Low doses of ionizing radiation induce immune-stimulatory responses in isolated human primary monocytes

International Journal of Molecular Medicine

Volumn 32, Issue 6, 2013, Pages 1407-1414

  El Saghire, Houssein ^a,b   Michaux, Arlette ^a   Thierens, Hubert ^b   Baatout, Sarah ^a,c  

^a BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

Damage; High dose; Human primary monocytes; Inflammatory response; Ionizing radiation; Low dose; MAPK; NF B; TLR

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PF4 PROTEIN; PROTEIN P53; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ARTICLE; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE DISRUPTION; HEALTH HAZARD; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOSTIMULATION; INFLAMMATION; IONIZING RADIATION; MONOCYTE; NORMAL HUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RADIATION DOSE; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL SEPARATION; CELL SURVIVAL; CELLS, CULTURED; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, RADIATION; DOWN-REGULATION; ENZYME ACTIVATION; HMGB1 PROTEIN; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MONOCYTES; NF-KAPPA B; PHOSPHORYLATION; PLATELET FACTOR 4; RADIATION, IONIZING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84892148609     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2013.1514     Document Type: Article

References (46)

1. Hall EJ and Brenner DJ: Cancer risks from diagnostic radiology. Br J Radiol 81: 362-378, 2008.
2. Pearce MS, Salotti JA, Little MP, et al: Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet 380: 499-505, 2012.
3. Pernot E, Hall J, Baatout S, et al: Ionizing radiation biomarkers for potential use in epidemiological studies. Mutat Res 751: 258-286, 2012.
4. Shah DJ, Sachs RK and Wilson DJ: Radiation-induced cancer: a modern view. Br J Radiol 85: e1166-e1173, 2012.
5. El-Saghire H, Thierens H, Monsieurs P, Michaux A, Vandevoorde C and Baatout S: Gene set enrichment analysis highlights different gene expression profiles in whole blood samples X-irradiated with low and high doses. Int J Radiat Biol 89: 628-638, 2013.
6. Hume DA: The mononuclear phagocyte system. Curr Opin Immunol 18: 49-53, 2006.
7. Bauer M, Goldstein M, Christmann M, Becker H, Heylmann D and Kaina B: Human monocytes are severely impaired in base and DNA double-strand break repair that renders them vulnerable to oxidative stress. Proc Natl Acad Sci USA 108: 21105-21110, 2011.
8. Kawai T and Akira S: The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384, 2010.
9. Krutzik SR, Tan B, Li H, et al: TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 11: 653-660, 2005.
10. Piccinini AM and Midwood KS: DAMPening inflammation by modulating TLR signalling. Mediators Inflamm 2010: 672395, 2010.
11. Kawai T and Akira S: Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650, 2011.
12. Shan YX, Jin SZ, Liu XD, Liu Y and Liu SZ: Ionizing radiation stimulates secretion of pro-inflammatory cytokines: dose-response relationship, mechanisms and implications. Radiat Environ Biophys 46: 21-29, 2007.
13. Ivanov S, Dragoi AM, Wang X, et al: A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 110: 1970-1981, 2007.
14. Menendez D, Shatz M, Azzam K, Garantziotis S, Fessler MB and Resnick MA: The Toll-like receptor gene family is integrated into human DNA damage and p53 networks. PLoS Genet 7: e1001360, 2011.
15. Cargnello M and Roux PP: Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 75: 50-83, 2011.
16. Hayden MS and Ghosh S: NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234, 2012.
17. Pfaffl MW: A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
18. UNSCEAR: Report of the fifty seventh session: Summary of low-dose radiation effects on health. 2010.
19. Liu C, Zhang C, Mitchel RE, et al: A critical role of toll-like receptor 4 (TLR4) and its' in vivo ligands in basal radio-resistance. Cell Death Dis 4: e649, 2013.
20. Liu C, Gao F, Li B, et al: TLR4 knockout protects mice from radiation-induced thymic lymphoma by downregulation of IL6 and miR-21. Leukemia 25: 1516-1519, 2011.
21. Lucas K and Maes M: Role of the Toll like receptor (TLR) radical cycle in chronic inflammation: possible treatments targeting the TLR4 pathway. Mol Neurobiol 48: 190-204, 2013.
22. Schaue D and McBride WH: Links between innate immunity and normal tissue radiobiology. Radiat Res 173: 406-417, 2010.
23. Wang FP, Li L, Li J, Wang JY, Wang LY and Jiang W: High mobility group box-1 promotes the proliferation and migration of hepatic stellate cells via TLR4-dependent signal pathways of PI3K/Akt and JNK. PLoS One 8: e64373, 2013.
24. Andersson U and Tracey KJ: HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 29: 139-162, 2011.
25. Weng H, Deng Y, Xie Y, Liu H and Gong F: Expression and significance of HMGB1, TLR4 and NF-κB p65 in human epidermal tumors. BMC Cancer 13: 311, 2013.
26. Mittal D, Saccheri F, Venereau E, Pusterla T, Bianchi ME and Rescigno M: TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. EMBO J 29: 2242-2252, 2010.
27. Ermakov AV, Konkova MS, Kostyuk SV, Egolina NA, Efremova LV and Veiko NN: Oxidative stress as a significant factor for development of an adaptive response in irradiated and nonirradiated human lymphocytes after inducing the bystander effect by low-dose X-radiation. Mutat Res 669: 155-161, 2009.
28. Kostyuk SV, Ermakov AV, Alekseeva AY, et al: Role of extracellular DNA oxidative modification in radiation induced bystander effects in human endotheliocytes. Mutat Res 729: 52-60, 2012.
29. Ichikawa S, Miyake M, Fujii R and Konishi Y: MyD88 associated ROS generation is crucial for Lactobacillus induced IL-12 production in macrophage. PLoS One 7: e35880, 2012.
30. Fiedler K, Kokai E, Bresch S and Brunner C: MyD88 is involved in myeloid as well as lymphoid hematopoiesis independent of the presence of a pathogen. Am J Blood Res 3: 124-140, 2013.
31. Windheim M, Stafford M, Peggie M and Cohen P: Interleukin-1 (IL-1) induces the Lys63-linked polyubiquitination of IL-1 receptor-associated kinase 1 to facilitate NEMO binding and the activation of IkappaBalpha kinase. Mol Cell Biol 28: 1783-1791, 2008.
32. Xiao Z, Visentin GP, Dayananda KM and Neelamegham S: Immune complexes formed following the binding of anti-platelet factor 4 (CXCL4) antibodies to CXCL4 stimulate human neutrophil activation and cell adhesion. Blood 112: 1091-1100, 2008.
33. Kasper B, Brandt E, Brandau S and Petersen F: Platelet factor 4 (CXC chemokine ligand 4) differentially regulates respiratory burst, survival, and cytokine expression of human monocytes by using distinct signaling pathways. J Immunol 179: 2584-2591, 2007.
34. Narang H and Krishna M: Mitogen-activated protein kinases: specificity of response to dose of ionizing radiation in liver. J Radiat Res 45: 213-220, 2004.
35. Rizvi A, Pecaut MJ, Slater JM, Subramaniam S and Gridley DS: Low-dose γ-rays modify CD4(+) T cell signalling response to simulated solar particle event protons in a mouse model. Int J Radiat Biol 87: 24-35, 2011.
36. Kim CS, Kim JM, Nam SY, et al: Low-dose of ionizing radiation enhances cell proliferation via transient ERK1/2 and p38 activation in normal human lung fibroblasts. J Radiat Res 48: 407-415, 2007.
37. Liang X, So YH, Cui J, et al: The low-dose ionizing radiation stimulates cell proliferation via activation of the MAPK/ERK pathway in rat cultured mesenchymal stem cells. J Radiat Res 52: 380-386, 2011.
38. Tsukimoto M, Homma T, Mutou Y and Kojima S: 0.5 Gy gamma radiation suppresses production of TNF-alpha through up-regulation of MKP-1 in mouse macrophage RAW264.7 cells. Radiat Res 171: 219-224, 2009.
39. Lödermann B, Wunderlich R, Frey S, et al: Low dose ionising radiation leads to a NF-κB dependent decreased secretion of active IL-1β by activated macrophages with a discontinuous dose-dependency. Int J Radiat Biol 88: 727-734, 2012.
40. Turtoi A, Brown I, Oskamp D and Schneeweiss FH: Early gene expression in human lymphocytes after gamma-irradiation-a genetic pattern with potential for biodosimetry. Int J Radiat Biol 84: 375-387, 2008.
41. Brengues M, Paap B, Bittner M, et al: Biodosimetry on small blood volume using gene expression assay. Health Physics 98: 179-185, 2010.
42. Kabacik S, Mackay A, Tamber N, et al: Gene expression following ionising radiation: identification of biomarkers for dose estimation and prediction of individual response. Int J Radiat Biol 87: 115-129, 2011.
43. Mayer C, Popanda O, Greve B, et al: A radiation-induced gene expression signature as a tool to predict acute radiotherapy-induced adverse side effects. Cancer Lett 302: 20-28, 2011.
44. Riecke A, Rufa CG, Cordes M, Hartmann J, Meineke V and Abend M: Gene expression comparisons performed for biodosimetry purposes on in vitro peripheral blood cellular subsets and irradiated individuals. Radiat Res 178: 234-243, 2012.
45. Rashi-Elkeles S, Elkon R, Shavit S, et al: Transcriptional modulation induced by ionizing radiation: p53 remains a central player. Mol Oncol 5: 336-348, 2011.
46. Wagner EF and Nebreda AR: Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 9: 537-549, 2009.