Effects of Local Heart Irradiation in a Glutathione S-Transferase Alpha 4-Null Mouse Model

Radiation Research

Volumn 183, Issue 6, 2015, Pages 610-619

  Boerma, Marjan ^a   Singh, Preeti ^b   Sridharan, Vijayalakshmi ^a   Tripathi, Preeti ^a   Sharma, Sunil ^c   Singh, Sharda P ^b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b Department of Pharmacology and Toxicology ^*  (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE FERREDOXIN OXIDOREDUCTASE; CASPASE 3; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE TRANSFERASE A1; GLUTATHIONE TRANSFERASE A2; GLUTATHIONE TRANSFERASE A3; GLUTATHIONE TRANSFERASE ALPHA; GLUTATHIONE TRANSFERASE ALPHA 4; GLUTATHIONE TRANSFERASE M1; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; PEROXIREDOXIN 6; PHOSPHOLIPID HYDROPEROXIDE GLUTATHIONE PEROXIDASE; PROTEIN BCL 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); THIOREDOXIN REDUCTASE 1; TRANSCRIPTION FACTOR NRF2; TROPONIN I; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; GLUTATHIONE TRANSFERASE; GSTA4-4 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTERIAL WALL THICKNESS; ARTICLE; CAPILLARY DENSITY; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; GAMMA RADIATION; GENE EXPRESSION; GENE TARGETING; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MITOCHONDRION; HEART OUTPUT; HEART STROKE VOLUME; IMMUNOHISTOCHEMISTRY; IONIZING RADIATION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY; UPREGULATION; X RAY; ANIMAL; ANIMAL EMBRYO; BLOOD; CYTOLOGY; DEFICIENCY; FIBROBLAST; GENE DELETION; GENETICS; HEART; METABOLISM; MITOCHONDRION; PHYSIOLOGY; RADIATION RESPONSE;

MUS;

ANIMALS; CELL SURVIVAL; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE DELETION; GLUTATHIONE TRANSFERASE; HEART; MALE; MICE; MITOCHONDRIA; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; OXYGEN; TROPONIN I;

EID: 84931299376     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13979.1     Document Type: Article

References (43)

1. Hiratsuka A, Tobita K, Saito H, Sakamoto Y, Nakano H, Ogura K, et al. (S)-preferential detoxification of 4-hydroxy-2(E)-nonenal enantiomers by hepatic glutathione S-transferase isoforms in guinea-pigs and rats. Biochem J 2001; 355:237-44.
2. Engle MR, Singh SP, Czernik PJ, Gaddy D, Montague DC, Ceci JD, et al. Physiological role of mGSTA4-4, a glutathione S-transferase metabolizing 4-hydroxynonenal: generation and analysis of mGsta4 null mouse. Toxicol Appl Pharmacol 2004; 194:296-308.
3. Singh SP, Niemczyk M, Saini D, Sadovov V, Zimniak L, Zimniak P. Disruption of the mGsta4 gene increases life span of C57BL mice. J Gerontol A Biol Sci Med Sci 2010; 65:14-23.
4. Singh SP, Niemczyk M, Saini D, Awasthi YC, Zimniak L, Zimniak P. Role of the electrophilic lipid peroxidation product 4-hydroxynonenal in the development and maintenance of obesity in mice. Biochemistry 2008; 47:3900-11.
5. Chen ZH, Saito Y, Yoshida Y, Sekine A, Noguchi N, Niki E. 4-Hydroxynonenal induces adaptive response and enhances PC12 cell tolerance primarily through induction of thioredoxin reductase 1 via activation of Nrf2. J Biol Chem 2005; 280:41921-7.
6. Sykiotis GP, Bohmann D. Stress-activated cap'n'collar transcription factors in aging and human disease. Sci Signal 2010; 3:re3.
7. Benes H, Vuong MK, Boerma M, McElhanon KE, Siegel ER, Singh SP. Protection from oxidative and electrophilic stress in the Gsta4-null mouse heart. Cardiovasc Toxicol 2013; 13:347-56.
8. Kaspar JW, Niture SK, Jaiswal AK. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009; 47:1304-9.
9. Takeda K, Komuro Y, Hayakawa T, Oguchi H, Ishida Y, Murakami S, et al. Mitochondrial phosphoglycerate mutase 5 uses alternate catalytic activity as a protein serine/threonine phosphatase to activate ASK1. Proc Natl Acad Sci U S A 2009; 106:12301-5.
10. Lo SC, Hannink M. PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp Cell Res 2008; 314:1789-803.
11. Lee MS, Finch W, Mahmud E. Cardiovascular complications of radiotherapy. Am J Cardiol 2013; 112:1688-96.
12. Sharma S, Moros EG, Boerma M, Sridharan V, Han EY, Clarkson R, et al. A novel technique for image-guided local heart irradiation in the rat. Technol Cancer Res Treat 2014; 13:593-603.
13. Kuznetsov AV, Schneeberger S, Seiler R, Brandacher G, Mark W, Steurer W, et al. Mitochondrial defects and heterogeneous cytochrome c release after cardiac cold ischemia and reperfusion. Am J Physiol Heart Circ Physiol 2004; 286:H1633-41.
14. Hughey CC, Hittel DS, Johnsen VL, Shearer J. Respirometric oxidative phosphorylation assessment in saponin-permeabilized cardiac fibers. J Vis Exp 2011; 48:1-7.
15. McElhanon KE, Bose C, Sharma R, Wu L, Awasthi YC, Singh SP. Null mouse embryonic fibroblasts exhibit enhanced sensitivity to oxidants: role of 4-hydroxynonenal in oxidant toxicity. Open J Apoptosis 2013; 2.
16. Franken NA, Rodermond HM, Stap J, Haveman J, van BC. Clonogenic assay of cells in vitro. Nat Protoc 2006; 1:2315-9.
17. Seemann I, Gabriels K, Visser NL, Hoving S, te Poele JA, Pol JF, et al. Irradiation induced modest changes in murine cardiac function despite progressive structural damage to the myocardium and microvasculature. Radiother Oncol 2012; 103:143-50.
18. Sridharan V, Aykin-Burns N, Tripathi P, Krager KJ, Sharma SK, Moros EG, et al. Radiation-induced alterations in mitochondria of the rat heart. Radiat Res 2014; 181:324-34.
19. Boerma M, Wang J, Wondergem J, Joseph J, Qiu X, Kennedy RH, et al. Influence of mast cells on structural and functional manifestations of radiation-induced heart disease. Cancer Res 2005; 65:3100-7.
20. Estensen RD. What is the role of myocardial mast cells? Hum Pathol 1985; 16:536-8.
21. Sperr WR, Bankl HC, Mundigler G, Klappacher G, Grossschmidt K, Agis H, et al. The human cardiac mast cell: localization, isolation, phenotype, and functional characterization. Blood 1994; 84:3876-84.
22. Boerma M, Zurcher C, Esveldt I, Schutte-Bart CI, Wondergem J. Histopathology of ventricles, coronary arteries and mast cell accumulation in transverse and longitudinal sections of the rat heart after irradiation. Oncol Rep 2004; 12:213-9.
23. Barjaktarovic Z, Schmaltz D, Shyla A, Azimzadeh O, Schulz S, Haagen J, et al. Radiation-induced signaling results in mitochondrial impairment in mouse heart at 4 weeks after exposure to x-rays. PLoS One 2011; 6:e27811.
24. Barjaktarovic Z, Shyla A, Azimzadeh O, Schulz S, Haagen J, Dorr W, et al. Ionising radiation induces persistent alterations in the cardiac mitochondrial function of C57BL/6 mice 40 weeks after local heart exposure. Radiother Oncol 2013; 106:404-10.
25. Franken NA, Hollaar L, Bosker FJ, Van Ravels FJ, van der Laarse A, Wondergem J. Effects of in vivo heart irradiation on myocardial energy metabolism in rats. Radiat Res 1993; 134:79-85.
26. Ludtmann MH, Angelova PR, Zhang Y, Abramov AY, Dinkova-Kostova AT. Nrf2 affects the efficiency of mitochondrial fatty acid oxidation. Biochem J 2014; 457:415-24.
27. Holmstrom KM, Baird L, Zhang Y, Hargreaves I, Chalasani A, Land JM, et al. Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol Open 2013; 2:761-70.
28. Raza H, Robin MA, Fang JK, Avadhani NG. Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem J 2002; 366:45-55.
29. Robin MA, Prabu SK, Raza H, Anandatheerthavarada HK, Avadhani NG. Phosphorylation enhances mitochondrial targeting of GSTA4-4 through increased affinity for binding to cytoplasmic Hsp70. J Biol Chem 2003; 278:18960-70.
30. Salata C, Ferreira-Machado SC, de Andrade CB, Mencalha AL, Mandarim-De-Lacerda CA, de Almeida CE. Apoptosis induction of cardiomyocytes and subsequent fibrosis after irradiation and neoadjuvant chemotherapy. Int J Radiat Biol 2014; 90:284-90.
31. Dogan I, Sezen O, Sonmez B, Zengin AY, Yenilmez E, Yulug E, et al. Myocardial perfusion alterations observed months after radiotherapy are related to the cellular damage. Nuklearmedizin 2010; 49:209-15.
32. Niture SK, Jaiswal AK. Nrf2 protein up-regulates antiapoptotic protein Bcl-2 and prevents cellular apoptosis. J Biol Chem 2012; 287:9873-86.
33. Zhang Y, Sano M, Shinmura K, Tamaki K, Katsumata Y, Matsuhashi T, et al. 4-hydroxy-2-nonenal protects against cardiac ischemia-reperfusion injury via the Nrf2-dependent pathway. J Mol Cell Cardiol 2010; 49:576-86.
34. Anuranjani, Bala M. Concerted action of Nrf2-ARE pathway, MRN complex, HMGB1 and inflammatory cytokines - Implication in modification of radiation damage. Redox Biol 2014; 2:832-46.
35. Mathew ST, Bergstrom P, Hammarsten O. Repeated Nrf2 stimulation using sulforaphane protects fibroblasts from ionizing radiation. Toxicol Appl Pharmacol 2014; 276:188-94.
36. Kim JH, Thimmulappa RK, Kumar V, Cui W, Kumar S, Kombairaju P, et al. NRF2-mediated Notch pathway activation enhances hematopoietic reconstitution following myelosuppressive radiation. J Clin Invest 2014; 124:730-41.
37. Kim SB, Pandita RK, Eskiocak U, Ly P, Kaisani A, Kumar R, et al. Targeting of Nrf2 induces DNA damage signaling and protects colonic epithelial cells from ionizing radiation. Proc Natl Acad Sci U S A 2012; 109:E2949-55.
38. Kato K, Takahashi K, Monzen S, Yamamoto H, Maruyama A, Itoh K, et al. Relationship between radiosensitivity and Nrf2 target gene expression in human hematopoietic stem cells. Radiat Res 2010; 174:177-84.
39. Chute JP. NRF2 mitigates radiation-induced hematopoietic death. J Clin Invest 2014; 124:960-1.
40. Mathew B, Jacobson JR, Siegler JH, Moitra J, Blasco M, Xie L, et al. Role of migratory inhibition factor in age-related susceptibility to radiation lung injury via NF-E2-related factor-2 and antioxidant regulation. Am J Respir Cell Mol Biol 2013; 49:269-78.
41. McDonald JT, Kim K, Norris AJ, Vlashi E, Phillips TM, Lagadec C, et al. Ionizing radiation activates the Nrf2 antioxidant response. Cancer Res 2010; 70:8886-95.
42. Travis EL, Rachakonda G, Zhou X, Korhonen K, Sekhar KR, Biswas S, et al. NRF2 deficiency reduces life span of mice administered thoracic irradiation. Free Radic Biol Med 2011; 51:1175-83.
43. Rana T, Schultz MA, Freeman ML, Biswas S. Loss of Nrf2 accelerates ionizing radiation-induced bone loss by upregulating RANKL. Free Radic Biol Med 2012; 53:2298-307.