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ATM-mediated mitochondrial damage response triggered by nuclear DNA damage in normal human lung fibroblasts

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Pages 2345-2354 | Received 07 Jul 2017, Accepted 29 Sep 2017, Published online: 29 Nov 2017

References

  • Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40:179–204. doi:10.1016/j.molcel.2010.09.019. PMID:20965415.
  • Wang X. The expanding role of mitochondria in apoptosis. Genes & development. 2001;15:2922–2933.
  • Somosy Z. Radiation response of cell organelles. Micron. 2000;31:165–181. doi:10.1016/S0968-4328(99)00083-9. PMID:10588063.
  • 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 biology & medicine. 2012;53:1838–1847. doi:10.1016/j.freeradbiomed.2012.08.589.
  • Kim GJ, Fiskum GM, Morgan WF. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res. 2006;66:10377–10383. doi:10.1158/0008-5472.CAN-05-3036. PMID:17079457.
  • Szumiel I. Ionizing radiation-induced oxidative stress, epigenetic changes and genomic instability: the pivotal role of mitochondria. International journal of radiation biology. 2015;91:1–12. doi:10.3109/09553002.2014.934929. PMID:24937368.
  • Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005;120:483–495. doi:10.1016/j.cell.2005.02.001. PMID:15734681.
  • Ernster L, Schatz G. Mitochondria: a historical review. J Cell Biol. 1981;91:227s–255s. doi:10.1083/jcb.91.3.227s. PMID:7033239.
  • Kam WW, Banati RB. Effects of ionizing radiation on mitochondria. Free radical biology & medicine. 2013;65:607–619. doi:10.1016/j.freeradbiomed.2013.07.024..
  • Meister A. Glutathione, ascorbate, and cellular protection. Cancer Res. 1994;54:1969s–1975s. PMID:8137322.
  • Richter C, Park JW, Ames BN. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc Natl Acad Sci U S A. 1988;85:6465–6467. doi:10.1073/pnas.85.17.6465. PMID:3413108.
  • 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;94:514–519. doi:10.1073/pnas.94.2.514. PMID:9012815.
  • Chen H, McCaffery JM, Chan DC. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell. 2007;130:548–562. doi:10.1016/j.cell.2007.06.026. PMID:17693261.
  • Ono T, Isobe K, Nakada K, Hayashi JI. Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria. Nature genetics. 2001;28:272–275. doi:10.1038/90116. PMID:11431699.
  • Tolkovsky AM. Mitophagy. Biochimica et biophysica acta. 2009;1793:1508–1515.
  • Kubli DA, Gustafsson AB. Mitochondria and mitophagy: the yin and yang of cell death control. Circulation research. 2012;111:1208–1221. doi:10.1161/CIRCRESAHA.112.265819. PMID:23065344.
  • Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J, May J, Tocilescu MA, Liu W, Ko HS, Magrane J, Moore DJ, Dawson VL, Grailhe R, Dawson TM, Li C, Tieu K, Przedborski S. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A. 2010;107:378–383. doi:10.1073/pnas.0911187107. PMID:19966284.
  • 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;100:4078–4083. doi:10.1073/pnas.0737556100. PMID:12642658.
  • Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. The Journal of cell biology. 2008;183:795–803. doi:10.1083/jcb.200809125. PMID:19029340.
  • 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 lowdose irradiated human fibroblasts. Oncotarget. 2016;7:3559–3570. doi:10.18632/oncotarget.6518. PMID:26657292.
  • Shimura T, Sasatani M, Kawai H, Kamiya K, Kobayashi J, Komatsu K, Kunugita N. A comparison of radiation-induced mitochondrial damage between neural progenitor stem cells and differentiated cells. Cell cycle. 2017;16:565–573.
  • Shimura T, Kunugita N. Mitochondrial reactive oxygen species-mediated genomic instability in low-dose irradiated human cells through nuclear retention of cyclin D1. Cell cycle. 2016;15:1410–1414. doi:10.1080/15384101.2016.1170271. PMID:27078622.
  • Perelman A, Wachtel C, Cohen M, Haupt S, Shapiro H, Tzur A. JC-1: alternative excitation wavelengths facilitate mitochondrial membrane potential cytometry. Cell death & disease. 2012;3:e430. doi:10.1038/cddis.2012.171.
  • 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;13:1248–1255. doi:10.4161/cc.28139. PMID:24583467.
  • Woodward GE, Hudson MT. The effect of 2-desoxy-D-glucose on glycolysis and respiration of tumor and normal tissues. Cancer research 1954;14:599–605. PMID:13199805.
  • Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature. 2000;408:433–439. doi:10.1038/35044005. PMID:11100718.
  • 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. Journal of radiation research. 2013;54:998–1004. doi:10.1093/jrr/rrt046. PMID:23645454.
  • 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. Radiation research. 2010;173:635–644. doi:10.1667/RR1737.1. PMID:20426663.
  • Gong B, Chen Q, Almasan A. Ionizing radiation stimulates mitochondrial gene expression and activity. Radiation research 1998;150:505–512. doi:10.2307/3579866. PMID:9806591.
  • Yamamori T, Yasui H, Yamazumi M, Wada Y, Nakamura Y, Nakamura H, Inanami O. 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 radical biology & medicine. 2012;53:260–270. doi:10.1016/j.freeradbiomed.2012.04.033.
  • Fu X, Wan S, Lyu YL, Liu LF, Qi H. Etoposide induces ATM-dependent mitochondrial biogenesis through AMPK activation. PloS one. 2008;3:e2009. doi:10.1371/journal.pone.0002009. PMID:18431490.
  • 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;15:1099–1107. doi:10.1080/15384101.2016.1156276. PMID:26940879.
  • 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;119:1490–1500. doi:10.1182/blood-2011-08-373639. PMID:22144182.
  • Kudin AP, Debska-Vielhaber G, Kunz WS. Characterization of superoxide production sites in isolated rat brain and skeletal muscle mitochondria. Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie. 2005;59:163–168. doi:10.1016/j.biopha.2005.03.012..
  • Muller FL, Liu Y, Van Remmen H. Complex III releases superoxide to both sides of the inner mitochondrial membrane. The Journal of biological chemistry. 2004;279:49064–49073. doi:10.1074/jbc.M407715200. PMID:15317809.
  • Kazak L, Reyes A, Holt IJ. Minimizing the damage: repair pathways keep mitochondrial DNA intact. Nature reviews Molecular cell biology. 2012;13:659–671. doi:10.1038/nrm3439. PMID:22992591.
  • Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiological reviews. 2014;94:909–950. doi:10.1152/physrev.00026.2013. PMID:24987008.
  • Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochimica et biophysica acta. 2006;1757:509–517. doi:10.1016/j.bbabio.2006.04.029. PMID:16829228.
  • 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. The Journal of experimental medicine. 2000;192:1001–1014. doi:10.1084/jem.192.7.1001. PMID:11015441.
  • Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, Pestell RG, Martinez-Outschoorn UE, Sotgia F, Lisanti MP. The reverse Warburg effect: aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell cycle. 2009;8:3984–4001. doi:10.4161/cc.8.23.10238. PMID:19923890.
  • Yu E, Mercer J, Bennett M. Mitochondria in vascular disease. Cardiovascular research. 2012;95:173–182. doi:10.1093/cvr/cvs111. PMID:22392270.
  • Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science. 2005;309:481–484. doi:10.1126/science.1112125. PMID:16020738.
  • Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006;443:787–795. doi:10.1038/nature05292. PMID:17051205.
  • Kobayashi J, Tauchi H, Sakamoto S, Nakamura A, Morishima K, Matsuura S, Kobayashi T, Tamai K, Tanimoto K, Komatsu K. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr Biol. 2002;12:1846–1851. doi:10.1016/S0960-9822(02)01259-9. PMID:12419185.
  • Komatsu K, Matsuura S, Tauchi H, Endo S, Kodama S, Smeets D, Weemaes C, Oshimura M. The gene for Nijmegen breakage syndrome (V2) is not located on chromosome 11. Am J Hum Genet. 1996;58:885–888. PMID:8644753.
  • Shimura T, Toyoshima M, Adiga SK, Kunoh T, Nagai H, Shimizu N, Inoue M, Niwa O. Suppression of replication fork progression in low-dose-specific p53-dependent S-phase DNA damage checkpoint. Oncogene. 2006;25:5921–5932. doi:10.1038/sj.onc.1209624. PMID:16682953.
  • Shimura T, Toyoshima M, Adiga SK, Kunoh T, Nagai H, Shimizu N, Inoue M, Niwa O. Suppression of replication fork progression in low-dose-specic p53-dependent S-phase DNA damage checkpoint. Oncogene. 2006;25:5921–5932. doi:10.1038/sj.onc.1209624. PMID:16682953.

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