Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology
Abstract
Exposure of eukaryotic cells to ionizing radiation (IR) results in the immediate formation of free radicals that last a matter of milliseconds. It has been assumed that the subsequent alterations in multiple intracellular processes following irradiation is due to the initial oxidative damage caused by these free radicals. However, it is becoming increasingly clear that intracellular metabolic oxidation/reduction (redox) reactions can be affected by this initial IR-induced free radical insult and may remain perturbed for minutes, hours, or days. It would seem logical that these cellular redox reactions might contribute to the activation of protective or damaging processes that could impact upon the damaging effects of IR. These processes include redox sensitive signaling pathways, transcription factor activation, gene expression, and metabolic activities that govern the formation of intracellular oxidants and reductants. The physiological manifestations of these radiation-induced alterations in redox sensitive processes have been suggested to contribute to adaptive responses, bystander effects, cell cycle perturbations, cytotoxicity, heat-induced radiosensitization, genomic instability, inflammation, and fibrosis. While a great deal is known about the molecular changes associated with the initial production of free radicals at the time of irradiation, the contribution of perturbations in redox sensitive metabolic processes to biological outcomes following exposure to IR is only recently becoming established. This review will focus on evidence supporting the concept that perturbations in intracellular metabolic oxidation/reduction reactions contribute to the biological effects of radiation exposure as well as new concepts emerging from the field of free radical biology that may be relevant to future studies in radiobiology.
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Generation of ROS is an important mediator of cellular alterations caused by radiation exposure, including mucositis.
“The generation of ROS is also an important mediator of the cellular alterations caused by radiation exposure (Diehn et al., 2009; Sonis, 2009; Spitz et al., 2004), including mucositis (Citrin et al., 2010; Cotrim et al., 2007; Cotrim et al., 2005).”
From mTOR inhibition prevents epithelial stem cell senescence and protects from radiation-induced mucositis (2012) · cites this paper as Spitz et al., 2004
Cites
Free radicals in biology and medicine
Gutteridge, J. M. C. (1991) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(91)90478-o · Cited by 17,178 · see citing works
Oxidants, oxidative stress and the biology of ageing
Finkel, T., & Holbrook, N. J. (2000) · Nature · doi:10.1038/35041687 · Cited by 9,413 · see citing works
Aging: a theory based on free radical and radiation chemistry
Harman, D. (1956) · Journal of Gerontology · doi:10.1093/geronj/11.3.298 · Cited by 8,567 · see citing works
Schafer, F. Q., & Buettner, G. R. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00480-4 · Cited by 4,587 · see citing works
Oxidative stress: oxidants and antioxidants
Sies, H. (1997) · Experimental Physiology · doi:10.1113/expphysiol.1997.sp004024 · Cited by 4,577 · see citing works
Radiobiology for the Radiologist.
(1974) · Annals of Internal Medicine · doi:10.7326/0003-4819-80-3-438_1 · Cited by 3,498 · see citing works
Cell transformation by the superoxide-generating oxidase Mox1
Suh, Y.-A., Arnold, R. S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., Chung, A. B., Griendling, K. K., & Lambeth, J. D. (1999) · Nature · doi:10.1038/43459 · Cited by 1,480 · see citing works
REDOX REGULATION OF CELLULAR ACTIVATION
Nakamura, H., Nakamura, K., & Yodoi, J. (1997) · Annual Review of Immunology · doi:10.1146/annurev.immunol.15.1.351 · Cited by 1,106 · see citing works
Oxygen poisoning and x-irradiation: a mechanism in common
Gerschman, R., Gilbert, D. L., Nye, S. W., Dwyer, P., & Fenn, W. O. (1954) · Science · doi:10.1126/science.119.3097.623 · Cited by 961 · see citing works
Wong, G. H. W., Elwell, J. H., Oberley, L. W., & Goeddel, D. V. (1989) · Cell · doi:10.1016/0092-8674(89)90944-6 · Cited by 802 · see citing works
Radiobiology for the Radiologist
Fowler, J., & Hall, E. J. (1988) · Radiation Research · doi:10.2307/3577489 · Cited by 786 · see citing works
Does oxidative damage to DNA increase with age?
Hamilton, M. L., Van Remmen, H., Drake, J. A., Yang, H., Guo, Z. M., Kewitt, K., Walter, C. A., & Richardson, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171202698 · Cited by 768 · see citing works
Keilin's Respiratory Chain Concept and Its Chemiosmotic Consequences
Mitchell, P. (1979) · Science · doi:10.1126/science.388618 · Cited by 738 · see citing works
Redox regulation of transcriptional activators
Sun, Y., & Oberley, L. W. (1996) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(96)00109-8 · Cited by 692 · see citing works
The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases
Cai, H., Griendling, K. K., & Harrison, D. G. (2003) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(03)00233-5 · Cited by 687 · see citing works
Nitric oxide as a unique signaling molecule in the vascular system: a historical overview.
Ignarro, L. J. (2002) · PubMed · Cited by 623 · see citing works
Chemical basis of inflammation-induced carcinogenesis
Ohshima, H., Tatemichi, M., & Sawa, T. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(03)00283-2 · Cited by 618 · see citing works
MAPK pathways in radiation responses
Dent, P., Yacoub, A., Fisher, P. B., Hagan, M. P., & Grant, S. (2003) · Oncogene · doi:10.1038/sj.onc.1206701 · Cited by 603 · see citing works
Mikkelsen, R. B., & Wardman, P. (2003) · Oncogene · doi:10.1038/sj.onc.1206663 · Cited by 591 · see citing works
Ueda, S., Masutani, H., Nakamura, H., Tanaka, T., Ueno, M., & Yodoi, J. (2002) · Antioxidants and Redox Signaling · doi:10.1089/15230860260196209 · Cited by 581 · see citing works
Function and Structure of Complex II of the Respiratory Chain
Cecchini, G. (2003) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.72.121801.161700 · Cited by 556 · see citing works
Morgan, W. F. (2003) · Radiation Research · doi:10.1667/0033-7587(2003)159[0581:nadeoe]2.0.co;2 · Cited by 533 · see citing works
Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen.
Leach, J. K., Tuyle, G. V., Lin, P.-S., Schmidt‐Ullrich, R., & Mikkelsen, R. B. (2001) · PubMed · Cited by 511 · see citing works
Claiborne, A., Yeh, J. I., Mallett, T. C., Luba, J. P., Crane, E. J., Charrier, V., & Parsonage, D. (1999) · Biochemistry · doi:10.1021/bi992025k · Cited by 500 · see citing works
A Tutorial on the Diffusibility and Reactivity of Free Nitric Oxide
Lancaster, J. R. (1997) · Nitric Oxide · doi:10.1006/niox.1996.0112 · Cited by 495 · see citing works
Targeted cytoplasmic irradiation with alpha particles induces mutations in mammalian cells
Wu, L., Randers-Pehrson, G., Xu, A., Waldren, C. A., Geard, C. R., Yu, Z., & Hei, T. K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.4959 · Cited by 444 · see citing works
Mitochondrial Production of Superoxide Radical and Hydrogen Peroxide
Boveris, A. (1977) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-9035-4_5 · Cited by 427 · see citing works
Sorescu, D., & Griendling, K. K. (2002) · Congestive Heart Failure · doi:10.1111/j.1527-5299.2002.00717.x · Cited by 403 · see citing works
NADPH oxidases: not just for leukocytes anymore!
Bokoch, G., & Knaus, U. G. (2003) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(03)00194-4 · Cited by 383 · see citing works
Cellular Regulation by Hydrogen Peroxide
Rhee, S. G., Chang, T.-S., Bae, Y. S., Lee, S.-R., & Kang, S. W. (2003) · Journal of the American Society of Nephrology · doi:10.1097/01.asn.0000077404.45564.7e · Cited by 348 · see citing works
The adaptive response in radiobiology: evolving insights and implications.
Wolff, S. (1998) · Environmental Health Perspectives · doi:10.1289/ehp.98106s1277 · Cited by 341 · see citing works
Spitz, D. R., Sim, J. E., Ridnour, L. A., Galoforo, S., & Lee, Y. J. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06199.x · Cited by 331 · see citing works
Azzam, E. I., Toledo, S. M. D., Spitz, D. R., & Little, J. B. (2002) · PubMed · Cited by 328 · see citing works
Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect
Azzam, E. I., de Toledo, S. M., & Little, J. B. (2003) · Oncogene · doi:10.1038/sj.onc.1206961 · Cited by 324 · see citing works
Redox Potential of Human Thioredoxin 1 and Identification of a Second Dithiol/Disulfide Motif
Watson, W. H., Pohl, J., Montfort, W. R., Stuchlik, O., Reed, M. S., Powis, G., & Jones, D. P. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211107200 · Cited by 293 · see citing works
Shadley, J. D., Afzal, V., & Wolff, S. M. (1987) · Radiation Research · doi:10.2307/3576936 · Cited by 271 · see citing works
Manganese Superoxide Dismutase-Mediated Gene Expression in Radiation-Induced Adaptive Responses
Guo, G., Yan-Sanders, Y., Lyn‐Cook, B. D., Wang, T., Tamae, D., Ogi, J., Khaletskiy, A., Li, Z., Weydert, C. J. D., Longmate, J., et al. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.7.2362-2378.2003 · Cited by 270 · see citing works
Gonzalez‐Zulueta, M., Ensz, L. M., Mukhina, G. L., Lebovitz, R. M., Zwacka, R. M., Engelhardt, J. F., Oberley, L. W., Dawson, V. L., & Dawson, T. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02040.1998 · Cited by 265 · see citing works
H2O2-induced O⨪2Production by a Non-phagocytic NAD(P)H Oxidase Causes Oxidant Injury
Li, W. G., Miller, F. J., Zhang, H. J., Spitz, D. R., Oberley, L. W., & Weintraub, N. L. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m102124200 · Cited by 265 · see citing works
Role of Glutaredoxin in Metabolic Oxidative Stress
Song, J. J., Rhee, J. G., Suntharalingam, M., Walsh, S. A., Spitz, D. R., & Lee, Y. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206826200 · Cited by 260 · see citing works
Clutton, S. M., Townsend, K. M. S., Walker, C., Ansell, J., & Wright, E. G. (1996) · Carcinogenesis · doi:10.1093/carcin/17.8.1633 · Cited by 259 · see citing works
The Role of Thiols in Cellular Response to Radiation and Drugs
Biaglow, J. E., Varnes, M. E., Clark, E. P., & Epp, E. R. (1983) · Radiation Research · doi:10.2307/3576092 · Cited by 255 · see citing works
Delanian, S. E., Baillet, F., Huart, J., Lefaix, J.-L., Maulard, C., & Housset, M. (1994) · Radiotherapy and Oncology · doi:10.1016/0167-8140(94)90444-8 · Cited by 229 · see citing works
Oxygen toxicity and reactive oxygen metabolites in mammals
Jamieson, D. (1989) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(89)90103-2 · Cited by 227 · see citing works
Lee, Y. J., Galoforo, S., Berns, C. M., Chen, J. C., Davis, B. H., Sim, J. E., Corry, P. M., & Spitz, D. R. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.9.5294 · Cited by 225 · see citing works
Redox regulation of the G1 to S phase transition in the mouse embryo fibroblast cell cycle.
Menon, S. G., Sarsour, E. H., Spitz, D. R., Higashikubo, R., Sturm, M. T., Zhang, H., & Goswami, P. C. (2003) · PubMed · Cited by 218 · see citing works
Spitz, D. R., Dewey, W. C., & Li, G. C. (1987) · Journal of Cellular Physiology · doi:10.1002/jcp.1041310308 · Cited by 216 · see citing works
Mitochondrial Aging: Open Questionsa
Beckman, K. B., & Ames, B. N. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09897.x · Cited by 211 · see citing works
Sj, W., Botero, A. C., Hirota, K., Cm, B., Markovina, S. S., Laszlo, A., Spitz, D. R., Goswami, P. C., Yodoi, J., & Gius, D. R. (2000) · PubMed · Cited by 201 · see citing works
Vujašković, Ž., Batinic̈‐Haberle, I., Rabbani, Z. N., Feng, Q.-F., Kang, S. K., Spasojević, I., Samulski, T. V., Fridovich, I., Dewhirst, M. W., & Anscher, M. S. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00980-2 · Cited by 192 · see citing works
Lu, C.-Y., Lee, H.-C., Fahn, H.-J., & Wei, Y.-H. (1999) · Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis · doi:10.1016/s0027-5107(98)00220-6 · Cited by 186 · see citing works
The role of glutathione in radiation and drug induced cytotoxicity.
Mitchell, J. B., & Russo, A. (1987) · PubMed · Cited by 185 · see citing works
Zinc Binding and Redox Control of p53 Structure and Function
Hainaut, P. L., & Mann, K. (2001) · Antioxidants and Redox Signaling · doi:10.1089/15230860152542961 · Cited by 183 · see citing works
Persistent oxidative stress in chromosomally unstable cells.
Limoli, C. L., Giedzinski, E., Morgan, W. F., Swarts, S. G., Jones, G. D. D., & Hyun, W. C. (2003) · PubMed · Cited by 168 · see citing works
Increase in manganese superoxide dismutase activity in the mouse heart after X-irradiation
Oberley, L. W., Clair, D. K. S., Autor, A. P., & Oberley, T. D. (1987) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(87)90082-8 · Cited by 168 · see citing works
Blackburn, R. V., Spitz, D. R., Liu, X. Z., Galoforo, S., Sim, J. E., Ridnour, L. A., Chen, J. C., Davis, B. H., Corry, P. M., & Lee, Y. J. (1999) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00217-2 · Cited by 158 · see citing works
Successful treatment of radiation-induced fibrosis using and Mn-SOD: An experimental study
Lefaix, J.-L., Delanian, S. E., Leplat, J. J. J. J., Tricaud, Y., Martin, M. T., Nimrod, A., Baillet, F., & Daburon, F. (1996) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(96)00061-2 · Cited by 153 · see citing works
Genomic instability and catalase gene amplification induced by chronic exposure to oxidative stress.
Hunt, C. R., Sim, J. E., Sullivan, S. J., Featherstone, T., Golden, W. L., Kapp-Herr, C. V., Hock, R. A., Gomez, R. A., Parsian, A., & Spitz, D. R. (1998) · PubMed · Cited by 151 · see citing works
SELECT: the selenium and vitamin E cancer prevention trial
Klein, E. A., Thompson, I. M., Lippman, S. M., Goodman, P. J., Albanes, D., Taylor, P. R., & Coltman, C. A. (2003) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/s1078-1439(02)00301-0 · Cited by 151 · see citing works
Clair, D. K. S., Wan, X. S., Oberley, T. D., Muse, K. E., & Clair, W. H. S. (1992) · Molecular Carcinogenesis · doi:10.1002/mc.2940060404 · Cited by 145 · see citing works
Oxidation of Zinc Finger Transcription Factors: Physiological Consequences
Webster, K. A., Prentice, H. M., & Bishopric, N. (2001) · Antioxidants and Redox Signaling · doi:10.1089/15230860152542916 · Cited by 145 · see citing works
Milgram, N. W., Head, E., Muggenburg, B. A., Holowachuk, D., Murphey, H. L., Estrada, J., Ikeda-Douglas, C. J., Zicker, S. C., & Cotman, C. W. (2002) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(02)00039-8 · Cited by 145 · see citing works
Claiborne, A., Mallett, T. C., Yeh, J. I., Luba, J. P., & Parsonage, D. (2001) · Advances in protein chemistry · doi:10.1016/s0065-3233(01)58006-7 · Cited by 139 · see citing works
Cell division in normal and transformed cells: The possible role of superoxide and hydrogen peroxide
Oberley, L. W., Oberley, T. D., & Buettner, G. R. (1981) · Medical Hypotheses · doi:10.1016/0306-9877(81)90018-9 · Cited by 138 · see citing works
Kang, S. K., Rabbani, Z. N., Folz, R. J., Golson, M. L., Huang, H., Yu, D., Samulski, T. V., Dewhirst, M. W., Anscher, M. S., & Vujašković, Ž. (2003) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(03)01369-5 · Cited by 133 · see citing works
Leach, J. K., Black, S. M., Schmidt‐Ullrich, R., & Mikkelsen, R. B. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110309200 · Cited by 133 · see citing works
Borek, C., & Troll, W. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.5.1304 · Cited by 123 · see citing works
Anticancer Therapy by Overexpression of Superoxide Dismutase
Oberley, L. W. (2001) · Antioxidants and Redox Signaling · doi:10.1089/15230860152409095 · Cited by 120 · see citing works
Karimpour, S., Lou, J., Lin, L. L., Rene, L. M., Lagunas, L., Ma, X., Karra, S., Bradbury, C. M., Markovina, S. S., Goswami, P. C., et al. (2002) · Oncogene · doi:10.1038/sj.onc.1205749 · Cited by 117 · see citing works
Identification of radiation-specific responses from gene expression profile
Park, W.-Y., Hwang, C.-I., Im, C.-N., Kang, M.-J., Woo, J.-H., Kim, J.-H., Kim, Y. S., Kim, J.-H., Kim, H., Kim, K.-A., et al. (2002) · Oncogene · doi:10.1038/sj.onc.1205977 · Cited by 113 · see citing works
Epperly, M. W., Epstein, C. J., Travis, E. L., & Greenberger, J. S. (2000) · Radiation Research · doi:10.1667/0033-7587(2000)154[0365:dprrom]2.0.co;2 · Cited by 93 · see citing works
Nonprotein Thiols and the Radiation Response of A549 Human Lung Carcinoma Cells
Biaglow, J. E., Clark, E. P., Epp, E. R., Morse-Guadio, M., Varnes, M. E., & Mitchell, J. B. (1983) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553008314551491 · Cited by 92 · see citing works
Superoxide lon as the cause of the oxygen effect.
Oberley, L. W., Lindgren, L. A., Baker, S. A., & Stevens, R. H. (1976) · PubMed · Cited by 89 · see citing works
Oxidative stress in ataxia telangiectasia
Watters, D. J. (2003) · Redox Report · doi:10.1179/135100003125001206 · Cited by 87 · see citing works
Greenberger, J. S., Epperly, M. W., Gretton, J. E., Jefferson, M., Nie, S., Bernarding, M., Kagan, V. E., & Guo, H. (2003) · Current Gene Therapy · doi:10.2174/1566523034578384 · Cited by 87 · see citing works
Szent‐Györgyi, A. (1977) · Elsevier eBooks · doi:10.1016/b978-0-12-395150-2.50031-3 · Cited by 84 · see citing works
Weichselbaum, R. R., Kufe, D. W., Hellmän, S., Rasmussen, H. S., King, C. R., Fischer, P. H., & Mauceri, H. J. (2002) · The Lancet Oncology · doi:10.1016/s1470-2045(02)00900-2 · Cited by 82 · see citing works
Protection of Post-irradiated Mice by Superoxide Dismutase
Petkau, A., Chelack, W. S., & Pleskach, S. D. (1976) · International Journal of Radiation Biology and Related Studies in Physics Chemistry and Medicine · doi:10.1080/09553007614550341 · Cited by 78 · see citing works
Zhao, W., Spitz, D. R., Oberley, L. W., & Robbins, M. E. C. (2001) · PubMed · Cited by 74 · see citing works
The importance of peroxide and superoxide in the X-ray response
Biaglow, J. E., Mitchell, J. B., & Held, K. (1992) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(92)90499-8 · Cited by 72 · see citing works
Oxidation of Zinc-Binding Cysteine Residues in Transcription Factor Proteins
Wilcox, D. E., Schenk, A. D., Feldman, B. M., & Xu, Y. F. (2001) · Antioxidants and Redox Signaling · doi:10.1089/15230860152542925 · Cited by 71 · see citing works
Zinc Finger Proteins as Molecular Targets for Nitric Oxide-Mediated Gene Regulation
Kröncke, K. (2001) · Antioxidants and Redox Signaling · doi:10.1089/15230860152542934 · Cited by 71 · see citing works
Tuttle, S. W., Varnes, M. E., Mitchell, J. B., & Biaglow, J. E. (1992) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/0360-3016(92)90500-h · Cited by 70 · see citing works
Cell Cycle-coupled Variation in Topoisomerase IIα mRNA Is Regulated by the 3′-Untranslated Region
Goswami, P. C., Sheren, J. E., Albee, L. D., Parsian, A. J., Sim, J. E., Ridnour, L. A., Higashikubo, R., Gius, D. R., Hunt, C. R., & Spitz, D. R. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005298200 · Cited by 70 · see citing works
Superoxide Ion as the Cause of the Oxygen Effect
Oberley, L. W., Lindgren, A. L., Baker, S. A., & Stevens, R. H. (1976) · Radiation Research · doi:10.2307/3574483 · Cited by 68 · see citing works
Superoxide-mediated clastogenesis and anticlastogenic effects of exogenous superoxide dismutase
Emerit, I., Garban, F., Vassy, J., Levy, A., Filipe, P., & Freitas, J. P. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.23.12799 · Cited by 67 · see citing works
Heinloth, A. N., Shackelford, R. E., Innes, C. L., Bennett, L., Li, L., Amin, R. P., Sieber, S. O., Flores, K. G., Bushel, P. R., & Paules, R. S. (2003) · Radiation Research · doi:10.1667/rr3047 · Cited by 62 · see citing works
Kim, S. G., Nam, S. Y., Kim, C. W., Kim, J. H., Cho, C. K., & Yoo, S. Y. (1997) · Molecular Pharmacology · doi:10.1124/mol.51.2.225 · Cited by 53 · see citing works
Arena, V. (1971) · Cited by 51 · see citing works
Ayene, I. S., Stamato, T. D., Mauldin, S. K., Biaglow, J. E., Tuttle, S. W., Jenkins, S. F., & Koch, C. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111366200 · Cited by 49 · see citing works
Bulger, E. M., & Maier, R. V. (2003) · Shock · doi:10.1097/00024382-200302000-00001 · Cited by 49 · see citing works
Copper ion-mediated sensitization of nuclear matrix attachment sites to ionizing radiation
Chiu, S.-M., Xue, L., Friedman, L. R., & Oleinick, N. L. (1993) · Biochemistry · doi:10.1021/bi00075a014 · Cited by 41 · see citing works
Protective Role of Glutathione Synthesis on Radiation-Induced DNA Damage in Rabbit Brain
Shimizu, T., Iwanaga, M., Yasunaga, A., Urata, Y., Goto, S., Shibata, S., & Kondo, T. (1998) · Cellular and Molecular Neurobiology · doi:10.1023/a:1022525214871 · Cited by 37 · see citing works
Irradiation increases superoxide dismutase in rat intestinal smooth muscle
Summers, R. W., Maves, B. V., Reeves, R. D., ARJES, L., & Oberley, L. W. (1989) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(89)90053-1 · Cited by 34 · see citing works
Antioxidant Vitamins E and C and Risk of Alzheimer's Disease
Martin-Marco, A. (2003) · Nutrition Reviews · doi:10.1301/nr.2003.febr.69-73 · Cited by 32 · see citing works
Lee, Y. J., Galoforo, S., Sim, J. E., Ridnour, L. A., Choi, J., Forman, H. J., Corry, P. M., & Spitz, D. R. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(99)00267-1 · Cited by 32 · see citing works
A stable O2-resistant cell line: role of lipid peroxidation byproducts in O2-mediated injury
Sullivan, S. J., Oberley, T. D., Roberts, R. J., & Spitz, D. R. (1992) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.1992.262.6.l748 · Cited by 29 · see citing works
Xu, Y., Greenstock, C. L., Trivedi, A., & Mitchel, R. E. J. (1996) · Radiation and Environmental Biophysics · doi:10.1007/bf02434030 · Cited by 28 · see citing works
Bradbury, C. M., Locke, J., Wei, S. J., Rene, L. M., Karimpour, S., Hunt, C. R., Spitz, D. R., & Gius, D. R. (2001) · PubMed · Cited by 27 · see citing works
Sullivan, S. J., Roberts, R. J., & Spitz, D. R. (1991) · Journal of Cellular Physiology · doi:10.1002/jcp.1041470307 · Cited by 24 · see citing works
Waldren, C. A. (1999) · Human & Experimental Toxicology · doi:10.1191/096032799678840363 · Cited by 19 · see citing works
Varnes, M. E. (1988) · PubMed · Cited by 16 · see citing works
Tribble, D. L., Krauss, R. M., Chu, B. M., Gong, E. L., Kullgren, B., Nagy, J. O., & Belle, M. L. (2000) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)32000-9 · Cited by 13 · see citing works
Xiao, J., Biaglow, J. E., Chae-Park, H.-J., Jin, J., Tuel-ahlgren, L., Myers, D. E., Burkhardt, A. L., Bolen, J. B., & Uckun, F. M. (1996) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428199609054780 · Cited by 10 · see citing works
Lee, A. K., Cho, C. K., Kim, M., & Kim, S. G. (2000) · PubMed · Cited by 1 · see citing works
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Sharifi-Rad, M., Anil Kumar, N. V., Zucca, P., Varoni, E. M., Dini, L., Panzarini, E., Rajkovic, J., Tsouh Fokou, P. V., Azzini, E., Peluso, I., et al. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00694 · Cited by 1,971 · see citing works
Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury
Azzam, E. I., Jay‐Gerin, J., & Pain, D. (2011) · Cancer Letters · doi:10.1016/j.canlet.2011.12.012 · Cited by 1,611 · see citing works
Lang, X., Green, M. D., Wang, W., Yu, J., Choi, J. E., Jiang, L., Liao, P., Zhou, J., Zhang, Q., Dow, A., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0338 · Cited by 1,066 · see citing works
Kim, H.-S., Patel, K., Muldoon-Jacobs, K., Bisht, K. S., Aykin-Burns, N., Pennington, J. D., van der Meer, R., Nguyen, P., Savage, J., Owens, K. M., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.11.023 · Cited by 785 · see citing works
Self-citationDash, U. C., Bhol, N. K., Swain, S. K., Samal, R. R., Nayak, P. K., Raina, V., Panda, S. K., Kerry, R. G., Duttaroy, A. K., & Jena, A. B. (2024) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2024.10.004 · Cited by 726 · see citing works
Combination strategies to maximize the benefits of cancer immunotherapy
Zhu, S., Zhang, T., Zheng, L., Liu, H., Song, W., Liu, D., Li, Z., & Pan, C.-X. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01164-5 · Cited by 654 · see citing works
Oxidative Stress and Pathogenesis of Inflammatory Bowel Disease: An Epiphenomenon or the Cause?
Rezaie, A. R., Parker, R. D., & Abdollahi, M. R. (2007) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9622-2 · Cited by 589 · see citing works
Lee, S. Y., Jeong, E. K., Ju, M. K., Jeon, H. M., Kim, M. Y., Kim, C. H., Park, H. G., Han, S. I., & Kang, H. S. (2017) · Molecular Cancer · doi:10.1186/s12943-016-0577-4 · Cited by 579 · see citing works
The Many Functions of APE1/Ref-1: Not Only a DNA Repair Enzyme
Tell, G., Quadrifoglio, F., Tiribelli, C., & Kelley, M. R. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2194 · Cited by 515 · see citing works
The Linear No-Threshold Relationship Is Inconsistent with Radiation Biologic and Experimental Data
Tubiana, M., Feinendegen, L. E., Yang, C., & Kaminski, J. (2009) · Radiology · doi:10.1148/radiol.2511080671 · Cited by 507 · see citing works
Fundamental Biological Features of Spaceflight: Advancing the Field to Enable Deep-Space Exploration
Afshinnekoo, E., Scott, R. T., MacKay, M. J., Pariset, E., Cekanaviciute, E., Barker, R. J., Gilroy, S., Hassane, D. C., Smith, S. M., Zwart, S. R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.10.050 · Cited by 484 · see citing works
Roles of Reactive Oxygen Species and Antioxidants in Ovarian Toxicity1
Devine, P. J., Perreault, S. D., & Luderer, U. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.095224 · Cited by 422 · see citing works
Reactive Oxygen Species in Normal and Tumor Stem Cells
Zhou, D.-H., Shao, L.-J., & Spitz, D. (2014) · Advances in Cancer Research · doi:10.1016/b978-0-12-420117-0.00001-3 · Cited by 323 · see citing works
Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR‐A radiation
Karu, T. I. (2010) · IUBMB Life · doi:10.1002/iub.359 · Cited by 394 · see citing works
Effects of ionizing radiation on mitochondria
Kam, W. W.-Y., & Banati, R. B. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.024 · Cited by 386 · see citing works
Colon, J. F., Hsieh, N., Ferguson, A., Kupelian, P., Seal, S., Jenkins, D. W., & Baker, C. H. (2010) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2010.01.010 · Cited by 381 · see citing works
Estresse oxidativo: conceito, implicações e fatores modulatórios
Barbosa, K. B. F., Costa, N. M. B., Alfenas, R. D. C. G., de Paula, S. O., Minim, V. P. R., & Bressan, J. (2010) · Revista de Nutrição · doi:10.1590/s1415-52732010000400013 · Cited by 357 · see citing works
DNA damage foci: Meaning and significance
Rothkamm, K., Barnard, S. G. R., Moquet, J., Ellender, M., Rana, Z., & Burdak‐Rothkamm, S. (2015) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21944 · Cited by 335 · see citing works
Spitz, D. R., Buettner, G. R., Petronek, M. S., St‐Aubin, J., Flynn, R. T., Waldron, T. J., & Limoli, C. L. (2019) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2019.03.028 · Cited by 310 · see citing works
Iglesias-Bartolome, R., Patel, V., Cotrim, A., Leelahavanichkul, K., Molinolo, A. A., Mitchell, J. B., & Gutkind, J. S. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.06.007 · Cited by 284 · see citing works
Redox regulation in stem-like cancer cells by CD44 variant isoforms
Nagano, O., Okazaki, S., & Saya, H. (2013) · Oncogene · doi:10.1038/onc.2012.638 · Cited by 279 · see citing works
Zinc oxide nanoparticles induce apoptosis and autophagy in human ovarian cancer cells
Bai, D.-P., Zhang, X., Zhang, G., Huang, Y.-F., & Gurunathan, S. (2017) · International Journal of Nanomedicine · doi:10.2147/ijn.s140071 · Cited by 280 · see citing works
Wang, Y., Liu, L., Pazhanisamy, S. K., Li, H., Meng, A., & Zhou, D. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.11.005 · Cited by 273 · see citing works
Cyclin B1/CDK1-regulated mitochondrial bioenergetics in cell cycle progression and tumor resistance
Xie, B., Wang, S., Jiang, N., & Li, J. J. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.11.019 · Cited by 262 · see citing works
Liu, Y., Wang, X., He, D., & Cheng, Y. (2020) · Phytomedicine · doi:10.1016/j.phymed.2020.153402 · Cited by 263 · see citing works
Cancer stem cells and radioresistance
Rycaj, K., & Tang, D. G. (2014) · International Journal of Radiation Biology · doi:10.3109/09553002.2014.892227 · Cited by 255 · see citing works
Wild-type and mutated IDH1/2 enzymes and therapy responses
Molenaar, R. J., Maciejewski, J. P., Wilmink, J. W., & Noorden, C. J. F. V. (2018) · Oncogene · doi:10.1038/s41388-017-0077-z · Cited by 243 · see citing works
Role of Mitochondria in Radiation Responses: Epigenetic, Metabolic, and Signaling Impacts
Averbeck, D., & Rodriguez‐Lafrasse, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011047 · Cited by 242 · see citing works
Radiation-Induced Normal Tissue Damage: Oxidative Stress and Epigenetic Mechanisms
Wei, J., Wang, B., Wang, H., Meng, L., Zhao, Q., Li, X., Xin, Y., & Jiang, X. M. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/3010342 · Cited by 211 · see citing works
Zhang, H., Zhai, Z., Wang, Y., Zhang, J., Wu, H., Wang, Y., Li, C., Li, D., Lu, L., Wang, X., et al. (2012) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.10.530 · Cited by 207 · see citing works
Vallée, A., Lecarpentier, Y., Guillevin, R., & Vallée, J.-N. (2017) · Oncotarget · doi:10.18632/oncotarget.21234 · Cited by 203 · see citing works
Tao, R., Vassilopoulos, A., Parisiadou, L., Yan, Y., & Gius, D. (2014) · Antioxidants & Redox Signaling · doi:10.1089/ars.2013.5482 · Cited by 194 · see citing works
Oxidative damage pathways in relation to normal tissue injury
Zhao, W., Diz, D. I., & Robbins, M. E. C. (2007) · British Journal of Radiology · doi:10.1259/bjr/18237646 · Cited by 201 · see citing works
Haigis, M. C., Deng, C., Finley, L. W. S., Kim, H., & Gius, D. R. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3633 · Cited by 196 · see citing works
Holo-lactoferrin: the link between ferroptosis and radiotherapy in triple-negative breast cancer
Zhang, Z., Lu, M., Chen, C., Tong, X., Li, Y., Yang, K., Lv, H., Xu, J., & Qin, L. (2021) · Theranostics · doi:10.7150/thno.52028 · Cited by 194 · see citing works
The Epidermal Growth Factor Receptor: A Role in Repair of Radiation-Induced DNA Damage
Chen, D. J., & Nirodi, C. S. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-1610 · Cited by 192 · see citing works
DNA oxidation: Investigating its key role in environmental mutagenesis with the comet assay
Azqueta, A., Shaposhnikov, S. A., & Collins, A. R. (2008) · Mutation Research/Genetic Toxicology and Environmental Mutagenesis · doi:10.1016/j.mrgentox.2008.10.013 · Cited by 191 · see citing works
Redox Signaling in Cancer Biology
Gius, D. R., & Spitz, D. R. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2006.8.1249 · Cited by 189 · see citing works
Slane, B. G., Aykin‐Burns, N., Smith, B. J., Kalen, A. L., Goswami, P. C., Domann, F. E., & Spitz, D. R. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0833 · Cited by 188 · see citing works
Yoshida, T., Goto, S., Kawakatsu, M., Urata, Y., & Li, T. (2011) · Free Radical Research · doi:10.3109/10715762.2011.645207 · Cited by 185 · see citing works
J.Kim, G., Chandrasekaran, K., & Morgan, W. F. (2006) · Mutagenesis · doi:10.1093/mutage/gel048 · Cited by 181 · see citing works
Antioxidant Intake and Antitumor Therapy: Toward Nutritional Recommendations for Optimal Results
Mut‐Salud, N., Alvarez, P. J., Garrido, J. M., Carrasco, E., Aránega, A., & Rodríguez‐Serrano, F. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/6719534 · Cited by 180 · see citing works
Radioprotection in Normal Tissue and Delayed Tumor Growth by Blockade of CD47 Signaling
Maxhimer, J. B., Soto‐Pantoja, D. R., Ridnour, L. A., Shih, H. B., DeGraff, W., Tsokos, M., Wink, D. A., Isenberg, J. S., & Roberts, D. D. (2009) · Science Translational Medicine · doi:10.1126/scitranslmed.3000139 · Cited by 176 · see citing works
Radiation-induced skin injury: pathogenesis, treatment, and management
Yang, X., Ren, H., Guo, X., Hu, C., & Jie, F. (2020) · Aging · doi:10.18632/aging.103932 · Cited by 172 · see citing works
Luo, M., Delaplane, S., Jiang, A., Reed, A. M., He, Y., Fishel, M. L., Nyland, R. L., Borch, R. F., Qiao, X., Georgiadis, M. M., et al. (2008) · Antioxidants and Redox Signaling · doi:10.1089/ars.2008.2120 · Cited by 167 · see citing works
Barjaktarović, Ž., Schmaltz, D., Shyla, A., Azimzadeh, O., Schulz, S., Haagen, J., Dörr, W., Sarioglu, H., Schäfer, A., Atkinson, M. J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027811 · Cited by 163 · see citing works
NF-κB-MediatedHER2Overexpression inRadiation-Adaptive Resistance
Cao, N., Li, S., Wang, Z., Ahmed, K. M., Degnan, M. E., Fan, M., Dynlacht, J. R., & Li, J. J. (2008) · Radiation Research · doi:10.1667/rr1472.1 · Cited by 162 · see citing works
Hydrogen therapy attenuates irradiation-induced lung damage by reducing oxidative stress
Terasaki, Y., Ohsawa, I., Terasaki, M., Takahashi, M., Kunugi, S., Kang, D., Urushiyama, H., Amenomori, S., Kaneko-Togashi, M., Kuwahara, N., et al. (2011) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00008.2011 · Cited by 162 · see citing works
Dauer, L. T., Brooks, A. L., Hoel, D. G., Morgan, W. F., Stram, D. O., & Tran, P. (2010) · Radiation Protection Dosimetry · doi:10.1093/rpd/ncq141 · Cited by 160 · see citing works
Buonanno, M., de Toledo, S. M., Pain, D., & Azzam, E. I. (2011) · Radiation Research · doi:10.1667/rr2461.1 · Cited by 159 · see citing works
A Role for Mitochondrial Dysfunction in Perpetuating Radiation-Induced Genomic Instability
Kim, G. J., Fiskum, G. M., & Morgan, W. F. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3036 · Cited by 158 · see citing works
Redox Control of the Survival of Healthy and Diseased Cells
Zhang, Y., Du, Y., Le, W., Wang, K., Kieffer, N., & Zhang, J. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3685 · Cited by 156 · see citing works
Zahra, A., Fath, M. A., Opat, E., Mapuskar, K. A., Bhatia, S. K., Ma, D. C., Rodman, S. N., Snyders, T. P., Chenard, C. A., Eichenberger‐Gilmore, J. M., et al. (2017) · Radiation Research · doi:10.1667/rr14668.1 · Cited by 151 · see citing works
Jin, M., Fang, J., Peng, J., Wang, X., Xing, P., Jia, K., Hu, J., Wang, D., Ding, Y., Wang, X., et al. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02176-8 · Cited by 156 · see citing works
Redox Paradox: A Novel Approach to Therapeutics-Resistant Cancer
Chaiswing, L., Clair, W. H. S., & Clair, D. K. S. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7485 · Cited by 147 · see citing works
Yahyapour, R., Motevaseli, E., Rezaeyan, A., Abdollahi, H., Farhood, B., Cheki, M., Rezapoor, S., Shabeeb, D., Musa, A. E., Najafi, M., et al. (2018) · Clinical & Translational Oncology · doi:10.1007/s12094-017-1828-6 · Cited by 142 · see citing works
Oxidative stress biomarkers in patients with endometriosis: systematic review
Carvalho, L. F. P., Samadder, A. N., Agarwal, A., Fernandes, L. F. C., & Abrão, M. S. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2439-7 · Cited by 140 · see citing works
Ionizing radiation, antioxidant response and oxidative damage: A meta-analysis
Einor, D., Bonisoli‐Alquati, A., Costantini, D., Mousseau, T. A., & Møller, A. P. (2016) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2016.01.027 · Cited by 138 · see citing works
Ovarian Toxicity from Reactive Oxygen Species
Luderer, U. (2014) · Vitamins and hormones · doi:10.1016/b978-0-12-800095-3.00004-3 · Cited by 136 · see citing works
Issues in Low Dose Radiation Biology: The Controversy Continues. A Perspective
Morgan, W. F., & Bair, W. J. (2013) · Radiation Research · doi:10.1667/rr3306.1 · Cited by 130 · see citing works
Reproductive hazards of space travel in women and men
Mishra, B., & Luderer, U. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0267-6 · Cited by 129 · see citing works
Metformin ameliorates ionizing irradiation-induced long-term hematopoietic stem cell injury in mice
Xu, G., Wu, H., Zhang, J., Li, D., Wang, Y., Wang, Y., Zhang, H., Lu, L., Li, C., Huang, S. M., et al. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.05.045 · Cited by 127 · see citing works
P‐glycoprotein: So Many Ways to Turn It On
Callaghan, R., Crowley, E. H., Biochem, M., Potter, S., & Kerr, I. D. (2007) · The Journal of Clinical Pharmacology · doi:10.1177/0091270007311568 · Cited by 123 · see citing works
Mitochondrial DNA : more than an evolutionary bystander
Ballard, J. W. O., & Pichaud, N. (2013) · Functional Ecology · doi:10.1111/1365-2435.12177 · Cited by 123 · see citing works
Harrison, J. F. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki759 · Cited by 120 · see citing works
Bauer, G. (2007) · International Journal of Radiation Biology · doi:10.1080/09553000701727523 · Cited by 120 · see citing works
Boehm, F., Edge, R., & Truscott, T. G. (2012) · Research Explorer (The University of Manchester) · doi:10.1002/mnfr.201100222 · Cited by 115 · see citing works
Morgan, W. F., & Sowa, M. B. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.09.009 · Cited by 115 · see citing works
Wilson, E. N., Bristol, M. L., Di, X. M., Maltese, W. A., Koterba, K. L., Beckman, M. J., & Gewirtz, D. A. (2011) · Hormones and Cancer · doi:10.1007/s12672-011-0081-7 · Cited by 111 · see citing works
Piccolomini, A., Iskandar, M. M., Lands, L. C., & Kubow, S. J. (2012) · Food & Nutrition Research · doi:10.3402/fnr.v56i0.17549 · Cited by 110 · see citing works
de Toledo, S. M., Asaad, N., Venkatachalam, P., Li, L., Howell, R. W., Spitz, D. R., & Azzam, E. I. (2006) · Radiation Research · doi:10.1667/rr0640.1 · Cited by 110 · see citing works
Qin, X., Cao, M., Lai, F.-N., Yang, F., Ge, W., Zhang, X., Cheng, S., Sun, X., Qin, G., Shen, W., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0127551 · Cited by 108 · see citing works
Effects of phytochemicals on ionization radiation-mediated carcinogenesis and cancer therapy
Nambiar, D. K., Rajamani, P., & Singh, R. P. (2011) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2011.07.005 · Cited by 108 · see citing works
Tran, A. N., Lai, A., Li, S., Pope, W. B., Teixeira, S., Harris, R. J., Woodworth, D. C., Nghiemphu, P. L., Cloughesy, T. F., & Ellingson, B. M. (2013) · Neuro-Oncology · doi:10.1093/neuonc/not198 · Cited by 108 · see citing works
Sirt3, Mitochondrial ROS, Ageing, and Carcinogenesis
Park, S., Özden, Ö., Jiang, H., Cha, Y. I., Pennington, J. D., Aykin‐Burns, N., Spitz, D. R., Gius, D. R., & Kim, H. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12096226 · Cited by 107 · see citing works
Melanin, a promising radioprotector: Mechanisms of actions in a mice model
Kunwar, A., Adhikary, B., Jayakumar, S., Barik, A., Chattopadhyay, S., Raghukumar, S., & Priyadarsini, K. I. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.08.002 · Cited by 106 · see citing works
Oxy-nitroso shielding burst model of cold atmospheric plasma therapeutics
Graves, D. B. (2014) · Clinical Plasma Medicine · doi:10.1016/j.cpme.2014.11.001 · Cited by 103 · see citing works
Altered redox status accompanies progression to metastatic human bladder cancer
Hempel, N., Ye, H., Abessi, B., Mian, B. M., & Melendez, J. A. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.09.020 · Cited by 102 · see citing works
Brooks, A. L., Hoel, D. G., & Preston, R. J. (2016) · International Journal of Radiation Biology · doi:10.1080/09553002.2016.1186301 · Cited by 101 · see citing works
Fan, M., Ahmed, K. M., Coleman, M. C., Spitz, D. R., & Li, J. J. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2728 · Cited by 101 · see citing works
The Role of Peroxiredoxin II in Radiation-Resistant MCF-7 Breast Cancer Cells
Wang, T., Tamae, D., LeBon, T. R., Shively, J. E., Yen, Y., & Li, J. J. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4614 · Cited by 101 · see citing works
DNA is a fractal antenna in electromagnetic fields
Blank, M., & Goodman, R. (2011) · International Journal of Radiation Biology · doi:10.3109/09553002.2011.538130 · Cited by 100 · see citing works
Space-type radiation induces multimodal responses in the mouse gut microbiome and metabolome
Casero, D., Gill, K., Sridharan, V., Koturbash, I., Nelson, G. A., Hauer‐Jensen, M., Boerma, M., Braun, J. G., & Cheema, A. K. (2017) · Microbiome · doi:10.1186/s40168-017-0325-z · Cited by 98 · see citing works
Xu, P., Cai, X., Zhang, W., Li, Y., Qiu, P., Lu, D., & He, X. (2016) · APOPTOSIS · doi:10.1007/s10495-016-1270-1 · Cited by 98 · see citing works
The Nrf2/GCH1/BH4 Axis Ameliorates Radiation-Induced Skin Injury by Modulating the ROS Cascade
Xue, J., Yu, C., Sheng, W., Zhu, W. Z., Luo, J., Zhang, Q., Yang, H., Cao, H., Wang, W., Zhou, J., et al. (2017) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2017.05.019 · Cited by 99 · see citing works
Dayal, D., Martin, S. M., Owens, K. M., Aykin‐Burns, N., Zhu, Y., Amutha, B., Pain, D., Limoli, C. L., Goswami, P. C., Domann, F. E., et al. (2009) · Radiation Research · doi:10.1667/rr1617.1 · Cited by 96 · see citing works
Concepts and challenges in cancer risk prediction for the space radiation environment
Barcellos‐Hoff, M. H., Blakely, E. A., Burma, S., Fornace, A. J., Gerson, S. L., Hlatky, L., Kirsch, D. G., Luderer, U., Shay, J. W., Wang, Y., et al. (2015) · Life Sciences in Space Research · doi:10.1016/j.lssr.2015.07.006 · Cited by 96 · see citing works
Glioblastoma Therapy Can Be Augmented by Targeting IDH1-Mediated NADPH Biosynthesis
Wahl, D. R., Dresser, J., Wilder-Romans, K., Parsels, J. D., Zhao, S. G., Davis, M. A., Zhao, L., Kachman, M. T., Wernisch, S., Burant, C., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-2008 · Cited by 97 · see citing works
An assessment of techniques to manipulate oxidative stress in animals
Koch, R. E., & Hill, G. E. (2016) · Functional Ecology · doi:10.1111/1365-2435.12664 · Cited by 95 · see citing works
Role of the translationally controlled tumor protein in DNA damage sensing and repair
Zhang, J., de Toledo, S. M., Pandey, B. N., Guo, G., Pain, D., Hong Li, A., & Azzam, E. I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106300109 · Cited by 93 · see citing works
Andrade, B., Jara‐Gutiérrez, C., Paz-Araos, M., Vázquez, M. C., Díaz, P., & Murgas, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315182 · Cited by 92 · see citing works
Redox modulation of the DNA damage response
Caputo, F., Vegliante, R., & Ghibelli, L. (2012) · Biochemical Pharmacology · doi:10.1016/j.bcp.2012.07.022 · Cited by 91 · see citing works
Metabolic defects provide a spark for the epigenetic switch in cancer
Hitchler, M. J., & Domann, F. E. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.04.010 · Cited by 91 · see citing works
Mechanisms for Tuning Engineered Nanomaterials to Enhance Radiation Therapy of Cancer
Clement, S., Campbell, J. M., Deng, W., Guller, A., Nisar, S., Liu, G., Wilson, B. C., & Goldys, E. M. (2020) · Advanced Science · doi:10.1002/advs.202003584 · Cited by 88 · see citing works
Collins-Underwood, J. R., Zhao, W., Sharpe, J. G., & Robbins, M. E. C. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.06.024 · Cited by 91 · see citing works
Kuonen, F., Secondini, C., & Rüegg, C. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1758 · Cited by 89 · see citing works
Thiol regulation by Mn porphyrins, commonly known as SOD mimics
Batinic-Haberle, I., & Tome, M. E. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101139 · Cited by 88 · see citing works
Little, M. P., Azizova, T. V., & Hamada, N. (2021) · International Journal of Radiation Biology · doi:10.1080/09553002.2021.1876955 · Cited by 88 · see citing works
Micro RNA responses to chronic or acute exposures to low dose ionizing radiation
Chaudhry, M. A., Omaruddin, R. A., Kreger, B. T., de Toledo, S. M., & Azzam, E. I. (2012) · Molecular Biology Reports · doi:10.1007/s11033-012-1589-9 · Cited by 84 · see citing works
Jiang, J., Belikova, N. A., Hoye, A. T., Zhao, Q., Epperly, M. W., Greenberger, J. S., Wipf, P., & Kagan, V. E. (2008) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2007.10.047 · Cited by 83 · see citing works
- Authors
- Spitz, D. R., Azzam, E. I., Jian Li, J., & Gius, D.
- Affiliations
- University of Iowa (US)
- Rutgers New Jersey Medical School (US)
- National Institutes of Health (US)
- Corresponding author
- Spitz, Douglas R.
- Venue
- Cancer and Metastasis Reviews
- Published
- 2004-08
- Volume
- 23
- Issue
- 3-4
- Pages
- 311-322
- ISSN
- 0167-7659 (ISSN-L)
- 1573-7233
- OpenAlex
- W2023627397
- Cited by
- 710
- References
- 105
- Citations by year
- 2026: 19 · 2025: 24 · 2024: 21 · 2023: 33 · 2022: 27 · 2021: 41 · 2020: 47 · 2019: 46 · 2018: 50 · 2017: 41 · 2016: 38 · 2015: 21 · 2014: 33 · 2013: 47 · 2012: 43
- FWCI
- 2.51
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Cancer and Metastasis Reviews (publishedVersion)
- PubMed (publishedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Toxicology › Bioactive Compounds and Antitumor Agents
- Keywords
- ionizing radiation, redox signaling, free radicals, radiation-induced oxidative damage, radiation adaptive response, bystander effect, cell cycle disruption, radiosensitization, genomic instability, inflammation, fibrosis, transcription factor activation, gene expression
- MeSH terms
- Animals, Cell Communication, Humans, Oxidation-Reduction, Radiation, Ionizing, Signal Transduction, Oxidative Stress, Genomic Instability
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