A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability

Cancer Research

Volumn 66, Issue 21, 2006, Pages 10377-10383

  Kim, Grace J ^a   Fiskum, Gary M ^a   Morgan, William F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CELL MEMBRANE PERMEABILITY; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; CYTOMETRY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENOMIC INSTABILITY; INCIDENCE; MUTATION; NONHUMAN; PRIORITY JOURNAL; RADIATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHO CELLS; CRICETINAE; GENOMIC INSTABILITY; HYDROGEN PEROXIDE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 33750633422     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-3036     Document Type: Article

References (55)

1. Little JB. Radiation carcinogenesis. Carcinogenesis 2000;21:397-404.
2. Morgan WF. Non-targeted and Delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res 2003;159:567-80.
3. Ullrich RL, Ponnaiya B. Radiation-induced instability and its relation to radiation carcinogenesis. Int J Radiat Biol 1998;74:747-54.
4. Snyder AR, Morgan WF. Radiation-induced chromosomal instability and gene expression profiling: searching for clues to initiation and perpetuation. Mutat Res 2004;568:89-96.
5. Limoli CL, Corcoran JJ, Milligan JH, Ward JF, Morgan WF. Critical target and dose and dose-rate responses for the induction of chromosomal instability by ionizing radiation. Radiat Res 1999;151:677-85.
6. Spitz DR, Azzam EI, Li JJ, Gius D. Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev 2004;23:311-22.
7. Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 1996;17:1633-9.
8. Limoli CL, Giedzinski E, Morgan WF, Swarts SG, Jones GD, Hyun W. Persistent oxidative stress in chromosomally unstable cells. Cancer Res 2003;63:3107-11.
9. Limoli CL, Hartmann A, Shephard L, et al. Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Res 1998;58:3712-8.
10. Hunt CR, Sim JE, Sullivan SJ, et al. Genomic instability and catalase gene amplification induced by chronic exposure to oxidative stress. Cancer Res 1998;58:3986-92.
11. Limoli CL, Giedzinski E. Induction of chromosomal instability by chronic oxidative stress. Neoplasia 2003;5:339-46.
12. Limoli CL, Kaplan MI, Giedzinski E, Morgan WF. Attenuation of radiation-induced genomic instability by free radical scavengers and cellular proliferation. Free Radic Biol Med 2001;31:10-9.
13. Roy K, Kodama S, Suzuki K, Fukase K, Watanabe M. Hypoxia relieves X-ray-induced delayed effects in normal human embryo cells. Radiat Res 2000;154:659-66.
14. Hall EJ. Radiobiology for the radiologist, 5th ed. Philadelphia: Lippincott Williams & Wilkins; 2000.
15. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005;120:483-95.
16. Boveris A, Oshino N, Chance B. The cellular production of hydrogen peroxide. Biochem J 1972;128:617-30.
17. Wei YH, Lu CY, Lee HC, Pang CY, Ma YS. Oxidative damage and mutation to mitochondrial DNA and age-dependent decline of mitochondrial respiratory function. Ann N Y Acad Sci 1998;854:155-70.
18. Singh KK. Mitochondrial dysfunction is a common phenotype in aging and cancer. Ann N Y Acad Sci 2004;1019:260-4.
19. Shidara Y, Yamagata K, Kanamori T, et al. Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 2005;65:1655-63.
20. Limoli CL, Ponnaiya B, Corcoran JJ, Giedzinski E, Morgan WF. Chromosomal instability induced by heavy ion irradiation. Int J Radiat Biol 2000;76:1599-606.
21. Marder BA, Morgan WF. Delayed chromosomal instability induced by DNA damage. Mol Cell Biol 1993;13:6667-77.
22. Limoli CL, Kaplan MI, Corcoran J, Meyers M, Boothman DA, Morgan WF. Chromosomal instability and its relationship to other end points of genomic instability. Cancer Res 1997;57:5557-63.
23. Nagar S, Smith LE, Morgan WF. Characterization of a novel epigenetic effect of ionizing radiation: the death-inducing effect. Cancer Res 2003;63:324-8.
24. 2 production by membrane potential and NAD(P)H redox state. J Neurochem 2003;86:1101-7.
25. Pendergrass W, Wolf N, Poot M. Efficacy of MitoTracker Green and CMXrosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A 2004;61:162-9.
26. Petit JM, Maftah A, Ratinaud MH, Julien R. 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 1992;209:267-73.
27. Garcia Fernandez MI, Ceccarelli D, Muscatello U. Use of the fluorescent dye 10-N-nonyl acridine orange in quantitative and location assays of cardiolipin: a study on different experimental models. Anal Biochem 2004;328:174-80.
28. Nisoli E, Clementi E, Paolucci C, et al. Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 2003;299:896-9.
29. Nass MM. Restriction map of Chinese hamster mitochondrial DNA containing replication coordinates: comparison with Syrian hamster mitochondrial genome. Gene 1983;21:249-55.
30. Fiskum G, Kowaltowksi AJ, Andreyev AY, Kushnareva YE, Starkov AA. Apoptosis-related activities measured with isolated mitochondria and digitonin-permeabilized cells. Methods Enzymol 2000;322:222-34.
31. Trounce IA, Kim YL, Jun AS, Wallace DC. Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 1996;264:484-509.
32. Storrie B, Madden EA. Isolation of subcellular organelles. Methods Enzymol 1990;182:203-25.
33. Spitz DR, Oberley LW. An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 1989;179:8-18.
34. Wredenberg A, Wibom R, Wilhelmsson H, et al. Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci U S A 2002;99:15066-71.
35. Wiedemann FR, Manfredi G, Mawrin C, Beal MF, Schon EA. Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J Neurochem 2002;80:616-25.
36. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol 2003;552:335-44.
37. Geromel V, Kadhom N, Cebalos-Picot I, et al. Superoxide-induced massive apoptosis in cultured skin fibroblasts harboring the neurogenic ataxia retinitis pigmentosa (NARP) mutation in the ATPase-6 gene of the mitochondrial DNA. Hum Mol Genet 2001;10:1221-8.
38. Steyn SJ, Pieterse DJ, Mienie LJ, Van der Schyf CJ. Measurement of mitochondrial respiration in permeabilized murine neuroblastoma (N-2α) cells, a simple and rapid in situ assay to investigate mitochondrial toxins. J Biochem Biophys Methods 2005;62:25-40.
39. Ishii T, Yasuda K, Akatsuka A, Hino O, Hartman PS, Ishii N. A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res 2005;65:203-9.
40. Bandy B, Davison AJ. Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radic Biol Med 1990;8:523-39.
41. Walker DW, Benzer S. Mitochondrial "swirls" induced by oxygen stress and in the Drosphila mutant hyperswirl. Proc Natl Acad Sci U S A 2004;101:10290-5.
42. Laurent A, Nicco C, Chereau C, et al. Controlling tumor growth by modulating endogenous production of reactive oxygen species. Cancer Res 2005;65:948-56.
43. Enns GM. The contribution of mitochondria to common disorders. Mol Genet Metab 2003;80:11-26.
44. Selvanayagam CS, Davis CM, Cornforth MN, Ullrich RL. Latent expression of p53 mutations and radiation-induced mammary cancer. Cancer Res 1995;55:3310-7.
45. Copeland WC, Wachsman JT, Johnson FM, Penta JS. Mitochondrial DNA alterations in cancer. Cancer Invest 2002;20:557-69.
46. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and implications in human pathology. IUBMB Life 2001;52:159-64.
47. Dawson TL, Gores GJ, Nieminen AL, Herman B, Lemasters JJ. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am J Physiol 1993;264:C961-7.
48. Kamendulis LM, Zhang H, Wang Y, Klaunig JE. Morphological transformation and oxidative stress induced by cyanide in Syrian hamster embryo (SHE) cells. Toxicol Sci 2002;68:437-43.
49. MacMillan-Crow LA, Thompson JA. Tyrosine modifications and inactivation of active site manganese superoxide dismutase mutant (Y34F) by peroxynitrite. Arch Biochem Biophys 1999;366:82-8.
50. Ramirez DC, Gomez Mejiba SE, Mason RP. Mechanism of hydrogen peroxide-induced Cu,Zn-superoxide dismutase-centered radical formation as explored by immuno-spin trapping: the role of copper- and carbonate radical anion-mediated oxidations. Free Radic Biol Med 2005;38:201-14.
51. Oberley LW. Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother 2005;59:143-8.
52. St. Clair DK, Wan XS, Oberley TD, Muse KE, St Clair WH. Suppression of radiation-induced neoplastic transformation by overexpression of mitochondrial superoxide dismutase. Mol Carcinog 1992;6:238-42.
53. Samper E, Nicholls DG, Melov S. Mitochondrial oxidative stress causes chromosomal instability of mouse embryonic fibroblasts. Aging Cell 2003;2:277-85.
54. Nagar S, Smith LE, Morgan WF. Variation in apoptosis profiles in radiation-induced genomically unstable cell lines. Radiat Res 2005;163:324-31.
55. Snyder AR, Morgan WF. Differential induction and activation of NF-κB transcription complexes in radiation-induced chromosomally unstable cell lines. Environ Mol Mutagen 2005;45:177-87.