Endoplasmic reticulum stress-induced cell death in dopaminergic cells: Effect of resveratrol

Journal of Molecular Neuroscience

Volumn 39, Issue 1-2, 2009, Pages 157-168

  Chinta, Shankar J ^a   Poksay, Karen S ^a   Kaundinya, Gaayatri ^b   Hart, Matthew ^a   Bredesen, Dale E ^a,c   Andersen, Julie K ^a   Rao, Rammohan V ^a  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b Marin Institute   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Caspase; Endoplasmic reticulum; Erstress; Programmed cell death; Resveratrol

Indexed keywords

CASPASE; CHAPERONE; ENZYME INHIBITOR; PARAQUAT; PROTEASOME; PROTEIN P23; RESVERATROL; SALUBRINAL; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL STRESS; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RAT;

ANIMALS; ANTIOXIDANTS; CASPASES; CELL DEATH; CELL LINE; CINNAMATES; DOPAMINE; ENDOPLASMIC RETICULUM; HUMANS; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; RATS; RNA INTERFERENCE; STILBENES; THIOUREA;

EID: 74149084501     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-008-9170-7     Document Type: Article

References (72)

1. Adams, F. S., La Rosa, F. G., Kumar, S., Edwards-Prasad, J., Kentroti, S., Vernadakis, A., et al. (1996). Characterization and transplantation of two neuronal cell lines with dopaminergic properties. Neurochemical Research, 21, 619-627. doi:10.1007/BF02527762.
2. Andersen, J. K. (2000). What causes the build-up of ubiquitincontaining inclusions in Parkinson's disease? Mechanisms of Ageing and Development, 118, 15-22. doi:10.1016/S0047-6374 (00) 00150-0.
3. Andersen, J. K. (2004). Oxidative stress in neurodegeneration: Cause or consequence? Nature Medicine, 10 (Suppl), S18-S25. doi:10.1038/nrn1434.
4. Bakhshi, J., Weinstein, L., Poksay, K. S., Nishinaga, B., Bredesen, D. E., & Rao, R. V. (2008). Coupling endoplasmic reticulum stress to the cell death program in mouse melanoma cells: Effect of curcumin. Apoptosis, 13, 904-914. doi:10.1007/s10495-008-0221-x.
5. Bauer, J. H., Goupil, S., Garber, G. B., & Helfand, S. L. (2004). An accelerated assay for the identification of lifespan-extending interventions in Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 101, 12980-12985. doi:10.1073/pnas.0403493101.
6. Blanchet, J., Longpre, F., Bureau, G., Morissette, M., Dipaolo, T., Bronchti, G., et al. (2008). Resveratrol, a red wine polyphenol, protects dopaminergic neurons in MPTP-treated mice. Progress in Neuro- Psychopharmacology & Biological Psychiatry, 32, 1243-1250. doi:10.1016/j.pnpbp. 2008.03.024.
7. Boocock, D. J., Faust, G. E., Patel, K. R., Schinas, A. M., Brown, V. A., Ducharme, M. P., et al. (2007). Phase I dose escalation pharmacokinetic study in healthy volunteers of resveratrol, a potential cancer chemopreventive agent. Cancer Epidemiology, Biomarkers & Prevention, 16, 1246-1252. doi:10.1158/1055-9965. EPI-07-0022.
8. Boyce, M., Bryant, K. F., Jousse, C., Long, K., Harding, H. P., Scheuner, D., et al. (2005). A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science, 307, 935-939. doi:10.1126/science.1101902.
9. Bredesen, D. E., Rao, R. V., & Mehlen, P. (2006). Cell death in the nervous system. Nature, 443, 796-802. doi:10.1038/nature05293.
10. Bureau, G., Longpre, F., & Martinoli, M. G. (2008). Resveratrol and quercetin, two natural polyphenols, reduce apoptotic neuronal cell death induced by neuroinflammation. Journal of Neuroscience Research, 86, 403-410. doi:10.1002/jnr.21503.
11. Bush, K. T., Goldberg, A. L., & Nigam, S. K. (1997). Proteasome inhibition leads to a heat-shock response, induction of endoplasmic reticulum chaperones, and thermotolerance. The Journal of Biological Chemistry, 272, 9086-9092. doi:10.1074/jbc.272.14.9086.
12. Calabrese, V., Cornelius, C, Mancuso, C, Pennisi, G., Calafato, S., Bellia, F., et al. (2008). Cellular stress response: a novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochemical Research, 33 (12), 2444-2471.
13. Caserta, T. M., Smith, A. N., Gultice, A. D., Reedy, M. A., & Brown, T. L. (2003). Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis, 8, 345-352.
14. Chao, J., Yu, M. S., Ho, Y. S., Wang, M., & Chang, R. C. (2008). Dietary oxyresveratrol prevents parkinsonian mimetic 6-hydroxydopamine neurotoxicity. Free Radical Biology & Medicine, 45, 1019-1026. doi:10.1016/j.freeradbiomed.2008.07.002.
15. Chinta, S. J., & Andersen, J. K. (2006). Reversible inhibition of mitochondrial complex I activity following chronic dopaminergic glutathione depletion in vitro: Implications for Parkinson's disease. Free Radical Biology & Medicine, 41, 1442-1448. doi:10.1016/j.freeradbiomed.2006.08. 002.
16. Chinta, S. J., Rane, A., Poksay, K. S., Bredesen, D. E., Andersen, J. K., & Rao, R. V. (2008). Coupling endoplasmic reticulum stress to the cell death program in dopaminergic cells: effect of paraquat. Neuromolecular Medicine, Epub ahead of print
17. Clarkson, E. D., Rosa, F. G, Edwards-Prasad, J., Weiland, D. A., Witta, S. E., Freed, C. R., et al. (1998). Improvement of neurological deficits in 6-hydroxydopamine-lesioned rats after transplantation with allogeneic simian virus 40 large tumor antigen gene-induced immortalized dopamine cells. Proceedings of the National Academy of Sciences of the United States of America, 95, 1265-1270.
18. Crowell, J. A., Korytko, P. J., Morrissey, R. L., Booth, T. D., & Levine, B. S. (2004). Resveratrol-associated renal toxicity. Toxicological Sciences, 82, 614-619. doi:10.1093/toxsci/kfh263.
19. de Almeida, L. M., Leite, M. C, Thomazi, A. P., Battu, C, Nardin, P., Tortorelli, L. S., et al. (2008). Resveratrol protects against oxidative injury induced by H (2) O (2) in acute hippocampal slice preparations from Wistar rats. Archives of Biochemistry and Biophysics, 480 (1), 27-32.
20. de la Lastra, C. A., & Villegas, I. (2005). Resveratrol as an antiinflammatory and anti-aging agent: Mechanisms and clinical implications. Molecular Nutrition & Food Research, 49, 405-430.
21. Duarte, J., Andriambeloson, E., Diebolt, M., & Andriantsitohaina, R. (2004). Wine polyphenols stimulate superoxide anion production to promote calcium signaling and endothelial-dependent vasodilatation. Physiological Research, 53, 595-602.
22. Dursun, B., He, Z., Somerset, H, Oh, D. J., Faubel, S., & Edelstein, C. L. (2006). Caspases and calpain are independent mediators of cisplatin-induced endothelial cell necrosis. American Journal of Physiology. Renal Physiology, 291, F578-F587. doi:10.1152/ajprenal.00455.2005.
23. Egger, L., Madden, D. T., Rheme, C, Rao, R. V., & Bredesen, D. E. (2007). Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death and Differentiation, 14, 1172-1180. doi:10.1038/sj.cdd.4402125.
24. Ellerby, H. M., Martin, S. J., Ellerby, L. M., Naiem, S. S., Rabizadeh, S., Salvesen, G. S., et al. (1997). Establishment of a cell-free system of neuronal apoptosis: Comparison of premitochondrial, mitochondrial, and postmitochondrial phases. The Journal of Neuroscience, 17, 6165-6178.
25. Forman, M. S., Lee, V. M., & Trojanowski, J. Q. (2003). 'Unfolding' pathways in neurodegenerative disease. Trends in Neurosciences, 26, 407-410. doi:10.1016/S0166-2236 (03) 00197-8.
26. Fribley, A., & Wang, C. Y. (2006). Proteasome inhibitor induces apoptosis through induction of endoplasmic reticulum stress. Cancer Biology & Therapy, 5, 745-748.
27. Harding, H. P., Calfon, M., Urano, F., Novoa, I., & Ron, D. (2002). Transcriptional and translational control in the Mammalian unfolded protein response. Annual Review of Cell and Developmental Biology, 18, 575-599. doi:10.1146/annurev. cellbio.18.011402.160624.
28. Holtz, W. A., & O'Malley, K. L. (2003). Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. The Journal of Biological Chemistry, 278, 19367-19377. doi:10.1074/jbc. M211821200.
29. Howitz, K. T., Bitterman, K. J., Cohen, H. Y., Lamming, D. W., Lavu, S., Wood, J. G., et al. (2003). Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature, 425, 191-196. doi:10.1038/nature01960.
30. Hwang, J. T., Kwon, D. Y., Park, O. J., & Kim, M. S. (2008). Resveratrol protects ROS-induced cell death by activating AMPK in H9c2 cardiac muscle cells. Genes and Nutrition, 2, 323-326. doi:10.1007/s12263-007- 0069-7.
31. Ishii, Y., Waxman, S., & Germain, D. (2007). Targeting the ubiquitinproteasome pathway in cancer therapy. Anti-cancer Agents in Medicinal Chemistry, 7, 359-365. doi:10.2174/18715200 7780618180.
32. Jin, F., Wu, Q., Lu, Y. F., Gong, Q. H., & Shi, J. S. (2008). Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson's disease in rats. European Journal of Pharmacology, 600 (1-3), 78-82.
33. Juan, M. E., Vinardell, M. P., & Planas, J. M. (2002). The daily oral administration of high doses of trans-resveratrol to rats for 28 days is not harmful. The Journal of Nutrition, 132, 257-260.
34. Kaufman, R. J. (1999). Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes & Development, 13, 1211-1233. doi:10.1101/gad.13.10.1211.
35. Kitamura, Y., Inden, M., Miyamura, A., Kakimura, J., Taniguchi, T., & Shimohama, S. (2002). Possible involvement of both mitochondria-and endoplasmic reticulum-dependent caspase pathways in rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Neuroscience Letters, 333, 25-28. doi:10.1016/S0304-3940 (02) 00964-3.
36. Kopito, R. R. (2000). Aggresomes, inclusion bodies and protein aggregation. Trends in Cell Biology, 10, 524-530. doi:10.1016/S0962-8924 (00) 01852-3.
37. Liu, H., Bowes 3rd, R. C., van de Water, B., Sillence, C., Nagelkerke, J. F., & Stevens, J. L. (1997). Endoplasmic reticulum chaperones GRP78 and calreticulin prevent oxidative stress, Ca2+ disturbances, and cell death in renal epithelial cells. The Journal of Biological Chemistry, 272, 21751-21759. doi:10.1074/jbc.272.35.21751.
38. Liu, H., Miller, E., van de Water, B., & Stevens, J. L. (1998). Endoplasmic reticulum stress proteins block oxidant-induced Ca2 + increases and cell death. The Journal of Biological Chemistry, 273, 12858-12862. doi:10.1074/jbc.273.21.12858.
39. Lu, K. T., Ko, M. C., Chen, B. Y., Huang, J. C., Hsieh, C. W., Lee, M. C., et al. (2008). Neuroprotective effects of resveratrol on MPTP-induced neuron loss mediated by free radical scavenging. Journal of Agricultural and Food Chemistry, 56, 6910-6913. doi:10.1021/jf8007212.
40. Ma, Y., & Hendershot, L. M. (2002). The mammalian endoplasmic reticulum as a sensor for cellular stress. Cell Stress & Chaperones, 7, 222-229. doi:10.1379/1466-1268 (2002) 007<0222:TMERAA>2.0.CO;2.
41. Mattson, M. P. (2006). Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders. Antioxidants & Redox Signalling, 8, 1997-2006. doi:10.1089/ars.2006.8.1997.
42. Nakamura, T., & Lipton, S. A. (2008). Emerging roles of S-nitrosylation in protein misfolding and neurodegenerative diseases. Antioxidants & Redox Signalling, 10, 87-101. doi:10.1089/ars.2007. 1858.
43. Okawara, M., Katsuki, H., Kurimoto, E., Shibata, H., Kume, T., & Akaike, A. (2007). Resveratrol protects dopaminergic neurons in midbrain slice culture from multiple insults. Biochemical Pharmacology, 73, 550-560. doi:10.1016/j.bcp. 2006.11.003.
44. Pallas, M., Verdaguer, E., Tajes, M., Gutierrez-Cuesta, J., & Camins, A. (2008). Modulation of sirtuins: New targets for antiageing. Recent Patents CNS Drug Discov, 3, 61-69.
45. Paschen, W., & Frandsen, A. (2001). Endoplasmic reticulum dysfunction-a common denominator for cell injury in acute and degenerative diseases of the brain? Journal of Neurochemistry, 79, 719-725. doi:10.1046/j.1471-4159.2001.00623.x.
46. Rajagopalan, S., & Andersen, J. K. (2001). Alpha synuclein aggregation: Is it the toxic gain of function responsible for neurodegeneration in Parkinson's disease? Mechanisms of Ageing and Development, 122, 1499-1510. doi:10.1016/S0047-6374 (01) 00283-4.
47. Rao, R. V., & Bredesen, D. E. (2004). Misfolded proteins, endoplasmic reticulum stress and neurodegeneration. Current Opinion in Cell Biology, 16, 653-662. doi:10.1016/j. ceb.2004.09.012.
48. Rao, R. V., Hermel, E., Castro-Obregon, S., del Rio, G., Ellerby, L. M., Ellerby, H. M., et al. (2001). Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. The Journal of Biological Chemistry, 276, 33869-33874. doi:10.1074/jbc. M102225200.
49. Rao, R. V., Castro-Obregon, S., Frankowski, H., Schuler, M., Stoka, V., Del Rio, G., et al. (2002a). Coupling Endoplasmic Reticulum Stress to the Cell Death Program. AN Apaf-1-INDEPENDENT INTRINSIC PATHWAY. The Journal of Biological Chemistry, 277, 21836-21842. doi:10.1074/jbc. M202726200.
50. Rao, R. V., Peel, A., Logvinova, A., del Rio, G., Hermel, E., Yokota, T., et al. (2002b). Coupling endoplasmic reticulum stress to the cell death program: Role of the ER chaperone GRP78. FEBS Letters, 514, 122-128.
51. Rao, R. V., Ellerby, H. M., & Bredesen, D. E. (2004a). Coupling endoplasmic reticulum stress to the cell death program. Cell Death and Differentiation, 11, 372-380. doi:10.1038/sj. cdd.4401378.
52. Rao, R. V., Poksay, K. S., Castro-Obregon, S., Schilling, B., Row, R. H., Del Rio, G., et al. (2004b). Molecular components of a cell death pathway activated by endoplasmic reticulum stress. The Journal of Biological Chemistry, 279, 177-187. doi:10.1074/jbc. M304490200.
53. Rao, R. V., Niazi, K., Mollahan, P., Mao, X., Crippen, D., Poksay, K. S., et al. (2006). Coupling endoplasmic reticulum stress to the cell-death program: A novel HSP90-independent role for the small chaperone protein p23. Cell Death and Differentiation, 13, 415-425. doi:10.1038/sj.cdd.4401761.
54. Reijonen, S., Putkonen, N., Norremolle, A., Lindholm, D., & Korhonen, L. (2008). Inhibition of endoplasmic reticulum stress counteracts neuronal cell death and protein aggregation caused by N-terminal mutant huntingtin proteins. Experimental Cell Research, 314, 950-960. doi:10.1016/j.yexcr.2007.12. 025.
55. Riedl, S. J., & Salvesen, G. S. (2007). The apoptosome: Signalling platform of cell death. Nature Reviews. Molecular Cell Biology, 8, 405-413. doi:10.1038/nrm2153.
56. Rocha-Gonzalez, H. I., Ambriz-Tututi, M., & Granados-Soto, V. (2008). Resveratrol: A natural compound with pharmacological potential in neurodegenerative diseases. CNS Neurosci Ther, 14, 234-247. doi:10.1111/j.1755-5949.2008.00045.x.
57. Ron, D. (2002). Translational control in the endoplasmic reticulum stress response. The Journal of Clinical Investigation, 110, 1383-1388.
58. Rubiolo, J. A., Mithieux, G., & Vega, F. V. (2008). Resveratrol protects primary rat hepatocytes against oxidative stress damage: Activation of the Nrf2 transcription factor and augmented activities of antioxidant enzymes. European Journal of Pharmacology, 591, 66-72. doi:10.1016/j.ejphar.2008. 06.067.
59. Rutkowski, D. T., & Kaufman, R. J. (2004). A trip to the ER: Coping with stress. Trends in Cell Biology, 14, 20-28. doi:10.1016/j. tcb.2003.11.001.
60. Ryu, E. J., Harding, H. P., Angelastro, J. M., Vitolo, O. V., Ron, D., & Greene, L. A. (2002). Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. The Journal of Neuroscience, 22, 10690-10698.
61. Sitia, R., & Braakman, I. (2003). Quality control in the endoplasmic reticulum protein factory. Nature, 426, 891-894. doi:10.1038/nature02262.
62. Smith, W. W., Jiang, H., Pei, Z., Tanaka, Y., Morita, H., Sawa, A., et al. (2005). Endoplasmic reticulum stress and mitochondrial cell death pathways mediate A53T mutant alpha-synuclein-induced toxicity. Human Molecular Genetics, 14, 3801-3811. doi:10.1093/hmg/ddi396.
63. Sokka, A. L., Putkonen, N., Mudo, G., Pryazhnikov, E., Reijonen, S., Khiroug, L., et al. (2007). Endoplasmic reticulum stress inhibition protects against excitotoxic neuronal injury in the rat brain. The Journal of Neuroscience, 27, 901-908. doi:10.1523/JNEUROSCI.4289-06.2007.
64. Takahashi, R., Imai, Y., Hattori, N., & Mizuno, Y. (2003). Parkin and endoplasmic reticulum stress. Annals of the New York Academy of Sciences, 991, 101-106.
65. Uehara, T., Nakamura, T., Yao, D., Shi, Z. Q., Gu, Z., Ma, Y., et al. (2006). S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature, 441, 513-517. doi:10.1038/nature04782.
66. Walle, T., Hsieh, F., DeLegge, M. H., Oatis Jr, J. E., & Walle, U. K. (2004). High absorption but very low bioavailability of oral resveratrol in humans. Drug Metabolism and Disposition: The Biological Fate of Chemicals, 32, 1377-1382. doi:10.1124/dmd.104.000885.
67. Welihinda, A. A., Tirasophon, W., & Kaufman, R. J. (1999). The cellular response to protein misfolding in the endoplasmic reticulum. Gene Expression, 7, 293-300.
68. Wenzel, E., & Somoza, V. (2005). Metabolism and bioavailability of trans-resveratrol. Molecular Nutrition & Food Research, 49, 472-481. doi:10.1002/mnfr.200500010.
69. Wood, J. G., Rogina, B., Lavu, S., Howitz, K., Helfand, S. L., Tatar, M., et al. (2004). Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature, 430, 686-689. doi:10.1038/nature02789.
70. Yang, L., Sugama, S., Mischak, R. P., Kiaei, M., Bizat, N., Brouillet, E., et al. (2004). A novel systemically active caspase inhibitor attenuates the toxicities of MPTP, malonate, and 3NP in vivo. Neurobiology of Disease, 17, 250-259. doi:10.1016/j.nbd.2004.07.021.
71. Yu, Z., Luo, H., Fu, W., & Mattson, M. P. (1999). The endoplasmic reticulum stress-responsive protein GRP78 protects neurons against excitotoxicity and apoptosis: Suppression of oxidative stress and stabilization of calcium homeostasis. Experimental Neurology, 155, 302-314. doi:10.1006/exnr.1998.7002.
72. Zhou, W., Hurlbert, M. S., Schaack, J., Prasad, K. N., & Freed, C. R. (2000). Overexpression of human alpha-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalon-derived cells. Brain Research, 866, 33-43. doi:10.1016/S0006-8993 (00) 02215-0.