An adoptive transfer method to detect low-dose radiation-induced bystander effects in vivo

Radiation Research

Volumn 173, Issue 2, 2010, Pages 125-137

  Blyth, Benjamin J ^a   Azzam, Edouard I ^b   Howell, Roger W ^b   Ormsby, Rebecca J ^a   Staudacher, Alexander H ^a   Sykes, Pamela J ^a,c  

^a FLINDERS UNIVERSITY   (Australia)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c FLINDERS MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

THYMIDINE; THYMIDINE H 3; TRITIUM; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CELL PROLIFERATION; CONTROLLED STUDY; EX VIVO STUDY; FEMALE; IN VIVO STUDY; ISOTOPE LABELING; LOW ENERGY RADIATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION; RADIATION DOSE; SPLEEN; SPLEEN CELL; T LYMPHOCYTE; X RAY;

ANIMALS; BYSTANDER EFFECT; DOSE-RESPONSE RELATIONSHIP, RADIATION; FEMALE; FLUORESCENT DYES; LYMPHOCYTES; MALE; MICE; MICE, INBRED C57BL; SPLEEN; THYMIDINE;

MUS;

EID: 75149147630     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR1899.1     Document Type: Article

References (76)

1. D. A. Pierce and D. L. Preston, Radiation-related cancer risks at low doses among atomic bomb survivors. Radiat. Res. 154, 178-186 (2000).
2. D. L. Preston, E. Ron, S. Tokuoka, S. Funamoto, N. Nishi, M. Soda, K. Mabuchi and K. Kodama, Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat. Res. 168, 1-64 (2007).
3. National Research Council, Committee to Assess Health Risks from Exposure to Low Levels of Ionizing Radiation, Health Risks from Exposure to Low Levels of Ionizing Radiation: BEIR VII-Phase 2. National Academies Press, Washington, DC, 2006
4. ICRP, Low-Dose Extrapolation of Radiation Related Cancer Risk. Publication 99, Annals of the ICRP, Vol.35, Elsevier, Amsterdam, 2006.
5. UNSCEAR, Sources and Effects of Ionizing Radiation, Vol.2. United Nations, New York, 2000.
6. W. F. Morgan and M. B. Sowa, Non-targeted bystander effects induced by ionizing radiation. Mutat. Res. 616, 159-164 (2007).
7. W. F. Morgan, Will radiation-induced bystander effects or adaptive responses impact on the shape of the dose response relationships at low doses of ionizing radiation? Dose Response 4, 257-262 (2006).
8. R. J. Preston, Bystander effects, genomic instability, adaptive response, and cancer risk assessment for radiation and chemical exposures. Toxicol. Appl. Pharmacol. 207, 550-556 (2005).
9. H. Nikjoo and I. K. Khvostunov, A theoretical approach to the role and critical issues associated with bystander effect in risk estimation. Hum. Exp. Toxicol. 23, 81-86 (2004).
10. G. Olivieri, J. Bodycote and S. Wolff, Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science 223, 594-597 (1984).
11. 3H]thymidine-induced adaptive response of human lymphocytes to subsequent doses of X-rays involves the induction of a chromosomal repair mechanism. Mutagenesis 1, 375-380 (1986).
12. J. D. Shadley, V. Afzal and S. Wolff, Characterization of the adaptive response to ionizing radiation induced by low doses of X rays to human lymphocytes. Radiat. Res. 111, 511-517 (1987). (Pubitemid 17144564)
13. S. Wolff, V. Afzal, J. K. Wiencke, G. Olivieri and A. Michaeli, Human lymphocytes exposed to low doses of ionizing radiations become refractory to high doses of radiation as well as to chemical mutagens that induce double-strand breaks in DNA. Int. J. Radiat. Biol. 53, 39-47 (1988).
14. D. Bhattacharjee, Role of radioadaptation on radiation-induced thymic lymphoma in mice. Mutat. Res. 358, 231-235 (1996).
15. Y. Ina and K. Sakai, Prolongation of life span associated with immunological modification by chronic low-dose-rate irradiation in MRL-lpr/lpr mice. Radiat. Res. 161, 168-173 (2004).
16. Y. Ina and K. Sakai, Further study of 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. 163, 418-423 (2005).
17. Y. Ina, H. Tanooka, T. Yamada and K. Sakai, Suppression of thymic lymphoma induction by life-long low-dose-rate irradiation accompanied by immune activation in C57BL/6 mice. Radiat. Res. 163, 153-158 (2005).
18. R. E. J. Mitchel, J. S. Jackson and S. M. Carlisle, Upper dose thresholds for radiation-induced adaptive response against cancer in high-dose-exposed, cancer-prone, radiation-sensitive Trp53 heterozygous mice. Radiat. Res. 162, 20-30 (2004).
19. R. E. J. Mitchel, J. S. Jackson, D. P. Morrison and S. M. Carlisle, Low doses of radiation increase the latency of spontaneous lymphomas and spinal osteosarcomas in cancer-prone, radiation-sensitive Trp53 heterozygous mice. Radiat. Res. 159, 320-327 (2003).
20. P. O'Neill and P. Wardman, Radiation chemistry comes before radiation biology. Int. J. Radiat. Biol. 85, 9-25 (2009).
21. C. Grandi and R. Moccaldi, Bystander effect: Critical review and implications for risk assessment in radioprotection. G. Ital. Med. Lav. Ergon. 27, 21-34 (2005).
22. A. I. Kassis, In vivo validation of the bystander effect. Hum. Exp. Toxicol. 23, 71 (2004).
23. A. L. Brooks, Evidence for 'bystander effects' in vivo. Hum. Exp. Toxicol. 23, 67 (2004).
24. E. I. Azzam and J. B. Little, The radiation-induced bystander effect: evidence and significance. Hum. Exp. Toxicol. 23, 61-65 (2004).
25. Y. Chai and T. K. Hei, Radiation induced bystander effect in vivo. Acta Med. Nagasaki 53, 65-69 (2009).
26. B. Djordjevic, Bystander effects: A concept in need of clarification. BioEssays 22, 286-290 (2000).
27. V. P. Bond, V. Benary, C. A. Sondhaus and L. E. Feinendegen, The meaning of linear dose-response relations, made evident by use of absorbed dose to the cell. Health Phys. 68, 786-792 (1995).
28. D. J. Brenner, J. B. Little and R. K. Sachs, The bystander effect in radiation oncogenesis: II. A quantitative model. Radiat. Res. 155, 402-408 (2001).
29. L. E. Feinendegen, The cell dose concept; potential application in radiation protection. Phys. Med. Biol. 35, 597-612 (1990).
30. C. A. Sondhaus, V. P. Bond and L. E. Feinendegen, Cell-oriented alternatives to dose, quality factor, and dose equivalent for low-level radiation. Health Phys 59, 35-48 (1990).
31. ICRP, 1990 Recommendations of the International Commission on Radiological Protection. Publication 60, Annals of the ICRP, Vol.21, Elsevier, Amsterdam, 1991.
32. M. Matsuoka, F. Nagawa, K. Okazaki, L. Kingsbury, K. Yoshida, U. Muller, D. T. Larue, J. A. Winer and H. Sakano, Detection of somatic DNA recombination in the transgenic mouse brain. Science 254, 81-86 (1991).
33. P. Sykes, A. Hooker, C. Harrington, A. Jacobs, L. Kingsbury and A. Morley, Induction of somatic intrachromosomal recombination inversion events by cyclophosphamide in a transgenic mouse model. Mutat. Res. 397, 209-219 (1998).
34. B. I. Gerashchenko and R. W. Howell, Proliferative response of bystander cells adjacent to cells with incorporated radioactivity. Cytometry 60A, 155-164 (2004).
35. S. M. Goddu, R. W. Howell, L. G. Bouchet, W. E. Bolch and D. V. Rao, MIRD Cellular S Values: Self-Absorbed Dose Per Unit Cumulate Selected Radionuclides and Monoenergetic Electron and Alpha Emitters Incorportated into Different Cell Compartments. Society of Nuclear Medicine, Reston, VA, 1997.
36. J. Sheridan and J. Finlay-Jones, Studies of a fractionated murine fibrosarcoma: a reproducible method for the cautious and a caution for the unwary. J. Cell. Physiol. 90, 535-552 (1977).
37. H. Kishikawa, K. Wang, S. J. Adelstein and A. I. Kassis, Inhibitory and stimulatory bystander effects are differentially induced by iodine-125 and iodine-123. Radiat. Res. 165, 688-694 (2006).
38. S. A. Lorimore, J. M. McIlrath, P. J. Coates and E. G. Wright, Chromosomal instability in unirradiated hemopoietic cells resulting from a delayed in vivo bystander effect of c radiation. Cancer Res. 65, 5668-5673 (2005).
39. G. E. Watson, S. A. Lorimore, D. A. Macdonald and E. G. Wright, Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res. 60, 5608-5611 (2000).
40. L. Y. Xue, N. J. Butler, G. M. Makrigiorgos, S. J. Adelstein and A. I. Kassis, Bystander effect produced by radiolabeled tumor cells in vivo. Proc. Natl. Acad. Sci. USA 99, 13765-13770 (2002).
41. M. L. K. Tang, D. A. Steeber, X-Q. Zhang and T. F. Tedder, Intrinsic differences in L-selectin expression levels affect T and B lymphocyte subset-specific recirculation pathways. J. Immunol. 160, 5113-5121 (1998).
42. D. J. Manfra, S. C. Chen, T. Y. Yang, L. Sullivan, M. T. Wiekowski, S. Abbondanzo, G. Vassileva, P. Zalamea, D. N. Cook and S. A. Lira, Leukocytes expressing green fluorescent protein as novel reagents for adoptive cell transfer and bone marrow transplantation studies. Am. J. Pathol. 158, 41-47 (2001).
43. F. Moeller, F. C. Nielsen and L. B. Nielsen, New tools for quantifying and visualizing adoptively transferred cells in recipient mice. J. Immunol. Methods 282, 73-82 (2003).
44. O. Belyakov, M. Folkard, C. Mothersill, K. M. Prise and B. D. Michael, A proliferation-dependent bystander effect in primary porcine and human urothelial explants in response to targeted irradiation. Br. J. Cancer 88, 767-774 (2003).
45. C. Mothersill and C. Seymour, Medium from irradiated human epithelial cells but not human fibroblasts reduces the clonogenic survival of unirradiated cells. Int. J. Radiat. Biol. 71, 421-427 (1997).
46. P. Ren, A. W. de Feijter, D. L. Paul and R. J. Ruch, Enhancement of liver cell gap junction protein expression by glucocorticoids. Carcinogenesis 15, 1807-1813 (1994).
47. S. B. Pruett, N. Obiri and J. L. Kiel, Involvement and relative importance of at least two distinct mechanisms in the effects of 2-mercaptoethanol on murine lymphocytes in culture. J. Cell. Physiol. 141, 40-45 (1989).
48. V. P. Bond, Dose, effect severity, and imparted energy in assessing biological effects. Stem Cells 13 (Suppl. 1), 21-29 (1995).
49. V. P. Bond, L. E. Feinendegen and J. Booz, What is a 'low dose' of radiation? Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 53, 1-12 (1988).
50. Z. Liu, W. V. Prestwich, R. D. Stewart, S. H. Byun, C. E. Mothersill, F. E. McNeill and C. B. Seymour, Effective target size for the induction of bystander effects in medium transfer experiments. Radiat. Res. 168, 627-630 (2007).
51. Z. Liu, C. E. Mothersill, F. E. McNeill, F. M. Lyng, S. H. Byun, C. B. Seymour and W. V. Prestwich, A dose threshold for a medium transfer bystander effect for a human skin cell line. Radiat. Res. 166, 19-23 (2006).
52. L. A. Ryan, R. W. Smith, C. B. Seymour and C. E. Mothersill, Dilution of irradiated cell conditioned medium and the bystander effect. Radiat. Res. 169, 188-196 (2008).
53. E. C. Butcher and W. L. Ford, Following cellular traffic: Methods of labeling lymphocytes and other cells to trace their migration in vivo. In Handbook of Experimental Immunology: Cellular Immunology (D. Weir, Ed.), pp. 1-23. Blackwell Scientific, Oxford, 1986.
54. J. W. Albright, R. C. Mease, C. Lambert and J. F. Albright, Effects of aging on the dynamics of lymphocyte organ distribution in mice: use of a radioiodinated cell membrane probe. Mech. Ageing Dev. 101, 197-211 (1998).
55. S. Elmore, Enhanced histopathology of the spleen. Toxicol. Pathol. 34, 648-655 (2006).
56. F. M. Lyng, P. Maguire, B. McClean, C. Seymour and C. Mothersill, The involvement of calcium and MAP kinase signaling pathways in the production of radiation-induced bystander effects. Radiat. Res. 165, 400-409 (2006).
57. F. M. Lyng, C. B. Seymour and C. Mothersill, Production of a signal by irradiated cells which leads to a response in unirradiated cells characteristic of initiation of apoptosis. Br. J. Cancer 83, 1223-1230 (2000).
58. C. Mothersill, R. J. Seymour and C. B. Seymour, Increased radiosensitivity in cells of two human cell lines treated with bystander medium from irradiated repair-deficient cells. Radiat. Res. 165, 26-34 (2006).
59. O. A. Sedelnikova, A. Nakamura, O. Kovalchuk, I. Koturbash, S. A. Mitchell, S. A. Marino, D. J. Brenner and W. M. Bonner, DNA double-strand breaks form in bystander cells after microbeam irradiation of three-dimensional human tissue models. Cancer Res. 67, 4295-4302 (2007).
60. H. Aviles, M. Johnson and F. Monroy, Effects of cold stress on spleen cell proliferation and cytokine production during chronic Toxoplasma gondii infection. Neuroimmunomodulation 11, 93-102 (2004).
61. K. Cho, L. Adamson, J. Park and D. Greenhalgh, Burn injury-mediated alterations in cell cycle progression in lymphoid organs of mice. Shock 19, 138-143 (2003).
62. S. Fan, S. Gao, L. Shao, Y. Li, L. Mei and G. Ding, A factor in lymph node and spleen induced by restraint stress in mice and rats suppresses lymphocyte proliferation. Neuroimmunomodulation 2, 274-281 (1995).
63. I. Kovshik, A. Silkov, S. Sennikov, A. Shurlygina and V. Trufakin, Proliferative activity of cells in mouse thymus and spleen under different diurnal regimens of interleukin-2 administration. Bull. Exp. Biol. Med. 142, 98-101 (2006).
64. Y. Sakaguchi, L. C. Stephens, M. Makino, T. Kaneko, F. R. Strebel, L. L. Danhauser, G. N. Jenkins and J. M. C. Bull, Apoptosis in tumors and normal tissues induced by whole body hyperthermia in rats. Cancer Res. 55, 5459-5464 (1995).
65. J. Wang, R. Charboneau, R. A. Barke, H. H. Loh and S. Roy, Mu-opioid receptor mediates chronic restraint stress-induced lymphocyte apoptosis. J. Immunol. 169, 3630-3636 (2002).
66. L. X. Wei, J. N. Zhou, A. I. Roberts and Y. F. Shi, Lymphocyte reduction induced by hindlimb unloading: distinct mechanisms in the spleen and thymus. Cell Res. 13, 465-471 (2003).
67. D. Yin, D. Tuthill, R. A. Mufson and Y. Shi, Chronic restraint stress promotes lymphocyte apoptosis by modulating CD95 expression. J. Exp. Med. 191, 1423-1428 (2000).
68. K X rays. Radiat. Res. 163, 332-336 (2005).
69. S. Z. Liu, S. Z. Jin and X. D. Liu, Radiation-induced bystander effect in immune response. Biomed. Environ. Sci. 17, 40-46 (2004).
70. B. I. Gerashchenko and R. W. Howell, Cell proximity is a prerequisite for the proliferative response of bystander cells co-cultured with cells irradiated with gamma-rays. Cytometry A 56, 71-80 (2003).
71. M. Boyd, S. C. Ross, J. Dorrens,N. E. Fullerton, K. W. Tan, M. R. Zalutsky and R. J. Mairs, Radiation-induced biologic bystander effect elicited in vitro by targeted radiopharmaceuticals labeled with a-, b-, and Auger electron-emitting radionuclides. J. Nucl. Med. 47, 1007-1015 (2006).
72. R. Persaud, H. Zhou, T. K. Hei and E. J. Hall, Demonstration of a radiation-induced bystander effect for low dose low LET beta-particles. Radiat. Environ. Biophys. 46, 395-400 (2007).
73. C. Mothersill, F. Lyng, C. Seymour, P. Maguire, S. Lorimore and E. Wright, Genetic factors influencing bystander signaling in murine bladder epithelium after low-dose irradiation in vivo. Radiat. Res. 163, 391-399 (2005).
74. S. A. Lorimore, J. A. Chrystal, J. I. Robinson, P. J. Coates and E. G. Wright, Chromosomal instability in unirradiated hemaopoietic cells induced by macrophages exposed in vivo to ionizing radiation. Cancer Res. 68, 8122-8126 (2008).
75. C. Mothersill, D. Rea, E. G. Wright, S. A. Lorimore, D. Murphy, C. B. Seymour and K. O'Malley, Individual variation in the production of a 'bystander signal' following irradiation of primary cultures of normal human urothelium. Carcinogenesis 22, 1465-1471 (2001).
76. A. Acheva, R. Georgieva, I. Rupova, R. Boteva and F. Lyng, Bystander responses in low dose irradiated cells treated with plasma from gamma irradiated blood. J. Phys. Conf. Ser. 101, 012005 (2008).