Nitric oxide is a key molecule serving as a bridge between radiation-induced bystander and adaptive responses

Current Molecular Pharmacology

Volumn 4, Issue 2, 2011, Pages 126-134

  Matsumoto, Hideki ^a   Tomita, Masanori ^b   Otsuka, Kensuke ^b   Hatashita, Masanori ^c   Hamada, Nobuyuki ^b  

^a UNIVERSITY OF FUKUI   (Japan)

^b CENTRAL RESEARCH INSTITUTE OF ELECTRIC POWER INDUSTRY   (Japan)

^c WAKASA WAN ENERGY RESEARCH CENTER   (Japan)

Author keywords

Bystander response; Ionizing radiation; Nitric oxide; Radioadaptive response; Reactive nitrogen species

Indexed keywords

NITRIC OXIDE; REACTIVE NITROGEN SPECIES;

ARTICLE; BYSTANDER EFFECT; CELL PROTECTION; CHROMOSOME ABERRATION; DNA DAMAGE; DNA PROTEIN COMPLEX; GENE MUTATION; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY; SIGNAL TRANSDUCTION;

EID: 79953777799     PISSN: 18744672     EISSN: 18744702     Source Type: Journal    
DOI: 10.2174/1874467211104020126     Document Type: Article

References (82)

1. ICRP, 1990 Recommendations of the International Commission on Radiobiological Protection. Publication 60, Annals of the ICRP, Vol. 21, No. 1-3, Pergamon Press, Oxford, 1991.
2. NCRP, Recommendation on Limits for Exposure to Ionizing Radiation. Report No. 116, National Council on Radiation Protection and Measurements, Bethesda, MD. 1993.
3. Olivieri, G.; Bodycote, J.; Wolff, S. Adaptive response of human lymphocytes to low concentrations of radioactive thymidine. Science, 1984, 223, 594-597.
4. Nagasawa, H.; Little, J.B. Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res., 1992, 52, 6394-6396.
5. Hickman, A.W.; Jaramillo, R.J.; Lechner, J.F.; Johnson, J.F. Alpha- particle-induced p53 protein expression in a rat lung-epithelial cell strain. Cancer Res., 1994, 54, 5797-5800.
6. Deshpande, A.; Goodwin, E.H.; Bailey, S.M.; Marrone, B.L.; Lehnert, B.E. Alpha-particle-induced sister chromatid exchange in normal human lung fibroblasts: Evidence for an extranuclear target. Radiât. Res., 1996,145, 260-267.
7. Little, J.B. Cellular radiation effects and the bystander response. Mutat. Res., 2006, 597, 113-118.
8. Hamada, N.; Maeda, M.; Otsuka, K.; Tomita, M. Signaling path- ways underpinning the manifestations of ionizing radiation-induced bystander effects. Curr. Mol. Pharmacol, 2011, 4, 79-95.
9. Hei, T.K.; Zhou, H.; Chai, Y.; Ponnaiya, B.; Ivanov, V.N. Radiation induced non-targeted response: mechanism and potential clinical implications. Curr. Mol. Pharmacol, 2011, 4, 96-105.
10. Jain M.R.; Li, M.; Chen, W.; Liu, T.; de Toledo, S.M.; Li, H.; Rabin, B.M.; Azzam, E.I. In vivo space radiation-induced non-targeted responses: late effects on molecular signaling in mitochondria. Curr. Mol. Pharmacol, 2011, 4, 106-114.
11. Tamminga, J.; Kovalchuk, O. Role of DNA damage and epigenetic DNA methylation changes in radiation-induced genomic instability and bystander effects in germline in vivo. Curr. Mol. Pharmacol, 2011, 4, 115-125.
12. Morgan, W.F. Communicating non-targeted effects of radiation to achieve adaptive homeostasis in tissues. Curr. Mol. Pharmacol, 2011, 4, 135-140.
13. Kadhim, M.A.; Moore, S.R.; Goodwin, E.H. Interrelationship amongst radiation-induced genomic instability, bystander effect, and the adaptive response. Mutat. Res., 2004, 568, 21-32.
14. Matsumoto, H.; Takahashi, A.; Ohnishi, T. Radiation-induced adaptive responses and bystander effects. Biol. Sei., Space, 2004, 18, 247-254.
15. Brooks, A.L. Paradigm shifts in radiation biology: their impact on intervention for radiation-induced disease. Radiât. Res., 2005, 164, 454-461.
16. Cai, L.; Liu, S.Z. Induction of cytogenetic adaptive responses of somatic and germ cells in vivo and in vitro by low dose X-irradiation. Int. J. Radiat. Biol, 1990, 58, 187-194.
17. Yonezawa, M.; Misonoh, J.; Hosokawa, Y. Two-types of X-ray-induced radio-resistance in mice: Presence of 4 dose ranges with distinct biological effects. Mutat. Res., 1996, 358, 237-243.
18. Wolff, S. The adaptive response in radiobiology: Evolving insights and implications. Environ. Health Perspect., 1998, 106 (Suppl 1), 277-283.
19. Cai, L. Research of the adaptive response induced by low-dose radiation: Where have we been and where should we go? Hum. Exp. Toxicol, 1999,18, 419-425.
20. Shadley, J.D.; Afzal, V.; Wolff, S. Characterization of the adaptive response to ionizing radiation induced by low doses of X rays to human lymphocytes. Radiât. Res., 1987, 777, 511-517.
21. Feinendegen, L.E. The role of adaptive responses following exposure to ionizing radiation. Hum. Exp. Toxicol, 1999,18, 426-432.
22. de Toledo, S.M.; Asaad, N.; Venkatachalam, P.; Li, L.; Howell, R.W.; Spitz, D.R.; Azzam, E.I. Adaptive responses to low-dose/low-dose-rate gamma rays in normal human fibroblasts: the role of growth architecture and oxidative metabolism. Radiât. Res., 2006, 766, 849-57.
23. Tannenbaum, S.R.; Tamir, S.; de Rojas-Walker, T.; Wishnok, J.S. DNA damage and cytotoxicity by nitric oxide, in: R.N. Loeppky, C.J. Michejda (Eds.), Nitrosamines and related W-nitroso compounds, Vol. 10, American Chemical Society, Washington, D.C., 1994, pp. 120-135.
24. Burney, S.; Caufield, J.L.; Niles, J.C.; Wishnok, J.S.; Tannenbaum, S.R. The chemistry of DNA damage from nitric oxide and perox-initrite. Mutat. Res., 1999, 424, 37-49.
25. Geidushek, E.P. Reversible DNA. Proc. Nati. Acad. Sei., USA, 1961, 47, 950-955.
26. Kennedy, L.J.; Moore Jr., K.; Caulfield, J.L.; Tannenbaum, S.R.; Dedon, P.C. Quantitation of 8-oxoguanine and strand breaks produced by four oxidizing agents. Chem. Res. Toxicol, 1997, 10, 386-392.
27. Gatti, R.M.; Alvarez, B.; Vasquez-Vivar, J.; Radi, R.; Augusto, O. Formation of spin trap adducts during the decomposition of per-oxynitrate. Arch. Biochem. Biophys., 1998, 349, 36-46.
28. Merenyi, G.; Lind, J. Free radical formation in the peroxynitrous acid (ONOOH)/peroxynitrite (ONOO) system. Chemical Res. Toxicol, 1998,77,243-246.
29. Coleman, M.A.; Yin, E.; Peterson, L.E.; Nelson, D.; Sorensen, K.; Tucker, J.D.; Wyrobek, A.J. Low-dose irradiation alters the transcript profiles of human lymphoblastoid cells including genes associated with cytogenetic radioadaptive response. Radiat. Res., 2005, 764, 369-382.
30. Schleiber, V.; Dantzer, F.; Amé, J.-C; de Murcia, G. Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol Cell Biol, 2006, 7,517-528.
31. Szabó, C. Poly(ADP-ribose) polymerase activation by reactive nitrogen species - Relevance for the pathogenesis of inflammation. Nitric Oxide, 2005,14, 169-17950
32. Xu, W.; Liu, L.; Smith, G.C.M.; Charles, I.G. Nitric oxide upregu-lates expression of DNA-PKcs to protect cells from DNA-damaging anti-tumour agents. Nat. Cell Biol, 2000, 2, 339-345.
33. Haimovitz-Friedman, A.; Kan, C.-C; Ehleiter, D.; Persaud, R.S.; McLoughlin, M.; Fuks, Z.; Kolesnick, R.N. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med., 1994,180, 525-535.
34. Leach, J.K.; Tuyle, G.V.; Lin, P.-S.; Schmidt-Ullrich, R.; Mikkel-sen, R.B. Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res., 2001, 67, 3894-3901.
35. Shankar, B.; Pandey, R.; Sainis, K. Radiation-induced bystander effects and adaptive response in murine lymphocytes. Int. J. Radial Biol, 2006, 82, 537-548.
36. Takahashi, A. Different inducibility of radiation- or heat-induced p53-dependent apoptosis after acute or chronic irradiation in human cultured squamous cell carcinoma cells, Int. J. Radiât. Biol, 2001, 77,215-224.
37. Takahashi, A.; Ohnishi, K.; Asakawa, I.; Kondo, N.; Nakagawa, H.; Yonezawa, M.; Tachibana, A.; Matsumoto, H.; Ohnishi, T. Radiation response of apoptosis in C57BL/6N mouse spleen after whole-body irradiation. Int. J. Radiât. Biol., 2001, 77, 939-945.
38. Komarova, E.A.; Diatchenko, L.; Rokhlin, O.W.; Hill, J.E.; Wang, Z.J.; Krivokrysenko, V.l.; Feinstein, E.; Gudkov, A.V. Stress-induced secretion of growth inhibitors: a novel tumor suppressor function of p53. Oncogene, 1998, 7 7, 1089-1096.
39. Forrester, K.; Ambs, S.; Lupold, S.E.; Kapust, R.B.; Spillare, E.A.; Weinberg, W.C.; Felley-Bosco, E.; Wang, X.W.; Geller, D.A.; Tzeng, E.; Billiar, T.R.; Harris, C.C. Nitric oxide-induced p53 accumulation and regulation of inducible nitric oxide synthase expression by wild-type p53. Proc. Nati. Acad. Sei. USA, 1996, 93, 2442-2447.
40. Ambs, S.; Ogunfusika, M.O.; Merrian, W.G.; Bennett, W.P.; Billiar, T.R.; Harris, C.C. Up-regulation of inducible nitric oxide synthase expression in cancer-prone p53 knockout mice. Proc. Nati. Acad. Sei. USA, 1998, 95, 8823-8828.
41. Matsumoto, H.; Hayashi, S.; Hatashita, M.; Shioura, H.; Ohtsubo, T.; Kitai, R.; Ohnishi, T.; Yukawa, O.; Furusawa, Y.; Kano, E. Induction of radioresistance to accelerated carbon-ion beams in recipient cells by nitric oxide excreted from irradiated donor cells of human glioblastoma. Int. J. Radiât. Biol, 2000, 76, 1649-1657.
42. Matsumoto, H.; Hayashi, S.; Hatashita, M.; Ohnishi, K.; Shioura, H.; Ohtsubo, T.; Kitai, R.; Ohnishi, T.; Kano, E. Induction of radioresistance by a nitric oxide-mediated bystander effect. Radiât. Res., 2001,155, 387-396.
43. Wang, X.; Michael, D.; de Murcia, G.; Oren, M. p53 activation by nitric oxide involves down-regulation of Mdm2. J. Biol. Chem., 2002, 277, 15697-702.
44. Nakaya, N.; Lowe, S.W.; Taya, Y.; Chenchik, A.; Enikolopov, G. Specific pattern of p53 phosphorylation during nitric oxide-induced cell cycle arrest. Oncogene, 2000,19, 6369-75.
45. Matsumoto, H.; Takahashi, A.; Ohnishi, T. Nitric oxide radicals choreograph a radioadaptive response. Cancer Res., 2007, 67, 8574-8579.
46. Lehnert, B.E.; Goodwin, E.H.; Deshpande, A. Extracellular factors) following exposure to a-particles can cause sister chromatid exchanges in normal human cells. Cancer Res., 1997, 57, 2164-2171.
47. Lorimore, S.A.; Kadhim, M.A.; Pocock, D.A.; Papworth, D.; Stevens, D.L.; Goodhead, D.T.; Wright, E.G. Chromosomal instability in the descendants of unirradiated surviving cells after alpha-particle irradiation. Proc. Nati. Acad. Sei. USA, 1998, 95, 5730-5733.
48. Azzam, E.I.; de Toledo, S.M.; Gooding, D.T.; Little, J.B. Intercellular communication is involved in the bystander regulation of gene expression in human cells exposed to very low fluences of alpha particles. Radiat. Res., 1998, 750, 497-504.
49. Prise, K.M.; Belyakov, O.V.; Folkard, M.; Micheal, B.D. Studies of bystander effects in human fibroblasts using a charged particle mi-crobeam. Int. J. Radiât. Biol, 1998, 74, 793-798.
50. Zhou, H.; Randers-Pehrson, G.; Waldren, CA.; Vannais, D.; Hall, E.J.; Hei, T.K. Induction of a bystander mutagenic effect of alpha particles in mammalian cells. Proc. Nati. Acad. Sei. USA, 2000, 97, 2099-2104.
51. Huo, L.; Nagasawa, H.; Little, J.B. HPRT mutants induced in bystander cells by very low fluences of alpha particles result primarily from point mutations. Radiât. Res., 2001, 756, 521-525.
52. Mothersill, C; Seymour, C.B. 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. Radiât. Res., 1998, 149, 256-262.
53. Ballarini, F.; Biaggi, M.; Ottolenghi, A.; Sapora, O. Cellular communication and bystander effects: a critical review for modelling low-dose radiation action. Mutat. Res., 2002, 507, 1-12.
54. Xue, L.Y.; Butler, N.J.; Makrigiorgos, G.M.; Adelstein, S.J.; Kas-sis, A.I. Bystander effect produced by radiolabeled tumor cells in vivo. Proc. Nati. Acad. Sei. USA, 2002, 99, 13765-13770.
55. Kassis, A.I. In vivo validation of the bystander effect. Hum. Exp. Toxicol, 2004, 23, 71-73.
56. Van der Meeren, A.; Monti, P.; Vandamme, M.; Squiban, C; Wysocki, J.; Griffiths, N. Abdominal radiation exposure elicits in-flammatory responses and abscopal effects in the lung of mice. Radial Res., 2005,163, 144-152.
57. Mancuso, M.; Pasquali, E.; Leonardi, S.; Tanori, M.; Rebessi, S.; Di Majo, V.; Pazzaglia, S.; Toni, M.P.; Pimpinella, M.; Covelli, V.; Saran, A. Oncogenic bystander radiation effects in Patched heterozygous mouse cerebellum. Proc. Nati. Acad. Sei. USA, 2008, 705, 1244512450.
58. Koturbash, I.; Loree, J.; Kutanzi, K.; Koganow, C; Pogribny, I.; Kovalchuk, O. In vivo bystander effect: cranial X-irradiation leads to elevated DNA damage, altered cellular proliferation and apoptosis, and increased p53 levels in shielded spleen. Int. J. Radial Oncol Biol Phys., 2008, 70, 554-562.
59. Prasad, K.N.; Cole, W.C.; Hasse, G.M. Health risks of low dose ionizing radiation in humans: a review. Exp. Biol Med., 2004, 229, 378-382.
60. Narayanan, P.K.; Goodwin, E.H.; Lehnert, B.E. Alpha particles initiate biological production of Superoxide anions and hydrogen peroxide in human cells. Cancer Res., 1997, 57, 3963-3971.
61. Iyer, R.; Lehnert, B.E. Factors underlying the cell growth-related bystander responses to a particles. Cancer Res., 2000, 60, 1290-1298.
62. Barcellos-Hoff, M.H.; Brooks, A.L. Extracellular signaling through the microenvironment: A hypothesis relating carcinogenesis, bystander effects, and genomic instability. Radiât. Res., 2001, 756, 618-627.
63. Moore, S.R.; Marsden, S.; Macdonald, D.; Mitchell, S.; Folkard, M.; Michael, B.; Goodhead, D.T.; Prise, K.M.; Kadhim, M.A. Genomic instability in human lymphocytes irradiated with individual charged particles: involvement of tumor necrosis factor a in irradiated cells but not bystander cells. Radial Res., 2005,163, 183-190.
64. Vodovotz, Y.; Chesler, L.; Chong, H.; Kim, S.J.; Simpson, J.T.; DeGraff, W.; Cox, G.W.; Roberts, A.B.; Wink, D.A.; Barcellos-Hoff, M.H. Regulation of transforming growth factor betal by nitric oxide. Cancer Res., 1999, 59, 2142-2149.
65. Shao, C; Furusawa, Y.; Aoki, M.; Matsumoto, H.; Ando, K. Nitric oxide-mediated bystander effect induced by heavy-ions in human salivary gland tumour cells, Int. J. Radial Biol, 2002, 78, 837-844.
66. Shao, C; Stewart, V.; Folkard, M.; Michael, B.D.; Prise, K.M. Nitric oxide-mediated signaling in the bystander response of individually targeted glioma cells. Cancer Res., 2003, 63, 8437-8442.
67. Shao, C; Lyng, F.M.; Folkard, M.; Prise, K.M. Calcium fluxes modulate the radiation-induced bystander responses in targeted glioma and fibroblast cells. Radiât. Res., 2006, 766, 479-487.
68. Han, W.; Wu, L.; Chen, S.; Bao, L.; Zhang, L.; Jiang, E.; Zhao, Y.; Xu, A.; Hei, T.K.; Yu, Z. 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, 2006, 26, 2330-2339.
69. Zhou, H.; Randers-Pehrson, G.; Geard, C.R.; Brenner, D.J.; Hall, E.J.; Hei, T.K. Interaction between radiation-induced adaptive response and bystander mutagenesis in mammalian cells. Radiât. Res., 2003, 760, 512-516.
70. Portess, D.I.; Bauer, G.; Hill, M.A.; O'Neill, P. Low-dose irradiation of nontransformed cells stimulates the selective removal of precancerous cells via intercellular induction of apoptosis. Cancer Res., 2007, 67, 1246-1253.
71. Iyer, R.; Lehnert, B.E. Alpha-particle-induced increases in the radioresistance of normal human bystander cells. Radiât. Res., 2002, 757, 3-7.
72. Iyer, R.; Lehnert, B.E. Low dose, Low- ionizing radiation-induced radioadaptation and associated early responses in unirradiated cells. Mutat. Res., 2002, 503, 1-9.
73. Takahashi, A. Pre-irradiation at a low dose-rate blunted p53 response. J. Radial Res., 2002, 43, 1-9.
74. Honda, S.; Migita, K.; Hirai, Y.; Tamasaki, S.; Urayama, S.; Ka-wabe, Y.; Fukuda, T.; Kawakami, A.; Kamachi, M.; Kita, M.; Ida, H.; Aoyagi, T.; Eguchi, K. Induction of COX-2 expression by nitric oxide in rheumatoid synovial cells. Biochem. Biophys. Res. Commun., 2000, 268,928-931.
75. Terakado, N.; Shintani, S.; Yano, J.; Chunnan, L.; Mihara, M.; Nakashiro, K.; Hamakawa, H. Overexpression of cyclooxygenase-2 is associated with radioresistance in oral squamous cell carcinoma. Oral Oncol, 2004, 70, 383-389.
76. Zhou, H.; Ivanov, V.N.; Gillespie, J.; Geard, C.R.; Amundson, S.A.; Brenner, D.J.; Yu, Z.; Lieberman, H. B.; Hei, T.K. Mechanism of radiation-induced bystander effect: Role of the cyclooxy-genase-2 signaling pathway. Proc. Nati. Acad. Sei. USA, 2005,102, 14641-14646.
77. Leach, J.K.; Black, S.M.; Schmidt-Ullrich, R.K.; Mikkelsen, R.B. Activation of constitutive nitric-oxide synthase activity is an early signaling event induced by ionizing radiation. J. Biol. Chem., 2002, 277, 15400-15406.
78. Vanegas, H.; Schaible, H.G. Prostaglandin and cyclooxygenases in the spinal cord. Prog. Neurobiol, 2001, 64, 327-363.
79. Bolaños, J.P.; Medina, J.M. Induction of nitric oxide synthase inhibits gap junction permeability in cultured rat astrocytes, J. Neureichem., 1996, 66, 2091-2099.
80. Sladek, S.M.; Westerhausen-Larson, A.; Roberts, J.M. Endogenous nitric oxide suppresses rat myometrial connexin 43 gap junction protein expression during pregnancy. Biol. Reproduct., 1999, 61, 8-13.
81. Anand, R.J.; Dai, S.; Rippel, C; Leaphart, C; Qureshi, F.; Griber, S.C.; Kohler, J.W.; Li, J.; Stolz, D.B.; Sodhi, C; Hackam, D.J. Activated macrophages inhibit enterocyte gap junction via the release of nitric oxide. Am. J. Physiol. Gastrointest. Liver Physiol, 2008, 294, G109-G119.
82. Liao, C.-K.; Wang, S.-M.; Chen, Y.-L.; Wang, H.-S.; Wu, J.-C. Lipopolysaccharide-induced inhibition of connexin43 gap junction communication in astrocytes is mediated by downregulation of caveolin-3. Int. J. Biochem. Cell Biol, 2010, 42, 762-770.