Analysis of the common deletions in the mitochondrial DNA is a sensitive biomarker detecting direct and non-targeted cellular effects of low dose ionizing radiation

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 716, Issue 1-2, 2011, Pages 33-39

  Schilling Tóth, Boglárka ^a   Sándor, Nikolett ^a   Kis, Eniko ^a   Kadhim, Munira ^b   Sáfrány, Géza ^a   Hegyesi, Hargita ^a  

^a National Research Institute for Radiobiology and Radiohygiene Budapest   (Hungary)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Bystander effect; Delayed effect; Individual radiosensitivity; Low dose radiation; Mitochondrial common deletion

Indexed keywords

BIOLOGICAL MARKER; MITOCHONDRIAL DNA;

ARTICLE; BYSTANDER EFFECT; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; FIBROBLAST; GENE DELETION; HUMAN; HUMAN CELL; IONIZING RADIATION; MITOCHONDRIAL GENE; PRIORITY JOURNAL; RADIATION RESPONSE; RADIOSENSITIVITY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME;

BIOLOGICAL MARKERS; BYSTANDER EFFECT; DNA, MITOCHONDRIAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; HUMANS; RADIATION TOLERANCE; RADIATION, IONIZING; REAL-TIME POLYMERASE CHAIN REACTION; SEQUENCE DELETION; TIME FACTORS;

EID: 80053574426     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2011.07.018     Document Type: Article

References (63)

1. The 2007 Recommendations of the International Commission on Radiological Protection, ICRP Publication 103, Ann. ICRP 37 (2-4) (2007) http://www.icrp.org/publication.asp?id=ICRP%20Publication%20103.
2. High Level Expert Group on European Low Dose Risk Research, http://www.hleg.de/fr.pdf.
3. Shao C., Folkard M., Michael B.D., Prise K.M. Targeted cytoplasmic irradiation induces bystander responses. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:13495-13500.
4. Morgan W.F., Sowa M.B. Non-targeted effects of ionizing radiation: implications for risk assessment and the radiation dose response profile. Health Phys. 2009, 97:426-432.
5. Seymour C.B., Mothersill C. Relative contribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Radiat. Res. 2000, 153:508-511.
6. Sowa M.B., Goetz W., Baulch J.E., Pyles D.N., Dziegielewski J., Yovino S., Snyder A.R., de Toledo S.M., Azzam E.I., Morgan W.F. Lack of evidence for low-LET radiation induced bystander response in normal human fibroblasts and colon carcinoma cells. Int. J. Radiat. Biol. 2010, 86:102-113.
7. Nagasawa H., Little J.B. Induction of sister chromatid exchanges by extremely low doses of α-particles. Cancer Res. 1992, 52:6394-6396.
8. Prise K.M., Belyakov O.V., Folkard M., Michael B.D. Studies of bystander effects in human fibroblasts using a charged particle microbeam. Int. J. Radiat. Biol. 1998, 74:793-798.
9. Azzam E.I., de Toledo S.M., Little J.B. Oxidative metabolism, gap junctions and the ionizing radiation-induced bystander effect. Oncogene 2003, 22:7050-7057.
10. Kadhim M.A Role of genetic background in induced instability. Oncogene 2003, 22:6994-6999.
11. Hu B., Wu L., Han W., Zhang L., Chen S., Xu A., Hei T.K., Yu Z. The time and spatial effects of bystander response in mammalian cells induced by low dose radiation. Carcinogenesis 2006, 27:245-251.
12. Hall E.J. The bystander effect. Health Phys. 2003, 85:31-35.
13. Ghandhi S.A., Yaghoubian B., Amundson S.A. Global gene expression analyses of bystander and alpha particle irradiated normal human lung fibroblasts: synchronous and differential responses. BMC Med. Genomics 2008, 1:63.
14. Yang H., Asaad N., Held K.D. Medium-mediated intercellular communication is involved in bystander responses of X-ray-irradiated normal human fibroblasts. Oncogene 2005, 24:2096-2103.
15. Mothersill C., Seymour C. Medium from irradiated human epithelial cells but not human fibroblasts reduces the clonogenic survival of unirradiated cells. Int. J. Radiat. Biol. 1997, 71:421-427.
16. Salomaa S.I., Wright E.G., Hildebrandt G., Kadhim M.A., Little M.P., Prise K.M., Belyakov O.V. Non-DNA targeted effect. Mutat. Res. 2010, 687:1-2.
17. Prithivirajsingh S., Story M.D., Bergh S.A., Geara F.B., Ang K.K., Ismail S.M., Stevens C.W., Buchholz T.A., Brock W.A. Accumulation of the common mitochondrial DNA deletion induced by ionizing radiation. FEBS Lett. 2004, 571:227-232.
18. Murphy J.E., Nugent S., Seymour C., Mothersill C. Mitochondrial DNA point mutations and a novel deletion induced by direct low-LET radiation and by medium from irradiated cells. Mutat. Res. 2005, 585:127-136.
19. Schon E.A., Rizzuto R., Moraes C.T., Nakase H., Zeviani M., DiMauro S. A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science 1989, 244:346-349.
20. Eshaghian A., Vleugels R.A., Canter J.A., McDonald M.A., Stasko T., Sligh J.E. Mitochondrial DNA deletions serve as biomarkers of aging in the skin, but are typically absent in nonmelanoma skin cancers. J. Invest. Dermatol. 2006, 126:336-344.
21. Fukui H., Moraes C.T. Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons. Hum. Mol. Genet. 2009, 18:1028-1036.
22. Ito S., Ohta S., Nishimaki K., Kagawa Y., Soma R., Kuno S.Y., Komatsuzaki Y., Mizusawa H., Hayashi J.I. Functional integrity of mitochondrial genomes in human platelets and autopsied brain tissues from elderly patients with Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A., Cell Biol. 1999, 96:2099-2103.
23. Zeviani M., Moraes C.T., DiMauro S., Nakase H., Bonilla E., Schon E.A., Rowland L.P. Deletions of mitochondrial DNA in Kearns-Sayre syndrome. Neurology 1998, 51:1525.
24. Ramirez-Miranda A., Navas-Perez A., Gurria-Quintana L., Vargas-Ortega J., Murillo-Correa C., Zenteno J.C. PCR-based detection of heteroplasmic deleted mitochondrial DNA in Kearns-Sayre syndrome. Arch. Soc. Esp. Ophtalmol. 2008, 83:155-160.
25. Rotig A., Cormier V., Blanche S., Bonnefont J.P., Ledeist F., Romero N., Schmitz J., Rustin P., Fischer A., Saudubray J.M. Pearson marrow pancreas syndrome - a multisystem mitochondrial disorder in infancy. J. Clin. Invest. 1990, 86:1601-1608.
26. Sciacco M., Bonilla E., Schon E.A., DiMauro S., Moraes C.T. Distribution of wild-type and common deletion forms of mtDNA in normal and respiration-deficient muscle-fibers from patients with mitochondrial myopathy. Hum. Mol. Genet. 1994, 3:687.
27. Wallace D.C. Mitochondrial diseases in man and mouse. Science 1999, 283:1482.
28. Zeviani M., Di Donauto S. Mitochondrial disorders. Brain 2004, 127:2153-2172.
29. Liu C.S., Ko L.Y., Lim P.S., Kao S.H., Wei Y.H. Biomarkers of DNA damage in patients with end-stage renal disease: mitochondrial DNA mutation in hair follicles. Nephrol. Dial. Transplant. 2001, 16:561-565.
30. Rogounovitch T.I., Saenko V.A., Shimizu-Yoshida Y., Abrosimov A.Y., Lushnikov E.F., Roumiantsev P.O., Ohtsuru A., Namba H., Tsyb A.F., Yamashita S. Large deletions in mitochondrial DNA in radiation-associated human thyroid tumors. Cancer Res. 2002, 62:7031-7041.
31. Dai J.G., Xiao Y.B., Min J.X., Zhang G.Q., Yao K., Zhou R.J. Mitochondrial DNA 4977 BP deletion mutations in lung carcinoma. Indian J. Cancer 2006, 43:20-25.
32. Polyak K., Li Y., Zhu H., Lengauer C., Willson J.K., Markowitz S.D., Trush M.A., Kinzler K.W., Vogelstein B. Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat. Genet. 1998, 20:291-293.
33. Tseng L.M., Yin P.H., Tsai Y.F., Chi C.W., Wu C.W., Lee L.M., Lee H.C. Association between mitochondrial DNA 4,977bp deletion and NAD(P)H:quinone oxidoreductase 1 C609T polymorphism in human breast tissues. Oncol. Rep. 2009, 21:1169-1174.
34. Berneburg M., Plettenberg H., Medve-König K., Pfahlberg A., Gers-Barlag H., Gefeller O., Krutmann J. Induction of the photoaging-associated mitochondrial common deletion in vivo in normal human skin. J. Invest. Dermatol. 2004, 122:1277-1283.
35. Wei Y.H., Lee H.C. Oxidative stress, mitochondrial DNA mutation, and impairment of antioxidant enzymes in aging. Exp. Biol. Med. 2002, 227:671-682.
36. Kubota N., Hayashi J.I., Inada T., Iwamura Y. Induction of a particular deletion in mitochondrial DNA by X-rays depends on the inherent radiosensitivity of the cells. Radiat. Res. 1997, 148:395-398.
37. Nicklas J.A., Brooks E.M., Hunter T.C., Single R., Branda R.F. Development of a quantitative PCR (TaqMan) assay for relative mitochondrial DNA copy number and the common mitochondrial DNA deletion in the rat. Environ. Mol. Mutagen. 2004, 44:313-320.
38. Kis E., Szatmári T., Keszei M., Farkas R., Ésik O., Lumniczky K., Falus A., Sáfrány G. Microarray analysis of radiation response genes in primary human fibroblasts. Int. J. Radiat. Oncol. Biol. Phys. 2006, 66:1506-1514.
39. Steel G.G. Cell survival as a determinant of tumour response. Basic Clinical Radiobiology 2002, 52-63. Arnold, London, UK. G.G. Steel (Ed.).
40. Natarajan A.T., Boei J.J., Darroudi F., Van Diemen P.C., Dulout F., Hande M.P., Ramalho A.T. Current cytogenetic methods for detecting exposure and effects of mutagens and carcinogens. Environ. Health Perspect. 1996, 104:445-448.
41. Blakely W.F., Miller A.C., Luo L., Lukas J., Hornby Z.D., Hamel C.J., Nelson J.T., Escalada N.E., Prasanna P.G. Nucleic acid molecular biomarkers for diagnostic biodosimetry applications: use of the fluorogenic 5'-nuclease polymerase chain reaction assay. Mil Med. 2002, 167:16-19.
42. Pogozelski W.K., Hamel C.J., Woeller C.F., Jackson W.E., Zullo S.J., Fischel-Ghodsian N., Blakely W.F. Quantification of total mitochondrial DNA and the 4977-bp common deletion in Pearson's syndrome lymphoblasts using a fluorogenic 5'-nuclease (TaqMan) real-time polymerase chain reaction assay and plasmid external calibration standards. Mitochondrion 2003, 2:415-427.
43. Krishnan K.J., Birch-Machin M.A. The incidence of both tandem duplications and the common deletion in mtDNA from three distinct categories of sun-exposed human skin and in prolonged culture of fibroblasts. J. Invest. Dermatol. 2006, 126:408-415.
44. Krishnan K.J., Bender A., Taylor R.W., Turnbull D.M. A multiplex real-time PCR method to detect and quantify mitochondrial DNA deletions in individual cells. Anal. Biochem. 2007, 370:127-129.
45. Koch H., Wittern K.P., Bergemann J. In human keratinocytes the common deletion reflects donor variabilities rather than chronologic aging and can be induced by ultraviolet A irradiation. J. Invest. Dermatol. 2001, 117:892-897.
46. Ouweland J.M., Klerk J.B., Corput M.P., Dirks R.W., Raap A.K., Scholte H.R., Huijmans J.G., Hart L.M., Bruining G.J., Maassen J.A. Characterization of a novel mitochondrial DNA deletion in a patient with a variant of the Pearson marrow-pancreas syndrome. Eur. J. Hum. Genet. 2000, 8:195-203.
47. Majora M., Wittkampf T., Schuermann B., Schneider M., Franke S., Grether-Beck S., Wilichowski E., Bernerd F., Schroeder P., Krutmann J. Functional consequences of mitochondrial DNA deletions in human skin fibroblasts: increased contractile strength in collagen lattices is due to oxidative stress-induced lysyl oxidase activity. Am. J. Pathol. 2009, 175:1019-1029.
48. Nagasawa H., Wilson P.F., Chen D.J., Thompson L.H., Bedford J.S., Little J.B. Low doses of alpha particles do not induce sister chromatid exchanges in bystander Chinese hamster cells defective in homologous recombination. DNA Repair 2008, 7:515-522.
49. Kadhim M.A., Lee R., Moore S.R., Macdonald D.A., Chapman K.L., Patel G., Prise K.M. Genomic instability after targeted irradiation of human lymphocytes: evidence for inter-individual differences under bystander conditions. Mutat. Res. 2010, 688:91-94.
50. Limoli C.L., Corcoran J.J., Milligan J.R., Ward J.F., Morgan W.F. Critical target and dose and dose-rate responses for the induction of chromosomal instability by ionizing radiation. Radiat. Res. 1999, 151:677-685.
51. Mothersill C., Seymour C.B., Joiner M.C. Relationship between radiation-induced low-dose hypersensitivity and the bystander effect. Radiat. Res. 2002, 157:526-532.
52. Vines A.M., Lyng F.M., McClean B., Seymour C., Mothersill C.E. Bystander signal production and response are independent processes which are cell line dependent. Int. J. Radiat. Biol. 2008, 84:83-90.
53. Laiakis E.C., Baulch J.E., Morgan W.F. Cytokine and chemokine responses after exposure to ionizing radiation: implications for the astronauts. Adv. Space Res. 2007, 39:1019-1025.
54. Morgan W.F., Sowa M.B. Non-targeted bystander effects induced by ionizing radiation. Mutat. Res. 2007, 616:159-164.
55. Lumniczky K., Sáfrány G. Cancer gene therapy: combination with radiation therapy and the role of the bystander cell killing in the anti-tumor effect. Pathol. Oncol. Res. 2006, 12:118-124.
56. Limoli C.L., Ponnaiya B., Corcoran J.J., Giedzinski E., Kaplan M.I., Hartmann A., Morgan W.F. Genomic instability induced by high and low LET ionizing radiation. Adv. Space Res. 2000, 25:2107-2117.
57. Rajendran S., Harrison S.H., Thomas R.A., Tucker J.D. The role of mitochondria in the radiation-induced bystander effect in human lymphoblastoid cells. Radiat. Res. 2011, 175:159-171.
58. Kim G.J., Fiskum G.M., Morgan W.F. Radiation-induced genomic instability. Cancer Res. 2006, 66:10377-10383.
59. Fournier C., Winter M., Zahnreich S., Nasonova E., Melnikova L., Ritter S. Interrelation amongst differentiation, senescence and genetic instability in long-term cultures of fibroblasts exposed to different radiation qualities. Radiother. Oncol. 2007, 83:277-282.
60. Huang L., Kim P.M., Nickoloff J.A., Morgan W.F. Targeted and nontargeted effects of low-dose ionizing radiation on delayed genomic instability in human cells. Cancer Res. 2007, 67:1099-1104.
61. Wallace D.C. Mitochondrial DNA mutations in disease and aging. Environ. Mol. Mutagen. 2010, 51:440-450.
62. Rossignol R., Faustin B., Rocher C., Malgat M., Mazat J.P., Letellier T. Mitochondrial threshold effects. Biochem. J. 2003, 370:751-762.
63. Kowald A., Kirkwood T.B. Mitochondrial mutations, cellular instability and ageing: modelling the population dynamics of mitochondria. Mutat. Res. 1993, 295:93-103.