Response of murine neural stem/progenitor cells to gamma-neutron radiation

References

• Acharya MM, Lan ML, Kan VH, Patel NH, Giedzinski E, Tseng BP, Limoli CL. 2010. Consequences of ionizing radiation-induced damage in human neural stem cells. Free Radic Biol Med. 49(12):1846–1855.
   PubMed Web of Science ®Google Scholar
• Aguirre A, Rubio ME, Gallo V. 2010. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature. 467(7313):323–327.
   PubMed Web of Science ®Google Scholar
• Arzumanov SS, Safronov VV, Strepetov AN. 2018. Determination of a dose absorbed in a biological sample under mixed gamma-neutron irradiation. Tech Phys. 63(10):1533–1536.
   Web of Science ®Google Scholar
• Asaithamby A, Hu B, Chen DJ. 2011. Unrepaired clustered DNA lesions induce chromosome breakage in human cells. Proc Natl Acad Sci USA. 108(20):8293–8298.
   PubMed Web of Science ®Google Scholar
• Ayuso-Sacido A, Moliterno JA, Kratovac S, Kapoor GS, O'Rourke DM, Holland EC, García-Verdugo JM, Roy NS, Boockvar JA. 2010. Activated EGFR signaling increases proliferation, survival, and migration and blocks neuronal differentiation in post-natal neural stem cells. J Neurooncol. 97(3):323–337.
   PubMed Web of Science ®Google Scholar
• Barazzuol L, Hopkins SR, Ju L, Jeggo PA. 2019. Distinct response of adult neural stem cells to low versus high dose ionising radiation. DNA Repair. 76:70–75.
   PubMed Web of Science ®Google Scholar
• Barazzuol L, Ju L, Jeggo PA. 2017. A coordinated DNA damage response promotes adult quiescent neural stem cell activation. PLOS Biol. 15(5):e2001264.
   PubMed Web of Science ®Google Scholar
• Bohgaki T, Bohgaki M, Hakem R. 2010. DNA double-strand break signaling and human disorders. Genome Integr. 1(1):15.
   PubMedGoogle Scholar
• Brooks AL, Hoel DG, Preston RJ. 2016. The role of dose rate in radiation cancer risk: evaluating the effect of dose rate at the molecular, cellular and tissue levels using key events in critical pathways following exposure to low LET radiation. Int J Radiat Biol. 92(8):405–426.
   PubMed Web of Science ®Google Scholar
• Buono KD, Goodus MT, Moore L, Ziegler AN, Levison SW. 2015. Chapter 15 – multimarker flow cytometric characterization, isolation and differentiation of neural stem cells and progenitors of the normal and injured mouse subventricular zone. In: Pruszak J, editor. Neural surface antigens. Boston (MA): Academic Press; p. 175–186.
   Google Scholar
• Buono KD, Vadlamuri D, Gan Q, Levison SW. 2012. Leukemia inhibitory factor is essential for subventricular zone neural stem cell and progenitor homeostasis as revealed by a novel flow cytometric analysis. Dev Neurosci. 34(5):449–462.
   PubMed Web of Science ®Google Scholar
• Cavazzin C, Neri M, Gritti A. 2013. Isolate and culture precursor cells from the adult periventricular area. Methods Mol Biol. 1059:25–40.
   PubMedGoogle Scholar
• Chen H, Goodus MT, de Toledo SM, Azzam EI, Levison SW, Souayah N. 2015. Ionizing radiation perturbs cell cycle progression of neural precursors in the subventricular zone without affecting their long-term self-renewal. ASN Neuro. 7(3):175909141557802.
   Web of Science ®Google Scholar
• Cochard LM, Levros LC Jr., Joppé SE, Pratesi F, Aumont A, Fernandes KJL. 2021. Manipulation of EGFR-induced signaling for the recruitment of quiescent neural stem cells in the adult mouse forebrain. Front Neurosci. 15:621076.
   PubMed Web of Science ®Google Scholar
• Codega P, Silva-Vargas V, Paul A, Maldonado-Soto AR, Deleo AM, Pastrana E, Doetsch F. 2014. Prospective identification and purification of quiescent adult neural stem cells from their in vivo niche. Neuron. 82(3):545–559.
   PubMed Web of Science ®Google Scholar
• Coskun V, Wu H, Blanchi B, Tsao S, Kim K, Zhao J, Biancotti JC, Hutnick L, Krueger RC, Fan G, et al. 2008. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc Natl Acad Sci USA. 105(3):1026–1031.
   PubMed Web of Science ®Google Scholar
• Daynac M, Chicheportiche A, Pineda JR, Gauthier LR, Boussin FD, Mouthon M-A. 2013. Quiescent neural stem cells exit dormancy upon alteration of GABAAR signaling following radiation damage. Stem Cell Res. 11(1):516–528.
   PubMed Web of Science ®Google Scholar
• Deleyrolle LP, Rietze RL, Reynolds BA. 2008. The neurosphere assay, a method under scrutiny. Acta Neuropsychiatr. 20(1):2–8.
   PubMed Web of Science ®Google Scholar
• Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med. 4(11):1313–1317.
   PubMed Web of Science ®Google Scholar
• Fukuda S, Kato F, Tozuka Y, Yamaguchi M, Miyamoto Y, Hisatsune T. 2003. Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J Neurosci. 23(28):9357–9366.
   PubMed Web of Science ®Google Scholar
• Goodhead DT. 2019. Neutrons are forever! Historical perspectives. Int J Radiat Biol. 95(7):957–984.
   PubMed Web of Science ®Google Scholar
• Haldbo-Classen L, Amidi A, Wu LM, Lukacova S, Oettingen GV, Gottrup H, Zachariae R, Høyer M. 2019. Long-term cognitive dysfunction after radiation therapy for primary brain tumors. Acta Oncol. 58(5):745–752.
   PubMed Web of Science ®Google Scholar
• Hartlerode AJ, Scully R. 2009. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J. 423(2):157–168.
   PubMedGoogle Scholar
• Hladik D, Tapio S. 2016. Effects of ionizing radiation on the mammalian brain. Mutat Res Rev Mutat Res. 770(Pt B):219–230.
   PubMedGoogle Scholar
• Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature. 461(7267):1071–1078.
   PubMed Web of Science ®Google Scholar
• Jakob B, Splinter J, Durante M, Taucher-Scholz G. 2009. Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc Natl Acad Sci USA. 106(9):3172–3177.
   PubMed Web of Science ®Google Scholar
• Jezkova L, Zadneprianetc M, Kulikova E, Smirnova E, Bulanova T, Depes D, Falkova I, Boreyko A, Krasavin E, Davidkova M, et al. 2018. Particles with similar LET values generate DNA breaks of different complexity and reparability: a high-resolution microscopy analysis of γH2AX/53BP1 foci [10.1039/C7NR06829H. Nanoscale. 10(3):1162–1179.
   PubMed Web of Science ®Google Scholar
• Jones B. 2020. Clinical radiobiology of fast neutron therapy: what was learnt? Front Oncol. 10:1537.
   PubMed Web of Science ®Google Scholar
• Kiyozuka M, Akimoto T, Fukutome M, Motegi A, Mitsuhashi N. 2013. Radiation-induced dimer formation of EGFR: implications for the radiosensitizing effect of cetuximab. Anticancer Res. 33(10):4337–4346.
   PubMed Web of Science ®Google Scholar
• Krasieva TB, Giedzinski E, Tran K, Lan M, Limoli CL, Tromberg BJ. 2011. Probing the impact of gamma-irradiation on the metabolic state of neural stem and precursor cells using dual-wavelength intrinsic signal two-photon excited fluorescence. J Innov Opt Health Sci. 4(3):289–300.
   PubMed Web of Science ®Google Scholar
• Lee H-C, An S, Lee H, Woo S-H, Jin H-O, Seo S-K, Choe T-B, Yoo D-H, Lee S-J, Hong Y-J, et al. 2008. Activation of epidermal growth factor receptor and its downstream signaling pathway by nitric oxide in response to ionizing radiation. Mol Cancer Res. 6(6):996–1002.
   PubMed Web of Science ®Google Scholar
• Liang X, Ho So Y, Cui J, Ma K, Xu X, Zhao Y, Cai L, Li W. 2011. The low-dose ionizing radiation stimulates cell proliferation via activation of the MAPK/ERK pathway in rat cultured mesenchymal stem cells. J Radiat Res. 52(3):380–386.
   PubMed Web of Science ®Google Scholar
• Lorat Y, Timm S, Jakob B, Taucher-Scholz G, Rübe CE. 2016. Clustered double-strand breaks in heterochromatin perturb DNA repair after high linear energy transfer irradiation. Radiother Oncol. 121(1):154–161.
   PubMed Web of Science ®Google Scholar
• Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA. 2008. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells. 26(4):988–996.
   PubMed Web of Science ®Google Scholar
• Merchant TE, Conklin HM, Wu S, Lustig RH, Xiong X. 2009. Late effects of conformal radiation therapy for pediatric patients with low-grade glioma: prospective evaluation of cognitive, endocrine, and hearing deficits. J Clin Oncol. 27(22):3691–3697.
   PubMed Web of Science ®Google Scholar
• Mich JK, Signer RA, Nakada D, Pineda A, Burgess RJ, Vue TY, Johnson JE, Morrison SJ. 2014. Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. Elife. 3:e02669.
   PubMed Web of Science ®Google Scholar
• Mineyeva OA, Barykina NV, Bezriadnov DV, Latushkin ST, Ryazanov AI, Unezhev VN, Shuvaev SA, Usova SV, Lazutkin AA. 2019. Suppressed neurogenesis without cognitive deficits: effects of fast neutron irradiation in mice. Neuroreport. 30(8):538–543.
   PubMed Web of Science ®Google Scholar
• Ming G, Song H. 2011. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 70(4):687–702.
   PubMed Web of Science ®Google Scholar
• Nakajima NI, Brunton H, Watanabe R, Shrikhande A, Hirayama R, Matsufuji N, Fujimori A, Murakami T, Okayasu R, Jeggo P, et al. 2013. Visualisation of γH2AX foci caused by heavy ion particle traversal; distinction between core track versus non-track damage. PLOS One. 8(8):e70107.
   PubMed Web of Science ®Google Scholar
• Narayanan G, Yu YH, Tham M, Gan HT, Ramasamy S, Sankaran S, Hariharan S, Ahmed S. 2016. Enumeration of neural stem cells using clonal assays. J Vis Exp. (116):e54456. DOI: 10.3791/54456.
   Google Scholar
• Nickoloff JA, Sharma N, Taylor L. 2020. Clustered DNA double-strand breaks: biological effects and relevance to cancer radiotherapy. Genes. 11(1):99.
   PubMed Web of Science ®Google Scholar
• Nikitaki Z, Nikolov V, Mavragani IV, Mladenov E, Mangelis A, Laskaratou DA, Fragkoulis GI, Hellweg CE, Martin OA, Emfietzoglou D, et al. 2016. Measurement of complex DNA damage induction and repair in human cellular systems after exposure to ionizing radiations of varying linear energy transfer (LET). Free Radic Res. 50(sup1):S64–S78.
   PubMed Web of Science ®Google Scholar
• Pacey L, Stead S, Gleave J, Tomczyk K, Doering L. 2006. Neural stem cell culture: neurosphere generation, microscopical analysis and cryopreservation. Protoc Exchange. DOI:10.1038/nprot.2006.215.
   Google Scholar
• Pazzaglia S, Briganti G, Mancuso M, Saran A. 2020. Neurocognitive decline following radiotherapy: mechanisms and therapeutic implications. Cancers. 12(1):146.
   Web of Science ®Google Scholar
• Perez RL, Best G, Nicolay NH, Greubel C, Rossberger S, Reindl J, Dollinger G, Weber K-J, Cremer C, Huber PE. 2016. Superresolution light microscopy shows nanostructure of carbon ion radiation-induced DNA double-strand break repair foci. FASEB J. 30(8):2767–2776.
   PubMed Web of Science ®Google Scholar
• Polo SE, Jackson SP. 2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25(5):409–433.
   PubMed Web of Science ®Google Scholar
• Posypanova GA, Ratushnyak MG, Semochkina YP, Abisheva AA, Moskaleva EY. 2019. The sensitivity of the cultured murine neural stem cells to the ionizing radiation. Tsitologiya. 61(10):806–816.
   Google Scholar
• Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255(5052):1707–1710.
   PubMed Web of Science ®Google Scholar
• Rockhill JK, Laramore GE. 2016. Chapter 20 – neutron radiotherapy. In: Gunderson LL, Tepper JE, editors. Clinical radiation oncology. 4th ed. Philadelphia (PA): Elsevier; p. 373–380.e372.
   Google Scholar
• Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol. 146(5):905–916.
   PubMed Web of Science ®Google Scholar
• Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. 2000. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem. 275(13):9390–9395.
   PubMed Web of Science ®Google Scholar
• Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 273(10):5858–5868.
   PubMed Web of Science ®Google Scholar
• Saad S, Wang TJ. 2015. Neurocognitive deficits after radiation therapy for brain malignancies. Am J Clin Oncol. 38(6):634–640.
   PubMed Web of Science ®Google Scholar
• Saha S, Woodbine L, Haines J, Coster M, Ricket N, Barazzuol L, Ainsbury E, Sienkiewicz Z, Jeggo P. 2014. Increased apoptosis and DNA double-strand breaks in the embryonic mouse brain in response to very low-dose X-rays but not 50 Hz magnetic fields. J R Soc Interface. 11(100):20140783.
   PubMed Web of Science ®Google Scholar
• Scherthan H, Lee JH, Maus E, Schumann S, Muhtadi R, Chojowski R, Port M, Lassmann M, Bestvater F, Hausmann M. 2019. Nanostructure of clustered DNA damage in leukocytes after in-solution irradiation with the alpha emitter Ra-223. Cancers. 11(12):1877.
   Web of Science ®Google Scholar
• Schmitt E, Paquet C, Beauchemin M, Bertrand R. 2007. DNA-damage response network at the crossroads of cell-cycle checkpoints, cellular senescence and apoptosis. J Zhejiang Univ Sci B. 8(6):377–397.
   PubMedGoogle Scholar
• Schröder A, Kriesen S, Hildebrandt G, Manda K. 2019. First insights into the effect of low-dose X-ray irradiation in adipose-derived stem cells. Int J Mol Sci. 20(23). DOI:10.3390/ijms20236075.
   Web of Science ®Google Scholar
• Scott SP, Pandita TK. 2006. The cellular control of DNA double-strand breaks. J Cell Biochem. 99(6):1463–1475.
   PubMed Web of Science ®Google Scholar
• Shen T, Huang S. 2012. The role of Cdc25A in the regulation of cell proliferation and apoptosis. Anticancer Agents Med Chem. 12(6):631–639.
   PubMed Web of Science ®Google Scholar
• Stucki M, Jackson SP. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair. 5(5):534–543.
   PubMed Web of Science ®Google Scholar
• Sturla LM, Amorino G, Alexander MS, Mikkelsen RB, Valerie K, Schmidt-Ullrichr RK. 2005. Requirement of Tyr-992 and Tyr-1173 in phosphorylation of the epidermal growth factor receptor by ionizing radiation and modulation by SHP2. J Biol Chem. 280(15):14597–14604.
   PubMed Web of Science ®Google Scholar
• Tamaishi N, Tsukimoto M, Kitami A, Kojima S. 2011. P2Y6 receptors and ADAM17 mediate low-dose gamma-ray-induced focus formation (activation) of EGF receptor. Radiat Res. 175(2):193–200.
   PubMed Web of Science ®Google Scholar
• Tseng BP, Giedzinski E, Izadi A, Suarez T, Lan ML, Tran KK, Acharya MM, Nelson GA, Raber J, Parihar VK, et al. 2014. Functional consequences of radiation-induced oxidative stress in cultured neural stem cells and the brain exposed to charged particle irradiation. Antioxid Redox Signaling. 20(9):1410–1422.
   PubMed Web of Science ®Google Scholar
• Urushibara A, Shikazono N, O'Neill P, Fujii K, Wada S, Yokoya A. 2008. LET dependence of the yield of single-, double-strand breaks and base lesions in fully hydrated plasmid DNA films by 4He(2+) ion irradiation. Int J Radiat Biol. 84(1):23–33.
   PubMed Web of Science ®Google Scholar
• Vítor AC, Huertas P, Legube G, de Almeida SF. 2020. Studying DNA double-strand break repair: an ever-growing toolbox. Front Mol Biosci. 7:24.
   PubMed Web of Science ®Google Scholar
• Xu Y, Shao Y, Voorhees JJ, Fisher GJ. 2006. Oxidative inhibition of receptor-type protein-tyrosine phosphatase kappa by ultraviolet irradiation activates epidermal growth factor receptor in human keratinocytes. J Biol Chem. 281(37):27389–27397.
   PubMed Web of Science ®Google Scholar
• Yang L, Liu Z, Chen C, Cong X, Li Z, Zhao S, Ren M. 2017. Low-dose radiation modulates human mesenchymal stem cell proliferation through regulating CDK and Rb. Am J Transl Res. 9(4):1914–1921.
   PubMed Web of Science ®Google Scholar
• Yang M, Kim H, Kim J, Kim SH, Kim JC, Bae CS, Kim JS, Shin T, Moon C. 2012. Fast neutron irradiation deteriorates hippocampus-related memory ability in adult mice. J Vet Sci. 13(1):1–6.
   PubMed Web of Science ®Google Scholar
• Yang M, Kim JS, Son Y, Kim J, Kim JY, Kim SH, Kim JC, Shin T, Moon C. 2011. Detrimental effect of fast neutrons on cultured immature rat hippocampal cells: relative biological effectiveness of in vitro cell death indices. Radiat Res. 176(3):303–310.
   PubMed Web of Science ®Google Scholar
• Yang M, Kim JS, Song MS, Kim JC, Shin T, Lee SS, Kim SH, Moon C. 2010. Dose-response and relative biological effectiveness of fast neutrons: induction of apoptosis and inhibition of neurogenesis in the hippocampus of adult mice. Int J Radiat Biol. 86(6):476–485.
   PubMed Web of Science ®Google Scholar