy by decompressing colorectal cancer vessels. IJN. 2018 Oct;Volume 13:6207–21.
Caracciolo G, Farokhzad OC, Mahmoudi M. Biological Identity of Nanoparticles In Vivo : Clinical Implications of the Protein Corona. Trends in Biotechnology. 2017 Mar;35(3):257–64.
Chaicharoenaudomrung N, Kunhorm P, Noisa P. Three-dimensional cell culture systems as an in vitro platform for cancer and stem cell modeling. WJSC. 2019 Dec 26;11(12):1065–83.
Van Zundert I, Fortuni B, Rocha S. From 2D to 3D Cancer Cell Models—The Enigmas of Drug Delivery Research. Nanomaterials. 2020 Nov 11;10(11):2236.
Duval K, Grover H, Han LH, Mou Y, Pegoraro AF, Fredberg J, et al. Modeling Physiological Events in 2D vs. 3D Cell Culture. Physiology. 2017 Jul;32(4):266–77.
Joudeh N, Linke D. Nanoparticle classification, physicochemical properties, characterization, and applications: a comprehensive review for biologists. J Nanobiotechnol. 2022 Jun 7;20(1):262.
Sontheimer-Phelps A, Hassell BA, Ingber DE. Modelling cancer in microfluidic human organs-on-chips. Nat Rev Cancer. 2019 Feb;19(2):65–81.
Prasad M, Kumar R, Buragohain L, Kumari A, Ghosh M. Organoid Technology: A Reliable Developmental Biology Tool for Organ-Specific Nanotoxicity Evaluation. Front Cell Dev Biol. 2021 Sep 23;9:696668.
Fang Y, Eglen RM. Three-Dimensional Cell Cultures in Drug Discovery and Development. SLAS Discovery. 2017 Jun;22(5):456–72.
Langhans SA. Three-Dimensional in Vitro Cell Culture Models in Drug Discovery and Drug Repositioning. Front Pharmacol. 2018 Jan 23;9:6.
Saydé T, El Hamoui O, Alies B, Gaudin K, Lespes G, Battu S. Biomaterials for Three-Dimensional Cell Culture: From Applications in Oncology to Nanotechnology. Nanomaterials. 2021 Feb 13;11(2):481.
Bielecka ZF, Maliszewska-Olejniczak K, Safir IJ, Szczylik C, Czarnecka AM. Three-dimensional cell culture model utilization in cancer stem cell research: 3D cell culture models in CSCs research. Biol Rev. 2017 Aug;92(3):1505–20.
Sokolova V, Ebel J, Kollenda S, Klein K, Kruse B, Veltkamp C, et al. Uptake of Functional Ultrasmall Gold Nanoparticles in 3D Gut Cell Models. Small. 2022 Aug;18(31):2201167.
Haisler WL, Timm DM, Gage JA, Tseng H, Killian TC, Souza GR. Three-dimensional cell culturing by magnetic levitation. Nat Protoc. 2013 Oct;8(10):1940–9.
Jensen C, Teng Y. Is It Time to Start Transitioning From 2D to 3D Cell Culture? Front Mol Biosci. 2020 Mar 6;7:33.
Fontoura JC, Viezzer C, dos Santos FG, Ligabue RA, Weinlich R, Puga RD, et al. Comparison of 2D and 3D cell culture models for cell growth, gene expression and drug resistance. Materials Science and Engineering: C. 2020 Feb;107:110264.
Foglietta F, Canaparo R, Muccioli G, Terreno E, Serpe L. Methodological aspects and pharmacological applications of three-dimensional cancer cell cultures and organoids. Life Sciences. 2020 Aug;254:117784.
Weiswald LB, Bellet D, Dangles-Marie V. Spherical Cancer Models in Tumor Biology. Neoplasia. 2015 Jan;17(1):1–15.
Białkowska K, Komorowski P, Bryszewska M, Miłowska K. Spheroids as a Type of Three-Dimensional Cell Cultures—Examples of Methods of Preparation and the Most Important Application. IJMS. 2020 Aug 28;21(17):6225.
Le VM, Lang MD, Shi WB, Liu JW. A collagen-based multicellular tumor spheroid model for evaluation of the efficiency of nanoparticle drug delivery. Artificial Cells, Nanomedicine, and Biotechnology. 2016 Feb 17;44(2):540–4.
Kapałczyńska M, Kolenda T, Przybyła W, Zajączkowska M, Teresiak A, Filas V, et al. 2D and 3D cell cultures – a comparison of different types of cancer cell cultures. aoms [Internet]. 2016 [cited 2023 Apr 4]; Available from: https://www.termedia.pl/doi/10.5114/aoms.2016.63743
Luca AC, Mersch S, Deenen R, Schmidt S, Messner I, Schäfer KL, et al. Impact of the 3D Microenvironment on Phenotype, Gene Expression, and EGFR Inhibition of Colorectal Cancer Cell Lines. Cordes N, editor. PLoS ONE. 2013 Mar 26;8(3):e59689.
Adcock AF. Three-Dimensional (3D) Cell Cultures in Cell-based Assays for in-vitro Evaluation of Anticancer Drugs. J Anal Bioanal Tech [Internet]. 2015 [cited 2023 May 5];06(03). Available from: https://www.omicsonline.org/open-access/threedimensional-3d-cell-cultures-in-cellbased-assays-for-invitro-evaluation-of-anticancer-drugs-2155-9872-1000249.php?aid=54848
Wu Z, Guan R, Tao M, Lyu F, Cao G, Liu M, et al. Assessment of the toxicity and inflammatory effects of different-sized zinc oxide nanoparticles in 2D and 3D cell cultures. RSC Adv. 2017;7(21):12437–45.
Worthington P, Pochan DJ, Langhans SA. Peptide Hydrogels – Versatile Matrices for 3D Cell Culture in Cancer Medicine. Front Oncol [Internet]. 2015 Apr 20 [cited 2023 May 5];5. Available from: http://journal.frontiersin.org/article/10.3389/fonc.2015.00092/abstract
Rossi M, Blasi P. Multicellular Tumor Spheroids in Nanomedicine Research: A Perspective. Front Med Technol. 2022 Jun 15;4:909943.
Costa EC, Moreira AF, De Melo-Diogo D, Gaspar VM, Carvalho MP, Correia IJ. 3D tumor spheroids: an overview on the tools and techniques used for their analysis. Biotechnology Advances. 2016 Dec;34(8):1427–41.
Saji Joseph J, Tebogo Malindisa S, Ntwasa M. Two-Dimensional (2D) and Three-Dimensional (3D) Cell Culturing in Drug Discovery. In: Ali Mehanna R, editor. Cell Culture [Internet]. IntechOpen; 2019 [cited 2023 May 5]. Available from: https://www.intechopen.com/books/cell-culture/two-dimensional-2d-and-three-dimensional-3d-cell-culturing-in-drug-discovery
Nunes AS, Barros AS, Costa EC, Moreira AF, Correia IJ. 3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs: NUNES ET AL. Biotechnology and Bioengineering. 2019 Jan;116(1):206–26.
Pampaloni F, Stelzer EH. Three-Dimensional Cell Cultures in Toxicology. Biotechnology and Genetic Engineering Reviews. 2009 Jan;26(1):117–38.
Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-Dimensional Cell Culture Systems and Their Applications in Drug Discovery and Cell-Based Biosensors. ASSAY and Drug Development Technologies. 2014 May;12(4):207–18.
Brajša K. Three-dimensional cell cultures as a new tool in drug discovery. Period Biol. 2016 Mar 31;118(1):59–65.
Lee SH, Shim KY, Kim B, Sung JH. Hydrogel‐based three‐dimensional cell culture for organ‐on‐a‐chip applications. Biotechnol Progress. 2017 May;33(3):580–9.
Yosef A, Kossover O, Mironi‐Harpaz I, Mauretti A, Melino S, Mizrahi J, et al. Fibrinogen‐Based Hydrogel Modulus and Ligand Density Effects on Cell Morphogenesis in Two‐Dimensional and Three‐Dimensional Cell Cultures. Adv Healthcare Mater. 2019 Jul;8(13):1801436.
Haycock JW. 3D Cell Culture: A Review of Current Approaches and Techniques. In: Haycock JW, editor. 3D Cell Culture [Internet]. Totowa, NJ: Humana Press; 2011 [cited 2023 May 5]. p. 1–15. (Methods in Molecular Biology; vol. 695). Available from: https://link.springer.com/10.1007/978-1-60761-984-0_1
Hickman JA, Graeser R, De Hoogt R, Vidic S, Brito C, Gutekunst M, et al. Three-dimensional models of cancer for pharmacology and cancer cell biology: Capturing tumor complexity in vitro/ex vivo. Biotechnology Journal. 2014 Sep;9(9):1115–28.
Wen Z, Liao Q, Hu Y, You L, Zhou L, Zhao Y. A spheroid-based 3-D culture model for pancreatic cancer drug testing, using the acid phosphatase assay. Braz J Med Biol Res. 2013 Jul;46(7):634–42.
Imamura Y, Mukohara T, Shimono Y, Funakoshi Y, Chayahara N, Toyoda M, et al. Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer. Oncology Reports. 2015 Apr;33(4):1837–43.
Daniel VC, Marchionni L, Hierman JS, Rhodes JT, Devereux WL, Rudin CM, et al. A primary xenograft model of small-cell lung cancer reveals irreversible changes in gene expression imposed by culture in vitro. Cancer Res. 2009 Apr 15;69(8):3364–73.
Colella G, Fazioli F, Gallo M, De Chiara A, Apice G, Ruosi C, et al. Sarcoma Spheroids and Organoids—Promising Tools in the Era of Personalized Medicine. IJMS. 2018 Feb 21;19(2):615.
Ravi M, Paramesh V, Kaviya SR, Anuradha E, Solomon FDP. 3D Cell Culture Systems: Advantages and Applications: 3D CELL CULTURE SYSTEMS. J Cell Physiol. 2015 Jan;230(1):16–26.
Behzadi S, Vatan NM, Lema K, Nwaobasi D, Zenkov I, Abadi PPSS, et al. Flat Cell Culturing Surface May Cause Misinterpretation of Cellular Uptake of Nanoparticles. Adv Biosys. 2018 Jun;2(6):1800046.
Bromma K, Chithrani DB. Advances in Gold Nanoparticle-Based Combined Cancer Therapy. Nanomaterials. 2020 Aug 26;10(9):1671.
Fratoddi I, Venditti I, Cametti C, Russo MV. The puzzle of toxicity of gold nanoparticles. The case-study of HeLa cells. Toxicol Res. 2015;4(4):796–800.
Park YS, Liz-Marzán LM, Kasuya A, Kobayashi Y, Nagao D, Konno M, et al. X-Ray Absorption of Gold Nanoparticles with Thin Silica Shell. j nanosci nanotechnol. 2006 Nov 1;6(11):3503–6.
Sani A, Cao C, Cui D. Toxicity of gold nanoparticles (AuNPs): A review. Biochemistry and Biophysics Reports. 2021 Jul;26:100991.
J. Yang C, B. Chithrani D. Nuclear Targeting of Gold Nanoparticles for Improved Therapeutics. CTMC. 2015 Oct 8;16(3):271–80.
Mendes R, Pedrosa P, Lima JC, Fernandes AR, Baptista PV. Photothermal enhancement of chemotherapy in breast cancer by visible irradiation of Gold Nanoparticles. Sci Rep. 2017 Sep 7;7(1):10872.
Li W, Cao Z, Liu R, Liu L, Li H, Li X, et al. AuNPs as an important inorganic nanoparticle applied in drug carrier systems. Artificial Cells, Nanomedicine, and Biotechnology. 2019 Dec 4;47(1):4222–33.
Bhumkar DR, Joshi HM, Sastry M, Pokharkar VB. Chitosan Reduced Gold Nanoparticles as Novel Carriers for Transmucosal Delivery of Insulin. Pharm Res. 2007 Jun 22;24(8):1415–26.
Rane TD, Armani AM. Two-Photon Microscopy Analysis of Gold Nanoparticle Uptake in 3D Cell Spheroids. Baptista PV, editor. PLoS ONE. 2016 Dec 9;11(12):e0167548.
Chithrani DB, Jelveh S, Jalali F, van Prooijen M, Allen C, Bristow RG, et al. Gold nanoparticles as radiation sensitizers in cancer therapy. Radiat Res. 2010 Jun;173(6):719–28.
Cruje C, Yang C, Uertz J, van Prooijen M, Chithrani BD. Optimization of PEG coated nanoscale gold particles for enhanced radiation therapy. RSC Adv. 2015;5(123):101525–32.
Souza GR, Molina JR, Raphael RM, Ozawa MG, Stark DJ, Levin CS, et al. Three-dimensional tissue culture based on magnetic cell levitation. Nature Nanotech. 2010 Apr;5(4):291–6.
Chen Y, Yang J, Fu S, Wu J. Gold Nanoparticles as Radiosensitizers in Cancer Radiotherapy. IJN. 2020 Nov;Volume 15:9407–30.
Musielak M, Boś-Liedke A, Piwocka O, Kowalska K, Markiewicz R, Szymkowiak B, et al. The Role of Functionalization and Size of Gold Nanoparticles in the Response of MCF-7 Breast Cancer Cells to Ionizing Radiation Comparing 2D and 3D In Vitro Models. Pharmaceutics. 2023 Mar 7;15(3):862.
Wang Y, Wang F, Chen Z, Song M, Yao X, Jiang G. In situ High-Throughput Single-Cell Analysis Reveals the Crosstalk between Nanoparticle-Induced Cell Responses. Environ Sci Technol. 2021 Apr 20;55(8):5136–42.
Guo F, Jiao Y, Du Y, Luo S, Hong W, Fu Q, et al. Enzyme-responsive nano-drug delivery system for combined antitumor therapy. International Journal of Biological Macromolecules. 2022 Nov;220:1133–45.
Nehmé A, Varadarajan P, Sellakumar G, Gerhold M, Niedner H, Zhang Q, et al. Modulation of docetaxel-induced apoptosis and cell cycle arrest by all- trans retinoic acid in prostate cancer cells. Br J Cancer. 2001 Jun 5;84(11):1571–6.
François A, Laroche A, Pinaud N, Salmon L, Ruiz J, Robert J, et al. Encapsulation of Docetaxel into PEGylated Gold Nanoparticles for Vectorization to Cancer Cells. ChemMedChem. 2011 Nov 4;6(11):2003–8.
Pawlik TM, Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. International Journal of Radiation Oncology*Biology*Physics. 2004 Jul;59(4):928–42.
Godet I, Doctorman S, Wu F, Gilkes DM. Detection of Hypoxia in Cancer Models: Significance, Challenges, and Advances. Cells. 2022 Feb 16;11(4):686.
Ideker T, Lauffenburger D. Building with a scaffold: emerging strategies for high- to low-level cellular modeling. Trends in Biotechnology. 2003 Jun;21(6):255–62.
Mó I, Sabino IJ, Melo-Diogo D de, Lima-Sousa R, Alves CG, Correia IJ. The importance of spheroids in analyzing nanomedicine efficacy. Nanomedicine. 2020 Jun;15(15):1513–25.
Bromma K, Alhussan A, Perez MM, Howard P, Beckham W, Chithrani DB. Three-Dimensional Tumor Spheroids as a Tool for Reliable Investigation of Combined Gold Nanoparticle and Docetaxel Treatment. Cancers. 2021 Mar 23;13(6):1465.
Huang K, Ma H, Liu J, Huo S, Kumar A, Wei T, et al. Size-Dependent Localization and Penetration of Ultrasmall Gold Nanoparticles in Cancer Cells, Multicellular Spheroids, and Tumors in Vivo. ACS Nano. 2012 May 22;6(5):4483–93.
Bugno J, Poellmann MJ, Sokolowski K, Hsu H jui, Kim DH, Hong S. Tumor penetration of Sub-10 nm nanoparticles: effect of dendrimer properties on their penetration in multicellular tumor spheroids. Nanomedicine: Nanotechnology, Biology and Medicine. 2019 Oct;21:102059.
Xie X, Liao J, Shao X, Li Q, Lin Y. The Effect of shape on Cellular Uptake of Gold Nanoparticles in the forms of Stars, Rods, and Triangles. Sci Rep. 2017 Jun 19;7(1):3827.
Huo S, Jin S, Ma X, Xue X, Yang K, Kumar A, et al. Ultrasmall Gold Nanoparticles as Carriers for Nucleus-Based Gene Therapy Due to Size-Dependent Nuclear Entry. ACS Nano. 2014 Jun 24;8(6):5852–62.
Nambara K, Niikura K, Mitomo H, Ninomiya T, Takeuchi C, Wei J, et al. Reverse Size Dependences of the Cellular Uptake of Triangular and Spherical Gold Nanoparticles. Langmuir. 2016 Nov 29;32(47):12559–67.
Jin S, Ma X, Ma H, Zheng K, Liu J, Hou S, et al. Surface chemistry-mediated penetration and gold nanorod thermotherapy in multicellular tumor spheroids. Nanoscale. 2013;5(1):143–6.
Kim JA, Åberg C, Salvati A, Dawson KA. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nature Nanotech. 2012 Jan;7(1):62–8.
Uboldi C, Bonacchi D, Lorenzi G, Hermanns MI, Pohl C, Baldi G, et al. Gold nanoparticles induce cytotoxicity in the alveolar type-II cell lines A549 and NCIH441. Part Fibre Toxicol. 2009;6(1):18.
Díez-Pascual AM. Surface Engineering of Nanomaterials with Polymers, Biomolecules, and Small Ligands for Nanomedicine. Materials. 2022 Apr 30;15(9):3251.
Li X, Hu Z, Ma J, Wang X, Zhang Y, Wang W, et al. The systematic evaluation of size-dependent toxicity and multi-time biodistribution of gold nanoparticles. Colloids and Surfaces B: Biointerfaces. 2018 Jul;167:260–6.
Jia YP, Ma BY, Wei XW, Qian ZY. The in vitro and in vivo toxicity of gold nanoparticles. Chinese Chemical Letters. 2017 Apr;28(4):691–702.
Musielak M, Boś-Liedke A, Piotrowski I, Kozak M, Suchorska W. The Role of Gold Nanorods in the Response of Prostate Cancer and Normal Prostate Cells to Ionizing Radiation—In Vitro Model. IJMS. 2020 Dec 22;22(1):16.
Kunz-Schughart LA, Freyer JP, Hofstaedter F, Ebner R. The Use of 3-D Cultures for High-Throughput Screening: The Multicellular Spheroid Model. SLAS Discovery. 2004 Jun;9(4):273–85.
Zhang. Toxicologic effects of gold nanoparticles in vivo by different administration routes. IJN. 2010 Sep;771.
Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA A Cancer J Clinicians. 2023 Jan;73(1):17–48.
This work is licensed under a Creative Commons Attribution-NoDerivatives 4.0 International License.
Copyright (c) 2023 Letters in Oncology Science