Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 9515809, 22 pages
https://doi.org/10.1155/2017/9515809
Research Article

Low-Dose Ionizing Radiation Affects Mesenchymal Stem Cells via Extracellular Oxidized Cell-Free DNA: A Possible Mediator of Bystander Effect and Adaptive Response

1Research Centre for Medical Genetics (RCMG), Moscow 115478, Russia
2V. A. Negovsky Research Institute of General Reanimatology, Moscow 107031, Russia
3Bach Institute of Biochemistry and Russian Academy of Sciences, 33 Leninskii Ave., Moscow 119071, Russia
4N. I. Pirogov Russian National Research Medical University, Moscow 117997, Russia

Correspondence should be addressed to V. A. Sergeeva; moc.liamg@enalpehtycart

Received 20 January 2017; Revised 17 April 2017; Accepted 18 May 2017; Published 22 August 2017

Academic Editor: Magdalena Skonieczna

Copyright © 2017 V. A. Sergeeva et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Hauptmann, S. Haghdoost, M. Gomolka et al., “Differential response and priming dose effect on the proteome of human fibroblast and stem cells induced by exposure to low doses of ionizing radiation,” Radiation Research, vol. 185, no. 3, pp. 299–312, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Sokolov and R. Neumann, “Global gene expression alterations as a crucial constituent of human cell response to low doses of ionizing radiation exposure,” International Journal of Molecular Sciences, vol. 17, no. 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Tubiana, L. E. Feinendegen, C. Yang, and J. M. Kaminski, “The linear no-threshold relationship is inconsistent with radiation biologic and experimental data,” Radiology, vol. 251, pp. 13–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. Z. Tao, Y. Zha, S. Akiba et al., “Cancer mortality in the high background radiation areas of Yangjiang, China during the period between 1979 and 1995,” Journal of Radiation Research, vol. 41, pp. 31–41, 2000. View at Publisher · View at Google Scholar
  5. G. Jaikrishan, K. R. Sudheer, V. J. Andrews et al., “Study of stillbirth and major congenital anomaly among newborns in the high-level natural radiation areas of Kerala, India,” Journal of Community Genetics, vol. 4, pp. 21–31, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. M. S. Pearce, J. A. Salotti, M. P. Little et al., “Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study,” Lancet, vol. 380, pp. 499–505, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. J. E. Cleaver, “Biology and genetics in the biological effects of ionizing radiation (BEIR VII) report,” Health Physics, vol. 89, pp. S32–S32, 2005. View at Google Scholar
  8. M. Tubiana, A. Aurengo, D. Averbeck, and R. Masse, “Recent reports on the effect of low doses of ionizing radiation and its dose-effect relationship,” Radiation and Environmental Biophysics, vol. 44, pp. 245–251, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Kundrát and W. Friedland, “Non-linear response of cells to signals leads to revised characteristics of bystander effects inferred from their modelling,” International Journal of Radiation Biology, vol. 88, no. 10, pp. 743–750, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. H. Matsumoto, A. Takahashi, and T. Ohnishi, “Radiation-induced adaptive responses and bystander effects,” Uchu Seibutsu Kagaku, vol. 18, no. 4, pp. 247–254, 2004. View at Google Scholar
  11. C. Mothersill and C. Seymour, “Radiation-induced bystander effects and adaptive responses—the yin and yang of low dose radiobiology?” Mutation Research, vol. 568, no. 1, pp. 121–128, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Ballarini, M. Biaggi, A. Ottolenghi, and O. Sapora, “Cellular communication and bystander effects: a critical review for modelling low-dose radiation action,” Mutation Research, vol. 501, no. 1-2, pp. 1–12, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. A. V. Ermakov, M. S. Konkova, S. V. Kostyuk, V. L. Izevskaya, A. Baranova, and N. N. Veiko, “Oxidized extracellular DNA as a stress signal in human cells,” Oxidative Medicine and Cellular Longevity, vol. 2013, Article ID 649747, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Mothersill and C. B. Seymour, “Cell-cell contact during gamma irradiation is not required to induce a bystander effect in normal human keratinocytes: evidence for release during irradiation of a signal controlling survival into the medium,” Radiation Research, vol. 149, no. 3, pp. 256–262, 1998. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Rzeszowska-Wolny, W. M. Przybyszewski, and M. Widel, “Ionizing radiation-induced bystander effects, potential targets for modulation of radiotherapy,” European Journal of Pharmacology, vol. 625, no. 1–3, pp. 156–164, 2009. View at Google Scholar
  16. K. M. Prise and J. M. OSullivan, “Radiation-induced bystander signaling in cancer therapy,” Nature Reviews Cancer, vol. 9, no. 5, pp. 351–360, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. S. Kon'kova, A. V. Ermakov, L. V. Efremova, S. V. Kostyuk, and N. N. Veiko, “Influence of X-ray and/or CpG-DNA induced oxidative stress on adaptive response in human lymphocytes,” International Journal of Low Radiation, vol. 7, no. 6, pp. 446–452, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. A. V. Ermakov, M. S. Kon'kova, S. V. Kostyuk et al., “Development of the adaptive response and bystander effect induced by low-dose ionizing radiation in human mesenchymal stem cells,” in Proceedings of the 6th International Conference on Circulating Nucleic Acids in Plasma and Serum (CNAPS ‘11), pp. 225–231, Springer Netherlands. View at Google Scholar
  19. K. V. Glebova, I. L. Konorova, A. V. Marakhonov, I. V. Barskov, L. G. Khaspekov, and N. N. Veiko, “Oxidative modification of ecDNA alter its biological action on rat neurons,” Journal of Nucleic Acids Investigation, vol. 2, no. 1, p. 28, 2011. View at Google Scholar
  20. S. V. Kostyuk, A. V. Ermakov, A. Y. Alekseeva et al., “Role of extracellular DNA oxidative modification in radiation induced bystander effects in human endotheliocytes,” Mutation Research, vol. 729, no. 1-2, pp. 52–60, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. D. M. Spitkovskiĭ, N. N. Veĭko, A. V. Ermakov et al., “Structural and functional changing induced by exposure to adaptive doses of X-rays in the human lymphocytes both normal and defective by reparation of DNA double strands breaks,” Radiation Biology, Radioecology, vol. 43, no. 2, pp. 136–143, 2003. View at Google Scholar
  22. T. Reya, S. J. Morrison, M. F. Clarke, and I. L. Weissman, “Stem cells, cancer, and cancer stem cells,” Nature, vol. 414, no. 6859, pp. 105–111, 2011. View at Google Scholar
  23. S. Kostyuk, T. Smirnova, L. Kameneva et al., “GC-rich extracellular DNA induces oxidative stress, double-strand DNA breaks, and DNA damage response in human adipose-derived mesenchymal stem cells,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 782123, 15 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Loseva, S. Kostyuk, E. Malinovskaya et al., “Extracellular DNA oxidation stimulates activation of NRF2 and reduces the production of ROS in human mesenchymal stem cells,” Expert Opinion on Biological Therapy, vol. 12, Supplement 1, pp. 85–97, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. D. Mangal, D. Vudathala, J. Park, H. L. Seon, T. M. Penning, and I. A. Blair, “Analysis of 7,8-dihydro-8-oxo-2-deoxyguanosine in cellular DNA during oxidative stress,” Chemical Research in Toxicology, vol. 22, no. 5, pp. 788–797, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. J. Ravanat, T. Douki, P. Duez et al., “Cellular background level of 8-oxo-7,8-dihydro-2-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up,” Carcinogenesis, vol. 23, no. 11, pp. 1911–1918, 2002. View at Publisher · View at Google Scholar
  27. J. K. Leach, G. van Tuyle, P. S. Lin, R. Schmidt-Ullrich, and R. B. Mikkelsen, “Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen,” Cancer Research, vol. 61, no. 10, pp. 3894–3901, 2001. View at Google Scholar
  28. L. B. CP, H. Ischiropoulos, and S. C. Bondy, “Bondy evaluation of the probe 2,7-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress,” Chemical Research in Toxicology, vol. 5, pp. 227–231, 1992. View at Publisher · View at Google Scholar
  29. A. Cossarizza, R. Ferraresi, L. Troiano et al., “Simultaneous analysis of reactive oxygen species and reduced glutathione content in living cells by polychromatic flow cytometry,” Nature Protocols, vol. 4, no. 12, pp. 1790–1797, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. H. Zhu, G. L. Bannenberg, P. Moldeus, and H. G. Shertzer, “Oxidation pathways for the intracellular probe 2_,7_-dichlorofluorescein,” Archives of Toxicology, vol. 68, pp. 582–587, 1994. View at Publisher · View at Google Scholar · View at Scopus
  31. U. Weyemi and C. Dupuy, “The emerging role of ROS-generating NADPH oxidase NOX4 in DNA-damage responses,” Mutation Research, vol. 751, no. 2, pp. 77–81, 2012. View at Google Scholar
  32. F. Chen, S. Haigh, S. Barman, and D. J. Fulton, “From form to function: the role of Nox4 in the cardiovascular system,” Frontiers in Physiology, vol. 1, no. 3, p. 412, 2012. View at Google Scholar
  33. A. N. Lyle, N. N. Deshpande, Y. Taniyama et al., “Poldip 2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells,” Circulation Research, vol. 105, pp. 249–259, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. A. R. Collins, “Measuring oxidative damage to DNA and its repair with the comet assay,” Biochimica et Biophysica Acta, vol. 13, pp. 150–155, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Löbrich, A. Shibata, A. Beucher et al., “GammaH2AX foci analysis for monitoring DNA double strand break repair: strengths, limitations and optimization,” Cell Cycle, vol. 9, no. 4, pp. 662–669, 2010. View at Publisher · View at Google Scholar
  36. K. J. McManus and M. J. Hendzel, “ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells,” Molecular Biology of the Cell, vol. 16, no. 10, pp. 5013–5025, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. A. A. Goodarzi and P. A. Jeggo, “The repair and signaling responses to DNA double-strand breaks,” Advances in Genetics, vol. 82, pp. 1–45, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Mermershtain and J. N. Glover, “Structural mechanisms underlying signaling in the cellular response to DNA double strand breaks,” Mutation Research, vol. 750, no. 1-2, pp. 15–22, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. R. E. Shackelford, W. K. Kaufmann, and R. S. Paules, “Oxidative stress and cell cycle checkpoint function,” Free Radical Biology & Medicine, vol. 28, no. 9, pp. 1387–1404, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. R. Bologna-Molina, A. Mosqueda-Taylor, N. Molina-Frechero, A. D. Mori-Estevez, and G. Sánchez-Acuña, “Comparison of the value of PCNA and Ki-67 as markers of cell proliferation in ameloblastic tumors,” Medicina Oral, Patología Oral y Cirugía Bucal, vol. 18, no. 2, pp. 174–179, 2013. View at Google Scholar
  41. A. Wells, L. Griffith, J. Z. Wells, and D. P. Taylor, “The dormancy dilemma: quiescence versus balanced proliferation,” Cancer Research, vol. 73, no. 13, pp. 3811–3816, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Cory, D. C. Huang, and J. M. Adams, “The Bcl-2 family: roles in cell survival and oncogenesis,” Oncogene, vol. 22, no. 53, pp. 590–607, 2003. View at Publisher · View at Google Scholar · View at Scopus
  43. T. W. Kensler and N. Wakabayashi, “Nrf2: friend or foe for chemoprevention?” Carcinogenesis, vol. 31, no. 1, pp. 90–99, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Jahr, H. Hentze, S. Englisch et al., “DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells,” Cancer Research, vol. 61, no. 4, pp. 1659–1665, 2001. View at Google Scholar
  45. M. van der Vaart and P. J. Pretorius, “Circulating DNA: its origin and fluctuation,” Annals of the New York Academy of Sciences, vol. 1137, pp. 18–26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Hajizadeh, J. DeGroot, M. TeKoppele, A. Tarkowski, and L. V. Collins, “Extracellular mitochondrial DNA and oxidatively damaged DNA in synovial fluid of patients with rheumatoid arthritis,” Arthritis Research & Therapy, vol. 5, no. 5, pp. R234–R240, 2001. View at Google Scholar
  47. B. Zhang, A. Angelidou, K. D. Alysandratos et al., “Mitochondrial DNA and anti-mitochondrial antibodies in serum of autistic children,” Journal of Neuroinflammation, vol. 7, pp. 80–85, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Cossarizza, M. Pinti, M. Nasi et al., “Increased plasma levels of extracellular mitochondrial DNA during HIV infection: a new role for mitochondrial damage-associated molecular patterns during inflammation,” Mitochondrion, vol. 11, no. 5, pp. 750–755, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Suter and C. Richter, “Fragmented mitochondrial DNA is the predominant carder of oxidized DNA bases,” Biochemistry, vol. 38, no. 1, pp. 459–464, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. I. B. Korzeneva, S. V. Kostuyk, E. S. Ershova et al., “Human circulating ribosomal DNA content significantly increases while circulating satellite III (1q12) content decreases under chronic occupational exposure to low-dose gamma- neutron and tritium beta-radiation,” Mutation Research, vol. 791-792, pp. 49–60, 2016. View at Publisher · View at Google Scholar · View at Scopus
  51. A. V. Ermakov, S. V. Kostyuk, M. S. Konkova, N. A. Egolina, E. M. Malinovskaya, and N. N. Veiko, “Extracellular DNA fragments,” Annals of the New York Academy of Sciences, vol. 1137, pp. 41–46, 2008. View at Google Scholar
  52. E. M. Malinovskaya, T. D. Smirnova, and N. A. Egolina, “Changes in human ribosomal genes ensemble with ageing,” Medical Genetics, vol. 7, no. 2, pp. 10–16, 2008. View at Google Scholar
  53. N. N. Veĭko, N. V. Bulycheva, O. A. Roginko et al., “Ribosomal repeat in cell free DNA as a marker for cell death,” Biochemistry (Moscow) Supplement Series B: Biomedical Chemistry, vol. 2, no. 2, pp. 198–207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. A. V. Ermakov, M. S. Kon'kova, S. V. Kostyuk et al., “An extracellular DNA mediated bystander effect produced from low dose irradiated endothelial cells,” Mutation Research, vol. 712, no. 1-2, pp. 1–10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. A. V. Ermakov, M. S. Kon'kova, S. V. Kostiuk et al., “Bystander effect development in human mesenchymal stem cells after exposure to adaptive dose of X-radiation,” Radiatsionnaia Biologiia, Radioecologiia, vol. 50, no. 1, pp. 42–51, 2010. View at Google Scholar
  56. S. V. Kostyuk, T. D. Smirnova, L. V. Efremova et al., “Enhanced expression of iNOS in human endothelial cells during long-term culturing with extracellular DNA fragments,” Bulletin of Experimental Biology and Medicine, vol. 149, no. 2, pp. 191–195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. L. V. Efremova, A. Y. Alekseeva, M. S. Kon'kova et al., “Extracellular DNA affects NO content in human endothelial cells,” Bulletin of Experimental Biology and Medicine, vol. 149, no. 2, pp. 196–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. F. M. Lyng, C. B. Seymour, and C. Mothersill, “Early events in the apoptotic cascade initiated in cells treated with medium from the progeny of irradiated cells,” Radiation Protection Dosimetry, vol. 99, no. 1–4, pp. 169–172, 2002. View at Google Scholar
  59. S. V. Kostyuk, M. S. Konkova, E. S. Ershova et al., “An exposure to the oxidized DNA enhances both instability of genome and survival in cancer cells,” PLoS One, vol. 8, no. 10, article e77469, 2013. View at Publisher · View at Google Scholar · View at Scopus
  60. P. Henneke, O. Takeuchi, R. Malley et al., “Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways,” The Journal of Immunology, vol. 169, no. 7, pp. 3970–3977, 2002. View at Publisher · View at Google Scholar
  61. L. József, T. Khreiss, D. El Kebir, and J. G. Filep, “Activation of TLR-9 induces IL-8 secretion through peroxynitrite signaling in human neutrophils,” The Journal of Immunology, vol. 176, no. 2, pp. 1195–1202, 2006. View at Publisher · View at Google Scholar
  62. Y. Adachi, A. L. Kindzelskii, A. R. Petty et al., “IFN-γ primes RAW264 macrophages and human monocytes for enhanced oxidant production in response to CpG DNA via metabolic signaling: roles of TLR9 and myeloperoxidase trafficking,” The Journal of Immunology, vol. 176, no. 8, pp. 5033–5040, 2006. View at Publisher · View at Google Scholar
  63. S. V. Kostiuk, E. M. Malinovskaia, A. V. Ermakov et al., “Cell-free DNA fragments increase transcription in human mesenchymal stem cells, activate TLR-dependent signal pathway and suppress apoptosis,” Biomeditsinskaya Khimiya, vol. 58, no. 6, pp. 673–683, 2012. View at Publisher · View at Google Scholar
  64. A. V. Ermakov, M. S. Kon'kova, S. V. Kostyuk, N. A. Egolina, L. V. Efremova, and N. N. Veiko, “Oxidative stress as a significant factor for development of an adaptive response in irradiated and nonirradiated human lymphocytes after inducing the bystander effect by low-dose X-radiation,” Mutation Research, vol. 669, no. 1-2, pp. 155–161, 2009. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Hornung and E. Latz, “Intracellular DNA recognition,” Nature Reviews Immunology, vol. 10, no. 2, pp. 123–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. P. Nagaria, C. Robert, and F. V. Rassool, “DNA double-strand break response in stem cells: mechanisms to maintain genomic integrity,” Biochimica et Biophysica Acta, vol. 1830, no. 2, pp. 2345–2353, 2013. View at Publisher · View at Google Scholar · View at Scopus