Vanguards of paradigm shift in radiation biology: Radiation-induced adaptive and bystander responses

Journal of Radiation Research

Volumn 48, Issue 2, 2007, Pages 97-106

  Matsumoto, Hideki ^a   Hamada, Nobuyuki ^b,c   Takahashi, Akihisa ^d   Kobayashi, Yasuhiko ^b,c   Ohnishi, Takeo ^d  

^a UNIVERSITY OF FUKUI   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN ATOMIC ENERGY AGENCY   (Japan)

^d NARA MEDICAL UNIVERSITY   (Japan)

Author keywords

Bystander response; Ionizing radiation; Nitric oxide (NO); Radioadaptive response; Reactive nitrogen species (RNS); Reactive oxygen species (ROS)

Indexed keywords

NITRIC OXIDE; NITROGEN; OXYGEN; RADIATION EFFECTS; RADIATION SHIELDING; RISK PERCEPTION;

BYSTANDER RESPONSE; HIGH DOSE; LOW DOSE; NITRIC OXIDE; RADIATION BIOLOGY; RADIOADAPTIVE RESPONSE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

IONIZING RADIATION;

EID: 34047202420     PISSN: 04493060     EISSN: 13499157     Source Type: Journal    
DOI: 10.1269/jrr.06090     Document Type: Review

References (104)

1. Olivieri, G., Bodycote, J. and Wolff, S. (1984) Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science, 223: 594-597.
2. Sanderson, B. J. and Morley, A. A. (1986) Exposure of human lymphocytes to ionizing radiation reduces mutagenesis by subsequent ionizing radiation. Mutat. Res., 164: 347-351.
3. Ikushima, T. (1987) Chromosomal responses to ionizing radiation reminiscent of an adaptive response in cultured Chinese hamster cells. Mutat. Res., 180: 215-221.
4. Nagasawa, H. and Little, J. B. (1992) Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res., 52: 6394-6396.
5. Hickman, A. W., Jaramillo, R. J., Lechner, J. F. and Johnson, J. F. (1994) Alpha-particle-induced p53 protein expression in a rat lung-epithelial cell strain. Cancer Res., 54: 5797-5800.
6. Deshpande, A., Goodwin, E. H., Bailey, S. M., Marrone, B. L. and Lehnert, B. E. (1996) Alpha-particle-induced sister chromatid exchange in normal human lung fibroblasts: Evidence for an extranuclear target. Radiat. Res., 145: 260-267.
7. Little, J. B. (2006) Cellular radiation effects and the bystander response. Mutat. Res., 597: 113-118.
8. Hamada, N., Matsumoto, H., Hara, T. and Kobayashi, Y. (2007) Intercellular and Intracellular signaling pathways mediating ionizing radiation-induced bystander effects. J. Radiat. Res., 48: 87-95.
9. Kadhim, M. A., Moore, S. R. and Goodwin, E. H. (2004) Interrelationship amongst radiation-induced genomic instability, bystander effect, and the adaptive response. Mutat. Res., 568: 21-32.
10. Matsumoto, H., Takahashi, A., Ohnishi, T. (2004) Radiationinduced adaptive responses and bystander effects. Biol. Sci. Space, 18: 247-254.
11. Brooks, A. L. (2005) Paradigm shifts in radiation biology: their impact on intervention for radiation-induced disease. Radiat. Res., 164: 454-461.
12. Cai, L. and Liu, S. Z. (1990) Induction of cytogenetic adaptive responses of somatic and germ cells in vivo and in vitro by low dose X-irradiation. Int. J. Radiat. Biol., 58: 187-194.
13. Yonezawa, M., Misonoh, J. and Hosokawa, Y. (1996) Twotypes of X-ray-induced radio-resistance in mice: Presence of 4 dose ranges with distinct biological effects. Mutat. Res., 358: 237-243.
14. Wolff, S. (1998) The adaptive response in radiobiology: Evolving insights and implications. Environ. Health Perspect., 106 (Suppl 1): 277-283.
15. 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., 18: 419-425.
16. Shadley, J. D., Afzal, X. and Wolff, S. (1987) Characterization of the adaptive response to ionizing radiation induced by low doses of X rays to human lymphocytes. Radiat. Res., 111: 511-517.
17. Feinendegen, L. E. (1999) The role of adaptive responses following exposure to ionizing radiation. Hum. Exp. Toxicol., 18: 426-432.
18. de Toledo SM, Asaad N, Venkatachalam P, Li L, Howell RW, Spitz DR, Azzam EI. Adaptive responses to low-dose/ low-dose-rate gamma rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiat Res. 2006 Dec;166 (6): 849-857.
19. Wolff, S. (1992) Is radiation all bad? The search for adaptation. Radiat. Res., 131: 117-132.
20. Wiencke, J. K., Afzal, G., Olivieri, G. and Wolff, S. (1986) Evidence that 3H-thymidine-induced adaptive response of human lymphocytes to subsequent dose of X-rays involves the induction of a DNA repair mechanism. Mutagenesis, 1: 375-380.
21. Iyer, R. and Lehnert, B. E. (2002) Alpha-particle-induced increases in the radioresistance of normal human bystander cells. . Radiat. Res., 157: 3-7.
22. Iyer, R. and Lehnert, B. E. (2002) Low dose, Low- ionizing radiation-induced radioadaptation and associated early responses in unirradiated cells. Mutat. Res., 503: 1-9.
23. Takahashi, A., Asakawa, I., Yuki, K., Matsumoto, T., Kumamoto, M., Kondo, N., Ohnishi, K., Tachibana, A., Ohnishi, T. (2002) Radiation-induced apoptosis in the scid mouse spleen after low dose-rate irradiation. Int. J. Radiat. Biol., 78: 689-693.
24. Coleman, M. A., Yin, E., Peterson, L. E., Nelson, D., Sorensen, K., Tucker, J. D. and Wyrobek, A. J. (2005) Lowdose irradiation alters the transcript profiles of human lymphoblastoid cells including genes associated with cytogenetic radioadaptive response. Radiat. Res., 164: 369-382.
25. Takahashi, A. (2002) Pre-irradiation at a low dose-rate blunted p53 response. J. Radiat. Res., 43: 1-9.
26. Sasaki, M. S., Ejima, Y., Tachibana, A., Yamada, T., Ishizaki, K., Shimizu, T. and Nomura, T. (2002) DNA damage response pathway in radioadaptive response. Mutat. Res., 504: 101-118.
27. Wang, X. and Ohnishi, T. (1997) p53-dependent signal transduction induced by stress. J. Radiat. Res., 38: 179-194.
28. Woloschack, G. E., Chang-Liu, C., Jones, P. S. and Jones, C. A. (1990) Modulation of gene expression in Syrian hamster embryo cells. Cancer Res., 50: 339-344.
29. Liu, S. Z. (1992) Multilevel mechanisms of stimulatory effect of low dose radiation on immunity. In: T. Sugahara, L. A. Sagan and T. Aoyama (ed), Low dose irradiation and biological defense mechanisms. Elsevier, Amsterdam. pp. 225-232.
30. Ikushima, T. (1992) Radio-adaptive response: Involvement of specific genes induction by low doses of ionizing radiation. In: T. Sugahara, L. A. Sagan, and T. Aoyama (ed), Low dose irradiation and biological defense mechanisms. Elsevier, Amsterdam. pp. 255-258.
31. Sasaki, M. S. (1995) On the reaction kinetics of the radioadaptive response in cultured mouse cells. Int. J. Radiat. Biol., 68: 281-291.
32. Shimizu, T., Kato, T. Jr., Tachibana, A. and Sasaki, M. S. (1999) Coordinated regulation of radioadaptive response by protein kinase C and p38 mitogen-activated protein kinase. Exp. Cell Res., 251: 424-432.
33. Khodarev, N., Beckett, M., Labay, E., Darga, T., Roizman, B. and Weichselbaum, R. (2004) STAT1 is overexpressed in tumors selected for radioresistance and confers protection from radiation in transduced sensitive cells. Proc. Natl. Acad. Sci., USA, 101: 1714-1719.
34. Lee, Y. J., Park, G. H., Cho, H. N., Cho, C. K., Park, Y. M., Lee, S. J. and Lee, Y. S. (2002) Induction of adaptive response by low-dose radiation in RIF cells transfected with Hspb1 (Hsp25) or inducible Hspa (Hsp70). Radiat. Res., 157: 371-377.
35. Kang, C. M., Park, K. P., Cho, C. K., Seo, S. J., Park, W. Y., Lee, S. J. and Lee, Y. S. (2002) Hspa4 (Hsp70) is involved in the radioadaptive response: results from mouse splenocytes. Radiat. Res., 157: 650-655.
36. Park, S. H., Lee, S. J., Chung, H. Y., Kim, T. H., Cho, C. K., Yoo, S. Y. and Lee, Y. S. (2000) Inducible heat-shock protein Hsp70 is involved in the radioadaptive response. Radiat. Res., 153: 318-326.
37. Seo, H. R., Chung, H. Y., Lee, Y. J., Bae, S., Lee, S. J. and Lee, Y. S. (2006) p27Cip/Kip is involved in hsp25 or inducible hsp70 mediated adaptive response by low dose radiation. J. Radiat. Res., 47: 83-90.
38. Henle, E. S. and Linn, S. (1997) Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem., 272: 19095-19098.
39. Valko, M., Izakovic, M., Mazur, M., Rhodes, C. J. and Telser, J. (2004) Role of oxygen radicals in DNA damage and cancer incidence. Mol. Cell. Biochem., 266: 37-56.
40. Tannenbaum, S. R., Tamir, S., deRojas-Walker, T. and Wishnok, J. S. (1994) DNA damage and cytotoxicity by nitric oxide, in: R. N. Loeppky, C. J. Michejda (Eds.), Nitrosamines and related N-nitroso compounds, Vol. 10, American Chemical Society, Washington, D. C., pp120-135.
41. Burney, S., Caufield, J. L., Niles, J. C., Wishnok, J. S. and Tannenbaum, S. R. (1999) The chemistry of DNA damage from nitric oxide and peroxinitrite. Mutat. Res., 424: 37-49.
42. Geidushek, E. P. (1961) Reversible DNA. Proc. Natl. Acad. Sci., USA, 47: 950-955.
43. deRojas-Walker, T., Tamir, S., Ji, H., Wishnok, J. S. and Tannenbaum, S. R. (1995) Nitric oxide induces oxidative damage in addition to Deamination in macrophage DNA. Chem. Res. Toxicol., 8: 473-477.
44. Kennedy, L. J., Moore Jr., K., Caulfield, J. L., Tannenbaum, S. R., Dedon, P. C. (1997) Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem. Res. Toxicol., 10: 386-392.
45. Nakaya, N., Lowe, S. W., Taya, Y., Chenchik, A. and Enikolopov, G. (2000) Specific pattern of p53 phosphorylation during nitric oxide-induced cell cycle arrest. Oncogene, 19: 6369-6375.
46. Wang, X., Michael, D., de Murcia, G. and Oren, M. (2002) p53 activation by nitric oxide involves down-regulation of Mdm2. J. Biol. Chem., 277: 15697-15702.
47. Schleiber, V., Dantzer, F., Amé, J. -C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol., 7: 517-528.
48. Szabó, C. (2006) Poly(ADP-ribose) polymerase activation by reactive nitrogen species - Relevance for the pathogenesis of inflammation. Nitric Oxide, 14: 169-179.
49. Ramana, C. V., Boldogh, I., Izumi, T. and Mitra, S. (1998) Activation of apurinic/apyrimidinic endonuclease in human cells by reactive oxygen species and its correlation with their adaptive response to genotoxicity of free radicals. Proc. Natl. Acad. Sci., USA, 95: 5061-5066.
50. Xu, W., Liu, L., Smith, G. C. M. and Charles, I. G. (2000) Nitric oxide upregulates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell Biol., 2: 339-345.
51. Haimovitz-Friedman, A., Kan, C. -C., Ehleiter, D., Persaud, R. S., McLoughlin, M., Fuks, Z. and Kolesnick, R. N. (1994) Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med., 180: 525-535.
52. Leach, J. K., Tuyle, G. V., Lin, P. -S., Schmidt-Ullrich, R. and Mikkelsen, R. B. (2001) Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res., 61: 3894-3901.
53. Miura, Y. (2004) Oxidative stress, radiation-adaptive responses, and aging. J. Radiat. Res., 45: 357-372.
54. Bravard, A., Luccioni, C., Moustacchi, E. and Rigaud, O. (1999) Contribution of antioxidant enzymes to the adaptive response to ionizing radiation of human lymphoblasts. Int. J. Radiat. Biol., 75: 639-645.
55. Otsuka, K., Koana, T., Tauchi, H. and Sakai, K. (2006) Activation of antioxidative enzymes induced by low-dose-rate whole-body γ irradiation: Adaptive response in term of initial damage. Radiat. Res., 166: 474-478.
56. Shankar, B., Pandey, R. and Sainis, K. (2006) Radiationinduced bystander effects and adaptive response in murine lymphocytes. Int. J. Radiat. Biol., 82: 537-548.
57. Deshpande, A., Goodwin, E. H., Bailey, S. M., Marrone, B. L. and Lehnert, B. E. (1996) Alpha-particle-induced sister chromatid exchange in normal human lung fibroblasts: Evidence for an extranuclear target. Radiat. Res., 145: 260-267.
58. Lehnert, B. E., Goodwin, E. H. and Deshpande A. (1997) Extracellular factor(s) following exposure to α-particles can cause sister chromatid exchanges in normal human cells. Cancer Res., 57: 2164-2171.
59. Lorimore, S. A., Kadhim, M. A., Pocock, D. A., Papworth, D., Stevens, D. L., Goodhead, D. T. and Wright, E. G. (1998) Chromosomal instability in the descendants of unirradiated surviving cells after alpha-particle irradiation. Proc. Natl. Acad. Sci., U.S.A., 95: 5730-5733.
60. Azzam, E. I., de Toledo, S. M., Gooding, T. and Little, J. B. (1998) Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluences of alpha particles. Radiat. Res., 150: 497-504.
61. Prise, K. M., Belyakov, O. V., Folkard, M. and Micheal, B. D. (1998) Studies of bystander effects in human fibroblasts using a charged particle microbeam. Int. J. Radiat. Biol., 74: 793-798.
62. Zhou, H., Randers-Pehrson, G., Waldren, C. A., Vannais, D., Hall, E. J. and Hei, T. K. (2000) Induction of a bystander mutagenic effect of alpha particles in mammalian cells. Proc. Natl. Acad. Sci., U.S.A., 97: 2099-2104.
63. Huo, L., Nagasawa, H. and Little, J. B. (2001) HPRT mutants induced in bystander cells by very low fluences of alpha particles result primarily from point mutations. Radiat. Res., 156: 521-525.
64. Mothersill, C. and Seymour, C. B. (1998) Cell-cell contact during gamma irradiation is not required to induce a bystander effect in normal human keratinocytes: Evidence for release during irradiation of a signal controlling survival into medium. Radiat. Res., 149: 256-262.
65. Ballarini, F., Biaggi, M., Ottolenghi, A. and Sapora, O. (2002) Cellular communication and bystander effects: a critical review for modelling low-dose radiation action. Mutat. Res., 501: 1-12.
66. Xue, L. Y., Butler, N. J., Makrigiorgos, G. M., Adelstein, S. J. and Kassis, A. I. (2002) Bystander effect produced by radiolabeled tumor cells in vivo. Proc. Natl. Acad. Sci., U.S.A., 99: 13765-13770.
67. Kassis, A. I. (2004) In vivo validation of the bystander effect. Hum. Exp. Toxicol., 23: 71-73.
68. Van der Meeren, A., Monti, P., Vandamme, M., Squiban, C., Wysocki, J. and Griffiths, N. (2005) Abdominal radiation exposure elicits inflammatory responses and abscopal effects in the lung of mice. Radiat. Res., 163: 144-152.
69. Snyder, A. R. (2004) Review of radiation-induced bystander effects. Hum. Exp. Toxicol., 23: 87-89.
70. Nobler, M. P. (1969) The abscopal effect in malignant lymphoma and its relationship to lymphocyte circulation. Radiology, 93: 410-412.
71. Prasad, K. N., Cole, W. C. and Hasse, G. M. (2004) Health risks of low dose ionizing radiation in humans: A review. Exp. Biol. Med., 229: 378-382.
72. Lehnert, B. E., Goodwin, E. H. and Deshpande A. (1997) Extracellular factor(s) following exposure to α-particles can cause sister chromatid exchanges in normal human cells. Cancer Res., 57: 2164-2171.
73. Narayanan, P. K., Goodwin, E. H. and Lehnert, B. E. (1997) Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res., 57: 3963-3971.
74. Iyer, R. and Lehnert, B. E. (2000) Factors underlying the cell growth-related bystander responses to a particles. Cancer Res., 60: 1290-1298.
75. Barcellos-Hoff, M. H. and Brooks, A. L. (2001) Extracellular signaling through the microenvironment: A hypothesis relating carcinogenesis, bystander effects, and genomic instability. Radiat. Res., 156: 618-627.
76. Ewan, K. B., Henshall-Powell, R. L., Ravani, S. A., Pajares, M. J., Arteaga, C., Warters, R., Akhurst, R. J. and Barcellos-Hoff, M. H. (2002) Transforming growth factor-β1 mediates cellular response to DNA damage in situ. Cancer Res., 62: 5627-5631.
77. Martin, M., Vozenin, M. C., Gault, N., Crechet, F., Pfarr, C. M. and Lefaix, J. L. (1997) Coactivation of AP-1 activity and TGF-β1 gene expression in the stress response of normal skin cells to ionizing radiation. Oncogene, 15: 981-989.
78. Matsumoto, H., Hayashi, S., Hatashita, M., Shioura, H., Ohtsubo, T., Kitai, R., Ohnishi, T., Yukawa, O., Furusawa, Y. and Kano, E. (2000) Induction of radioresistance to accelerated carbon-ion beams in recipient cells by nitric oxide excreted from irradiated donor cells of human glioblastoma. Int. J. Radiat. Biol., 76: 1649-1657.
79. Matsumoto, H., Hayashi, S., Hatashita, M., Ohnishi, K., Shioura, H., Ohtsubo, T., Kitai, R., Ohnishi, T. and Kano, E. (2001) Induction of radioresistance by a nitric oxide-mediated bystander effect. Radiat. Res, 155: 387-396.
80. Shao, C., Furusawa, Y., Aoki, M., Matsumoto, H. and Ando, K. (2002) Nitric oxide-mediated bystander effect induced by heavy-ions in human salivary gland tumour cells. Int. J. Radiat. Biol., 78: 837-844.
81. Hancock, J. T. and Jones, T. G. (1987) The inhibition by diphenyleneiodonium and its analogues of superoxide generation by macrophage. Biochem. J., 242: 103-107.
82. Azzam, E. I., de Toledo, S. M., Spitz, D. R. and Little, J. B. (2002) Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from α-particle-irradiated normal human fibroblast cultures. Cancer Res., 62: 5436-5442.
83. Azzam, E. I., de Toledo, S. M. and Little, J. B. (2002) Oxidative metabolism, gap junctions and the ionizing radiationinduced bystander effect. Oncogene, 22: 7050-7057.
84. Nathan C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J, 6: 3051-3064.
85. MacNaul K. L. and Hutchinson N. I. (1993) Differential expression of iNOS and cNOS mRNA in human vascular smooth muscle cells and endothelial cells under normal and inflammatory conditions. Biochem. Biophys. Res. Commun., 196: 1330-1334.
86. Malyshev I. Y., Manukhina E. B., Mikoyan V. D., Kubrina L. N. and Vanin A. F. (1995) Nitric oxide is involved in heatinduced HSP70 accumulation. FEBS Lett, 370: 159-162.
87. Melillo G., Musso T., Sica A., Taylor L. S., Cox G. W. and Varesio, L. A. (1995) Hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med, 182: 1683-1693.
88. Gorbunov, K. V., Pogue-Geile, K. L., Epperly, M. W., Bigbee, W. L., Draviam, R., Day, B. W., Wald, N., Watkins, S. C. and Greenberger, J. S. (2000) Activation of the nitric oxide synthase 2 pathway in the response of bone marrow stromal cells to high doses of ionizing radiation. Radiat. Res., 154: 73-86.
89. Lee, K. C., Crowe, A. J. and Barton, M. C. (1999) p53-mediated repression of α-fetoprotein gene expression by specific DNA binding. Mol. Cell. Biol., 19: 1279-1288.
90. Kanaya, T., Kyo, S., Hamada, K., Takakura, M., Kitagawa, Y., Harada, H. and Inoue, M. (2000) Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin. Cancer Res., 6: 1239-1247.
91. Martin, D. W., Munoz, R. M., Subler, M. A. and Deb, S. (1993) p53 binds to the TATA-binding protein-TATA complex. J. Biol. Chem., 268: 13062-13067.
92. Johnson, R. A., Ince, T. A. and Scotto, K. W. (2001) Transcriptional repression by p53 through direct binding to a novel DNA element. J. Biol. Chem., 276: 27716-27720.
93. Leach, J. K., Black, S. M., Schmidt-Ullrich, R. K. and Mikkelsen, R. B. (2002) Activation of constitutive nitricoxide synthase activity is an early signaling event induced by ionizing radiation. J. Biol. Chem., 277: 15400-15406.
94. Wink D. A., Kasprzak K. S., Maragos C. M., Elespuru R. K., Misra M., Dunams,. M., Cebula T. A., Koch W. H., Andrews A. W., Allen J. S. and Keefer L. K. (1991) DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science, 254: 1001-1003.
95. Nguyen T., Brunson D., Crespi C. L., Penman B. W., Wishnok J. S. and Tannenbaum, S. R. (1992) DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc Natl Acad Sci USA, 89: 3030-3034.
96. Moncada S., Palmer R. M. and Higgs E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev, 43: 109-142.
97. Brüne B., von Knethen A. and Sandau K. B. (1998) Nitric oxide and its role in apoptosis. Eur J Pharmacol, 351: 261-272.
98. Shao, C., Stewart, V., Folkard, M., Michael, B. D. and Prise, K. M. (2003) Nitric oxide-mediated signaling in the bystander response of individually targeted glioma cells. Cancer Res., 63: 8437-8442.
99. Shao, C., Lyng, F. M., Folkard, M. and Prise, K. M. (2006) Calcium fluxes modulate the radiation-induced bystander responses in targeted glioma and fibroblast cells. Radiat. Res., 166: 479-487.
100. Han, W., Wu, L., Chen, S., Bao, L., Zhang, L., Jiang, E., Zhao, Y., Xu, A., Hei, T. K. and Yu, Z. (2006) Constitutive nitric oxide acting as a possible intercellular signaling molecule in the initiation of radiation-induced DNA double strand breaks in non-irradiated bystander cells. Oncogene, in press.
101. Honda, S., Migita, K., Hirai, Y., Tamasaki, S., Urayama, S., Kawabe, Y., Fukuda, T., Kawakami, A., Kamachi, M., Kita, M., Ida, H., Aoyagi, T. and Eguchi, K. (2000) Induction of COX-2 expression by nitric oxide in rheumatoid synovial cells. Biochem. Biophys. Res. Commun., 268: 928-931.
102. Terakado, N., Shintani, S., Yano, J., Chunnan, L., Mihara, M., Nakashiro, K. and Hamakawa, H. (2004) Overexpression of cyclooxygenase-2 is associated with radioresistance in oral squamous cell carcinoma. Oral Oncol., 70: 383-389.
103. Zhou, H., Ivanov, V. N., Gillespie, J., Geard, C. R., Amundson, S. A., Brenner, D. J., Yu, Z., Lieberman, H. B. and Hei, T. K. (2005) Mechanism of radiation-induced bystander effect: Role of the cyclooxygenase-2 signaling pathway. Proc Natl Acad Sci USA, 102: 14641-14646.
104. Vanegas, H. and Schaible, H. G. (2001) Prostaglandin and cyclooxygenases in the spinal cord. Prog. Neurobiol., 64: 327-363.