Radiation-induced signaling results in mitochondrial impairment in mouse heart at 4 weeks after exposure to X-rays

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Barjaktarovic, Zarko ^a   Schmaltz, Dominik ^a   Shyla, Alena ^a   Azimzadeh, Omid ^a   Schulz, Sabine ^a   Haagen, Julia ^b   Dörr, Wolfgang ^b   Sarioglu, Hakan ^a   Schäfer, Alexander ^a   Atkinson, Michael J ^a,c   Zischka, Hans ^a   Tapio, Soile ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL PROTEIN; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE E1ALPHA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; CYTOCHROME C1; REACTIVE NITROGEN SPECIES;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ELECTROSPRAY MASS SPECTROMETRY; HEART MITOCHONDRION; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; METABOLISM; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEOMICS; PYRUVATE METABOLISM; RADIATION DOSE; RADIATION EXPOSURE; RADIATION INJURY; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; X RAY; ANIMAL; BIOLOGY; C57BL MOUSE; DRUG EFFECT; HEART MUSCLE; IMMUNOBLOTTING; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; RADIATION RESPONSE; REPRODUCIBILITY; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; ULTRASTRUCTURE;

ANIMALS; COMPUTATIONAL BIOLOGY; CYTOCHROMES C1; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; IMMUNOBLOTTING; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MYOCARDIUM; OXIDATION-REDUCTION; PHOSPHORYLATION; PROTEOMICS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; SUCCINIC ACID; X-RAYS;

EID: 82955241393     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027811     Document Type: Article

References (86)

1. Demirci S, Nam J, Hubbs JL, Nguyen T, Marks LB, (2009) Radiation-induced cardiac toxicity after therapy for breast cancer: interaction between treatment era and follow-up duration. Int J Radiat Oncol Biol Phys 73: 980-987.
2. Darby S, Hill D, Auvinen A, Barros-Dios JM, Baysson H, et al. (2005) Radon in homes and risk of lung cancer: collaborative analysis of individual data from 13 European case-control studies. Bmj 330: 223.
3. Darby S, McGale P, Peto R, Granath F, Hall P, et al. (2003) Mortality from cardiovascular disease more than 10 years after radiotherapy for breast cancer: nationwide cohort study of 90 000 Swedish women. Bmj 326: 256-257.
4. Clarke M, Collins R, Darby S, Davies C, Elphinstone P, et al. (2005) Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet 366: 2087-2106.
5. Swerdlow AJ, Higgins CD, Smith P, Cunningham D, Hancock BW, et al. (2007) Myocardial infarction mortality risk after treatment for Hodgkin disease: a collaborative British cohort study. J Natl Cancer Inst 99: 206-214.
6. Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, et al. (2010) Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol 28: 1308-1315.
7. Hauptmann M, Mohan AK, Doody MM, Linet MS, Mabuchi K, (2003) Mortality from diseases of the circulatory system in radiologic technologists in the United States. Am J Epidemiol 157: 239-248.
8. Howe GR, Zablotska LB, Fix JJ, Egel J, Buchanan J, (2004) Analysis of the mortality experience amongst U.S. nuclear power industry workers after chronic low-dose exposure to ionizing radiation. Radiat Res 162: 517-526.
9. Ivanov VK, (2007) Late cancer and noncancer risks among Chernobyl emergency workers of Russia. Health Phys 93: 470-479.
10. McGeoghegan D, Binks K, Gillies M, Jones S, Whaley S, (2008) The non-cancer mortality experience of male workers at British Nuclear Fuels plc, 1946-2005. Int J Epidemiol 37: 506-518.
11. Muirhead CR, O'Hagan JA, Haylock RG, Phillipson MA, Willcock T, et al. (2009) Mortality and cancer incidence following occupational radiation exposure: third analysis of the National Registry for Radiation Workers. Br J Cancer 100: 206-212.
12. Azizova TV, Muirhead CR, Druzhinina MB, Grigoryeva ES, Vlasenko EV, et al. (2010) Cardiovascular diseases in the cohort of workers first employed at Mayak PA in 1948-1958. Radiat Res 174.
13. Carr ZA, Land CE, Kleinerman RA, Weinstock RW, Stovall M, et al. (2005) Coronary heart disease after radiotherapy for peptic ulcer disease. Int J Radiat Oncol Biol Phys 61: 842-850.
14. Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, et al. (2010) Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950-2003. Bmj 340: b5349.
15. Preston DL, Shimizu Y, Pierce DA, Suyama A, Mabuchi K, (2003) Studies of mortality of atomic bomb survivors. Report 13: Solid cancer and noncancer disease mortality: 1950-1997. Radiat Res 160: 381-407.
16. Kreuzer M, Grosche B, Schnelzer M, Tschense A, Dufey F, et al. (2010) Radon and risk of death from cancer and cardiovascular diseases in the German uranium miners cohort study: follow-up 1946-2003. Radiat Environ Biophys 49: 177-185.
17. Kreuzer M, Kreisheimer M, Kandel M, Schnelzer M, Tschense A, et al. (2006) Mortality from cardiovascular diseases in the German uranium miners cohort study, 1946-1998. Radiat Environ Biophys 45: 159-166.
18. Darby SC, Doll R, Gill SK, Smith PG, (1987) Long term mortality after a single treatment course with X-rays in patients treated for ankylosing spondylitis. Br J Cancer 55: 179-190.
19. Davis FG, Boice JD Jr, Hrubec Z, Monson RR, (1989) Cancer mortality in a radiation-exposed cohort of Massachusetts tuberculosis patients. Cancer Res 49: 6130-6136.
20. Richardson DB, Wing S, (1999) Radiation and mortality of workers at Oak Ridge National Laboratory: positive associations for doses received at older ages. Environ Health Perspect 107: 649-656.
21. Talbott EO, Youk AO, McHugh-Pemu KP, Zborowski JV, (2003) Long-term follow-up of the residents of the Three Mile Island accident area: 1979-1998. Environ Health Perspect 111: 341-348.
22. Little MP, Tawn EJ, Tzoulaki I, Wakeford R, Hildebrandt G, et al. (2010) Review and meta-analysis of epidemiological associations between low/moderate doses of ionizing radiation and circulatory disease risks, and their possible mechanisms. Radiat Environ Biophys 49: 139-153.
23. Spitz DR, Azzam EI, Li JJ, Gius D, (2004) Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev 23: 311-322.
24. Takano H, Zou Y, Hasegawa H, Akazawa H, Nagai T, et al. (2003) Oxidative stress-induced signal transduction pathways in cardiac myocytes: involvement of ROS in heart diseases. Antioxid Redox Signal 5: 789-794.
25. Hayashi T, Morishita Y, Kubo Y, Kusunoki Y, Hayashi I, et al. (2005) Long-term effects of radiation dose on inflammatory markers in atomic bomb survivors. Am J Med 118: 83-86.
26. Nakachi K, Hayashi T, Hamatani K, Eguchi H, Kusunoki Y, (2008) Sixty years of follow-up of Hiroshima and Nagasaki survivors: current progress in molecular epidemiology studies. Mutat Res 659: 109-117.
27. Goh K, Sumner H, (1968) Breaks in normal human chromosomes: are they induced by a transferable substance in the plasma of persons exposed to total-body irradiation? Radiat Res 35: 171-181.
28. Hollowell JG Jr, Littlefield LG, (1968) Chromosome damage induced by plasma of x-rayed patients: an indirect effect of x-ray. Proc Soc Exp Biol Med 129: 240-244.
29. Emerit I, Levy A, Cernjavski L, Arutyunyan R, Oganesyan N, et al. (1994) Transferable clastogenic activity in plasma from persons exposed as salvage personnel of the Chernobyl reactor. J Cancer Res Clin Oncol 120: 558-561.
30. White MY, Edwards AV, Cordwell SJ, Van Eyk JE, (2008) Mitochondria: A mirror into cellular dysfunction in heart disease. Proteomics Clin Appl 2: 845-861.
31. Schlattner U, Tokarska-Schlattner M, Wallimann T, (2006) Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 1762: 164-180.
32. Dhalla NS, Temsah RM, Netticadan T, (2000) Role of oxidative stress in cardiovascular diseases. J Hypertens 18: 655-673.
33. Ballinger SW, (2005) Mitochondrial dysfunction in cardiovascular disease. Free Radic Biol Med 38: 1278-1295.
34. Misra MK, Sarwat M, Bhakuni P, Tuteja R, Tuteja N, (2009) Oxidative stress and ischemic myocardial syndromes. Med Sci Monit 15: RA209-219.
35. Allan IM, Vaughan AT, Milner AE, Lunec J, Bacon PA, (1988) Structural damage to lymphocyte nuclei by H2O2 or gamma irradiation is dependent on the mechanism of OH. radical production. Br J Cancer 58: 34-37.
36. Eny KM, El-Sohemy A, Cornelis MC, Sung YK, Bae SC, (2005) Catalase and PPARgamma2 genotype and risk of systemic lupus erythematosus in Koreans. Lupus 14: 351-355.
37. Coyle CH, Kader KN, (2007) Mechanisms of H2O2-induced oxidative stress in endothelial cells exposed to physiologic shear stress. Asaio J 53: 17-22.
38. Wolf G, (2000) Free radical production and angiotensin. Curr Hypertens Rep 2: 167-173.
39. Garlid KD, Costa AD, Quinlan CL, Pierre SV, Dos Santos P, (2009) Cardioprotective signaling to mitochondria. J Mol Cell Cardiol 46: 858-866.
40. Hausenloy DJ, Yellon DM, (2008) Preconditioning and postconditioning: new strategies for cardioprotection. Diabetes Obes Metab 10: 451-459.
41. 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.
42. Azimzadeh O, Scherthan H, Sarioglu H, Barjaktarovic Z, Conrad M, et al. (2011) Rapid proteomic remodeling of cardiac tissue caused by total body ionizing radiation. Proteomics 11: 3299-3311.
43. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, et al. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031.
44. Susin SA, Larochette N, Geuskens M, Kroemer G, (2000) Purification of mitochondria for apoptosis assays. Methods Enzymol 322: 205-208.
45. Schmidt A, Bisle B, Kislinger T, (2009) Quantitative peptide and protein profiling by mass spectrometry. Methods Mol Biol 492: 21-38.
46. Sarioglu H, Brandner S, Jacobsen C, Meindl T, Schmidt A, et al. (2006) Quantitative analysis of 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced proteome alterations in 5 L rat hepatoma cells using isotope-coded protein labels. Proteomics 6: 2407-2421.
47. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
48. Heukeshoven J, Dernick R, (1985) Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis 6: 103-112.
49. Chevallet M, Luche S, Rabilloud T, (2006) Silver staining of proteins in polyacrylamide gels. Nat Protoc 1: 1852-1858.
50. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
51. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.
52. Geiger T, Cox J, Mann M, (2010) Proteomic changes resulting from gene copy number variations in cancer cells. PLoS Genet 6.
53. Mayburd AL, Martlinez A, Sackett D, Liu H, Shih J, et al. (2006) Ingenuity network-assisted transcription profiling: Identification of a new pharmacologic mechanism for MK886. Clin Cancer Res 12: 1820-1827.
54. Wu J, Liu W, Bemis A, Wang E, Qiu Y, et al. (2007) Comparative proteomic characterization of articular cartilage tissue from normal donors and patients with osteoarthritis. Arthritis Rheum 56: 3675-3684.
55. Burnette WN, (1981) "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112: 195-203.
56. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
57. Kiebish MA, Han X, Cheng H, Lunceford A, Clarke CF, et al. (2008) Lipidomic analysis and electron transport chain activities in C57BL/6J mouse brain mitochondria. J Neurochem 106: 299-312.
58. Birch-Machin MA, Turnbull DM, (2001) Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol 65: 97-117.
59. Fu C, Hu J, Liu T, Ago T, Sadoshima J, et al. (2008) Quantitative analysis of redox-sensitive proteome with DIGE and ICAT. J Proteome Res 7: 3789-3802.
60. Murray AJ, Cole MA, Lygate CA, Carr CA, Stuckey DJ, et al. (2008) Increased mitochondrial uncoupling proteins, respiratory uncoupling and decreased efficiency in the chronically infarcted rat heart. J Mol Cell Cardiol 44: 694-700.
61. Heather LC, Carr CA, Stuckey DJ, Pope S, Morten KJ, et al. (2010) Critical role of complex III in the early metabolic changes following myocardial infarction. Cardiovasc Res 85: 127-136.
62. Tahara EB, Navarete FD, Kowaltowski AJ, (2009) Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med 46: 1283-1297.
63. Kennedy CH, Church DF, Winston GW, Pryor WA, (1992) tert-Butyl hydroperoxide-induced radical production in rat liver mitochondria. Free Radic Biol Med 12: 381-387.
64. Shenker BJ, Guo TL, Shapiro IM, (2000) Mercury-induced apoptosis in human lymphoid cells: evidence that the apoptotic pathway is mercurial species dependent. Environ Res 84: 89-99.
65. Bindoff L, (2003) Mitochondria and the heart. Eur Heart J 24: 221-224.
66. Davidson SM, (2010) Endothelial mitochondria and heart disease. Cardiovasc Res 88: 58-66.
67. Korotchkina LG, Patel MS, (2001) Probing the mechanism of inactivation of human pyruvate dehydrogenase by phosphorylation of three sites. J Biol Chem 276: 5731-5738.
68. Boja ES, Phillips D, French SA, Harris RA, Balaban RS, (2009) Quantitative mitochondrial phosphoproteomics using iTRAQ on an LTQ-Orbitrap with high energy collision dissociation. J Proteome Res 8: 4665-4675.
69. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ, (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278: 36027-36031.
70. Drose S, Brandt U, (2008) The mechanism of mitochondrial superoxide production by the cytochrome bc1 complex. J Biol Chem 283: 21649-21654.
71. Orrenius S, (2007) Reactive oxygen species in mitochondria-mediated cell death. Drug Metab Rev 39: 443-455.
72. Ott M, Gogvadze V, Orrenius S, Zhivotovsky B, (2007) Mitochondria, oxidative stress and cell death. Apoptosis 12: 913-922.
73. Eriksson P, Fischer C, Stenerlow B, Fredriksson A, Sundell-Bergman S, (2010) Interaction of gamma-radiation and methyl mercury during a critical phase of neonatal brain development in mice exacerbates developmental neurobehavioural effects. Neurotoxicology 31: 223-229.
74. Forner F, Foster LJ, Campanaro S, Valle G, Mann M, (2006) Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver. Mol Cell Proteomics 5: 608-619.
75. Boldogh IR, Pon LA, (2006) Interactions of mitochondria with the actin cytoskeleton. Biochim Biophys Acta 1763: 450-462.
76. Boldogh IR, Pon LA, (2007) Mitochondria on the move. Trends Cell Biol 17: 502-510.
77. Tang HL, Lung HL, Wu KC, Le AH, Tang HM, et al. (2008) Vimentin supports mitochondrial morphology and organization. Biochem J 410: 141-146.
78. Rappaport L, Oliviero P, Samuel JL, (1998) Cytoskeleton and mitochondrial morphology and function. Mol Cell Biochem 184: 101-105.
79. Capetanaki Y, (2002) Desmin cytoskeleton: a potential regulator of muscle mitochondrial behavior and function. Trends Cardiovasc Med 12: 339-348.
80. Linden M, Li Z, Paulin D, Gotow T, Leterrier JF, (2001) Effects of desmin gene knockout on mice heart mitochondria. J Bioenerg Biomembr 33: 333-341.
81. Milner DJ, Mavroidis M, Weisleder N, Capetanaki Y, (2000) Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 150: 1283-1298.
82. Tolstonog GV, Shoeman RL, Traub U, Traub P, (2001) Role of the intermediate filament protein vimentin in delaying senescence and in the spontaneous immortalization of mouse embryo fibroblasts. DNA Cell Biol 20: 509-529.
83. Hu Q, Suzuki G, Young RF, Page BJ, Fallavollita JA, et al. (2009) Reductions in mitochondrial O(2) consumption and preservation of high-energy phosphate levels after simulated ischemia in chronic hibernating myocardium. Am J Physiol Heart Circ Physiol 297: H223-232.
84. Page B, Young R, Iyer V, Suzuki G, Lis M, et al. (2008) Persistent regional downregulation in mitochondrial enzymes and upregulation of stress proteins in swine with chronic hibernating myocardium. Circ Res 102: 103-112.
85. Fedorova M, Kuleva N, Hoffmann R, (2009) Reversible and irreversible modifications of skeletal muscle proteins in a rat model of acute oxidative stress. Biochim Biophys Acta 1792: 1185-1193.
86. Bayeva M, Ardehali H, (2010) Mitochondrial dysfunction and oxidative damage to sarcomeric proteins. Curr Hypertens Rep 12: 426-432.