Role of ROS in the protective effect of silibinin on sodium nitroprusside-induced apoptosis in rat pheochromocytoma PC12 cells

Free Radical Research

Volumn 45, Issue 7, 2011, Pages 835-847

  Liu, Binbin ^a   Yang, Pengfei ^a   Ye, Yuanchao ^a   Zhou, Yan ^a   Li, Lingzhi ^a   Tashiro, Shin Ichi ^b   Onodera, Satoshi ^b   Ikejima, Takashi ^a  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

^b SHOWA PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

apoptosis; autophagy; PC12 cells; ROS; silibinin

Indexed keywords

3 METHYLADENINE; HYDROXYL RADICAL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NITROPRUSSIDE SODIUM; PHOSPHATIDYLINOSITOL 3 KINASE; RAF PROTEIN; RAPAMYCIN; RAS PROTEIN; REACTIVE OXYGEN METABOLITE; SILIBININ;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOSYNTHESIS; CELL PROTECTION; CELL STRAIN; CELL STRUCTURE; CONTROLLED STUDY; DRUG MECHANISM; FEEDBACK SYSTEM; FLOW CYTOMETRY; NEUROPROTECTION; NONHUMAN; PHEOCHROMOCYTOMA CELL; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADENINE; ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLOW CYTOMETRY; MAP KINASE KINASE 1; NF-KAPPA B; NITROPRUSSIDE; ONCOGENE PROTEIN P21(RAS); PC12 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; RAF KINASES; RATS; REACTIVE OXYGEN SPECIES; SILYMARIN; SIROLIMUS;

RATTUS;

EID: 79957905224     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2011.580343     Document Type: Article

References (65)

1. Pradhan SC, Girish C Hepatoprotective herbal drug, sily-marin from experimental pharmacology to clinical medicine. Indian J Med Res 2006;124:491-504. (Pubitemid 46157708)
2. Zhou B, Wu LJ, Li LH, Tashiro S, Onodera S, Uchiumi F, et al. Silibinin protects against Isoproterenol-induced rat cardiac myocyte injury through mitochondrial pathway after up-regulation of SIRT1. J Pharmacol Sci 2006;102:387-395. (Pubitemid 44954598)
3. Wang MJ, Lin WW, Chen HL, Chang YH, Ou HC, Kuo JS, et al. Silymarin protects dopaminergic neurons against lipopolysaccharide-induced neurotoxicity by inhibiting micro-glia activation. Eur J Neurosci 2002;16:2103-2112.
4. Lu P, Mamiya T, Lu LL, Mouri A, Niwa M, Kim H-C, et al. Silibinin attenuates cognitive defi cits and decreases of dopamine and serotonin induced by repeated methampheta-mine treatment. Behav Brain Res 2010;207:387-393.
5. Kidd P, Head K. Review of the bioavailability and clinical Efficacy of milk thistle phytosome: a silybin-phosphatidylcho-line complex (Siliphos). Altern Med Rev 2005;10:193-203. (Pubitemid 41384033)
6. Wu J-W, Lin L-C, Hung S-C, Lin C-H, Chi C-W, Tsai T-H. Hepatobiliary excretion of silibinin in normal and liver cirrhotic rats. Am Soc Pharmacol Exp Ther 2008;36: 589-596. (Pubitemid 351397985)
7. Wang Q, Zou L, Liu W, Hao W, Tashiro S, Onodera S, Inkejima T. Inhibiting NF-?B activation and ROS production are involved in the mechanism of silibinin ' s protection against D-galactose-induced senescence. Pharmacol Biochem Behav 2011;98:140-149.
8. Rui YC, Zhang DZ, Sun DX, Zeng GQ. Effects of silybin on production of oxygen free radical, lipoperoxide and leukot-rienes in brain following ischemia and reperfusion. Zhongguo Yao Li Xue Bao 1990;11:418-421.
9. Westerink RHS, Ewing AG. The PC12 cell as model for neu-rosecretion. Acta Physiol (Oxf) 2008;192:273-285.
10. Liu S, Han Y, Zhang T, Yang Z. Protective effect of trifl uop-erazine on hydrogen peroxide-inducedapoptosis in PC12 cells. Brain Res Bull 2011;84:183-188.
11. +-induced apoptosis in PC12cells by inhibiting the NO pathway. Brain Res 2011; Epub ahead of print.
12. Tan B, Luan Z, Wei X, He Y, Wei G, Johnstone BH, et al. AMPK mediates adipose stem cell-stimulated neuritogenesis of PC12 cells. Neuroscience 2011; Epub ahead of print.
13. Mittar D, Sehajpal PK, Lander HM. Nitric oxide activates Rap1 and Ral in a Ras-independent manner. Biochem Bio-phys Res Commun 2004;322:203-209. (Pubitemid 39099256)
14. Bolanos JP, Almeida A, Stewart V, Peuchen S, Land JM, Clark JB, Heales SJ. Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases. J Neurochem 1997;68:2227-2240. (Pubitemid 27218141)
15. Togo T, Katsuse O, Iseki E. Nitric oxide pathways in Alzheimer's disease and other neurodegenerative dementias. Neurol Res 2004;26:563-600.
16. Kühn K, Lotz M. Mechanisms of sodium nitroprusside-induced death in human chondrocytes. Rheumatol Int 2003; 23: 241-247.
17. Gui J, Song Y, Reena Han N-L, Sheu F-S. Characterization of transcriptional regulation of neurogranin by nitric oxide and the role of neurogranin in SNP-induced cell death: impli-cation of neurogranin in an increased neuronal susceptibility to oxidative stress. Int J Biol Sci 2007;3:212-224. (Pubitemid 46340920)
18. Pytlowany M, Strosznajder JN, Jeśko H, Ca kała M, Stroszna-jder RP. Molecular mechanism of PC12 cell death evoked by sodiumnitroprusside, a nitric oxide donor. Acta Biochim Polonica 2008;55:339-347. (Pubitemid 351947548)
19. Bartosz G. Reactive oxygen species: destroyers or messengers. Biochem Pharmacol 2009;77:1303-1315.
20. Fenton H.J.H. Oxidation of tartaric acid in presence of iron. J Chem Soc Trans 1894;65:899-911.
21. Oravecz K, Bazs ó-Dombi E, Jeney F, Nagy K, Gecse M, Zs.-Nagy I. The involvement of hydroxyl free radicals in differentiation of the PC-12 rat pheochromocytoma cell line. Arch Gerontol Geriatr 2001;33:61-69. (Pubitemid 32666221)
22. Lockshin RA, Zakeri Z. Apoptosis, autophagy, and more. Int J Biochem Cell Biol 2004;36:2405-2419. (Pubitemid 39119755)
23. Levine B. Autophagy and cancer. Nature 2007;446:745-747.
24. Mari ñ o G, L ó pez-Ot í n C Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci 2004;61:1439-1454.
25. Pan T, Rawal P, Wu Y, Xie W, Jankovic J, Le W. Rapamycin protects against rotenone-induced apoptosis through auto-phagy induction. Neuroscience 2009;164:541-551.
26. Wang Y, Singh R, Massey AC, Kane SS, Kaushik S, Grant T et al. Loss of macroautophagy promotes or prevents fi broblast apoptosis depending on the death stimulus. J Biol Chem 2008;283:4766-4777.
27. Choi YT, Jung CH, Lee SR, Bae JH, Baek WK, Suh MH, et al. The green tea polyphenol (-)-epigallocatechin gallate attenuates-amyloid-induced neurotoxicity in cultured hip-pocampal neurons. Life Sci 2001;70:603-614.
28. Nalini K, Rayudu G, Usha G, Jinah C, Henry JF. Role of protein kinase C in basal and hydrogen peroxide-stimulated NF-κB activation in the murine macrophage J774A.1 Cell line. Arch Biochem Biophys 1998;350:206-221.
29. Rizzardini M, Lupi M, Bernasconi S, Mangolini A, Cantoni L. Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid. J Neurol Sci 2003;207:51-58. (Pubitemid 36287103)
30. Rego AC, Vesce S, Nicholls DG. The mechanism of mitochon-drial membrane potential retention following release of cyto-chrome c in apoptotic GT1-7 neural cells. Cell Death Diff 2001;8:995-1003. (Pubitemid 32994650)
31. Pocernich CB, La Fontaine M, Butterfield DA. In-vivo glutathione elevation protects against hydroxyl free radical-induced protein oxidation in rat brain. Neurochem Int 2000;36:185-191. (Pubitemid 30047009)
32. Ross D. Glutathione, free radicals and chemotherapeutic agents. Mechanisms of free-radical induced toxicity and glutathione-dependent protection. Pharmacol Ther 1988;37: 231-249.
33. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T Beclin-phosphati-dylinositol3- kinase complex functions at the trans-Golgi net-work. EMBO Rep 2001;2:330-335. (Pubitemid 32401529)
34. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-5728.
35. Palmer AM. Pharmacotherapy for Alzheimer ' s disease: progress and prospects. Trends Pharmacol Sci 2002;23:426-433. (Pubitemid 35247772)
36. Blennow K, de Leon MJ, Zetterberg H. Alzheimer ' s disease. Lancet 2006;368:387-403.
37. Alkam T, Nitta A, Mzoguchi H, Saito K, Seshima M, Itoh A, et al. Restraining tumor necrosis factor-alpha by thalidomide prevents the Amyloid b-induced impairment of recognition memory in mice. Behav Brain Res 2008;189:100-106.
38. Smith MA, Richey Harris PL, Sayre LM, Beckman JS, Perry G. Widespread peroxynitrite-mediated damage in Alzheimer ' s disease. J Neurosci 1997;17:2653-2657. (Pubitemid 27154998)
39. Lichtenstein MP, Carriba P, Masgrau R, Pujol A, Galea Staging E. Anti-infl ammatory therapy in alzheimer's disease. Front Ageing Neurosci 2010;2:142-142.
40. 25 35 peptide-induced memory impairments: implication of inducible nitric-oxide synthase and tumor necrosis factor-α in mice. JPET 2009;331: 319-326.
41. Hou YC, Liou KT, Chern CM, Wang YH, Liao JF, Chang S, et al. Preventive effect of silymarin in cerebral ischemia-reperfusion-induced brain injury in rats possibly through impairing NF-κB and STAT-1 activation. Phytomedicine 2010;17:963-973.
42. Bannwart CF, Pera ç oli JC, Nakaira-Takahagi E, Pera ç oli MT Inhibitory effect of silibinin on tumour necrosis factor-alpha and hydrogen peroxide production by human monocytes. Nat Prod Res 2010;24:1747-1757.
43. Duan WJ, Li QS, Xia MY, Tashiro S, Onodera S, Ikejima T Silibinin. Activated p53 and induced autophagic death in human fi brosarcoma HT1080 cells via reactive oxygen species-p38 and c-Jun N-Terminal kinase pathways. Biol Pharm Bull 2011;34:47-53.
44. Wang HJ, Wei XF, Jiang YY, Huang H, Yang Y, Fan SM, ET AL. Silibinin induces the generation of nitric oxide in human breast cancer MCF-7 cells. Free Radic Res 2010;44:577-584.
45. Nagy K, Pa ́ sti G, Bene L, Zs.-Nagy I. Induction of granulo-cytic maturation of HL-60 human leukemia cells by free radicals. A hypothesis of cell differentiation involving hydroxyl radicals. Free Rad Res Commun 1993;19:10-15.
46. Nagy K, Pa ́ sti G, Bene L, Zs.-Nagy I. Involvement of Fenton reaction products in differentiation induction of K562 human leukemia cells. Leukemia Res1995;19:203-212.
47. Bishop NA, Liu T, Yankner BA. Neural mechanisms of ageing and cognitive decline. Nature 2010;464125:529-535.
48. Arico S, Petiot A, Bauvy C, Dubbelhuis PF, Meijer AJ, Codogno P, et al. The tumor suppressor PTEN positively regulates macro-autophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J Biol Chem 2001; 276:35243-35246.
49. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-1101. (Pubitemid 40262113)
50. Kondo Y, Kanzawa T, Sawaya R, Kondo S. The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 2005;5:726-734. (Pubitemid 41486365)
51. Lefranc F, Kiss R. Autophagy, the Trojan horse to combat glioblastomas. Neurosurg Focus 2006;20:E7.
52. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005;307:1098-1101. (Pubitemid 40262113)
53. Schmitz KJ, Wohlschlaeger J, Alakus H, Bohr J, Stauder MA, Worm K, et al. Activation of extracellular regulated kinases (ERK1/2) but not AKT predicts poor prognosis in colorectal carcinoma and is associated with k-ras mutations. Virchows Arch 2007;450:151-159. (Pubitemid 46295230)
54. Yamamoto S, Tomita Y, Hoshida Y, Morooka T, Nagano H, Dono K, et al. Prognostic signifi cance of activated Akt expression in pancreatic ductal adenocarcinoma. Clin Cancer Res 2004;10:2846-2850. (Pubitemid 38509164)
55. Settakorn J, Kaewpila N, Burns GF, Leong AS. FAT, Ecadherin, beta catenin, HER 2/neu; Ki67 immuno-expression, and histological grade in intrahepatic cholangiocarcinoma. J Clin Pathol 2005;59:1249-1254. (Pubitemid 41752767)
56. Watanabe S, Itoh T, Arai K JAK2 is essential for acti vation of c-fos and c-myc promoters and cell proliferation through the human granulocyte-macrophage colony-stimulating factor receptor in BA/F3 cells. J Biol Chem 1996;271: 12681-12686. (Pubitemid 26160945)
57. Tian SS, Tapley P, Sincich C, Stein RB, Rosen J, Lamb P. Multiple signaling pathways induced by granulocyte colony-stimulating factor involving activation of JAKs, STAT5, and/or STAT3 are required for regulation of three distinct classes of immediate early genes. Blood 1996;88:4435-4444. (Pubitemid 26419126)
58. Chang F, Lee JT, Navolanic PM, Steelman JG, Blalock WL, Franklin RA, et al. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transfor-mation: a target for cancer chemotherapy. Leukemia 2003;17: 590-603. (Pubitemid 36395654)
59. Chang F, Steelman LS, Shelton JG, Lee JT, Navolanic PN, Blalock WL, et al. Regulation of cell cycle progression and apoptosis by the Ras/Raf/MEK/ERK pathway. Int J Oncol 2003;22:469-480.
60. Chang F, Steelman LS, Lee JT, Shelton JG, Navolanic PM, Blalock WL, et al. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcrip-tion factors: potential targeting for therapeutic intervention. Leukemia 2003;17:1263-1293. (Pubitemid 36857335)
61. Yan J, Roy S, Apolloni A, Lane A, Hancock JF. Ras isoforms vary in their ability to activate Raf-1 and phosphoinositide 3-kinase. J Biol Chem 1998;273:24052-24056. (Pubitemid 28435747)
62. Matallanas D, Arozarena I, Berciano MT, Aaronson DS, Pellicer A, Lafarga M, et al. Differences on the inhibitory specifi cities of HRas, K-Ras and N-Ras (N17) dominant negative mutants are related to their membrane microlocalization. J Biol Chem 2003;278:4572-4581. (Pubitemid 36800954)
63. Pells S, Divjak M, Romanowski P, Impey H, Hawkins NJ, Clarke AR, et al. Developmentally-regulated expression of murine K-ras isoforms. Oncogene 1997;15:781-786.
64. Jiang H, Zhang L, Koubi D, Kuo J, Groc L, Rodriguez AI, et al. Roles of Ras-Erk in apoptosis of PC12 cells induced by trophic factor withdrawal or oxidative stress. J Mol Neurosci 2005;25:133-140. (Pubitemid 41389354)
65. Lee SB, Hong SH, Kim H, Um HD. Co-induction of cell death and survival pathways by phosphoinositide 3-kinase. Life Sci 2005;78:81-91.