Involvement of Hsp70, a stress protein, in the resistance of long-term culture of PC12 cells against sodium nitroprusside (SNP)-induced cell death

Archives of Toxicology

Volumn 84, Issue 9, 2010, Pages 699-708

  Romero, Carmen ^a   Benedí, Juana ^a   Villar, Angel ^a   Martín Aragón, Sagrario ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Hsp70; Long term culture; PC12 cell line; Resistance; Short term culture; Sodium nitroprusside (SNP)

Indexed keywords

CASPASE 3; CATALASE; HEAT SHOCK PROTEIN 70; LACTATE DEHYDROGENASE; MALONALDEHYDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRITE; NITROPRUSSIDE SODIUM;

ARTICLE; CELL CULTURE; CELL DAMAGE; CELL DEATH; CELL LEVEL; CELL STRAIN; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; IC 50; INCUBATION TIME; LONG TERM CULTURE; NEUROTOXICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RELIABILITY; SHORT TERM CULTURE; STANDARDIZATION;

ANIMALS; APOPTOSIS; CASPASE 3; CELL CULTURE TECHNIQUES; CELL DEATH; CELL SURVIVAL; HSP70 HEAT-SHOCK PROTEINS; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; PC12 CELLS; POLY(ADP-RIBOSE) POLYMERASES; RATS;

EID: 77957762387     PISSN: 03405761     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00204-010-0565-1     Document Type: Article

References (46)

1. H Aebi 1984 Catalase in vitro Methods Enzymol 105 121 126 1:CAS:528:DyaL2cXltVKis7s%3D 10.1016/S0076-6879(84)05016-3 6727660
2. K Bellmann M Jaattela D Wissing V Burkart H Kolb 1996 Heat shock protein hsp70 overexpression confers resistance against nitric oxide FEBS Lett 391 185 188 1:CAS:528:DyaK28XkvFWiu7o%3D 10.1016/0014-5793(96)00730-2 8706913 (Pubitemid 26325740)
3. J Benedi R Arroyo C Romero S Martin-Aragon AM Villar 2004 Antioxidant properties and protective effects of a standardized extract of Hypericum perforatum on hydrogen peroxide-induced oxidative damage in PC12 cells Life Sci 75 1263 1276 1:CAS:528:DC%2BD2cXltF2rtLk%3D 10.1016/j.lfs.2004.05.001 15219814 (Pubitemid 38829351)
4. P Bermejo P Gomez-Serranillos J Santos E Pastor P Gil S Martin-Aragon 1997 Determination of malonaldehyde in Alzheimer's disease: a comparative study of high-performance liquid chromatography and thiobarbituric acid test Gerontology 43 218 222 1:CAS:528:DyaK2sXktlGmsLs%3D 10.1159/000213853 9222750
5. S Cardaci G Filomeni G Rotilio MR Ciriolo 2008 Reactive oxygen species mediate p53 activation and apoptosis induced by sodium nitroprusside in SH-SY5Y cells Mol Pharmacol 74 1234 1245 1:CAS:528:DC%2BD1cXhtlCntrbF 10.1124/mol.108.048975 18676676
6. DN Dixon RA Loxley A Barron S Cleary JK Phillips 2005 Comparative studies of PC12 and mouse pheochromocytoma-derived rodent cell lines as models for the study of neuroendocrine systems In Vitro Cell Dev Biol Anim 41 197 206 1:CAS:528:DC%2BD2MXhtF2qu7%2FN 10.1290/0411077.1 16223334 (Pubitemid 41504523)
7. B Eftekharzadeh F Khodagholi A Abdia N Maghsoudia 2010 Alginate protects NT2 neurons against H2O2-induced neurotoxicity Carbohydr Polym 79 1063 1072 1:CAS:528:DC%2BC3cXnvFWqsA%3D%3D 10.1016/j.carbpol.2009.10.040
8. S Fiorucci L Santucci B Federici E Antonelli E Distrutti O Morelli 1999 Nitric oxide-releasing NSAIDs inhibit interleukin-1beta converting enzyme-like cysteine proteases and protect endothelial cells from apoptosis induced by TNFalpha Aliment Pharmacol Ther 13 421 435 1:CAS:528:DyaK1MXisFOgsr4%3D 10.1046/j.1365-2036.1999.00442.x 10102977 (Pubitemid 29142053)
9. J Fonager R Beedholm BF Clark SI Rattan 2002 Mild stress-induced stimulation of heat-shock protein synthesis and improved functional ability of human fibroblasts undergoing aging in vitro Exp Gerontol 37 1223 1228 1:CAS:528:DC%2BD38XptFeku7g%3D 10.1016/S0531-5565(02)00128-6 12470835 (Pubitemid 35418280)
10. CH Fu S Martin-Aragon KI Weinberg VC Ardi PV Danenberg VI Avramis 2001 Reversal of cytosine arabinoside (ara-C) resistance by the synergistic combination of 6-thioguanine plus ara-C plus PEG-asparaginase (TGAP) in human leukemia lines lacking or expressing p53 protein Cancer Chemother Pharmacol 48 123 133 1:CAS:528:DC%2BD3MXltlyqtLk%3D 10.1007/s002800100289 11561778 (Pubitemid 32710223)
11. AM Gorman B Heavey E Creagh TG Cotter A Samali 1999 Antioxidant-mediated inhibition of the heat shock response leads to apoptosis FEBS Lett 445 98 102 1:CAS:528:DyaK1MXht1Ogsr4%3D 10.1016/S0014-5793(99)00094-0 10069381 (Pubitemid 29101542)
12. CE Hanzel SV Verstraeten 2009 Tl(I) and Tl(III) activate both mitochondrial and extrinsic pathways of apoptosis in rat pheochromocytoma (PC12) cells Toxicol Appl Pharmacol 236 59 70 1:CAS:528:DC%2BD1MXjtFKqtLo%3D 10.1016/j.taap.2008.12.029 19371624
13. HJ Heo HY Cho B Hong HK Kim TR Heo EK Kim 2002 Ursolic acid of Origanum majorana L. reduces Abeta-induced oxidative injury Mol Cells 13 5 11 1:CAS:528:DC%2BD38XitFSlurk%3D 11911474
14. HD Hill JG Straka 1988 Protein determination using bicinchoninic acid in the presence of sulfhydryl reagents Anal Biochem 170 1 203 208 1:CAS:528:DyaL1cXhs1Churs%3D 10.1016/0003-2697(88)90109-1 3389511
15. DG Hom D Jiang EJ Hong JQ Mo JK Andersen 1997 Elevated expression of glutathione peroxidase in PC12 cells results in protection against methamphetamine but not MPTP toxicity Brain Res Mol 46 154 160 1:CAS:528:DyaK2sXislems7o%3D 10.1016/S0169-328X(96)00296-3 (Pubitemid 27214366)
16. D Imahashi 1968 Quantitation of LDH isoenzymes by the fluorimetric and colorimetric methods Can J Med Technol 30 235 248 1:CAS:528:DyaF1MXmsVGgtw%3D%3D 5727167
17. JY Jung CR Han YJ Jeong HJ Kim HS Lim KH Lee 2007 Epigallocatechin gallate inhibits nitric oxide-induced apoptosis in rat PC12 cells Neurosci Lett 411 222 227 1:CAS:528:DC%2BD28Xht1KgurjN 10.1016/j.neulet.2006.09.089 17116366 (Pubitemid 44828279)
18. YJ Kang MD Enger 1990 Cadmium cytotoxicity correlates with the changes in glutathione content that occur during the logarithmic growth phase of A549-T27 cells Toxicol Lett 51 23 28 1:CAS:528:DyaK3cXitFaitr0%3D 10.1016/0378-4274(90) 90220-G 2315955
19. IP Khomenko LY Bakhtina OM Zelenina SV Kruglov EB Manukhina LA Bayda 2007 Role of heat shock proteins HSP70 and HSP32 in the protective effect of adaptation of cultured HT22 hippocampal cells to oxidative stress Bull Exp Biol Med 144 174 177 1:CAS:528:DC%2BD2sXhtlyqsrzL 10.1007/s10517-007-0282-9 18399273 (Pubitemid 350238521)
20. CP LeBel H Ischiropoulos SC Bondy 1992 Evaluation of the probe 2', 7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress Chem Res Toxicol 5 227 231 1:CAS:528:DyaK38XhsVGmtr8%3D 10.1021/tx00026a012 1322737
21. JY Lee YJ Kim TY Kim JY Koh YH Kim 2008 Essential role for zinc-triggered p75NTR activation in preconditioning neuroprotection J Neurosci 28 10919 10927 10.1523/JNEUROSCI.3421-08.2008 18945899
22. F Majlessipour R Kwock S Martin-Aragon KI Weinberg VI Avramis 2001 Development of a double-drug-resistant human leukemia model to cytosine arabinoside and L-asparaginase: evaluation of cross-resistance to other treatment modalities Anticancer Res 21 11 22 1:CAS:528:DC%2BD3MXivFCnurw%3D 11299723
23. S Marklund G Marklund 1974 Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase Eur J Biochem 47 469 474 1:CAS:528:DyaE2MXhtlGm 10.1111/j.1432-1033.1974. tb03714.x 4215654
24. S Martin-Aragon JM Benedi AM Villar 1997 Effects of fraxetin on glutathione redox status Z Naturforsch C 52 55 59 1:CAS:528:DyaK2sXitVemsLc%3D 9162171
25. S Martin-Aragon JM Benedi AM Villar 1997 Modifications on antioxidant capacity and lipid peroxidation in mice under fraxetin treatment J Pharm Pharmacol 49 49 52 1:CAS:528:DyaK2sXhtVygs74%3D 9120770
26. S Martin-Aragon JM Benedi AM Villar 1998 Effects of the antioxidant (6, 7-dihydroxycoumarin) esculetin on the glutathione system and lipid peroxidation in mice Gerontology 44 21 25 1:CAS:528:DyaK2sXotFamtbc%3D 10.1159/000021978 9436011
27. S Martin-Aragon SK Mukherjee BJ Taylor SP Ivy CH Fu VC Ardi 2000 Cytosine arabinoside (ara-C) resistance confers cross-resistance or collateral sensitivity to other classes of anti-leukemic drugs Anticancer Res 20 139 150 1:CAS:528:DC%2BD3cXisl2nsL4%3D 10769646
28. S Martin-Aragon B de las Heras MI Sanchez-Reus J Benedi 2001 Pharmacological modification of endogenous antioxidant enzymes by ursolic acid on tetrachloride-induced liver damage in rats and primary cultures of rat hepatocytes Exp Toxicol Pathol 53 199 206 1:CAS:528:DC%2BD3MXmt1antLg%3D 10.1078/0940-2993-00185 11484840
29. KM Miranda MG Espey DA Wink 2001 A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite Nitric Oxide 5 62 71 1:CAS:528:DC%2BD3MXhtFemsrs%3D 10.1006/niox.2000.0319 11178938 (Pubitemid 34146173)
30. MF Molina-Jimenez MI Sanchez-Reus J Benedi 2003 Effect of fraxetin and myricetin on rotenone-induced cytotoxicity in SH-SY5Y cells: comparison with N-acetylcysteine Eur J Pharmacol 472 81 87 1:CAS:528:DC%2BD3sXlsVams78%3D 10.1016/S0014-2999(03)01902-2 12860476 (Pubitemid 36830994)
31. MF Molina-Jimenez MI Sanchez-Reus D Andres M Cascales J Benedi 2004 Neuroprotective effect of fraxetin and myricetin against rotenone-induced apoptosis in neuroblastoma cells Brain Res 1009 9 16 1:CAS:528: DC%2BD2cXjs1Wlsb8%3D 10.1016/j.brainres.2004.02.065 15120578 (Pubitemid 38553843)
32. MF Molina-Jimenez MI Sanchez-Reus M Cascales D Andres J Benedi 2005 Effect of fraxetin on antioxidant defense and stress proteins in human neuroblastoma cell model of rotenone neurotoxicity. Comparative study with myricetin and N-acetylcysteine Toxicol Appl Pharmacol 209 214 225 1:CAS:528:DC%2BD2MXht1OlsrnO 10.1016/j.taap.2005.04.009 15904944 (Pubitemid 41713946)
33. T Mosmann 1983 Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J Immunol Methods 65 55 63 1:STN:280:DyaL2c%2FovFSmtw%3D%3D 10.1016/0022-1759(83)90303-4 6606682
34. DD Mosser AW Caron L Bourget C Denis-Larose B Massie 1997 Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis Mol Cell Biol 17 5317 5327 1:CAS:528:DyaK2sXlslartL8%3D 9271409
35. DE Paglia WN Valentine 1967 Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase J Lab Clin Med 70 158 169 1:CAS:528:DyaF2sXks1Wjur8%3D 6066618
36. E Papp G Nardai C Soti P Csermely 2003 Molecular chaperones, stress proteins and redox homeostasis Biofactors 17 249 257 1:CAS:528: DC%2BD3sXlsl2rtLs%3D 10.1002/biof.5520170124 12897446
37. DJ Quigney AM Gorman A Samali 2003 Heat shock protects PC12 cells against MPP + toxicity Brain Res 993 133 139 1:CAS:528:DC%2BD3sXpt1eltL0%3D 10.1016/j.brainres.2003.09.004 14642838 (Pubitemid 37464590)
38. A Samali S Orrenius 1998 Heat shock proteins: regulators of stress response and apoptosis Cell Stress Chaperones 3 228 236 1:CAS:528: DyaK1MXht1Wgs7s%3D 10.1379/1466-1268(1998)003<0228:HSPROS>2.3.CO;2 9880235 (Pubitemid 29051822)
39. R Saminathan A Pachiappan L Feng EG Rowan P Gopalakrishnakone 2009 Transcriptome profiling of neuronal model cell PC12 from rat pheochromocytoma Cell Mol Neurobiol 29 533 548 1:CAS:528:DC%2BD1MXntVGns7c%3D 10.1007/s10571-009-9345-y 19194798
40. MI Sanchez-Reus II Peinado MF Molina-Jimenez J Benedi 2005 Fraxetin prevents rotenone-induced apoptosis by induction of endogenous glutathione in human neuroblastoma cells Neurosci Res 53 48 56 1:CAS:528:DC%2BD2MXmvFSjsbc%3D 10.1016/j.neures.2005.05.009 15996779 (Pubitemid 41073727)
41. MI Sanchez-Reus MA Gomez del Rio I Iglesias M Elorza K Slowing J Benedi 2007 Standardized Hypericum perforatum reduces oxidative stress and increases gene expression of antioxidant enzymes on rotenone-exposed rats Neuropharmacology 52 606 616 1:CAS:528:DC%2BD2sXhtVGjt7k%3D 10.1016/j. neuropharm.2006.09.003 17070561 (Pubitemid 46123375)
42. M Sasaki H Nakamura S Tsuchiya S Horie M Kashiwayanagi T Saito 2007 Quercetin-induced PC12 cell death accompanied by caspase-mediated DNA fragmentation Biol Pharm Bull 30 682 686 1:CAS:528:DC%2BD2sXls1aktLo%3D 10.1248/bpb.30.682 17409502 (Pubitemid 46570988)
43. DI Sinn K Chu ST Lee EC Song KH Jung EH Kim 2007 Pharmacological induction of heat shock protein exerts neuroprotective effects in experimental intracerebral hemorrhage Brain Res 1135 167 176 1:CAS:528:DC%2BD2sXhtlWisrw%3D 10.1016/j.brainres.2006.11.098 17208204 (Pubitemid 46188430)
44. NA Thornberry Y Lazebnik 1998 Caspases: enemies within Science 281 1312 1316 1:CAS:528:DyaK1cXlvVegsLs%3D 10.1126/science.281.5381.1312 9721091
45. L Yang X Liu J Hao Y Yang M Zhao J Zuo 2008 Glucose-regulated protein 75 suppresses apoptosis induced by glucose deprivation in PC12 cells through inhibition of Bax conformational change Acta Biochim Biophys Sin (Shanghai) 40 339 348 1:CAS:528:DC%2BD1cXmt1als7o%3D 10.1111/j.1745-7270.2008.00409.x (Pubitemid 351572115)
46. K Yuyama H Yamamoto K Nakamura T Kato I Sora T Yamamoto 2001 Resistance of PC12 cells against nitric oxide (NO)-induced toxicity in long-term culture: implication of neuronal NO synthase expression Neurosci Lett 309 169 172 1:CAS:528:DC%2BD3MXmtFWisro%3D 10.1016/S0304-3940(01)02078-X 11514068 (Pubitemid 32763166)