From radioresistance to radiosensitivity: In vitro evolution of L5178Y lymphoma

References

• Alexander P. 1961. Mouse lymphoma cells with different radiosensitivities. Nature 192:572–573.
   PubMed Web of Science ®Google Scholar
• Atkuri KR, Herzenberg LA, Niemi AK, Cowan T, Herzenberg LA. 2007. Importance of culturing primary lymphocytes at physiological oxygen levels. Proc Natl Acad Sci USA 104:4547–4552.
   PubMed Web of Science ®Google Scholar
• Ayouaz A, Raynaud C, Heride C, Revaud D, Sabatier L. 2008. Telomeres: Hallmarks of radiosensitivity. Biochimie 90:60–72.
   PubMed Web of Science ®Google Scholar
• Aypar U, Morgan WF, Baulch JE. 2011. Radiation-induced genomic instability: Are epigenetic mechanisms the missing link? Int J Radiat Biol 87:179–191.
   PubMed Web of Science ®Google Scholar
• Azzam EI, Jay-Gerin JP, Pain D. 2012. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett 327:48–60.
   PubMed Web of Science ®Google Scholar
• Bailey SM, Cornforth MN, Ullrich RL, Goodwin EH. 2004. Dysfunctional mammalian telomeres join with DNA double-strand breaks. DNA Repair 3:349–357.
   PubMed Web of Science ®Google Scholar
• Ballinger SW. 2013. Beyond retrograde and anterograde signalling: Mitochondrial-nuclear interactions as a means for evolutionary adaptation and contemporary disease susceptibility. Biochem Soc Trans 41:111–117.
   PubMedGoogle Scholar
• Beer JZ, Budzicka E, Niepokojczycka E, Rosiek O, Szumiel I, Walicka M. 1983. Loss of tumorigenicity with simultaneous changes in radiosensitivity and photosensitivity during in vitro growth of L5178Y murine lymphoma cells. Cancer Res 43:4736–4742.
   PubMed Web of Science ®Google Scholar
• Bellizzi D, D’Aquila P, Giordano M, Montesanto A, Passarino G. 2012. Global DNA methylation levels are modulated by mitochondrial DNA variants. Epigenomics 4:17–27.
   PubMed Web of Science ®Google Scholar
• Boużyk E, Grądzka I, Iwaneńko T, Kruszewski M, Sochanowicz B, Szumiel I. 2000. The response of L5178Y lymphoma sublines to oxidative stress: Antioxidant defence, iron content and nuclear translocation of the p65 subunit of NF-kappaB. Acta Biochim Pol 47:881–888.
   PubMed Web of Science ®Google Scholar
• Cabuy E, Newton C, Joksic G, Woodbine L, Koller B, Jeggo PA, Slijepcevic P. 2005. Accelerated telomere shortening and telomere abnormalities in radiosensitive cell lines. Radiat Res 164:53–62.
   PubMed Web of Science ®Google Scholar
• Castella M, Puerto S, Creus A, Marcos R, Surralles J. 2007. Telomere length modulates human radiation sensitivity in vitro. Toxicol Lett 172:29–36.
   PubMed Web of Science ®Google Scholar
• Chinnery PF, Elliott HR, Hudson G, Samuels DC, Relton CL. 2012. Epigenetics, epidemiology and mitochondrial DNA diseases. Int J Epidemiol 41:177–187.
   PubMed Web of Science ®Google Scholar
• Chiodi I, Mondello C. 2012. Telomere-independent functions of telomerase in nuclei, cytoplasm, and mitochondria. Front Oncol 2:133.
   PubMedGoogle Scholar
• Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG. 1996. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17:1633–1639.
   PubMed Web of Science ®Google Scholar
• D’Andrea FP, Horsman MR, Kassem M, Overgaard J, Safwat A. 2012. Tumourigenicity and radiation resistance of mesenchymal stem cells. Acta Oncol 51:669–679.
   PubMed Web of Science ®Google Scholar
• Desquiret-Dumas V, Gueguen N, Barth M, Chevrollier A, Hancock S, Wallace DC, Amati-Bonneau P, Henrion D, Bonneau D, Reynier P, Procaccio V. 2012. Metabolically induced heteroplasmy shifting and l-arginine treatment reduce the energetic defect in a neuronal-like model of MELAS. Biochim Biophys Acta 1822:1019–1029.
   PubMedGoogle Scholar
• Drissi R, Wu J, Hu Y, Bockhold C, Dome JS. 2011. Telomere shortening alters the kinetics of the DNA damage response after ionizing radiation in human cells. Cancer Prev Res 4:1973–1981.
   PubMed Web of Science ®Google Scholar
• Dunbar DR, Moonie PA, Jacobs HT, Holt IJ. 1995. Different cellular backgrounds confer a marked advantage to either mutant or wild-type mitochondrial genomes. Proc Natl Acad Sci USA 92: 6562–6566.
   PubMed Web of Science ®Google Scholar
• Erickson GA, Koppenol WH. 1987. Effects of gamma-irradiation on isolated rat liver mitochondria. Int J Radiat Biol 51:147–155.
   Web of Science ®Google Scholar
• Espejel S, Franco S, Sgura A, Gae D, Bailey SM, Taccioli GE, Blasco MA. 2002. Functional interaction between DNA-PKcs and telomerase in telomere length maintenance. EMBO J 21:6275–6287.
   PubMed Web of Science ®Google Scholar
• Fan W, Lin CS, Potluri P, Procaccio V, Wallace DC. 2012. mtDNA lineage analysis of mouse L-cell lines reveals the accumulation of multiple mtDNA mutants and intermolecular recombination. Genes Dev 26:384–394.
   PubMedGoogle Scholar
• Goytisolo FA, Samper E, Martin-Caballero J, Finnon P, Herrera E, Flores JM, Bouffler SD, Blasco MA. 2000. Short telomeres result in organismal hypersensitivity to ionizing radiation in mammals. J Exp Med 192:1625–1636.
   PubMed Web of Science ®Google Scholar
• Gudz TI, Pandelova IG, Novgorodov SA. 1994. Stimulation of respiration in rat thymocytes induced by ionizing radiation. Radiat Res 138:114–120.
   PubMedGoogle Scholar
• Guha M, Avadhani NG. 2013. Mitochondrial retrograde signaling at the crossroads of tumor bioenergetics, genetics and epigenetics. Mitochondrion 2013:S1567–7249.
   Google Scholar
• Hayashi J, Tagashira Y, Watanabe T, Yoshida MC. 1984. Effect of mitochondrial DNA transmitted cytoplasmically from nontumorigenic to tumorigenic rat cells on the phenotypic expression of tumorigenicity. Cancer Res 44:3957–3960.
   PubMedGoogle Scholar
• He Y, Wu J, Dressman DC, Iacobuzio-Donahue C, Markowitz SD, Velculescu VE, Diaz LA, Jr., Kinzler KW, Vogelstein B, Papadopoulos N. 2010. Heteroplasmic mitochondrial DNA mutations in normal and tumour cells. Nature 464:610–614.
   PubMed Web of Science ®Google Scholar
• Houben JM, Moonen HJ, van Schooten FJ, Hageman GJ. 2008. Telomere length assessment: Biomarker of chronic oxidative stress? Free Radic Biol Med 44:235–246.
   PubMed Web of Science ®Google Scholar
• Huang L, Snyder AR, Morgan WF. 2003. Radiation-induced genomic instability and its implications for radiation carcinogenesis. Oncogene 22:5848–5854.
   PubMed Web of Science ®Google Scholar
• Ilnytskyy Y, Kovalchuk O. 2011. Non-targeted radiation effects-an epigenetic connection. Mutat Res 714:113–125.
   PubMed Web of Science ®Google Scholar
• Ishikawa K, Takenaga K, Akimoto M, Koshikawa N, Yamaguchi A, Imanishi H, Nakada K, Honma Y, Hayashi J. 2008. ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320:661–664.
   PubMed Web of Science ®Google Scholar
• Israel BA, Schaeffer WI. 1987. Cytoplasmic suppression of malignancy. In Vitro Cell Dev Biol 123:627–632.
   Google Scholar
• Israel BA, Schaeffer WI. 1988. Cytoplasmic mediation of malignancy. In Vitro Cell Dev Biol 24:487–490.
   PubMedGoogle Scholar
• Jazwinski SM. 2013. The retrograde response: when mitochondrial quality control is not enough. Biochim Biophys Acta 2013;1833: 400–409.
   PubMed Web of Science ®Google Scholar
• Kadhim M, Salomaa S, Wright E, Hildebrandt G, Belyakov OV, Prise KM, Little MP. 2013. Non-targeted effects of ionising radiation-Implications for low dose risk. Mutat Res 752:84–98.
   PubMed Web of Science ®Google Scholar
• Kaipparettu BA, Ma Y, Park JH, Lee TL, Zhang Y, Yotnda P, Creighton CJ, Chan WY, Wong LJ. 2013. Crosstalk from non-cancerous mitochondria can inhibit tumor properties of metastatic cells by suppressing oncogenic pathways. PLoS One 8:e61747.
   Web of Science ®Google Scholar
• Kim GJ, Fiskum GM, Morgan WF. 2006a. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res 66:10377–10383.
   PubMed Web of Science ®Google Scholar
• Kim GJ, Chandrasekaran K, Morgan WF. 2006b. Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: A review. Mutagenesis 21:361–367.
   PubMed Web of Science ®Google Scholar
• Kmiec B, Woloszynska M, Janska H. 2006. Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr Genet 50:149–159.
   PubMed Web of Science ®Google Scholar
• Kotiadis VN, Duchen MR, Osellame LD. 2014. Mitochondrial quality control and communications with the nucleus are important in maintaining mitochondrial function and cell health. Biochim Biophys Acta 1840:1254–1265.
   PubMed Web of Science ®Google Scholar
• Kruszewski M, Wojewodzka M, Iwanenko T, Szumiel I, Okuyama A. 1998. Differential inhibitory effect of OK-1035 on DNA repair in L5178Y murine lymphoma sublines with functional or defective repair of double strand breaks. Mutat Res 409:31–36.
   PubMed Web of Science ®Google Scholar
• Kryston TB, Georgiev AB, Pissis P, Georgakilas AG. 2011. Role of oxidative stress and DNA damage in human carcinogenesis. Mutat Res 711:193–201.
   PubMed Web of Science ®Google Scholar
• Latre L, Genesca A, Martin M, Ribas M, Egozcue J, Blasco MA, Tusell L. 2004. Repair of DNA broken ends is similar in embryonic fibroblasts with and without telomerase. Radiat Res 162:136–142.
   PubMedGoogle Scholar
• Leach JK, Van TG, Lin PS, Schmidt-Ullrich R, Mikkelsen RB. 2001. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61:3894–3901.
   PubMed Web of Science ®Google Scholar
• Lee HC, Kim DW, Jung KY, Park IC, Park MJ, Kim MS, Woo SH, Rhee CH, Yoo H, Lee SH, Hong SI. 2004. Increased expression of antioxidant enzymes in radioresistant variant from U251 human glioblastoma cell line. Int J Mol Med 13:883–887.
   PubMed Web of Science ®Google Scholar
• Limoli CL, Hartmann A, Shephard L, Yang CR, Boothman DA, Bartholomew J, Morgan WF. 1998. Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Res 58:3712–3718.
   PubMed Web of Science ®Google Scholar
• Limoli CL, Giedzinski E, Morgan WF, Swarts SG, Jones GD, Hyun W. 2003. Persistent oxidative stress in chromosomally unstable cells. Cancer Res 63:3107–3111.
   PubMed Web of Science ®Google Scholar
• Lipinski P, Drapier JC, Oliveira L, Retmanska H, Sochanowicz B, Kruszewski M. 2000. Intracellular iron status as a hallmark of mammalian cell susceptibility to oxidative stress: A study of L5178Y mouse lymphoma cell lines differentially sensitive to H(2)O(2). Blood 95:2960–2966.
   PubMed Web of Science ®Google Scholar
• McIlrath J, Bouffler SD, Samper E, Cuthbert A, Wojcik A, Szumiel I, Bryant PE, Riches AC, Thompson A, Blasco MA, Newbold RF, Slijepcevic P. 2001. Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res 61:912–915.
   PubMed Web of Science ®Google Scholar
• Minocherhomji S, Tollefsbol TO, Singh KK. 2012. Mitochondrial regulation of epigenetics and its role in human diseases. Epigenetics 7:326–334.
   PubMed Web of Science ®Google Scholar
• Morgan WF, Hartmann A, Limoli CL, Nagar S, Ponnaiya B. 2002. Bystander effects in radiation-induced genomic instability. Mutat Res 504:91–100.
   PubMed Web of Science ®Google Scholar
• Park JS, Sharma LK, Li H, Xiang R, Holstein D, Wu J, Lechleiter J, Naylor SL, Deng JJ, Lu J, Bai Y. 2009. A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet 18:1578–1589.
   PubMedGoogle Scholar
• Payne BA, Wilson IJ, Yu-Wai-Man P, Coxhead J, Deehan D, Horvath R, Taylor RW, Samuels DC, Santibanez-Koref M, Chinnery PF. 2013. Universal heteroplasmy of human mitochondrial DNA. Hum Mol Genet 22:384–390.
   PubMed Web of Science ®Google Scholar
• Rubio MA, Kim SH, Campisi J. 2002. Reversible manipulation of telomerase expression and telomere length. Implications for the ionizing radiation response and replicative senescence of human cells. J Biol Chem 277:28609–28617.
   PubMedGoogle Scholar
• Rugo RE, Schiestl RH. 2004. Increases in oxidative stress in the progeny of X-irradiated cells. Radiat Res 162:416–425.
   PubMed Web of Science ®Google Scholar
• Rugo RE, Mutamba JT, Mohan KN, Yee T, Chaillet JR, Greenberger JS, Engelward BP. 2011. Methyltransferases mediate cell memory of a genotoxic insult. Oncogene 30:751–756.
   PubMed Web of Science ®Google Scholar
• Saretzki G. 2014. Extra-telomeric functions of human telomerase: Cancer, mitochondria and oxidative stress. Curr Pharm Des [Publication ahead of print] PMID:24975608
   PubMedGoogle Scholar
• Seyfried TN, Flores RE, Poff AM, D’Agostino DP. 2014. Cancer as a metabolic disease: Implications for novel therapeutics. Carcinogenesis 35:515–527.
   PubMed Web of Science ®Google Scholar
• Sharma PK, Bhardwaj R, Dwarakanath BS, Varshney R. 2010. Metabolic oxidative stress induced by a combination of 2-DG and 6-AN enhances radiation damage selectively in malignant cells via non-coordinated expression of antioxidant enzymes. Cancer Lett 295:154–166.
   PubMed Web of Science ®Google Scholar
• Shim G, Ricoul M, Hempel WM, Azzam EI, Sabatier L. 2014. Crosstalk between telomere maintenance and radiation effects: A key player in the process of radiation-induced carcinogenesis. Mutat Res Rev Mutat Res S1383-S5742. pii: S1383-5742(14)00002-7 [Epub ahead of print] PMID: 24486376.
   Google Scholar
• Singhapol C, Pal D, Czapiewski R, Porika M, Nelson G, Saretzki GC. 2013. Mitochondrial telomerase protects cancer cells from nuclear DNA damage and apoptosis. PLoS One 8:e52989.
   PubMed Web of Science ®Google Scholar
• Smiraglia DJ, Kulawiec M, Bistulfi GL, Gupta SG, Singh KK. 2008. A novel role for mitochondria in regulating epigenetic modification in the nucleus. Cancer Biol Ther 7:1182–1190.
   PubMed Web of Science ®Google Scholar
• Smirnova A, Gamba R, Khoriauli L, Vitelli V, Nergadze SG, Giulotto E. 2013. TERRA expression levels do not correlate with telomere length and radiation sensitivity in human cancer cell lines. Front Oncol 3:115.
   PubMedGoogle Scholar
• Sun J, Chen Y, Li M, Ge Z. 1998. Role of antioxidant enzymes on ionizing radiation resistance. Free Radic Biol Med 24:586–593.
   PubMed Web of Science ®Google Scholar
• Szumiel I. 1979. Response of two strains of L5178Y cells to cis- dichlorobis (cyclopentylamine)platinum(II). I. Cross-sensitivity to cis-PAD and UV light. Chem Biol Interact 24:51–72.
   PubMed Web of Science ®Google Scholar
• Szumiel I. 2005a. L5178Y sublines: A look back from 40 years. Part 1: General characteristics. Int J Radiat Biol 81:339–352.
   PubMed Web of Science ®Google Scholar
• Szumiel I. 2005b. L5178Y sublines: A look back from 40 years. Part 2: Response to ionizing radiation. Int J Radiat Biol 81:353–365.
   PubMed Web of Science ®Google Scholar
• Takasugi M, Yagi S, Hirabayashi K, Shiota K. 2010. DNA methylation status of nuclear-encoded mitochondrial genes underlies the tissue-dependent mitochondrial functions. BMC Genomics 11:481.
   PubMed Web of Science ®Google Scholar
• Tang T, Zhou FX, Lei H, Yu HJ, Xie CH, Zhou YF, Liu SQ. 2009. Increased expression of telomere-related proteins correlates with resistance to radiation in human laryngeal cancer cell lines. Oncol Rep 21: 1505–1509.
   PubMedGoogle Scholar
• Tang W, Chowdhury AR, Guha M, Huang L, Van Winkle T, Rustgi AK, Avadhani NG. 2012. Silencing of IkBβ mRNA causes disruption of mitochondrial retrograde signaling and suppression of tumor growth in vivo. Carcinogenesis 33:1762–1768.
   PubMedGoogle Scholar
• Timp W, Feinberg AP. 2013. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat Rev Cancer 13:497–510.
   PubMed Web of Science ®Google Scholar
• Wallace DC. 2010a. Bioenergetics and the epigenome: Interface between the environment and genes in common diseases. Dev Disabil Res Rev 16:114–119.
   PubMedGoogle Scholar
• Wallace DC. 2010b. The epigenome and the mitochondrion: bioenergetics and the environment [corrected]. Genes Dev 24: 1571–1573.
   PubMed Web of Science ®Google Scholar
• Wallace DC, Fan W. 2010. Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10:12–31.
   PubMed Web of Science ®Google Scholar
• Whelan SP, Zuckerbraun BS. 2013. Mitochondrial signaling: forwards, backwards, and in between. Oxid Med Cell Longev 2013:351613.
   Google Scholar
• Williams ES, Klingler R, Ponnaiya B, Hardt T, Schrock E, Lees-Miller SP, Meek K, Ullrich RL, Bailey SM. 2009. Telomere dysfunction and DNA-PKcs deficiency: Characterization and consequence. Cancer Res 69:2100–2107.
   PubMed Web of Science ®Google Scholar
• Wlodek D, Hittelman WN. 1987. The repair of double-strand DNA breaks correlates with radiosensitivity of L5178Y-S and L5178Y-R cells. Radiat Res 112:146–155.
   PubMed Web of Science ®Google Scholar
• Wojewodzka M, Kruszewski M, Sochanowicz B, Szumiel I. 2004. Differential DNA double strand break fixation dependence on poly(ADP-ribosylation) in L5178Y and CHO cells. Int J Radiat Biol 80:473–482.
   PubMed Web of Science ®Google Scholar
• Yamamori T, Yasui H, Yamazumi M, Wada Y, Nakamura Y, Nakamura H, Inanami O. 2012. Ionizing radiation induces mitochondrial reactive oxygen species production accompanied by upregulation of mitochondrial electron transport chain function and mitochondrial content under control of the cell cycle checkpoint. Free Radic Biol Med 53:260–270.
   PubMed Web of Science ®Google Scholar
• Yoshida T, Goto S, Kawakatsu M, Urata Y, Li TS. 2012. Mitochondrial dysfunction, a probable cause of persistent oxidative stress after exposure to ionizing radiation. Free Radic Res 46: 147–153.
   PubMed Web of Science ®Google Scholar
• Zhang C, Huang VH, Simon M, Sharma LK, Fan W, Haas R, Wallace DC, Bai Y, Huang T. 2012. Heteroplasmic mutations of the mitochondrial genome cause paradoxical effects on mitochondrial functions. FASEB J 26:4914–4924.
   PubMedGoogle Scholar
• Zhong YH, Liao ZK, Zhou FX, Xie CH, Xiao CY, Pan DF, Luo ZG, Liu SQ, Zhou YF. 2008. Telomere length inversely correlates with radiosensitivity in human carcinoma cells with the same tissue background. Biochem Biophys Res Commun 367:84–89.
   PubMedGoogle Scholar
• Zhou FX, Xiong J, Luo ZG, Dai J, Yu HJ, Liao ZK, Lei H, Xie CH, Zhou YF. 2010. cDNA expression analysis of a human radiosensitive- radioresistant cell line model identifies telomere function as a hallmark of radioresistance. Radiat Res 174:550–557.
   PubMedGoogle Scholar
• Zongaro S, Verri A, Giulotto E, Mondello C. 2008. Telomere length and radiosensitivity in human fibroblast clones immortalized by ectopic telomerase expression. Oncol Rep 19:1605–1609.
   PubMedGoogle Scholar