{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T09:02:23Z","timestamp":1789635743581,"version":"4.0.0"},"reference-count":28,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2026,8,14]],"date-time":"2026-08-14T00:00:00Z","timestamp":1786665600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2026,8,14]],"date-time":"2026-08-14T00:00:00Z","timestamp":1786665600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["24-14-00250"],"award-info":[{"award-number":["24-14-00250"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Biochem Biophys"],"DOI":"10.1007\/s12013-026-02121-0","type":"journal-article","created":{"date-parts":[[2026,8,14]],"date-time":"2026-08-14T07:07:40Z","timestamp":1786691260000},"page":"4321-4330","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Long-Term Culture of U87MG Glioblastoma Cells Reprograms Metabolism, Impacts Aggressiveness and Alters Drug Responses"],"prefix":"10.1007","volume":"84","author":[{"given":"Alina A.","family":"Isakova","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadezhda V.","family":"Antipova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diana V.","family":"Mazur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Irina N.","family":"Druzhkova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alena I.","family":"Gavrina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margarita L.","family":"Shuvalova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga I.","family":"Patsap","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry A.","family":"Bondarenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arkadiy N.","family":"Murashev","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mikhail P.","family":"Kirpichnikov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marine E.","family":"Gasparian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne V.","family":"Yagolovich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry A.","family":"Dolgikh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2026,8,14]]},"reference":[{"issue":"8","key":"2121_CR1","doi-asserted-by":"publisher","first-page":"2049","DOI":"10.1002\/bit.28496","volume":"120","author":"CP Prasad","year":"2023","unstructured":"Prasad, C. P., Tripathi, S. C., Kumar, M., & Mohapatra, P. (2023). Passage number of cancer cell lines: Importance, intricacies, and way-forward. Biotechnology and Bioengineering, 120(8), 2049\u20132055. https:\/\/doi.org\/10.1002\/bit.28496","journal-title":"Biotechnology and Bioengineering"},{"key":"2121_CR2","doi-asserted-by":"publisher","first-page":"27","DOI":"10.21037\/tbcr-24-36","volume":"5","author":"A Podsednik","year":"2024","unstructured":"Podsednik, A., Xu, H. N., & Li, L. Z. (2024). Passage dependence of NADH redox status and reactive oxygen species level in vitro in triple-negative breast cancer cell lines with different invasiveness. Translational Breast Cancer Research, 5, 27\u201327. https:\/\/doi.org\/10.21037\/tbcr-24-36","journal-title":"Translational Breast Cancer Research"},{"issue":"12","key":"2121_CR3","doi-asserted-by":"publisher","first-page":"798","DOI":"10.31083\/ph.2015.5106","volume":"70","author":"SMDKG Senarathna","year":"2015","unstructured":"Senarathna, S. M. D. K. G., & Crowe, A. (2015). The influence of passage number for Caco2 cell models when evaluating P-gp mediated drug transport. Die Pharmazie, 70(12), 798\u2013803.","journal-title":"Die Pharmazie"},{"issue":"3","key":"2121_CR4","doi-asserted-by":"publisher","first-page":"1582","DOI":"10.1021\/acs.jproteome.0c00806","volume":"20","author":"J Cao","year":"2021","unstructured":"Cao, J., Wu, X., Qin, X., & Li, Z. (2021). Uncovering the Effect of Passage Number on HT29 Cell Line Based on the Cell Metabolomic Approach. Journal of Proteome Research, 20(3), 1582\u20131590. https:\/\/doi.org\/10.1021\/acs.jproteome.0c00806","journal-title":"Journal of Proteome Research"},{"issue":"1","key":"2121_CR5","doi-asserted-by":"publisher","first-page":"e1000832","DOI":"10.1371\/journal.pgen.1000832","volume":"6","author":"MJ Clark","year":"2010","unstructured":"Clark, M. J., Homer, N., O\u2019Connor, B. D., Chen, Z., Eskin, A., Lee, H., & Nelson, S. F. (2010). U87MG Decoded: The Genomic Sequence of a Cytogenetically Aberrant Human Cancer Cell Line. PLoS Genetics, 6(1), e1000832. https:\/\/doi.org\/10.1371\/journal.pgen.1000832","journal-title":"PLoS Genetics"},{"issue":"6","key":"2121_CR6","doi-asserted-by":"publisher","first-page":"1245","DOI":"10.1007\/s10571-018-0592-7","volume":"38","author":"Y Zeng","year":"2018","unstructured":"Zeng, Y., Wang, X., Wang, J., Yi, R., Long, H., Zhou, M., & Qi, S. (2018). The Tumorgenicity of Glioblastoma Cell Line U87MG Decreased During Serial In Vitro Passage. Cellular and Molecular Neurobiology, 38(6), 1245\u20131252. https:\/\/doi.org\/10.1007\/s10571-018-0592-7","journal-title":"Cellular and Molecular Neurobiology"},{"key":"2121_CR7","doi-asserted-by":"publisher","unstructured":"Alhaddad, L., Nofal, Z., Pustovalova, M., Osipov, A. N., & Leonov, S. (2023). Long-Term Cultured Human Glioblastoma Multiforme Cells Demonstrate Increased Radiosensitivity and Senescence-Associated Secretory Phenotype in Response to Irradiation. International Journal of Molecular Sciences, 24(3), 2002. https:\/\/doi.org\/10.3390\/ijms24032002","DOI":"10.3390\/ijms24032002"},{"key":"2121_CR8","doi-asserted-by":"publisher","unstructured":"Wang, L., Jin, H., Jochems, F., Wang, S., Lieftink, C., Martinez, I. M., \u2026 Bernards,R. (2022). cFLIP suppression and DR5 activation sensitize senescent cancer cells to senolysis. Nature Cancer, 3(11), 1284\u20131299. https:\/\/doi.org\/10.1038\/s43018-022-00462-2.","DOI":"10.1038\/s43018-022-00462-2."},{"issue":"6","key":"2121_CR9","doi-asserted-by":"publisher","first-page":"627","DOI":"10.1134\/S0006297919060051","volume":"84","author":"AV Yagolovich","year":"2019","unstructured":"Yagolovich, A. V., Artykov, A. A., Dolgikh, D. A., Kirpichnikov, M. P., & Gasparian, M. E. (2019). A New Efficient Method for Production of Recombinant Antitumor Cytokine TRAIL and Its Receptor-Selective Variant DR5-B. Biochemistry (Moscow), 84(6), 627\u2013636. https:\/\/doi.org\/10.1134\/S0006297919060051","journal-title":"Biochemistry (Moscow)"},{"key":"2121_CR10","doi-asserted-by":"publisher","unstructured":"Gray, D. A., & Woulfe, J. (2005). Lipofuscin and Aging: A Matter of Toxic Waste. Science of Aging Knowledge Environment, 2005(5). https:\/\/doi.org\/10.1126\/sageke.2005.5.re1","DOI":"10.1126\/sageke.2005.5.re1"},{"key":"2121_CR11","doi-asserted-by":"publisher","unstructured":"Pak, V. V., Ezeri\u0146a, D., Lyublinskaya, O. G., Pedre, B., Tyurin-Kuzmin, P. A., Mishina,N. M., \u2026 Belousov, V. V. (2020). Ultrasensitive Genetically Encoded Indicator for Hydrogen Peroxide Identifies Roles for the Oxidant in Cell Migration and Mitochondrial Function. Cell Metabolism, 31(3), 642\u2013653.e6. https:\/\/doi.org\/10.1016\/j.cmet.2020.02.003.","DOI":"10.1016\/j.cmet.2020.02.003."},{"issue":"9","key":"2121_CR12","doi-asserted-by":"publisher","first-page":"6226","DOI":"10.3390\/ijms12096226","volume":"12","author":"SH Park","year":"2011","unstructured":"Park, S. H., Ozden, O., Jiang, H., Cha, Y. I., Pennington, J. D., Aykin-Burns, N., & Kim, H. S. (2011). Sirt3, Mitochondrial ROS, Ageing, and Carcinogenesis. International Journal of Molecular Sciences, 12(9), 6226\u20136239. https:\/\/doi.org\/10.3390\/ijms12096226","journal-title":"International Journal of Molecular Sciences"},{"issue":"9","key":"2121_CR13","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1016\/j.molmed.2012.05.004","volume":"18","author":"LWS Finley","year":"2012","unstructured":"Finley, L. W. S., & Haigis, M. C. (2012). Metabolic regulation by SIRT3: implications for tumorigenesis. Trends in Molecular Medicine, 18(9), 516\u2013523. https:\/\/doi.org\/10.1016\/j.molmed.2012.05.004","journal-title":"Trends in Molecular Medicine"},{"key":"2121_CR14","doi-asserted-by":"publisher","first-page":"969812","DOI":"10.3389\/fonc.2022.969812","volume":"12","author":"M Morelli","year":"2022","unstructured":"Morelli, M., Lessi, F., Barachini, S., Liotti, R., Montemurro, N., Perrini, P., & Mazzanti, C. M. (2022). Metabolic-imaging of human glioblastoma live tumors: A new precision-medicine approach to predict tumor treatment response early. Frontiers in Oncology, 12, 969812. https:\/\/doi.org\/10.3389\/fonc.2022.969812","journal-title":"Frontiers in Oncology"},{"issue":"1","key":"2121_CR15","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1038\/s42003-024-06123-7","volume":"7","author":"A Song","year":"2024","unstructured":"Song, A., Zhao, N., Hilpert, D. C., Perry, C., Baur, J. A., Wallace, D. C., & Schaefer, P. M. (2024). Visualizing subcellular changes in the NAD(H) pool size versus redox state using fluorescence lifetime imaging microscopy of NADH. Communications Biology, 7(1), 428. https:\/\/doi.org\/10.1038\/s42003-024-06123-7","journal-title":"Communications Biology"},{"key":"2121_CR16","doi-asserted-by":"publisher","unstructured":"Isakova, A. A., Mazur, D. V., Antipova, N. V., Druzhkova, I. N., Mozherov, \u0410. \u041c., Krasnov, K. S., \u2026 Yagolovich, A. V. (2025). Temozolomide-induced senescent glioblastoma cells acquire sensitivity to TRAIL death receptor 5-mediated apoptosis. Medical Oncology, 43(1), 4. https:\/\/doi.org\/10.1007\/s12032-025-03130-4.","DOI":"10.1007\/s12032-025-03130-4."},{"key":"2121_CR17","doi-asserted-by":"publisher","first-page":"897839","DOI":"10.3389\/fonc.2022.897839","volume":"12","author":"D Yuzhakova","year":"2022","unstructured":"Yuzhakova, D., Kiseleva, E., Shirmanova, M., Shcheslavskiy, V., Sachkova, D., Snopova, L., & Baklaushev, V. (2022). Highly Invasive Fluorescent\/Bioluminescent Patient-Derived Orthotopic Model of Glioblastoma in Mice. Frontiers in Oncology, 12, 897839. https:\/\/doi.org\/10.3389\/fonc.2022.897839","journal-title":"Frontiers in Oncology"},{"key":"2121_CR18","doi-asserted-by":"publisher","unstructured":"Pokorn\u00e1, M., Hudec, M., Ju\u0159\u00ed\u010dkov\u00e1, I., V\u00e1cha, M., Pol\u00edvkov\u00e1, Z., K\u00fatna, V., \u2026 O\u2019Leary,V. B. (2021). All-Trans Retinoic Acid Fosters the Multifarious U87MG Cell Line as a Model of Glioblastoma. Brain Sciences, 11(6), 812. https:\/\/doi.org\/10.3390\/brainsci11060812.","DOI":"10.3390\/brainsci11060812."},{"issue":"2","key":"2121_CR19","doi-asserted-by":"publisher","first-page":"e32117","DOI":"10.1371\/journal.pone.0032117","volume":"7","author":"C Lawless","year":"2012","unstructured":"Lawless, C., Jurk, D., Gillespie, C. S., Shanley, D., Saretzki, G., Von Zglinicki, T., & Passos, J. F. (2012). A Stochastic Step Model of Replicative Senescence Explains ROS Production Rate in Ageing Cell Populations. Plos One, 7(2), e32117. https:\/\/doi.org\/10.1371\/journal.pone.0032117","journal-title":"Plos One"},{"key":"2121_CR20","doi-asserted-by":"publisher","unstructured":"Yin, H., Liu, Y., Dong, Q., Wang, H., Yan, Y., Wang, X., \u2026 Pan, Y. (2024). The mechanism of extracellular CypB promotes glioblastoma adaptation to glutamine deprivation microenvironment.Cancer Letters, 597, 216862. https:\/\/doi.org\/10.1016\/j.canlet.2024.216862.","DOI":"10.1016\/j.canlet.2024.216862."},{"issue":"8","key":"2121_CR21","doi-asserted-by":"publisher","first-page":"740","DOI":"10.1038\/s41419-022-05175-z","volume":"13","author":"K Luo","year":"2022","unstructured":"Luo, K., Liu, A., Wu, H., Liu, Q., Dai, J., Liu, Y., & Wang, Z. (2022). CircKIF4A promotes glioma growth and temozolomide resistance by accelerating glycolysis. Cell Death & Disease, 13(8), 740. https:\/\/doi.org\/10.1038\/s41419-022-05175-z","journal-title":"Cell Death & Disease"},{"issue":"24","key":"2121_CR22","doi-asserted-by":"publisher","first-page":"e71331","DOI":"10.1096\/fj.202503048R","volume":"39","author":"X Li","year":"2025","unstructured":"Li, X., Guo, F., Xu, L., & Piao, H. (2025). TRIM67 Suppresses Glioblastoma Glycolysis and Increases Temozolomide Sensitivity by Promoting ARSD Ubiquitinated Degradation to Inactivate the \u03b2-Catenin Pathway. The FASEB Journal, 39(24), e71331. https:\/\/doi.org\/10.1096\/fj.202503048R","journal-title":"The FASEB Journal"},{"issue":"4","key":"2121_CR23","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1016\/j.bbrc.2008.05.148","volume":"372","author":"D Kwon","year":"2008","unstructured":"Kwon, D., Choi, K., Choi, C., & Benveniste, E. N. (2008). Hydrogen peroxide enhances TRAIL-induced cell death through up-regulation of DR5 in human astrocytic cells. Biochemical and Biophysical Research Communications, 372(4), 870\u2013874. https:\/\/doi.org\/10.1016\/j.bbrc.2008.05.148","journal-title":"Biochemical and Biophysical Research Communications"},{"key":"2121_CR24","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.freeradbiomed.2017.01.004","volume":"104","author":"S Galadari","year":"2017","unstructured":"Galadari, S., Rahman, A., Pallichankandy, S., & Thayyullathil, F. (2017). Reactive oxygen species and cancer paradox: To promote or to suppress? Free Radical Biology and Medicine, 104, 144\u2013164. https:\/\/doi.org\/10.1016\/j.freeradbiomed.2017.01.004","journal-title":"Free Radical Biology and Medicine"},{"key":"2121_CR25","doi-asserted-by":"publisher","unstructured":"Torsvik, A., Stieber, D., Enger, P. \u00d8., Golebiewska, A., Molven, A., Svendsen, A.,\u2026 Bjerkvig, R. (2014). U-251 revisited: genetic drift and phenotypic consequences of long\u2010term cultures of glioblastoma cells. Cancer Medicine, 3(4), 812\u2013824. https:\/\/doi.org\/10.1002\/cam4.219.","DOI":"10.1002\/cam4.219."},{"key":"2121_CR26","doi-asserted-by":"publisher","unstructured":"Mouriaux, F., Zaniolo, K., Bergeron, M.-A., Weidmann, C., De La Fouchardi\u00e8re, A.,Fournier, F., \u2026 Gu\u00e9rin, S. L. (2016). Effects of Long-term Serial Passaging on the Characteristics and Properties of Cell Lines Derived From Uveal Melanoma Primary Tumors.Investigative Opthalmology & Visual Science, 57(13), 5288. https:\/\/doi.org\/10.1167\/iovs.16-19317.","DOI":"10.1167\/iovs.16-19317."},{"key":"2121_CR27","doi-asserted-by":"publisher","unstructured":"Allen, M., Bjerke, M., Edlund, H., Nelander, S., & Westermark, B. (2016). Origin of the U87MG glioma cell line: Good news and bad news. Science Translational Medicine, 8(354). https:\/\/doi.org\/10.1126\/scitranslmed.aaf6853","DOI":"10.1126\/scitranslmed.aaf6853"},{"issue":"1","key":"2121_CR28","doi-asserted-by":"publisher","first-page":"44984","DOI":"10.1038\/s41598-025-29424-1","volume":"15","author":"S Liu","year":"2025","unstructured":"Liu, S., Peng, H., Meng, J., Zhuo, L., Fu, S., & Yang, W. (2025). Cell passage number drives transcriptomic drift as an overlooked factor in experimental reproducibility. Scientific Reports, 15(1), 44984. https:\/\/doi.org\/10.1038\/s41598-025-29424-1","journal-title":"Scientific Reports"}],"container-title":["Cell Biochemistry and Biophysics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12013-026-02121-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12013-026-02121-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12013-026-02121-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T08:13:41Z","timestamp":1789632821000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12013-026-02121-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,14]]},"references-count":28,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["2121"],"URL":"https:\/\/doi.org\/10.1007\/s12013-026-02121-0","relation":{},"ISSN":["1559-0283"],"issn-type":[{"value":"1559-0283","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,14]]},"assertion":[{"value":"5 July 2026","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 August 2026","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All procedures with animals in this study were carried out in accordance with relevant guidelines and regulations and approved by the Institutional Commission for the Care and Use of Animals (IACUC) of BIBCH RAS for compliance with ethical requirements for the treatment of laboratory animals (protocol no. 841\/22).","order":1,"name":"Ethics","label":"Ethics information","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","label":"Conflict of Interests","group":{"name":"EthicsHeading","label":"Declarations"}}]}}