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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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“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
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BackgroundGenotoxic repercussion of high‐intensity radiation (x‐rays) on hospital radiographers
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“As seen before, the radiation builds up free radicals to cause breaks in chromosomes, or the chromosome remains structurally flustered for a long time resulting in chromatid exchanges (Spitz et al., 2004).”
BackgroundDanışan, G., Taydaş, O., Özdemir, M., Ateş, Ö. F., Kupeli, A., Öğüşlü, U., Erkin, A., Neşeli̇oğlu, S., & Eren, F. K. (2023) · Clinical Radiology · doi:10.1016/j.crad.2023.02.016 · Cited by 2
Abdelrahman, A. M., Mohammed, A. A., Badawy, M. M. M., & bassuony, W. I. E. (2023) · Cell Biochemistry and Function · doi:10.1002/cbf.3861 · Cited by 2
“Lethal Mutations” a Misnomer or the Start of a Scientific Revolution?
Mothersill, C. E., Desai, R., Seymour, C. B., & Mendonca, M. S. (2024) · Radiation Research · doi:10.1667/rade-24-00018.1 · Cited by 2
MANSOUR, D., Morsi, R. M., & Mousa, A. M. (2024) · International Journal of Radiation Research · doi:10.61186/ijrr.22.4.1027 · Cited by 2
Chan, E., Sivagnanam, T., Zhang, Q., Lewis, C. R., & Thomas, P. S. (2012) · Journal of Cancer Therapy · doi:10.4236/jct.2012.324059 · Cited by 2
Aller, M., Vara, E., Garcı́a, C., Méndez, M., Méndez, M., Mejía, I., López, L., Árias, J., & Árias, J. (2008) · Pathophysiology · doi:10.1016/j.pathophys.2008.09.003 · Cited by 2
PANC-1 cells proliferative response to ionizing radiation is related to GSK-3β phosphorylation
Mohamad, N. A., Cricco, G., Cocca, C., Rivera, E., BERGOC, R. M., & Martín, G. (2012) · Biochemistry and Cell Biology · doi:10.1139/o2012-032 · Cited by 2
Metabolic Production of H2O2 in Carcinogenesis and Cancer Treatment
Allen, B. G., & Spitz, D. R. (2016) · Oxidative stress in applied basic research and clinical practice · doi:10.1007/978-3-319-30705-3_6 · Cited by 3
Ivanova, T. I., Fesenko, E. V., Анатольевна, Д. Л., Degtyareva, E. S., Сирекановна, М. Л., Ovsyannikova, N. C., Алексеевна, Х. В., & Krikunova, L. I. (2018) · Radiation and Risk Bulletin of the National Radiation and Epidemiological Registry · doi:10.21870/0131-3878-2018-27-2-46-61 · Cited by 2
“Проводимые ранее другими авторами исследования показали, что после облучения в малых дозах повышается уровень экспрессии митохондриальной супероксиддисмутазы [29].”
Role of Radiation in DNA Damage and Radiation Induced Cancer
Chandel, V., Seth, G., Shukla, P., & Kumar, D. (2019) · Environmental science and engineering · doi:10.1007/978-3-319-96511-6_1 · Cited by 2
Stanojević, B., Đukić, M., Stevanović, I. D., Ninković, M., Đurić, A., Gobeljić, B., Apostolović, M., Pantelić, A., Zebić, G., Todorović, L., et al. (2018) · Hrana i ishrana · doi:10.5937/hraish1801026s · Cited by 2
“It is well known that ionizing radiation induces OS in living organisms [10].”
BackgroundCaenorhabitidis elegans as an animal model in toxicological studies
Machado, M. L., Zamberlan, D. C., Arantes, L. P., Aschner, M., & Soares, F. A. A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813602-7.00038-7 · Cited by 2
Choudhuri, S., Arvidson, K. B., & Chanderbhan, R. F. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-385926-6.00026-0 · Cited by 2
FLASH-Radiotherapy: A Potential Innovation Driver in Radiation Therapy
Seo, Y.-S., Park, W., Min, B. J., Choi, K., & Kim, K.-W. (2020) · Journal of the Korean Physical Society · doi:10.3938/jkps.77.357 · Cited by 2
Bouameur, S., Menad, A., hamadou, T., rgensen, B. J. O., & Ameddah, S. (2021) · Egyptian Journal of Chemistry · doi:10.21608/ejchem.2021.88910.4293 · Cited by 2
Ahmad, I. M., Bartenhagen, L., Michael, K., & Abdalla, M. Y. (2023) · International Journal of Radiation Biology · doi:10.1080/09553002.2023.2258194 · Cited by 2
“This increase was shown to be involved in pathological health effects including inflammation, fibrosis, necrosis, and cancer (Spitz et al. 2004; Jacob et al. 2009; Zielinski et al. 2009; Zakeri and Hirobe 2010).”
BackgroundInfluence of Local Temporary Ischemia on Radiotherapy Effects
Walichiewicz, P., Sochanik, A., & Przybyszewski, W. M. (2011) · Journal of Cancer Therapy · doi:10.4236/jct.2011.22027 · Cited by 2
“Mitochondrial dysfunction contributes to the development of persistent genetic instability observed not only in vitro in cell cultures for many generation but also in vivo in animals progeny [21].”
BackgroundPandey, B. N., Kumar, A., Rastogi, L., & Mishra, K. P. (2008) · International Journal of Low Radiation · doi:10.1504/ijlr.2008.020979 · Cited by 2
In-situ observation of mitochondrial biogenesis as the early event of apoptosisPreprint
Shao, C., Zhou, X., Miao, Y., Wang, P., Zhang, Q., & Huang, Q. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.23.263152 · Cited by 3
“…dual fluorescence report system, we have316 observed radiation-induced mitochondrial biogenesis preceding the cell apoptosis.317 Ionizing radiation has been used for cancer therapy for they can directly or indirectly318 cause DNA damage and kill the cancer cells (Spitz et al., 2004) .”
Thiol disulfide homeostasis in ionizing radiation and chemotherapeutic drug exposure
Eroğlu, N. (2021) · Northern Clinics of Istanbul · doi:10.14744/nci.2021.59913 · Cited by 1
“Protein, lipids, and DNA of the cell can be affected by ROS overproduction, destroying the function, and structure of cells [9, 10].”
BackgroundÖzbek, D. Ü., & KURUÇAY, D. (2022) · Cumhuriyet Science Journal · doi:10.17776/csj.1088724 · Cited by 2
Annual gamma-ray background dose rates in dwellings of rural Tumkur
Udagani, C. (2023) · Radiation Protection Dosimetry · doi:10.1093/rpd/ncad210 · Cited by 1
Pontoriero, A., Critelli, P., Zeppieri, M., Brogna, A., Angileri, F. F., Bottari, A., Stagno, A., Parisi, S., & Pergolizzi, S. (2024) · Annali Italiani di Chirurgia · doi:10.62713/aic.3360 · Cited by 1
Shu, P., Wang, F., & Wang, X. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1536689 · Cited by 1
“Speci fi cally, RT stimulates the release of tumor antigens, promotes danger-associated molecular patterns (DAMPs), generates reactive oxygen species (ROS), and increases the expression of major histocompatibility complex I and FAS, leading to anti-tumor activity (20 – 22).”
Sitagliptin Alleviates Radiation-Induced Kidney and Testis Degeneration in Rats
Celik, H. T., Temelli, Ö., Özhan, O., Taşlıdere, E., & Dogru, F. (2025) · Biomolecules · doi:10.3390/biom15121702 · Cited by 1
“Kidney tubule epithelia and spermatocytes also have high metabolic activity and are, hence, prone to cellular degeneration caused by numerous insults [28].”
Advances in redox imaging for cancer diagnosis and therapy
Yasui, H., Kato, K., Bo, T., & Inanami, O. (2025) · Journal of Clinical Biochemistry and Nutrition · doi:10.3164/jcbn.25-211 · Cited by 2
“(16) Ferroptosis, an iron-dependent form of regulated cell death driven by lipid peroxidation, is a crucial mechanism in radiation-induced cancer cell death.”
Kura, B., Pavelkova, P., Kaločayová, B., Sýkora, M., Vlkovičová, J., Kluknavský, M., LeBaron, T. W., Pobijakova, M., Šagátová, A., & Slezák, J. (2026) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2025-0085 · Cited by 1
Kamar, A. E., Mavroudis, I. A., Ciobica, A., Gheban, D., Morosan, C., Gurzu, I. L., & Novac, O. (2026) · Frontiers in Public Health · doi:10.3389/fpubh.2026.1803266 · Cited by 1
Metadata
- 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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