Glutathione elevation by γ-glutamyl cysteine ethyl ester as a potential therapeutic strategy for preventing oxidative stress in brain mediated by in vivo administration of adriamycin: Implication for chemobrain

Journal of Neuroscience Research

Volumn 85, Issue 3, 2007, Pages 497-503

  Joshi, Gururaj ^a   Hardas, Sarita ^a   Sultana, Rukhsana ^a   St Clair, Daret K ^a   Vore, Mary ^a   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

glutamyl cysteine ethyl ester (GCEE); Adriamycin; Chemobrain; Glutathione; Oxidative stress

Indexed keywords

DOXORUBICIN; GAMMA GLUTAMYL CYSTEINE ETHYL ESTER; GLUTATHIONE; GLUTATHIONE REDUCTASE; GLUTATHIONE TRANSFERASE; INDUCIBLE NITRIC OXIDE SYNTHASE; MULTIDRUG RESISTANCE PROTEIN 1; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN METABOLISM; CANCER CHEMOTHERAPY; CONTROLLED STUDY; ENZYME ACTIVITY; IN VIVO STUDY; LIPID PEROXIDATION; MALE; MOUSE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL;

ANIMALS; BRAIN; CARBON MONOXIDE; DIPEPTIDES; DOXORUBICIN; GLUTATHIONE; GLUTATHIONE TRANSFERASE; MALE; MICE; MICE, INBRED STRAINS; MODELS, ANIMAL; OXIDATIVE STRESS; TYROSINE;

EID: 33847307470     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21158     Document Type: Article

References (62)

1. Adair JC, Knoefel JE, Morgan N. 2001. Controlled trial of N-acetylcysteine for patients with probable Alzheimer's disease. Neurology 57:1515-1517.
2. Anderson ME, Luo JL. 1998. Glutathione therapy: from prodrugs to genes. Semin Liver Dis 18:415-424.
3. Behl C, Davis J, Cole GM, Schubert D. 1992. Vitamin E protects nerve cells from amyloid beta protein toxicity. Biochem Biophys Res Commun 186:944-950.
4. Behl C, Skutella T, Lezoualc'h F, Post A, Widmann M, Newton CJ, Holsboer F. 1997. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol Pharmacol 51:535-541.
5. Benzi G, Moretti A. 1995. Age- and peroxidative stress-related modifications of the cerebral enzymatic activities linked to mitochondria and the glutathione system. Free Radic Biol Med 19:77-101.
6. Bigotte L, Arvidson B, Olsson Y. 1982a. Cytofluorescence localization of adriamycin in the nervous system. I. Distribution of the drug in the central nervous system of normal adult mice after intravenous injection. Acta Neuropathol 57:121-129.
7. Bigotte L, Arvidson B, Olsson Y. 1982b. Cytofluorescence localization of adriamycin in the nervous system. II. Distribution of the drug in the somatic and autonomic peripheral nervous systems of normal adult mice after intravenous injection. Acta Neuropathol 57:130-136.
8. Boyd-Kimball D, Sultana R, Abdul HM, Butterfield DA. 2005a. Gamma-glutamylcysteine ethyl ester-induced up-regulation of glutathione protects neurons against Abeta(1-42)-mediated oxidative stress and neurotoxicity: implications for Alzheimer's disease. J Neurosci Res 79:700-706.
9. Boyd-Kimball D, Sultana R, Poon HF, Mohmmad-Abdul H, Lynn BC, Klein JB, Butterfield DA. 2005b. Gamma-glutamylcysteine ethyl ester protection of proteins from Abeta(1-42)-mediated oxidative stress in neuronal cell culture: a proteomics approach. J Neurosci Res 79:707-713.
10. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
11. Butterfield DA, Kanski J. 2001. Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech Ageing Dev 122:945-962.
12. Butterfield DA, Lauderback CM. 2002. Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic Biol Med 32:1050-1060.
13. Butterfield DA, Drake J, Pocernich C, Castegna A. 2001. Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol Med 7:548-554.
14. Butterfield D, Castegna A, Pocernich C, Drake J, Scapagnini G, Calabrese V. 2002. Nutritional approaches to combat oxidative stress in Alzheimer's disease. J Nutr Biochem 13:444.
15. Butterfield DA, Poon HF, St. Clair D, Keller JN, Pierce WM, Klein JB, Markesbery WR. 2006. Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer's disease. Neurobiol Dis 22:223-232.
16. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 1992. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G→T and A→C substitutions. J Biol Chem 267:166-172.
17. Chuang RY, Chuang LF. 1979. Inhibition of chicken myeloblastosis RNA polymerase II activity by adriamycin. Biochemistry 18:2069-2073.
18. Conseil G, Deeley RG, Cole SP. 2005. Polymorphisms of MRP1 (ABCC1) and related ATP-dependent drug transporters. Pharmacogenet Genom 15:523-533.
19. Cooper J. 1997. Glutathione in the brain: disorders of glutathione metabolism. In: The Molecular and Genetic Basis of Neurological Disease. Barchi R, Kunk L, editors. Boston: Butterworth-Heinemann.
20. Cummings J, Anderson L, Willmott N, Smyth JF. 1991. The molecular pharmacology of doxorubicin in vivo. Eur J Cancer 27:532-535.
21. DeAtley SM, Aksenov MY, Aksenova MV, Carney JM, Butterfield DA. 1998. Adriamycin induces protein oxidation in erythrocyte membranes. Pharmacol Toxicol 83:62-68.
22. DeAtley SM, Aksenov MY, Aksenova MV, Harris B, Hadley R, Cole Harper P, Carney JM, Butterfield DA. 1999. Antioxidants protect against reactive oxygen species associated with adriamycin-treated cardiomyocytes. Cancer Lett 136:41-46.
23. Deres P, Halmosi R, Toth A, Kovacs K, Palfi A, Habon T, Czopf L, Kalai T, Hideg K, Sumegi B, Toth K. 2005. Prevention of doxorubicin-induced acute cardiotoxicity by an experimental antioxidant compound. J Cardiovasc Pharmacol 45:36-43.
24. Doroshow JH, Davies KJ. 1986. Redox cycling of anthracyclines by cardiac mitochondria. II. Formation of superoxide anion, hydrogen peroxide, and hydroxyl radical. J Biol Chem 261:3068-3074.
25. Drake J, Kanski J, Varadarajan S, Tsoras M, Butterfield DA. 2002. Elevation of brain glutathione by gamma-glutamylcysteine ethyl ester protects against peroxynitrite-induced oxidative stress. J Neurosci Res 68:776-784.
26. Drake J, Sultana R, Aksenova M, Calabrese V, Butterfield DA. 2003. Elevation of mitochondrial glutathione by gamma-glutamylcysteine ethyl ester protects mitochondria against peroxynitrite-induced oxidative stress. J Neurosci Res 74:917-927.
27. Freeman JR, Broshek DK. 2002. Assessing cognitive dysfunction in breast cancer: what are the tools? Clin Breast Cancer 3(Suppl 3):S91-S99.
28. Good PF, Werner P, Hsu A, Olanow CW, Perl DP. 1996. Evidence of neuronal oxidative damage in Alzheimer's disease. AmJ Pathol 149:21-28.
29. Goodman Y, Bruce AJ, Cheng B, Mattson MP. 1996. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. J Neurochem 66:1836-1844.
30. Gutierrez PL. 2000. The role of NAD(P)H oxidoreductase (DT-diaphorase) in the bioactivation of quinone-containing antitumor agents: a review. Free Radic Biol Med 29:263-275.
31. Habig WH, Pabst MJ, Jakoby WB. 1974. Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130-7139.
32. Halliwell B. 2001. Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 18:685-716.
33. Halliwell B, Gutteridge J. 1999. Free radical biology and medicine. New York: Oxford University Press. p 246-343.
34. Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, Aksenova M, Gabbita SP, Wu JF, Carney JM, et al. 1995. Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J Neurochem 65:2146-2156.
35. Joshi G. 2006. Multifunctional potential therapeutics for oxidative stress-related disorders and models thereof. Ph.D. Dissertation: University of Kentucky.
36. 2 or 2,2-azobis-(2-amidinopropane) dihydrochloride by the glutathione mimetic tricyclodecan-9-yl-xanthogenate. Free Radic Biol Med 38:1023-1031.
37. Joshi G, Sultana R, Tangpong J, Cole MP, St. Clair DK, Vore M, Estus S, Butterfield DA. 2005b. Free radical mediated oxidative stress and toxic side effects in brain induced by the anticancer drug adriamycin: insight into chemobrain. Free Radic Res 39:1147-1154.
38. Lauderback CM, Kanski J, Hackett JM, Maeda N, Kindy MS, Butterfield DA. 2002. Apolipoprotein E modulates Alzheimer's Abeta(1-42)-induced oxidative damage to synaptosomes in an allele-specific manner. Brain Res 924:90-97.
39. Lovell MA, Xie C, Markesbery WR. 1998. Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer's disease. Neurology 51:1562-1566.
40. Markesbery WR, Lovell MA. 1998. Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol Aging 19:33-36.
41. Meister A, Anderson ME. 1983. Glutathione. Annu Rev Biochem 52:711-760.
42. Meyers CA. 2000. Neurocognitive dysfunction in cancer patients. Oncology 14:75-79 [discussion 79, 81-82, 85].
43. Moreira PI, Smith MA, Zhu X, Nunomura A, Castellani RJ, Perry G. 2005. Oxidative stress and neurodegeneration. Ann N Y Acad Sci 1043:545-552.
44. Nies AT, Jedlitschky G, Konig J, Herold-Mende C, Steiner HH, Schmitt HP, Keppler D. 2004. Expression and immunolocalization of the multidrug resistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129:349-360.
45. Pappolla MA, Sos M, Omar RA, Bick RJ, Hickson-Bick DL, Reiter RJ, Efthimiopoulos S, Robakis NK. 1997. Melatonin prevents death of neuroblastoma cells exposed to the Alzheimer amyloid peptide. J Neurosci 17:1683-1690.
46. Pocernich CB, Cardin AL, Racine CL, Lauderback CM, Butterfield DA. 2001. Glutathione elevation and its protective role in acrolein-induced protein damage in synaptosomal membranes: relevance to brain lipid peroxidation in neurodegenerative disease. Neurochem Int 39:141-149.
47. Pocernich CB, Sultana R, Mohmmad-Abdul H, Nath A, Butterfield DA. 2005. HIV-dementia, Tat-induced oxidative stress, and antioxidant therapeutic considerations. Brain Res Brain Res Rev 50:14-26.
48. Poon HF, Calabrese V, Calvani M, Butterfield DA. 2006. Proteomics analyses of specific protein oxidation and protein expression in aged rat brain and its modulation by L-acetylcarnitine: insights into the mechanisms of action of this proposed therapeutic agent for CNS disorders associated with oxidative stress. Antiox Redox Signal 8:381-394.
49. Renes J, de Vries EE, Hooiveld GJ, Krikken I, Jansen PL, Muller M. 2000. Multidrug resistance protein MRP1 protects against the toxicity of the major lipid peroxidation product 4-hydroxynonenal. Biochem J 350:555-561.
50. Sarvazyan N. 1996. Visualization of doxorubicin-induced oxidative stress in isolated cardiac myocytes. Am J Physiol 271:H2079-H2085.
51. Schagen SB, Hamburger HL, Muller MJ, Boogerd W, van Dam FS. 2001. Neurophysiological evaluation of late effects of adjuvant high-dose chemotherapy on cognitive function. J Neurooncol 51:159-165.
52. Sies H, Sharov VS, Klotz LO, Briviba K. 1997. Glutathione peroxidase protects against peroxynitrite-mediated oxidations. A new function for selenoproteins as peroxynitrite reductase. J Biol Chem 272:27812-27817.
53. Smith JV, Luo Y. 2003. Elevation of oxidative free radicals in Alzheimer's disease models can be attenuated by Ginkgo biloba extract EGb 761. J Alzheimers Dis 5:287-300.
54. Stadtman ER, Berlett BS. 1997. Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10:485-494.
55. Steinherz LJ, Steinherz PG, Tan CT, Heller G, Murphy ML. 1991. Cardiac toxicity 4 to 20 years after completing anthracycline therapy. JAMA 266:1672-1677.
56. Sultana R, Butterfield DA. 2004. Oxidatively modified GST and MRP1 in Alzheimer's disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res 29:2215-2220.
57. Sultana R, Perluigi M, Butterfield DA. 2006. Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Abeta(1-42). J Chromatogr B Anal Technol Biomed Life Sci 833:3-11.
58. Tangpong J, Cole MP, Sultana R, Estus S, Vore M, St. Clair W, Ratanachaiyavong S, St. Clair D, Butterfield D. 2006a. Adriamycin-mediated nitration of manganese superoxide dismutase in the central nervous system: Insight into the mechanism of chemobrain. J Neurochem (in press).
59. Tangpong J, Cole MP, Sultana R, Joshi G, Estus S, Vore M, St. Clair W, Ratanachaiyavong S, St. Clair DK, Butterfield DA. 2006b. Adriamycin-induced, TNF-alpha-mediated central nervous system toxicity. Neurobiol Dis 23:127-139.
60. Vasquez-Vivar J, Martasek P, Hogg N, Masters BS, Pritchard KA Jr, Kalyanaraman B. 1997. Endothelial nitric oxide synthase-dependent superoxide generation from adriamycin. Biochemistry 36:11293-11297.
61. Wang J, Xiong S, Xie C, Markesbery WR, Lovell MA. 2005. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease. J Neurochem 93:953-962.
62. Yen HC, Oberley TD, Gairola CG, Szweda LI, St. Clair DK. 1999. Manganese superoxide dismutase protects mitochondrial complex I against adriamycin-induced cardiomyopathy in transgenic mice. Arch Biochem Biophys 362:59-66.