Enhanced Glycolysis Confers Resistance Against Photon but Not Carbon Ion Irradiation in Human Glioma Cell Lines

References

• Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004;4(11):891–899. doi:10.1038/nrc1478
   PubMed Web of Science ®Google Scholar
• Cairns RA, Harris IS, Mak TW. Regulation of cancer cell metabolism. Nat Rev Cancer. 2011;11:85–95. doi:10.1038/nrc2981
   PubMed Web of Science ®Google Scholar
• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144:646–674. doi:10.1016/j.cell.2011.02.013
   PubMed Web of Science ®Google Scholar
• Faubert B, Solmonson A, DeBerardinis RJ. Metabolic reprogramming and cancerprogression. Science. 2020;368:6487. doi:10.1126/science.aaw5473
   Web of Science ®Google Scholar
• Hanahan D. Hallmarks of Cancer: new Dimensions. Cancer Discov. 2022;12:31–46. doi:10.1158/2159-8290.CD-21-1059
   PubMed Web of Science ®Google Scholar
• Miranda-Galvis M, Teng Y. Targeting hypoxia-driven metabolic reprogramming to constrain tumor progression and metastasis. Int J Mol Sci. 2020;21(15):5487. doi:10.3390/ijms21155487
   PubMed Web of Science ®Google Scholar
• Singh S, Pandey S, Chawla AS, et al. Dietary 2-deoxy-D-glucose impairs tumor growth and metastasis by inhibiting angiogenesis. Eur J Cancer. 2019;123:11–24. doi:10.1016/j.ejca.2019.09.005
   PubMed Web of Science ®Google Scholar
• Prasanna VK, Venkataramana NK, Dwarakanath BS, Santhosh V. Differential responses of tumors and normal brain to the combined treatment of 2-DG and radiation in glioblastoma. J Cancer Res Ther. 2009;1:S44–7.
   Google Scholar
• Gupta S, Farooque A, Adhikari JS, Singh S, Dwarakanath BS. Enhancement of radiation and chemotherapeutic drug responses by 2-deoxy-D-glucose in animal tumors. J Cancer Res Ther. 2009;S16–20. doi:10.4103/0973-1482.55135
   PubMed Web of Science ®Google Scholar
• Dwarakanath BS. Cytotoxicity, radiosensitization, and chemosensitization of tumor cells by 2-deoxy-D-glucose in vitro. J Cancer Res Ther. 2009;1:S27–31. doi:10.4103/0973-1482.55137
   Google Scholar
• Farooque A, Singh N, Adhikari JS, Afrin F, Dwarakanath BS. Enhanced antitumor immunity contributes to the radio-sensitization of Ehrlich ascites tumor by the glycolytic inhibitor 2-deoxy-D-glucose in mice. PLoS One. 2014;9(9):e108131. doi:10.1371/journal.pone.0108131
   PubMed Web of Science ®Google Scholar
• Farooque A, Afrin F, Adhikari JS, Dwarakanath BS. Polarization of macrophages towards M1 phenotype by a combination of 2-deoxy-d-glucose and radiation: implications for tumor therapy. Immunobiology. 2016;221(2):269–281. doi:10.1016/j.imbio.2015.10.009
   PubMed Web of Science ®Google Scholar
• Gupta S, Roy A, Dwarakanath BS. Metabolic cooperation and competition in the tumor microenvironment: implications for therapy. Front Oncol. 2017;7:68. doi:10.3389/fonc.2017.00068
   PubMed Web of Science ®Google Scholar
• Singh S, Pandey S, Chawla AS, et al. Dietary 2-deoxy-D-glucose impairs tumor growth and metastasis by inhibiting angiogenesis. Eur J Cancer. 2019;123:11–24.
   PubMed Web of Science ®Google Scholar
• Dwarakanath BS, Singh D, Banerji AK, et al. Clinical studies for improving radiotherapy with 2-deoxy-D-glucose: present status and future prospects. J Cancer Res Ther. 2009;1:S21–6. doi:10.4103/0973-1482.55136
   Google Scholar
• Heminger K, Jain V, Kadakia M, Dwarakanath B, Berberich SJ. Altered gene expression induced by ionizing radiation and glycolytic inhibitor 2-deoxy-glucose in a human glioma cell line: implications for radiosensitization. Cancer Biol Ther. 2006;5(7):815–823. doi:10.4161/cbt.5.7.2812
   PubMed Web of Science ®Google Scholar
• Mohanti BK, Rath GK, Anantha N, et al. Improving cancer radiotherapy with 2-deoxy-D-glucose: Phase I/II clinical trials on human cerebral gliomas. Int J Radiat Oncol Biol Phys. 1996;35(1):103–111. doi:10.1016/S0360-3016(96)85017-6
   PubMed Web of Science ®Google Scholar
• Schulz A, Meyer F, Dubrovska A, Borgmann K. Cancer Stem Cells and Radioresistance: DNA Repair and Beyond. Cancers. 2019;11(6):862. doi:10.3390/cancers11060862
   PubMed Web of Science ®Google Scholar
• Sertorio M, Perentesis JP, Vatner RE, Mascia AE, Zheng Y, Wells SI. Cancer Cell Metabolism: implications for X-ray and Particle Radiation Therapy. Int J Part Ther. 2018;5(1):40–48. doi:10.14338/IJPT-18-00023.1
   PubMedGoogle Scholar
• Bhatt AN, Chauhan A, Khanna S, et al. Transient elevation of glycolysis confers radio-resistance by facilitating DNA repair in cells. BMC Cancer. 2015;1(15):335. doi:10.1186/s12885-015-1368-9
   Google Scholar
• Cook KM, Shen H, McKelvey KJ, Gee HE, Hau E. Targeting glucose metabolism of cancer cells with dichloroacetate to radiosensitize high-grade gliomas. Int J Mol Sci. 2021;22(14):7265. doi:10.3390/ijms22147265
   PubMed Web of Science ®Google Scholar
• Shen H, Decollogne S, Dilda PJ, et al. Dual-targeting of aberrant glucose metabolism in glioblastoma. J Exp Clin Cancer Res. 2015;34(1):14. doi:10.1186/s13046-015-0130-0
   PubMedGoogle Scholar
• Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–996. doi:10.1056/NEJMoa043330
   PubMed Web of Science ®Google Scholar
• Loeffler JS, Durante M. Charged particle therapy--optimization, challenges and future directions. Nat Rev Clin Oncol. 2013;10(7):411–424. doi:10.1038/nrclinonc.2013.79
   PubMed Web of Science ®Google Scholar
• Durante M, Orecchia R, Loeffler JS. Charged particle therapy in cancer: clinical uses and future perspectives. Nat Rev Clin Oncol. 2017;14(8):483–495. doi:10.1038/nrclinonc.2017.30
   PubMed Web of Science ®Google Scholar
• Durante M, Loeffler JS. Charged particles in radiation oncology. Nat Rev Clin Oncol. 2010;7:37–43. doi:10.1038/nrclinonc.2009.183
   PubMed Web of Science ®Google Scholar
• Durante M, Flanz J. Charged particle beams to cure cancer: strengths and challenges. Semin Oncol. 2019;46(3):219–225. doi:10.1053/j.seminoncol.2019.07.007
   PubMed Web of Science ®Google Scholar
• Yoshida GJ. Metabolic reprogramming: the emerging concept and associated therapeutic strategies. J Exp Clin Cancer Res. 2015;34:111. doi:10.1186/s13046-015-0221-y
   PubMed Web of Science ®Google Scholar
• Bhatt AN, Chauhan A, Khanna S, et al. Transient elevation of glycolysis confers radio-resistance by facilitating DNA repair in cells. BMC Cancer. 2015;15:335.
   PubMed Web of Science ®Google Scholar
• Bao C, Sun Y, Dwarakanath B, et al. Carbon ion triggered immunogenic necroptosis of nasopharyngeal carcinoma cells involving necroptotic inhibitor BCL-x. J Cancer. 2021;12(5):1520–1530. doi:10.7150/jca.46316
   PubMed Web of Science ®Google Scholar
• Bao C, Sun Y, Dong Y, Le Z, Lin L-C. The relative biological effectiveness of proton and carbon ion beams in photon-sensitive and resistant nasopharyngeal cancer cells. Translate Cancer Res. 2018;7:548.
   Web of Science ®Google Scholar
• Bing Z, Yang G, Zhang Y, et al. Proteomic analysis of effects by x-rays and heavy ion in HeLa cells. Radiol Oncol. 2014;48(2):142–154. doi:10.2478/raon-2013-0087
   PubMed Web of Science ®Google Scholar
• Kumar V, Vashishta M, Kong L, et al. Carbon Ion Irradiation Downregulates Notch Signaling in Glioma Cell Lines, Impacting Cell Migration and Spheroid Formation. Cells. 2022;11(21):3354. doi:10.3390/cells11213354
   PubMed Web of Science ®Google Scholar
• Fenech M. Cytokinesis-block micronucleus cytome assay. Nat Protoc. 2007;2(5):1084–1104. doi:10.1038/nprot.2007.77
   PubMed Web of Science ®Google Scholar
• Pawlik TM, Keyomathe K. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 2004;59:928–942. doi:10.1016/j.ijrobp.2004.03.005
   PubMed Web of Science ®Google Scholar
• Durante M, Formenti SC. Radiation-Induced Chromosomal Aberrations and Immunotherapy: micronuclei, Cytosolic DNA, and Interferon-Production Pathway. Front Oncol. 2018;8:192. doi:10.3389/fonc.2018.00192
   PubMed Web of Science ®Google Scholar
• Verma A, Venkateswaran K, Farooque A, et al. Cytotoxic and radio- sensitizingradio-sensitizing effects of polyphenolic acetates in a human glioma cell line (BMG-1). Curr Pharm Des. 2020;2020(7):1161–1169.
   Google Scholar
• Dwarakanath BS. Cytotoxicity, radiosensitization, and chemosensitization of tumor cells by 2-deoxy-D-glucose in vitro. J Cancer Res Ther. 2009;5(Suppl 1):S27–31.
   PubMedGoogle Scholar
• Fei Y, Xiong Y, Shen X, et al. Cathepsin L promotes ionizing radiation-induced U251 glioma cell migration and invasion through regulating the GSK-3β/CUX1 pathway. Cell Signal. 2018;44:62–71. doi:10.1016/j.cellsig.2018.01.012
   PubMed Web of Science ®Google Scholar
• Rieken S, Habermehl D, Wuerth L, et al. Carbon ion irradiation inhibits glioma cell migration through downregulation of integrin expression. Int J Radiat Oncol Biol Phys. 2012;83(1):394–399. doi:10.1016/j.ijrobp.2011.06.2004
   PubMed Web of Science ®Google Scholar
• Yan S, Wang Y, Yang Q, et al. Low-dose radiation-induced epithelial-mesenchymal transition through NF-κB in cervical cancer cells. Int J Oncol. 2013;42(5):1801–1806. doi:10.3892/ijo.2013.1852
   PubMed Web of Science ®Google Scholar
• Koppenol WH, Bounds PL, Dang CV. Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer. 2011;11(5):325–337. doi:10.1038/nrc3038
   PubMed Web of Science ®Google Scholar
• Schwartz L, Supuran CT, Alfarouk KO, Warburg T. Effect and the Hallmarks of Cancer. Anticancer Agents Med Chem. 2017;17(2):164–170. doi:10.2174/1871520616666161031143301
   PubMed Web of Science ®Google Scholar
• Moncharmont C, Guy JB, Wozny AS, et al. Carbon ion irradiation withstands cancer stem cells’ migration/invasion process in Head and Neck Squamous Cell Carcinoma (HNSCC). Oncotarget. 2016;7(30):47738–47749. doi:10.18632/oncotarget.10281
   PubMedGoogle Scholar
• Chiblak S, Tang Z, Lemke D, et al. Carbon irradiation overcomes glioma radioresistance by eradicating stem cells and forming an antiangiogenic and immunopermissive niche. JCI Insight. 2019;4(2):e123837. doi:10.1172/jci.insight.123837
   PubMed Web of Science ®Google Scholar
• Rai Y, Anita KN, Singh S, Kalra N, Soni R, Bhatt AN. Mild mitochondrial uncoupling protects from ionizing radiation-induced cell death by attenuating oxidative stress and mitochondrial damage. Biochem Biophys Acta Bioenerg. 2021;1862(1):148325. doi:10.1016/j.bbabio.2020.148325
   PubMed Web of Science ®Google Scholar
• Okayasu R. Repair of DNA damage induced by accelerated heavy ions--a mini review. Int J Cancer. 2012;130(5):991–1000. doi:10.1002/ijc.26445
   PubMed Web of Science ®Google Scholar
• Oike T, Niimi A, Okonogi N, et al. Visualization of complex DNA double-strand breaks in a tumor treated with carbon ion radiotherapy. Sci Rep. 2016;6:22275. doi:10.1038/srep22275
   PubMed Web of Science ®Google Scholar
• Kam WWY, Banati RB. Effects of ionizing radiation on mitochondria. Free Radic Biol Med. 2013;65:607–619. doi:10.1016/j.freeradbiomed.2013.07.024
   PubMed Web of Science ®Google Scholar
• Azzam EI, Jay-Gerin JP, Pain D. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 2012;327(1–2):48–60. doi:10.1016/j.canlet.2011.12.012
   PubMed Web of Science ®Google Scholar
• Lu J, Tan M, Cai Q. The Warburg effect in tumor progression: mitochondrial oxidative metabolism as an anti-metastasis mechanism. Cancer Lett. 2015;356(2Pt A):156–164. doi:10.1016/j.canlet.2014.04.001
   PubMedGoogle Scholar
• Zhou YC, Liu JY, Li J, et al. Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition. Int J Radiat Oncol Biol Phys. 2011;81(5):1530–1537. doi:10.1016/j.ijrobp.2011.06.1956
   PubMed Web of Science ®Google Scholar
• Wozny AS, Vares G, Alphonse G, et al. ROS Production and Distribution: a New Paradigm to Explain the Differential Effects of X-ray and Carbon Ion Irradiation on Cancer Stem Cell Migration and Invasion. Cancers. 2019;11(4):468. doi:10.3390/cancers11040468
   PubMed Web of Science ®Google Scholar
• Khaitan D, Chandna S, Arya MB, Dwarakanath BS. Differential mechanisms of radiosensitization by 2-deoxy-D-glucose in the monolayers and multicellular spheroids of a human glioma cell line. Cancer Biol Ther. 2006;5(9):1142–1151. doi:10.4161/cbt.5.9.2986
   PubMed Web of Science ®Google Scholar
• Dwarakanath BS, Jain VK. Modification of the radiation-induced damage by 2-deoxy-D-glucose in organ cultures of human cerebral gliomas. Int J Radiat Oncol Biol Phys. 1987;13(5):741–746. doi:10.1016/0360-3016(87)90293-8
   PubMed Web of Science ®Google Scholar
• Taghizadeh-Hesary F, Akbari H, Bahadori M, Behnam B. Targeted Anti-Mitochondrial Therapy: the Future of Oncology. Genes. 2022;13(10):1728. doi:10.3390/genes13101728
   PubMed Web of Science ®Google Scholar
• Ray S, Cekanaviciute E, Lima IP, Sørensen BS, Costes SV. Comparing Photon and Charged Particle Therapy Using DNA Damage Biomarkers. Int J Part Ther. 2018;5(1):15–24. doi:10.14338/IJPT-18-00018.1
   PubMedGoogle Scholar