Variation of 4 MV X-ray dose rate in fractionated irradiation strongly impacts biological endothelial cell response in vitro

References

• Ben Kacem M, Benadjaoud MA, Dos Santos M, Soysouvanh F, Buard V, Tarlet G, Le Guen B, Francois A, Guipaud O, Milliat F, et al. 2020. Variation of 4 MV X-ray dose rate strongly impacts biological response both in vitro and in vivo. Sci Rep. 10(1):7021.
   PubMed Web of Science ®Google Scholar
• Bentzen SM, Dorr W, Gahbauer R, Howell RW, Joiner MC, Jones B, Jones DT, van der Kogel AJ, Wambersie A, Whitmore G. 2012. Bioeffect modeling and equieffective dose concepts in radiation oncology-terminology, quantities and units. Radiother Oncol. 105(2):266–268.
   PubMed Web of Science ®Google Scholar
• Boerma M, Schutte-Bart CI, Wedekind LE, Beekhuizen H, Wondergem J. 2003. Effects of multiple doses of ionizing radiation on cytokine expression in rat and human cells. Int J Radiat Biol. 79(11):889–896.
   PubMed Web of Science ®Google Scholar
• Brodin O, Lennartsson L, Nilsson S. 1991. Single-dose and fractionated irradiation of four human lung cancer cell lines in vitro. Acta Oncol. 30(8):967–974.
   PubMed Web of Science ®Google Scholar
• Cervelli T, Panetta D, Navarra T, Andreassi MG, Basta G, Galli A, Salvadori PA, Picano E, Turco SD. 2014. Effects of single and fractionated low-dose irradiation on vascular endothelial cells. Atherosclerosis. 235(2):510–518.
   PubMed Web of Science ®Google Scholar
• Chow M, Rubin H. 1996. Evidence for cellular aging in long-term confluent cultures: heritable impairment of proliferation, accumulation of age pigments and their loss in neoplastic transformation. Mech Ageing Dev. 89(3):165–183.
   PubMed Web of Science ®Google Scholar
• Dale RG. 1985. The application of the linear-quadratic dose-effect equation to fractionated and protracted radiotherapy. Br J Radiol. 58(690):515–528.
   PubMed Web of Science ®Google Scholar
• Debacq-Chainiaux F, Erusalimsky JD, Campisi J, Toussaint O. 2009. Protocols to detect senescence-associated beta-galactosidase (SA-betagal) activity, a biomarker of senescent cells in culture and in vivo. Nat Protoc. 4(12):1798–1806.
   PubMed Web of Science ®Google Scholar
• Dey S, Spring PM, Arnold S, Valentino J, Chendil D, Regine WF, Mohiuddin M, Ahmed MM. 2003. Low-dose fractionated radiation potentiates the effects of Paclitaxel in wild-type and mutant p53 head and neck tumor cell lines. Clin Cancer Res. 9(4):1557–1565.
   PubMed Web of Science ®Google Scholar
• Dos Santos MV, Paget M, Ben Kacem F, Trompier M, Benadjaoud A, Francois O, Guipaud M, Benderitter F., Milliat   2018. Importance of dosimetry protocol for cell irradiation on a low X-rays facility and consequences for the biological response. Int J Radiat Biol. 94(6):597–606.
   Web of Science ®Google Scholar
• Dunne AL, Price ME, Mothersill C, McKeown SR, Robson T, Hirst DG. 2003. Relationship between clonogenic radiosensitivity, radiation-induced apoptosis and DNA damage/repair in human colon cancer cells. Br J Cancer. 89(12):2277–2283.
   PubMed Web of Science ®Google Scholar
• Fast M, van de Schoot A, van de Lindt T, Carbaat C, van der Heide U, Sonke JJ. 2019. Tumor trailing for liver SBRT on the MR-Linac. Int J Radiat Oncol Biol Phys. 103(2):468–478.
   PubMed Web of Science ®Google Scholar
• Feofanova N, Geraldo JM, de Andrade LM. 2014. Radiation oncology in vitro: trends to improve radiotherapy through molecular targets. Biomed Res Int. 2014:1–13.
   Web of Science ®Google Scholar
• Fowler JF. 2010. 21 years of biologically effective dose. Br J Radiol. 83(991):554–568.
   PubMed Web of Science ®Google Scholar
• Fridlyanskaya I, Alekseenko L, Nikolsky N. 2015. Senescence as a general cellular response to stress: a mini-review. Exp Gerontol. 72:124–128.
   PubMed Web of Science ®Google Scholar
• Georg D, Knoos T, McClean B. 2011. Current status and future perspective of flattening filter free photon beams. Med Phys. 38(3):1280–1293.
   PubMed Web of Science ®Google Scholar
• Golanov AV, Konovalov NA, Antipina NA, Vetlova ER, Zolotova SV, Galkin MV, Arutyunov NV, Chamorsov АY, Krasnyanskiy SA, Nazarenko AG, et al. 2015. Stereotactic radiotherapy for spinal meningiomas and neurinomas. Zh Vopr Neirokhir Im N N Burdenko. 79(1):4–13.
   Google Scholar
• Gomolka M, Rossler U, Hornhardt S, Walsh L, Panzer W, Schmid E. 2005. Measurement of the initial levels of DNA damage in human lymphocytes induced by 29 kV X rays (mammography X rays) relative to 220 kV X rays and gamma rays. Radiat Res. 163(5):510–519.
   PubMed Web of Science ®Google Scholar
• Guipaud O, Jaillet C, Clement-Colmou K, Francois A, Supiot S, Milliat F. 2018. The importance of the vascular endothelial barrier in the immune-inflammatory response induced by radiotherapy. BJR. 91(1089):20170762.
   Google Scholar
• Gupta S, Koru-Sengul T, Arnold SM, Devi GR, Mohiuddin M, Ahmed MM. 2011. Low-dose fractionated radiation potentiates the effects of cisplatin independent of the hyper-radiation sensitivity in human lung cancer cells. Mol Cancer Ther. 10(2):292–302.
   PubMed Web of Science ®Google Scholar
• Hall EJ, Brenner DJ. 1991. The dose-rate effect revisited: radiobiological considerations of importance in radiotherapy. Int J Radiat Oncol Biol Phys. 21(6):1403–1414.
   PubMed Web of Science ®Google Scholar
• Hedman M, Bergqvist M, Brattstrom D, Brodin O. 2011. Fractionated irradiation of five human lung cancer cell lines and prediction of survival according to a radiobiology model. Anticancer Res. 31(4):1125–1130.
   PubMed Web of Science ®Google Scholar
• Helm A, Lee R, Durante M, Ritter S. 2016. The influence of C-ions and X-rays on human umbilical vein endothelial cells. Front Oncol. 6:5.
   PubMed Web of Science ®Google Scholar
• Ho JH, Chen YF, Ma WH, Tseng TC, Chen MH, Lee OK. 2011. Cell contact accelerates replicative senescence of human mesenchymal stem cells independent of telomere shortening and p53 activation: roles of Ras and oxidative stress. Cell Transplant. 20(8):1209–1220.
   PubMed Web of Science ®Google Scholar
• Jagetic LJ, Newhauser WD. 2015. A simple and fast physics-based analytical method to calculate therapeutic and stray doses from external beam, megavoltage x-ray therapy. Phys Med Biol. 60(12):4753–4775.
   PubMed Web of Science ®Google Scholar
• Jakl L, Markova E, Kolarikova L, Belyaev I. 2020. Biodosimetry of low dose ionizing radiation using DNA repair foci in human lymphocytes. Genes (Basel.) 11(1):58.
   PubMed Web of Science ®Google Scholar
• Jiang L, Xiong XP, Hu CS, Ou ZL, Zhu GP, Ying HM. 2013. In vitro and in vivo studies on radiobiological effects of prolonged fraction delivery time in A549 cells. J Radiat Res. 54(2):230–234.
   PubMed Web of Science ®Google Scholar
• Jones B, Dale RG, Deehan C, Hopkins KI, Morgan DA. 2001. The role of biologically effective dose (BED) in clinical oncology. Clin Oncol (R Coll Radiol). 13(2):71–81.
   PubMed Web of Science ®Google Scholar
• Kaderka R, Schardt D, Durante M, Berger T, Ramm U, Licher J, Tessa CL. 2012. Out-of-field dose measurements in a water phantom using different radiotherapy modalities. Phys Med Biol. 57(16):5059–5074.
   PubMed Web of Science ®Google Scholar
• Kim BC, Yoo HJ, Lee HC, Kang KA, Jung SH, Lee HJ, Lee M, Park S, Ji YH, Lee YS, et al. 2014. Evaluation of premature senescence and senescence biomarkers in carcinoma cells and xenograft mice exposed to single or fractionated irradiation. Oncol Rep. 31(5):2229–2235.
   PubMed Web of Science ®Google Scholar
• Kirkpatrick JP, Brenner DJ, Orton CG. 2009. Point/Counterpoint. The linear-quadratic model is inappropriate to model high dose per fraction effects in radiosurgery. Med Phys. 36(8):3381–3384.
   PubMed Web of Science ®Google Scholar
• Kirkpatrick JP, Meyer JJ, Marks LB. 2008. The linear-quadratic model is inappropriate to model high dose per fraction effects in radiosurgery. Semin Radiat Oncol. 18(4):240–243.
   PubMed Web of Science ®Google Scholar
• Kochan JA, Desclos ECB, Bosch R, Meister L, Vriend LEM, van Attikum H, Krawczyk PM. 2017. Meta-analysis of DNA double-strand break response kinetics. Nucleic Acids Res. 45(22):12625–12637.
   PubMed Web of Science ®Google Scholar
• Korpela E, Liu SK. 2014. Endothelial perturbations and therapeutic strategies in normal tissue radiation damage. Radiat Oncol. 9:266.
   PubMed Web of Science ®Google Scholar
• Koyama S, Narita E, Shinohara N, Miyakoshi J. 2018. Recovery kinetics of micronucleus formation by fractionated X-ray irradiation in various types of human cells. J Radiat Res. 59(5):547–554.
   PubMed Web of Science ®Google Scholar
• Krishnan EC, Krishnan L, Jewell B, Bhatia P, Jewell WR. 1987. Dose-dependent radiation effect on microvasculature and repair. J Natl Cancer Inst. 79(6):1321–1325.
   PubMedGoogle Scholar
• Laurent PA, Kownacka A, Boidot R, Richard C, Limagne E, Morgand V, Froidurot L, Bonin C, Aubignac L, Ghiringhelli F, et al. 2020. In-vivo and in-vitro impact of high-dose rate radiotherapy using flattening-filter-free beams on the anti-tumor immune response. Clin Transl Radiat Oncol. 24:116–122.
   PubMed Web of Science ®Google Scholar
• Mariotti LG, Pirovano G, Savage KI, Ghita M, Ottolenghi A, Prise KM, Schettino G. 2013. Use of the γ-H2AX assay to investigate DNA repair dynamics following multiple radiation exposures. PLoS One. 8(11):e79541.
   PubMed Web of Science ®Google Scholar
• Marthandan S, Priebe S, Hemmerich P, Klement K, Diekmann S. 2014. Long-term quiescent fibroblast cells transit into senescence. PLoS One. 9(12):e115597.
   PubMed Web of Science ®Google Scholar
• Matsui T, Nuryadi E, Komatsu S, Hirota Y, Shibata A, Oike T, Nakano T. 2019. Robustness of clonogenic assays as a biomarker for cancer cell radiosensitivity. Int J Mol Sci. 20(17):4148.
   Web of Science ®Google Scholar
• Mori R, Matsuya Y, Yoshii Y, Date H. 2018. Estimation of the radiation-induced DNA double-strand breaks number by considering cell cycle and absorbed dose per cell nucleus. J Radiat Res. 59(3):253–260.
   PubMed Web of Science ®Google Scholar
• Munro J, Steeghs K, Morrison V, Ireland H, Parkinson EK. 2001. Human fibroblast replicative senescence can occur in the absence of extensive cell division and short telomeres. Oncogene. 20(27):3541–3552.
   PubMed Web of Science ®Google Scholar
• Nikzad S, Hashemi B, Mahmoudi G, Baradaran-Ghahfarokhi M. 2015. Estimation of cell response in fractionation radiotherapy using different methods derived from linear quadratic model. Radiol Oncol. 49(4):347–356.
   PubMed Web of Science ®Google Scholar
• Noppe G, Dekker P, de Koning-Treurniet C, Blom J, van Heemst D, Dirks RW, Tanke HJ, Westendorp RG, Maier AB. 2009. Rapid flow cytometric method for measuring senescence associated beta-galactosidase activity in human fibroblasts. Cytometry A. 75(11):910–916.
   PubMed Web of Science ®Google Scholar
• Ogino H, Shibamoto Y, Sugie C, Ito M. 2005. Biological effects of intermittent radiation in cultured tumor cells: influence of fraction number and dose per fraction. J Radiat Res. 46(4):401–406.
   PubMed Web of Science ®Google Scholar
• Paget V, Ben Kacem M, Dos Santos M, Benadjaoud MA, Soysouvanh F, Buard V, Georges T, Vaurijoux A, Gruel G, Francois A, et al. 2019. Multiparametric radiobiological assays show that variation of X-ray energy strongly impacts relative biological effectiveness: comparison between 220 kV and 4 MV. Sci Rep. 9(1):14328.
   PubMed Web of Science ®Google Scholar
• Park KR, Monsky WL, Lee CG, Song CH, Kim DH, Jain RK, Fukumura D. 2016. Mast cells contribute to radiation-induced vascular hyperpermeability. Radiat Res. 185(2):182–189.
   PubMed Web of Science ®Google Scholar
• Pawlik TM, Keyomarsi K. 2004. Role of cell cycle in mediating sensitivity to radiotherapy. Int J Radiat Oncol Biol Phys. 59(4):928–942.
   PubMed Web of Science ®Google Scholar
• Puck TT, Marcus PI. 1956. Action of x-rays on mammalian cells. J Exp Med. 103(5):653–666.
   PubMed Web of Science ®Google Scholar
• Rannou E, Francois A, Toullec A, Guipaud O, Buard V, Tarlet G, Mintet E, Jaillet C, Iruela-Arispe ML, Benderitter M, et al. 2015. In vivo evidence for an endothelium-dependent mechanism in radiation-induced normal tissue injury. Sci Rep. 5:15738.
   PubMed Web of Science ®Google Scholar
• Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM. 2011. Recent developments in the use of γ-H2AX as a quantitative DNA double-strand break biomarker. Aging (Albany NY). 3(2):168–174.
   PubMedGoogle Scholar
• Redon CE, Dickey JS, Bonner WM, Sedelnikova OA. 2009. γ-H2AX as a biomarker of DNA damage induced by ionizing radiation in human peripheral blood lymphocytes and artificial skin. Adv Space Res. 43(8):1171–1178.
   PubMed Web of Science ®Google Scholar
• Sharma PM, Ponnaiya B, Taveras M, Shuryak I, Turner H, Brenner DJ. 2015. High throughput measurement of gammaH2AX DSB repair kinetics in a healthy human population. PLoS One. 10(3):e0121083.
   PubMed Web of Science ®Google Scholar
• Sheikh-Bagheri D, Rogers DW. 2002. Monte Carlo calculation of nine megavoltage photon beam spectra using the BEAM code. Med Phys. 29(3):391–402.
   PubMed Web of Science ®Google Scholar
• Słonina D, Spekl K, Panteleeva A, Brankovic K, Hoinkis C, Dörr W. 2003. Induction of micronuclei in human fibroblasts and keratinocytes by 25 kV x-rays. Radiat Environ Biophys. 42(1):55–61.
   PubMed Web of Science ®Google Scholar
• Smith LG, Miller RC, Richards M, Brenner DJ, Hall EJ. 1999. Investigation of hypersensitivity to fractionated low-dose radiation exposure. Int J Radiat Oncol Biol Phys. 45(1):187–191.
   PubMed Web of Science ®Google Scholar
• Terashima S, Hosokawa Y, Tsuruga E, Mariya Y, Nakamura T. 2017. Impact of time interval and dose rate on cell survival following low-dose fractionated exposures. J Radiat Res. 58(6):782–790.
   PubMed Web of Science ®Google Scholar
• Toullec A, Buard V, Rannou E, Tarlet G, Guipaud O, Robine S, Iruela-Arispe ML, Francois A, Milliat F. 2018. HIF-1α deletion in the endothelium, but not in the epithelium, protects from radiation-induced enteritis. Cell Mol Gastroenterol Hepatol. 5(1):15–30.
   PubMed Web of Science ®Google Scholar
• Tsamou M, Jennen DG, Claessen SM, Magkoufopoulou C, Kleinjans JC, van Delft JH. 2012. Performance of in vitro γH2AX assay in HepG2 cells to predict in vivo genotoxicity. Mutagenesis. 27(6):645–652.
   PubMed Web of Science ®Google Scholar
• Valentin J. 2003. Relative biological effectiveness (RBE), quality factor (Q), and radiation weighting factor (wR):ICRP Publication 92: Approved by the Commission in. January 2003. " Ann Icrp. 33(4):1–121.
   Google Scholar
• van den Berg J, Castricum KCM, Meel MH, Goedegebuure RSA, Lagerwaard FJ, Slotman BJ, Hulleman E, Thijssen V. 2020. Development of transient radioresistance during fractionated irradiation in vitro. Radiother Oncol. 148:107–114.
   PubMed Web of Science ®Google Scholar
• Venkatesulu BP, Mahadevan LS, Aliru ML, Yang X, Bodd MH, Singh PK, Yusuf SW, Abe JI, Krishnan S. 2018. Radiation-induced endothelial vascular injury: a review of possible mechanisms. JACC Basic Transl Sci. 3(4):563–572.
   PubMedGoogle Scholar
• Williams MV, Denekamp J, Fowler JF. 1985. A review of alpha/beta ratios for experimental tumors: implications for clinical studies of altered fractionation. Int J Radiat Oncol Biol Phys. 11(1):87–96.
   PubMed Web of Science ®Google Scholar
• Yau TM, Kim SC, Nygaard OF, Gregg EC, Crissman HA. 1980. Correlation of cell cycle parameters with radiation sensitivity in a series of murine L5178Y cells. Int J Radiat Biol Relat Stud Phys Chem Med. 37(4):429–435.
   PubMed Web of Science ®Google Scholar
• Yoon J, Heins D, Zhao X, Sanders M, Zhang R. 2017. Measurement and modeling of out-of-field doses from various advanced post-mastectomy radiotherapy techniques. Phys Med Biol. 62(23):9039–9053.
   PubMed Web of Science ®Google Scholar