Protection from oxidative and electrophilic stress in the gsta4-null mouse heart

Cardiovascular Toxicology

Volumn 13, Issue 4, 2013, Pages 347-356

  Beneš, Helen ^a   Vuong, Mai K ^a   Boerma, Marjan ^b   McElhanon, Kevin E ^a   Siegel, Eric R ^a   Singh, Sharda P ^a,c  

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

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

^c CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

Author keywords

4 Hydroxynonenal; Cardiac function; Doxorubicin; Electrophilic stress; Glutathione transferase; Nrf2; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; AKR1B7 PROTEIN; CATALASE; CELL PROTEIN; GLUTATHIONE TRANSFERASE A4; MESSENGER RNA; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ELECTROPHILIC STRESS; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GLUTATHIONE TRANSFERASE ALPHA 4 GENE; IN VIVO STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STEADY STATE; WILD TYPE;

ALDEHYDES; ANIMALS; DOXORUBICIN; GLUTATHIONE TRANSFERASE; HEART; MALE; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MYOCARDIUM; NF-E2 TRANSCRIPTION FACTOR, P45 SUBUNIT; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN BINDING;

EID: 84890496509     PISSN: 15307905     EISSN: 15590259     Source Type: Journal    
DOI: 10.1007/s12012-013-9215-1     Document Type: Article

References (69)

1. Heistad, D. D.; Wakisaka, Y.; Miller, J.; Chu, Y.; & Pena-Silva, R. (2009). Novel aspects of oxidative stress in cardiovascular diseases. Circulation Journal: Official Journal of the Japanese Circulation Society, 73, 201-207.
2. Ari, E.; Kaya, Y.; Demir, H.; Cebi, A.; Alp, H. H.; Bakan, E.; et al. (2011). Oxidative DNA damage correlates with carotid artery atherosclerosis in hemodialysis patients. Hemodialysis International, 15, 453-459.
3. Fadel, P. J.; Farias Iii, M.; Gallagher, K. M.; Wang, Z.; & Thomas, G. D. (2012). Oxidative stress and enhanced sympathetic vasoconstriction in contracting muscles of nitrate-tolerant rats and humans. Journal of Physiology (Lond), 590, 395-407.
4. Hollander, J. M.; Baseler, W. A.; & Dabkowski, E. R. (2011). Proteomic remodeling of mitochondria in heart failure. Congestive Heart Failure, 17, 262-268.
5. Schlage, W. K.; Westra, J. W.; Gebel, S.; Catlett, N. L.; Mathis, C.; Frushour, B. P.; et al. (2011). A computable cellular stress network model for non-diseased pulmonary and cardiovascular tissue. BMC Systems Biology, 5, 168.
6. Lee, S.; Park, Y.; Zuidema, M. Y.; Hannink, M.; & Zhang, C. (2011). Effects of interventions on oxidative stress and inflammation of cardiovascular diseases. World Journal of Cardiology, 3, 18-24.
7. Chen, Le, & Knowlton, A. A. (2011). Mitochondrial dynamics in heart failure. Congestive Heart Failure, 17, 257-261.
8. Dai, D. F.; Rabinovitch, P. S.; & Ungvari, Z. (2012). Mitochondria and cardiovascular aging. Circulation Research, 110, 1109-1124.
9. Zimniak, P. (2011). Relationship of electrophilic stress to aging. Free Radical Biology and Medicine, 51, 1087-1105.
10. Churchill, E. N.; Disatnik, M. H.; & Mochly-Rosen, D. (2009). Time-dependent and ethanol-induced cardiac protection from ischemia mediated by mitochondrial translocation of varepsilonPKC and activation of aldehyde dehydrogenase 2. Journal of Molecular and Cellular Cardiology, 46, 278-284.
11. Dhiman, M.; Zago, M. P.; Nunez, S.; Amoroso, A.; Rementeria, H.; Dousset, P.; et al. (2012). Cardiac-oxidized antigens are targets of immune recognition by antibodies and potential molecular determinants in chagas disease pathogenesis. PLoS ONE, 7, e28449.
12. Hayashida, K.; Sano, M.; Kamimura, N.; Yokota, T.; Suzuki, M.; Maekawa, Y.; et al. (2012). H(2) gas improves functional outcome after cardiac arrest to an extent comparable to therapeutic hypothermia in a rat model. Journal of the American Heart Association, 1, e003459.
13. Awasthi, Y. C.; Sharma, R.; Sharma, A.; Yadav, S.; Singhal, S. S.; Chaudhary, P.; et al. (2008). Self-regulatory role of 4-hydroxynonenal in signaling for stress-induced programmed cell death. Free Radical Biology and Medicine, 45, 111-118.
14. Uchida, K.; Shiraishi, M.; Naito, Y.; Torii, Y.; Nakamura, Y.; & Osawa, T. (1999). Activation of stress signaling pathways by the end product of lipid peroxidation - 4-hydroxy-2-nonenal is a potential inducer of intracellular peroxide production. Journal of Biological Chemistry, 274, 2234-2242.
15. Ma, H.; Guo, R.; Yu, L.; Zhang, Y.; & Ren, J. (2011). Aldehyde dehydrogenase 2 (ALDH2) rescues myocardial ischaemia/reperfusion injury: Role of autophagy paradox and toxic aldehyde. European Heart Journal, 32, 1025-1038.
16. Pajaud, J.; Kumar, S.; Rauch, C.; Morel, F.; & Aninat, C. (2012). Regulation of signal transduction by glutathione transferases. International Journal of Hepatology, 2012, 137676.
17. Kansanen, E.; Jyrkkanen, H. K.; & Levonen, A. L. (2012). Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids. Free Radical Biology and Medicine, 52, 973-982.
18. Zhang, D. D.; Lo, S. C.; Cross, J. V.; Templeton, D. J.; & Hannink, M. (2004). Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Molecular and Cellular Biology, 24, 10941-10953.
19. Taylor, R. C.; Acquaah-Mensah, G.; Singhal, M.; Malhotra, D.; & Biswal, S. (2008). Network inference algorithms elucidate Nrf2 regulation of mouse lung oxidative stress. PLoS Computational Biology, 4, e1000166.
20. Zhu, H.; Jia, Z.; Misra, B. R.; Zhang, L.; Cao, Z.; Yamamoto, M.; et al. (2008). Nuclear factor E2-related factor 2-dependent myocardiac cytoprotection against oxidative and electrophilic stress. Cardiovascular Toxicology, 8, 71-85.
21. Aleksunes, L. M.; & Klaassen, C. D. (2012). Coordinated regulation of hepatic phase I and II drug-metabolizing genes and transporters using AhR-, CAR-, PXR-, PPARalpha-, and Nrf2-null mice. Drug Metabolism and Disposition: The Biological Fate of Chemicals, 40, 1366-1379.
22. Balogh, L. M.; & Atkins, W. M. (2011). Interactions of glutathione transferases with 4-hydroxynonenal. Drug Metabolism Reviews, 43, 165-178.
23. Engle, M. R.; Singh, S. P.; Czernik, P. J.; Gaddy, D.; Montague, D. C.; Ceci, J. D.; et al. (2004). Physiological role of mGSTA4-4, a glutathione S-transferase metabolizing 4-hydroxynonenal: Generation and analysis of mGsta4 null mouse. Toxicology and Applied Pharmacology, 194, 296-308.
24. Raza, H.; Robin, M. A.; Fang, J. K.; & Avadhani, N. G. (2002). Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochemical Journal, 366, 45-55.
25. Desmots, F.; Rissel, M.; Loyer, P.; Turlin, B.; & Guillouzo, A. (2001). Immunohistological analysis of glutathione transferase A4 distribution in several human tissues using a specific polyclonal antibody. Journal of Histochemistry and Cytochemistry, 49, 1573-1580.
26. Chaiswing, L.; Cole, M. P.; St Clair, D. K.; Ittarat, W.; Szweda, L. I.; & Oberley, T. D. (2004). Oxidative damage precedes nitrative damage in adriamycin-induced cardiac mitochondrial injury. Toxicologic Pathology, 32, 536-547.
27. Menna, P.; Salvatorelli, E.; & Minotti, G. (2007). Doxorubicin degradation in cardiomyocytes. Journal of Pharmacology and Experimental Therapeutics, 322, 408-419.
28. Jungsuwadee, P.; Nithipongvanitch, R.; Chen, Y.; Oberley, T. D.; Butterfield, D. A.; St Clair, D. K.; et al. (2009). Mrp1 localization and function in cardiac mitochondria after doxorubicin. Molecular Pharmacology, 75, 1117-1126.
29. Zhao, Y.; McLaughlin, D.; Robinson, E.; Harvey, A. P.; Hookham, M. B.; Shah, A. M.; et al. (2010). Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with Doxorubicin chemotherapy. Cancer Research, 70, 9287-9297.
30. Richard, C.; Ghibu, S.; Delemasure-Chalumeau, S.; Guilland, J. C.; Des Rosiers, C.; Zeller, M.; et al. (2011). Oxidative stress and myocardial gene alterations associated with Doxorubicin-induced cardiotoxicity in rats persist for 2 months after treatment cessation. Journal of Pharmacology and Experimental Therapeutics, 339, 807-814.
31. Xi, L.; Zhu, S. G.; Das, A.; Chen, Q.; Durrant, D.; Hobbs, D. C.; et al. (2012). Dietary inorganic nitrate alleviates doxorubicin cardiotoxicity: Mechanisms and implications. Nitric Oxide, 26, 274-284.
32. Octavia, Y.; Tocchetti, C. G.; Gabrielson, K. L.; Janssens, S.; Crijns, H. J.; & Moens, A. L. (2012). Doxorubicin-induced cardiomyopathy: From molecular mechanisms to therapeutic strategies. Journal of Molecular and Cellular Cardiology, 52, 1213-1225.
33. Grée, R.; Tourbah, H.; & Carrié, R. (1986). Furaldehyde monodimethyl acetal: An easily accessible and versatile intermediate. Tetrahedron Letters, 27, 4983-4986.
34. Chandra, A.; & Srivastava, S. K. (1997). A synthesis of 4-hydroxy-2-trans-nonenal and 4-(3H) 4-hydroxy-2-trans-nonenal. Lipids, 32, 779-782.
35. Wollenberger, A.; Ristau, O.; & Schoffa, G. (1960). A simple technic for extremely rapid freezing of large pieces of tissue. Pflügers Archiv für die Gesamte Physiologie des Menschen und der Tiere, 270, 399-412.
36. Singh, S. P.; Niemczyk, M.; Saini, D.; Awasthi, Y. C.; Zimniak, L.; & Zimniak, P. (2008). Role of the electrophilic lipid peroxidation product 4-hydroxynonenal in the development and maintenance of obesity in mice. Biochemistry (Mosc), 47, 3900-3911.
37. Singh, S. P.; Niemczyk, M.; Saini, D.; Sadovov, V.; Zimniak, L.; & Zimniak, P. (2010). Disruption of the mGsta4 gene increases life span of C57BL mice. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 65, 14-23.
38. Chomczynski, P.; & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162, 156-159.
39. Mohanty, J. G.; Jaffe, J. S.; Schulman, E. S.; & Raible, D. G. (1997). A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. Journal of Immunological Methods, 202, 133-141.
40. Manthey, C. L.; & Sladek, N. E. (1988). Kinetic characterization of the catalysis of "activated" cyclophosphamide (4- hydroxycyclophosphamide/aldophosphamide) oxidation to carboxyphosphamide by mouse hepatic aldehyde dehydrogenases. Biochemical Pharmacology, 37, 2781-2790.
41. Bunting, K. D.; Lindahl, R.; & Townsend, A. J. (1994). Oxazaphosphorine-specific resistance in human MCF-7 breast carcinoma cell lines expressing transfected rat class 3 aldehyde dehydrogenase. Journal of Biological Chemistry, 269, 23197-23203.
42. Burczynski, M. E.; Sridhar, G. R.; Palackal, N. T.; & Penning, T. M. (2001). The reactive oxygen species-and Michael acceptor-inducible human aldo-keto reductase AKR1C1 reduces the alpha, beta-unsaturated aldehyde 4-hydroxy-2-nonenal to 1,4-dihydroxy-2-nonene. Journal of Biological Chemistry, 276, 2890-2897.
43. Zhang, Y.; Sano, M.; Shinmura, K.; Tamaki, K.; Katsumata, Y.; Matsuhashi, T.; et al. (2010). 4-Hydroxy-2-nonenal protects against cardiac ischemia-reperfusion injury via the Nrf2-dependent pathway. Journal of Molecular and Cellular Cardiology, 49, 576-586.
44. Srivastava, S.; Chandra, A.; Wang, L. F.; Seifert, W. E, Jr, DaGue, B. B.; Ansari, N. H.; et al. (1998). Metabolism of the lipid peroxidation product, 4-hydroxy-trans-2-nonenal, in isolated perfused rat heart. Journal of Biological Chemistry, 273, 10893-10900.
45. Sterba, M.; Popelova, O.; Vavrova, A.; Jirkovsky, E.; Kovarikova, P.; Gersl, V.; et al. (2013). Oxidative stress, redox signaling, and metal chelation in anthracycline cardiotoxicity and pharmacological cardioprotection. Antioxidants & Redox Signaling, 18, 899-929.
46. Luo, X.; Evrovsky, Y.; Cole, D.; Trines, J.; Benson, L. N.; & Lehotay, D. C. (1997). Doxorubicin-induced acute changes in cytotoxic aldehydes, antioxidant status and cardiac function in the rat. Biochimica et Biophysica Acta, 1360, 45-52.
47. Zimniak, P.; Singhal, S. S.; Srivastava, S. K.; Awasthi, S.; Sharma, R.; Hayden, J. B.; et al. (1994). Estimation of genomic complexity, heterologous expression, and enzymatic characterization of mouse glutathione S-transferase mGSTA4-4 (GST 5.7). Journal of Biological Chemistry, 269, 992-1000.
48. Knight, T. R.; Choudhuri, S.; & Klaassen, C. D. (2007). Constitutive mRNA expression of various glutathione S-transferase isoforms in different tissues of mice. Toxicological Sciences, 100, 513-524.
49. Prosser, B. L.; Ward, C. W.; & Lederer, W. J. (2011). X-ROS signaling: Rapid mechano-chemo transduction in heart. Science, 333, 1440-1445.
50. Thimmulappa, R. K.; Mai, K. H.; Srisuma, S.; Kensler, T. W.; Yamamoto, M.; & Biswal, S. (2002). Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Research, 62, 5196-5203.
51. Lou, H.; Du, S.; Ji, Q.; & Stolz, A. (2006). Induction of AKR1C2 by phase II inducers: Identification of a distal consensus antioxidant response element regulated by NRF2. Molecular Pharmacology, 69, 1662-1672.
52. Goldring, C. E.; Kitteringham, N. R.; Elsby, R.; Randle, L. E.; Clement, Y. N.; Williams, D. P.; et al. (2004). Activation of hepatic Nrf2 in vivo by acetaminophen in CD-1 mice. Hepatology, 39, 1267-1276.
53. Li, Y.; Paonessa, J. D.; & Zhang, Y. (2012). Mechanism of chemical activation of Nrf2. PLoS ONE, 7, e35122.
54. Doroshow, J. H.; Locker, G. Y.; Ifrim, I.; & Myers, C. E. (1981). Prevention of doxorubicin cardiac toxicity in the mouse by N-acetylcysteine. Journal of Clinical Investigation, 68, 1053-1064.
55. Lu, M.; Merali, S.; Gordon, R.; Jiang, J.; Li, Y.; Mandeli, J.; et al. (2011). Prevention of Doxorubicin cardiopathic changes by a benzyl styryl sulfone in mice. Genes Cancer, 2, 985-992.
56. Todorova, V. K.; Beggs, M. L.; Delongchamp, R. R.; Dhakal, I.; Makhoul, I.; Wei, J. Y.; et al. (2012). Transcriptome profiling of peripheral blood cells identifies potential biomarkers for Doxorubicin cardiotoxicity in a rat model. PLoS ONE, 7, e48398.
57. Yen, H. C.; Oberley, T. D.; Gairola, C. G.; Szweda, L. I.; & St Clair, D. K. (1999). Manganese superoxide dismutase protects mitochondrial complex I against adriamycin-induced cardiomyopathy in transgenic mice. Archives of Biochemistry and Biophysics, 362, 59-66.
58. Cole, M. P.; Chaiswing, L.; Oberley, T. D.; Edelmann, S. E.; Piascik, M. T.; Lin, S. M.; et al. (2006). The protective roles of nitric oxide and superoxide dismutase in adriamycin-induced cardiotoxicity. Cardiovascular Research, 69, 186-197.
59. Kang, Y. J.; Sun, X.; Chen, Y.; & Zhou, Z. (2002). Inhibition of doxorubicin chronic toxicity in catalase-overexpressing transgenic mouse hearts. Chemical Research in Toxicology, 15, 1-6.
60. Bell, R. M.; & Yellon, D. M. (2012). Conditioning the whole heart-not just the cardiomyocyte. Journal of Molecular and Cellular Cardiology, 53, 24-32.
61. Ito, H.; Shimojo, T.; Fujisaki, H.; Tamamori, M.; Ishiyama, S.; Adachi, S.; et al. (1999). Thermal preconditioning protects rat cardiac muscle cells from doxorubicin-induced apoptosis. Life Sciences, 64, 755-761.
62. Liu, X.; Chen, Z.; Chua, C. C.; Ma, Y. S.; Youngberg, G. A.; Hamdy, R.; et al. (2002). Melatonin as an effective protector against doxorubicin-induced cardiotoxicity. American Journal of Physiology: Heart and Circulatory Physiology, 283, H254-H263.
63. Hofmann, P. A.; Israel, M.; Koseki, Y.; Laskin, J.; Gray, J.; Janik, A.; et al. (2007). N-Benzyladriamycin-14-valerate (AD 198): A non-cardiotoxic anthracycline that is cardioprotective through PKC-epsilon activation. Journal of Pharmacology and Experimental Therapeutics, 323, 658-664.
64. Kim, K. H.; Oudit, G. Y.; & Backx, P. H. (2008). Erythropoietin protects against doxorubicin-induced cardiomyopathy via a phosphatidylinositol 3-kinase-dependent pathway. Journal of Pharmacology and Experimental Therapeutics, 324, 160-169.
65. Calvert, J. W.; Coetzee, W. A.; & Lefer, D. J. (2010). Novel insights into hydrogen sulfide-mediated cytoprotection. Antioxidants & Redox Signaling, 12, 1203-1217.
66. Hydock, D. S.; Lien, C. Y.; Jensen, B. T.; Schneider, C. M.; & Hayward, R. (2011). Exercise preconditioning provides long-term protection against early chronic doxorubicin cardiotoxicity. Integrative Cancer Therapies, 10, 47-57.
67. Muthusamy, V. R.; Kannan, S.; Sadhaasivam, K.; Gounder, S. S.; Davidson, C. J.; Boeheme, C.; et al. (2012). Acute exercise stress activates Nrf2/ARE signaling and promotes antioxidant mechanisms in the myocardium. Free Radical Biology and Medicine, 52, 366-376.
68. Zhu, H.; Zhang, L.; Xi, X.; Zweier, J. L.; & Li, Y. (2006). 4-Hydroxy-2-nonenal upregulates endogenous antioxidants and phase 2 enzymes in rat H9c2 myocardiac cells: Protection against overt oxidative and electrophilic injury. Free Radical Research, 40, 875-884.
69. Giudice, A.; Arra, C.; & Turco, M. C. (2010). Review of molecular mechanisms involved in the activation of the Nrf2-ARE signaling pathway by chemopreventive agents. Methods in Molecular Biology, 647, 37-74.