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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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“The decrease in TAC could be attributed to the consumption of endogenous antioxidants because of free radical generation after radiation exposure [37].”
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“Radiation exposure induces the immediate formation of short-lived free radicals; the activation of protective or damaging processes might depend on the cellular handling of this oxidative damage (Spitz et al. 2004).”
BackgroundNADPH Oxidase Activation Contributes to Heavy Ion Irradiation–Induced Cell Death
Wang, Y., Liu, Q., Zhao, W., Zhou, X. H., Miao, G., Sun, C., & Zhang, H. (2017) · Dose-Response · doi:10.1177/1559325817699697 · Cited by 18
Golz, A.-L., & Bradshaw, C. (2019) · Frontiers in Environmental Science · doi:10.3389/fenvs.2019.00100 · Cited by 18
“When a cell is under oxidative stress, the antioxidant defense from ROS scavenging is not effective enough and ROS can readily attack PUFAs in the cell membrane (Mylonas and Kouretas, 1999).”
BackgroundInfluentialSzejk, M., Czubak-Prowizor, K., Macieja, A., Popławski, T., Olejnik, A. K., Pawlaczyk‐Graja, I., Gancarz, R. A., & Żbikowska, H. M. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.11.186 · Cited by 18
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Snyder, A. R., & Morgan, W. F. (2005) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20092 · Cited by 18
“The oxidative stress exhibited in these systems may perpetuate chromosomal instability [Spitz et al., 2004] and may also lead to increased rates of apoptosis in chromosomally unstable cells [Limoli et al.”
Intestinal injury can be effectively prevented by Dunaliella salina in gamma irradiated rats
Khayyal, M. T., El-Baz, F. K., Meselhy, M. R., Ali, G. H., & El‐Hazek, R. M. (2019) · Heliyon · doi:10.1016/j.heliyon.2019.e01814 · Cited by 18
Ancha, H. R., Kurella, R. R., McKimmey, C. C., Lightfoot, S. A., & Harty, R. F. (2008) · Experimental Biology and Medicine · doi:10.3181/0805-rm-140 · Cited by 18
“In this latter instance, ROS are formed as byproducts of oxygen metabolism under physiological or non-stress conditions and their levels are regulated by both non-enzymatic and enzymatic antioxidants (1, 8).”
BackgroundSofra, X., & Badami, S. (2020) · Health · doi:10.4236/health.2020.128076 · Cited by 17
Whitaker, J., Zei, P. C., Ahmad, S., Niederer, S., O'Neill, M. D., & Rinaldi, C. A. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.989886 · Cited by 17
“RT induced mitochondrial dysfunction promote cellular aging and apoptosis (13).”
BackgroundMao, X. W., Stanbouly, S., Holley, J. M., Pecaut, M. J., & Crapo, J. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087362 · Cited by 17
“Radiation-induced oxidative stress can damage critical cellular structure and biomolecules [42], resulting in inflammatory responses, cell death, and tissue remodeling [43,44].”
BackgroundFerroptosis: A Targetable Vulnerability for Melanoma Treatment
Yu, M., Zhou, Q., Dian, Y., Zeng, F., Deng, G., & Chen, X. (2025) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2024.11.007 · Cited by 19
A radiation-induced adaptive response prolongs the survival of prion-infected mice
Plews, M., Simon, S. L. R., Boreham, D. R., Parchaliuk, D. L., Wyatt, H., Mantha, R., Frost, K. L., Lamoureux, L., Stobart, M. J., Czub, S., et al. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.07.025 · Cited by 17
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Hypo-CpG methylation controls PTEN expression and cell apoptosis in irradiated lung
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“Increased NADPH oxidase expression and activity are possible sources of increased ROS production postirradiation [36].”
BackgroundEvaluation of thiol-disulphide homeostasis in radiation workers
Koç, U., Tan, S., Ertem, A. G., Gümüş, M., İpteç, B. Ö., & Erel, Ö. (2017) · International Journal of Radiation Biology · doi:10.1080/09553002.2017.1304668 · Cited by 17
“The fact that IR leads to oxidative injury, upon both acute and chronic exposure to free radicals by inducing oxidative stress, has been demonstrated in many studies using a range of biochemical parameters (Sugisawa and Umegaki 2002; Spitz et al. 2004; Malekirad et al. 2005; Eken et al. 2012).”
BackgroundYi, J., Cheng, C., Li, S., Wang, D., Wang, L., & Wang, Z. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.02.131 · Cited by 17
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“iological changes that lead to tissue damage, including apoptosis (25, 26).”
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“This could be a radioadaptive response, which has been under debate for radiation protection guidelines (23, 24).”
BackgroundModulation of Radiation Response by the Tetrahydrobiopterin Pathway
Pathak, R., Cheema, A. K., Boca, S. M., Krager, K. J., Hauer‐Jensen, M., & Aykin‐Burns, N. (2015) · Antioxidants · doi:10.3390/antiox4010068 · Cited by 17
“Thus, it is becoming more evident that disruption in intracellular metabolic redox homeostasis will remain compromised for longer periods of time following IR [11,29,30].”
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Pathobiology of Cancer Regimen-Related Toxicities
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DNA strand breakage by bivalent metal ions and ionizing radiation
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“Several investigators (see, e.g., Thornalley & Vasak 1985, Spitz et al. 2004) have proposed that oxidative stress induced by radiation plays a significant role in radiation induced cell death, beyond the role played by the well known effects of radiation on DNA.”
BackgroundDivergent Molecular and Cellular Responses to Low and High-Dose Ionizing Radiation
Sampadi, B. K., Vermeulen, S., Mišovic, B., Boei, J. J. W. A., Batth, T. S., Chang, J.-G., Paulsen, M. T., Magnuson, B., Schimmel, J., Kool, H., et al. (2022) · Cells · doi:10.3390/cells11233794 · Cited by 18
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The Role of Radiation Induced Injury on Lung Cancer
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“This manuscript is designed to evaluate the role of dose per cell turnover, tissue disorganization, and the breakdown of cell/cell and cell/tissue communication [12,13] increased cell turnover [14], cell killing [15,16], and chronic inflammatory disease [17,18] on lung cancer induction.”
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Pantelić, N. Đ., Zmejkovski, B. B., Božić, B. D., Dojčinović, B., Banjac, N. R., Wessjohann, L. A., & Kaluđerović, G. N. (2020) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2020.111207 · Cited by 16
Aberrant miRNA expression response to UV irradiation in human liver cancer cells
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“However, radiation causes damage mostly via ionization and formation of reactive oxygen species (ROS), and the increased ROS induces rapid primordial follicle loss in the ovaries [5, 6].”
BackgroundBioSentinel: Validating Sensitivity of Yeast Biosensors to Deep Space Relevant Radiation
Liddell, L. C., Gentry, D. M., Gilbert, R., Marina, D. B., Tieze, S. M., Padgen, M. R., Akiyama, K., Keenan, K., Bhattacharya, S., & Maria, S. R. S. (2023) · Astrobiology · doi:10.1089/ast.2022.0124 · Cited by 15
“In addition, inter-cellular metabolic redox reactions can be affected by IR-induced free radical formation and can remain perturbed for minutes, hours, or even days (Kohen and Abraham, 2002; Spitz et al. , 2004).”
Wang, Y., Yang, L., Liu, B., Liao, S., Fu, X., Zhou, Y., & Zhou, P. (2023) · Advanced Therapeutics · doi:10.1002/adtp.202300024 · Cited by 15
Effect of low-dose X-rays on the liver of whole-body irradiated rats
Abdelrazzak, A. B., El-Missiry, M. A., Ahmed, M. T., & Elnady, B. F. (2018) · International Journal of Radiation Biology · doi:10.1080/09553002.2019.1554925 · Cited by 15
“In contrast with the data showing an increase in the endogenous antioxidant following irradiation as an evidence of adaptive response (Shimizu et al. 1998; Guo et al. 2003; Spitz et al. 2004), the current antioxidant data indicated that there was no adaptive response induced in the present model system.”
BackgroundResult
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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