In vivo protection of synaptosomes by ferulic acid ethyl ester (FAEE) from oxidative stress mediated by 2,2-azobis(2-amidino-propane)dihydrochloride (AAPH) or Fe2+/H2O2: Insight into mechanisms of neuroprotection and relevance to oxidative stress-related neurodegenerative disorders

Neurochemistry International

Volumn 48, Issue 4, 2006, Pages 318-327

  Joshi, Gururaj ^a   Perluigi, Marzia ^a,c   Sultana, Rukhsana ^a   Agrippino, Ravagna ^d   Calabrese, Vittorio ^d   Butterfield, D Allan ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF CATANIA   (Italy)

Author keywords

Ferulic acid ethyl ester (FAEE); Heat shock protein; Heme oxygenase 1; Inducible nitric oxide synthase (iNOS); Oxidative stress in vivo

Indexed keywords

2,2 AZOBIS(2 AMIDINO PROPANE) DIHYDROCHLORIDE; 3 NITROTYROSINE; 4 HYDROXYNONENAL; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CARBONYL DERIVATIVE; CHLORINE DERIVATIVE; DIMETHYL SULFOXIDE; ESTER DERIVATIVE; FERROUS ION; FERULIC ACID ETHYL ESTER; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; HYDROGEN PEROXIDE; NITRIC OXIDE SYNTHASE; OXIDIZING AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DEGENERATIVE DISEASE; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; FLUORESCENCE; GERBIL; IN VIVO STUDY; LIPOPHILICITY; MALE; NEUROPROTECTION; NITRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATISTICAL ANALYSIS; SYNAPTOSOME; WESTERN BLOTTING;

ALDEHYDES; AMIDINES; ANIMALS; CAFFEIC ACIDS; FERROUS COMPOUNDS; GERBILLINAE; HEME OXYGENASE (DECYCLIZING); HSP70 HEAT-SHOCK PROTEINS; HYDROGEN PEROXIDE; MALE; NEURODEGENERATIVE DISEASES; NEUROPROTECTIVE AGENTS; NITRATES; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SYNAPTOSOMES;

ANIMALIA; GERBILLINAE;

EID: 31744434516     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2005.11.006     Document Type: Article

References (70)

1. Y.C. Awasthi, R. Sharma, J.Z. Cheng, Y. Yang, A. Sharma, S.S. Singhal, and S. Awasthi Role of 4-hydroxynonenal in stress-mediated apoptosis signaling Mol. Aspects Med. 24 2003 219 230
2. K. Ayasolla, M. Khan, A.K. Singh, and I. Singh Inflammatory mediator and beta-amyloid (25-35)-induced ceramide generation and iNOS expression are inhibited by vitamin E Free Radic. Biol. Med. 37 2004 325 338
3. J.S. Beckman, T.W. Beckman, J. Chen, P.A. Marshall, and B.A Freeman Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide Proc. Natl. Acad. Sci. U.S.A. 87 1990 1620 1624
4. D. Boyd-Kimball, R. Sultana, H.F. Poon, H. Mohmmad-Abdul, B.C. Lynn, J.B. Klein, and D.A. Butterfield 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 2005 707 713
5. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
6. D.S. Bredt Endogenous nitric oxide synthesis: biological functions and pathophysiology Free Radic. Res. 31 1999 577 596
7. D. Butterfield, A. Castegna, C. Pocernich, J. Drake, G. Scapagnini, and V. Calabrese Nutritional approaches to combat oxidative stress in Alzheimer's disease J. Nutr. Biochem. 13 2002 444
8. D. Butterfield, and E.R. Stadtman Protein oxidation processes in aging brain Adv. Cell Aging Gerontol. 2 1997 161 191
9. D.A. Butterfield Beta-amyloid-associated free radical oxidative stress and neurotoxicity: implications for Alzheimer's disease Chem. Res. Toxicol. 10 1997 495 506
10. D.A. Butterfield Amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review Free Radic. Res. 36 2002 1307 1313
11. D.A. Butterfield, A. Castegna, C.M. Lauderback, and J. Drake Evidence that amyloid beta-peptide-induced lipid peroxidation and its sequelae in Alzheimer's disease brain contribute to neuronal death Neurobiol. Aging 23 2002 655 664
12. D.A. Butterfield, J. Drake, C. Pocernich, and A. Castegna Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide Trends Mol. Med. 7 2001 548 554
13. D.A. Butterfield, and C.M. Lauderback 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 2002 1050 1060
14. V. Calabrese, A.M. Stella, D.A. Butterfield, and G. Scapagnini Redox regulation in neurodegeneration and longevity: role of the heme oxygenase and HSP70 systems in brain stress tolerance Antioxid. Redox Signal. 6 2004 895 913
15. V. Calabrese, A.M. Stella, D.A. Butterfield, and G. Scapagnini Redox regulation in neurodegeneration and longevity: role of the heme oxygenase and HSP70 systems in brain stress tolerance Antioxid. Redox Signal. 6 2004 895 913
16. A. Castegna, M. Aksenov, M. Aksenova, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery, and D.A. Butterfield Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I. Creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1 Free Radic. Biol. Med. 33 2002 562 571
17. A. Castegna, M. Aksenov, V. Thongboonkerd, J.B. Klein, W.M. Pierce, R. Booze, W.R. Markesbery, and D.A. Butterfield Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part II. Dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71 J. Neurochem. 82 2002 1524 1532
18. A. Castegna, V. Thongboonkerd, J.B. Klein, B. Lynn, W.R. Markesbery, and D.A. Butterfield Proteomic identification of nitrated proteins in Alzheimer's disease brain J. Neurochem. 85 2003 1394 1401
19. K. Chen, K. Gunter, and M.D. Maines Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death J. Neurochem. 75 2000 304 313
20. S. Dore Decreased activity of the antioxidant heme oxygenase enzyme: implications in ischemia and in Alzheimer's disease Free Radic. Biol. Med. 32 2002 1276 1282
21. S.P. Gabbita, M.A. Lovell, and W.R. Markesbery Increased nuclear DNA oxidation in the brain in Alzheimer's disease J. Neurochem. 71 1998 2034 2040
22. T. Grune, and K.J. Davies The proteasomal system and HNE-modified proteins Mol. Aspects Med. 24 2003 195 204
23. E.D. Hall, M.R. Detloff, K. Johnson, and N.C. Kupina Peroxynitrite- mediated protein nitration and lipid peroxidation in a mouse model of traumatic brain injury J. Neurotrauma 21 2004 9 20
24. B. Halliwell Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment Drugs Aging 18 2001 685 716
25. K. Hensley, J. Carney, N. Hall, W. Shaw, and D.A. Butterfield Electron paramagnetic resonance investigations of free radical-induced alterations in neocortical synaptosomal membrane protein infrastructure Free Radic. Biol. Med. 17 1994 321 331
26. K. Hensley, N. Hall, R. Subramaniam, P. Cole, M. Harris, M. Aksenov, M. Aksenova, S.P. Gabbita, J.F. Wu, and J.M. Carney Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation J. Neurochem. 65 1995 2146 2156
27. G. Joshi, R. Sultana, M. Perluigi, and D. Allan Butterfield In vivo protection of synaptosomes from oxidative stress mediated by Fe(2+)/H(2)O(2) or 2,2-azobis-(2-amidinopropane)dihydrochloride by the glutathione mimetic tricyclodecan-9-yl-xanthogenate Free Radic. Biol. Med. 38 2005 1023 1031
28. J. Kanski, M. Aksenova, A. Stoyanova, and D.A. Butterfield Ferulic acid antioxidant protection against hydroxyl and peroxyl radical oxidation in synaptosomal and neuronal cell culture systems in vitro: structure-activity studies J. Nutr. Biochem. 13 2002 273 281
29. J. Kanski, C. Lauderback, and D.A. Butterfield 5-Aminosalicylic acid protection against oxidative damage to synaptosomal membranes by alkoxyl radicals in vitro Neurochem. Res. 26 2001 23 29
30. R. Katzman, and T. Saitoh Advances in Alzheimer's disease Faseb J. 5 1991 278 286
31. J.N. Keller, C.M. Lauderback, D.A. Butterfield, M.S. Kindy, J. Yu, and W.R. Markesbery Amyloid beta-peptide effects on synaptosomes from apolipoprotein E-deficient mice J. Neurochem. 74 2000 1579 1586
32. H. Kikuzaki, M. Hisamoto, K. Hirose, K. Akiyama, and H. Taniguchi Antioxidant properties of ferulic acid and its related compounds J. Agric. Food Chem. 50 2002 2161 2168
33. H.S. Kim, J.Y. Cho, D.H. Kim, J.J. Yan, H.K. Lee, H.W. Suh, and D.K. Song Inhibitory effects of long-term administration of ferulic acid on microglial activation induced by intracerebroventricular injection of beta-amyloid peptide (1-42) in mice Biol. Pharm. Bull. 27 2004 120 121
34. C.M. Lauderback, J.M. Hackett, F.F. Huang, J.N. Keller, L.I. Szweda, W.R. Markesbery, and D.A. Butterfield The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer's disease brain: the role of Abeta1-42 J. Neurochem. 78 2001 413 416
35. C.M. Lauderback, J. Kanski, J.M. Hackett, N. Maeda, M.S. Kindy, and D.A. Butterfield Apolipoprotein E modulates Alzheimer's Abeta(1-42)-induced oxidative damage to synaptosomes in an allele-specific manner Brain Res. 924 2002 90 97
36. W.D. Le, W.J. Xie, and S.H. Appel Protective role of heme oxygenase-1 in oxidative stress-induced neuronal injury J. Neurosci. Res. 56 1999 652 658
37. M.A. Lovell, S.P. Gabbita, and W.R. Markesbery Increased DNA oxidation and decreased levels of repair products in Alzheimer's disease ventricular CSF J. Neurochem. 72 1999 771 776
38. H.J. Luth, G. Munch, and T. Arendt Aberrant expression of NOS isoforms in Alzheimer's disease is structurally related to nitrotyrosine formation. Brain Res. 953 2002 135 143
39. R.J. Mark, M.A. Lovell, W.R. Markesbery, K. Uchida, and M.P. Mattson A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide J. Neurochem. 68 1997 255 264
40. W.R. Markesbery Oxidative stress hypothesis in Alzheimer's disease Free Radic. Biol. Med. 23 1997 134 147
41. W.R. Markesbery, and M.A. Lovell Four-hydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease Neurobiol. Aging 19 1998 33 36
42. M.P. Mattson Calcium and Free Radicals: Mediators of neurotrophic factor and excitatory transmitter-regulated developmental plasticity and cell death Persp. Dev. Neurobiol. 3 1996 79 91
43. L.J. McIntosh, M.A. Trush, and J.C. Troncoso Increased susceptibility of Alzheimer's disease temporal cortex to oxygen free radical-mediated processes Free Radic. Biol. Med. 23 1997 183 190
44. T. Ogiwara, K. Satoh, Y. Kadoma, Y. Murakami, S. Unten, T. Atsumi, H. Sakagami, and S. Fujisawa Radical scavenging activity and cytotoxicity of ferulic acid Anticancer Res. 22 2002 2711 2717
45. R.A. Omar, Y.J. Chyan, A.C. Andorn, B. Poeggeler, N.K. Robakis, and M.A. Pappolla Increased expression but reduced activity of antioxidant enzymes in Alzheimer's disease J. Alzheimers Dis. 1 1999 139 145
46. M.A. Pappolla, Y.J. Chyan, R.A. Omar, K. Hsiao, G. Perry, M.A. Smith, and P. Bozner Evidence of oxidative stress and in vivo neurotoxicity of beta-amyloid in a transgenic mouse model of Alzheimer's disease: a chronic oxidative paradigm for testing antioxidant therapies in vivo Am. J. Pathol. 152 1998 871 877
47. C.S. Park, G. Krishna, M.S. Ahn, J.H. Kang, W.G. Chung, D.J. Kim, H.K. Hwang, J.N. Lee, S.G. Paik, and Y.N. Cha Differential and constitutive expression of neuronal, inducible, and endothelial nitric oxide synthase mRNAs and proteins in pathologically normal human tissues Nitric Oxide 4 2000 459 471
48. C.B. Pocernich, A.L. Cardin, C.L. Racine, C.M. Lauderback, and D.A. Butterfield 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 2001 141 149
49. H.F. Poon, V. Calabrese, G. Scapagnini, and D.A. Butterfield Free radicals: key to brain aging and heme oxygenase as a cellular response to oxidative stress J. Gerontol. Series A: Biol. Sci. Med. Sci. 59 2004 478 493
50. L.M. Sayre, D.A. Zelasko, P.L. Harris, G. Perry, R.G. Salomon, and M.A. Smith 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer's disease J. Neurochem. 68 1997 2092 2097
51. G. Scapagnini, R. Foresti, V. Calabrese, A.M. Giuffrida Stella, C.J. Green, and R. Motterlini Caffeic acid phenyl ester and curcumin: a novel class of heme oxygenase-1 inducers Mol. Pharmacol. 61 2002 554 561
52. G. Scapagnini, D.A. Butterfield, C. Colombrita, R. Sultana, A. Pascale, and V. Calabrese Ethyl ferulate, a lipophilic polyphenol, induces HO-1 and protects rat neurons against oxidative stress Antioxid. Redox Signal. 6 2004 811 818
53. H.M. Schipper Heme oxygenase-1: role in brain aging and neurodegeneration Exp. Gerontol. 35 2000 821 830
54. E.P. Simpson, Y.K. Henry, J.S. Henkel, R.G. Smith, and S.H. Appel Increased lipid peroxidation in sera of ALS patients: a potential biomarker of disease burden Neurology 62 2004 1758 1765
55. E.R. Stadtman, and B.S. Berlett Reactive oxygen-mediated protein oxidation in aging and disease Chem. Res. Toxicol. 10 1997 485 494
56. R. Subramaniam, F. Roediger, B. Jordan, M.P. Mattson, J.N. Keller, G. Waeg, and D.A. Butterfield The lipid peroxidation product, 4-hydroxy-2-trans- nonenal, alters the conformation of cortical synaptosomal membrane proteins J. Neurochem. 69 1997 1161 1169
57. R. Sultana, and D.A. Butterfield Oxidatively modified GST and MRP1 in Alzheimer's disease brain: implications for accumulation of reactive lipid peroxidation products Neurochem. Res. 29 2004 2215 2220
58. R. Sultana, A. Ravagna, H. Mohmmad-Abdul, V. Calabrese, and D.A. Butterfield Ferulic acid ethyl ester protects neurons against amyloid beta-peptide(1-42)-induced oxidative stress and neurotoxicity: relationship to antioxidant activity J. Neurochem. 92 2005 749 758
59. M. Takahashi, S. Dore, C.D. Ferris, T. Tomita, A. Sawa, H. Wolosker, D.R. Borchelt, T. Iwatsubo, S.H. Kim, G. Thinakaran, S.S. Sisodia, and S.H. Snyder Amyloid precursor proteins inhibit heme oxygenase activity and augment neurotoxicity in Alzheimer's disease Neuron 28 2000 461 473
60. A. Takeda, G. Perry, N.G. Abraham, B.E. Dwyer, R.K. Kutty, J.T. Laitinen, R.B. Petersen, and M.A. Smith Overexpression of heme oxygenase in neuronal cells, the possible interaction with Tau J. Biol. Chem. 275 2000 5395 5399
61. R. Tyrrell Redox regulation and oxidant activation of heme oxygenase-1 Free Radic. Res. 31 1999 335 340
62. S. Varadarajan, S. Yatin, M. Aksenova, and D.A. Butterfield Review: Alzheimer's amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity J. Struct. Biol. 130 2000 184 208
63. H. Wang, and J.A. Joseph Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader Free Radic. Biol. Med. 27 1999 612 616
64. V.P. Whittaker Thirty years of synaptosome research J. Neurocytol. 22 1993 735 742
65. C. Xie, M.A. Lovell, and W.R. Markesbery Glutathione transferase protects neuronal cultures against four hydroxynonenal toxicity Free Radic. Biol. Med. 25 1998 979 988
66. J.J. Yan, J.Y. Cho, H.S. Kim, K.L. Kim, J.S. Jung, S.O. Huh, H.W. Suh, Y.H. Kim, and D.K. Song Protection against beta-amyloid peptide toxicity in vivo with long-term administration of ferulic acid Br. J. Pharmacol. 133 2001 89 96
67. B.P. Yu Cellular defenses against damage from reactive oxygen species Physiol. Rev. 74 1994 139 162
68. H. Yu, J. Hong, and D. Wu Effect of sodium ferulate on proliferation of rabbit aortic smooth muscle cells induced by oxidized LDL Zhongguo Zhong Yao Za Zhi 24 1999 365 366 384
69. K. Zarkovic 4-Hydroxynonenal and neurodegenerative diseases Mol. Aspects Med. 24 2003 293 303
70. D. Zhou, C.M. Lauderback, T. Yu, S.A. Brown, D.A. Butterfield, and J.S. Thompson D609 inhibits ionizing radiation-induced oxidative damage by acting as a potent antioxidant J. Pharmacol. Exp. Ther. 298 2001 103 109