Experimental and Molecular Medicine

Korean Society for Biochemistry and Molecular Biongy (생화학분자생물학회)
권호 표지

Resveratrol protects SH-SY5Y neuroblastoma cells from apoptosis induced by dopamine

Lee, Mi-Kyung;Kang, Soon-Ja;Poncz, Mortimer;Song, Ki-Joon;Park, Kwang-Sook

  • Published : 20070600
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Abstract

Dopamine (DA) is an oxidant that may contribute to the degeneration of dopaminergic neurons. The present study demonstrates that DA-induced cytotoxicity in human-derived neurotypic cells, SH-SY5Y, is prevented by resveratrol, one of the major antioxidative constituents found in the skin of grapes. SH-SY5Y cells, a neuroblastoma cell line, treated with DA at 300 and 500 M for 24 h underwent apoptotic death as determined by characteristic morphological features, including nuclear conden-sation, and loss of mitochondrial membrane poten-tial (MMP). Flow cytometric analysis using Annexin V showed that DA can induce significant and severe apoptosis. Exposure to resveratrol (5 M) for 1 h prior to the DA treatment attenuated DA-induced cyto-toxicity, and rescued the loss of MMP. To investigate the apoptotic signaling pathways relevant to the restoration of DA-induced apoptosis by resveratrol, we carried out quantitative analysis of Bcl-2, cas-pase-3, and cleaved poly ADP-ribose polymerase (PARP) by immunoblot analysis. Resveratrol pre-treatment led to a decrease in cleavage of PARP, an increase in the Bcl-2 protein, and activation of cas-pase-3. These results suggest that DA may be a potential oxidant of neuronal cells at biologically relevant concentrations. Resveratrol may protect SH-SY5Y cells against this cytotoxicity, reducing intracellular oxidative stress through canonical signal pathways of apoptosis and may be of bio-logical importance in the prevention of a dopami-nergic neurodegenerative disorder such as Parkin-son disease.

Keywords

References

  1. Akao M, O'Rourke B, Teshima Y, Seharaseyon J, Marba'n E. Mechanistically distinct steps in the mitochondrial death pathway triggered by oxidative stress in cardiac myocytes. Circ Res 2003;92:186-94 https://doi.org/10.1161/01.RES.0000051861.21316.E9
  2. Bastianetto S, Zheng WH, Quirion R. Neuroprotective abilities of resveratrol and other red wine constituents against nitric oxide-related toxicity in cultured hippocampal neurons. Br J Pharmacol 2000;131:711-20 https://doi.org/10.1038/sj.bjp.0703626
  3. Borg J, London J. Copper/zinc superoxide dismutase overexpression promotes survival of cortical neurons exposed to neurotoxins in vitro. J Neurosci Res 2002;70:180-9 https://doi.org/10.1002/jnr.10404
  4. Cohen G, Heikkila RE. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem 1974;249:2447-52
  5. Crompton M. Bax, Bid and the permeabilization of the mitochondrial outer membrane in apoptosis. Curr Opin Cell Biol 2000;12:414-9 https://doi.org/10.1016/S0955-0674(00)00110-1
  6. Emdadul Haque M, Asanuma M, Higashi Y, Migazaki I, Tanaka K, Ogawa N. Apoptosis-inducing neurotoxicity of dopamine and its metabolites via reactive quinone generation in neuroblastoma cells. Biochim Biophys Acta 2003;1619:39-52 https://doi.org/10.1016/S0304-4165(02)00440-3
  7. Graham DG. Oxidative pathways for catecholamines in the genesis of neuromelanin and cytotoxic quinones. Mol Pharmacol 1978;14:633-43
  8. Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem 1992;59:1609-23 https://doi.org/10.1111/j.1471-4159.1992.tb10990.x
  9. Hanrott K, Gudmunsen L, O'Neill MJ, Wonnacott S. 6-hydroxydopamine-induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cdelta. J Biol Chem 2006;281:5373-82 https://doi.org/10.1074/jbc.M511560200
  10. Hastings TG. Enzymatic oxidation of dopamine: the role of prostaglandin H synthase. J Neurochem 1995;64:919-24 https://doi.org/10.1046/j.1471-4159.1995.64020919.x
  11. Howard S, Bottino C, Brooke S, Cheng E, Giffard RG, Sapolsky R. Neuroprotective effects of bcl-2 overexpression in hippocampal cultures: interactions with pathways of oxidative damage. J Neurochem 2002;83:914-23 https://doi.org/10.1046/j.1471-4159.2002.01198.x
  12. Hwang SG, Lee HC, Lee DW, Kim YS, Joo WH, Cho YK, Moon JY. Induction of apoptotic cell death by a p53-independent pathway in neuronal SK-N-MC cells after treatment with 2,20,5,50-tetrachlorobiphenyl. Toxicology 2001;165:179-88 https://doi.org/10.1016/S0300-483X(01)00432-2
  13. Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 1997;275:218-20 https://doi.org/10.1126/science.275.5297.218
  14. Jang YH, Lee YC, Park NH, Shin HY, Mun KC, Choi MS, Lee MY, Kim AR, Kim JM, Lee SR, Park HR. Polyphenol (-)-epigallocatechin gallate protection from ischemia/reperfusion-induced renal injury in normotensive and hypertensive rats. Transplant Proc 2006;38:2190-4 https://doi.org/10.1016/j.transproceed.2006.06.101
  15. Jellinger K, Kienzl E, Rumpelmair G, Riederer P, Stachelberger H, Ben-Shachar D, Youdim MB. Neuromelanin and nigrostriatal dopamine neuron degeneration. J Neurochem 1993;59:1168-71 https://doi.org/10.1111/j.1471-4159.1992.tb08362.x
  16. Jiang H, Zhang L, Kuo J, Kuo K, Gautam SC, Groc L, Rodriguez AI, Koubi D, Hunter TJ, Corcoran GB, Seidman MD, Levine RA. Resveratrol-induced apoptotic death in human U251 glioma cells. Mol Cancer Ther 2005;4:554-61 https://doi.org/10.1158/1535-7163.MCT-04-0056
  17. Junn E, Mouradian MM. Apoptotic signaling in dopamine-induced cell death: the role of oxidative stress, p38 mitogen-activated protein kinase, cytochrome c and caspases. J Neurochem 2001;78:374-83 https://doi.org/10.1046/j.1471-4159.2001.00425.x
  18. Kim JE, Oh JH, Choi WS, Chang II, Sohn S, Krajewski S, Reed JC, O'Malley KL, Oh YJ. Sequential cleavage of poly(ADP-ribose) polymerase and appearance of a small Bax-immunoreactive protein are blocked by Bcl-X(L) and caspase inhibitors during staurosporine induced dopaminergic neuronal apoptosis. J Neurochem 1999;72:2456-63 https://doi.org/10.1046/j.1471-4159.1999.0722456.x
  19. Lai CT, Yu PH. Dopamine- and L-beta-3,4-dihydroxyphenylalamine hydrochloride (L-Dopa)-induced cytotoxicity towards catecholaminergic neuroblastoma SH-SY5Y cells. Effects of oxidative stress and antioxidative factors. Biochem Pharmacol 1997;53:363-72 https://doi.org/10.1016/S0006-2952(96)00731-9
  20. Luo Y, Umegaki H, Wang X, Abe R, Roth GS. Dopamine induces apoptosis through an oxidation-involved SAPK/JNK activation pathway. J Biol Chem 1998;273:3756-64 https://doi.org/10.1074/jbc.273.6.3756
  21. Marchetti P, Hirsch T, Zamzami N, Castedo M, Decaudin D, Susin SA, Masse B, Kroemer G. Mitochondrial permeability transition triggers lymphocyte apoptosis. J Immunol 1996;157:4830-6
  22. Markus GG. Caspases: key players in programmed cell death. Curr Opin Struct Biol 2000;10:649-55 https://doi.org/10.1016/S0959-440X(00)00146-9
  23. Mohan J, Gandhi AA, Bhavya BC, Rashmi R, Karunagaran D, Indu R, Santhoshkumar TR. Caspase-2 triggers Bax-Bak-dependent and -independent cell death in colon cancer cells treated with resveratrol. J Biol Chem 2006;281:17599-611 https://doi.org/10.1074/jbc.M602641200
  24. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T-T, Yu VL, Miller DK. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995;376:37-43 https://doi.org/10.1038/376037a0
  25. Nicolini G, Rigolio R, Miloso M, Bertelli AAE, Tredici G. Anti-apoptotic effect of trans-resveratrol on paclitaxel-induced apoptosis in the human neuroblastoma SH-SY5Y cell line. Neurosci Lett 2001;302:41-4 https://doi.org/10.1016/S0304-3940(01)01654-8
  26. Offen D, Ziv I, Panet H, Wasserman L, Stein R, Melamed E, Barzilai A. Dopamine-induced apoptosis is inhibited in PC12 cells expressing Bcl-2. Cell Mol Neurobiol 1997;17:289-304 https://doi.org/10.1023/A:1026390201168
  27. Olanow CW. A rationale for monoamine oxidase inhibition as neuroprotective therapy for Parkinson's disease. Mov Disord 1993;8 Suppl 1:S1-7
  28. Perkins CL, Fang G, Kim CN, Bhalla KN. The role of Apaf-1, caspase-9, and bid proteins in etoposide- or paclitaxel-induced mitochondrial events during apoptosis. Cancer Res 2000;60:1645-53
  29. Qiu JH, Asai A, Chi S, Saito N, Hamada H, Kirino T. Proteasome inhibitors induce cytochrome c-caspase-3-like proteasemediated apoptosis in cultured cortical neurons. J Neurosci 2000;20:259-65 https://doi.org/10.1523/JNEUROSCI.20-01-00259.2000
  30. Saito A, Hayashi T, Okuno S, Ferrand-Drake M, Chan PH. Overexpression of copper/zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci 2003;23:1710-8 https://doi.org/10.1523/JNEUROSCI.23-05-01710.2003
  31. Sawada M, Nakashima S, Banno Y, Yamakawa H, Takenaka K, Shinoda J, Nishimura Y, Sakai N, Nozawa Y. Influence of Bax or Bcl-2 overexpression on the ceramide-dependent apoptotic pathway in glioma cells. Oncogene 2000;19:3508-20 https://doi.org/10.1038/sj.onc.1203699
  32. Schulz JB, Weller M, Moskowitz MA. Caspases as treatment targets in stroke and neurodegenerative diseases. Ann Neurol 1999;45:421-9 https://doi.org/10.1002/1531-8249(199904)45:4<421::AID-ANA2>3.0.CO;2-Q
  33. Skrzydlewska E, Augustyniak A, Michalak K, Farbiszewski R. Green tea supplementation in rats of different ages mitigates ethanol-induced changes in brain antioxidant abilities. Alcohol 2005;37:89-98 https://doi.org/10.1016/j.alcohol.2005.12.003
  34. Soleas GJ, Diamandis EP, Goldberg DM. Resveratrol: a molecule whose time has come? And gone? Clin Biochem 1997;30:91-113 https://doi.org/10.1016/S0009-9120(96)00155-5
  35. Stervbo U, Vang O, Bonnesen C. Time- and concentration- dependent effects of Resveratrol in HL-60 and HepG2 cells. Cell Prolif 2006;39:479-93 https://doi.org/10.1111/j.1365-2184.2006.00406.x
  36. Surh YJ. Molecular mechanisms of chemopreventive effects of selected dietary and medicinal phenolic substances. Mutat Res 1999;428:305-27 https://doi.org/10.1016/S1383-5742(99)00057-5
  37. Tang XQ, Zhi JL, Cui YU, Feng JQ, Chen PX. Hydrogen peroxide preconditioning protects PC12 cells against apoptosis induced by dopamine. Life Sci 2005a;78:61-6 https://doi.org/10.1016/j.lfs.2005.04.048
  38. Tang XQ, Feng JQ, Chen J, Chen PX, Zhi JL, Cui Y, Guo RX, Yu HM. Protection of oxidative preconditioning against apoptosis induced by H2O2 in PC 12 cells: mechanisms via MMP, ROS, and Bcl-2. Brain Res 2005b;1057:57-64 https://doi.org/10.1016/j.brainres.2005.07.072
  39. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly (ADP-ribose) polymerase. Cell 1995;81:801-9 https://doi.org/10.1016/0092-8674(95)90541-3
  40. Tsujimoto Y. Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells 1998;3:697-707 https://doi.org/10.1046/j.1365-2443.1998.00223.x
  41. Ulrich S, Wolter F, Stein JM. Molecular mechanisms of the chemopreventive effects of resveratrol and its analogs in carcinogenesis. Mol Nutr Food Res 2005;49:452-61 https://doi.org/10.1002/mnfr.200400081
  42. Verheij M, Bose R, Lin XH, Yao B, Jarvis WD, Grant S, Birrer MJ, Szabo E, Zon LI, Kyriakis JM, Haimovitz-Friedman A, Fuks Z, Kolesnick RN. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 1996;380:75-9 https://doi.org/10.1038/380075a0
  43. Virgili M, Contestabile A. Partial neuroprotection of in vivo excitotoxic brain damage by chronic administration of the red wine antioxidant agent, trans-resveratrol in rats. Neurosci Lett 2000;281:123-6 https://doi.org/10.1016/S0304-3940(00)00820-X
  44. Wang XJ, Xu JX. Salvianic acid A protects human neuroblastoma SH-SY5Y cells against $MPP^-induced$ cytotoxicity. Neurosci Res 2005;51:129-38 https://doi.org/10.1016/j.neures.2004.10.001
  45. Yamakawa H, Ito Y, Naganawa T, Banno Y, Nakashima S, Yoshimura S, Sawada M, Nishimura Y, Nozawa Y, Sakai N. Activation of caspase-9 and -3 during $H_2O_2-induced$ apoptosis of PC12 cells independent of ceramide formation. Neurol Res 2000;22:556-64 https://doi.org/10.1080/01616412.2000.11740718
  46. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 1997;275:1129-32 https://doi.org/10.1126/science.275.5303.1129
  47. Youdim K, Joseph J. A possible emerging role of phytochemicals in improving age-related neurological dysfunctions: a multiplicity of effects. Free Radic Biol Med 2001;30:583-94 https://doi.org/10.1016/S0891-5849(00)00510-4