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Review

Mitochondrial reactive oxygen species-mediated genomic instability in low-dose irradiated human cells through nuclear retention of cyclin D1

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Pages 1410-1414 | Received 18 Feb 2016, Accepted 20 Mar 2016, Published online: 06 May 2016

References

  • Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000; 408:433-9; PMID:11100718; http://dx.doi.org/10.1038/35044005.
  • Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature 2012; 481:287-94; PMID:22258607; http://dx.doi.org/10.1038/nature10760.
  • Persson HL, Kurz T, Eaton JW, Brunk UT. Radiation-induced cell death: importance of lysosomal destabilization. Biochem J 2005; 389:877-84; PMID:15813701; http://dx.doi.org/10.1042/BJ20050271.
  • Moretti L, Cha YI, Niermann KJ, Lu B. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress? Cell Cycle 2007; 6:793-8; PMID:17377498; http://dx.doi.org/10.4161/cc.6.7.4036.
  • Gabrys D, Greco O, Patel G, Prise KM, Tozer GM, Kanthou C. Radiation effects on the cytoskeleton of endothelial cells and endothelial monolayer permeability. Int J Radiat Oncol Biol Phys 2007; 69:1553-62; PMID:17920784; http://dx.doi.org/10.1016/j.ijrobp.2007.08.039.
  • Kam WW, Banati RB. Effects of ionizing radiation on mitochondria. Free Radical Biol Med 2013; 65:607-19; http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.024.
  • Shao C, Folkard M, Michael BD, Prise KM. Targeted cytoplasmic irradiation induces bystander responses. Proc Natl Acad Sci U S A 2004; 101:13495-500; PMID:15345742; http://dx.doi.org/10.1073/pnas.0404930101.
  • Belyakov OV, Malcolmson AM, Folkard M, Prise KM, Michael BD. Direct evidence for a bystander effect of ionizing radiation in primary human fibroblasts. Br J Cancer 2001; 84:674-9; PMID:11237389; http://dx.doi.org/10.1054/bjoc.2000.1665.
  • Kowaltowski AJ, de Souza-Pinto NC, Castilho RF, Vercesi AE. Mitochondria and reactive oxygen species. Free Radical Biol Med 2009; 47:333-43; http://dx.doi.org/10.1016/j.freeradbiomed.2009.05.004.
  • Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012; 48:158-67; PMID:23102266; http://dx.doi.org/10.1016/j.molcel.2012.09.025.
  • Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 2011; 29:486-95; PMID:21425411; http://dx.doi.org/10.1002/stem.590.
  • Chiu J, Dawes IW. Redox control of cell proliferation. Trends Cell Biol 2012; 22:592-601; PMID:22951073; http://dx.doi.org/10.1016/j.tcb.2012.08.002.
  • Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 2011; 194:7-15; PMID:21746850; http://dx.doi.org/10.1083/jcb.201102095.
  • Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24:981-90; PMID:22286106; http://dx.doi.org/10.1016/j.cellsig.2012.01.008.
  • Kehrer JP, Klotz LO. Free radicals and related reactive species as mediators of tissue injury and disease: implications for Health. Critical Rev Toxicol 2015; 45:765-98; http://dx.doi.org/10.3109/10408444.2015.1074159.
  • Little JB, Nagasawa H, Pfenning T, Vetrovs H. Radiation-induced genomic instability: delayed mutagenic and cytogenetic effects of X rays and α particles. Radiat Res 1997; 148:299-307; PMID:9339945; http://dx.doi.org/10.2307/3579514.
  • Streffer C. Strong association between cancer and genomic instability. Radiat Environ Biophys 2010; 49:125-31; PMID:20033424; http://dx.doi.org/10.1007/s00411-009-0258-4.
  • Kadhim M, Salomaa S, Wright E, Hildebrandt G, Belyakov OV, Prise KM, Little MP. Non-targeted effects of ionising radiation–implications for low dose risk. Mutation Res 2013; 752:84-98; PMID:23262375; http://dx.doi.org/10.1016/j.mrrev.2012.12.001.
  • Murnane JP. Role of induced genetic instability in the mutagenic effects of chemicals and radiation. Mutation Res 1996; 367:11-23; PMID:8596542; http://dx.doi.org/10.1016/S0165-1218(96)90017-8.
  • Timp W, Feinberg AP. Cancer as a dysregulated epigenome allowing cellular growth advantage at the expense of the host. Nat Rev Cancer 2013; 13:497-510; PMID:23760024; http://dx.doi.org/10.1038/nrc3486.
  • Kim GJ, Chandrasekaran K, Morgan WF. Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: a review. Mutagenesis 2006; 21:361-7; PMID:17065161; http://dx.doi.org/10.1093/mutage/gel048.
  • Kim GJ, Fiskum GM, Morgan WF. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res 2006; 66:10377-83; PMID:17079457; http://dx.doi.org/10.1158/0008-5472.CAN-05-3036.
  • Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 1996; 17:1633-9; PMID:8761419; http://dx.doi.org/10.1093/carcin/17.8.1633.
  • Kohen R, Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicologic pathol 2002; 30:620-50; http://dx.doi.org/10.1080/01926230290166724.
  • Goitre L, Balzac F, Degani S, Degan P, Marchi S, Pinton P, Retta SF. KRIT1 regulates the homeostasis of intracellular reactive oxygen species. PloS One 2010; 5:e11786; PMID:20668652; http://dx.doi.org/10.1371/journal.pone.0011786.
  • Shimura T, Kobayashi J, Komatsu K, Kunugita N. Severe mitochondrial damage associated with low-dose radiation sensitivity in ATM- and NBS1-deficient cells. Cell Cycle 2016; http://dx.doi.org/10.1080/15384101.2016.1156276.
  • Yu J, Wang Q, Chen N, Sun Y, Wang X, Wu L, Chen S, Yuan H, Xu A, Wang J. Mitochondrial transcription factor A regulated ionizing radiation-induced mitochondrial biogenesis in human lung adenocarcinoma A549 cells. J Radiat Res 2013; 54:998-1004; PMID:23645454; http://dx.doi.org/10.1093/jrr/rrt046.
  • Kulkarni R, Marples B, Balasubramaniam M, Thomas RA, Tucker JD. Mitochondrial gene expression changes in normal and mitochondrial mutant cells after exposure to ionizing radiation. Radiat Res 2010; 173:635-44; PMID:20426663; http://dx.doi.org/10.1667/RR1737.1.
  • Chien L, Chen WK, Liu ST, Chang CR, Kao MC, Chen KW, Chiu SC, Hsu ML, Hsiang IC, Chen YJ, et al. Low-dose ionizing radiation induces mitochondrial fusion and increases expression of mitochondrial complexes I and III in hippocampal neurons. Oncotarget 2015; 6:30628-39; PMID:26415228.
  • Chen H, McCaffery JM, Chan DC. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 2007; 130:548-62; PMID:17693261; http://dx.doi.org/10.1016/j.cell.2007.06.026.
  • Chen H, Chan DC. Mitochondrial dynamics–fusion, fission, movement, and mitophagy–in neurodegenerative diseases. Hum Mol Genetics 2009; 18:R169-76; http://dx.doi.org/10.1093/hmg/ddp326.
  • Ono T, Isobe K, Nakada K, Hayashi JI. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nat Genetics 2001; 28:272-5; PMID:11431699; http://dx.doi.org/10.1038/90116.
  • Tolkovsky AM. Mitophagy. Biochim Et Biophysica Acta 2009; 1793:1508-15; http://dx.doi.org/10.1016/j.bbamcr.2009.03.002.
  • Zhang J. Autophagy and Mitophagy in Cellular Damage Control. Redox Biol 2013; 1:19-23; PMID:23946931; http://dx.doi.org/10.1016/j.redox.2012.11.008.
  • Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A 2003; 100:4078-83; PMID:12642658; http://dx.doi.org/10.1073/pnas.0737556100.
  • Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183:795-803; PMID:19029340; http://dx.doi.org/10.1083/jcb.200809125.
  • Epperly MW, Gretton JE, Sikora CA, Jefferson M, Bernarding M, Nie S, Greenberger JS. Mitochondrial localization of superoxide dismutase is required for decreasing radiation-induced cellular damage. Radiat Res 2003; 160:568-78; PMID:14565825; http://dx.doi.org/10.1667/RR3081.
  • Hosoki A, Yonekura S, Zhao QL, Wei ZL, Takasaki I, Tabuchi Y, Wang LL, Hasuike S, Nomura T, Tachibana A, et al. Mitochondria-targeted superoxide dismutase (SOD2) regulates radiation resistance and radiation stress response in HeLa cells. J Radiat Res 2012; 53:58-71; PMID:22302046; http://dx.doi.org/10.1269/jrr.11034.
  • Murley JS, Kataoka Y, Cao D, Li JJ, Oberley LW, Grdina DJ. Delayed radioprotection by NFkappaB-mediated induction of Sod2 (MnSOD) in SA-NH tumor cells after exposure to clinically used thiol-containing drugs. Radiat Res 2004; 162:536-46; PMID: 15624308; http://dx.doi.org/10.1667/RR3256.
  • Eldridge A, Fan M, Woloschak G, Grdina DJ, Chromy BA, Li JJ. Manganese superoxide dismutase interacts with a large scale of cellular and mitochondrial proteins in low-dose radiation-induced adaptive radioprotection. Free Radical Biol Med 2012; 53:1838-47; http://dx.doi.org/10.1016/j.freeradbiomed.2012.08.589.
  • Park HS, Seong KM, Kim JY, Kim CS, Yang KH, Jin YW, Nam SY. Chronic low-dose radiation inhibits the cells death by cytotoxic high-dose radiation increasing the level of AKT and acinus proteins via NF-kappaB activation. Int J Radiat Biol 2013; 89:371-7; PMID:23205493; http://dx.doi.org/10.3109/09553002.2013.754560.
  • Zhou H, Ivanov VN, Lien YC, Davidson M, Hei TK. Mitochondrial function and nuclear factor-kappaB-mediated signaling in radiation-induced bystander effects. Cancer Res 2008; 68:2233-40; PMID:18381429; http://dx.doi.org/10.1158/0008-5472.CAN-07-5278.
  • Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001; 15:2922-33; PMID:11711427.
  • Shimura T, Sasatani M, Kamiya K, Kawai H, Inaba Y, Kunugita N. Mitochondrial reactive oxygen species perturb AKT/cyclin D1 cell cycle signaling via oxidative inactivation of PP2A in low-dose irradiated human fibroblasts. Oncotarget 2016; 7(3):3559-70.
  • McKinnon PJ. ATM and ataxia telangiectasia. EMBO Rep 2004; 5:772-6; PMID:15289825; http://dx.doi.org/10.1038/sj.embor.7400210.
  • Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science 2010; 330:517-21; PMID:20966255; http://dx.doi.org/10.1126/science.1192912.
  • Guo Z, Deshpande R, Paull TT. ATM activation in the presence of oxidative stress. Cell Cycle 2010; 9:4805-11; PMID:21150274; http://dx.doi.org/10.4161/cc.9.24.14323.
  • Reichenbach J, Schubert R, Schwan C, Muller K, Bohles HJ, Zielen S. Anti-oxidative capacity in patients with ataxia telangiectasia. Clin Exp Immunol 1999; 117:535-9; PMID:10469059; http://dx.doi.org/10.1046/j.1365-2249.1999.01000.x.
  • Fu X, Wan S, Lyu YL, Liu LF, Qi H. Etoposide induces ATM-dependent mitochondrial biogenesis through AMPK activation. PloS One 2008; 3:e2009.
  • Valentin-Vega YA, Maclean KH, Tait-Mulder J, Milasta S, Steeves M, Dorsey FC, Cleveland JL, Green DR, Kastan MB. Mitochondrial dysfunction in ataxia-telangiectasia. Blood 2012; 119:1490-500; PMID:22144182; http://dx.doi.org/10.1182/blood-2011-08-373639.
  • Richter C, Park JW, Ames BN. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A 1988; 85:6465-7; PMID:3413108; http://dx.doi.org/10.1073/pnas.85.17.6465.
  • Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 1997; 94:514-9; PMID:9012815; http://dx.doi.org/10.1073/pnas.94.2.514.
  • Kazak L, Reyes A, Holt IJ. Minimizing the damage: repair pathways keep mitochondrial DNA intact. Nat Rev Mol Cell Biol 2012; 13:659-71; PMID:22992591; http://dx.doi.org/10.1038/nrm3439.
  • Longley MJ, Nguyen D, Kunkel TA, Copeland WC. The fidelity of human DNA polymerase gamma with and without exonucleolytic proofreading and the p55 accessory subunit. J Biol Chem 2001; 276:38555-62; PMID:11504725; http://dx.doi.org/10.1074/jbc.M105230200.
  • Copeland WC, Longley MJ. DNA polymerase gamma in mitochondrial DNA replication and repair. Scientific World J 2003; 3:34-44; http://dx.doi.org/10.1100/tsw.2003.09.
  • Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 2014; 94:909-50; PMID:24987008; http://dx.doi.org/10.1152/physrev.00026.2013.
  • Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Et Biophysica Acta 2006; 1757:509-17; http://dx.doi.org/10.1016/j.bbabio.2006.04.029.
  • Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000; 192:1001-14; PMID:11015441; http://dx.doi.org/10.1084/jem.192.7.1001.
  • Polyak K, Li Y, Zhu H, Lengauer C, Willson JK, Markowitz SD, Trush MA, Kinzler KW, Vogelstein B. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genetics 1998; 20:291-3; PMID:9806551; http://dx.doi.org/10.1038/3108.
  • Fliss MS, Usadel H, Caballero OL, Wu L, Buta MR, Eleff SM, Jen J, Sidransky D. Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Sci 2000; 287:2017-9; http://dx.doi.org/10.1126/science.287.5460.2017.
  • Liu VW, Shi HH, Cheung AN, Chiu PM, Leung TW, Nagley P, Wong LC, Ngan HY. High incidence of somatic mitochondrial DNA mutations in human ovarian carcinomas. Cancer Res 2001; 61:5998-6001; PMID:11507041.
  • Chatterjee A, Mambo E, Sidransky D. Mitochondrial DNA mutations in human cancer. Oncogene 2006; 25:4663-74; PMID:16892080; http://dx.doi.org/10.1038/sj.onc.1209604.
  • van Gisbergen MW, Voets AM, Starmans MH, de Coo IF, Yadak R, Hoffmann RF, Boutros PC, Smeets HJ, Dubois L, Lambin P. How do changes in the mtDNA and mitochondrial dysfunction influence cancer and cancer therapy? Challenges, opportunities and models. Mutation Res Rev Mutat Res 2015; 764:16-30; http://dx.doi.org/10.1016/j.mrrev.2015.01.001.
  • Chandra D, Singh KK. Genetic insights into OXPHOS defect and its role in cancer. Biochim Et Biophysica Acta 2011; 1807:620-5; http://dx.doi.org/10.1016/j.bbabio.2010.10.023.
  • Yu E, Mercer J, Bennett M. Mitochondria in vascular disease. Cardio Vascular Res 2012; 95:173-82; http://dx.doi.org/10.1093/cvr/cvs111.
  • Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005; 309:481-4; PMID:16020738; http://dx.doi.org/10.1126/science.1112125.
  • Staal FJ, Roederer M, Herzenberg LA, Herzenberg LA. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc Natl Acad Sci U S A 1990; 87:9943-7; PMID:2263644; http://dx.doi.org/10.1073/pnas.87.24.9943.
  • Benhar M, Engelberg D, Levitzki A. ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep 2002; 3:420-5; PMID:11991946; http://dx.doi.org/10.1093/embo-reports/kvf094.
  • Liu W, Akhand AA, Takeda K, Kawamoto Y, Itoigawa M, Kato M, Suzuki H, Ishikawa N, Nakashima I. Protein phosphatase 2A-linked and -unlinked caspase-dependent pathways for downregulation of Akt kinase triggered by 4-hydroxynonenal. Cell Death Differentiation 2003; 10:772-81; PMID:12815460; http://dx.doi.org/10.1038/sj.cdd.4401238.
  • Shimura T, Hamada N, Sasatani M, Kamiya K, Kunugita N. Nuclear accumulation of cyclin D1 following long-term fractionated exposures to low-dose ionizing radiation in normal human diploid cells. Cell Cycle 2014; 13:1248-55; PMID:24583467; http://dx.doi.org/10.4161/cc.28139.
  • Shimura T, Kakuda S, Ochiai Y, Nakagawa H, Kuwahara Y, Takai Y, Kobayashi J, Komatsu K, Fukumoto M. Acquired radioresistance of human tumor cells by DNA-PK/AKT/GSK3beta-mediated cyclin D1 overexpression. Oncogene 2010; 29:4826-37; PMID:20562919; http://dx.doi.org/10.1038/onc.2010.238.
  • Shimura T, Ochiai Y, Noma N, Oikawa T, Sano Y, Fukumoto M. Cyclin D1 overexpression perturbs DNA replication and induces replication-associated DNA double-strand breaks in acquired radioresistant cells. Cell Cycle 2013; 12:773-82; PMID:23388457; http://dx.doi.org/10.4161/cc.23719.
  • Aggarwal P, Lessie MD, Lin DI, Pontano L, Gladden AB, Nuskey B, Goradia A, Wasik MA, Klein-Szanto AJ, Rustgi AK, et al. Nuclear accumulation of cyclin D1 during S phase inhibits Cul4-dependent Cdt1 proteolysis and triggers p53-dependent DNA rereplication. Genes Dev 2007; 21:2908-22; PMID:18006686; http://dx.doi.org/10.1101/gad.1586007.
  • Leontieva OV, Lenzo F, Demidenko ZN, Blagosklonny MV. Hyper-mitogenic drive coexists with mitotic incompetence in senescent cells. Cell Cycle 2012; 11:4642-9; PMID:23187803; http://dx.doi.org/10.4161/cc.22937.
  • Dulic V, Drullinger LF, Lees E, Reed SI, Stein GH. Altered regulation of G1 cyclins in senescent human diploid fibroblasts: accumulation of inactive cyclin E-Cdk2 and cyclin D1-Cdk2 complexes. Proc Natl Acad Sci U S A 1993; 90:11034-8; PMID:8248208; http://dx.doi.org/10.1073/pnas.90.23.11034.

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