Low-dose gamma irradiation enhances superoxide anion production by nonirradiated cells through TGF-β1-dependent bystander signaling

Radiation Research

Volumn 179, Issue 4, 2013, Pages 422-432

  Temme, Jennifer ^a   Bauer, Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; SMALL INTERFERING RNA; SUPEROXIDE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CANCER CELL; CARCINOMA CELL; CELL COUNT; CELL POPULATION; CELL TRANSFORMATION; CONTROLLED STUDY; GAMMA IRRADIATION; GENE SILENCING; HUMAN; HUMAN CELL; KINETICS; LOW ENERGY RADIATION; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION RESPONSE; RAT; SIGNAL TRANSDUCTION; STOMACH CARCINOMA; TARGET CELL;

ANIMALS; BYSTANDER EFFECT; GAMMA RAYS; HUMANS; HYDRAZINES; NITRIC OXIDE; RATS; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDES; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84876262800     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR3161.2     Document Type: Article

References (55)

1. Nagasawa H, Little JB. Induction of sister chromatid exchanges by extremely low doses of alpha particles. Cancer Res 1992; 52:6394-6.
2. Kadhim MA, MacDonal DA, Goodhead DT, Lorimore SA,Marsden SJ, Wright EG. Transmission of chromosomal aberrations and genomic instablility after plutonium alpha particle irradiation. Nature 1992; 355:738-40.
3. Prise KM, Belyakov OV, Folkhard M, Michael BD. Studies of bystander effects in human fibroblasts using a charged particle microbeam. Int J Radiat Biol 1998; 74:793-8.
4. Little JB. Radiation carcinogenesis. Carcinogenesis 2000; 21:397-404.
5. Barcellos-Hoff MH, Brooks AL. Extracellular signaling through the microenvironment: a hypothesis relating carcinogenesis,bystander effects, and genomic instability. Radiat Res 2001; 156:618-27.
6. Little JB, Azzam EI, de Toledo SM, Nagasawa H. Bystander effects: intercellular transmission of radiation damage signals. Rad Protect Dosimetry 2002; 99:159-62.
7. Azzam EI, de Toledo SM, Little JB. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 2003; 22:7050-7.
8. Kadhim MA. Role of genetic background in induced instability. Oncogene 2003; 22:6994-9.
9. Lorimore SA, Coates PJ, Wright EG. Radiation-induced genomic instability and bystander effects: inter-related nontargeted effects of exposure to ionizing radiation. Oncogene 2003; 22:7058-69.
10. Mothersill C, Seymour C. Radiation-induced bystander effects, carcinogenesis and models. Oncogene 2003; 22:7028-33.
11. Matsumoto H, Hamada N, Takahashi A, Kobayashi Y, Ohnishi T. Vanguards of paradigm shift in radiation biology: radiationinduced adaptive and bystander responses. J Radiat Res 2007; 48:97-106.
12. Spitz DR, Azzam EI, Li JJ, Gius D. Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifiying concept in stress response biology. Cancer Metast Rev 2004: 23:311-22.
13. Bauer G. Low dose radiation and intercellular induction of apoptosis: potential implications for the control of oncogenesis. Int J Radiat Biol 2007; 83:887-902.
14. Portess DI, Bauer G, Hill MA, O'Neill P. Low dose irradiation of nontransformed cells stimulates the selective removal of precancerous cells via intercellular induction of apoptosis. Cancer Res 2007; 67:1246-53.
15. Bauer G. Reactive oxygen and nitrogen species: efficient, selective and interactive signals during intercellular induction of apoptosis. Anticancer Res 2000; 20:4115-40.
16. Jürgensmeier J, Schmitt CP, Viesel E, Höfler P, Bauer G. TGFbeta- treated normal fibroblasts eliminate transformed fibroblasts by induction of apoptosis. Cancer Res 1994; 54:393-8.
17. Herdener M, Heigold S, Saran M, Bauer G. Target cell-derived superoxide anions cause efficiency and selectivity of intercellular induction of apoptosis. Free Radic Biol Med 2000; 29:1260-71.
18. Bechtel W, Bauer G. Catalase protects tumor cells from apoptosis induction by intercellular ROS signaling. Anticancer Res 2009; 29:4541-57.
19. Bauer G. Low dose gamma irradiation enhances defined signaling components of intercellular reactive oxygen-mediated apoptosis induction. J Physicians Conf Ser 2011; 261:012001.
20. Bauer G. Tumor cell protective catalase as a novel target for rational therapeutic approaches based on specific intercellular ROS signaling. Anticancer Res 2012; 32: 2599-624.
21. Heinzelmann S, Bauer G. Multiple protective functions of catalase against intercellular apoptosis-inducing ROS signaling of human tumor cells. Biol Chem 2010; 391:675-93.
22. Heigold S, Sers C, Bechtel W, Ivanovas B, Schafer R, Bauer G. Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts. Carcinogenesis 2002; 23:929-41.
23. Engelmann I, Eichholtz-Wirth H, Bauer G. Ex vivo tumor cell lines are resistant against intercellular induction of apoptosis and independent of exogenous survival factors. Anticancer Res 2000; 20:2361-70.
24. Bauer G, Höfler P, Simon M. Epstein-Barr virus induction by a serum factor. Purification of a high molecular weight protein that is responsible for induction. J Biol Chem 1982; 257:11405-10.
25. Schwieger A, Bauer L, Hanusch J, Sers C, Schafer R, Bauer G. Ras oncogene expression determines sensitivity for intercellular induction of apoptosis. Carcinogenesis 2001; 22:1385-92.
26. Beck E, Schafer R, Bauer G. Sensitivity of transformed fibroblasts for intercellular induction of apoptosis is determined by their transformed phenotype. Exp Cell Res 1997; 234:47-56.
27. Barcellos-Hoff MH. Latency and Activation in the Control of TGF-b. J Mammary Gland Biol Neoplasia 1996; 1:353-63.
28. Massagué J, ChenY-G. Controlling TGF-beta signaling. Genes and Devel 2000; 14:627-44.
29. Barcellos-Hoff MH. How tissues respond to damage at the cellular level: orchestration by transforming growth factor-beta (TGFbeta). Br J Radiol 2005; 27(Suppl.):123-7.
30. Barcellos-Hoff MH, Park C, Wright EG. Radiation and the microenvironment - tumorigenesis and therapy. Nature Rev Cancer 2005; 5:867-75.
31. Fleisch MC, Maxwell CA, Barcellos-Hoff MH. The pleiotropic roles of transforming growth factor beta in homeostasis and carcinogenesis of endocrine organs. Endocr Cancer 2006; 13:379-400.
32. Kaminska B, Wesolowska A, Danilkiewicz M. TGF beta signalling and its role in tumour pathogenesis. Acta Biochim Polon 2005; 52:329-37.
33. Thannickal VJ, Fanberg BL. Activation of an H2O2-generating NADH oxidase in human lung fibroblasts by transforming growth factor beta1. J Biol Chem 1995; 270:30334-8.
34. Lafon C, Mathieu C, Guerrin M, Pierro O, Vidal S, Valetta A. Transforming growth factor beta-induced apoptosis in human ovarian carcinoma cells: Protection by the antioxidant Nacetylcysteine and bcl-2. Cell Growth Differ 1996; 7:1095-104.
35. Sànchez A, Alvarez AM, Benito M, Fabregat I. Apoptosis induced by transforming growth factor-beta in fetal hepatocyte primary cultures: Involvement of reactive oxygen intermediates. J Biol Chem 1996; 271:7416-22.
36. Ribeiro A, Bronk SF, Roberts PJ, Urrutia R, Gores GJ. The transforming growth factor beta(1)-inducible transcription factor TIEG1 mediates apoptosis through oxidative stress. Hepatol 1999; 30:1490-7.
37. Chiu C, Maddock DA, Zhang Q, Souza KP, Townsend AR, Wan Y. TGF-beta-induced p38 activation is mediated by Rac-1- regulated generation of reactive oxygen species in cultured human keratinocytes. Int J Mol Med 2001; 8:251-5.
38. Hu T, RamachandraRao SP, Siva S, Valancius C, Zhu Y, Mahadev K, Toh I, et al. Reactive oxygen species production via NADPH oxidase mediates TGF-beta-induced cytoskeletal alterations in endothelial cells. Am J Physiol Renal Physiol 2005; 289:816-25.
39. Carmona-Cuenca I, Roncero C, Sancho P, Caja L, Fausto N,Fernandez M, Fabregat I. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J Hepatol 2008; 49:965-76.
40. Sturrock A, Cahill B, Normann K, Hueckstadedt TP, Hill K,Sanders K, Karvande SV, Stringham JC, Bull DA, Gleich M,Kennedy TP, Hoidal Jr. Transforming growth factor beta-1 induces NOX4 NAD(P)H oxidase and reactive oxygen speciesdependent proliferation in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 2006; 290:L661-73.
41. Proell V, Carmona-Cuenca I, Murillo MM, Huber H, Fabregat I,Mikulits W. TGF-b-dependent regulation of oxygen radicals during transdifferentiation of activated hepatic stellate cells to myofibroblastoid cells. Comp Hepatol 2007; 6:1-12.
42. Sancho P, Bertram E, Caja L, Carmona-Cuenca I, Murillo MM,Fabregat I. The inhibition of the epidermal growth factor (EGF) pathway enhances TGF-beta-induced apoptosis in rat hepatoma cells through inducing oxidative stress coincident with a change in the expression pattern of the NADPH oxidases (NOX) isoforms. Biochim Biophys Acta 2009; 1793:253-63.
43. Ehrhardt EJ, Segarini P, Tsang MLS, Carroll AG, Barcellos-Hoff MH. Latent transforming growth factor b1 activation in situ: quantitative and functional evidence after low-dose c-irradiation. Faseb J 1997; 11:991-1002.
44. Shao C, Folkard M, Prise KM. Role of TGF-beta1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 2008; 27:434-40.
45. Barcellos-Hoff MH, Dix TA. Redox-mediated activation of latent transforming growth factor-beta-1. Mol Endocrinol 1996; 10:1077-83
46. Van Obberghen-Schilling E, Roche NS, Flanders KC, Sporn MB,Roberts AB. Transforming growth factor beta 1 positively regulates its own expression in normal and transformed cells. J Biol Chem 1988; 263:7741-6.
47. Kim S-J, Angel P, Lafyatis R, Hattori K, Kim KY, Sporn MB, et al. Autoinduction of transforming growth factor beta-1 is mediated by the AP-1 complex. Mol Cell Biol 1990; 10:1492-7.
48. Jobling ME, Mott JD, Finnegan MT, Jurukovski V, Erickson AC,Walian PJ, et al. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiat Res 2006; 166:839-48.
49. Nath KA, Grande J, Croatt A, Haugen J, Kim Y, Rosenberg ME. Redox regulation of renal DNA synthesis, transforming growth factor-b1 and collagen gene expression. Kidney Internat 1998; 53:367-81.
50. Iglesias-De La Cruz MC, Ruiz-Torres P, Alcamí J, Di'ez-Marque's L, Ortega-Vela'zquez R, Chen S, et al. Hydrogen peroxide increases extracellular matrix mRNA trough TGF-beta in human mesangial cells. Kidney Internat 2001; 59:87-95.
51. Vodovotz Y, Chesler L, Chong HK, Kim SJ, Simpson JT, DeGraff W, et al. Regulation of transforming growth factor beta 1 by nitric oxide. Cancer Res 1999; 59:2142-9.
52. Azzam EI, de Toledo SM, Raaphorst GP, Mitchel RE. Low-dose ionizing radiation decreases the frequency of neoplastic transformation to a level below the spontaneous rate in C3H 10 T1/2 cells. Radiat Res 1996; 146:369-73.
53. Pant MC, Liao XY, Lu O, Molloi S, Elmore E, Redpath JL. Mechanisms of suppression of neoplastic transformation in vitro by low doses of low LET radiation. Carcinogenesis 2003; 24:1961-5.
54. Redpath JL, Lu Q, Lao X, Molloi S, Elmore E. Low doses of diagnostic X-rays protect against neoplastic transformation in vitro. Int J Radiat Biol 2003; 79:235-40.
55. Elmore E, Lao XY, Kapadia R, Redpath JL. The effect of dose rate on radiation induced neoplastic transformation in vitro by low doses of low-LET radiation. Radiat Res 2006; 166:832-8.