Foxp3+-treg cells enhanced by repeated low-dose gamma-irradiation attenuate ovalbumin-induced allergic asthma in mice

Radiation Research

Volumn 179, Issue 5, 2013, Pages 570-583

  Park, Bum Soo ^a   Hong, Gwan Ui ^a   Ro, Jai Youl ^a  

^a Sungkyunkwan University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CESIUM 137; CHEMOKINE RECEPTOR CCR2; COLLAGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 35; OVALBUMIN; OX40 LIGAND; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR RUNX1; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC AIRWAY INFLAMMATION; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL MIGRATION; DISEASE EXACERBATION; ENZYME ACTIVITY; FEMALE; GAMMA IRRADIATION; GOBLET CELL; INFLAMMATORY CELL; LUNG PARENCHYMA; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION RESPONSE; RADIOSENSITIZATION; RESPIRATORY TRACT ALLERGY; WHOLE BODY RADIATION;

ANIMALS; ANTIBODY SPECIFICITY; ASTHMA; BONE MARROW CELLS; BRONCHOALVEOLAR LAVAGE FLUID; CELL SIZE; CHEMOKINES; DOSE-RESPONSE RELATIONSHIP, RADIATION; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GAMMA RAYS; GENE EXPRESSION REGULATION; HISTONES; HYPERSENSITIVITY; IMMUNOGLOBULIN E; LUNG; MAST CELLS; MICE; MICE, INBRED C57BL; NF-KAPPA B; ORGAN SPECIFICITY; OVALBUMIN; OX40 LIGAND; PROTEIN TRANSPORT; RECEPTORS, CHEMOKINE; RECEPTORS, OX40; RNA, MESSENGER; SPLEEN; T-LYMPHOCYTES, REGULATORY; TRANSCRIPTION FACTOR AP-1;

MUS;

EID: 84876974920     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR3082.1     Document Type: Article

References (63)

1. Luckey TD, Lawrence KS. Radiation hormesis: the good, the bad, and the ugly. Dose Response 2006; 9:169-90.
2. Rho HS, Park SS, Lee CE. Gamma irradiation up-regulates expression of B cell differentiation molecule CD23 by NF-kappaB activation. J Biochem Mol Biol 2004; 37 (4):507-14.
3. Bogdándri EN, Balogh A, Felgyinszki N, et al. Effects of low-dose radiation on the immune system of mice after total-body irradiation. Radiat Res 2010; 174:450-89.
4. Safwat A. The role of low-dose total body irradiation in treatment of non-Hodgkin's lymphoma: a new look at an old method. Radiother Oncol 2000; 56:1-8. (Pubitemid 30408379)
5. Luckey TD. Low dose irradiation as a treatment for gingivitis. Med Hypoth 2006; 66(4): 695-7. (Pubitemid 43181614)
6. Tanaka T, Tago F, Fang SP, Shimura N, Kojima S. Repeated 0.5-Gy gamma-ray irradiation attenuates autoimmune manifestations in MRL-lpr/lpr mice. Int J Radiat Biol 2005; 81(10):731-40. (Pubitemid 43200508)
7. Tsukimoto M, Nakatsukasa H, Sugawara K, Yamashita K, Kojima S. Repeated 0.5-Gy c irradiation attenuates experimental autoimmune encephalomyelitis with up-regulation of regulatory T cells and suppression of IL-17 production. Radiat Res 2008; 17:429-36.
8. Nakatsukasa H, Tsukimoto M, Tokunaga A, Kojima S. Repeated gamma irradiation attenuates collage-induced arthritis via upregulation of regulatory T cells but not by damaging lymphocytes directly. Radiat Res 2010; 174:313-24.
9. Kachikwu EK, Iwamoto KS, Liao Y-P, et al. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys 2011; 81 (4):1128-35.
10. Seo JH, Kim JH, Lee JW, Yoo YC, Kim MR, Park KS, et al. Ovalbumin modified by gamma irradiation alters its immunological functions and allergic responses. Int Immunopharma 2007; 7(4):464-72. (Pubitemid 46275554)
11. Fang SP, Tago F, Tanaka T, Simura N, Muto Y, Goto R, et al. Repeated irradiations with gamma-rays at a dose of 0.5 Gy may exacerbate asthma. J Radiat Res 2005; 46:151-6. (Pubitemid 41190650)
12. Voisard R, Wiegmann D, Baur R, Hombach V, Kamenz J. Lowdose irradiation stimulates TNF-alpha-induced ICAM-1 mRNA expression in human coronary vascular cells. Med Sci Monit 2007; 13(5):107-11.
13. Shin SC, Lee K-M, Kang YM, Kim K, Kim CS, Yang KH, et al. Alteration of cytokine profiles in mice exposed to chronic lowdose ionized radiation. Biochem Biophys Res Com 2010; 397:644-9.
14. Zhou Y, Xia L, He ZS, Ouyang W, Xie CH. Modulation of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in RAW264.7 cells by irradiation. Mol Med Report 2010; 3(5): 809-13.
15. Joo HM, Nam SY, Yang KH, Kim CS, Jin YW, Kim JY. The effects of low-dose ionized radiation in the activated rat basophilic leukemia (RBL-2H3) mast cells. J Biol Chem 2012. DOI/10.1074.jbc.m112.378497.
16. Shum BO, Rolph MS, Sewell WA. Mechanisms in allergic airway inflammation-lessons from studies in the mouse. Expert Rev Mol Med 2008; 27:10-5.
17. Zimmermann N, Hershey GK, Foster PS, Rothenberg ME. Chemokines in asthma: Cooperative interaction between chemokines and IL-13. J Allergy Clin Immunol 2003; 111:227-42.
18. Kim DY, Park BS, Hong GU, Lee BJ, Park JW, Kim SY, et al. Anti-inflammatory effects of R2 peptide on OVA-specific allergic asthma in mice. Br J Pharmacol 2011; 162:210-25.
19. Collington SJ, Hallgren J, Pease JE, Jones TG, Rollins BJ, Westwick J, et al. The role of the CCL2/CCR2 axis in mouse mast cell migration in vitro and in vivo. J Immunol 2010; 184:6114-23.
20. Sun L, Louie MC, Vannella KM, Wilke CA, LeVine ML, Moore BB, et al. New concepts of IL-10-induced lung fibrosis: fibrocyte recruitment and M2 activation in a CCL2/CCR2 axis. Am J Physiol Lung Cell Mol Physiol 2011; 300:L341-53.
21. Ring S, Schafer SC, Mahnke K, Lehr HA, Enk AH. CD4\+ CD25\+ regulatory T cells suppress contact hypersensitivity reactions by blocking influx of effector T cells into inflamed tissue. Eur J Immunol 2006; 36:2981-92. (Pubitemid 44782572)
22. Meiler F, Klunker S, Zimmermann M, Akdis CA, Akdis M. Distinct regulation of IgE, IgG4 and IgA by T regulatory cells and toll-like receptors. Allergy 2008; 63:1455-63.
23. Lloyd CM, Hawrylowicz CM. Regulatory T cells in asthma. Immunity 2009; 31:438-49.
24. Robinson DS. Regulatory T cells and asthma. Clin Exp Allergy 2009; 39:1314-23.
25. Palomares O, Yaman G, Azkur AK, Akkoc T, Akdis M, Akdis CA. Role of Treg in immune regulation of allergic diseases. Eur J Immunol 2010; 40:1232-40.
26. Poojary KV, Kong YM, Farrar MA. Control of Th2-mediated inflammation by regulatory T cells. Am J Pathol 2010; 177:525-3.
27. Piconese S, Gri G, Tripodo C, Musio S, Gorzanelli A, Frossi B, et al. Mast cells counteract regulatory T-cell suppression through interleukin-6 and OX40/OX40L axis toward Th17-cell differentiation. Blood 2009; 114 (13):2639-48.
28. Gri G, Piconese S, Frossi B, Manfroi V, Merluzzi S, Tripodo C, et al. CD4\+ CD25\+ regulatory T cells suppress mast cell degranulation and allergic responses through OX40-Ox40L interaction. Immunity 2010; 29:771-81.
29. Klunker S, Chong MMW, Mantel P-Y, Palomares O, Bassin C, Ziegler M, et al. Transcription factors RUNX1 and RUNX3 in the induction and suppressive function of Foxp3\+ inducible regulatory T cells. J Exp Med 2009; 206:2701-15.
30. Long M, Park S-G, Strickland I, Hayden MS, Ghosh S. Nuclear factor-jB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity 2009; 31:921-31.
31. Kim DY, Jeoung D, Ro JY. Signaling pathways in the activation of mast cells co-cultured with astrocytes and colocalization of both cells in experimental allergic encephalomyelitis. J Immunol 2010; 185:273-83.
32. Kim JS, Kim DY, Lee JK, Ro JY, Chung MH. 8-oxo-20-de3oxyguanosine suppresses allergy-induced lung tissue remodeling in mice. Eur J Pharmacol 2011; 651:218-26.
33. Pecaut MJ, Gridley DS, Smith AL, Nelson GA. Dose and dose rate effects of whole-body proton-irradiation on lymphocyte blastogenesis and hematological variables: part II. Immunol Lett 2002; 80:67-73. (Pubitemid 33096317)
34. Manirarora JN, Kosiewicz MM, Parnell SA, Alard P. APC activation restores functional CD4(\+)CD25(\+) regulatory T cells in NOD mice that can prevent diabetes development. PLoS ONE 2008; 3(11):e3739.
35. Neurauter AA, Bonyhadi M, Lien E, Nokleby L, Ruud E, Camacho S, et al. Cell isolation and expression using Dynabeads. Adv Biochem Eng Biotechnol 2007; 106:41-73.
36. Begum N, Prasad NR, Kanimozhi G, Hasan AQ. Apigenin ameliorates gamma radiation-induced cytogenetic alterations in cultured human blood lymphocytes. Mutat Res 2012; 747:71-6.
37. Ribatti D, Nico B, Finato N, Crivellato E, Beltrami CA. Colocalization of tryptase and cathepsin-G in mast cells in cutaneous mastocytosis. Cancer Lett 2009; 279(2):209-12.
38. Ivashkevich A, Redon CE, Nakamura AJ, Martin RF, Martin OA. Use of the c-H2AX assay to monitor DNA damage and repair in translational cancer research. Cancer Lett 2012; 327:123-33.
39. Plager DA, Loegering DA, Checkel JL, Tang J, Kephart GM, Caffes PL, et al. Major basic protein homolog (MBP2): A specific human eosinophil marker. J Immunol 2006; 177:7340-5. (Pubitemid 44715104)
40. Kirstein F, Horsnell WGC, Kuperman DA, Huang X, Erle DJ, Lopata AL, et al. Expression of IL-4 receptor a on smooth muscle cells is not necessary for development of experimental allergic asthma. J Allergy Clin Immunol 2010; 126:347-54.
41. Makinde T, Murphy RF, Agrawal DK. The regulatory role of TGF-beta in airway remodeling in asthma. Immunol Cell Biol 2007; 85:348-56. (Pubitemid 47035605)
42. Von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005; 6:338-44. (Pubitemid 41716770)
43. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-8.
44. Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH, et al. IOD activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 2009; 183:2475-85.
45. Burchill MA, Yang J, Vang KB, Farrar MA. Interleukin-2 receptor signaling in regulatory T cells development and homeostasis. Immuol Lett 2007; 114:1-8.
46. Collison LW, Pillal MR, Chaturvedi V, Vignali DA. Regulatory T cells suppression is potentiated by target T cells I a cell contact, IL-35-and IL-10-dependent manner. J Immunol 2009; 182:6121-8.
47. Collison LW, Chaturvedi V, Henderson AL, Giacomin PR, Guy C, Bankoti J, et al. IL-35-mediated induction of a potent regulatory T cell population. Nat Immunol 2010; 11(12):1093-102.
48. Cao M, Cabrera R, Xu Y, et al. Different radiosensitivity of CD4(\+)CD25(\+) regulatory T cells and effector T cells to low dose gamma irradiation in vitro. Int J Radiat Biol 2011; 87(1): 71-80.
49. Moo-Young TA, Larson JW, Belt BA, Tan MC, Hawkins WG, Eberlein TJ, et al. Tumor-derived TGF-beta mediates conversion of CD4\+Foxp3\+ regulatory T cells in a murine model of pancreas cancer. J Immunother 2009; 32:12-21.
50. Zheng SG, Wang J, Wang P, Gray JD, Horwitz DA. IL-2 is essential for TGF-beta to convert naive CD4\+CD25-cells to CD25\+Foxp3\+ regulatory T cells and for expansion of these cells. J Immunol 2007; 78:2018-27. (Pubitemid 46233398)
51. Schuliga M, Ong SC, Soon L, Zal F, Harris T, Stewart AG. Airway smooth muscle remodels pericellular collagen fibrils: implications for proliferation. Am J Physiol Lung Cell Mol Physiol 2010; 298 (4):584-92.
52. Min HJ, Won HY, Kim YC, Sung SH, Byun MR, Hwang JH, et al. Suppression of Th2-driven, allergen-induced airway inflammation by sauchinone. Biochem Biophys Res Commun 2009; 385(2): 204-9.
53. Edwards MR, Bartlett NW, Clarke D, Birrell M, Belvisi M, Johnston SL. Targeting the NF-kappaB pathway in asthma and chronic obstructive pulmonary disease. Pharmacol Ther 2009; 121(1):1-13.
54. Sheller JR, Polosukhin VV, Mitchell D, Cheng DS, Peebles RS, Blackwell TS. Nuclear factor kappa B induction in airway epithelium increases lung inflammation in allergen-challenged mice. Exp Lung Res 2009; 35(10): 883-95.
55. Akdis M, Verhagen J, Taylor A, Karamloo F, Karagiannidis C, Crameri R, et al. Immune responses in health and allergic individuals are characterized by a fine balance between allergenspecific T regulatory 1 and T helper 2 cells. J Exp Med 2004; 199:1567-75. (Pubitemid 38780411)
56. Jabara HH, Geha RS. Jun N-terminal kinase is essential for CD40-mediated IgE class switching in B cells. J Allergy Clin Immunol 2005; 115(4):856-63. (Pubitemid 40460865)
57. Holgate S, Smith N, Massanari M, Jimenez P. Effects of omalizumab on markers of inflammation in patients with allergic asthma. Allergy 2009; 12:1728-36.
58. Hinz D, Simon JC, Maier-Simon C, Milkova L, Roder S, Sack U, et al. Reduced maternal regulatory T cell numbers and increased T helper type 2 cytokine production are associated with elevated levels of immunoglobulin E in cord blood. Clin Exp Allergy 2010; 40:419-26.
59. Scherf W, Burdach S, Hansen G. Reduced expression of transforming growth factor beta 1 exacerbates pathology in an experimental asthma model. Eur J Immunol 2005; 35:198-206. (Pubitemid 40123866)
60. Joetham A, Takada K, Taube C, Miyahara N, Matsubara S, Koya T, et al. Naturally occurring lung CD4\+CD25\+ T cell regulation of airway allergic responses depends on IL-10 induction of TGF-beta. J Immuol 2007; 178:1433-42. (Pubitemid 46154614)
61. O'Garra A, Barrat FJ, Castro AG, Vicari A, Hawrylowicz G. Strategies for use of IL-10 or its antagonists in human disease. Immunol Rev 2008; 223:114-31. (Pubitemid 351986180)
62. Kearley J, Robinson DS, Lloyd CM. CD4\+CD25\+ regulatory T cells reverse established allergic airway inflammation and prevent airway remodeling. J Allergy Clin Immunol 2008; 122:617-24.
63. Jones TG, Finkelman FD, Austen KF, Gurish MF. T regulatory cells control antigen-induced recruitment of mast cell progenitors to the lung of C57BL/6 mice. J Immunol 2010; 185:1804-11.