Radiation‐induced tissue damage and response
Open accessAbstract
Normal tissue responses to ionizing radiation have been a major subject for study since the discovery of X-rays at the end of the 19th century. Shortly thereafter, time-dose relationships were established for some normal tissue endpoints that led to investigations into how the size of dose per fraction and the quality of radiation affected outcome. The assessment of the radiosensitivity of bone marrow stem cells using colony-forming assays by Till and McCulloch prompted the establishment of in situ clonogenic assays for other tissues that added to the radiobiology toolbox. These clonogenic and functional endpoints enabled mathematical modeling to be performed that elucidated how tissue structure, and in particular turnover time, impacted clinically relevant fractionated radiation schedules. More recently, lineage tracing technology, advanced imaging and single cell sequencing have shed further light on the behavior of cells within stem, and other, cellular compartments, both in homeostasis and after radiation damage. The discovery of heterogeneity within the stem cell compartment and plasticity in response to injury have added new dimensions to the consideration of radiation-induced tissue damage. Clinically, radiobiology of the 20th century garnered wisdom relevant to photon treatments delivered to a fairly wide field at around 2 Gy per fraction, 5 days per week, for 5-7 weeks. Recently, the scope of radiobiology has been extended by advances in technology, imaging and computing, as well as by the use of charged particles. These allow radiation to be delivered more precisely to tumors while minimizing the amount of normal tissue receiving high doses. One result has been an increase in the use of schedules with higher doses per fraction given in a shorter time frame (hypofractionation). We are unable to cover these new technologies in detail in this review, just as we must omit low-dose stochastic effects, and many aspects of dose, dose rate and radiation quality. We argue that structural diversity and plasticity within tissue compartments provides a general context for discussion of most radiation responses, while acknowledging many omissions. © 2020 The Authors. The Journal of Pathology published by John Wiley & Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In general, tissues that proliferate very slowly are less radiosensitive and will demonstrate radiation-induced damage much later than more rapidly proliferating tissues.
“In general, tissues that proliferate very slowly are less radiosensitive and will demonstrate radiation induced damage much later than more rapidly proliferating tissues ( 20 ).”
From Normal-Tissue Tolerance to Radiopharmaceutical Therapies, the Knowns and the Unknowns (2021) · cites this paper as [20]
The Conclusions state that tissues with slow turnover respond late to irradiation, supporting the timing comparison. The Introduction says the link between reproductive activity and radiosensitivity holds only partly, with many exceptions; greater sparing of slow-responding tissues under dose fractionation does not establish that they are generally less radiosensitive. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells1
Till, J. E., & McCulloch, E. A. (2010) · Radiation Research · doi:10.1667/rrxx28.1 · Cited by 4,036 · see citing works
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells
Till, J. E., & McCulloch, E. A. (1961) · Radiation Research · doi:10.2307/3570892 · Cited by 3,770 · see citing works
Kiel, M. J., Yilmaz, Ö. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., & Morrison, S. J. (2005) · Cell · doi:10.1016/j.cell.2005.05.026 · Cited by 3,168 · see citing works
The relationship between the spleen colony-forming cell and the haemopoietic stem cell.
Schofield, R. (1978) · PubMed · Cited by 2,319 · see citing works
Out of Eden: Stem Cells and Their Niches
Watt, F. M., & Hogan, A. B. L. M. (2000) · Science · doi:10.1126/science.287.5457.1427 · Cited by 1,754 · see citing works
ACTION OF X-RAYS ON MAMMALIAN CELLS
Puck, T. T., & Marcus, P. I. (1956) · The Journal of Experimental Medicine · doi:10.1084/jem.103.5.653 · Cited by 1,696 · see citing works
The cGAS–cGAMP–STING pathway connects DNA damage to inflammation, senescence, and cancer
Li, T., & Chen, Z. J. (2018) · Journal of Experimental Medicine · doi:10.1084/jem.20180139 · Cited by 1,293 · see citing works
Endothelial Apoptosis as the Primary Lesion Initiating Intestinal Radiation Damage in Mice
Paris, F., FUKS, Z. Y., Kang, A. D., Capodieci, P., Juan, G., Ehleiter, D., Haimovitz‐Friedman, A., Cordon‐Cardo, C., & Kolesnick, R. (2001) · Science · doi:10.1126/science.1060191 · Cited by 1,281 · see citing works
Cell intrinsic alterations underlie hematopoietic stem cell aging
Rossi, D. J., Bryder, D., Zahn, J. M., Ahlenius, H., Sonu, R., Wagers, A. J., & Weissman, I. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503280102 · Cited by 1,152 · cited 1× · see citing works
“These radiation-induced changes appear to be remarkably similar to aging with its LT-HSC defects [71], and upregulation of genes specifying the myeloid cells at the expense of those of the lymphoid system [72].”
BackgroundA p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity
Marión, R. M., Strati, K., Li, H., Murga, M., Blanco, R., Ortega, S., Fernandez-Capetillo, O., Serrano, M., & Blasco, M. A. (2009) · Nature · doi:10.1038/nature08287 · Cited by 1,028 · cited 5× · see citing works
“Immune DDR involves damage-associated molecular pattern (DAMP) molecules released from damaged cells, like HMGB1 [60], and cytoplasmic RNA and DNA [82].”
BackgroundInfluentialTales from the crypt: new insights into intestinal stem cells
Gehart, H., & Clevers, H. C. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0081-y · Cited by 984 · see citing works
Thames, H. D., Withers, H. R., Peters, L. J., et al. (1982) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(82)90517-x · Cited by 843 · see citing works
The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations
Yan, K. S., Chia, L. A., Li, X., Ootani, A., Su, J., Lee, J. Y., Su, N. Y., Luo, Y., Heilshorn, S. C., Amieva, M. R., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1118857109 · Cited by 817 · see citing works
Self-renewing diploid Axin2+ cells fuel homeostatic renewal of the liver
Wang, B., Zhao, L., Fish, M., Logan, C. Y., & Nusse, R. (2015) · Nature · doi:10.1038/nature14863 · Cited by 674 · see citing works
Oguro, H., Ding, L., & Morrison, S. J. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.05.014 · Cited by 657 · see citing works
The R-spondin/Lgr5/Rnf43 module: regulator of Wnt signal strength
de Lau, W., Peng, W. C., Gros, P., & Clevers, H. (2014) · Genes & Development · doi:10.1101/gad.235473.113 · Cited by 656 · see citing works
Long-term neurocognitive benefits of FLASH radiotherapy driven by reduced reactive oxygen species
Montay‐Gruel, P., Acharya, M. M., Petersson, K., Alikhani, L., Yakkala, C., Allen, B. D., Ollivier, J., Petit, B., Jorge, P. G., Syage, A. R., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901777116 · Cited by 603 · see citing works
Xu, J., Escamilla, J., Mok, S., David, J., Priceman, S. J., West, B. L., Bollag, G. E., McBride, W. H., & Wu, L. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-3981 · Cited by 571 · see citing works
Self-citationTreatment volume and tissue tolerance
Withers, H. R., Taylor, J. M. G., & Maciejewski, B. (1988) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(88)90098-3 · Cited by 446 · see citing works
Extreme sensitivity of some intestinal crypt cells to X and γ irradiation
Potten, C. S. (1977) · Nature · doi:10.1038/269518a0 · Cited by 441 · see citing works
Cytokines in Radiobiological Responses: A Review
Schaue, D., Kachikwu, E. L., & McBride, W. (2012) · Radiation Research · doi:10.1667/rr3031.1 · Cited by 372 · see citing works
Self-citationA new isoeffect curve for change in dose per fraction
Withers, H. R., Thames, H. D., & Peters, L. J. (1983) · Radiotherapy and Oncology · doi:10.1016/s0167-8140(83)80021-8 · Cited by 355 · see citing works
Induction of acute phase gene expression by brain irradiation
Hong, J., Chiang, C., Campbell, I. L., Sun, J.-R., Withers, H. R., & McBride, W. H. (1995) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(95)00279-8 · Cited by 349 · see citing works
Self-citationIdentifying the Stem Cell of the Intestinal Crypt: Strategies and Pitfalls
Barker, N., van Oudenaarden, A., & Clevers, H. C. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.09.009 · Cited by 320 · see citing works
Withers, H. R. (1975) · Advances in radiation biology · doi:10.1016/b978-0-12-035405-4.50012-8 · Cited by 305 · see citing works
Injury-Induced Senescence Enables In Vivo Reprogramming in Skeletal Muscle
Chiche, A., Le Roux, I., von Joest, M., Sakai, H., Aguín, S. B., Cazin, C., Salam, R., Fiette, L., Alegria, O., Flamant, P., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2016.11.020 · Cited by 295 · see citing works
Schaue, D., Micewicz, E. D., Ratikan, J. A., Xie, M. W., Cheng, G., & McBride, W. H. (2014) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2014.07.007 · Cited by 257 · see citing works
Self-citationThe Dose-survival Relationship for Irradiation of Epithelial Cells of Mouse Skin
Withers, H. R. (1967) · British Journal of Radiology · doi:10.1259/0007-1285-40-471-187 · Cited by 220 · see citing works
Circulating hematopoietic stem and progenitor cells are myeloid-biased in cancer patients
Wu, W.-C., Sun, H.-W., Chen, H.-T., Liang, J.-L., Yu, X.-J., Wu, C., Wang, Z.-L., & Zheng, L.-M. (2014) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1320753111 · Cited by 215 · see citing works
Tumor necrosis factor‐α inhibits seizures in mice via p75 receptors
Balosso, S., Ravizza, T., Perego, C., Peschon, J. J., Campbell, I. L., Simoni, M. G. D., & Vezzani, A. (2005) · Annals of Neurology · doi:10.1002/ana.20480 · Cited by 209 · see citing works
Crypt Base Columnar Stem Cells in Small Intestines of Mice Are Radioresistant
Hua, G., Thin, T. H., Feldman, R., Haimovitz‐Friedman, A., Clevers, H. C., FUKS, Z. Y., & Kolesnick, R. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.07.106 · Cited by 206 · see citing works
Nrf2 regulates haematopoietic stem cell function
Tsai, J. J.-Y., Dudakov, J. A., Takahashi, K., Shieh, J.-H., Velardi, E., Holland, A. M., Singer, N. V., West, M. L., Smith, O. M., Young, L. F., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2699 · Cited by 202 · see citing works
Nakorn, T. N., Traver, D. J., Weissman, I. L., & Akashi, K. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15272 · Cited by 200 · see citing works
Radiation-induced astrocytic and microglial responses in mouse brain
Chiang, C., McBride, W. H., & Withers, H. R. (1993) · Radiotherapy and Oncology · doi:10.1016/0167-8140(93)90174-7 · Cited by 190 · see citing works
Self-citationRadiation Survival and Regeneration Characteristics of Spermatogenic Stem Cells of Mouse Testis
Withers, H. R., Hunter, N. R., Barkley, H. T., et al. (1974) · Radiation Research · doi:10.2307/3573759 · Cited by 190 · see citing works
Gradual Regeneration of Mouse Testicular Stem Cells after Exposure to Ionizing Radiation
Meistrich, M. L., Hunter, N. R., Suzuki, N., Trostle‐Weige, P. K., & Withers, H. R. (1978) · Radiation Research · doi:10.2307/3574894 · Cited by 190 · see citing works
Radiation-induced damage in the central nervous system: an interpretation of target cell responses.
Aj, V. D. K. (1986) · PubMed · Cited by 184 · see citing works
Nrf2 protects against pulmonary fibrosis by regulating the lung oxidant level and Th1/Th2 balance
Kikuchi, N., Ishii, Y., Morishima, Y., Yageta, Y., Haraguchi, N., Itoh, K., Yamamoto, M. P., & Hizawa, N. (2010) · Respiratory Research · doi:10.1186/1465-9921-11-31 · Cited by 176 · see citing works
Shao, L., Feng, W., Li, H., Gardner, D., Luo, Y., Wang, Y., Liu, L., Meng, A., Sharpless, N. E., & Zhou, D. (2014) · Blood · doi:10.1182/blood-2013-07-515619 · Cited by 165 · see citing works
Nakorn, T. N., Traver, D. J., Weissman, I. L., & Akashi, K. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215272 · Cited by 165 · see citing works
Mills, J. C., & Sansom, O. J. (2015) · Science Signaling · doi:10.1126/scisignal.aaa7540 · Cited by 142 · see citing works
Large‐Scale Production of LGR5‐Positive Bipotential Human Liver Stem Cells
Schneeberger, K., Sánchez‐Romero, N., Ye, S., van Steenbeek, F. G., Oosterhoff, L. A., Pla Palacin, I., Chen, C., van Wolferen, M. E., van Tienderen, G., Lieshout, R., et al. (2020) · Hepatology · doi:10.1002/hep.31037 · Cited by 141 · see citing works
Neural Precursor Cells and Central Nervous System Radiation Sensitivity
Fike, J. R., Rosi, S., & Limoli, C. L. (2009) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2008.12.003 · Cited by 131 · see citing works
Differential roles of TNFR1 and TNFR2 signaling in adult hippocampal neurogenesis
Chen, Z., & Palmer, T. D. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.01.083 · Cited by 131 · see citing works
Links between Innate Immunity and Normal Tissue Radiobiology
Schaue, D., & McBride, W. H. (2010) · Radiation Research · doi:10.1667/rr1931.1 · Cited by 129 · see citing works
Self-citationLong-Term Impairment of Subependymal Repopulation Following Damage by Ionizing Irradiation
Tada, E., Yang, C., Gobbel, G. T., Lamborn, K. R., & Fike, J. R. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7172 · Cited by 122 · see citing works
Michalowski, A. S. (1981) · Radiation and Environmental Biophysics · doi:10.1007/bf01324183 · Cited by 121 · see citing works
Mammalian Radiation Lethality: A Disturbance in Cellular Kinetics
Jennings, F. L. (1966) · JAMA · doi:10.1001/jama.1966.03100210113044 · Cited by 116 · see citing works
Radiation effects on male fertility
Felice, F. D., Marchetti, C., Marampon, F., Cascialli, G., Muzii, L., & Tombolini, V. (2018) · Andrology · doi:10.1111/andr.12562 · Cited by 107 · see citing works
Bacteria and the etiology of colonic cancer
Hill, M. J. (1974) · Cancer · doi:10.1002/1097-0142(197409)34:3+ · Cited by 104 · see citing works
Late radiation response of kidney assayed by tubule-cell survival
Withers, H. R., Mason, K. A., & Thames, H. D. (1986) · British Journal of Radiology · doi:10.1259/0007-1285-59-702-587 · Cited by 102 · see citing works
The Role of Intestinal Stem Cells in Epithelial Regeneration Following Radiation-Induced Gut Injury
Kim, C.-K., Yang, V. W., & Bialkowska, A. B. (2017) · Current Stem Cell Reports · doi:10.1007/s40778-017-0103-7 · Cited by 101 · see citing works
Jirtle, R. L., Michalopoulos, G. K., McLain, J. R., et al. (1981) · PubMed · Cited by 99 · see citing works
Delayed brain radiation necrosis: pathological review and new molecular targets for treatment
Furuse, M., Nonoguchi, N., Kawabata, S., Miyatake, S., & Kuroiwa, T. (2015) · Medical Molecular Morphology · doi:10.1007/s00795-015-0123-2 · Cited by 94 · see citing works
HEALTH EFFECTS IN THOSE WITH ACUTE RADIATION SICKNESS FROM THE CHERNOBYL ACCIDENT
Mettler, F. A., Guskova, A. K., & Gusev, I. A. (2007) · Health Physics · doi:10.1097/01.hp.0000278843.27969.74 · Cited by 94 · see citing works
Rodrigues-Moreira, S., Moreno, S. G., Ghinatti, G., Lewandowski, D., Hoffschir, F., Ferri, F., Gallouët, A.-S., Gay, D. L., Motohashi, H., Yamamoto, M. P., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.09.013 · Cited by 94 · see citing works
Scaramozza, A., Park, D., Kollu, S., Beerman, I., Sun, X., Rossi, D. J., Lin, C. P., Scadden, D. T., Crist, C., & Brack, A. S. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.020 · Cited by 93 · see citing works
Comparison of the Gastrointestinal Syndrome after Total-Body or Total-Abdominal Irradiation
Mason, K. A., Withers, H. R., McBride, W. H., et al. (1989) · Radiation Research · doi:10.2307/3577353 · Cited by 89 · see citing works
Self-citationChua, H. L., Plett, P. A., Sampson, C. H., Joshi, M., Tabbey, R., Katz, B. P., MacVittie, T. J., & Orschell, C. M. (2012) · Health Physics · doi:10.1097/hp.0b013e3182666d6f · Cited by 84 · see citing works
Switching roles: the functional plasticity of adult tissue stem cells
Wabik, A., & Jones, P. H. (2015) · The EMBO Journal · doi:10.15252/embj.201490386 · Cited by 81 · see citing works
Morizur, L., Chicheportiche, A., Gauthier, L., Daynac, M., Boussin, F. D., & Mouthon, M. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.06.005 · Cited by 81 · see citing works
The role of tumor necrosis factor signaling pathways in the response of murine brain to irradiation.
Daigle, J. L., Hong, J., Chiang, C., & McBride, W. H. (2001) · PubMed · Cited by 80 · see citing works
Self-citationDose-Survival Characteristics of Epithelial Cells of Mouse Intestinal Mucosa
Withers, H. R., & Elkind, M. M. (1968) · Radiology · doi:10.1148/91.5.998 · Cited by 77 · see citing works
Function and Dysfunction of Adult Hippocampal Neurogenesis in Regeneration and Disease
Peng, L., & Bonaguidi, M. A. (2017) · American Journal Of Pathology · doi:10.1016/j.ajpath.2017.09.004 · Cited by 67 · see citing works
Radiation therapy for brain tumors
Wara, W. M. (1985) · Cancer · doi:10.1002/1097-0142(19850501)55:9+ · Cited by 65 · see citing works
Purbey, P. K., Scumpia, P. O., Kim, P. J., Tong, A.-J., Iwamoto, K. S., McBride, W. H., & Smale, S. T. (2017) · Immunity · doi:10.1016/j.immuni.2017.08.017 · Cited by 65 · see citing works
Self-citationTracking cells in their native habitat: lineage tracing in epithelial neoplasia
Alcolea, M. P., & Jones, P. H. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3460 · Cited by 58 · see citing works
Granulocyte colony-stimulating factor exacerbates hematopoietic stem cell injury after irradiation
Li, C., Lu, L., Zhang, J., Huang, S. M., Xing, Y., Zhao, M., Zhou, D., Li, D., & Meng, A. (2015) · Cell & Bioscience · doi:10.1186/s13578-015-0057-3 · Cited by 55 · see citing works
Heineke, H. (1905) · Deutsche Zeitschrift für Chirurgie · doi:10.1007/bf02798721 · Cited by 52 · see citing works
Bmi1 Confers Resistance to Oxidative Stress on Hematopoietic Stem Cells
Nakamura, S., Oshima, M., Yuan, J., Saraya, A., Miyagi, S., Konuma, T., Yamazaki, S., Osawa, M., Nakauchi, H., Koseki, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036209 · Cited by 46 · see citing works
Early Human Hemogenic Endothelium Generates Primitive and Definitive Hematopoiesis In Vitro
García-Alegría, E., Menegatti, S., Fadlullah, M. Z. H., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.09.013 · Cited by 45 · see citing works
Röntgen, W. C. (1896) · Science · doi:10.1126/science.3.72.726 · Cited by 44 · see citing works
Fertility impairment in radiotherapy
Biedka, M., Kuźba-Kryszak, T., Nowikiewicz, T., et al. (2016) · Współczesna Onkologia · doi:10.5114/wo.2016.57814 · Cited by 42 · see citing works
A dose-surviving fraction curve for mouse colonic mucosa
Tucker, S. L., Withers, H. R., Mason, K. A., et al. (1983) · European Journal of Cancer and Clinical Oncology · doi:10.1016/0277-5379(83)90143-8 · Cited by 41 · see citing works
The effect of single doses of radiation on mouse spinal cord
Lo, Y., McBride, W. H., & Withers, H. R. (1992) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(92)90982-n · Cited by 40 · see citing works
Self-citationRatikan, J. A., Micewicz, E. D., Xie, M. W., & Schaue, D. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.03.031 · Cited by 37 · see citing works
Self-citationStewart, F. A., Oussoren, Y. G., van Tinteren, H., & Bentzen, S. M. (1994) · International Journal of Radiation Biology · doi:10.1080/09553009414551071 · Cited by 34 · see citing works
Implications of irradiating the subventricular zone stem cell niche
Capilla‐González, V., Bonsu, J. M., Redmond, K. J., García‐Verdugo, J. M., & Quiñones‐Hinojosa, A. (2016) · Stem Cell Research · doi:10.1016/j.scr.2016.02.031 · Cited by 34 · see citing works
Iskander, K. S., Barrios, R. J., & Jaiswal, A. K. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0766 · Cited by 32 · see citing works
Fisher, D. R., & Hendry, J. H. (1988) · Radiation Research · doi:10.2307/3577179 · Cited by 29 · see citing works
Sasine, J. P., Yeo, K. T., & Chute, J. P. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2016-0254 · Cited by 28 · see citing works
Bujko, K., Cymer, M., Adamiak, M., & Ratajczak, M. Z. (2019) · Stem Cell Reviews and Reports · doi:10.1007/s12015-019-09920-4 · Cited by 27 · see citing works
Adult stem cells as a tool for kidney regeneration
Suzuki, E. (2016) · World Journal of Nephrology · doi:10.5527/wjn.v5.i1.43 · Cited by 23 · see citing works
The Aftermath of Surviving Acute Radiation Hematopoietic Syndrome and its Mitigation
Micewicz, E. D., Iwamoto, K. S., Ratikan, J. A., Nguyen, C., Xie, M. W., Cheng, G., Boxx, G. M., Deriu, E., Damoiseaux, R. D., Whitelegge, J. P., et al. (2019) · Radiation Research · doi:10.1667/rr15231.1 · Cited by 23 · see citing works
Self-citationNrf2 regulates PU.1 expression and activity in the alveolar macrophage
Staitieh, B. S., Fan, X., Neveu, W. A., & Guidot, D. M. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00355.2014 · Cited by 22 · see citing works
Birbrair, A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-11096-3_1 · Cited by 21 · see citing works
Distinct response of adult neural stem cells to low versus high dose ionising radiation
Barazzuol, L., Hopkins, S. R., Ju, L., et al. (2019) · DNA repair · doi:10.1016/j.dnarep.2019.01.004 · Cited by 20 · see citing works
Kobayashi, T., Ohmori, T., YANAI, M., et al. (1991) · Microbiology and Immunology · doi:10.1111/j.1348-0421.1991.tb01560.x · Cited by 18 · see citing works
Epilation in mice after single and multifractionated irradiation
Vegesna, V., Withers, H. R., & Taylor, J. M. G. (1988) · Radiotherapy and Oncology · doi:10.1016/0167-8140(88)90266-6 · Cited by 17 · see citing works
4-(Nitrophenylsulfonyl)piperazines mitigate radiation damage to multiple tissues
Micewicz, E. D., Kim, K., Iwamoto, K. S., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181577 · Cited by 17 · see citing works
Über den Einfluß der Becquerelstrahlen auf die Haut
Halkin, H. (1903) · Archives of Dermatological Research · doi:10.1007/bf01826933 · Cited by 16 · see citing works
The Action of Radium upon the Formation of Blood Capillaries and Connective Tissue
Takahashi, T. (1930) · British Journal of Radiology · doi:10.1259/0007-1285-3-34-439 · Cited by 14 · see citing works
Bhat, K., Duhachek-Muggy, S., Ramanathan, R., et al. (2018) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2018.11.011 · Cited by 11 · see citing works
Studies of the Roentgen Erythema of the Human Skin
Pohle, E. A. (1926) · Radiology · doi:10.1148/6.3.236 · Cited by 10 · see citing works
Are animal models a necessity for acute radiation syndrome drug discovery?
Schaue, D., & McBride, W. H. (2019) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2019.1591364 · Cited by 6 · see citing works
Self-citationA Reaction in the Skin occurring during the Latent Period following X-Radiation
Mottram, J. C. (1933) · Nature · doi:10.1038/132317a0 · Cited by 4 · see citing works
Post-irradiation promotes susceptibility to reprogramming to pluripotent state in human fibroblasts
Lee, S. B., Han, S.-H., Kim, M., et al. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1371887 · Cited by 4 · see citing works
Supra-lethal dose—a concept never explained
Bosch, A. (1976) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(76)90134-6 · Cited by 3 · see citing works
HSC senescence upon irradiation
Geiger, H. (2014) · Blood · doi:10.1182/blood-2014-03-563718 · Cited by 2 · see citing works
Hemopoietic stem cells "age" structure revealed by the exogenous colony forming method.
Kv, G., Tsyrlova, I. G., & Va, K. (1986) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
Research works printed but not linked: 10
- [2]Heineke H. Experimentelle Untersuchungen ueber die Einwirkung der Roentgenstrahlenauf das Knochermark, nebst einiigen Bemerkungenueber die Roentgentherapie der Leukemie und Pseudoleukaemie und des Sarkoms. Deut Z Chir 1905; 78: 196– 230.
- [3]Miescher G. Das Rontgenerythem. Stralentherapie 1924; 16: 333.
- [5]Gassman A. Zur Histologie der Roentgenulcera. Fortschr Roentgenstr 1898; 2: 199– 207.
- [10]Heineke H. Uber die Einwirkung der Röntgenstrahlen auf Tiere. München med Wchnsch 1903; 1: 2090– 2092.
- [11]Heineke H. Ueber die Einwirkung der Roentgenstrahlen auf innere Organe. Münch med Wchnsch 1904; 51: 785.
- [12]Regaud C, Blanc J. Actions des rayons X sur les diverses générations de la lignée spermatique: extreme sensibilité des spermatogonies à ces rayons. Compt Rend Soc de Biol 1906; 61: 163– 165.
- [13]Bergonie J, Tribondeau L. Aspermatogenèse experimentale apres une seule exposition aux rayons X. Compt Rend Soc de Biol 1905; 58: 282– 284.
- [14]Bergonié J, Tribondeau L. Interpretation de quelques résultats de la radiotherapie et essai de fixation d'une technique rationnelle. C R Acad Sci 1906; 143: 983– 985.
- [15]Regaud C, Nogier T. Stérilization rontgenienne totale et definitive, sans radiodermite, des testicules du Belier adulte; conditions de sa réalisation. Compt Rend Soc de Biol 1911; 70: 202– 203.
- [26]Withers HR. The 4Rs of radiotherapy. Adv Radiat Biol 1975; 5: 241– 249.
Cited by
Sorted by citations
Ionizing Radiation as a Source of Oxidative Stress—The Protective Role of Melatonin and Vitamin D
Nuszkiewicz, J., Woźniak, A., & Szewczyk-Golec, K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165804 · Cited by 156 · see citing works
Normal-Tissue Tolerance to Radiopharmaceutical Therapies, the Knowns and the Unknowns
Wahl, R. L., Sgouros, G., Iravani, A., Jacene, H., Pryma, D., Saboury, B., Capala, J., & Graves, S. A. (2021) · Journal of Nuclear Medicine · doi:10.2967/jnumed.121.262751 · Cited by 95 · see citing works
- Authors
- McBride, W. H., & Schaue, D.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- McBride, William H
- Venue
- The Journal of Pathology
- Publisher
- Wiley
- Published
- 2020-02-21
- Volume
- 250
- Issue
- 5
- Pages
- 647-655
- ISSN
- 0022-3417 (ISSN-L)
- 1096-9896
- PMC
- PMC7216989
- OpenAlex
- W3003926400
- Cited by
- 155
- References
- 100
- Citations by year
- 2026: 23 · 2025: 31 · 2024: 33 · 2023: 30 · 2022: 16 · 2021: 17 · 2020: 4 · 2019: 1
- FWCI
- 2.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The Journal of Pathology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- Center for Scientific Review (1R01CA226875‐01, 5R01CA191234‐05, 5U19AI067769‐15)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Radiation Therapy and Dosimetry
- Physical Sciences › Physics and Astronomy › Radiation › Advanced Radiotherapy Techniques
- Keywords
- radiation-induced tissue damage, normal tissue response, ionizing radiation, radiosensitivity, clonogenic assay, fractionated radiotherapy, hypofractionated radiotherapy, stem cell compartment, tissue turnover, radiation quality, particle therapy, tissue plasticity
- MeSH terms
- DNA Damage, Dose-Response Relationship, Radiation, Humans, Neoplasms, Radiation Tolerance, Time Factors, Acute Radiation Syndrome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
