Cytochrome-c mediated a bystander response dependent on inducible nitric oxide synthase in irradiated hepatoma cells

British Journal of Cancer

Volumn 106, Issue 5, 2012, Pages 889-895

  He, M ^a   Ye, S ^a   Ren, R ^a   Dong, C ^a   Xie, Y ^a   Yuan, D ^a   Shao, C ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

bystander effect; cytochrome c; iNOS; ionising radiation; ROS

Indexed keywords

ALPHA TUBULIN; CYCLOSPORIN A; CYTOCHROME C; FREE RADICAL; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE;

ARTICLE; BYSTANDER EFFECT; CONTROLLED STUDY; GAMMA IRRADIATION; HUMAN; HUMAN CELL; IRRADIATION; LIVER CELL CARCINOMA; MICRONUCLEUS; PRIORITY JOURNAL; RADIATION DOSE; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

BYSTANDER EFFECT; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CYCLOSPORINE; CYTOCHROMES C; GAMMA RAYS; HEP G2 CELLS; HUMANS; ISOTHIURONIUM; LIVER NEOPLASMS; MICRONUCLEUS TESTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84857790898     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.9     Document Type: Article

References (56)

1. Asur RS, Thomas RA, Tucker JD (2009) Chemical induction of the bystander effect in normal human lymphoblastoid cells. Mutat Res 676: 11-16
2. Aykin-Burns N, Slane BG, Liu AT, Owens KM, O'Malley MS, Smith BJ, Domann FE, Spitz DR (2011) Sensitivity to low-dose/low-LET ionizing radiation in mammalian cells harboring mutations in succinate dehydrogenase subunit C is governed by mitochondria-derived reactive oxygen species. Radiat Res 175: 150-158
3. Azzam EI, de Toledo SM, Gooding T, Little JB (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 (Pubitemid 28499048)
4. Azzam EI, de Toledo SM, Little JB (2004) Stress signaling from irradiated to non-irradiated cells. Curr Cancer Drug Targets 4: 53-64 (Pubitemid 38332564)
5. Azzam EI, de Toledo SM, Waker AJ, Little JB (2000) High and low fluences of alpha-particles induce a G1 checkpoint in human diploid fibroblasts. Cancer Res 60: 2623-2631 (Pubitemid 30318236)
6. Baskar R, Balajee AS, Geard CR (2007) Effects of low and high LET radiations on bystander human lung fibroblast cell survival. Int J Radiat Biol 83: 551-559 (Pubitemid 47035913)
7. Camphausen K, Moses MA, Menard C, Sproull M, Beecken WD, Folkman J, O'Reilly MS (2003) Radiation abscopal antitumor effect is mediated through p53. Cancer Res 63: 1990-1993 (Pubitemid 36460868)
8. Chen Q, Chai YC, Mazumder S, Jiang C, Macklis RM, Chisolm GM, Almasan A (2003) The late increase in intracellular free radical oxygen species during apoptosis is associated with cytochrome c release, caspase activation, and mitochondrial dysfunction. Cell Death Differ 10: 323-334 (Pubitemid 36582370)
9. Chen S, Zhao Y, Zhao G, Han W, Bao L, Yu KN, Wu L (2009) Up-regulation of ROS by mitochondria-dependent bystander signaling contributes to genotoxicity of bystander effects. Mutat Res 666: 68-73
10. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon 3rd RO, Gladwin MT (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9: 1498-1505 (Pubitemid 38004777)
11. Dickey JS, Baird BJ, Redon CE, Sokolov MV, Sedelnikova OA, Bonner WM (2009) Intercellular communication of cellular stress monitored by gamma-H2AX induction. Carcinogenesis 30: 1686-1695
12. Fenech M (2007) Cytokinesis-block micronucleus cytome assay. Nat Protoc 2: 1084-1104 (Pubitemid 46901289)
13. Gow MD, Seymour CB, Ryan LA, Mothersill CE (2010) Induction of bystander response in human glioma cells using high-energy electrons: a role for TGF-beta1. Radiat Res 173: 769-778
14. Han W, Wu L, Chen S, Bao L, Zhang L, Jiang E, Zhao Y, Xu A, Hei TK, Yu Z (2007) 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 26: 2330-2339 (Pubitemid 46572816)
15. Han W, Wu L, Chen S, Yu KN (2009) Exogenous carbon monoxide protects the bystander Chinese hamster ovary cells in mixed coculture system after alpha-particle irradiation. Carcinogenesis 31: 275-280
16. Harada K, Nonaka T, Hamada N, Sakurai H, Hasegawa M, Funayama T, Kakizaki T, Kobayashi Y, Nakano T (2009) Heavy-ion-induced bystander killing of human lung cancer cells: role of gap junctional intercellular communication. Cancer Sci 100: 684-688
17. Harada T, Kashino G, Suzuki K, Matsuda N, Kodama S, Watanabe M (2008) Different involvement of radical species in irradiated and bystander cells. Int J Radiat Biol 84: 809-814
18. He M, Zhao M, Shen B, Prise KM, Shao C (2011) Radiation-induced intercellular signaling mediated by cytochrome-c via a p53-dependent pathway in hepatoma cells. Oncogene 30: 1947-1955
19. Ilnytskyy Y, Koturbash I, Kovalchuk O (2009) Radiation-induced bystander effects in vivo are epigenetically regulated in a tissue-specific manner. Environ Mol Mutagen 50: 105-113
20. Koturbash I, Boyko A, Rodriguez-Juarez R, McDonald RJ, Tryndyak VP, Kovalchuk I, Pogribny IP, Kovalchuk O (2007) Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis 28: 1831-1838 (Pubitemid 47289047)
21. Lehnert BE, Goodwin EH (1997) A new mechanism for DNA alterations induced by alpha particles such as those emitted by radon and radon progeny. Environ Health Perspect 105(Suppl 5): 1095-1101
22. Lemay R, Archambault M, Tremblay L, Bujold R, Lepage M, Paquette B (2011) Irradiation of normal mouse tissue increases the invasiveness of mammary cancer cells. Int J Radiat Biol 87: 472-482
23. Lewis DA, Mayhugh BM, Qin Y, Trott K, Mendonca MS (2001) Production of delayed death and neoplastic transformation in CGL1 cells by radiation-induced bystander effects. Radiat Res 156: 251-258 (Pubitemid 32801094)
24. Lyng FM, Seymour CB, Mothersill C (2002) Initiation of apoptosis in cells exposed to medium from the progeny of irradiated cells: a possible mechanism for bystander-induced genomic instability? Radiat Res 157: 365-370 (Pubitemid 34267248)
25. Mancuso M, Pasquali E, Leonardi S, Tanori M, Rebessi S, Di Majo V, Pazzaglia S, Toni MP, Pimpinella M, Covelli V, Saran A (2008) Oncogenic bystander radiation effects in Patched heterozygous mouse cerebellum. Proc Natl Acad Sci USA 105: 12445-12450
26. Matsumoto H, Hayashi S, Hatashita M, Ohnishi K, Shioura H, Ohtsubo T, Kitai R, Ohnishi T, Kano E (2001) Induction of radioresistance by a nitric oxide-mediated bystander effect. Radiat Res 155: 387-396 (Pubitemid 32204254)
27. Morgan WF, Sowa MB (2007) Non-targeted bystander effects induced by ionizing radiation. Mutat Res 616: 159-164 (Pubitemid 46206080)
28. Nagasawa H, Little JB (1992) Induction of sister chromatid exchanges by extremely low doses of alpha-particles. Cancer Res 52: 6394-6396
29. Narayanan PK, Goodwin EH, Lehnert BE (1997) Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res 57: 3963-3971 (Pubitemid 27427684)
30. Narayanan PK, LaRue KE, Goodwin EH, Lehnert BE (1999) Alpha particles induce the production of interleukin-8 by human cells. Radiat Res 152: 57-63 (Pubitemid 29296246)
31. Nathan C (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J 6: 3051-3064
32. Ogawa Y, Nishioka A, Kobayashi T, Kariya S, Hamasato S, Saibara T, Nakayama K, Seguchi H, Yoshida S (2002) Mitochondrial cytochrome c release in radiation-induced apoptosis of human peripheral T cells. Int J Mol Med 10: 263-268
33. Ogura A, Oowada S, Kon Y, Hirayama A, Yasui H, Meike S, Kobayashi S, Kuwabara M, Inanami O (2009) Redox regulation in radiation-induced cytochrome c release from mitochondria of human lung carcinoma A549 cells. Cancer Lett 277: 64-71
34. Palacios-Callender M, Hollis V, Mitchison M, Frakich N, Unitt D, Moncada S (2007) Cytochrome c oxidase regulates endogenous nitric oxide availability in respiring cells: a possible explanation for hypoxic vasodilation. Proc Natl Acad Sci USA 104: 18508-18513 (Pubitemid 350210727)
35. Peixoto PM, Ryu SY, Pruzansky DP, Kuriakose M, Gilmore A, Kinnally KW (2009) Mitochondrial apoptosis is amplified through gap junctions. Biochem Biophys Res Commun 390: 38-43
36. Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65: 27-33 (Pubitemid 24063526)
37. Sawant SG, Randers-Pehrson G, Geard CR, Brenner DJ, Hall EJ (2001) The bystander effect in radiation oncogenesis: I. Transformation in C3H 10T1/2 cells in vitro can be initiated in the unirradiated neighbors of irradiated cells. Radiat Res 155: 397-401 (Pubitemid 32204255)
38. Schagger H (2002) Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta 1555: 154-159 (Pubitemid 35246021)
39. Schettino G, Folkard M, Prise KM, Vojnovic B, Held KD, Michael BD (2003) Low-dose studies of bystander cell killing with targeted soft × rays. Radiat Res 160: 505-511 (Pubitemid 38055197)
40. Seymour CB, Mothersill C (1997) Delayed expression of lethal mutations and genomic instability in the progeny of human epithelial cells that survived in a bystander-killing environment. Radiat Oncol Investig 5: 106-110 (Pubitemid 27357906)
41. Shao C, Aoki M, Furusawa Y (2001) Medium-mediated bystander effects on HSG cells co-cultivated with cells irradiated by X-rays or a 290 MeV/u carbon beam. J Radiat Res (Tokyo) 42: 305-316 (Pubitemid 33613208)
42. Shao C, Aoki M, Furusawa Y (2003a) Bystander effect on cell growth stimulation in neoplastic HSGc cells induced by heavy-ion irradiation. Radiat Environ Biophys 42: 183-187 (Pubitemid 37518062)
43. Shao C, Aoki M, Furusawa Y (2004) Bystander effect in lymphoma cells vicinal to irradiated neoplastic epithelial cells: nitric oxide is involved. J Radiat Res (Tokyo) 45: 97-103 (Pubitemid 38698655)
44. Shao C, Folkard M, Held KD, Prise KM (2008a) Estrogen enhanced cell-cell signalling in breast cancer cells exposed to targeted irradiation. BMC Cancer 8: 184
45. Shao C, Folkard M, Michael BD, Prise KM (2005) Bystander signaling between glioma cells and fibroblasts targeted with counted particles. Int J Cancer 116: 45-51 (Pubitemid 40827753)
46. Shao C, Folkard M, Prise KM (2008b) Role of TGF-beta1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 27: 434-440
47. Shao C, Furusawa Y, Aoki M, Matsumoto H, Ando K (2002) Nitric oxidemediated bystander effect induced by heavy-ions in human salivary gland tumour cells. Int J Radiat Biol 78: 837-844
48. Shao C, Furusawa Y, Kobayashi Y, Funayama T, Wada S (2003b) Bystander effect induced by counted high-LET particles in confluent human fibroblasts: a mechanistic study. FASEB J 17: 1422-1427 (Pubitemid 36935656)
49. Shao C, Lyng FM, Folkard M, Prise KM (2006) Calcium fluxes modulate the radiation-induced bystander responses in targeted glioma and fibroblast cells. Radiat Res 166: 479-487 (Pubitemid 44353431)
50. Shao C, Prise KM, Folkard M (2008c) Signaling factors for irradiated glioma cells induced bystander responses in fibroblasts. Mutat Res 638: 139-145
51. Shao C, Stewart V, Folkard M, Michael BD, Prise KM (2003c) Nitric oxidemediated signaling in the bystander response of individually targeted glioma cells. Cancer Res 63: 8437-8442 (Pubitemid 37549500)
52. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA (1997) Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 276: 2034-2037 (Pubitemid 27443606)
53. Szabo C, Southan GJ, Thiemermann C (1994) Beneficial effects and improved survival in rodent models of septic shock with S-methylisothiourea sulfate, a potent and selective inhibitor of inducible nitric oxide synthase. Proc Natl Acad Sci USA 91: 12472-12476
54. Torres J, Sharpe MA, Rosquist A, Cooper CE, Wilson MT (2000) Cytochrome c oxidase rapidly metabolises nitric oxide to nitrite. FEBS Lett 475: 263-266 (Pubitemid 30408465)
55. Yang G, Wu L, Chen S, Zhu L, Huang P, Tong L, Zhao Y, Zhao G, Wang J, Mei T, Xu A, Wang Y (2009) Mitochondrial dysfunction resulting from loss of cytochrome c impairs radiation-induced bystander effect. Br J Cancer 100: 1912-1916
56. Yang H, Asaad N, Held KD (2005) Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 24: 2096-2103 (Pubitemid 40516203)