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Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells

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A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cellular Immunology".

Deadline for manuscript submissions: closed (10 November 2021) | Viewed by 21773

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Special Issue Editors

Dr. Serge Candéias

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Guest Editor

French Alternative Energies and Atomic Energy Commission (CEA), 38000 Grenoble, France
Interests: radiation biology; immunology; low dose; bystander effects; normal tissues; inflammation; lymphocyte development; V(D)J recombination

Dr. Katalin Lumniczky

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Guest Editor

Department of Radiation Medicine, National Public Health Institute, 1097 Budapest, Hungary
Interests: radiation biology; immunology; non-targeted effects; extracellular vesicles; intercellular communication
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Dear Colleagues,

The interactions between the immune system and the response to radiation are complex. On the one hand, irradiation of any part of the body directly affects the immune system, as circulating immune cells are distributed throughout the organism via the blood. Furthermore, immune cells can be concentrated in normal and pathological structures such as lymph nodes and solid tumors, which may be the target of radiation, for example during cancer treatment. On the other hand, as part of the organism’s defenses, the immune system will try to counteract the detrimental effects of radiation exposure and participate in the restoration of tissue homeostasis and functions.

A lot of knowledge have accumulated over time on the effects of high dose radiation on the immune system, and especially on the various forms of radiation-induced cell death and the consequences for immune system activation. In contrast, much less data are available on the effects of low dose radiation exposure, despite the surge in interest for this topic during the last years. Indeed, ionizing radiation exposure in the low to intermediate range induces much less genotoxic damage and cell death, and the effects of such exposures will be dominated by the consequences of cell stress and damage to the various cellular compartments, including an imbalance of the redox status. These effects may manifest as cell autonomous events, or be more diffuse, transmitted to neighboring cells, irradiated or not, by inter-cellular communication, via either cell-cell contact or soluble factors, including inflammatory mediators, and extracellular vesicles. Thus, these effects can result from direct exposure of immune cells, or from their response to irradiated cells, or a combination of both.

In this special issue, we welcome articles from all fields of radiation biology (environmental, occupational and accidental exposure, in vitro and in vivo pre-clinical models, medical applications of ionizing radiation) addressing the specific effects of low dose radiation (<100 mGy) on the homeostasis and direct or indirect activation of the immune system, when compared to intermediate and higher dose exposures. These articles can be original research articles or reviews aimed at summarizing a dedicated aspect of the effects of low dose exposure on immune cells.

Dr. Serge Candéias
Dr. Katalin Lumniczky
Guest Editors

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Keywords

low dose ionizing radiation
immune system
quality of radiation
homeostasis
activation
development
inflammation
bystander effects
exosomes

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Published Papers (7 papers)

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Research

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14 pages, 1441 KiB

Open AccessArticle

Genotoxicity Associated with ¹³¹I and ^99mTc Exposure in Nuclear Medicine Staff: A Physical and Biological Monitoring Study

by Justyna Miszczyk, Aleksander Gałaś, Agnieszka Panek, Aldona Kowalska, Magdalena Kostkiewicz, Eliza Borkowska and Kamil Brudecki

Cells 2022, 11(10), 1655; https://doi.org/10.3390/cells11101655 - 16 May 2022

Cited by 4 | Viewed by 2479

Abstract

Nuclear medicine staff are constantly exposed to low doses of ionizing radiation. This study investigated the level of genotoxic effects in hospital employees exposed to routinely used ¹³¹I and ^99mTc in comparison with a control group. The study compared the results of physical and biological monitoring in peripheral blood lymphocytes. The effects of confounding factors, such as smoking status and physical activity, were also considered. Physical dosimetry monitoring revealed differences in the individual annual effective dose as measured by finger ring dosimeter and whole-body dosimeter between the ¹³¹I- and ^99mTc-exposed groups. The DNA damage studies revealed differences between the groups in terms of excess premature chromosome condensation (PCC) fragments and tail DNA. Physical activity and smoking status differentiated the investigated groups. When assessed by the level of physical activity, the highest mean values of tail DNA were observed for the ^99mTc group. When assessed by work-related physical effort, excess PCC fragments were significantly higher in the ¹³¹I group than in the control group. In the investigated groups, the tail DNA values were significantly different between non-smokers and past or current smokers, but excess PCC fragments did not significantly differ by smoking status. It is important to measure exposure to low doses of ionizing radiation and assess the potential risk from this exposure. Such investigations support the need to continue epidemiological and experimental studies to improve our understanding of the mechanisms of the health effects of radionuclides and to develop predictive models of the behavior of these complex systems in response to low-dose radiation. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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23 pages, 5231 KiB

Open AccessArticle

Radon Improves Clinical Response in an Animal Model of Rheumatoid Arthritis Accompanied by Increased Numbers of Peripheral Blood B Cells and Interleukin-5 Concentration

by Lisa Deloch, Stephanie Hehlgans, Michael Rückert, Andreas Maier, Annika Hinrichs, Ann-Sophie Flohr, Denise Eckert, Thomas Weissmann, Michaela Seeling, Falk Nimmerjahn, Rainer Fietkau, Franz Rödel, Claudia Fournier, Benjamin Frey and Udo S. Gaipl

Cells 2022, 11(4), 689; https://doi.org/10.3390/cells11040689 - 16 Feb 2022

Cited by 4 | Viewed by 3478

Abstract

Radon treatment is used as an established therapy option in chronic painful inflammatory diseases. While analgesic effects are well described, little is known about the underlying molecular effects. Among the suspected mechanisms are modulations of the anti-oxidative and the immune system. Therefore, we aimed for the first time to examine the beneficial effects of radon exposure on clinical outcome as well as the underlying mechanisms by utilizing a holistic approach in a controlled environment of a radon chamber with an animal model: K/BxN serum-induced arthritic mice as well as isolated cells were exposed to sham or radon irradiation. The effects on the anti-oxidative and the immune system were analyzed by flow-cytometry, qPCR or ELISA. We found a significantly improved clinical disease progression score in the mice, alongside significant increase of peripheral blood B cells and IL-5. No significant alterations were visible in the anti-oxidative system or regarding cell death. We conclude that neither cell death nor anti-oxidative systems are responsible for the beneficial effects of radon exposure in our preclinical model. Rather, radon slightly affects the immune system. However, more research is still needed in order to fully understand radon-mediated effects and to carry out reasonable risk-benefit considerations. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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25 pages, 5004 KiB

Open AccessArticle

Extracellular Vesicles Derived from Bone Marrow in an Early Stage of Ionizing Radiation Damage Are Able to Induce Bystander Responses in the Bone Marrow

by Dávid Kis, Ilona Barbara Csordás, Eszter Persa, Bálint Jezsó, Rita Hargitai, Tünde Szatmári, Nikolett Sándor, Enikő Kis, Katalin Balázs, Géza Sáfrány and Katalin Lumniczky

Cells 2022, 11(1), 155; https://doi.org/10.3390/cells11010155 - 4 Jan 2022

Cited by 5 | Viewed by 2709

Abstract

Ionizing radiation (IR)-induced bystander effects contribute to biological responses to radiation, and extracellular vesicles (EVs) play important roles in mediating these effects. In this study we investigated the role of bone marrow (BM)-derived EVs in the bystander transfer of radiation damage. Mice were irradiated with 0.1Gy, 0.25Gy and 2Gy, EVs were extracted from the BM supernatant 24 h or 3 months after irradiation and injected into bystander mice. Acute effects on directly irradiated or EV-treated mice were investigated after 4 and 24 h, while late effects were investigated 3 months after treatment. The acute effects of EVs on the hematopoietic stem and progenitor cell pools were similar to direct irradiation effects and persisted for up to 3 months, with the hematopoietic stem cells showing the strongest bystander responses. EVs isolated 3 months after irradiation elicited no bystander responses. The level of seven microRNAs (miR-33a-3p, miR-140-3p, miR-152-3p, miR-199a-5p, miR-200c-5p, miR-375-3p and miR-669o-5p) was altered in the EVs isolated 24 hour but not 3 months after irradiation. They regulated pathways highly relevant for the cellular response to IR, indicating their role in EV-mediated bystander responses. In conclusion, we showed that only EVs from an early stage of radiation damage could transmit IR-induced bystander effects. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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20 pages, 3316 KiB

Open AccessArticle

ROS- and Radiation Source-Dependent Modulation of Leukocyte Adhesion to Primary Microvascular Endothelial Cells

by Denise Eckert, Felicitas Rapp, Ayele T. Tsedeke, Jessica Molendowska, Robert Lehn, Markus Langhans, Claudia Fournier, Franz Rödel and Stephanie Hehlgans

Cells 2022, 11(1), 72; https://doi.org/10.3390/cells11010072 - 27 Dec 2021

Cited by 14 | Viewed by 2864

Abstract

Anti-inflammatory effects of low-dose irradiation often follow a non-linear dose–effect relationship. These characteristics were also described for the modulation of leukocyte adhesion to endothelial cells. Previous results further revealed a contribution of reactive oxygen species (ROS) and anti-oxidative factors to a reduced leukocyte adhesion. Here, we evaluated the expression of anti-oxidative enzymes and the transcription factor Nrf2 (Nuclear factor-erythroid-2-related factor 2), intracellular ROS content, and leukocyte adhesion in primary human microvascular endothelial cells (HMVEC) upon low-dose irradiation under physiological laminar shear stress or static conditions after irradiation with X-ray or Carbon (C)-ions (0–2 Gy). Laminar conditions contributed to increased mRNA expression of anti-oxidative factors and reduced ROS in HMVEC following a 0.1 Gy X-ray and 0.5 Gy C-ion exposure, corresponding to reduced leukocyte adhesion and expression of adhesion molecules. By contrast, mRNA expression of anti-oxidative markers and adhesion molecules, ROS, and leukocyte adhesion were not altered by irradiation under static conditions. In conclusion, irradiation of endothelial cells with low doses under physiological laminar conditions modulates the mRNA expression of key factors of the anti-oxidative system, the intracellular ROS contents of which contribute at least in part to leucocyte adhesion, dependent on the radiation source. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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16 pages, 2965 KiB

Open AccessArticle

Dose and Dose Rate-Dependent Effects of Low-Dose Irradiation on Inflammatory Parameters in ApoE-Deficient and Wild Type Mice

by Annegret Glasow, Ina Patties, Nicholas D. Priest, Ronald E. J. Mitchel, Guido Hildebrandt and Katrin Manda

Cells 2021, 10(11), 3251; https://doi.org/10.3390/cells10113251 - 20 Nov 2021

Cited by 3 | Viewed by 2311

Abstract

Anti-inflammatory low-dose therapy is well established, whereas the immunomodulatory impact of doses below 0.1 Gy is much less clear. In this study, we investigated dose, dose rate and time-dependent effects in a dose range of 0.005 to 2 Gy on immune parameters after whole body irradiation (IR) using a pro-inflammatory (ApoE−/−) and a wild type mouse model. Long-term effects on spleen function (proliferation, monocyte expression) were analyzed 3 months, and short-term effects on immune plasma parameters (IL6, IL10, IL12p70, KC, MCP1, INFγ, TGFβ, fibrinogen, sICAM, sVCAM, sE-selectin/CD62) were analyzed 1, 7 and 28 days after Co60 γ-irradiation (IR) at low dose rate (LDR, 0.001 Gy/day) and at high dose rate (HDR). In vitro measurements of murine monocyte (WEHI-274.1) adhesion and cytokine release (KC, MCP1, IL6, TGFβ) after low-dose IR (150 kV X-ray unit) of murine endothelial cell (EC) lines (H5V, mlEND1, bEND3) supplement the data. RT-PCR revealed significant reduction of Ki67 and CD68 expression in the spleen of ApoE−/− mice after 0.025 to 2 Gy exposure at HDR, but only after 2 Gy at LDR. Plasma levels in wild type mice, showed non-linear time-dependent induction of proinflammatory cytokines and reduction of TGFβ at doses as low as 0.005 Gy at both dose rates, whereas sICAM and fibrinogen levels changed in a dose rate-specific manner. In ApoE−/− mice, levels of sICAM increased and fibrinogen decreased at both dose rates, whereas TGFβ increased mainly at HDR. Non-irradiated plasma samples revealed significant age-related enhancement of cytokines and adhesion molecules except for sICAM. In vitro data indicate that endothelial cells may contribute to systemic IR effects and confirm changes of adhesion properties suggested by altered sICAM plasma levels. The differential immunomodulatory effects shown here provide insights in inflammatory changes occurring at doses far below standard anti-inflammatory therapy and are of particular importance after diagnostic and chronic environmental exposures. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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17 pages, 3755 KiB

Open AccessArticle

Cisplatin Reduces the Frequencies of Radiotherapy-Induced Micronuclei in Peripheral Blood Lymphocytes of Patients with Gynaecological Cancer: Possible Implications for the Risk of Second Malignant Neoplasms

by Aneta Węgierek-Ciuk, Anna Lankoff, Halina Lisowska, Piotr Kędzierawski, Pamela Akuwudike, Lovisa Lundholm and Andrzej Wojcik

Cells 2021, 10(10), 2709; https://doi.org/10.3390/cells10102709 - 9 Oct 2021

Cited by 4 | Viewed by 2359

Abstract

Gynaecologic cancers are common among women and treatment includes surgery, radiotherapy or chemotherapy, where the last two methods induce DNA damage in non-targeted cells like peripheral blood lymphocytes (PBL). Damaged normal cells can transform leading to second malignant neoplasms (SMN) but the level of risk and impact of risk modifiers is not well defined. We investigated how radiotherapy alone or in combination with chemotherapy induce DNA damage in PBL of cervix and endometrial cancer patients during therapy. Blood samples were collected from nine endometrial cancer patients (treatment with radiotherapy + chemotherapy—RC) and nine cervical cancer patients (treatment with radiotherapy alone—R) before radiotherapy, 3 weeks after onset of radiotherapy and at the end of radiotherapy. Half of each blood sample was irradiated ex vivo with 2 Gy of gamma radiation in order to check how therapy influenced the sensitivity of PBL to radiation. Analysed endpoints were micronucleus (MN) frequencies, apoptosis frequencies and cell proliferation index. The results were characterised by strong individual variation, especially the MN frequencies and proliferation index. On average, despite higher total dose and larger fields, therapy alone induced the same level of MN in PBL of RC patients as compared to R. This result was accompanied by a higher level of apoptosis and stronger inhibition of cell proliferation in RC patients. The ex vivo dose induced fewer MN, more apoptosis and more strongly inhibited proliferation of PBL of RC as compared to R patients. These results are interpreted as evidence for a sensitizing effect of chemotherapy on radiation cytotoxicity. The possible implications for the risk of second malignant neoplasms are discussed. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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28 pages, 1988 KiB

Open AccessReview

COVID-19: The Disease, the Immunological Challenges, the Treatment with Pharmaceuticals and Low-Dose Ionizing Radiation

by Jihang Yu, Edouard I. Azzam, Ashok B. Jadhav and Yi Wang

Cells 2021, 10(9), 2212; https://doi.org/10.3390/cells10092212 - 27 Aug 2021

Cited by 4 | Viewed by 4013

Abstract

The year 2020 will be carved in the history books—with the proliferation of COVID-19 over the globe and with frontline health workers and basic scientists worldwide diligently fighting to alleviate life-threatening symptoms and curb the spread of the disease. Behind the shocking prevalence of death are countless families who lost loved ones. To these families and to humanity as a whole, the tallies are not irrelevant digits, but a motivation to develop effective strategies to save lives. However, at the onset of the pandemic, not many therapeutic choices were available besides supportive oxygen, anti-inflammatory dexamethasone, and antiviral remdesivir. Low-dose radiation (LDR), at a much lower dosage than applied in cancer treatment, re-emerged after a 75-year silence in its use in unresolved pneumonia, as a scientific interest with surprising effects in soothing the cytokine storm and other symptoms in severe COVID-19 patients. Here, we review the epidemiology, symptoms, immunological alterations, mutations, pharmaceuticals, and vaccine development of COVID-19, summarizing the history of X-ray irradiation in non-COVID diseases (especially pneumonia) and the currently registered clinical trials that apply LDR in treating COVID-19 patients. We discuss concerns, advantages, and disadvantages of LDR treatment and potential avenues that may provide empirical evidence supporting its potential use in defending against the pandemic. Full article

(This article belongs to the Special Issue Low Dose Radiation Effects on the Homeostasis and Activation of Immune Cells)

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