Exposure to heavy ion radiation induces persistent oxidative stress in mouse intestine

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Datta, Kamal ^a   Suman, Shubhankar ^a   Kallakury, Bhaskar V S ^b   Fornace, Albert J ^a,c  

^a GEORGETOWN UNIVERSITY   (United States)

^b GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; FEMALE; GAMMA RADIATION; INTESTINE; INTESTINE EPITHELIUM CELL; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MEMBRANE DAMAGE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOGENESIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; RADIATION DOSE; RADIATION EXPOSURE;

ANIMALS; CELLS, CULTURED; COSMIC RADIATION; DNA DAMAGE; EPITHELIAL CELLS; FEMALE; GAMMA RAYS; HEAVY IONS; INTESTINES; MICE; MICE, INBRED C57BL; NADPH OXIDASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84865287006     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042224     Document Type: Article

References (73)

1. Setlow RB, (2003) The hazards of space travel. EMBO Rep 4: 1013-1016.
2. Datta K, Purkayastha S, Neumann RD, Pastwa E, Winters TA, (2011) Base damage immediately upstream from double-strand break ends is a more severe impediment to nonhomologous end joining than blocked 3′-termini. Radiat Res 175: 97-112.
3. Sutherland BM, Bennett PV, Sidorkina O, Laval J, (2000) Clustered DNA damages induced in isolated DNA and in human cells by low doses of ionizing radiation. Proc Natl Acad Sci U S A 97: 103-108.
4. Hayatsu K, Hareyama M, Kobayashi S, Yamashita N, Sakurai K, et al. (2009) HZE Particle and Neutron Dosages from Cosmic Rays on the Lunar Surface. J Phys Soc Jpn 78: 149-152.
5. Durante M, Cucinotta FA, (2008) Heavy ion carcinogenesis and human space exploration. Nat Rev Cancer 8: 465-472.
6. Goodhead DT, (1994) Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol 65: 7-17.
7. Setlow RB, (1999) The U.S. National Research Council's views of the radiation hazards in space. Mutat Res 430: 169-175.
8. Datta K, Suman S, Trani D, Doiron K, Rotolo JA, et al. (2012) Accelerated hematopoietic toxicity by high energy (56)Fe radiation. Int J Radiat Biol 88: 213-222.
9. Reitz G, Beaujean R, Heckeley N, Obe G, (1993) Dosimetry in the space radiation field. Clin Investig 71: 710-717.
10. Cucinotta FA, Townsend LW, Wilson JW, Golightly MJ, Weyland M, (1994) Analysis of radiation risk from alpha particle component of solar particle events. Adv Space Res 14: 661-670.
11. Schimmerling W, (2010) Accepting space radiation risks. Radiat Environ Biophys 49: 325-329.
12. Stewart LH, Trunkey D, Rebagliati GS, (2007) Emergency medicine in space. J Emerg Med 32: 45-54.
13. CDC http://www.cdc.gov/cancer/colorectal/statistics.
14. Dupree-Ellis E, Watkins J, Ingle JN, Phillips J, (2000) External radiation exposure and mortality in a cohort of uranium processing workers. Am J Epidemiol 152: 91-95.
15. Gribbin MA, Weeks JL, Howe GR, (1993) Cancer mortality (1956-1985) among male employees of Atomic Energy of Canada Limited with respect to occupational exposure to external low-linear-energy-transfer ionizing radiation. Radiat Res 133: 375-380.
16. Thompson DE, Mabuchi K, Ron E, Soda M, Tokunaga M, et al. (1994) Cancer incidence in atomic bomb survivors. Part II: Solid tumors, 1958-1987. Radiat Res 137: S17-67.
17. Trani D, Datta K, Doiron K, Kallakury B, Fornace AJJ, (2010) Enhanced intestinal tumor multiplicity and grade in vivo after HZE exposure: mouse models for space radiation risk estimates. Radiat Environ Biophys 49: 389-396.
18. Brenner DJ, Miller RC, Huang Y, Hall EJ, (1995) The biological effectiveness of radon-progeny alpha particles. III. Quality factors. Radiat Res 142: 61-69.
19. Hamada N, (2009) Recent insights into the biological action of heavy-ion radiation. J Radiat Res (Tokyo) 50: 1-9.
20. Lenarczyk M, Cohen EP, Fish BL, Irving AA, Sharma M, et al. (2009) Chronic oxidative stress as a mechanism for radiation nephropathy. Radiat Res 171: 164-172.
21. Robbins ME, Zhao W, Davis CS, Toyokuni S, Bonsib SM, (2002) Radiation-induced kidney injury: a role for chronic oxidative stress? Micron 33: 133-141.
22. Datta K, Sinha S, Chattopadhyay P, (2000) Reactive oxygen species in health and disease. Natl Med J India 13: 304-310.
23. Robbins ME, Zhao W, (2004) Chronic oxidative stress and radiation-induced late normal tissue injury: a review. Int J Radiat Biol 80: 251-259.
24. Kim GJ, Fiskum GM, Morgan WF, (2006) A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Res 66: 10377-10383.
25. Leach JK, Van Tuyle G, Lin PS, Schmidt-Ullrich R, Mikkelsen RB, (2001) Ionizing radiation-induced, mitochondria-dependent generation of reactive oxygen/nitrogen. Cancer Res 61: 3894-3901.
26. Yoshida T, Goto S, Kawakatsu M, Urata Y, Li TS, (2011) Mitochondrial dysfunction, a probable cause of persistent oxidative stress after exposure to ionizing radiation. Free Radic Res.
27. Pazhanisamy SK, Li H, Wang Y, Batinic-Haberle I, Zhou D, (2011) NADPH oxidase inhibition attenuates total body irradiation-induced haematopoietic genomic instability. Mutagenesis 26: 431-435.
28. Wang Y, Liu L, Pazhanisamy SK, Li H, Meng A, et al. (2010) Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med 48: 348-356.
29. Bedard K, Krause KH, (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313.
30. Szanto I, Rubbia-Brandt L, Kiss P, Steger K, Banfi B, et al. (2005) Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J Pathol 207: 164-176.
31. Khor B, Gardet A, Xavier RJ, (2011) Genetics and pathogenesis of inflammatory bowel disease. Nature 474: 307-317.
32. Keskek M, Gocmen E, Kilic M, Gencturk S, Can B, et al. (2006) Increased expression of cyclooxygenase-2 (COX-2) in radiation-induced small bowel injury in rats. J Surg Res 135: 76-84.
33. Klaunig JE, Xu Y, Isenberg JS, Bachowski S, Kolaja KL, et al. (1998) The role of oxidative stress in chemical carcinogenesis. Environ Health Perspect 106 Suppl 1: 289-295.
34. Klaunig JE, Kamendulis LM, (2004) The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44: 239-267.
35. Toyokuni S, Okamoto K, Yodoi J, Hiai H, (1995) Persistent oxidative stress in cancer. FEBS Lett 358: 1-3.
36. Limoli CL, Giedzinski E, Baure J, Rola R, Fike JR, (2007) Redox changes induced in hippocampal precursor cells by heavy ion irradiation. Radiat Environ Biophys 46: 167-172.
37. Roig AI, Hight SK, Shay JW, (2009) Two- and three-dimensional models for risk assessment of radiation-enhanced colorectal tumorigenesis. Radiat Res 171: 33-40.
38. Asaithamby A, Uematsu N, Chatterjee A, Story MD, Burma S, et al. (2008) Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat Res 169: 437-446.
39. Desai N, Davis E, O'Neill P, Durante M, Cucinotta FA, et al. (2005) Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat Res 164: 518-522.
40. Takahashi A, Yamakawa N, Kirita T, Omori K, Ishioka N, et al. (2008) DNA damage recognition proteins localize along heavy ion induced tracks in the cell nucleus. J Radiat Res 49: 645-652.
41. Bissonnette R, Lee MJ, Wang E, (1990) The differentiation process of intestinal epithelial cells is associated with the appearance of statin, a non-proliferation-specific nuclear protein. J Cell Sci 95: 247-254.
42. Macartney KK, Baumgart DC, Carding SR, Brubaker JO, Offit PA, (2000) Primary murine small intestinal epithelial cells, maintained in long-term culture, are susceptible to rotavirus infection. J Virol 74: 5597-5603.
43. Sallmyr A, Fan J, Datta K, Kim KT, Grosu D, et al. (2008) Internal tandem duplication of FLT3 (FLT3/ITD) induces increased ROS production, DNA damage, and misrepair: implications for poor prognosis in AML. Blood 111: 3173-3182.
44. Huigsloot M, Tijdens IB, Mulder GJ, van de Water B, (2002) Differential regulation of doxorubicin-induced mitochondrial dysfunction and apoptosis by Bcl-2 in mammary adenocarcinoma (MTLn3) cells. J Biol Chem 277: 35869-35879.
45. Petrosillo G, Casanova G, Matera M, Ruggiero FM, Paradies G, (2006) Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release. FEBS Lett 580: 6311-6316.
46. Jacobson J, Duchen MR, Heales SJ, (2002) Intracellular distribution of the fluorescent dye nonyl acridine orange responds to the mitochondrial membrane potential: implications for assays of cardiolipin and mitochondrial mass. J Neurochem 82: 224-233.
47. Cui XL, Douglas JG, (1997) Arachidonic acid activates c-jun N-terminal kinase through NADPH oxidase in rabbit proximal tubular epithelial cells. Proc Natl Acad Sci U S A 94: 3771-3776.
48. Miro O, Alonso JR, Jarreta D, Casademont J, Urbano-Marquez A, et al. (1999) Smoking disturbs mitochondrial respiratory chain function and enhances lipid peroxidation on human circulating lymphocytes. Carcinogenesis 20: 1331-1336.
49. Machella N, Regoli F, Cambria A, Santella RM, (2004) Oxidative damage to DNA: an immunohistochemical approach for detection of 7,8-dihydro-8-oxodeoxyguanosine in marine organisms. Mar Environ Res 58: 725-729.
50. Leverkoehne I, Holle H, Anton F, Gruber AD, (2006) Differential expression of calcium-activated chloride channels (CLCA) gene family members in the small intestine of cystic fibrosis mouse models. Histochem Cell Biol 126: 239-250.
51. Skaland I, Janssen EA, Gudlaugsson E, Klos J, Kjellevold KH, et al. (2007) Phosphohistone H3 expression has much stronger prognostic value than classical prognosticators in invasive lymph node-negative breast cancer patients less than 55 years of age. Mod Pathol 20: 1307-1315.
52. Shillingford JM, Piontek KB, Germino GG, Weimbs T, (2010) Rapamycin ameliorates PKD resulting from conditional inactivation of Pkd1. J Am Soc Nephrol 21: 489-497.
53. Cucinotta FA, Schimmerling W, Wilson JW, Peterson LE, Badhwar GD, et al. (2001) Space radiation cancer risks and uncertainties for Mars missions. Radiat Res 156: 682-688.
54. Council NR (1999) Health Effects of Exposure to Radon: BEIR VI.
55. Morgan WF, (2003) Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene 22: 7094-7099.
56. Kurz DJ, Decary S, Hong Y, Trivier E, Akhmedov A, et al. (2004) Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J Cell Sci 117: 2417-2426.
57. Minter-Dykhouse K, Ward I, Huen MS, Chen J, Lou Z, (2008) Distinct versus overlapping functions of MDC1 and 53BP1 in DNA damage response and tumorigenesis. J Cell Biol 181: 727-735.
58. Ward IM, Difilippantonio S, Minn K, Mueller MD, Molina JR, et al. (2005) 53BP1 cooperates with p53 and functions as a haploinsufficient tumor suppressor in mice. Mol Cell Biol 25: 10079-10086.
59. Sam F, Kerstetter DL, Pimental DR, Mulukutla S, Tabaee A, et al. (2005) Increased reactive oxygen species production and functional alterations in antioxidant enzymes in human failing myocardium. J Card Fail 11: 473-480.
60. Yano S, Yano N, (2002) Regulation of catalase enzyme activity by cell signaling molecules. Mol Cell Biochem 240: 119-130.
61. Dumont P, Burton M, Chen QM, Gonos ES, Frippiat C, et al. (2000) Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radic Biol Med 28: 361-373.
62. von Zglinicki T, (2000) Role of oxidative stress in telomere length regulation and replicative senescence. Ann N Y Acad Sci 908: 99-110.
63. Dent P, Yacoub A, Contessa J, Caron R, Amorino G, et al. (2003) Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res 159: 283-300.
64. Fornace AJJ, Amundson SA, Do KT, Meltzer P, Trent J, et al. (2002) Stress-gene induction by low-dose gamma irradiation. Mil Med 167: 13-15.
65. Hickling KC, Hitchcock JM, Oreffo V, Mally A, Hammond TG, et al. (2010) Evidence of oxidative stress and associated DNA damage, increased proliferative drive, and altered gene expression in rat liver produced by the cholangiocarcinogenic agent furan. Toxicol Pathol 38: 230-243.
66. Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG, (1996) Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17: 1633-1639.
67. Limoli CL, Hartmann A, Shephard L, Yang CR, Boothman DA, et al. (1998) Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Res 58: 3712-3718.
68. Rugo RE, Schiestl RH, (2004) Increases in oxidative stress in the progeny of X-irradiated cells. Radiat Res 162: 416-425.
69. Goodhead DT, (1999) Mechanisms for the biological effectiveness of high-LET radiations. J Radiat Res (Tokyo) 40 Suppl: 1-13.
70. Katz R, Sharma SC, (1974) Heavy particles in therapy: an application of track theory. Phys Med Biol 19: 413-435.
71. Buonanno M, de Toledo SM, Pain D, Azzam EI, (2011) Long-term consequences of radiation-induced bystander effects depend on radiation quality and dose and correlate with oxidative stress. Radiat Res 175: 405-415.
72. Jain MR, Li M, Chen W, Liu T, de Toledo SM, et al. (2011) In vivo space radiation-induced non-targeted responses: late effects on molecular signaling in mitochondria. Curr Mol Pharmacol 4: 106-114.
73. Iborra M, Moret I, Rausell F, Bastida G, Aguas M, et al. (2011) Role of oxidative stress and antioxidant enzymes in Crohn's disease. Biochem Soc Trans 39: 1102-1106.