Human Cancer Cell Radiation Response Investigated through Topological Analysis of 2D Cell Networks.
Cancer diagnosis
Clonogenic assays
Networks analysis
Radiation therapy
Radio-resistance
Small world networks
Topology
Journal
Annals of biomedical engineering
ISSN: 1573-9686
Titre abrégé: Ann Biomed Eng
Pays: United States
ID NLM: 0361512
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
17
01
2023
accepted:
17
04
2023
medline:
10
7
2023
pubmed:
24
4
2023
entrez:
24
04
2023
Statut:
ppublish
Résumé
Clonogenic assays are routinely used to evaluate the response of cancer cells to external radiation fields, assess their radioresistance and radiosensitivity, estimate the performance of radiotherapy. However, classic clonogenic tests focus on the number of colonies forming on a substrate upon exposure to ionizing radiation, and disregard other important characteristics of cells such their ability to generate structures with a certain shape. The radioresistance and radiosensitivity of cancer cells may depend less on the number of cells in a colony and more on the way cells interact to form complex networks. In this study, we have examined whether the topology of 2D cancer-cell graphs is influenced by ionizing radiation. We subjected different cancer cell lines, i.e. H4 epithelial neuroglioma cells, H460 lung cancer cells, PC3 bone metastasis of grade IV of prostate cancer and T24 urinary bladder cancer cells, cultured on planar surfaces, to increasing photon radiation levels up to 6 Gy. Fluorescence images of samples were then processed to determine the topological parameters of the cell-graphs developing over time. We found that the larger the dose, the less uniform the distribution of cells on the substrate-evidenced by high values of small-world coefficient (cc), high values of clustering coefficient (cc), and small values of characteristic path length (cpl). For all considered cell lines, [Formula: see text] for doses higher or equal to 4 Gy, while the sensitivity to the dose varied for different cell lines: T24 cells seem more distinctly affected by the radiation, followed by the H4, H460 and PC3 cells. Results of the work reinforce the view that the characteristics of cancer cells and their response to radiotherapy can be determined by examining their collective behavior-encoded in a few topological parameters-as an alternative to classical clonogenic assays.
Identifiants
pubmed: 37093401
doi: 10.1007/s10439-023-03215-z
pii: 10.1007/s10439-023-03215-z
pmc: PMC10326123
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1859-1871Subventions
Organisme : Associazione Italiana per la Ricerca sul Cancro
ID : 25656
Organisme : H2020 Marie Skłodowska-Curie Actions
ID : 800924
Informations de copyright
© 2023. The Author(s).
Références
Aprile, F., V. Onesto, and F. Gentile. The small world coefficient 4.8±1 optimizes information processing in 2D neuronal networks. NPJ Syst. Biol. Appl. 8:1–11, 2022.
doi: 10.1038/s41540-022-00215-y
Barabási, A.-L. Network science. Glasgow: Cambridge University Press, p. 475, 2016.
Bullmore, E., and O. Sporns. The economy of brain network organization. Nat. Rev. Neurosci. 13:336–349, 2012.
doi: 10.1038/nrn3214
pubmed: 22498897
Carlos-Reyes, A., M. A. Muñiz-Lino, S. Romero-Garcia, C. López-Camarillo, and O. N. Hernández-de la Cruz. Biological adaptations of tumor cells to radiation therapy. Front. Oncol. 11:718636, 2021.
doi: 10.3389/fonc.2021.718636
pubmed: 34900673
pmcid: 8652287
Dunne, A. L. Relationship between clonogenic radiosensitivity, radiation-induced apoptosis and DNA damage/repair in human colon cancer cells. Br. J. Cancer. 89:2277–2283, 2003.
doi: 10.1038/sj.bjc.6601427
pubmed: 14676806
pmcid: 2395286
Franken, N. A. P., H. M. Rodermond, J. Stap, J. Haveman, and C. van Bree. Clonogenic assay of cells in vitro. Nat. Protoc. 1:2315–2319, 2006.
doi: 10.1038/nprot.2006.339
pubmed: 17406473
Gabaya, T., E. Jakobsa, E. Ben-Jacobb, and Y. Hanein. Engineered self-organization of neural networks using carbon nanotube clusters. Physica A. 350:611–621, 2005.
doi: 10.1016/j.physa.2004.11.007
Gray, M., A. K. Turnbull, J. Meehan, C. Martínez-Pérez, C. Kay, L. Y. Pang, and D. J. Argyle. Comparative analysis of the development of acquired radioresistance in canine and human mammary cancer cell lines. Front. Vet. Sci. 7:439, 2020.
doi: 10.3389/fvets.2020.00439
pubmed: 32851022
pmcid: 7396503
Humphries, M. D., and K. Gurney. Network ‘Small-World-Ness’: a quantitative method for determining canonical network equivalence. PLoS ONE.3:e0002051, 2008.
doi: 10.1371/journal.pone.0002051
pubmed: 18446219
Komoshvili, K., T. Becker, J. Levitan, A. Yahalom, A. Barbora, and S. Liberman-Aronov. Morphological changes in H1299 human lung cancer cells following w-band millimeter-wave irradiation. Appl. Sci. 10:3187, 2020.
doi: 10.3390/app10093187
Latora, V., and M. Marchiori. Efficient behavior of small-world networks. Phys. Rev. Lett.87:198701, 2001.
doi: 10.1103/PhysRevLett.87.198701
pubmed: 11690461
Matsui, T., E. Nuryadi, S. Komatsu, Y. Hirota, A. Shibata, T. Oike, and T. Nakano. Robustness of clonogenic assays as a biomarker for cancer cell radiosensitivity. Int. J. Mol. Sci. 20:4148, 2019.
doi: 10.3390/ijms20174148
pubmed: 31450688
pmcid: 6747107
Maurer, C., R. Qi, and V. Raghavan. A linear time algorithm for computing exact Euclidean distance transforms of binary images in arbitrary dimensions. IEEE Trans. Pattern Anal Mach. Intell. 25:265–270, 2003.
doi: 10.1109/TPAMI.2003.1177156
McIlwrath, A. J., P. A. Vasey, G. M. Ross, and R. Brown. Cell cycle arrests and radiosensitivity of human tumor cell lines: dependence on wild-type p53 for radiosensitivity. Cancer Res. 54:3718–3722, 1994.
pubmed: 8033090
Meyer, F. Topographic distance and watershed lines. Signal Process. 38:113–125, 1994.
doi: 10.1016/0165-1684(94)90060-4
Nuryadi, E., and T. Mayang-Permata. Inter-assay precision of clonogenic assays for radiosensitivity in cancer cell line A549. Oncotarget. 9:13706–13712, 2018.
doi: 10.18632/oncotarget.24448
pubmed: 29568388
pmcid: 5862609
Oike, T., S. Komatsu, Y. Komatsu, A. Nachankar, N. D. M. Darwis, A. Shibata, and T. Ohno. Reporting of methodologies used for clonogenic assays to determine radiosensitivity. J. Radiat. Res. 61:828–831, 2020.
doi: 10.1093/jrr/rraa064
pubmed: 32823284
pmcid: 7674694
Onesto, V., L. Cancedda, M. Coluccio, M. Nanni, M. Pesce, N. Malara, M. Cesarelli, E. D. Fabrizio, F. Amato, and F. Gentile. Nano-topography enhances communication in neural cells networks. Sci. Rep. 7:1–13, 2017.
doi: 10.1038/s41598-017-09741-w
Onesto, V., R. Narducci, F. Amato, L. Cancedda, and F. Gentile. The effect of connectivity on information in neural networks. Integrat. Biol. 10:121–127, 2018.
doi: 10.1039/C7IB00190H
Otsu, N. A threshold selection method from gray-level histograms. IEEE Trans. Syst. Man Cybern. 9:62–66, 1979.
doi: 10.1109/TSMC.1979.4310076
Ronny, Sham N., and F., N. Hasan, N. Abdul Hamid Hasani, M. K. Karim and M. J. Ibahim,. Study of morphological changes and survival fraction in EMT6 cell line post-gamma ray irradiation. J. Phys. 1497:012032, 2019.
Sia, J., R. Szmyd, E. Hau, and H. E. Gee. Molecular mechanisms of radiation-induced cancer cell death: a primer. Front. Cells Dev. Biol. 8:15, 2020.
Song, G., L. Cheng, Y. Chao, K. Yang, and Z. Liu. Emerging nanotechnology and advanced materials for cancer radiation therapy. Adv. Mater. 29:1–26, 2017.
doi: 10.1002/adma.201700996
Thompson, M. K., P. Poortmans, A. J. Chalmers, C. Faivre-Finn, E. Hall, R. A. Huddart, Y. Lievens, D. Sebag-Montefiore, and C. E. Coles. Practice-changing radiation therapy trials for the treatment of cancer: where are we 150 years after the birth of Marie Curie? Br. J. Cancer. 119:389–407, 2018.
doi: 10.1038/s41416-018-0201-z
pubmed: 30061587
pmcid: 6117262
Tirinato, L., V. Onesto, D. Garcia-Calderon, F. Pagliari, M.-F. Spadea, J. Seco, and F. Gentile. Human lung-cancer-cell radioresistance investigated through 2D network topology. Sci. Rep. 12:1–14, 2022.
doi: 10.1038/s41598-022-17018-0
Vassiliev, O. N. Accumulation of sublethal radiation damage and its effect on cell survival. Phys. Med. Biol. 68:015004, 2023.
doi: 10.1088/1361-6560/aca5e7
Voos, P., S. Fuck, F. Weipert, L. Babel, D. Tandl, T. Meckel, S. Hehlgans, C. Fournier, A. Moroni, F. Rödel, and G. Thiel. Ionizing radiation induces morphological changes and immunological modulation of Jurkat cells. Front. Immunol. 9:922, 2018.
doi: 10.3389/fimmu.2018.00922
pubmed: 29760710
pmcid: 5936756
Watts, D. J. Small worlds: The dynamics of networks between order and randomness. Woodstock: Princeton University Press, 2003.
Watts, D. J., and S. H. Strogatz. Collective dynamics of ‘small-world’ networks. Nature. 393:440–442, 1998.
doi: 10.1038/30918
pubmed: 9623998
Waxman, B. Routing of multipoint connections. IEEE J. Select. Areas Commun. 6:1617–1622, 1988.
doi: 10.1109/49.12889
Yasser, M., R. Shaikh, M. K. Chilakapati, and T. Teni. Raman spectroscopic study of radioresistant oral cancer sublines established by fractionated ionizing radiation. PLoS ONE. 9:e97777, 2014.
doi: 10.1371/journal.pone.0097777
pubmed: 24841281
pmcid: 4026477