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Mesenchymal Properties of Glioma Cell Lines

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Bulletin of Experimental Biology and Medicine Aims and scope

Screening of cell surface markers of three glioma cell lines (astrocytoma 1321N1, glioblastoma T98g, and glioblastoma astrocytoma U373 MG) was performed. Glioma cells expressed common mesenchymal cell markers, although the expression levels varied between the cell lines. The expression of proneural markers and glioma cancer stem cell markers was very low and also varied. Induction of differentiation towards the mesodermal cell lineages showed effective adipogenic and osteogenic differentiation for only the U373 MG cell line, while the 1321N1 and T98g lines demonstrated weak adipogenic potential and failed to undergo osteogenic differentiation. The obtained results point to the intratumor phenotypical heterogeneity of cells in gliomas and to the differences between the three studied types of gliomas with regard to the content of cells with mesenchymal phenotype.

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References

  1. Mohammed S, Dinesan M, Ajayakumar T. Survival and quality of life analysis in glioblastoma multiforme with adjuvant chemoradiotherapy: a retrospective study. Rep. Pract. Oncol. Radiother. 2022;27(6):1026-1036. https://doi.org/10.5603/RPOR.a2022.0113

    Article  PubMed  PubMed Central  Google Scholar 

  2. Seker-Polat F, Pinarbasi Degirmenci N, Solaroglu I, Bagci-Onder T. Tumor cell infiltration into the brain in glioblastoma: from mechanisms to clinical perspectives. Cancers (Basel). 2022;14(2):443. https://doi.org/10.3390/cancers14020443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Gisina A, Kholodenko I, Kim Y, Abakumov M, Lupatov A, Yarygin K. Glioma stem cells: novel data obtained by single-cell sequencing. Int. J. Mol. Sci. 2022;23(22):14224. https://doi.org/10.3390/ijms232214224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Behnan J, Finocchiaro G, Hanna G. The landscape of the mesenchymal signature in brain tumours. Brain. 2019;142(4):847-866. https://doi.org/10.1093/brain/awz044

    Article  PubMed  PubMed Central  Google Scholar 

  5. Dénes A, Bontell TO, Barchéus H, Vega SF, Carén H, Lindskog C, Jakola AS, Smits A. The clinical value of proneural, classical and mesenchymal protein signatures in WHO 2021 adult-type diffuse lower-grade gliomas. PLoS One. 2023;18(5):e0285732. https://doi.org/10.1371/journal.pone.0285732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Joo KM, Kim J, Jin J, Kim M, Seol HJ, Muradov J, Yang H, Choi YL, Park WY, Kong DS, Lee JI, Ko YH, Woo HG, Lee J, Kim S, Nam DH. Patient-specific orthotopic glioblastoma xenograft models recapitulate the histopathology and biology of human glioblastomas in situ. Cell Rep. 2013;3(1):260-273. https://doi.org/10.1016/j.celrep.2012.12.013

    Article  CAS  PubMed  Google Scholar 

  7. Garnier D, Renoult O, Alves-Guerra MC, Paris F, Pecqu-eur C. Glioblastoma stem- like cells, metabolic strategy to kill a challenging target. Front. Oncol. 2019;9:118. https://doi.org/10.3389/fonc.2019.00118

    Article  PubMed  PubMed Central  Google Scholar 

  8. Mao P, Joshi K, Li J, Kim SH, Li P, Santana-Santos L, Luthra S, Chandran UR, Benos PV, Smith L, Wang M, Hu B, Cheng SY, Sobol RW, Nakano I. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc. Natl Acad. Sci. USA. 2013;110(21):8644-8649. https://doi.org/10.1073/pnas.1221478110

    Article  PubMed  PubMed Central  Google Scholar 

  9. Halliday J, Helmy K, Pattwell SS, Pitter KL, LaPlant Q, Ozawa T, Holland EC. In vivo radiation response of proneural glioma characterized by protective p53 transcriptional program and proneural-mesenchymal shift. Proc. Natl Acad. Sci. USA. 2014;111(14):5248-5253. https://doi.org/10.1073/pnas.1321014111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, Williams PM, Modrusan Z, Feuerstein BG, Aldape K. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006;9(3):157-173. https://doi.org/10.1016/j.ccr.2006.02.019

    Article  CAS  PubMed  Google Scholar 

  11. Tso CL, Shintaku P, Chen J, Liu Q, Liu J, Chen Z, Yoshimoto K, Mischel PS, Cloughesy TF, Liau LM, Nelson SF. Primary glioblastomas express mesenchymal stem-like properties. Mol. Cancer Res. 2006;4(9):607-619. https://doi.org/10.1158/1541-7786.MCR-06-0005

    Article  CAS  PubMed  Google Scholar 

  12. Gelsleichter NE, Azambuja JH, Rubenich DS, Braganhol E. CD73 in glioblastoma: Where are we now and what are the future directions? Immunol. Lett. 2023;256-257:20-27. https://doi.org/10.1016/j.imlet.2023.03.005

    Article  CAS  PubMed  Google Scholar 

  13. Bastos AGP, Carvalho B, Silva R, Leitão D, Linhares P, Vaz R, Lima J. Endoglin (CD105) and proliferation index in recurrent glioblastoma treated with anti-angiogenic therapy. Front. Oncol. 2022;12:910196. https://doi.org/10.3389/fonc.2022.910196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Li J, Ek F, Olsson R, Belting M, Bengzon J. Glioblastoma CD105+ cells define a SOX2— cancer stem cell-like subpopulation in the pre-invasive niche. Acta Neuropathol. Commun. 2022;10(1):126. https://doi.org/10.1186/s40478-022-01422-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Drachsler M, Kleber S, Mateos A, Volk K, Mohr N, Chen S, Cirovic B, Tüttenberg J, Gieffers C, Sykora J, Wirtz CR, Mueller W, Synowitz M, Martin-Villalba A. CD95 maintains stem cell-like and non-classical EMT programs in primary human glioblastoma cells. Cell Death Dis. 2016;7(4):e2209. https://doi.org/10.1038/cddis.2016.102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tchoghandjian A, Baeza N, Colin C, Cayre M, Metellus P, Beclin C, Ouafik L, Figarella-Branger D. A2B5 cells from human glioblastoma have cancer stem cell properties. Brain Pathol. 2010;20(1):211-221. https://doi.org/10.1111/j.1750-3639.2009.00269.x

    Article  PubMed  Google Scholar 

  17. Figarella-Branger D, Colin C, Baeza-Kallee N, Tchoghandjian A. A2B5 expression in central nervous system and gliomas. Int. J. Mol. Sci. 2022;23(9):4670. https://doi.org/10.3390/ijms23094670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Auvergne RM, Sim FJ, Wang S, Chandler-Militello D, Burch J, Al Fanek Y, Davis D, Benraiss A, Walter K, Achanta P, Johnson M, Quinones-Hinojosa A, Natesan S, Ford HL, Goldman SA. Transcriptional differences between normal and glioma-derived glial progenitor cells identify a core set of dysregulated genes. Cell Rep. 2013;3(6):2127-2141. https://doi.org/10.1016/j.celrep.2013.04.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Gilliam DT, Menon V, Bretz NP, Pruszak J. The CD24 surface antigen in neural development and disease. Neurobiol. Dis. 2017;99:133-144. https://doi.org/10.1016/j.nbd.2016.12.011

    Article  CAS  PubMed  Google Scholar 

  20. Deng J, Gao G, Wang L, Wang T, Yu J, Zhao Z. CD24 expression as a marker for predicting clinical outcome in human gliomas. J. Biomed. Biotechnol. 2012;2012:517172. https://doi.org/10.1155/2012/517172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Haddock S, Alban TJ, Turcan Ş, Husic H, Rosiek E, Ma X, Wang Y, Bale T, Desrichard A, Makarov V, Monette S, Wu W, Gardner R, Manova K, Boire A, Chan TA. Phenotypic and molecular states of IDH1 mutation-induced CD24-positive glioma stem-like cells. Neoplasia. 2022;28:100790. https://doi.org/10.1016/j.neo.2022.100790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Heinzen D, Divé I, Lorenz NI, Luger AL, Steinbach JP, Ronellenfitsch MW. Second generation mTOR inhibitors as a double-edged sword in malignant glioma treatment. Int. J. Mol. Sci. 2019;20(18):4474. https://doi.org/10.3390/ijms20184474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Patil V, Pal J, Somasundaram K. Elucidating the cancer-specific genetic alteration spectrum of glioblastoma derived cell lines from whole exome and RNA sequencing. Oncotarget. 2015;6(41):43452-43471. https://doi.org/10.18632/oncotarget.6171

    Article  PubMed  PubMed Central  Google Scholar 

  24. Ditlevsen DK, Povlsen GK, Berezin V, Bock E. NCAM-induced intracellular signaling revisited. J. Neurosci. Res. 2008;86(4):727-743. https://doi.org/10.1002/jnr.21551

    Article  CAS  PubMed  Google Scholar 

  25. Balik V, Mirossay P, Bohus P, Sulla I, Mirossay L, Sarissky M. Flow cytometry analysis of neural differentiation markers expression in human glioblastomas may predict their response to chemotherapy. Cell Mol. Neurobiol. 2009;29(6-7):845-858. https://doi.org/10.1007/s10571-009-9366-6

    Article  CAS  PubMed  Google Scholar 

  26. Yang M, Adla S, Temburni MK, Patel VP, Lagow EL, Brady OA, Tian J, Boulos MI, Galileo DS. Stimulation of glioma cell motility by expression, proteolysis, and release of the L1 neural cell recognition molecule. Cancer Cell Int. 2009;9:27. https://doi.org/10.1186/1475-2867-9-27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kholodenko IV, Kalinovsky DV, Doronin II, Deyev SM, Kholodenko RV. Neuroblastoma origin and therapeutic targets for immunotherapy. J. Immunol. Res. 2018;2018:7394268. https://doi.org/10.1155/2018/7394268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Woo SR, Oh YT, An JY, Kang BG, Nam DH, Joo KM. Glioblastoma specific antigens, GD2 and CD90, are not involved in cancer stemness. Anat. Cell Biol. 2015;48(1):44-53. https://doi.org/10.5115/acb.2015.48.1.44

    Article  PubMed  PubMed Central  Google Scholar 

  29. Mabe NW, Huang M, Dalton GN, Alexe G, Schaefer DA, Geraghty AC, Robichaud AL, Conway AS, Khalid D, Mader MM, Belk JA, Ross KN, Sheffer M, Linde MH, Ly N, Yao W, Rotiroti MC, Smith BAH, Wernig M, Bertozzi CR, Monje M, Mitsiades CS, Majeti R, Satpathy AT, Stegmaier K, Majzner RG. Transition to a mesenchymal state in neuroblastoma confers resistance to anti-GD2 antibody via reduced expression of ST8SIA1. Nat. Cancer. 2022;3(8):976-993. https://doi.org/10.1038/s43018-022-00405-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Liu J, Wang X, Chen AT, Gao X, Himes BT, Zhang H, Chen Z, Wang J, Sheu WC, Deng G, Xiao Y, Zou P, Zhang S, Liu F, Zhu Y, Fan R, Patel TR, Saltzman WM, Zhou J. ZNF117 regulates glioblastoma stem cell differentiation towards oligodendroglial lineage. Nat. Commun. 2022;13(1):2196. https://doi.org/10.1038/s41467-022-29884-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Uneda A, Kurozumi K, Fujimura A, Fujii K, Ishida J, Shimazu Y, Otani Y, Tomita Y, Hattori Y, Matsumoto Y, Tsuboi N, Makino K, Hirano S, Kamiya A, Date I. Differentiated glioblastoma cells accelerate tumor progression by shaping the tumor microenvironment via CCN1-mediated macrophage infiltration. Acta Neuropathol. Commun. 2021;9(1):29. https://doi.org/10.1186/s40478-021-01124-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sun Y, Jiang Y, Wang Y, Yu P, Su X, Song Y, Wang M, Li Y, Zhao L. The epithelial-mesenchymal transition of glioma cells promotes tissue factor expression via the miR200a/ZEB1 axis. Brain Res. 2022;1778:147782. https://doi.org/10.1016/j.brainres.2022.147782

    Article  CAS  PubMed  Google Scholar 

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Correspondence to R. V. Kholodenko.

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Translated from Kletochnye Tekhnologii v Biologii i Meditsine, No. 3, pp. 147-156, September, 2024

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Kholodenko, I.V., Lupatov, A.Y., Kim, Y.S. et al. Mesenchymal Properties of Glioma Cell Lines. Bull Exp Biol Med 178, 122–129 (2024). https://doi.org/10.1007/s10517-024-06294-7

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  • DOI: https://doi.org/10.1007/s10517-024-06294-7

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