Ion Transport and Radioresistance.
DNA damage response
Hypoxia adaptation
Ion channels
Ion transport
Oncochannels
Radiogenic reprogramming
Radioresistance
Journal
Reviews of physiology, biochemistry and pharmacology
ISSN: 0303-4240
Titre abrégé: Rev Physiol Biochem Pharmacol
Pays: Germany
ID NLM: 0434624
Informations de publication
Date de publication:
2022
2022
Historique:
pubmed:
2
8
2020
medline:
7
5
2022
entrez:
2
8
2020
Statut:
ppublish
Résumé
Neoplastic transformation is associated with alterations of the ion transports across plasma and intracellular membranes. These alterations are crucial elements of the phenotypical reprogramming of the transformed cells and may promote adaptation to hypoxia, malignant progression, tumor spreading and metastasis, as well as therapy resistance. The present review article focuses on ion transport processes in tumor cells that are induced by ionizing radiation and that contribute to radioresistance and therapy failure. In particular, this article introduces radiogenic ion transports across plasma and mitochondrial membranes and discusses their functional significance for cell cycle control, DNA repair, accelerated repopulation, cell migration and metastasis, metabolic reprogramming, adaptation to hypoxia, and radiogenic formation of reactive oxygen species.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
217-249Informations de copyright
© 2020. Springer Nature Switzerland AG.
Références
Anoopkumar-Dukie S, Conere T, Sisk GD et al (2009) Mitochondrial modulation of oxygen-dependent radiosensitivity in some human tumour cell lines. Br J Radiol 82:847–854
pubmed: 19366737
Archer SL, Gomberg-Maitland M, Maitland ML et al (2008) Mitochondrial metabolism, redox signaling, and fusion: a mitochondria-ROS-HIF-1alpha-K
pubmed: 18083891
Arif T, Stern O, Pittala S et al (2019) Rewiring of cancer cell metabolism by mitochondrial VDAC1 depletion results in time-dependent tumor reprogramming: Glioblastoma as a proof of concept. Cell 8:1330
Arthur GK, Duffy SM, Roach KM et al (2015) KCa3.1 K+ channel expression and function in human bronchial epithelial cells. PLoS One 10:e0145259
pubmed: 26689552
pmcid: 4687003
Ataga KI, Smith WR, De Castro LM et al (2008) Efficacy and safety of the Gardos channel blocker, senicapoc (ICA-17043), in patients with sickle cell anemia. Blood 111:3991–3997
pubmed: 18192510
Averaimo S, Milton RH, Duchen MR et al (2010) Chloride intracellular channel 1 (CLIC1): sensor and effector during oxidative stress. FEBS Lett 584:2076–2084
pubmed: 20385134
Baffy G (2017) Mitochondrial uncoupling in cancer cells: liabilities and opportunities. Biochim Biophys Acta Bioenerg 1858:655–664
pubmed: 28088333
Bauer TM, Murphy E (2020) Role of mitochondrial calcium and the permeability transition pore in regulating cell death. Circ Res 126:280–293
pubmed: 31944918
pmcid: 8317591
Birch JL, Strathdee K, Gilmour L et al (2018) A novel small-molecule inhibitor of MRCK prevents radiation-driven invasion in Glioblastoma. Cancer Res 78:6509–6522
pubmed: 30279244
Bouchard G, Therriault H, Geha S et al (2017) Radiation-induced lung metastasis development is MT1-MMP-dependent in a triple-negative breast cancer mouse model. Br J Cancer 116:479–488
pubmed: 28103615
pmcid: 5318978
Brahimi-Horn MC, Ben-Hail D, Ilie M et al (2012) Expression of a truncated active form of VDAC1 in lung cancer associates with hypoxic cell survival and correlates with progression to chemotherapy resistance. Cancer Res 72:2140–2150
pubmed: 22389449
Braun N, Klumpp D, Hennenlotter J et al (2015) UCP-3 uncoupling protein confers hypoxia resistance to renal epithelial cells and is upregulated in renal cell carcinoma. Sci Rep 5:13450
pubmed: 26304588
pmcid: 4548255
Brisson L, Gillet L, Calaghan S et al (2011) Na
pubmed: 21170089
Brisson L, Driffort V, Benoist L et al (2013) Na
pubmed: 23902689
Britschgi A, Bill A, Brinkhaus H et al (2013) Calcium-activated chloride channel ANO1 promotes breast cancer progression by activating EGFR and CAMK signaling. Proc Natl Acad Sci U S A 110:E1026–E1034
pubmed: 23431153
pmcid: 3600458
Brown A, Geiger H (2018) Chromosome integrity checkpoints in stem and progenitor cells: transitions upon differentiation, pathogenesis, and aging. Cell Mol Life Sci 75:3771–3779
pubmed: 30066086
pmcid: 6154040
Cadenas S (2018) Mitochondrial uncoupling, ROS generation and cardioprotection. Biochim Biophys Acta Bioenerg 1859:940–950
pubmed: 29859845
Campbell TM, Main MJ, Fitzgerald EM (2013) Functional expression of the voltage-gated Na
pubmed: 23986482
Chao HX, Poovey CE, Privette AA et al (2017) Orchestration of DNA damage checkpoint dynamics across the human cell cycle. Cell Syst 5:445–459.e445
pubmed: 29102360
pmcid: 5700845
Chen JM, Sepramaniam S, Armugam A et al (2008) Water and ion channels: crucial in the initiation and progression of apoptosis in central nervous system? Curr Neuropharmacol 6:102–116
Chen TJ, He HL, Shiue YL et al (2018) High chloride channel accessory 1 expression predicts poor prognoses in patients with rectal cancer receiving chemoradiotherapy. Int J Med Sci 15:1171–1178
pubmed: 30123054
pmcid: 6097263
Cheng Y, Debska-Vielhaber G, Siemen D (2010) Interaction of mitochondrial potassium channels with the permeability transition pore. FEBS Lett 584:2005–2012
pubmed: 20036666
Cloos CR, Daniels DH, Kalen A et al (2009) Mitochondrial DNA depletion induces radioresistance by suppressing G
pubmed: 19580493
pmcid: 2707769
Cone CD Jr, Cone CM (1976) Induction of mitosis in mature neurons in central nervous system by sustained depolarization. Science 192:155–158
pubmed: 56781
Cone CD Jr, Tongier M Jr (1971) Control of somatic cell mitosis by simulated changes in the transmembrane potential level. Oncology 25:168–182
pubmed: 5148061
Coultrap SJ, Bayer KU (2012) CaMKII regulation in information processing and storage. Trends Neurosci 35:607–618
pubmed: 22717267
pmcid: 3461103
Crottes D, Jan LY (2019) The multifaceted role of TMEM16A in cancer. Cell Calcium 82:102050
pubmed: 31279157
pmcid: 6711484
Cruz-Gregorio A, Martinez-Ramirez I, Pedraza-Chaverri J et al (2019) Reprogramming of energy metabolism in response to radiotherapy in head and neck squamous cell carcinoma. Cancers (Basel) 11:182
Cuddapah VA, Sontheimer H (2010) Molecular interaction and functional regulation of ClC-3 by Ca
pubmed: 20139089
pmcid: 2856996
Cuddapah VA, Habela CW, Watkins S et al (2012) Kinase activation of ClC-3 accelerates cytoplasmic condensation during mitotic cell rounding. Am J Physiol Cell Physiol 302:C527–C538
pubmed: 22049206
Cuddapah VA, Turner KL, Seifert S et al (2013) Bradykinin-induced chemotaxis of human gliomas requires the activation of KCa3.1 and ClC-3. J Neurosci 33:1427–1440
pubmed: 23345219
pmcid: 3711544
D’alessandro G, Catalano M, Sciaccaluga M et al (2013) KCa3.1 channels are involved in the infiltrative behavior of glioblastoma in vivo. Cell Death Dis 4:e773
pubmed: 23949222
pmcid: 3763441
D’alessandro G, Monaco L, Catacuzzeno L et al (2019) Radiation increases functional KCa3.1 expression and invasiveness in glioblastoma. Cancers (Basel) 11:279
Davies A, Hendrich J, Van Minh AT et al (2007) Functional biology of the alpha
pubmed: 17403543
Davis FM, Peters AA, Grice DM et al (2012) Non-stimulated, agonist-stimulated and store-operated Ca
pubmed: 22666335
pmcid: 3364242
Denko NC (2008) Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat Rev Cancer 8:705–713
pubmed: 19143055
Dittmann K, Mayer C, Kehlbach R et al (2008) Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol Cancer 7:69
pubmed: 18789131
pmcid: 2546440
Dittmann K, Mayer C, Kehlbach R et al (2009) Radiation-induced lipid peroxidation activates SRC kinase and triggers nuclear EGFR transport. Radiother Oncol 92:379–382
pubmed: 19560222
Dittmann K, Mayer C, Rodemann HP et al (2013) EGFR cooperates with glucose transporter SGLT1 to enable chromatin remodeling in response to ionizing radiation. Radiother Oncol 107:247–251
pubmed: 23602371
Dittmann K, Mayer C, Paasch A et al (2015) Nuclear EGFR renders cells radio-resistant by binding mRNA species and triggering a metabolic switch to increase lactate production. Radiother Oncol 116:431–437
pubmed: 26320552
Djamgoz MBA, Fraser SP, Brackenbury WJ (2019) In vivo evidence for voltage-gated Sodium Channel expression in carcinomas and potentiation of metastasis. Cancers (Basel) 11:1675
Driffort V, Gillet L, Bon E et al (2014) Ranolazine inhibits Na
pubmed: 25496128
pmcid: 4295566
Dupre AM, Hempling HG (1978) Osmotic properties of Ehrlich ascites tumor cells during the cell cycle. J Cell Physiol 97:381–396
pubmed: 569663
Eckert F, Schilbach K, Klumpp L et al (2018) Potential role of CXCR4 targeting in the context of radiotherapy and immunotherapy of cancer. Front Immunol 9:3018
pubmed: 30622535
pmcid: 6308162
Eckert F, Zwirner K, Boeke S et al (2019) Rationale for combining radiotherapy and immune checkpoint inhibition for patients with hypoxic tumors. Front Immunol 10:407
pubmed: 30930892
pmcid: 6423917
Edalat L, Stegen B, Klumpp L et al (2016) BK K
pubmed: 26893360
pmcid: 4924713
Eke I, Storch K, Kastner I et al (2012) Three-dimensional invasion of human glioblastoma cells remains unchanged by X-ray and carbon ion irradiation in vitro. Int J Radiat Oncol Biol Phys 84:e515–e523
pubmed: 22901381
Ewing D (1998) The oxygen fixation hypothesis: a reevaluation. Am J Clin Oncol 21:355–361
pubmed: 9708633
Faubert B, Solmonson A, Deberardinis RJ (2020) Metabolic reprogramming and cancer progression. Science 368(6487):eaaw5473
Foller M, Bobbala D, Koka S et al (2010) Functional significance of the intermediate conductance Ca
pubmed: 20857305
Fraser SP, Diss JK, Chioni AM et al (2005) Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin Cancer Res 11:5381–5389
pubmed: 16061851
Fu C, Cao CM, Xia Q et al (2003) Reactive oxygen species and mitochondrial KATP-sensitive channels mediated cardioprotection induced by TNF-alpha during hypoxia and reoxygenation. Sheng Li Xue Bao 55:284–289
pubmed: 12817295
Gibhardt CS, Roth B, Schroeder I et al (2015) X-ray irradiation activates K+ channels via H2O2 signaling. Sci Rep 5:13861
pubmed: 26350345
pmcid: 4642570
Gillet L, Roger S, Besson P et al (2009) Voltage-gated sodium channel activity promotes cysteine cathepsin-dependent invasiveness and colony growth of human cancer cells. J Biol Chem 284:8680–8691
pubmed: 19176528
pmcid: 2659227
Gonzalez-Gonzalez L, Gonzalez-Ramirez R, Flores A et al (2019) Epidermal growth factor potentiates migration of MDA-MB 231 breast cancer cells by increasing Na
pubmed: 31430760
Gopel SO, Kanno T, Barg S et al (2000) Patch-clamp characterisation of somatostatin-secreting -cells in intact mouse pancreatic islets. J Physiol 528:497–507
pubmed: 11060127
pmcid: 2270149
Gu XQ, Siemen D, Parvez S et al (2007) Hypoxia increases BK channel activity in the inner mitochondrial membrane. Biochem Biophys Res Commun 358:311–316
pubmed: 17481584
Gu XQ, Pamenter ME, Siemen D et al (2014) Mitochondrial but not plasmalemmal BK channels are hypoxia-sensitive in human glioma. Glia 62:504–513
pubmed: 24446243
Gueguinou M, Chantome A, Fromont G et al (1843) K
Guo L, Tang X, Tian H et al (2008) Subacute hypoxia suppresses K
pubmed: 18430420
Heise N, Palme D, Misovic M et al (2010) Non-selective cation channel-mediated Ca
pubmed: 21063097
Holley AK, Miao L, St Clair DK et al (2014) Redox-modulated phenomena and radiation therapy: the central role of superoxide dismutases. Antioxid Redox Signal 20:1567–1589
pubmed: 24094070
pmcid: 3942704
Hu J, Qin K, Zhang Y et al (2011) Downregulation of transcription factor Oct4 induces an epithelial-to-mesenchymal transition via enhancement of Ca
pubmed: 21798248
Huang L, Li B, Tang S et al (2015) Mitochondrial KATP channels control glioma radioresistance by regulating ROS-induced ERK activation. Mol Neurobiol 52:626–637
pubmed: 25249341
Huang Y, Fliegert R, Guse AH et al (2020) A structural overview of the ion channels of the TRPM family. Cell Calcium 85:102111
pubmed: 31812825
Huber SM (2013) Oncochannels. Cell Calcium 53:241–255
pubmed: 23357407
Huber SM, Tschop J, Braun GS et al (1999) Bradykinin-stimulated Cl
pubmed: 10370087
Huber SM, Misovic M, Mayer C et al (2012) EGFR-mediated stimulation of sodium/glucose cotransport promotes survival of irradiated human A549 lung adenocarcinoma cells. Radiother Oncol 103:373–379
pubmed: 22516777
Huber SM, Butz L, Stegen B et al (2013) Ionizing radiation, ion transports, and radioresistance of cancer cells. Front Physiol 4:212
pubmed: 23966948
pmcid: 3743404
Jentsch TJ, Pusch M (2018) CLC chloride channels and transporters: structure, function, physiology, and disease. Physiol Rev 98:1493–1590
pubmed: 29845874
Jesse RH, Lindberg RD (1975) The efficacy of combining radiation therapy with a surgical procedure in patients with cervical metastasis from squamous cancer of the oropharynx and hypopharynx. Cancer 35:1163–1166
pubmed: 1116107
Kaczmarek LK, Zhang Y (2017) Kv3 channels: enablers of rapid firing, neurotransmitter release, and neuronal endurance. Physiol Rev 97:1431–1468
pubmed: 28904001
pmcid: 6151494
Kandasamy SB, Howerton TC, Hunt WA (1991) Reductions in calcium uptake induced in rat brain synaptosomes by ionizing radiation. Radiat Res 125:158–162
pubmed: 1996373
Kaplan HS, Murphy ED (1949) The effect of local roentgen irradiation on the biological behavior of a transplantable mouse carcinoma; increased frequency of pulmonary metastasis. J Natl Cancer Inst 9:407–413
pubmed: 18153815
Kim JS, Chang JW, Yun HS et al (2010) Chloride intracellular channel 1 identified using proteomic analysis plays an important role in the radiosensitivity of HEp-2 cells via reactive oxygen species production. Proteomics 10:2589–2604
pubmed: 20461716
Kim MJ, Kim RK, Yoon CH et al (2011) Importance of PKC
pubmed: 21878493
Kim W, Lee S, Seo D et al (2019) Cellular stress responses in radiotherapy. Cell 8:1105
Kizub IV, Pavlova OO, Ivanova IV et al (2010) Protein kinase C-dependent inhibition of BK
pubmed: 20353339
Klumpp D, Misovic M, Szteyn K et al (2016a) Targeting TRPM2 channels impairs radiation-induced cell cycle arrest and fosters cell death of T cell leukemia cells in a Bcl-2-dependent manner. Oxidative Med Cell Longev 2016:8026702
Klumpp L, Sezgin EC, Eckert F et al (2016b) Ion channels in brain metastasis. Int J Mol Sci 17:1513
Klumpp D, Frank SC, Klumpp L et al (2017) TRPM8 is required for survival and radioresistance of glioblastoma cells. Oncotarget 8:95896–95913
pubmed: 29221175
pmcid: 5707069
Klumpp L, Sezgin EC, Skardelly M et al (2018) KCa3.1 channels and glioblastoma: in vitro studies. Curr Neuropharmacol 16:627–635
pubmed: 28786347
pmcid: 5997865
Krebs C (1929) Effect of roentgen irradiation on the interrelation between malignant tumors and their hosts. Acta Radiol Supp 8:1–133
Kulawiak B, Kudin AP, Szewczyk A et al (2008) BK channel openers inhibit ROS production of isolated rat brain mitochondria. Exp Neurol 212:543–547
pubmed: 18572168
Kunzelmann K, Ousingsawat J, Benedetto R et al (2019) Contribution of Anoctamins to cell survival and cell death. Cancers (Basel) 11:382
Kyrychenko S, Tishkin S, Dosenko V et al (2012) The BK(Ca) channels deficiency as a possible reason for radiation-induced vascular hypercontractility. Vasc Pharmacol 56:142–149
Lang F, Pelzl L, Hauser S et al (2018) To die or not to die SGK1-sensitive ORAI/STIM in cell survival. Cell Calcium 74:29–34
pubmed: 29807219
Leach JK, Van Tuyle G, Lin PS et al (2001) Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61:3894–3901
pubmed: 11358802
Leanza L, O'reilly P, Doyle A et al (2014) Correlation between potassium channel expression and sensitivity to drug-induced cell death in tumor cell lines. Curr Pharm Des 20:189–200
pubmed: 23701546
Li F, Sonveaux P, Rabbani ZN et al (2007) Regulation of HIF-1alpha stability through S-nitrosylation. Mol Cell 26:63–74
pubmed: 17434127
pmcid: 2905600
Lin S, Lv Y, Xu J et al (2019) Over-expression of Na
pubmed: 31672162
pmcid: 6824047
Littler DR, Harrop SJ, Goodchild SC et al (2010) The enigma of the CLIC proteins: ion channels, redox proteins, enzymes, scaffolding proteins? FEBS Lett 584:2093–2101
pubmed: 20085760
Liu W, Lu M, Liu B et al (2012) Inhibition of Ca
pubmed: 22820160
Liu J, Chen Y, Shuai S et al (2014) TRPM8 promotes aggressiveness of breast cancer cells by regulating EMT via activating AKT/GSK-3
pubmed: 24903376
Mahdi SH, Cheng H, Li J et al (2015) The effect of TGF-beta-induced epithelial-mesenchymal transition on the expression of intracellular calcium-handling proteins in T47D and MCF-7 human breast cancer cells. Arch Biochem Biophys 583:18–26
pubmed: 26247838
Maldonado EN (2017) VDAC-tubulin, an anti-Warburg pro-oxidant switch. Front Oncol 7:4
pubmed: 28168164
pmcid: 5256068
Martin OA, Anderson RL, Russell PA et al (2014) Mobilization of viable tumor cells into the circulation during radiation therapy. Int J Radiat Oncol Biol Phys 88:395–403
pubmed: 24315565
Masumoto K, Tsukimoto M, Kojima S (2013) Role of TRPM2 and TRPV1 cation channels in cellular responses to radiation-induced DNA damage. Biochim Biophys Acta 1830:3382–3390
pubmed: 23458684
Matsuya Y, Ohtsubo Y, Tsutsumi K et al (2014) Quantitative estimation of DNA damage by photon irradiation based on the microdosimetric-kinetic model. J Radiat Res 55:484–493
pubmed: 24515253
pmcid: 4014172
Mazure NM (2016) News about VDAC1 in hypoxia. Front Oncol 6:193
pubmed: 27625993
pmcid: 5004482
Meng Y, Xu X, Luan H et al (2019) The progress and development of GLUT1 inhibitors targeting cancer energy metabolism. Future Med Chem 11:2333–2352
pubmed: 31581916
Miranda-Goncalves V, Granja S, Martinho O et al (2016) Hypoxia-mediated upregulation of MCT1 expression supports the glycolytic phenotype of glioblastomas. Oncotarget 7:46335–46353
pubmed: 27331625
pmcid: 5216802
Mohammed FH, Khajah MA, Yang M et al (2016) Blockade of voltage-gated sodium channels inhibits invasion of endocrine-resistant breast cancer cells. Int J Oncol 48:73–83
pubmed: 26718772
Mohr CJ, Gross D, Sezgin EC et al (2019) K
Munro TR (1970) The relative radiosensitivity of the nucleus and cytoplasm of Chinese hamster fibroblasts. Radiat Res 42:451–470
pubmed: 5463516
Nagy JA, Chang SH, Dvorak AM et al (2009) Why are tumour blood vessels abnormal and why is it important to know? Br J Cancer 100:865–869
pubmed: 19240721
pmcid: 2661770
Neher E, Sakmann B (1976) Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260:799–802
pubmed: 1083489
Nelson M, Yang M, Dowle AA et al (2015a) The sodium channel-blocking antiepileptic drug phenytoin inhibits breast tumour growth and metastasis. Mol Cancer 14:13
pubmed: 25623198
pmcid: 4320839
Nelson M, Yang M, Millican-Slater R et al (2015b) Nav1.5 regulates breast tumor growth and metastatic dissemination in vivo. Oncotarget 6:32914–32929
pubmed: 26452220
pmcid: 4741739
Nishino K, Tanamachi K, Nakanishi Y et al (2016) Radiosensitizing effect of TRPV1 channel inhibitors in cancer cells. Biol Pharm Bull 39:1224–1230
pubmed: 27150432
Noyer L, Grolez GP, Prevarskaya N et al (2018) TRPM8 and prostate: a cold case? Pflugers Arch 470:1419–1429
pubmed: 29926226
Ogawa K, Utsunomiya T, Mimori K et al (2006) Differential gene expression profiles of radioresistant pancreatic cancer cell lines established by fractionated irradiation. Int J Oncol 28:705–713
pubmed: 16465376
Palme D, Misovic M, Schmid E et al (2013) K
pubmed: 23443853
Palme D, Misovic M, Ganser K et al (2020) hERG K
pubmed: 32390841
pmcid: 7194033
Peitzsch C, Perrin R, Hill RP et al (2014) Hypoxia as a biomarker for radioresistant cancer stem cells. Int J Radiat Biol 90:636–652
pubmed: 24844374
Peng JB, Suzuki Y, Gyimesi G et al (2018) TRPV5 and TRPV6 calcium-selective channels. In: Kozak JA, Putney JW Jr (eds) Calcium entry channels in non-excitable cells. CRC Press, Taylor & Francis Group, Boca Raton, pp 241–274
Proudfoot JM, Murrey MW, Mclean S et al (2018) F2-isoprostanes affect macrophage migration and CSF-1 signalling. Free Radic Biol Med 126:142–152
pubmed: 30096434
Qu Y, Zhang H, Zhao S et al (2010) The effect on radioresistance of manganese superoxide dismutase in nasopharyngeal carcinoma. Oncol Rep 23:1005–1011
pubmed: 20204285
Ravi M, Paramesh V, Kaviya SR et al (2015) 3D cell culture systems: advantages and applications. J Cell Physiol 230:16–26
pubmed: 24912145
Redfern A, Agarwal V, Thompson EW (2019) Hypoxia as a signal for prison breakout in cancer. Curr Opin Clin Nutr Metab Care 22:250–263
pubmed: 31116106
Reisz JA, Bansal N, Qian J et al (2014) Effects of ionizing radiation on biological molecules--mechanisms of damage and emerging methods of detection. Antioxid Redox Signal 21:260–292
pubmed: 24382094
pmcid: 4060780
Richardson RB, Harper ME (2016) Mitochondrial stress controls the radiosensitivity of the oxygen effect: implications for radiotherapy. Oncotarget 7:21469–21483
pubmed: 26894978
pmcid: 5008299
Rodemann HP, Dittmann K, Toulany M (2007) Radiation-induced EGFR-signaling and control of DNA-damage repair. Int J Radiat Biol 83:781–791
pubmed: 18058366
Roth B, Gibhardt CS, Becker P et al (2015) Low-dose photon irradiation alters cell differentiation via activation of hIK channels. Pflugers Arch 467:1835–1849
pubmed: 25277267
Ruggieri P, Mangino G, Fioretti B et al (2012) The inhibition of K
pubmed: 23110108
pmcid: 3478269
Ruoslahti E (1996) Brain extracellular matrix. Glycobiology 6:489–492
pubmed: 8877368
Sala-Rabanal M, Yurtsever Z, Nichols CG et al (2015) Secreted CLCA1 modulates TMEM16A to activate Ca
Sanguinetti MC (2010) HERG1 channelopathies. Pflugers Arch 460:265–276
pubmed: 20544339
Sausbier M, Hu H, Arntz C et al (2004) Cerebellar ataxia and Purkinje cell dysfunction caused by Ca
pubmed: 15194823
pmcid: 439001
Schumann T, Konig J, Henke C et al (2020) Solute carrier transporters as potential targets for the treatment of metabolic disease. Pharmacol Rev 72:343–379
pubmed: 31882442
Sheldon PW, Fowler JF (1976) The effect of low-dose pre-operative X-irradiation of implanted mouse mammary carcinomas on local recurrence and metastasis. Br J Cancer 34:401–407
pubmed: 974005
pmcid: 2025262
Si H, Heyken WT, Wolfle SE et al (2006) Impaired endothelium-derived hyperpolarizing factor-mediated dilations and increased blood pressure in mice deficient of the intermediate-conductance Ca
pubmed: 16873714
Skonieczna M, Cieslar-Pobuda A, Saenko Y et al (2017) The impact of DIDS-induced inhibition of voltage-dependent anion channels (VDAC) on cellular response of Lymphoblastoid cells to ionizing radiation. Med Chem 13:477–483
pubmed: 28427245
Soloviev A, Tishkin S, Ivanova I et al (2009) Functional and molecular consequences of ionizing irradiation on large conductance Ca
pubmed: 19070626
Soltysinska E, Bentzen BH, Barthmes M et al (2014) KCNMA1 encoded cardiac BK channels afford protection against ischemia-reperfusion injury. PLoS One 9:e103402
pubmed: 25072914
pmcid: 4114839
Song MS, Ryu PD, Lee SY (2017) K
pubmed: 28522852
pmcid: 5437029
Sontheimer H (2008) An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med (Maywood) 233:779–791
Sorensen MV, Matos JE, Sausbier M et al (2008) Aldosterone increases K
pubmed: 18617563
pmcid: 2652187
Stegen B, Butz L, Klumpp L et al (2015) Ca
pubmed: 26041939
Stegen B, Klumpp L, Misovic M et al (2016) K
pubmed: 27165704
Steinle M, Palme D, Misovic M et al (2011) Ionizing radiation induces migration of glioblastoma cells by activating BK K
pubmed: 21704404
Steudel FA, Mohr CJ, Stegen B et al (2017) SK4 channels modulate Ca
pubmed: 28557306
pmcid: 5579333
Strong MS, Vaughan CW, Kayne HL et al (1978) A randomized trial of preoperative radiotherapy in cancer of the oropharynx and hypopharynx. Am J Surg 136:494–500
pubmed: 360853
Sui X, Geng JH, Li YH et al (2018) Calcium channel alpha2delta1 subunit (CACNA2D1) enhances radioresistance in cancer stem-like cells in non-small cell lung cancer cell lines. Cancer Manag Res 10:5009–5018
pubmed: 30464601
pmcid: 6208517
Tartier L, Gilchrist S, Burdak-Rothkamm S et al (2007) Cytoplasmic irradiation induces mitochondrial-dependent 53BP1 protein relocalization in irradiated and bystander cells. Cancer Res 67:5872–5879
pubmed: 17575156
pmcid: 3014567
Terry S, Faouzi Zaarour R, Hassan Venkatesh G et al (2018) Role of hypoxic stress in regulating tumor immunogenicity, resistance and plasticity. Int J Mol Sci 19:3044
Teshima K, Yamamoto A, Yamaoka K et al (2000) Involvement of calcium ion in elevation of mRNA for gamma-glutamylcysteine synthetase (gamma-GCS) induced by low-dose gamma-rays. Int J Radiat Biol 76:1631–1639
pubmed: 11133045
Thoday JM, Read J (1947) Effect of oxygen on the frequency of chromosome aberrations produced by X-rays. Nature 160:608
pubmed: 20271559
Todd DG, Mikkelsen RB (1994) Ionizing radiation induces a transient increase in cytosolic free [Ca
pubmed: 7923144
Toulany M (2019) Targeting DNA double-strand break repair pathways to improve radiotherapy response. Genes (Basel) 10:25
Trautmann F, Cojoc M, Kurth I et al (2014) CXCR4 as biomarker for radioresistant cancer stem cells. Int J Radiat Biol 90:687–699
pubmed: 24650104
Tyszka-Czochara M, Konieczny P, Majka M (2018) Recent advances in the role of AMP-activated protein kinase in metabolic reprogramming of metastatic cancer cells: targeting cellular bioenergetics and biosynthetic pathways for anti-tumor treatment. J Physiol Pharmacol:69
Uysal-Onganer P, Djamgoz MB (2007) Epidermal growth factor potentiates in vitro metastatic behaviour of human prostate cancer PC-3M cells: involvement of voltage-gated sodium channel. Mol Cancer 6:76
pubmed: 18036246
pmcid: 2211503
Valerie K, Povirk LF (2003) Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22:5792–5812
pubmed: 12947387
Vercesi AE, Kowaltowski AJ, Grijalba MT et al (1997) The role of reactive oxygen species in mitochondrial permeability transition. Biosci Rep 17:43–52
pubmed: 9171920
Vilalta M, Rafat M, Graves EE (2016) Effects of radiation on metastasis and tumor cell migration. Cell Mol Life Sci 73:2999–3007
pubmed: 27022944
pmcid: 4956569
Voehringer DW, Hirschberg DL, Xiao J et al (2000) Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci U S A 97:2680–2685
pubmed: 10716996
pmcid: 15989
Voos P, Fuck S, Weipert F et al (2018) Ionizing radiation induces morphological changes and immunological modulation of Jurkat cells. Front Immunol 9:922
pubmed: 29760710
pmcid: 5936756
Vullhorst D, Klocke R, Bartsch JW et al (1998) Expression of the potassium channel K
pubmed: 9468318
Warburg O (1956) On respiratory impairment in cancer cells. Science 124:269–270
pubmed: 13351639
Weaver AK, Bomben VC, Sontheimer H (2006) Expression and function of calcium-activated potassium channels in human glioma cells. Glia 54:223–233
pubmed: 16817201
pmcid: 2562223
Wojewodzka M, Walicka M, Sochanowicz B et al (1994) Calcium antagonist, TMB-8, prevents the induction of adaptive response by hydrogen peroxide or X-rays in human lymphocytes. Int J Radiat Biol 66:99–109
pubmed: 8027616
Wondergem R, Bartley JW (2009) Menthol increases human glioblastoma intracellular Ca2+, BK channel activity and cell migration. J Biomed Sci 16:90
pubmed: 19778436
pmcid: 2758849
Wondergem R, Ecay TW, Mahieu F et al (2008) HGF/SF and menthol increase human glioblastoma cell calcium and migration. Biochem Biophys Res Commun 372:210–215
pubmed: 18485891
Wright EM, Ghezzi C, Loo DDF (2017) Novel and unexpected functions of SGLTs. Physiology (Bethesda) 32:435–443
Xie H, Simon MC (2017) Oxygen availability and metabolic reprogramming in cancer. J Biol Chem 292:16825–16832
pubmed: 28842498
pmcid: 5641881
Xu Y, Miriyala S, Fang F et al (2015) Manganese superoxide dismutase deficiency triggers mitochondrial uncoupling and the Warburg effect. Oncogene 34:4229–4237
pubmed: 25362851
Yamamoto T (1936) Experimental study on effect of x-ray on metastasis of malignant tumor, especially in bones. Jpn J Obst Gynec 19:559–569
Yamazaki H, Yoshida K, Yoshioka Y et al (2008) Impact of mitochondrial DNA on hypoxic radiation sensitivity in human fibroblast cells and osteosarcoma cell lines. Oncol Rep 19:1545–1549
pubmed: 18497963
Yang M, Brackenbury WJ (2013) Membrane potential and cancer progression. Front Physiol 4:185
pubmed: 23882223
pmcid: 3713347
Yang M, Kozminski DJ, Wold LA et al (2012) Therapeutic potential for phenytoin: targeting Na
pubmed: 22678159
pmcid: 3401508
Yang B, Cao L, Liu J et al (2015) Low expression of chloride channel accessory 1 predicts a poor prognosis in colorectal cancer. Cancer 121:1570–1580
pubmed: 25603912
Yildirim S, Altun S, Gumushan H et al (2012) Voltage-gated sodium channel activity promotes prostate cancer metastasis in vivo. Cancer Lett 323:58–61
pubmed: 22484465
Yom SS (2015) Accelerated repopulation as a cause of radiation treatment failure in non-small cell lung cancer: review of current data and future clinical strategies. Semin Radiat Oncol 25:93–99
pubmed: 25771413
Yoshida S (1997) Effects of X-irradiation on the calcium channel of the mouse oocyte. Life Sci 60:1377–1383
pubmed: 9096258
Zhang B, Davidson MM, Hei TK (2014) Mitochondria regulate DNA damage and genomic instability induced by high LET radiation. Life Sci Space Res 1:80–88
Zhang J, Mao W, Dai Y et al (2019) Voltage-gated sodium channel Na
pubmed: 31139826
Zhang C, Ye L, Zhang Q et al (2020) The role of TRPV1 channels in atherosclerosis. Channels (Austin) 14:141–150
Zhou H, Hong M, Chai Y et al (2009) Consequences of cytoplasmic irradiation: studies from microbeam. J Radiat Res 50(Suppl A):A59–A65
pubmed: 19346686
Zhou XB, Feng YX, Sun Q et al (2015) Nucleoside diphosphate kinase B-activated intermediate conductance potassium channels are critical for neointima formation in mouse carotid arteries. Arterioscler Thromb Vasc Biol 35:1852–1861
pubmed: 26088577