A novel thiol antioxidant that crosses the blood brain barrier protects dopaminergic neurons in experimental models of Parkinson's disease

European Journal of Neuroscience

Volumn 21, Issue 3, 2005, Pages 637-646

  Bahat Stroomza, Merav ^a   Gilgun Sherki, Yossi ^a   Offen, Daniel ^a   Panet, Hana ^a   Saada, Ann ^c   Krool Galron, Nili ^a   Barzilai, Aari ^a   Atlas, Daphne ^b   Melamed, Eldad ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c SHAARE ZEDEK MEDICAL CENTER   (Israel)

Author keywords

6 OHDA; AD4; Antioxidants; MPTP; Oxidative stress; Parkinson's disease; Rotenone

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; AD4; AMPHETAMINE; ANTIOXIDANT; NEUROTOXIN; OXIDOPAMINE; ROTENONE; THIOL DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; DISEASE COURSE; DOPAMINERGIC NERVE CELL; DRUG MECHANISM; DRUG PENETRATION; MALE; NERVE CELL DEGENERATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIOXIDANTS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CELL LINE, TUMOR; CELLS, CULTURED; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; MALE; NEURONS; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSONIAN DISORDERS; PC12 CELLS; RATS; RATS, INBRED LEW; RATS, SPRAGUE-DAWLEY; SULFHYDRYL COMPOUNDS;

EID: 14944376569     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03889.x     Document Type: Article

References (71)

1. Akaneya, Y., Takahashi, M. & Hatanaka, H. (1995) Involvement of free radicals in MPP+ neurotoxicity against rat dopaminergic neurons in culture. Neurosci. Lett., 193, 53-56.
2. Aruoma, O.I., Halliwell, B., Hoey, B.M. & Butler, J. (1988) The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem. J., 256, 251-255.
3. Aruoma, O.I., Halliwell, B., Hoey, B.M. & Butler, J. (1989) The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free Rad. Biol. Med., 6, 593-597.
4. Atlas, D., Melamed, E. & Offen, D. (1999) Brain targeted low molecular weight hydrophobic antioxidant compounds. United States Patent #US5874468.
5. Bains, J.S. & Shaw, C.A. (1997) Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res. Rev., 25, 335-358.
6. Banaclocha, M.M. (2001) Therapeutic potential of N-acetylcysteine in age-related mitochondrial neurodegenerative diseases. Med. Hypotheses, 56, 472-477.
7. Beal, M.F. (1998) Excitotoxicity and nitric oxide in Parkinson's disease pathogenesis. Ann. Neurol., 44, S110-S114.
8. Betarbet, R., Sherer, T.B., Mackenzie, G., Garcia-Osuna, M., Panov, A.V. & Greenamyre, J.T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nature Neuro., 3, 1301-1306.
9. Birch-Machin, M.A. & Turnbull, D.M. (2001) Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissue. Meth. Cell Biol., 65, 97-117.
10. Borefreund, E. & Purner, J.A. (1984) A simple quantitative procedure using monolayer cultures for cytotoxicity assay. J. Tiss. Cult. Meth., 9, 7-9.
11. Carman, L.S., Gage, F.H. & Shults, C.W. (1991) Partial lesion of the substantia nigra: relation between extent of lesion and rotational behavior. Brain Res., 553, 275-283.
12. Dajas-Bailador, F.A., Martinez-Borges, A., Costa, G., Abin, J.A., Martignoni, E., Nappi, G. & Dajas, F. (1998) Hydroxyl radical production in the substantia nigra after 6-hydroxydopamine and hypoxia-reoxygenation. Brain Res., 813, 18-25.
13. Damier, P., Hirsch, E.C., Zhang, P., Agid, Y. & Javoy-Agid, F. (1993) Glutathione peroxidase, glial cells and Parkinson's disease. Neuroscience, 52, 1-7.
14. Dehmer, T., Lindenau, J., Haid, S., Dichgans, J. & Schulz, J.B. (2000) Deficiency of inducible nitric oxide synthase protects against MPTP toxicity in vivo. J. Neurochem., 74, 2213-2216.
15. Deneke, S.M. (2000) Thiol-based antioxidants. Curr. Topics Cell Regul., 36, 151-180.
16. Dexter, D.T., Carter, C.J., Wells, F.R., Javoy-Agid, F., Agid, Y., Lees, A., Jenner, P. & Marsden, C.D. (1989) Basal lipid peroxidation in substantia nigra is increased in Parkinson's disease. J. Neurochem., 52, 381-389.
17. Dringen, R., Gutterer, J.M. & Hirlinger, J. (2000) Glutathione metabolism in the brain. Eur. J. Biochem., 267, 4912-4916.
18. Fahn, S. & Cohen, G. (1992) The oxidant stress hypothesis in Parkinson's disease. Evidence supporting it. Ann. Neurol., 32, 804-812.
19. Fitzmaurice, P., Ang, L., Guttman, M., Rajput, A., Furukawa, Y. & Kish, S.J. (2003) Nigral glutathione deficiency is not specific for idiopathic Parkinson's disease. Mov. Disord., 9, 969-976.
20. Floor, E. & Wetzel, M.G. (1998) Increased protein oxidation in human substantia nigra pars compacta in comparison with basal ganglia and preforontal cortex measured with an improved dinitrophenylhydrazine assay. J. Neurochem., 70, 2675-2682.
21. Gao, H.M., Hong, J.S., Zhang, W. & Liu, B. (2002) Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci., 22, 782-790.
22. 2 and 6-hydroxydopamine. Mov. Disord., 13, 242-248.
23. Gilgun-Sherki, Y., Melamed, E. & Offen, D. (2001) Oxidative stress induced-neurodegenerative diseases: the need for antioxidants that penetrate the blood brain barrier. Neuropharmacology, 40, 959-975.
24. Greenamyre, J.T., Sherer, T.B., Betarbet, R. & Panov, A.V. (2001) Complex I and Parkinson's disease. IUBMB Life, 52, 135-141.
25. Griffith, O.W. (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem., 106, 207-212.
26. Hefti, F., Enz, A. & Melamed, E. (1982) Partial lesions of the nigrostriatal pathway in the rat. Acceleration of transmitter synthesis and release of surviving dopaminergic neurones by drugs. Neuropharmacology, 24, 19-23.
27. Hudson, J.L., Craig, V.H.G., Stromberg, I., Brock, S., Clayton, J., Masserano, J., Hoffer, B.J. & Gerhardt, G.A. (1993) Correlation of apomorphine and amphetamine-induced turning with nigrostriatal dopamine content in inilateral 6-hydroxydopamine lesioned rats. Brain Res., 626, 167-174.
28. Ishiyama, M., Tominaga, H., Shiga, M., Sasamoto, K., Ohkura, Y. & Ueno, K. (1996) A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet. Biol. Pharm. Bull., 19, 1518-1520.
29. Jackson-Lewis, V. & Liberatore, G. (2000) Effects of a unilateral stereotaxic injection of Tinuvin 123 into the substantia nigra on the nigrostriatal dopaminergic pathway in the rat. Brain Res., 866, 197-210.
30. Jenner, P. (1998) Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov. Disord., 13, 24-34.
31. Jenner, P. & Olanow, C.W. (1998) Understanding cell death in Parkinson's disease. Ann. Neurol., 3, 72-84.
32. Jenner, P. & Olnaw, C.W. (1996) Oxidative stress and the pathogenesis of Parkinson's disease. Neurology, 47, S161-S176.
33. Kim, D.H., Jang, Y.Y., Han, E.S. & Lee, C.S. (2001) Protective effect of harmaline and harmalol against dopamine- and 6-hydroxydopamine-induced oxidative damage of brain mitochondria and synaptosomes, and viability loss of PC12 cells. Eur. J. Neurosci., 13, 1861-1872.
34. LeBel, C.P. & Bondy, S.C. (1990) Sensitive and rapid quantification of reactive oxygen species in rat synatptosoraes. Neurochem. Int., 17, 435-440.
35. Martinez, M., Martinez, N., Hernandez, A.I. & Ferrandiz, M.L. (1999) Hypothesis: can N-acetylcysteine be beneficial in Parkinson's disease. Life Sci., 64, 1253-1257.
36. Meister, A. & Anderson, M.E. (1983) Glutathione. Ann. Rev. Biochem., 52, 711-760.
37. Melamed, E., Offen, D., Shirvan, A. & Ziv, I. (2000) Levodopa - an exotoxin or a therapeutic drug? J. Neurol., 247, 135-139.
38. Mytilineou, C., Walker, R.H., JnoBaptiste, R. & Olanow, C.W. (2003) Levodopa is toxic to dopamine neurons in an in vitro but not an in vivo model of oxidative stress. J. Pharmacol. Exp. Ther., 304, 792-800.
39. Offen, D., Gilgun-Sherki, Y., Barhum, Y., Benhar, M., Grinberg, L., Reich, R., Melamed, E. & Atlas, D. (2004) A low molecular weight copper chelator crosses the blood brain barrier and attenuates experimental autoimmune encephalomyelitis. J. Neurochem., 89, 1241-1251.
40. Offen, D., Gorodin, S., Melamed, E., Hanania, J. & Malik, Z. (1999) Dopamine melanin is actively phagocytized by PC12 cells and cerebellar granular cells. Possible implications for the etiology of Parkinson's disease. Neurosci. Lett., 260, 101-104.
41. Offen, D., Sherki, Y., Melamed, E., Fridkin, M., Brenneman, D.E. & Gozes, I. (2000) Vasoactive intestinal peptide (VIP) prevents neurotoxicity in neuronal cultures: relevance to neuroprotection in Parkinson's disease. Brain Res., 854, 257-262.
42. Offen, D., Ziv, I., Gorodin, S., Barzilai, A., Malik, Z. & Melamed, E. (1995) Dopamine induced programmed cell death in mouse thymocytes. Biochem. Biophys. Acta., 1268, 171-177.
43. Offen, O., Ziv, I., Sternin, H., Melamed, E. & Hochman, A. (1996) Prevention of dopamine-induced cell death by thiol antioxidants: possible implications for treatment of Parkinson's disease. Exp. Neurol., 141, 32-39.
44. Pavon, N., Vidal, L., Alvarez, P., Blanco, L., Torres, A., Rodriguez, A. & Macias, R. (1998) Behavioral evaluation of the unilateral lesion model in rats using 6-hydroxydopamine. Correlation between the rotations induced by D-amphetamine, apomorphine and the manual dexterity test. Rev. Neurol., 26, 915-918.
45. Paxinos, G. & Watson, C. (1986) The rat brain in stereotaxic coordinate. Academic Press, New York.
46. Perese, D.A., Ulman, J., Viola, J., Ewing, S.E. & Bankiewicz, K.S. (1989) 6-hydroxydopamine-induced selective parkinsonian rat model. Brain Res., 494, 285-293.
47. Petroske, E., Meredith, G.E., Callen, S., Totterdell, S. & Lau, Y.S. (2001) Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience, 106, 589-601.
48. Przedborski, S., Jackson-Lewis, V., Djaldetti, R., Liberatore, G., Vila, M., Vukosavic, S. & Almer, G. (2000) The parkinsonian toxin MPTP: action and mechanism. Restor. Neurol. Neurosci., 16, 135-142.
49. Rao, A.V. & Balachandran, B. (2002) Role of oxidative stress and antioxidants in neurodegenerative diseases. Nutr. Neurosci., 5, 291-309.
50. Reid, M. & Jahoor, F. (2001) Glutathione in disease. Curr. Opin. Clin. Nutr. Metab. Care, 4, 65-71.
51. Ruffmann, R. & Wendel, A. (1991) GSH rescue by N-acetylcysteine. Klin Wochenschr., 69, 857-862.
52. Sandstrom, P.A., Mannie, M.D. & Buttke, T.M. (1994) Inhibition of activation-induced death in T cell hybridomas by thiol antioxidants: oxidative stress as a mediator of apoptosis. J. Leukoc. Biol., 55, 221-226.
53. Schober, A. (2004) Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res., 318, 215-224.
54. Schultz, J.B., Lindenau, J., Seyfried, J. & Dichgans, J. (2000) Glutathione, oxidative stress and neurodegeneration. Eur. J. Biochem., 267, 4904-4911.
55. Sechi, G., Deeden, M.G., Bua, G., Satta, W.M., Deiana, G.A., Pes, G.M. & Rosati, G. (1996) Reduced intravenous glutathione in the treatment of early Parkinson's disease. Prog. Neuro. Psychopharmacol. Biol. Psychiat., 20, 1159-1170.
56. Shepherd, J.A. & Garland, P.B. (1969) The kinetic properties of citrate synthase from rat liver mitochondria. Biochem. J., 114, 597-610.
57. Sherer, T.B., Betarbet, R., Kim, J.H. & Greenamyre, J.T. (2003a) Selective microglial activation in the rat rotenone model of Parkinson's disease. Neurosci. Lett., 341, 87-90.
58. Sherer, T.B., Betarbet, R., Testa, C.M., Seo, B.B., Richardson, J.R., Kim, J.H., Miller, G.W., Yagi, T., Matsuno-Yagi, A. & Greenamyre, J.T. (2003b) Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci., 23, 10756-10764.
59. Sian, J., Dexter, D.T., Lees, A., Daniel, S., Agid, Y., Javoy-Agid, F., Jenner, P. & Marsden, C.D. (1994) Alteration in glutathione levels in Parkinson's disease and other neurodegenerative disorders affective basal ganglia. Ann. Neurol., 36, 348-355.
60. Sies, H. (1999) Glutathione and its role in cellular functions. Free Radic. Biol. Med., 27, 916-921.
61. Simonian, N.A. & Coyle, J.T. (1996) Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol., 36, 83-106.
62. Sofic, E., Paulus, W., Jellinger, K., Riederer, P. & Youdim, M.B. (1991) Selective increase of iron in substantia nigra zona compacta of parkinsonian brains. J. Neurochem., 56, 978-982.
63. Sriram, K., Pai, K.S., Boyd, M.R. & Ravindranath, V. (1997) Evidence for generation of oxidative stress in brain by MPTP: in vitro and in vivo studies in mice. Brain Res., 749, 44-52.
64. Thomas, J., Wang, J., Takubo, H., Sheng, J., de Jesus, S. & Bankiewicz, K.S. (1994) A 6-hydroxydopamine-induced selective parkinsonian rat model: further biochemical and behavioral characterization. Exp. Neurol., 126, 159-167.
65. Tietze, F. (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Ann. Biochem., 27, 502-522.
66. Tolwani, R.J., Jakowec, M.W., Petzinger, G.M., Green, S. & Waggie, K. (1999) Experimental models of Parkinson's disease: insights from many models. Lab. Anim. Sci., 49, 363-371.
67. Wong, S.S., Li, R.H. & Stadlin, A. (1999) Oxidative stress induced by MPTP and MPP(+): selective vulnerability of cultured mouse astrocytes. Brain Res., 836, 237-244.
68. Zhang, S.Z., Lipsky, M.M., Trump, B.F. & Hsu, I.C. (1990) Neutral red (NR) assay for cell viability and xenobiotic-induced cytotoxicity in primary cultures of human and rat hepatocytes. Cell Biol. Toxicol., 6, 219-234.
69. Zhang, J., Perry, G., Smith, M.A., Robertson, D., Olson, S.J., Graham, D.G. & Montine, T.J. (1999) Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol., 154, 1423-1429.
70. Ziv, I., Melamed, E., Nardi, N., Luria, D., Achiron, A., Offen, D. & Barzilai, A. (1994) Dopamine induces apoptosis like cell death in cultured sympathetic neurons: a possible novel pathogenic mechanism in Parkinson's disease. Neurosci. Lett., 170, 136-140.
71. Ziv, I., Zilkha-Falb, R., Offen, D., Shirvan, A., Barzilai, A. & Melamed, E. (1997) Levodopa induces apoptosis in cultured neuronal cells - a possible accelerator of nigrostriatal degeneration in Parkinson's disease? Mov. Disord., 12, 17-23.