Single or fractionated irradiations of mice with low doses of X-rays stimulate innate immune mechanisms

International Journal of Low Radiation

Volumn 6, Issue 4, 2009, Pages 325-342

  Cheda, Aneta ^a   Nowosielska, Ewa ^a   Wrembel Wargocka, Jolanta ^a   Janiak, Marek K ^a  

^a MILITARY INSTITUTE OF HYGIENE AND EPIDEMIOLOGY   (Poland)

Author keywords

Anti tumour activity; Cytotoxicity; Fractionated irradiation; Immune mechanisms; Low dose X rays; Low radiation; Macrophages; NK cells; Single irradiation

Indexed keywords

FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; IMMUNOSTIMULATION; INNATE IMMUNITY; IRRADIATION; LOW ENERGY RADIATION; LUNG TUMOR; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN SYNTHESIS; RADIATION DOSE; RADIATION EXPOSURE; WHOLE BODY RADIATION; X RAY;

EID: 70450227402     PISSN: 14776545     EISSN: 17419190     Source Type: Journal    
DOI: 10.1504/IJLR.2009.029312     Document Type: Article

References (78)

1. Al-Sarireh, B. and Eremin, O. (2000) 'Tumour-Associated Macrophages (TAMS): disordered function, immune suppression and progressive tumour growth', J. R. Coll. Surg. Edinb., Vol. 45, pp.1-16.
2. Bai, O., Liu, S.Z. and Mu, Y. (1998) 'Effect of low dose radiation on Th1 and Th2 of thymocytes and splenocytes in mice', Chin. J. Radiol. Med. Prot., Vol. 18, pp.106-109.
3. Barao, I. and Ascensao, J.L. (1998) 'Human natural killer cells', Arch. Immunol. Ther. Exp., Vol. 46, pp.213-229.
4. Belardelli, F. and Ferrantini, M. (2002) 'Cytokines as a link between innate and adaptive antitumour immunity', Trends. Immunol., Vol. 23, pp.201-208.
5. Bergmann-Leitner, E.S. and Abrams, S.I. (2000) 'Differential role of Fas/Fas ligand interactions in cytolysis of primary and metastatic colon carcinoma cell lines by human antigen-specific CD81 CTL', J. Immunol., Vol. 164, pp.4941-4954.
6. Berrington, A., Darby, S.C., Weiss, H.A. and Doll, R. (2001) '100 years of observation on British radiologists: mortality from cancer and other causes 1897-1997', Br. J. Radiol., Vol. 74, pp.507-519.
7. Cai, L. (1999) 'Research of the adaptive response induced by low-dose radiation: where have we been and where should we go?', Hum. Exp. Toxicol., Vol. 18, pp.419-425.
8. Caldwell, S.A., Ryan, M.H., McDuffie, E. and Abrams, S.I. (2003) 'The Fas/Fas ligand pathway is important for optimal tumor regression in a mouse model of CTL adoptive immunotherapy of experimental CMS4 lung metastases', J. Immunol., Vol. 171, pp.2402-2412.
9. Caratero, A., Courtade, M., Bonnet, L., Planel, H. and Caratero, C. (1998) 'Effect of a continuous gamma irradiation at a very low dose on the life span of mice', Gerontology, Vol. 44, pp.272-276.
10. Cardis, E., Gilbert, E.S., Carpenter, L., Howe, G., Kato, I., Armstrong, K., Beral, V., Cowper, G. and Douglas, A. (1995) 'Effects of low doses and low dose rates of external ionizing radiation: cancer mortality among nuclear industry workers in three countries', Radiat. Res., Vol. 142, pp.117-132.
11. Cheda, A., Wrembel-Wargocka, J., Lisiak, E., Marciniak, M., Nowosielska, E.M. and Janiak, M.K. (2004a) 'Inhibition of the development of pulmonary tumor nodules and stimulation of the activity of NK cells and macrophages in mice by single low doses of low-LET radiation', Int. J. Low Radiation, Vol. 1, pp.171-179.
12. Cheda, A., Wrembel-Wargocka, J., Lisiak, E., Nowosielska, E.M., Marciniak, M. and Janiak, M.K. (2004b) 'Single low doses of X-rays inhibit the development of experimental tumor metastases and trigger the activities of NK cells in mice', Radiat. Res., Vol. 161, pp.335-340.
13. Cheda, A., Wrembel-Wargocka, J., Nowosielska, E.M. and Janiak, M.K. (2006) 'Immune mechanism of the retarded growth of tumor nodules in mice exposed to single low-level irradiations with X-rays', Centr. Eur. J. Immunol., Vol. 31, pp.44-50.
14. Chen, W.L., Luan, Y.C., Shieh, M.C., Chen, S.T., Kung, H.T., Soong, K.L., Yeh, Y.C., et al. (2004) 'Is chronic radiation an effective prophylaxis against cancer?', J. Am. Physicians. Surg., Vol. 9, pp.6-10.
15. Cohen, B.L. (1995) 'Test the linear-no threshold theory of radiation carcinogenesis for inhaled radon decay products', Health Phys., Vol. 86, pp.157-174.
16. Cohen, B.L. (1997) 'Problems in the radon vs lung cancer test of linear no-threshold theory and a procedure for resolving them', Health Phys., Vol. 72, pp.623-628.
17. Cui, S., Reichner, J.S., Mateo, R.B. and Albina, J.E. (1994) 'Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or -independent mechanisms', Cancer Res., Vol. 54, pp.2462-2467.
18. DeBlaker-Hohe, D.F., Yamauchi, A., Yu, C.R., Horvath-Arcidiacono, J.A. and Bloom, E.T. (1995) 'IL-12 synergises with IL-2 to induce lymphokine-activated cytotoxicity and perforin and granzyme gene expression in fresh human NK cells', Cell Immunol., Vol. 165, pp.33-43.
19. Farias-Eisner, R., Sherman, M.P., Aeberhard, E. and Chaudhuri, G. (1994) 'Nitric oxide is an important mediator for tumoricidal activity in vivo', Proc. Natl. Acad. Sci. USA, Vol. 91, pp.9407-9411.
20. Frank, J., Born, K., Barker, J.H. and Marzi, I. (2003) 'In vivo effect of tumor necrosis factor alpha on wound angiogenesis and epithelialization', Eur. J. Trauma., Vol. 29, pp.208-219.
21. Fu, H., Li, X., Chen, Y., Zhang, Y. and Liu, S.Z. (1997) 'Mechanism of suppressive effect of low dose radiation on cancer cell dissemination in mice', J. Radiat. Res. Radiat. Process., Vol. 15, pp.40-43.
22. Fu, H., Li, X., Li, Y. and Liu, S.Z. (1996) 'Whole-body low dose irradiation suppresses cancer cell dissemination in mice', Chin. J. Radiol. Med. Prot., Vol. 16, pp.307-309.
23. Gong, S., Liu, J., Liu, S., Zhang, Y. and Liu, S.Z. (1997) 'Effect of splenocyte extracellular fluid irradiated with low dose X-rays on thymocyte apoptosis after larger dose X-irradiation in mice', J. Radiat. Res. Radiat. Process., Vol. 15, pp.36-39.
24. Harhaji, L., Vuckovic, O., Miljkovic, D., stosic-Grujicic, S. and Trajkovic, V. (2004) 'Iron down-regulated macrophage anti-tumour activity by blocking nitric oxide production', Clin. Exp. Immunol., Vol. 137, pp.109-116.
25. Harrington, N.P., Chambers, K.A., Ross, W.M. and Filion, L.G. (1997) 'Radiation damage and immune suppression in splenic mononuclear cell populations', Clin. Exp. Immunol., Vol. 107, pp.417-424.
26. Hashimoto, S., Shirato, H., Hosokawa, M., Nishioka, T., Kuramitsu, Y., Matushita, K., Kobayashi, M. and Miyasaka, K. (1999) 'The suppression of metastases and the change in host immune response after low-dose total-body irradiation in tumor-bearing rats', Radiat. Res., Vol. 151, pp.717-724.
27. Hosoi, Y. and Sakamoto, K. (1993) 'Suppressive effect of low dose total body irradiation on lung metastasis: dose dependency and effective period', Radiother. Oncol., Vol. 26, pp.177-179.
28. Ibuki, Y. and Goto, R. (1995) 'Augmentation of NO production and cytolytic activity of Mφ obtained from mice irradiated with a low dose of γ-rays', J. Radiat. Res., Vol. 36, pp.209-220.
29. Ibuki, Y. and Goto, R. (1997) 'Enhancement of NO production from resident peritoneal macrophages by in vitro gamma-irradiation and its relationship to reactive oxygen intermediates', Free Radic. Biol. Med., Vol. 22, pp.1029-1035.
30. Ibuki, Y. and Goto, R. (1999) 'Contribution of inflammatory cytokine release to activation of resident peritoneal macrophages after in vivo low-dose γ-irradiation', J. Radiat. Res., Vol. 40, pp.253-262.
31. Ina, Y. and Sakai, K. (2004) 'Prolongation of life span associated with immunological modification by chronic low-dose-rate irradiation in MRL-lpr/lpr mice', Radiat. Res., Vol. 16, pp.168-173.
32. Ina, Y. and Sakai, K. (2005a) 'Activation of immunological network by chronic low-dose-rate irradiation in wild-type mouse strains; Analysis of immune cell populations surface molecules', Int. J. Radiat. Biol., Vol. 81, pp.721-729.
33. Ina, Y. and Sakai, K. (2005b) 'Further study on prolongation of life span associated with immunological modification by chronic low-dose-rate irradiation in MRL-lpr/lpr mice: effects of whole-life irradiation', Radiat. Res., Vol. 163, pp.418-423.
34. Ina, Y., Tanooka, H., Yamada, T. and Sakai, K. (2005) 'Suppression of thymic lymphoma induction by life-long low-dose-rate irradiation accompanied by immune activation in C57BL/6 mice', Radiat. Res., Vol. 163, pp.153-158.
35. Ishii, K., Hosoi, Y., Yamada, S., Ono, T. and Sakamoto, K. (1996) 'Decreased incidence of thymic lymphoma in AKR mice as a result of chronic, fractionated low-dose total-body X irradiation', Radiat. Res., Vol. 146, pp.582-585.
36. Jagger, J. (1998) 'Natural background radiation and cancer death in Rocky Mountain states and Gulf Coast states', Health Phys., Vol. 7, pp.428-430.
37. Janik, P., Bertram, J.S. and Szaniawska, B. (1981) 'Modulation of lung tumour colony formation by a subcutaneously growing tumour', J. Natl. Cancer Inst., Vol. 66, pp.1155-1158.
38. Jenkins, D.C., Charles, I.G., Thomsen, L.L., Moss, D.W., Holmes, L.S., Baylis, S.A., Rhodes, P., Westmore, K., Emson, P.C. and Moncada, S. (1995) 'Roles of nitric oxide in tumor growth', Proc. Natl. Acad. Sci. USA, Vol. 92, pp.4392-4396.
39. Ju, G.Z., Liu, S.Z., Li, X.Y., Liu, W.H. and Fu, H.Q. (1995) 'Effect of high versus low dose radiation on the immune system', in U. Hagen, D. Harder, H. Jung and C. Streffer (Eds.) Radiation Research 1895-1995. Proc of the Tenth Int Congress of Radiation Research, IARR, Würzburg, Germany, pp.709-714.
40. Kataoka, T., Shinohara, N., Takayama, H., Takaku, K., Kondo, S., Yonehara, S. and Nagai, K. (1996) 'Concanamycin a, a powerful tool for characterization and estimation of contribution of perforyn- and Fas-based lytic pathways in cell-mediated cytotoxicity', J. Immunol., Vol. 156, pp.3678-3686.
41. Katayama, H., Matsuura, M., Enndo, S., Hosoi, M., Othaki, M. and Hayakawa, N. (2002) 'Reassessment of the cancer mortality risk among Hiroshima atomic-bomb survivors using a new dosimetry system, ABS2000D, compared with ABS93D', J. Radiat. Res., Vol. 43, pp.53-64.
42. Kesavan, P.C. (1997) 'Indian research on high levels of natural radiation: pertinent observations for further studies', in L. Wei, T. Sugahara and Z. Tao (Eds.) High Levels of Natural Radiation, 1996: Radiation Dose and Health Effects. Proc. of 4th International Conference on High Levels of Natural Radiation, Beijing, China/Amsterdam, The Netherlands: Elsevier pp.112-117.
43. Kojima, S., Ishida, H., Takahashi, M. and Yamaoka, K. (2002) 'Elevation of glutathione induced by low-dose gamma rays and its involvement in increased natural killer activity', Radiat. Res., Vol. 157, pp.275-280.
44. Kojima, S., Nakayama, K. and Ishida, H. (2004) 'Low dose γ-rays activate immune functions via induction of glutathione and delay tumor growth', J. Radiat. Res., Vol. 45, pp.33-39.
45. Lin, I.H., Hau, D.M., Chen, W.C. and Chen, K.T. (1996) 'Effects of low dose gamma-ray irradiation on peripheral leukocyte counts and spleen of mice', Chin. Med. J., Vol. 109, pp.210-214.
46. Little, M.P., Weiss, H.A. and Boice, J.D. (1999) 'Risks of leukemia in Japanese atomic bomb survivors, in women treated for cervical cancer, and in patients treated for ankylosing spondylitis', Radiat. Res., Vol. 152, pp.280-292.
47. Liu, S.Z. (2003a) 'Nonlinear dose-response relationship in the immune system following exposure to ionizing radiation: mechanisms and implications', Nonlinearity Biol. Toxicol. Med., Vol. 1, pp.71-92.
48. Liu, S.Z. (2003b) 'On radiation hormesis expressed in the immune system', Crit. Rev. Toxicol., Vol. 33, pp.431-441.
49. Liu, S.Z. (2004) 'Cancer control related to stimulation of immunity by low dose radiation', Proc. of 14th Pacific Basin Nuclear Conference, Honolulu, USA, American Nuclear Society, La Grange Park, Illinois, pp.368-372.
50. Liu, S.Z., Han, Z.B. and Liu, W.H. (1994a) 'Changes in lymphocyte reactivity to modulatory factors following low dose ionizing radiation', Biomed. Environ. Sci., Vol. 7, pp.130-135.
51. Liu, S.Z., Jin, S.Z., Liu, X.D. and Sun, Y.M. (2001) 'Role of CD28/B7 costimulation and IL-12/IL-10 interaction in the radiation-induced immune changes', BMI Immunology, Vol. 2, pp.8-15.
52. Liu, S.Z., Su, X., Zhang, Y.C. and Zhao, Y. (1994b) 'Signal transduction in lymphocytes after low dose radiation', Chin. Med. J., Vol. 107, pp.431-436.
53. Lord, S.J., Rajotte, R.V., Korbutt, G.S. and Blezckley, R.C. (2003) 'Granzyme B: a natural born killer', Immunol. Rev., Vol. 193, pp.31-38.
54. Luckey, T.D. (1999) 'Nurture with ionising radiation: a provocative hypothesis', Nutr. Cancer, Vol. 34, pp.1-11.
55. Miller, G.M., Kim, D.W., Andres, M.L., Green, L.M. and Gridley, D.S. (2003) 'Changes in the activation and reconstitution of lymphocytes resulting from total-body irradiation correlate with slowed tumor growth', Oncology, Vol. 65, pp.229-241.
56. Mitchel, R.E., Jackson, J.S., McCann, R.A. and Boreham, D.R. (1999) 'The adaptive response modifies latency for radiation-induced myeloid leukemia in CBAH mice', Radiat. Res., Vol. 152, pp.273-279.
57. Mitchel, R.E., Jackson, J.S., Morrison, D.P. and Carlisle, S.M. (2003) 'Low doses of radiation increase the latency of spontaneous lymphomas and spinal osteosarcomas in cancer-prone, radiation-sensitive Trp53 heterozygous mice', Radiat. Res., Vol. 159, pp.320-327.
58. Moretta, L., Ciccone, E., Poggi, A., Mingari, M.C. and Moretta, A. (1994) 'Origin and functions of human natural killer cells', Int. J. Clin. Lab. Res., Vol. 24, pp.181-186.
59. Nathan, C. (1991) 'Mechanisms and modulation of macrophage activation', Behrings Inst. Mitt., Vol. 88, pp.200-207.
60. Nowosielska, E.M., Cheda, A., Wrembel-Wargocka, J. and Janiak, M.K. (2008) 'Modulation of the growth of pulmonary tumour colonies in mice after single or fractionated low-level irradiations with X-rays', Nukleonika, Vol. 53, Suppl. 1, pp.S9-S15.
61. Nowosielska, E.M., Wrembel-Wargocka, J., Cheda, A. and Janiak, M.K. (2006a) 'A single low-dose irradiation with X-rays stimulates NK cells and macrophages to release factors related to the cytotoxic functions of these cells', Centr. Eur. J. Immunol., Vol. 31, pp.51-57.
62. Nowosielska, E.M., Wrembel-Wargocka, J., Cheda, A., Lisiak, E. and Janiak, M.K. (2005) 'Low-level exposures to ionising radiation modulate the anti-tumour activity of murine NK cells', Nukleonika, Vol. 50, Suppl. 2, pp.S21-S24.
63. Nowosielska, E.M., Wrembel-Wargocka, J., Cheda, A., Lisiak, E. and Janiak, M.K. (2006b) 'Enhanced cytotoxic activity of macrophages and suppressed tumor metastases in mice irradiated with low doses of X- rays', J. Radiat. Res., Vol. 47, pp.229-236.
64. Pandey, R., Shankar, B.S., Sharma, D. and Sainis, K.B. (2005) 'Low dose radiation induced immunomodulation: effect on macrophages and CD8+ T cells', Int. J. Radiat. Biol., Vol. 81, pp.801-812.
65. Pierce, D.A., Shimizu, Y., Preston, D.L., Vaeth, M. and Mabuchi, K. (1996) 'Studies of the mortality of atomic bomb survivors. Report 12, Part I Cancer: 1950-1990', Radiat. Res., Vol. 146, pp.1-27.
66. Reyburn, H., Mandelboim, O., Vales-Gomez, M., Sheu, E.G., Pazmany, L., Davis, D.M. and Strominger, J.L. (1997) 'Human NK cells: their ligands, receptors and functions', Immunol. Rev., Vol. 155, pp.119-125. (Pubitemid 27076063)
67. Safwat, A. (2000) 'The immunology of low-dose total-body irradiation: more questions than answers', Radiat. Res., Vol. 153, pp.599-604.
68. Sakai, K., Hosoi, Y., Nokamura, T., Oda, T., Iwasaki, T. and Yamada, T. (2003) 'Suppression of carcinogenic processes in mice by chronic low doses rate gamma-irradiation', Int. J. Low Radiation, Vol. 1, pp.142-146.
69. Shan, Y.X., Jin, S.Z., Liu, X.D., Liu, Y. and Liu, S.Z. (2007) 'Ionizing radiation stimulates secretion of pro-inflammatory cytokines: dose-response relationship, mechanisms and implications', Radit. Environ. Biophys., Vol. 46, pp.21-29.
70. Smyth, M.J., Cretney, E., Kelly, J.M., Westwood, J.A., Street, S.E., Yagita, H., Takeda, K., van Dommelen, S.L., Degli-Esposti, M.A. and Hayakawa, Y. (2005) 'Activation of NK cell cytotoxicity', Mol. Immunol., Vol. 42, pp.501-510.
71. Wang, Z., Lubin, J.H., Wang, L., Zhang, S., Boice, J.D., Cui, H., Zhang, S., et al. (2002) 'Residential radon and lung cancer risk in a high-exposure area of Gansu Province', China. Am. J. Epidemiol., Vol. 155, pp.554-564.
72. Wei, L. and Sugahara, T. (2000) 'An introductory overview of the epidemiological study on the population at the high background radiation areas in Yangjiang, China', J. Radiat. Res., Vol. 41, Suppl., pp.1-7.
73. Xie, K. and Fidler, I.J. (1998) 'Therapy of cancer metastasis by activation of the inducible nitric oxide synthase', Cancer Met. Rev., Vol. 17, pp.55-75.
74. Young, H.A. and Ortaldo, J. (2006) 'Cytokines as critical co-stimulatory molecules in modulating the immune response of natural killer cells', Cell Res., Vol. 16, pp.20-24. (Pubitemid 43129305)
75. Zhang, M., Chen, Z. and Liu, S.Z. (1996) 'Effects of low dose irradiation on the splenic macrophage function in mice', J. N. Bethune Univ. Med. Sci., Vol. 22, pp.131-133.
76. Zhang, Y., Li, X., Li, X. and Liu, S.Z. (1999) 'Stimulatory effect of low dose radiation on the immune function in tumor-bearing mice', J. N. Bethune Univ. Med. Sci., Vol. 25, pp.592-594.
77. Zhang, Y., Sun, Y., Li, X., Mu, Y. and Liu, S.Z. (1998a) 'An experimental study on the enhanced macrophage (M#) function in tumor-bearing mice treated with low dose radiation', J. Radiat. Res. Radiat. Proces., Vol. 16, pp.249-252.
78. Zhang, Y., Sun, Y., Li, X., Mu, Y. and Liu, S.Z. (1998b) 'Low dose radiation increases the mRNA transcriptional levels of IL-1beta and TNF-alpha in peritoneal macrophages of tumor-bearing mice', J. N. Bethune Univ. Med. Sci., Vol. 24, pp.565-567.